Components of the Human – Farm Animal Relationship

Components of the human – farm animal relationship

A literature review

Vonne Lund

______SLU Specialarbete 8 Institutionen för husdjurens miljö och hälsa

Swedish University of Agricultural Sciences Skara 1999 Faculty of Veterinary Medicine ISSN 1402-3342 Department of Animal Environment and Health ISBN 91-576-5672-X ______2

Table of content

ABSTRACT 5

INTRODUCTION 7

THE SCIENTIFIC STUDY OF THE HUMAN - FARM ANIMAL RELATIONSHIP 9

Problems encountered when studying the interaction 10

Registration of animal responses to the interaction with humans 11 Animal response 11 Behavior and other clinical responses 11 Subclinical registrations 13

Techniques used to include the human caretaker in the study 14 Skilled observation and participant observation 14 Content study and socialization study 14 Self assessment and peer rating assessment 14 Attitude and intervention studies 14

The basis for a good relation 15 The human interaction 15 Components due for a good relation 17 Individuality 18

Effects of domestication 19 The effect of the domestication process 19 Tameness and fear response 20 Implications of fear 21 Genetic differences 23

HOW DO FARM ANIMALS PERCEIVE THE HUMAN CARETAKER? 25

The human role 25

The experiential component of tameness/fear 26 Early handling and critical times for habituation 27 Food awards 30

Ability for discrimination 31 Cues for identification 31 Discrimination between humans and other stimuli 31 Discrimination between humans 32

Importance of the environment 35

HOW DOES THE HUMAN CARETAKER INFLUENCE THE RELATIONSHIP? 37

Pleasant or aversive handling – does it matter? 37 Pleasant handling 38 Aversive or threatening action 39 Inconsistent handling 39 Effects on production 40 Indications of a chronic stress response 42 Effects on behavior, ease of handling, animal welfare and product quality 43

Effects of stockman personality and attitudes 44 Attitude and beliefs 47 Vocal interaction as reflecting stockman attitude 49 Aggression 50

“Stockmanship” – managing the interaction 50 Definitions 50 “Eye for the animals” 52 Human habituation – the importance of setting good examples 53

Effects of modern technology on the human – animal relation 53 Large scale animal husbandry 55

DISCUSSION 57

The study of the human - farm animal relationship 57 Animal reactions to human handling 57 The human component 59

Practical consequences 61 Daily interaction and routines 61 Minimize fear of humans through habituation 62 Minimize the effects of unavoidable negative handling 63 Assessment of animal individuality ("temperament") 64 The effects of modern technology 64

Conclusions 65

SUMMARY 67

ACKNOWLEDGEMENTS 69

LITERATURE 71

Abstract

Although the relationship between the farm animal and its environment has been extensively studied for the past 30 years, the relationship between the human caretaker and the farm animal has quite recently become focus for scientific interest. This literature study covers the scientific literature published in the latter field until 1998 dealing with cattle, pigs and poultry. It has been undertaken as part of a comprehensive project studying the relationship between the human caretaker and the farm animal, including ethical aspects.

The first part of this study gives an overview of different methods used to register animal responses to human interaction and methods that study the role of the human caretaker. Then the concept of a good human – farm animal relation is presented, as viewed in the scientific papers, and effects of domestication are discussed. In the second part research results are presented regarding how farm animals perceive the human caretaker, both socially and physically. It is supposed that a human can take several roles in relation to the animal, e.g. boss animal, mother substitute, leader or “companion” but the details around this are not much known. Also insights in how animals perceive humans are limited – even basic knowledge is incomplete e.g. regarding how discrimination between humans is made and to what extent.

In the third part research results are surveyed concerning how the human affects the relationship. The effects of pleasant or aversive handling are quite well studied and these are discussed, as well as effects of stockman personality and attitudes and the complex concept of stockmanship.

In the discussion suggestions are made regarding how to apply the scientific findings in everyday animal husbandry in order to improve the human – farm animal relationship and thus obtain better animal welfare, higher production and farmers/stockmen more sensitive to animal needs.

Conclusions are that the human – animal relation depends on different factors related to the human part as well as to the animal part, and that the relation can be manipulated in several ways. It is possible to substantially improve the relationship in order to improve animal and human welfare. These improvements need not always cost a lot to implement, rather they can pay off well due to increased human and animal productivity.

Introduction

Beginning in the 1950’s, radically new methods were introduced for the husbandry of farm animals. Gradually “animal husbandry” was changed into intensive “animal production” (Ekesbo 1991). The changes also had consequences for farm animal health and welfare. This eventually brought about scientific studies of the relationship between animal environment, including management, and animal health (e.g. Ekesbo 1966; Bäckström 1973). These studies revealed the role of several environmental factors for animal health and well being. However, the role of the most important factor, the human caretaker, is so far only briefly investigated. But there is an increasing scientific interest in the human – animal relationship, and a significant number of results can be expected in the next few years which should considerably increase our knowledge in this field.

The human – farm animal relation is not only a technical question, it also brings about ethical considerations. This is true both regarding the direct interaction between the human and the individual animal but also regarding the impact on animal health and well being of environmental factors under human control. The ethical implications are recognized for example in the animal welfare legislation which can be seen as society's moral guidelines for human interaction with animals. Ethical issues in animal husbandry have become increasingly important, not least due to increased consumer concerns. For decision making in ethical issues it is of great importance that there is knowledge upon which conclusions can be based. To be able to decide whether an action is to be considered good or bad, the consequences of that action must be known. Thus, in order to make ethical statements e.g. regarding new production systems in animal husbandry, their effects on the animals concerned should be investigated and analyzed.

This literature study has been undertaken as part of a comprehensive project studying the relationship between the human caretaker and the farm animal, including ethical aspects. The aim of the project was to find out what answers research can present regarding different aspects of this relationship, asking questions like:  How does the human - farm animal relationship affect the animal?  What are the components of the relationship, and how can these be measured and scientifically studied?  How can these components be developed to create an optimal relation both for the human caretaker and the farm animal?  How is farm animal behavior influenced by human behavior?

This study is focusing on the traditional farm animals i.e. cattle, pigs and poultry. Literature in adjacent areas, such as pet animals, fur animals or laboratory animals, has not been included. It covers literature published until 1998.

The scientific study of the human - farm animal relationship

The human species has for thousands of years had close relations with some animal species utilized for agricultural purposes. In parts of the world with harsh climatic conditions, like in the Scandinavian countries, the co-existence with farm animals has up until modern times been a precondition for human survival. The behavior of animals has been scientifically studied since the beginning of this century, with Niko Tinbergen and Konrad Lorenz as forerunners in creating the new scientific discipline of ethology. The scientific study focusing on different aspects of the relationship between the farm animal and the human caretaker started in the 1960’s. But the interaction between the human and individual animals has become focus for scientific studies only lately. This leaves us with many unanswered questions regarding the interaction. Even many basic questions still need answers, like how and to what extent animals discriminate between humans (de Passillé et al. 1996).

Both practical experience and scientific research performed so far show that stockman behavior is of great importance for animals in intensive livestock systems, affecting animal welfare as well as production performance (e.g. Seabrook 1972a, 1972b; Seabrook and Mount 1995; Coleman et al. 1995; Hemsworth and Barnett 1987b). Some authors even claim that man's interaction with the animals is one of the main causes of reduced welfare in such systems (Duncan 1990; Hemsworth and Barnett 1987b).

The English researcher Dr. Martin Seabrook was one of the first to scientifically study the effects of the close relationship between the stockman and the cow. In 1969 he commenced a study to determine the influence of the stockman’s personality on milk yield (Seabrook 1972a, 1972b).

Extensive work, mainly on pigs but also on cattle and poultry, has been performed by scientists at the Victorian Institute of Animal Science (VIC), Melbourne, Australia, lead by Dr. Paul H. Hemsworth.

In the last years interest in the relationship between the human caretaker and the farm animal has increased considerably, with scientists in a number of institutes worldwide carrying out research in the field from different aspects.

Most studies have focused on animal reactions to different types of handling (such as ”pleasant” or ”aversive”), while some studies have put focus on the relationship as such and have also included the caretaker in the study. Studies in laboratory scale on experimental farms as well as studies on commercial units have been used. The research methods and techniques have varied accordingly. The Hemsworth group has e.g. in

addition to traditional scientific research also performed action research (intervention studies), developing training procedures to change attitudes and behavior of the stockmen and thereby implying increased animal welfare and productivity.

Problems encountered when studying the interaction

The interaction between animal and human is a very complex. The research area is beset with many methodological and epistemological problems, including the fact that as soon as one starts studying the interaction one may also influence it (Seabrook 1984b). Seabrook and Mount (1995) point at the following problems when trying to scientifically evaluate animal reactions connected to interaction with humans:  Animals are individuals and the same handling treatment may cause different responses in different animals.  Imposing behaviors on animal groups may cause problems since the whole group may be affected by the handling of an individual animal in the group, as well as the individual animal may be influenced by the behavior of other animals in the group having previous experiences with humans.  The space available to the animal may influence the effect of treatment and the behavior as well.  Indoor or outdoor environment can make a big difference, in that the human is not such a dominant stimulus in the outdoor environment as in the indoor environment.  Previous experience and perceptions may influence the reactions of the animal.  Time delays in reaction may be present.  Habituation to treatment may occur.  The behavior and degree of interaction given by any persons responsible for the maintenance of the animals must be taken into consideration, unless it is performed by one and the same experimenter throughout the experiment.  Diurnal variations might be present, and it is important that the testing is performed during the same time of the day.  Even ”pleasant” handling may affect e.g. animal heart rate. The quality of any handling treatment is a perceived construct and an animal may perceive any applied ”pleasant” or ”unpleasant” stimuli as undesirable or even desirable (Seabrook 1995; Dryden and Seabrook 1986).

The upbringing of the animal appears to be of great importance for later reactions towards humans (e.g. Arave et al. 1985). It can for example make a big difference for the response of cattle in test situations (e.g. in restraint tests) if the animals are reared under range conditions or in traditional dairy husbandry (Boivin et al. 1992b).

Seabrook and Bartle (1992b) point out that the setting in which handling is performed can make a difference. For example, ”aversive” handling performed by a confident personality type stockman in a stable and consistent environment is likely to have a different animal response as compared to the apparently similar interaction performed by a non-confident stockman in an unstable inconsistent type of environment. By 10

”confidence” is meant a reflection of an ability and willingness to get within the group if animals, relating stability with firm, sure and steady movements (Seabrook 1984a).

Registration of animal responses to the interaction with humans

Animal response

The animal perceptual and response process is a very complex one. Basically, there are three types of interrelated biological responses available in contact with humans:  behavioral  autonomic and  neuroendocrine. These responses provide the principal resources the animal utilizes in its attempts to cope with a stressor. Behavior is the functional response to internal and external stimuli. The autonomic and neuroendocrine responses function to mobilize the body’s reserves for appropriate action to the challenge, e.g. increase in heart rate and availability of glucose. They are of importance for example when the human is perceived as fear provoking by the animal (Hemsworth et al. 1993a).

Behavior and other clinical responses

Approach test

The approach test is a technique frequently used to rate animal fear of humans: The approach behavior towards an experimenter within an experimental test area is used as an index of the fear response experienced by the animal, i.e. an animal which approaches the experimenter is supposed not to be fearful of humans (Seabrook and Mount 1995).

The Hemsworth-group has developed a standard approach test used in their experiments. Basically the animal is individually introduced into a 3 x 4 meter arena for a 2 minute familiarization period. The objective of the familiarization period is to allow each pig to become reasonably familiar with the arena. After this, the experimenter enters the arena and remain stationary, and during the next 3 minutes the approach behavior of the pig is recorded (Hemsworth and Barnett 1987a). The test has mainly been used for pigs but similar approach tests have also been used for cattle and poultry (e.g. Hemsworth et al. 1989b, 1994b, 1995; Barnett et al. 1992).

However, factors other than fear may be involved in the response, such as lack of interest in the experimenter, or a greater interest in the environment in which the test takes place (Seabrook and Mount 1995; Marchant and Whittaker 1997). This supposition is supported by an experiment performed with gilts, where a heart rate

monitor was attached to the gilts tested. There were no significant differences between quick and slow approaching gilts in heart rate responses to an experimenter entering the pen or to the experimenter’s approach. Quick approaching gilts also made more short vocalizations, which may be associated with investigation (Marchant and Whittaker 1997).

Conversely, the approach could be motivated by exploratory behavior or even a desire to investigate a situation that invokes a degree of fear.

Pigs in an outdoor environment may not approach an experimenter because of over familiarity and a knowledge that approach has no beneficial outcome. The presence of a food reward will make the animals much more prone to approach, also when aversively handled (Seabrook and Mount 1993).

Seabrook and Mount (1995) also points out that both ”pleasant” and ”aversive” handling may be perceived as aversive by individual animals. ”Aversive” handling indoors may be perceived as greater threat than ”aversive” handling outdoors, due to the inability of the outdoor animal to ”escape”. They conclude that the concept that avoidance equates directly to fear should be regarded with skepticism.

A variant also used is the avoidance test, where an experimenter approaches the animal and the amount of avoidance is measured (e.g. Hemsworth and Barnett 1987a). Flight distance in cattle is a well-established indicator of the man-animal interaction (Seabrook 1984a).

Handling tests

Different types of handling tests are used in research. They discriminate between animals according to their previous human experience. They are repeatable and easy to do. Reactions to humans does not seem to be influenced by the handlers themselves, at least if they are experienced in cattle handling and unknown to the animals.

The restraint test measures how long it takes to restrain an animal e.g. in a corner of the pen, and/or how long the animal can remain restrained. A similar type of test is the sorting test, measuring the time it takes to isolate an animal from its social group. A disadvantage with both these tests is that they may measure the social bonding between the individual animal and the social group, rather than handling ability or the relation to the human. Also, reactions of the other animals may greatly influence results. Neither can these tests be used to distinguish between very tame animals (Boivin et al. 1992b).

Leading an animal with a halter is used as a testing procedure in some experiments. Sato et al. (1984) used it to test the reactions of caressed vs. non-handled calves towards humans. They point out that the avoidance behavior of the tested animals differed depending on testing method. The caressed calves showed no or little avoidance reaction when being touched or when an experimenter entered the pen. However in the leading test the avoidance behavior of caressed calves did not differ from that of control calves.

Vocalizations

Preliminary studies have been performed to document vocalizations made by pigs during handling. The results indicate that the domestic pig performs a number of distinct vocalizations during isolation. Short single grunts appear to be clearly associated with investigation. Long single grunts may be a form of contact call, the rate of which is related to physiological and behavioral activity. With further research, certain pig vocalizations may be identified as providing useful additional information about an individual’s welfare (Braithwaite et al. 1995; Marchant and Whittaker 1997).

Subclinical registrations

Level of plasma free corticosteroids

There is an enormous body of literature on the use of corticosteroids to indicate a stress response. There is general agreement that elevated corticosteroids indicate a physiologic adaptation by animals, and that a sustained elevation of corticosteroids is potentially detrimental to animals’ welfare because of their actions on protein metabolism, reproduction and the immune system (Hemsworth and Barnett 1987b).

There is evidence that farm animals respond to short term (acute) physical and psychological stressors with an elevation in plasma corticosteroid levels. If the stressor continues, the response proceeds into long term or chronic response. In this phase it can also have detrimental consequences on nitrogen balance, secondary metabolism, the cardiovascular, digestive and immune system (Danzer and Mormède 1983; Barnett and Hemsworth 1986). The measurement of plasma free corticosteroids through blood sampling has been frequently used (particularly by the Hemsworth research group) to measure chronic stress responses in farm animals, especially pigs but also chickens and cattle.

However, any interaction involving blood sampling is likely to influence the behavioral and physiological responses. Even ”hiding behind a screen” will not eliminate the effect of the sound and smell of the human, thus evoking a human response in the animal (Seabrook and Bartle 1992a).

Heart rate

Recordings of non-motor heart rate can provide a good assessment of stress, on the grounds that it indicates the animal’s anticipation of the possible need for rapid escape from dangers posed by predators or conspecifics. However, when interpreting heart rate change, allowance must be made for the effects of individual identity, season and behavioral time budget (Baldock and Sibly 1990). Non-motor heart rate can thus be used e.g. for assessing stress in animals in an animal-human relation situation. Telemetric heart rate measurement has been used by several authors, using a radio

transmitter attached to the chest of the animal prior to handling (e.g. Seabrook and Bartle 1992a; Knierim and Waran 1993; Marchant et al. 1997).

Techniques used to include the human caretaker in the study

Seabrook (1984a) has adopted the following six different techniques for the study of the stockman and his/her effect on the herd: Skilled observation, participant observation, content study, socialization study, self assessment and peer rating assessment.

Skilled observation and participant observation

During skilled observation, the stockman’s behavior is watched and recorded. The technique is difficult and requires considerable patience and long hours of study to ensure the behavior of the observed is not modified.

The technique of participant observation has proven successful for studies on commercial units, since the observer either is becoming part of the working team or fulfilling another role on the unit, and so is achieving a natural situation in which to observe, record and question the working staff.

Content study and socialization study

Content study is a full study of all the activities of the stockman inside and outside his/her work including those unrelated to dairying. This approach may lead to a fuller understanding of the personality and motivation. The socialization study also includes the whole socialization process, including previously held occupations.

Self assessment and peer rating assessment

The self-assessment is performed by giving stockmen a questionnaire which attempts to assess personality traits. Peer rating assessment is made by persons who know the stockman well, who are asked to describe the person (using a questionnaire). Results obtained by self-assessment or peer rating assessments express some of the most objective conclusions.

Attitude and intervention studies

The Hemsworth group has for a number of years worked closely together with G. J. Coleman from the Dept. of Psychology at Monash University, Melbourne. Much of the work has been directed towards stockman attitudes and how these affect animal

handling. A person’s attitude toward a behavior can be measured by the use of questions relating to that behavior (Ajzen and Fishbein 1980). Questionnaires have thus been used to determine stockman attitudes, and the attitude studies have been supplemented by skilled observation studies performed by trained observers in the herds. Intervention studies in the pig and dairy industry have been performed, using cognitive-behavioral modification techniques for behavioral retraining of stockmen as well as for changing their attitudes. The training has targeted those attitudes and behaviors that have a direct effect on animal fear and productivity, by providing information on how animals function as well as practical training in actual handling techniques (Hemsworth et al. 1994b).

The basis for a good relation

The human interaction

Sambraus and Unshelm (1983) state that there are three ways in which man can influence the behavior of animals:  selective breeding of individuals with special (hereditary) behavioral characteristics  creation of the physical environment  direct influence on behavior by conditioning.

Seabrook (1995) states that human interaction with animals involves much more than just ”handling”. It will include such aspects as voice tones, gestures, smell, sound of foot movements or other ”signals” from human to animal.

According to Seabrook the interaction can be considered as three interrelated components: hand and arm interaction, vocal interaction and holistic empathetic interaction.

The hand and arm interaction can be considered as an active interaction and can be identified into two patterns: ”pleasant”, involving patting, stroking and touching the animal, and ”aversive”, involving slapping or light hitting (however not overt aggression). Extensive research has been performed regarding the effects of this type of interaction.

Vocal interaction has been much less investigated, in spite of that it is an important means of interaction. Talking to animals is a reflection of interaction and empathy (Seabrook and Bartle 1992a).

Holistic empathetic interaction can be considered as passive interaction. Seabrook (1995) includes factors important for the environment and created by the human but having received only limited systematic research. Some of these might even be difficult

to study and perceived as being at the ”fringe” of science. The following is a list of such factors:  Smells and other chemicals secreted by the stockman  Patterns of movement and behavior perceived by the animal  Perception of changes from ”normal” behavior of the stockman  Manner of hand movements, e.g. degree of shaking  Other forces emitted by the body of man and picked up by animals; these may not yet be identified (Seabrook 1986)  Nature of other messages and signals transmitted by the stockman, e.g. creating environmental stability and an air of ”calm and confidence”.

The way the human is perceived by the animal, and thereby the interaction, is also different depending on if the interaction takes place outdoors or indoors (table 1). The human-animal relation will also be dependent on the species and type of production. The relation established in a dairy herd is very different as compared to in a pig herd. In the dairy herd there is much closer contact with the animals (Dryden and Seabrook 1986). Seabrook (1984b) found when investigating English dairy herds that the daily contact for each animal lasted up to 20 minutes per day and each animal was known individually. In modern pig production individual recognition of animals is minimized as well as the opportunity for contact with individual animals. Hemsworth et al. (1987a) suggest that the human-animal relationship probably has more implications for the breeding pig than the grower pig, since the breeding pig is likely to receive more contact with the stockman.

The human-animal relation is even more brief in poultry production. The average time spent per egg layer is in average 0,2 seconds per week (Algers, pers. comm.)

Table 1. Interaction components, as perceived by the animals (from Seabrook and Mount 1993).

Interaction factor Indoors Outdoors

Human hand Perceived as large Perceived as small Human body Part seen See full body Relative size of human body Perceived as large Perceived as small Human voice Crucial; one of main Human voice less crucial variations in sound environment Human smell Strong Weak ”Sympathizer” with animal in distress Human role ”Other” animals Taste Mainly from food and with From environment contact with humans Human tactile role Effective, e.g. scratching Ineffective, scratching self- skin performed

Components due for a good relation

Only few authors have expressed a general opinion on which are the components that form the basis for a good relation between human and farm animal (table 2).

English (1991) emphasizes the central role of empathy in a good relation between man and animal. Empathy describes the reciprocal relationship between man and the animal with which he associates. It involves emotional attachment of man and animal in a way that both parties thrive from it. (This use of the concept of empathy is however criticized by Coleman et al. (1998), who claim that empathy only refers to the capacity to vicariously experience the emotions of another.)

Albright (1986) states that a sound relationship is based on communication as well as confidence.

Hemsworth and Barnett (1987a) propose that the level of fear of humans by pigs reflects the quality of the relationship existing between the stockman and these pigs. However Seabrook (1995) states that although this might have relevance when the aversive/unpleasant handling is severe, in normal husbandry the situation is more complex.

Seabrook (1995) states that all stockmen should attempt to create a stable, consistent and caring environment. He suggests that the stockman should adopt the stimuli used by the animals in social communication, e.g. social grooming, to establish a social bond with the animal (Seabrook 1988). Food awards should be used to diminish the effects of

unavoidable aversive handling (se page XX). Seabrook (1995) also suggests that the human should imitate social signals of dominance. This is applied as a refined method of mastering the animals in several nomadic cultures performing animal husbandry (Lott and Hart 1979).

Seabrook (1986) has developed the following list over general symptoms in a herd of a good relationship between animals and human:

1. Animals have short flight distances. 2. Animals tend to move towards the person (some of this may be conditioned learning, since they may receive a reward such as extra food). 3. Animals are not restless in the presence of the stockman. 4. Animals are not easily frightened (i.e. not ”jumpy”). 5. Animals defecate less in the presence of the stockman. 6. Stockman touches the animals 7. Stockman communicates with animals (talking to and talking with). 8. Stockman likes being with the animals and spends more of his available time in contact with them. 9. At time of stress (e.g. farrowing) stockman touches and communicates more with animal. 10.Man appears as the ”boss” animal but can also accept a more submissive and caring role (that is, mother substitute).

Table 2. Different authors’ views of the basis for a good relation between human and animal.

Author/s Important for a good relation

Seabrook (1988) Mutual emotional attachment Albright (1986) Communication and confidence Hemsworth Maximize positive behavior, minimize negative behavior to minimize and Barnett (1987b) fear

English (1991) Empathy: the reciprocal relationship between man and animal

Individuality

One feature to take into account when discussing the human-animal interaction is the individuality of the animal. Research on rats and mice have revealed great individual differences in reaction patterns, and these differences appear to be hereditary. Much less research of this type is performed on farm animals, but some results are published. Forkman et al. (1995) indicate presence of personality traits in piglets. Seabrook and Mount (1995) point out that individual responses by different animals to the same 18

environments or human stimuli/contact are the norm and not the exception. The expression of behaviors in response to interactive stimuli is a function which may relate closely to ”temperament”, as considered in the context of the perceptive capacity of the animal.

Seabrook and Mount have registered individual patterns of reaction in sows (i.e. consistent relative differences) using telemetric heart rate measurements as well as an approach test. The individual animal may also react differently on human handling at different times, as shown in the approach test. Thus, animals are individuals and they may respond with a range of behaviors and physiological responses to the same treatment (Seabrook and Bartle 1992a; Marchant et al. 1997).

For milking cows the reaction on different types of handling may vary with stage of lactation. The influence of milker on milk production and milk fat content was studied in a 121 cow herd with 18 different caretakers. It showed that high yielding cows were most affected, especially in the beginning of the lactation period (Schlichting and Schmidt 1986).

Effects of domestication

The effect of the domestication process

For the traditional farm animal species the domestication process has been going on for several thousand years (Zeuner 1963). Some contemporary definitions of domestication postulates that it is a condition in which the breeding, care and feeding of animals are more or less controlled by man (Price 1984). Price suggests the following definition: “that process by which a population of animals becomes adapted to man and to the captive environment by some combination of genetic changes occurring over generations and environmentally induced developmental events reoccurring during each generation”. Domestication also involves the formation of a symbiotic relationship between man and other animals or plants (Rindos 1980, in: Price 1984).

Domestication affects animal behavior since a mild response to humans is essential when breeding stock is selected: The selected animals should accept the presence of humans, not try to flee, react violently or manifest intense stress reactions (Le Neindre et al. 1993).

There are studies supporting that differences do exist between domestic animals and their wild counterparts in their behavioral response to human beings, e.g. shorter flight distances and less avoidance reactions for the domestic animals (Hemsworth et al. 1987a, Price 1984).

Tameness and fear response

In wild animals, a definition of tameness would include not fleeing at human approach (Kretchmer and Fox 1975; Price 1984). For farm animals reared without contact with humans the initial response is still fear, in spite of the long domestication process. Thus behavior control through forced compliance and confinement is a general rule on farms, also today (Murphy and Duncan 1978; Murphy et al. 1981). The fear response can be explained from an evolutionary point of view, since the original relationship between mankind and the progenitors of our present farm animals was a predator – prey one (Duncan 1990). It can be modified by human behavior, as shown below.

It is generally accepted that fear reactions function to protect the animal from harmful stimuli (Hemsworth et al. 1993a; Jones 1985). Fear can be viewed as a form of emotional reaction to the threat of punishment, where punishment refers to a stimulus which the animal works to terminate, escape from or avoid (Gray 1987, in Hemsworth 1993). Fear elicits escape or avoidance reactions (Hemsworth 1993).

Tameness has both a genetic and an experiential (learning) component (Price 1984). Le Neindre et al. (1993) state that both genetic and epigenetic factors are involved in the differences of animal response to humans. Artificial selection as well as regular handling and early environmental enrichment can thus be used to modify domestic chicks’ responsiveness to man (Jones 1985).

No difference in fear reactions towards humans were found between bulls and steers and steers and heifers having similar experience of humans, using a standard approach test (Tilbrook et al. 1989).

A large number of reports state that regular gentle handling is a potent and reliable method of reducing domestic chicks’ fear and avoidance of human beings (e.g. Gilman et al. 1950; Jones and Faure 1981; Gross and Siegel 1982b). Simply placing one’s hand into the home cage of female chicks twice daily with no attempt to initiate physical contact was sufficient to reduce the tonic immobility fear response and avoidance of the experimenter. The same was true if human contact was reduced to visual contact with a human being twice daily standing in front of the cage and touching the wire-mesh wall of the cage. Interestingly, the same results were obtained by letting chicks regularly observe their neighbors being picked up and handled. It is proposed that the fear- reduction was achieved by the visual exposure of the experimenter, rather than through imitating tamed companions (Jones 1993).

Waran (1995) points out that there appears to be an optimum level of handling that leads to a reduction in fear responses toward humans, but still leaves the human the 20

dominant figure in the animal’s environment. Too much handling may result in animals difficult to handle since their flight zone is reduced so much that they no longer move away from a human.

Implications of fear

Much of the research carried out so far regarding the relation between human and farm animal has concerned fear of humans in domestic animals. The Hemsworth group in particular has worked with this issue.

Fear has implications for animal welfare, since in situations where fearful farm animals are regularly or frequently handled there is a risk that the animal will experience an acute or chronic stress response (Hemsworth et al. 1993a; Le Neindre et al. 1993). Particularly in the case of big animals such as cattle, fearful animals pose a risk of physical harm for both caretaker and animal and make handling more dangerous (Duncan 1990; Boivin et al. 1992b; Le Neindre et al. 1993).

However, Jones (1985) suggests that the potential deleterious conditions to be avoided are those of ”over”- and ”under-stimulation”. The solution could lie in determining and maintaining an optimal level of emotional states such as fear.

Fear of humans can be related to low production, which is indicated by three lines of evidence (de Passillé et al. 1996):  A change of stockman can lead to changes in productivity (e.g. Seabrook 1984b).  There is often lower production on farms where the animals show more fear of people (e.g. Hemsworth et al. 1981a, 1989a).  Aversive handling of animals can reduce their production (see below).

Sows in one-man operated Dutch farms displayed significantly more fear (as shown in a greater withdrawal response to an experimenter’s hand) on farms where the average total number of piglets born per sow and year were low (Hemsworth et al. 1981b). The same was found on Australian commercial pig farms (Hemsworth et al. 1989a), where fear of humans accounted for 20% of the variation in reproductive performance between farms.

Fear of humans in sows may adversely affect the survival of their piglets. It is hypothesized that this may be due to disruption in the delivery process, caused by the caretaker’s activities in the farrowing unit (Hemsworth et al. 1997).

Dairy cows’ fear of a specific person, present at milking, can substantially reduce milk yield, possibly by reducing oxytocin secretion (Rushen et al. 1997).

There are also studies however, when no effects on pregnancy rate or litter size have been recorded in spite of a significant withdrawal response towards humans, interpreted as fear of humans, in the animals. For example, Hemsworth et al. (1990) did not register any difference in pregnancy rate or litter size in gilts which were classified into two fear 21

categories (low or high). The classification was based on whether or not they physically interacted with an experimenter in a standard approach test.

Poultry

The relation between chronic stress, interpreted as fear of humans, and productivity has also been shown to apply to poultry (e.g. Hemsworth and Barnett 1989; Barnett et al. 1992). Barnett et al. (1994) found that hens receiving human contact 15 minutes per day for 17 weeks from 19 weeks of age, in addition to the daily routine husbandry, had significantly lower corticosterone response and higher egg production as compared to hens receiving minimal human contact. The hen-day egg production was 89.4 vs. 83.1% (p<0.05). Cell-mediated immunity was significantly greater, but only at the first of three sampling periods (p<0.01).

Hemsworth et al. (1994b) found a significant relation between fear in broiler chicken and feed conversion on commercial broiler farms, so that feed conversion was poor on farms in which birds avoided an experimenter in two standard tests. The variable studied accounted for 28% of the variance in feed conversion at the farms.

However, the effects of human handling of chickens have yielded somewhat different results (Albright 1986; Duncan 1990; Hemsworth et al. 1994b). Most studies have found a positive relation between regular handling, which is known to reduce chickens’ fear of humans, and production performance. Thus, regular handling has been associated with improved feed conversion, greater resistance to infection, increased growth and better food conversion rate in young layers and broiler chickens (e.g. Gross and Siegel 1979; Jones and Huges 1981; Hemsworth et al. 1994b). However, other studies found no effects of handling on the growth of young broilers and layers (e.g. Reichmann et al. 1978; Leonard and Fairful 1992), or even a negative effect (Freeman and Manning 1979). However, slight differences in procedure can probably account for major differences in results (Duncan 1990).

Jones and Hughes (1981) found that regular handling in broilers and females of layer strains significantly enhanced growth. Males were not affected. Gain:food ratios were generally greater in the handled birds.

Socialized chickens (habituated to persons) were less affected by fasting. Socialization also affected the reaction to a Staphylococcus aureus infection (Gross and Siegel 1982a). In another experiment, birds were either ”ignored”, ”hassled” (subject to loud noises and banging of their cages) or ”socialized” (habituated to humans by being handled gently, talked to and offered food). Socialization reduced mortality, pericarditis and avoidance of humans, improved feed efficiency and increased resistance to infection with Escherichia coli (Gross and Siegel 1982b). The authors propose that habituation to human beings decreases the physiological effort required to respond to human contact and that these resources could then be used for responding to environmental stressors or growth. They concluded that their results indicate that productivity and resistance to environmental changes should be increased by the socialization of animals used in commercial agriculture.

Genetic differences

Genetic changes take place over generations. It appears that there are three main ways in which domestication can affect the animal’s fear of human beings (Hemsworth and Barnett 1987b). These are:  Artificial selection; individuals that are highly fearful of human beings will be difficult to inspect closely and handle during routine husbandry, and thus the animal breeder may be less likely to select these individuals as breeding stock.  Natural selection, which usually accompanies artificial selection in a captive population (Price 1984). High levels of fear in the presence of human beings may adversely affect the survival or reproductive success of the individual.  Relaxation of natural selection; certain behaviors may lose their adaptive significance in captivity and consequently both genetic and phenotypic variability for such traits may increase. One such behavior might be predator avoidance, and this might cause the initial response to human contact to change in captivity.

The trait ”fear of humans” was studied in gilts at 25-30 weeks of age by measuring the time it took them to interact with a stationary experimenter. It was found to be moderately heritable with a heritability of ± s.e. 0,376 ± 0,19 (Hemsworth et al. 1990).

Breed differences

Breed differences may be related to differences in social behavior, e.g. the degree of tolerance of human presence.

Murphey et al. (1980, 1981) found that dairy cattle in an outdoor environment have less flight distance than do beef breeds. Raising dairy breeds for meat and raising beef breeds as milk cows had little overall effect on their approachability. Breed differences were also evident for investigatory (approach) behavior. (However, age took precedence over breed affiliation in that heifers showed more of an investigatory behavior irrespective of breed.)

Animals of Friesian breed (a dairy breed) were more willing to accept social isolation and had fewer social interactions than did Salers animals, a beef (Le Neindre and Garel 1990). It seems likely that the genetic selection for docility has been greater in dairy cattle where this trait is of much greater importance than in beef cattle.

Boivin et al. (1992b) found no differences in the ease of handling between heifers of three different dairy breeds. All were easy to handle.

Boivin et al. (1994) found significant differences in handling tests between Salers (a combined milk- and beef breed) and Limousin animals, the former being more motionless when handled.

Murphy and Duncan (1978) found strain differences in chickens responding to exposure to human beings. Jones (1985) refers to several studies showing the existence of differences in fearfulness and/or general reactivity between lines and between individual chickens.

Difference between sires

A study with 617 Limousin heifers from 24 different bulls recorded big differences in behavior between the offspring of different sires. A heritability of 0.28 was estimated for a four level variable (Le Neindre et al. 1993).

Le Neindre et al. (1995) performed docility tests over three years on 906 Limousin heifers sired by 34 males. The heifers were tested individually with seven different handlers at the age of 10-11 months. The effects of handler, year, birth period, husbandry system and sire had significant effects. Animals reared indoors were more docile than those reared outdoors. The authors point out that this handler effect implies that handlers should test heifers off different bulls, and should preferably not be changed from year to year.

Heritability estimates for docility score and for docility criterion (a categorical trait with four classes) were 0.22 and 0.18, respectively. However, estimates might have been higher if the heifers would all have been raised on the same farm with the same handlers.

Boivin et al. (1994) found significant differences in aggressiveness towards humans between heifers of different Limousin sires (p<0,05).

How do farm animals perceive the human caretaker?

The human role

Seabrook (1986) states that the stockman may assume one or several of the following roles: boss animal, mother substitute, leader or friend. Provided that the term ”boss animal” implies firm but sensitive control of his charges, all these terms imply mutual emotional attachment. For some species, humans can also take on the role of a social object (i.e. “companion”) whose presence itself is rewarding (Price 1984).

Sambraus and Unshelm (1983) suggest that man can have the following meanings for the animal: Enemy, prey, symbiont, part of the environment or being of the same species. The latter only by imprinting, which can only be realized if an animal is isolated from animals of the same species at a very early date and lives in close contact with human beings.

The human caretaker can be considered by animals as a predator, a negative element of the environment, but also as a social partner with a dominant or junior role (Le Neindre et al. 1993).

Sato and Okamoto (1996) tested sheep under distress and found that stress reactions such as vocalization or biting fences were less performed when a human was present. They concluded that a stockman might be able to be an alternative to conspecifics. This result was confirmed by Korff and Dyckhoff (1997), who found that the presence of a familiar person is capable of reducing the stress reaction in lambs to an unfamiliar novel situation. In such a situation, the person may play the role of social support.

Se also table 3.

Table 3. The assigned role/s of the stockman in the herd

Author/s Role/s of stockman (one or several):

Seabrook (1986) Boss animal, mother substitute, leader, friend Sambraus Enemy, prey, symbiont, part of the environment, being of the same species and Unshelm (1983) (only by imprinting) Price (1984) Social object, ”companion”

Le Neindre et al. Predator, a negative element of the environment, social partner with a (1993) dominant or junior role Sato and Okamoto An alternative to conspecifics (1996); Korff and Dyckhoff (1997)

The experiential component of tameness/fear

Price (1984) states that the experiential component of tameness can be achieved by habituation, positive associative conditioning or imitative learning. Duncan (1990) recognizes three different mechanisms through which farm animals get over the fearful reaction towards human beings: habituation, reciprocal inhibition and imprinting.

Habituation is a simple form of learning whereby repeated applications of a stimulus result in a decreased responsiveness (Duncan 1990). It can also be defined as: ”the relatively persistent waning of a response as a result of repeated stimulation which is not followed by any kind of reinforcement” (Hinde 1970; in Hemsworth and Barnett 1987b).

Habituation is likely to occur when the stockman interacts with his/her animals. For example, cattle accustomed to handling react less to humans than do non-handled animals (Fordyce et al. 1985; Boissy and Bouissou 1988). Hemsworth et al. (1986c) found a significant increase in approach by pigs to a human when being handled over four three minutes tests over an eight-day period, suggesting habituation of the pigs’ fear responses.

Conditioning refers to the situation in which an animal forms an association between a previously significant stimulus and a previously neutral stimulus or response. For example, the level of fear of human beings in the individual animal is markedly affected by any previous experience of humans (Hemsworth and Barnett 1987a).

Imitative learning occurs when the animal observes other animals approaching and interacting with human beings which may reduce the animal’s level of fear of human beings. However, the social buffering effect is somewhat temporary in that the animal

may not show shorter flight distances when tested alone with human beings (Hemsworth and Barnett 1987b).

Reciprocal inhibition is the process whereby arousal of the parasympathetic nervous system tends to inhibit activity in the sympathetic nervous system (Duncan 1990). An example of this is when a food reward is used to make the animal overcome its fear of (novel) human contact. Usually the term habituation is used to also include reciprocal inhibition.

Imprinting takes place during the early ontogenetic process, when new neural connections are formed in the brain of a newly hatched chick or newborn young mammal. In this period the organism receives but may also more actively gather information that drastically and often irreversibly determines the “hardware” of the brain; that is the final neural pattern of numbers and types of neurons and their interconnections. During early life events in the surrounding environment (the “Umwelt”) profoundly fasten down brain faculties operating during adulthood. The information gathered during these early life stages mainly pertains to the development of adequate social skills like recognizing and interacting with conspecifics. Imprinting of non-conspecifics may also take place, which is the case at domestication (Wiepkema 1987).

The special form of learning in which long-term social or species attachments are acquired during a ”sensitive” period early in an animal’s lifetime is also called socialization (McFarland 1981, in: Hemsworth and Barnett 1987b).

Early handling and critical times for habituation

General

Research has been performed to find out if there exist any particularly sensitive periods when farm animals are more prone to bond to humans than at other times. This has been shown to be true for several other species, e.g. fox (Belyaev et al. 1985). In poultry the phenomenon of imprinting is well known since described by Konrad Lorentz, and it is possible only during a certain time of early life.

Bateson (1979) has suggested that sensitive periods represent times of rapid reorganization when the developing animal is more easily destabilized by deprivation or environmental disturbance. He proposes that birth and weaning may represent such periods.

Boivin et al. (1992b) found that husbandry systems directly seem to influence animal handling ability. They conclude that there might exist an early period during which animals integrate humans into their social environment.

However, the critical times for habituation need not be early in the animal’s life. Hemsworth et al. (1987b, 1989b) found that dairy cows receiving brief but intense 27

human contact around the time of their first calving displayed a lower number of fear responses during milking than control cows. Bouissou et al. (1997) found that environmental enrichment for a few days around parturition was effective reducing fear reactions in ewes.

Further findings are presented below.

Cattle

Sato et al. (1984) studied five individually reared dairy calves (although reared with visual contact with other calves) which had been caressed for the first 35 days of life, and compared them to a control group receiving no caressing. The calves were tested one week, one month, three months and ten months after being group housed at two months of age. Although the difference between the two groups of calves was big to begin with, the avoidance behavior of the caressed calves gradually increased over time. The conclusion was that temporary early caressing has hardly any lasting influence on later behavior towards man.

Boissy and Bouissou (1988) tested four groups of Friesian heifers, which for 30 days were brushed twice daily and led with a halter, but during different periods in life. When 15 months old they were tested for fearfulness. The test indicated that only prolonged handling for 9 months during early life substantially reduced fearfulness and thus influences the man-animal relationships. No long-term influence of early handling could be observed.

Boivin et al. (1992a) studied calves, reared with their mothers in a free range system. The calves were handled for ten days either after birth or six weeks after birth, or not handled at all by humans. At a handling test performed 3,5 months after birth, calves handled at six weeks after birth seemed least disturbed by human contact. None of the handled calves were aggressive at the test, which was the case with 40% of the non- handled calves.

Heifers 8 months old were also tested. One group had no handling after weaning, while two other groups were handled for 13 days just after weaning or six weeks after weaning. Animals were easier to handle at weaning than six weeks later, and this pattern of behavior remained when tests were performed 7,5 months after weaning. As in the previous test, some of the non-handled heifers showed aggressiveness towards the handler (57% of the tests).

The authors suggest that the new born calves might be less open for human contact since it naturally does not display a social behavior during the first weeks of life. Similarly would suckling calves be more open for socializing with humans just after weaning than during the suckling period when the calf has a strong bonding towards the mother. The discrepancy of results compared to Boissy and Bouissou (1988) could be partly explained by breed differences. The Friesian heifers were reared in an artificial rearing system and thus dependent on humans from birth. Additional handling beyond a certain 28

level of taming had perhaps a non-significant effect on the subsequent reactions to humans.

These findings are confirmed in later experiments. Boivin et al. (1994) showed that calves traditionally reared and separated from their mothers were much easier to handle in a standard test (more quickly restrained in a corner of the testing pen) than free range calves reared with their mothers and with little human contact. In a subsequent experiment this difference persisted at least until twenty months of age (Boivin et al. 1995). The authors noted that tying up the animals at 9-15 months of age without additional handling gave no such effect.

Intensive handling of Salers and Limousin (beef breeds) heifers during the first three months of life significantly improved subsequent docility. The most favorable times for handling were found to be a few weeks after birth and at weaning. This is probably because the social upheaval caused by weaning (Le Neindre et al. 1993). Calves reared together during the same period are observed to considerably increase their social interactions (Vessier 1989, in: Le Neindre et al. 1993).

Arave et al. (1985) found that calves reared in isolation produced significantly more milk. They suggest this can depend on that aggressive behavior of isolates generally is inhibited, sensory stimuli is dampened and close social contact with herd mates avoided. In addition perhaps isolate calves become “imprinted” on their surrogate mother”, making them more docile and enter the milking routine socialized to man more so than other cows.

Calves reared in isolation (including visual isolation from other calves) seemed to display an enhanced human-animal bond towards their human feeder (Purcell and Arave 1991).

This is confirmed by a study of female calves reared under four different conditions during the first three months of life: (1) Open single boxes, (2) closed single boxes which allowed no visual and tactile contact with other animals, (3) group boxes (5 calves per box) or (4) group boxes with calves and mothers together (although cows were machine milked twice daily). When tested the heifers were 15-18 months old and on pasture. Heifers reared in closed single boxes (group 2) showed the least fear of humans, whereas heifers reared with their mothers (group 4) were very reserved towards humans. The author concludes that this indicates a sensitive period for imprinting in calves during the first three months of life (Krohn 1996). However, Creel and Albright (1988) did not find that calves reared in isolation socialized easier to humans as compared to individually reared control calves. All calves were reared according to the normal procedures for the dairy unit.

Intensive handling during rearing (including bucket feeding of milk to calves) of Simmental x Angus steers reduced both flightiness and sociability (level of attraction of herd mates). Moderate handling (e.g. intermittent yarding and drafting) reduced only flightiness. It was shown that the ease of drafting a single animal from its group in a pen

is improved most by handling experiences that reduce both flight responses to humans and the attractiveness of cattle (Matthews et al. 1997).

Pigs

Hemsworth et al. (1986b) found that early handling of pigs by humans in the first eight weeks of life increased their approach behavior to an experimenter in standard tests from 10 to 24 weeks of age. They concluded that early handling of pigs will influence the pig’s behavioral response to humans later in life. The authors could however not find any differences in approach to humans between pigs that had been artificially reared and pigs reared with the sow.

Hemsworth and Barnett (1992) studied pigs handled daily at 0-3 weeks, 3-6 weeks, 6-9 weeks or 9-12 weeks of age. Piglets in the 0-3 weeks and the 9-12 weeks handling treatments displayed reduced levels of fear of humans at 18 weeks of age. Results indicate that the 0-3 week period might be a sensitive period for socialization in which social contact may influence subsequent social relationships. The 9-12 week period was also effective, but this might be since it was the most recent period for handling. However, the results also indicate that the effects of early handling may dissipate or be overridden by the effects of handling later in life.

Pleasant handling of gilts six minutes daily during ten days at puberty was more effective in reducing fear of humans as compared to the same handling at two weeks of age (Pedersen 1997). The author concludes that handling closer to the period of puberty may have larger effects on fear response towards humans during reproduction, a time when frequent interactions between the caretaker and the animal are necessary.

Food awards

Chicks responded more easily to a food award to overcome fear towards humans, than did adult birds (Murphy and Duncan 1978).

In heifers, positive handling was reinforced with a food award (Boivin et al. 1992a).

Sows made more approaches and were much faster in approaching when an approach test was carried out in the presence of food (Seabrook and Mount 1993). Even ”aversively” handled animals approached more rapidly if small amounts of food were given. Seabrook therefore strongly recommends that food should be used as an operant conditioning in situations when negative stimuli cannot be avoided, such as castration and vaccination. Hemsworth et al. (1996b) found that pigs associate a rewarding experience of feeding with the handler, and that this conditioning results in pigs being less fearful of the handler and other humans.

Ability for discrimination

Stimulus discrimination can be defined as ”the tendency for stimuli similar to the original stimulus in a learning situation to produce the response originally acquired” (Reber 1988, in Hemsworth et al. 1994c). Through this process, the behavioral response of an animal to an individual human may extend to all humans. Such a generalized response to all humans may develop as a result of learning processes such as conditioning (in which conditioned approach-avoidance responses develop as a consequence of associations between the stockman and aversive and rewarding events), habituation or familiarity with the stockman (Hemsworth et al. 1996b).

The question is to what extent farm animals have ability to discriminate between humans and other stimuli and between different humans.

Cues for identification

Animals use cues to discriminate between humans. The most likely process underlying the discrimination ability is classical conditioning by which the animals learn which cues best predict how they are to be treated. Animals will learn to avoid cues associated with aversive events, and handler identity is one such predictive cue for the calves. More research is however needed to determine what cues animals can use to distinguish between people (de Passillé et al. 1996). Animals will often associate a negative experience with a particular place, and the location in which the handling occurs is another of the cues used. It has been shown that when handled in an aversive manner, cows will develop an aversion to the cue that best predicts the occurrence of the handling procedure (Rushen et al. 1995). Color appears to be yet another cue. Cows’ responses to people can change markedly when clothing color is changed, although this seems not to be true for poultry (Rushen 1997).

Discrimination between humans and other stimuli

Experiments have been performed to study whether or not animal behavioral responses to regular exposure to either humans or novel objects are stimulus-specific or generalized. It is generally found that while the reaction of a naïve animal may include a response of novelty or unfamiliarity, at subsequent experience there is a development of a stimulus-specific response to humans. This is found to be true both for cattle (Hemsworth et al. 1996a), pigs (Hemsworth and Barnett 1991; Hemsworth et al. 1990, 1991, 1996a), sheep (Baldock and Sibly 1990) and poultry (Jones and Faure 1981; Hemsworth and Barnett 1989). For example, Hemsworth et al. (1996a) found that both pigs and cattle reacted stimulus specific to humans performing positive handling. Baldock and Sibly (1990) studied a flock of five sheep. When it was approached by a man with a dog an average heart beat was induced of 79 beats per minute, while approach by man alone caused 45 beats per minute.

Handling does not depress general fearfulness in domestic chicks, but specifically reduces fear of human beings, presumably through habituation. Two strains of layer and one of broiler chicks were studied (Jones and Faure 1981). This was also found to be valid for Japanese quail chicks (Jones et al. 1991).

Duncan et al. (1986) compared the stressfulness of harvesting broiler chickens in a large flock by hand and machine. It was found that machine harvesting caused less stress in chickens, since chicken heartbeat returned to normal more quickly after machine handling, suggesting that the chickens were less frightened. Also, duration of tonic immobility was much longer in manually caught birds.

Discrimination between humans

Handling treatments varying in the nature of human contact, but not in the amount of human contact, can result in rapid changes in the level of fear of humans by farm animals (Hemsworth et al. 1981a; Hemsworth et al. 1986a, 1987a; Gonyou et al. 1986; Hemsworth and Barnett 1991). Farm animals may learn to associate rewarding or aversive elements of the husbandry with he handler conducting the procedure (e.g. Seabrook and Mount 1995; de Passillé et al. 1996).

In other cases, however, stimulus generalization may occur, in which the response to one human extends to all humans. Some of the few experiments performed in this field support this. It was found that pigs do not discriminate between different handlers, or even between familiar and unfamiliar people, but tend to generalize from their experience with one handler to all other handlers (Hemsworth et al. 1994c). Poultry handled gently by one person became less fearful of people in general and showed little evidence for discrimination between people (Jones 1994). Furthermore, as shown above adequate early handling of both cattle and poultry can reduce their fear of people in general and not just of a specific handler (e.g. Boissy and Bouissou 1988; Boivin et al. 1994; Jones 1994).

This discrepancy in results may be due to species differences or methodological differences between studies, such as lack of suitable cues on which the animals can discriminate (de Passillé et al. 1996). The different reactions may also be the result of a learning process. De Passillé et al. (1996) showed that calves treated in an aversive, neutral or positive manner by three different handlers (each handler giving consistent treatment) would first tend to avoid all three handlers. A kind of generalization had thus occurred. However, with further treatments, the calves’ contact with the positive handler increased and the aversive handler decreased, whereas the contact with the neutral handler remained constant. This also shows that some positive handling, not just an absence of aversive handling, is required for the calves to discriminate between handlers and to overcome a generalized fear of people resulting from aversive handling.

Cattle

For cows the color of the clothing is an important cue. Cows can readily learn to distinguish between two people wearing different color clothes, but have much greater difficulty distinguishing between people wearing the same color. (Rushen 1997). Munksgaard et al. (1997) found that adult dairy cows can distinguish between handlers based on how the handlers treat them, also in other locations than where the handling occurred. Their recognition is not based solely on the color of the clothes worn. Also, cows may not generalize their aversion to other people wearing the same colored clothes. The cows did not however respond to life size slide projections of the handlers.

Cows can learn to avoid or approach the same person in different locations, if they are handled differently in those locations. They can also readily generalize an approach or avoidance behavior to unfamiliar people based on the location (Rushen et al. 1995). Calves can have trouble generalizing a learned aversion to a specific person to locations other than where the handling occurred (de Passillé et al. 1996).

Boivin et al. (1992b) performed a series of tests with calves and young cattle, which indicated that the reaction to humans in animals having some experience with humans is stimulus-specific.

Dairy cows differed in their heart rate responses both in the holding area and in the milking parlor, depending on who was herding and milking them, with the relief milkers provoking the higher responses (p<0.01). This was in spite of the fact that the cows were milked in a herringbone parlor where most types of contact between the milker and the cow (like speaking to the cow or touching it) were difficult or impossible to perform. However, these findings should be interpreted with care since only a small number of animals were tested (Knierim and Waran 1993).

Dairy bull calves could after relatively few treatments learn not only to distinguish between friendly and unfriendly persons, but to some degree also that treatment can be related both to a person and to a special location (Ladewig et al. 1993).

That ability of dairy cows to distinguish between a gentle and an aversive handler may also affect milk yield. The presence of an aversive handler at milking reduced milk yield by 10% compared to baseline milkings or when the gentle handler was present (Rushen et al. 1997).

Holstein calves could readily discriminate between different people based on their previous experience. It was concluded that calves can develop a general fear of people as a result of aversive handling, and positive handling is required to overcome this. However, some calves do not generalize their fear of an aversive handler to places other than those in which they were handled (de Passillé et al. 1996).

Taylor and Davis (1996) tested dairy cattle for their ability to use individual humans as discriminative stimuli for the performance of an operant response. They concluded that

the ability of animals to differentiate individual humans has far reaching implications for research involving hedonic stimuli.

Sheep

Artificially reared female lambs could clearly discriminate between a familiar and unfamiliar caretaker (Boivin et al. 1997). Weaning occurred at 6 weeks of age, after which only a minimum of human contact was obtained, and lambs were then tested for human presence at 3, 6 and 14 weeks of age. The difference persisted for two weeks after the treatment concluded. At 14 weeks of age no difference was apparent. It was found that artificially raised lambs got as much ”social support” from the visual image of a familiar person through a plexi-glass panel, as from the real (Korff and Dyckhoff 1997).

Pigs

Pigs appear to use multiple cues to distinguish people, although visual cues are clearly important (Rushen 1997).

Hemsworth et al. (1994c) found that in situations in which pigs are briefly handled by one of two stockmen in a predominantly negative manner, or in which pigs are briefly handled by stockmen who differ markedly in the nature of their behavior towards pigs, it is likely that the pigs exhibit stimulus generalization as measured by their behavioral responses to humans. In such handling situations the behavioral response of commercial pigs to one handler is thus likely to extend to other humans.

Further experiments indicate that the pig associates a rewarding experience of hand feeding with the handler and that this causes the pig to be less fearful of the handler and other humans (Hemsworth et al. 1996b). On the contrary, gilts receiving frequent positive handling failed to associate an apparently aversive estrous detection procedure with the handler bringing her to the boar. There was also a tendency for the gilts to interact more frequently with a familiar experimenter than an unfamiliar one. The authors conclude that in some situations commercial pigs may learn to discriminate between humans.

Seabrook and Mount (1993) state that generalization of stimuli does not occur in pigs. The sows studied perceived, by experience and acquisition, different people in different ways depending on their behavior and actions. This was confirmed in a later study that showed that gilts can differentiate between different people (Seabrook and Mount 1995). It was also confirmed by a study by Tanida et al. (1995), in which pigs were individually handled by the same person for 10 minutes per day, five days per week in three weeks. Handled pigs interacted with both the handler and unfamiliar humans significantly (p<0.01) sooner and longer than did pigs in a non-handling control group, but given a choice they significantly preferred to interact with the handler. In conclusion, the handled pigs reduced their fear of humans in general, but they responded differently to familiar and unfamiliar humans.

Poultry

The behavioral response of caged laying hens to humans can generalize across a range of human attributes, including sex, height and the presence of spectacles, at least in those situations where the birds have previously been exposed to humans (Barnett et al. 1993).

Importance of the environment

Housing pigs in enriched pens significantly reduced their fear of humans, regardless of handling treatment (aversive or pleasant) (Pearce et al. 1989). When pigs were housed in groups, which can be considered as a kind of enriched environment, both Hemsworth et al. (1986a) and Paterson and Pearce (1989) found no effect of unpleasant handling measured as growth rate. This is also supported by the work of Arnone and Dantzer (1980), who showed that social interactions between members of a group made pigs able to resist the effects of stressors.

If the animal is kept in an indoor or outdoor environment makes a big difference in how humans are perceived by the animals, table 1 (Seabrook 1994). Outdoor environments are much more diverse than indoor environments, making the human less dominant.

The enriched environment of outdoor environment may also make the animals more able to cope with short-term acute stress and not get chronically stressed (Seabrook and Mount 1993). It is suggested that the space available per animal is an important factor also, making it possible for the animal in an outdoor environment to move away when handled unpleasantly or aversively (Seabrook and Bartle 1992a).

For poultry it has been suggested that the additional stimulation provided by early environmental enrichment may enhance the animal’s ability to adapt to novelty and hence reduce its fear-inducing properties (Jones 1985). The higher fear levels observed in hens housed in the top rather than lower tiers of a battery system may reflect this (Jones and Faure 1981; Jones 1985; Barnett and Hemsworth 1989).

How does the human caretaker influence the relationship?

In intensive livestock systems it is not possible to consider animal behavior in isolation from the behavior of the stockman.

Handling studies on cattle, pigs, poultry and sheep have clearly shown that the behavior of humans has a major influence on the behavioral response of these animals (e.g. Murphy and Duncan 1978; Hemsworth et al. 1981a; Boissy and Bouissou 1988; Hargreaves and Hutson 1990; Boivin et al. 1992a; Jones 1993). It has also been shown that stockman behavior influences animal production (see below).

Brushing (which implies a certain degree of restraint) did not seem to have a greater effect on beef heifers than did a simple passive presence. Weighing did not have the same effect as a less coercive contact. It was concluded that if human contact should improve subsequent relationships, animals should probably have an active role during handling (Le Neindre et al. 1993).

Schlichting and Schmidt (Schlichting and Schmidt 1986) found that the milker had an influence both on milk production and the fat content of the milk in a 121 cow university herd with 18 different caretakers.

In a study on commercial farms the time cows spent tongue-playing correlated negatively with the length the stockman spent in each farm (Sato and Okamoto 1996).

Studies of fear reactions to humans in laying hens showed that persistent changes in adult bird behavior, physiology and production can be made by manipulating human contact (Hemsworth and Barnett 1989; Barnett et al. 1994). Handling may improve growth rate, feed efficiency and resistance to pathogens in chickens (Jones et al. 1991; Gross and Siegel 1982a).

Pleasant or aversive handling – does it matter?

Studies regarding the effects of ”pleasant” or ”aversive” handling of farm animals have been performed both under laboratory conditions and on commercial farms. Most of this research has been performed at the Victorian Institute of Animal Science (VIC) under Dr. Paul Hemsworth, mainly on pigs but also on dairy cattle and laying hens. In the pig research the ”aversive” handling treatment discouraged pig approach to humans by either slapping or briefly shocking the pig with a battery-operated prodder whenever it tried to approach the experimenter. The ”pleasant” handling encouraged approach to humans by either patting or stroking the pig whenever it approached. Treatment was only imposed on pigs approaching or remaining close to the 37

experimenter. The handling treatments were in most cases conducted for short time (usually corresponding to actual handling regimes under commercial circumstances) either three or five times per week for a period of time. Fear of humans was recorded in a standard human approach test, measuring the time it takes the pig to approach an unknown human experimenter (Hemsworth and Barnett 1987a).

Research results show that the type of handling performed by the human caretaker has a profound effect on the farm animal (table 4, 5 and 6). The handling effects may show in several areas, e.g.:  general behavior  approach behavior  ease of handling  animal welfare  productivity  product quality.

Table 4. General response of dairy cows under different handling treatments (after Seabrook 1991 b) (p<0.05).

Action of cow Pleasant handling Aversive handling 9.9 16.1 Mean entry time to parlor, seconds per cow Flight distance (nervousness), 0,5 2.5 meters Dunging in parlor, 3.0 18.2 no. per hour Free approaches to humans, 10.2 3.0 per minute

Pleasant handling

Pleasant treatment consists of giving the animal pleasant stimuli, to make it associate the handler with pleasant feelings. It could be e.g. pats and strokes, handfeeding, consistent handling and communication (Seabrook 1984a; Hemsworth 1993).

Seabrook and Bartle (1992a) used telemetric heart rate measurements to register heart rate in ”aversively” or ”pleasantly” handled sows. Heart rates during ”aversive” handling treatments rose up to 230 beats per minute (bpm). For sows treated ”pleasantly” heart rates during treatment were in almost all cases below 130 bpm, implying that this handling did not stimulate the same ”emotional” response as ”aversive” handling.

There is little evidence that the mere presence of gentle people can have a positive effect on farm animals. The presence of a gentle handler was not found to increase milk yield of cows, or to reduce cows’ responses to novelty/isolation stress (Rushen 1997).

Aversive or threatening action

Aversive human behavior such as regular kicking, hitting and using a battery-operated goader will increase the level of fear of humans by the animals, measured for example as sustained elevation of plasma corticosteroid concentrations, heart beat rate or approach behavior. Aversive handling of pigs resulted for example in a marked reduction in the approach behavior to a stationary experimenter in a standard approach test (Gonyou et al. 1986; Hemsworth et al. 1981a, 1986a, 1987a; Hemsworth and Barnett 1991).

However, also some behavioral patterns which humans not intuitively perceive as threatening to the animals can appear so to them. Hemsworth et al. (1986c) found that a human standing in an erect posture, wearing gloves and approaching pigs is more threatening than a human in squatting posture, showing bare hands and remaining stationary. The regular performance of the former behavioral patterns by an experimenter was found to significantly reduce growth rate of young pigs to levels similar to that found with an aversive handling treatment (Gonyou et al. 1986).

In studies with poultry, fear reactions were greater when the experimenter stood 30 rather than 60 cm from the cage, and when the experimenter positioned himself so that his eyes were 30 cm below rather than above the height of the bird’s eyes. More fear reactions occurred when placing the hand rather than face 30 cm in front of the cage (Hemsworth et al. 1993b).

Inconsistent handling

Wiepkema (1987) emphasizes the importance of predictability and control by animals of their environment on their stress physiology. This is also underlined by Hemsworth et al. (1993a). Animals that can exercise some degree of control over an aversive stimulus and can predict its occurrence experience a lower stress response as compared to animals with less control over and less opportunity to predict the stressor. Aversive treatment can thus be experienced as less aversive if it is predictable and/or controllable.

Inconsistent handling can thus result in a negative human-animal relation and decreased growth in pigs. Hemsworth et al. (1987a) found the effects of inconsistent handling to be similar to those of negative handling, although negative handling in the experiment was imposed only on one out of five occasions. They concluded that this result has big implications for big commercial piggeries, where aversive handling by only one stockman is likely to have a substantial negative effect on animal welfare and production. 39

In a dairy herd, Hemsworth et al. (1989b) studied two different stockmen with different behavior, one person displaying a higher proportion of negative physical interaction with the cows. However, the stockman did not significantly affect the behavior of the cow. If this was due to inconsistent handling or other causes could not be determined.

Effects on production

The effects of pleasant vs. aversive handling have been studied in relation to growth rate as well as fertility in pigs, and significant effects have been found (see table 5). A few studies regarding dairy cattle have also been performed (Hemsworth et al. 1989b, 1995; Breuer et al. 1997).

Aversively handled animals have been found to have lower production. It is suggested that the decrease in production is caused by fear causing a chronic stress response which affects animal productivity. This has been shown for pigs in a number of studies (e.g. Hemsworth et al. 1981a, 1981b, 1986a, 1987a, 1989a, 1997; Gonyou et al. 1986; Hemsworth and Barnett 1991).

It was found that positively handled heifers, studied over early lactation, had lower weight loss than did negatively handled heifers (66.1 vs. 79.9 kg, p<0.05) and a tendency to higher milk yield. However, the experiment was terminated after a short time since a large percentage of the negatively handled animals became lame (44% compared to 11%) (Breuer et al. 1997).

In a study of commercial dairy farms, a highly positive correlation was found between the approach behavior of cows to a stationary experimenter in a standard test and the milk yield of cows. This indicates that the productivity of commercial dairy cows is depressed in situations in which the animals show marked avoidance of humans (Hemsworth et al. 1995).

Table 5. The effects of pleasant or aversive handling in pig production as reported by different authors. (Based on Seabrook and Bartle 1992a.)

Author/s Production Pleasant Aversive handling handling

Dryden and Seabrook Growth rate, kg/day 0,205a 0,192a (1986) 0-4 weeks

Hemsworth et al. (1987a) Growth rate, kg/day 0,456a 0,404a 7-13 weeks

Gonyou et al. (1986) Growth rate, kg/day 0,897a 0,837a 8-18 weeks

Hemsworth and Barnett Growth rate, kg/day 0,656a 0,641b (1991) 8-18 weeks (from 15 kg and for 10 weeks)

Hemsworth et al. (1981a) Growth rate, kg/day 0,709a 0,669a 11-22 weeks

Hemsworth et al. (1986a) Pregnancy rate % 88a 33a

Hemsworth et al. (1986a) Boar testicle size cm2 63a 53a

Hemsworth et al. (1986a) Age for fully days 161b 193b co-ordinated male mating

Seabrook (1991) Piglets born alive no. 10,1a 9,3a per farrowing – indoor sows

Seabrook (1991) Piglet mortality at 3 % 11,1a 15,2a weeks – indoor sows

Seabrook and Mount Piglets born alive no. 10,9a 10,8a (1993) per farrowing – outdoor sows

Hemsworth et al. (1996) Growth rate from kg/day 0,97 0,94 63 kg for four weeks a = p<0.05 b = p<0.01

The presence of an aversive handler at milking reduced milk yield by 10% compared to baseline milkings or when a gentle handler was present (Rushen et al. 1997).

”Pleasant” handling of sows alters their behavior. Stroking and scratching the sow’s head for a few minutes three times per day increased piglet growth and made the sows less restless. Slapping and hitting the sows made the sows restless and less easy to handle (Dryden and Seabrook 1986).

However, both ”pleasant” and ”unpleasant” treatment can cause piglet growth well over the control. This might suggest that handling provides a useful distraction for the sow from an otherwise monotonous life, thus both actions might act as stress reducing and lead to increased milk production (Dryden and Seabrook 1986). In chicks, application of a rough handling regime (regular suspension by the legs) reduced the chicks’ subsequent avoidance of the experimenter. This was interpreted as though human contact may have been rewarding in the context of the otherwise barren rearing environment (Jones 1993).

In some of the experiments, negatively handled pigs showed a significantly depressed growth rate compared to ”pleasantly” handled pigs but only in the beginning of the treatment period (Gonyou et al. 1986; Hemsworth et al. 1987a; Hemsworth and Barnett 1991). This could be interpreted as that habituation to the negative handling occurs, or that the treatments were most aversive to the pigs early in the study.

Indications of a chronic stress response

In a number of experiments, animals receiving aversive treatment had a sustained elevation of free corticosteroid concentrations, interpreted as a chronic stress response (Hemsworth et al. 1981a, 1986a, 1987a). Also in the absence of humans the mean daytime free corticosteroid concentrations of these pigs were higher than those of pigs in the ”pleasant” treatment group. They were also highly fearful of humans.

It is shown that aversive treatment resulted in adrenal morphology (increased area of cortex) which is indicative of chronic stress (Gonyou et al. 1986).

Hemsworth et al. (1981a) suggest that ”pleasant” treatment gives less adrenaline release and less stress in pigs, thus explaining the better production performance in ”pleasantly” handled pigs. In a further study it was concluded that the detrimental effects of stress are responsible for failures in the reproductive performance in aversively handled gilts (Hemsworth et al. 1987a). The impact seems to be bigger on the reproductive performance than on animal growth.

It is also suggested that the reduction in growth rate is due to the actions of elevated corticosteroid concentrations decreasing the incorporation of amino acids into tissues and mobilizing energy reserves, particularly proteins, to provide glucose as an energy source for the central nervous system. In relation to reproduction the adverse effects of stress on reproduction in farm animals are well documented, particularly for females (Hemsworth et al. 1991).

However, Hemsworth and Barnett (1991), Paterson and Pearce (1989; 1992) and Pearce et al. (1989) did not find any signs of chronic stress in aversively handled pigs, performing similar types of studies as the ones mentioned above. Paterson and Pearce strongly question the proposal that pigs are being chronically stressed by the aversive behavior performed, and also suggest that the measuring of cortisol secretion may not always be adequate for describing cortisol secretion.

Hemsworth and Barnett (1991) suggest that the discrepancy of their result compared to the majority of their findings is due to that a smaller sample of pigs were cannulated and tested for corticosteroid level in the blood. They explain the discrepancy of results obtained by Paterson and Pearce (1989) and Pearce et al. (1989) by different experimental set-up such as space allowance and endurance of treatment. These arguments are however rejected by Paterson and Pearce (1992).

Seabrook and Bartle (1992a) suggest that pigs’ ability to discriminate between people may explain these differences in results in spite of similar treatments. They also suggest that the differences in space allowance are of importance for the discrepancy, in that pigs with greater possibility to move away from an ”aversive” handling treatment will perceive the handling as less aversive as compared to the same treatment performed with constrained animals.

Hemsworth et al. (1993a) also point at that the animal’s ability to predict and control the handling might cause different results.

The aversive treatment in the above mentioned experiments did however influence the pig behavior, in that the aversively handled pigs were significantly more fearful of humans. Also, aversively handled pigs spent significantly more time resting and sitting and standing inactive and less time interacting with other pigs, as compared to pigs handled pleasantly.

Effects on behavior, ease of handling, animal welfare and product quality

”Pleasantly” treated sows in a large commercial unit behaved differently in the presence of the experimenter from sows treated ”aversively”. The pleasantly treated sows were relaxed and quietly grunting, looking ”expectantly” at experimenter. They appeared to be welcoming the experimenter by standing or sitting up slowly into a more accessible position for contact. The sows in the unpleasant treatment group appeared very restless in the presence of the experimenter, preparing either to fight or run away (Dryden and Seabrook 1986).

Increased amount of positive contact may improve the ease of handling of the animals (Gonyou et al. 1986). “Pleasantly” handled sows and gilts could generally be approached by the handler (Seabrook and Mount 1995). Sows handled ”aversively” could not so readily be approached by the handler.

There is limited evidence indicating that animals which are the most difficult to handle may have meat quality problems when slaughtered. Beef cattle that were most active and vocal when restrained in a weighing scale had most carcass bruising and tended to have tougher meat (Fordyce et al. 1985). The occurrence of pale, soft, exudative (PSE) meat in slaughtered pigs and dark firm dry (DFD) meat in cattle is known to be related to fear or stress before slaughter; thus handling which is fear provoking may increase the occurrence of PSE- or DFD-incidences.

In cases when animals experience a chronic stress response from aversive handling animal welfare is endangered (e.g. Hemsworth et al. 1993a).

Effects of stockman personality and attitudes

Personality is the dynamic organization within the individual of psychophysical systems that define his/her characteristic behavior and thought. Personality thus involves a person’s intelligence, bodily strength and health, interests, emotional and social qualities, drives, sentiments and interests (Seabrook 1984a). Seabrook also points out that personality consists of relationships between the individual and his/her observer, thus also being a process.

The personality or temperament of the stockman influences the temperament and behavior of the farm animals (Seabrook 1972a, 1972b; Stricklin and Kautz-Scanavy 1983).

Several studies have been performed on commercial farms, where the personality of the human caretaker has been studied and also related to animal production (e.g. Seabrook 1972b, 1984b; Hemsworth et al. 1989a; Coleman et al. 1995). Seabrook (1984b) showed that the average yield per cow and year radically changed with the change of herdsman in a group of twelve herds where all environmental, agricultural and husbandry factors were identical (table 6).

Table 6. Index of yield (average yield per cow and year) obtained from a six year study of 12 identical one-person dairy units (Seabrook and Bartle 1992a). Base year: 1966 (100) Average yield 1966: 2 917 litres per cow and year (low input/low output system)

Year 1 2 3 4 5 6

Mean index for 8 herds with no 100 99 102 89 98 97 change of stockperson Herds with a change of stockperson: Herd no. 1 100 102 * 91 * 92 * 72 * 74 Herd no. 2 100 98 104 108 * 72 * 74 Herd no. 3 100 102 * 118 * 135 118 120 Herd no. 4 100 101 102 * 125 * 124 119

* * indicates a change of stockperson

Seabrook (1990c) isolated the following traits of high-achievement, high-interaction stockmen (see also figure 1):  confident  emotionally stable  self-sufficient  independent  not affected by the system.

High producing herdsmen were attuned to the individuality of their cows and had a close identification with the herd. Another common trait among them was an interest in growing vegetables and roses, gladiolus or chrysanthemums – plants that all require specific treatment at specific times of the year (Reid 1977, in: Seabrook 1980).

Seabrook and Mount (1993) have related stockman characteristics and the type of animal interaction performed by the stockman (table 7).

The animals will also react on the day-to-day variations in the temperament of the caretaker. Purcell et al. (1988) observed that if the milker was in a hurry or appeared anxious, the cows’ flight and approach distances tended to increase.

Figure 1. Profile of the high achievement stockmen compared with the average profile of other stockmen (from Seabrook and Bartle 1992a).

Table 7. Stockman characteristics and animal interaction (Seabrook and Mount 1993)

Good interaction Poor interaction Source

Traits of stockman Confident Under confident Seabrook (1991b) Consistent Non-consistent Gonyou et al. (1986) Seabrook (1991b) Emotionally stable Less emotionally stable Seabrook (1991b) Independent Dependent Seabrook (1991b) Not affected by the Affected by the system Seabrook (1991b) system Low aggression High aggression Gonyou et al. (1986) Action of stockman Physical contact Lack of physical contact Gonyou et al. (1986) Seabrook (1991b) Use of voice in kind Aggressive tone of voice Seabrook and Bartle tone (1992a) Constant use of Lack of use of Seabrook (1991b) observational skills observational skills Operant conditioning; Punishment by Seabrook (1993) rewarding wanted aggressive handling behavior

Attitude and beliefs

The strongest predictors of stockman behavior have been found to be stockman attitudes. These attitudes and consequent behaviors predominantly affect the animal’s fear of humans (Coleman et al. 1995). Stockman attitudes may also be related to aspects of work apart form handling of pigs (Hemsworth et al. 1994a). These findings were later confirmed by a similar study performed in a large commercial piggery (Coleman et al. 1998).

Hemsworth et al. (1989a) refer to the work of Ajzen and Fishbein (1980), who have developed a theory of reasoned action, which they propose can be used to predict human behavior. According to this theory, a person’s intention to perform a behavior is a function of the person’s attitude towards the behavior and the person’s perceptions of the social pressures on the performance of the behavior (referred to as the subjective norm). In addition, it is proposed that both attitudes and subjective norms are a function of beliefs. This approach is summarized in figure 2. The attitude towards a behavior can be measured by questions relating to that specific behavior.

Applying this theory to pig production on large commercial farms, Hemsworth et al. (1989a) found that the attitude of the stockman towards petting pigs and the proportion of physical interactions by the stockman that were negative in nature, were significantly (p<0.01) related to the time taken for sows to physically interact with a human in a standard test. The stockman attitude could also be linked to the animal performance. For 47

example, the attitude to the use of verbal effort in moving pigs and the number of physical interactions of an intense negative nature were both highly (p<0.01) related to the total litter size.

Figure 2. Factors determining a person’s behavior according to Ajzen and Fishbein (1980). Arrows indicate the direction of influences. (From Hemsworth et al. 1989a).

Coleman et al. (1995) showed that negative beliefs about pigs as animals correlated significantly (p<0.05) with the observed number of negative interactions by stockmen. The same was true for positive beliefs.

It is most likely that the stockman’s attitude and behavior become mutually reinforcing through interactions with pigs. For example, if negative or aversive behavior by the

stockman towards the pig leads to avoidance or escape behavior by pigs, then in time this would reinforce the belief that pigs are difficult to handle (Hemsworth et al. 1993a).

Changes in attitude will also change the relationship between the stockman and the animal (Coleman et al. 1995).

Stockmen on farms with 75-300 breeding sows could successfully be trained to change behavior as well as change attitudes and beliefs, using a short training program (Hemsworth et al. 1994a). As a result of the training, stockmen displayed significantly less negative physical interaction with the pigs and an increase in total score in attitude tests. These changes corresponded to a reduction in fear level among the pigs, and a strong tendency to improved reproduction among sows (p<0.11).

Similar results were obtained in a study on large Australian commercial farms. A significant improvement in stockman attitude towards interacting with pigs was noted in the modification group as compared to a control group, which had received no training to modify attitudes and behavior towards pigs. There was a significant decrease in the proportion of negative interactions with pigs by the modification group compared to the control group, and a reduction in time for pigs to withdraw from an approaching stockman (Coleman et al. 1995).

Vocal interaction as reflecting stockman attitude

Seabrook and Mount (1993) have indicated that the vocal interaction between the stockman and the animal occurs at different levels: talking ”to” the animal, issuing commands or comments, as opposed to talking ”with” the animal, where there is almost an expectation of a response (table 8).

In one study, 73% of the stockmen with low aggression scores spent more than 15 minutes per day talking with their animals, while none of the stockmen with high aggression scores spent more than 15 minutes talking to their animals (Seabrook 1994).

Hemsworth et al. (1994a) conducted attitudinal profiles of a sample of stockmen. Their results show that the attitude to the use of verbal effort in moving pigs was highly (p<0.01) correlated to the total litter size.

Aggression

Seabrook (1994) used Cattell’s 16 Factor Questionnaire to establish the stockman aggression level in a study performed on six very large intensive indoor pig units. He recorded that 73% of the stockmen with low aggression scores spent more than 15 minutes per day talking with their animals, while none of the stockmen with high aggression scores spent more than 15 minutes per day talking to their animals. The level of aggression can however change over times and is e.g. dependent on the prevalent attitude of the farm workers on the farm unit and the management (see ”Human habituation” below).

Table 8. Vocal interactions as recorded in two pig units (from Seabrook and Mount 1995) (p<0.05).

Type of stockman Talking ”with” sows Talking ”to” sows Times Words Times Words / sow / hour / sow / hour / sow / hour / sow / hour

Stockmen showing good 5.8 84.4 4.3 55.6 interaction Stockman showing weak 0.0 0.0 0.4 2.1 interaction

“Stockmanship” – managing the interaction

Definitions

Stockmanship can be defined as “knowing the individual behavior of every animal in one’s charge, and having the ability to recognize small changes in the behavior of any animal or all of the animals collectively” (Seabrook 1980).

Observation is a key ingredient in stockmanship with a willingness on the part of the stockman to correct the conditions causing the deviation from normal behavior patterns (Albright 1986).

Hemsworth and Barnett (1987a) states that one of the main objectives of good stockmanship should be to achieve and maintain a good human-animal relationship in which pigs are not fearful of humans.

English (1991) have presented a more comprehensive definition:

Good stockmanship involves a well-molded combination of 1. A sound basic knowledge of the animals and their requirements. 2. A basic attachment to and patience with the stock. 3. The ability and willingness to communicate and develop a good relationship with the stock (empathy). 4. Ability to recognize all individual animals and to remember their particular eccentricities 5. Keen sensitivity for recognizing the slightest departure from normal behavior of individual animals. 6. An ability to organize the working time well. 7. Having a keen appreciation of priorities with a ready willingness to be sidetracked from routine duties as pressing needs arise to attend to individual animals in most need of attention. Empathy is included in number 2,3,5 and also influences number 6. It thus appears as a very crucial component of stockmanship.

Coleman et al. (1998) are however criticizing the use of the word “empathy” as made by English (1991). They state that the word refers to the capacity to “vicariously experience the emotions of another”, and that it is not necessary that there be a pre- existing bond between the observer and the other. From a computerized questionnaire survey made on stockmen in a large industrial piggery they found that stockman empathy did not predict the behavior towards pigs but there was some limited evidence to suggest that empathy might contribute to predicting other job-related variables.

Beynon (1991) states: ”Stockmanship can be seen as a human activity that applies the ability, knowledge, skills and common sense necessary in optimizing health, welfare, husbandry, management, and thereby both physical and financial performance, in animal production.”

Seabrook and Bartle (1992b) identify three components of stockmanship: 1. Management of environment – e.g. breeding and feeding policy, effective record- keeping, routine health care etc. 2. Operative stockmanship – e.g. technical ability and stock skills 3. Empathetic stockmanship – e.g. the qualitative manner of interaction; the manner of handling the animals, the degree of which small changes in the behavior of animals are observed, the perceptive and observational skills applied. All three are considered essential for ”good stockmanship”. The authors comment that to some extent the Management of environment component and the Operative stockmanship component are more easily described than the Empathetic component. Table 9 presents interaction factors associated with the development of good empathetic stockmanship.

Table 9. Developing interaction factors associated with the development of good empathetic stockmanship (Seabrook 1988; Seabrook and Bartle 1992a).

Factor in the relationship Action of the stockman

Operant conditioning Reward favorable behavior of animal; use food and other positive stimuli as a distraction for negative interaction Physical contact Stroking, scratching head and patting pig Social identification with the animals Use of voice and social gestures Stability Consistent and confident actions Handling Non-aggressive behavior Observation of animals Effective development of perceptual skills

“Eye for the animals”

A Swedish research project tried to pinpoint a trait which in Sweden is called “an eye for the animals”, i.e. that special kind of competence and special attention by which a stockman is sensitive to the special needs of the animal and at the same time makes it produce well (Ledin and Lema 1996). Based on interviews and participatory observations in dairy herds the authors came up with the following list of characteristics of a person having this “eye for the animals”:  A sincere and deep interest for the animals and the production  Good knowledge of the normal animal behavior, thus ability to discover aberrations on an early stage  Willing to put down the time needed in the herd  Excellent ability for observation  Some experience from milk production and animal husbandry  A calm and collected person with a lot of patience.

In a study of high-producing dairy herds it was concluded that the high production stockman is able to minimize the output of adrenaline by the cow and thus obtain a higher percentage of the milk yield permitted by her genetic capacity. This is achieved by the constant attention to the behavior patterns or performance of each individual cow in the herd. The best stockmen were attuned to the individuality of their cows, and had a close identification with the herd (Reid 1977, in Seabrook 1980).

Loose housing dairy herds where the farmer showed an intimate contact with his cows displayed a low frequency of agonistic behavior between cows and a high frequency of licking (Menke et al. 1994).

Human habituation – the importance of setting good examples

Seabrook (1994) has pointed out the importance of good management. He studied very big commercial indoor pig units in England, and found that if the unit manager himself was a high interacter with animals and had a low aggression score, the levels of aggression in the staff in those units were less (see table 10). He explains this by ”habituation”, i.e. the process in which an action towards animals becomes accepted by frequent application or custom. It can occur in response to the workload and pressures created in the system, and it also reflects the fact that for many stockmen coming into the units their only role model was the existing staff.

Seabrook also describes other psychological mechanisms reinforcing the habituation process (exemplified by statements made by stockmen in the study) such as:

Suppression, where feelings of basic desire to care may be suppressed in order to cope with a basically unacceptable situation for the animals, or

The terminal concept, where the stockman may wish to reinforce their psychological distance from the animal by deliberately not relating or interacting with it, knowing that the animal will be killed and eaten.

Table 10. The distance piglets were thrown into the transport trolley by different groups of stockmen working in farrowing houses; entries are % of group. (Seabrook 1994) (p<0.05).

Group Average distance per stockman

< 0,5 m 0,5-1,0 m > 1,0 m

All new staff at 1 month (n=18) 66,6 27,8 5,5 New staff at 1 month, on units where managers 50,0 33,3 16,7 had low aggression scores (n=6) All new staff after 6 months (n=18) 33,3 50,0 16,7 New staff after 6 months, on units where 83,3 16,7 0,0 managers had low aggression scores (n=6)

Effects of modern technology on the human – animal relation

It should be noted that no separate literature search has been performed on the effects of the introduction of modern techniques on the human – animal relation. However, findings in the literature obtained with other search words are considered interesting enough to be presented under a separate heading in this paper.

In the best case, the introduction of modern technology in animal production may release people from a routine workload, allowing more human-animal interactions and better care. The reduced work and drudgery could ease the stress on the worker which in turn may lead to a more humane handling of livestock (Albright 1993).

Other authors claim that the introduction of new technology have reduced both time and closeness in human-animal interactions (Ekesbo 1983; Seabrook 1984a; Knierim and Waran 1993). New technique has not denied the possibility of physical interaction between man and animal, but has created an environment in which the work ceases to demand such interaction. However, research results conclude that if the interaction is effective herd results will be better (Seabrook 1984a).

Increasing automation reduces the opportunities for habituation to occur. All the necessary contacts with human beings during husbandry are then likely to become more traumatic to the animals (Duncan 1990). Seabrook (1994) states that the benefits of electronics to the animals from a welfare point of view will accrue only if the stockman spends time interacting with the animals. In particular the role of operant conditioning is important, using food and other pleasant stimuli to reward desired behaviors and provide positive interaction with the animals.

Hemsworth and Barnett (1987a) put forward a different view on the introduction of modern technology. They are of the opinion that animal husbandry in early agriculture, when the herder provided the animals with food, water, shelter, protection and grooming, provided a close contact between human and animal. As agriculture advanced further with the introduction of technology and push for management efficiency, the animals were transferred into more intense systems in which they were enclosed in pastures or fields, with more animals managed per unit of labor. Thus the amount of contact between human beings and animals was decreased. In modern production systems the level of contact with human beings is more intense again. They point at the pig industry, which has induced a higher level of contact e.g. when the stockman detects estrous in the sow, assists the sow to mate or to farrow.

The use of modern technique and machinery can also mean less stress for animals not used to human handling. Duncan et al. (1986) compared the stressfulness of harvesting broiler chickens in a large flock by hand and by machine. The manual method was the traditional technique of catching the birds by hand, inverting them and carrying them by one leg in a group of five over a short distance. The machine picked up the birds by two counter-rotating rotors fitted with soft rubber fingers. Heart rate of birds was measured as they were harvested, using telemetric technique. The results suggest that stress could be reduced and welfare improved by using a carefully designed machine rather than by hand. It is thought that one of the advantages of the machine is that it restrains the birds for a very short time (Duncan 1990).

The effect of the milker was found to be different in different types of housing systems. The milker had less effect in a strawless tying stall or in a cubicle house, as compared to a tying stall with straw. The authors conclude that ”people-neutral” housing systems

should be promoted to reduce the negative influence of people on milk yield of cows (Schlichting and Schmidt 1986).

In a study of ten Swiss farms it was found that in cowsheds cows were more touched but less talked to during milking time, as compared to cows in cubicle stalls (Wyss et al. 1993). The mean number for the "sum of touching and talking" per cow was higher for cows in cow-sheds (1.59) than for cows in cubicles (0.68).

However, the use of new technique ought to be considered from many aspects. The milking position in the herringbone parlor (from behind and partly under the cow) resembles the natural suckling from behind, which naturally occurs in only 5-8% of the natural sucklings. Only the hind legs and the udder can be touched by the milker. These parts are not normally used for petting or communicating with the cow. In addition, the throughflow of the herd is usually high, allowing only a minimum amount of time spent per animal (Knierim and Waran 1993). The conclusion is that the human-animal relation could possibly be affected if the method used for milking more resembled the natural parallel-inverse suckling position of the calf. They also suggest that ethological aspects should be given more considerations in the construction of milking parlors in order to increase animal and human well being.

The human-animal relation might also moderate the effects of the technique used, e.g. the housing system. It has previously been shown that the housing system affects the welfare of the animal (e.g. Ekesbo 1966; Barnett et al. 1991). One preliminary study has been made to test the hypothesis that an improved human-animal relationship might obviate previously demonstrated negative effects of a housing condition, in this case for pregnant sows in tether stalls. The results support the hypothesis that the nature of the human-animal relationship affects the physiology of tethered pigs, and that a positive human-animal relationship obviated some of the negative effects by lowering the physiological stress level and by strengthening the immunity (Pedersen et al. 1998).

Large scale animal husbandry

The agricultural structural rationalization tends to continuously increase herd sizes. This creates special problems, for example that the herdsman can spend less time with each individual animal. What this means for the individual animal as well as for the herdsman has not been studied in particular in any of the articles included in this study. Albright (1993) is mentioning the problem, stating that in smaller herds the stockman can to a certain degree allow the cows to develop their own individual personality. Mass handling of cows dictates that individual cows fit into the system rather than the system conforming to the habits of the cow.

The effects of the scale also depend on the human involved to run the system. Seabrook (1975) questioned a homogenous group of cowmen, working on one-man units with herringbone parlor/cubicle housing systems where silage was fed, how many cows they would be prepared to milk in their present system. Their answers were related to their present milking herd and their personality. 55

Also, one study revealed a strong correlation between herd size and occurrence of diseases at different education levels of the stockman, the disease incidence being inversely related to the subjectively assessed ability and training of the cowman (Hamann 1994). Hamann further argues that there seems to be a certain minimum of man-hours per cow necessary to get an optimum efficiency in milking. This period should not be shortened, even in connection to additional automation.

Discussion

The study of the human - farm animal relationship

A close relation between man and animal was a necessity for earlier generations of farmers and the relation still is an important part of the everyday life of the modern stockman. The relatively few numbers of scientific studies presented within this field of study do not correspond to its importance. This implies that many aspects of the relation still remain to be scrutinized by science, a task necessary in order to create an optimal relation both for the human caretaker and the farm animal. This is a question of animal welfare as well as of human welfare (expressed as a good working environment and increased work satisfaction). However, most studies covered in this literature study are performed only recently, indicating a growing interest in this field among researchers as well as funding agencies and a recognition of its importance.

It is interesting to note that the historical development seems to be looked upon somewhat different depending on the cultural background of the viewer. In Northern Europe the development is generally perceived as going from an intense relation in the traditional farming systems to a reduction in closeness when modern techniques are introduced (Ekesbo 1983; Seabrook 1984a; Knierim and Waran 1993). The Australian authors Hemsworth and Barnett (1987a) consider contemporary farming to increase closeness between man and animal as compared to the extensive grazing systems prevailing earlier. Thus the industrial farming systems face problems related to fear of humans and animal stress associated with this. The initial response for all animals reared without contact with humans is still fear, in spite of the long history of domestication in the case of farm animals (Murphy and Duncan 1978; Murphy et al. 1981). Modern large scale farming systems where human presence is minimized due to labor costs often do not allow animals getting used to the necessary handling, in spite of the forced closeness in certain situations. The Hemsworth group has focused their extensive research on these problems, reaching their great achievements from a problem understanding that (at least to start out with) differed from how the situation was perceived in Europe.

One reason why the research area has not been penetrated by research earlier is probably that the human - farm animal relationship is not easy to study scientifically. The problems vary with the different aspects of the relationship that are scrutinized. These will be considered in the following.

Animal reactions to human handling

This literature study clearly shows that there are many methodological problems related to the study of animal reactions to human handling. The list put together by Seabrook and Mount (1995) includes the individuality of animals in their reactions to the same type of handling and that there may be e.g. diurnal patterns in their ethological as well as physiological traits. Great individual differences are also displayed between human handlers, causing unforeseen variations in the experimental accomplishment. Some of these variations may be due to factors mentioned by Seabrook as “holistic empathetic interaction”, having received only limited interest from research so far.

The animal’s earlier experiences of humans have impact on its reactions when handled. This includes the early imprinting and socialization that develop the social skills in the young animal, including in relation to humans. The importance of these early experiences has probably been overlooked in many studies. It is for example of great importance if the animals are reared in visual isolation from others of the same species (Krohn 1996). Conditioning is also important in this context: The way studied animals are handled by the maintenance personnel influences their reaction towards an experimenter. The setting where the experiment is performed (indoors/outdoors, individual testing/group situation etc.) is also of importance when interpreting the results. Habituation to handling may also occur over an experimental period (Gonyou et al. 1986; Hemsworth et al. 1987a; Hemsworth and Barnett 1991).

A major difficulty is that we cannot read the minds of the animals. What we believe to be a pleasant/aversive handling might not be perceived as such by the animal. Humans in an erect posture wearing gloves may be perceived as aversive (Hemsworth et al. 1986c) while intendedly aversive handling may for example be perceived as a positive change in a monotonous environment (Dryden and Seabrook 1986).

A major problem is that once you try to measure animal reactions to a certain type of handling you may also influence it. Thus there has been criticism raised against the use of plasma free corticosteroids parameters for measuring the stress reaction in animals (e.g. Seabrook and Bartle 1992a). The use of non-invasive techniques (such as measuring heart beat via radiotransmitters or the analysis of vocalizations) seems to be a possible way around this problem. The standard approach test used by the Hemsworth group for testing fear of humans in pigs entails the problems that the pig might not be interested in socializing with the experimenter, or pig approach time may well be influenced by other human messages/signals and environmental influences. Seabrook and Bartle conclude that while the results are of interest they must be seen to have limitations. (This statement is supported by reference to unpublished data by Seabrook.) This could explain some of the discrepancies in results, e.g. regarding whether pigs generalize their experience from one human to all humans or not (Hemsworth et al. 1994a, 1996b; Seabrook and Mount 1993).

An area where basic knowledge is lacking is how the animal actually perceives its environment including the human caretaker. To be able to create an optimal close environment and also from an animal welfare point of view it is of great importance to know such facts.

The human component

The human is the other component in the human – farm animal relationship, and a complete study of this relationship must of course include the human. Although few studies have included the human, it has been shown that the personality and attitudes of the stockman influence the behavior and production performance of the farm animals (e.g. Seabrook 1972a, 1972b; Coleman et al. 1998; Stricklin and Kautz-Scanavy 1983).

In many modern systems the human is crucial for animal welfare since farm animals are almost completely dependent on the human in these systems. Hemsworth and Coleman (1998) state: “Understanding stockman behavior appears to be the key to manipulating these human – animal interactions to improve animal performance and welfare, as well as the stockman’s attitude and motivation regarding the job.”

The type of handling performed has a profound effect on the animal. Significant results have been obtained when negative handling is limited to very short periods but performed regularly. Aversive handling treatments involving brief shocks with a battery-operated prodder or brief slaps whenever the animal approached or failed to avoid the experimenter, daily imposed for only 15-30 seconds, consistently resulted in pigs showing less approach to humans when subsequently tested with a stationary experimenter in an unfamiliar arena (Hemsworth et al. 1981a, 1986a, 1987a; Gonyou et al. 1986; Paterson and Pearce 1989; Pearce et al. 1989; Hemsworth and Barnett 1991).

However, the study of the human component in the relation poses difficulties. Here a true interdisciplinary scientific work is needed, where natural scientists must work in close co-operation with psychologists or social scientists to create a complete picture. There is a reluctance to establish this type of scientific studies due to tradition and the fact that such are not encouraged by the present academic reward system. This can be one reason why such studies are not very frequent in the literature. However, some successful work of this kind has been performed. Seabrook has used validated psychological tests of personality in several studies to explore stockman personality (Seabrook 1972b; 1975; 1991). Similar methods have also been used by Hemsworth and Coleman (e.g. Hemsworth and Coleman 1998). Lidfors et al. (1999) collaborated with psychologists, who made several different personality tests with the milkers in a large Estonian dairy heard. An innovative study in this field concerns “an eye for the animals”, where an animal scientist and a sociologist worked in close co-operation to analyze this subtle phenomenon (Ledin and Lema 1996).

An interesting question not yet studied is if there are gender differences in the interaction with animals. If so, this could account for some of the obtained discrepancies in results, e.g. for pigs when discriminating between humans on the basis of previous handling experience.

Unfortunately it has not been possible in this study to also include the importance of the animal relation for the human. Although there are several studies regarding the importance of pet animals for their owners (see e.g. Edney 1992), few studies seem to be made regarding this aspect of animal husbandry. Hemsworth and Coleman (1998) has touched upon the issue, reporting a survey made within the Australian pig and dairy industry. Several hundred stockmen were interviewed regarding various aspects of their job. A clear majority (86% and 76% of the pig and dairy stockmen respectively) enjoyed working with their animals. The authors draw the conclusion that it is not unreasonable to suggest that working with animals provides stockmen with a number of benefits, such as companionship and a commitment and interest that offer both responsibility and a sense of satisfaction for the health and welfare of lives other than those of themselves or their families.

Seabrook (1995) has drawn some general conclusions regarding the different aspects of the human – animal interaction and divided them into three interrelated components: hand and arm interaction, vocal interaction and holistic empathetic interaction. This division demonstrates where scientific efforts are lacking, namely regarding the last component. Very little basic research has been done in this area. Interdisciplinary research of the kind mentioned above is required to further develop this field. The work by Ledin and Lema (1996) can be seen as an introduction into this field.

Lack of this kind of research is probably one reason why basic knowledge is lacking regarding the components constituting a good relation. Only few authors have stated something about this, and they make it in general terms such as: “Mutual emotional attachment” (Seabrook 1986) “communication and confidence” (Albright 1986), “empathy” (English 1991). Seabrook is one of the relatively few authors who, based on his own and others’ research, is elaborating these ideas and drawing extensive conclusions for the everyday handling of farm animals (e.g. Seabrook 1992; Seabrook and Mount 1993). Empathy is also considered to be an important part of good stockmanship, although Coleman et al. (1998) criticize the use of the word empathy arguing that it does not presuppose a relation. Hemsworth and Barnett (1987a) present a more limited definition of stockmanship, focusing only on fear: “Maximize positive behavior, minimize negative behavior to minimize fear”. They relate to the large scale Australian farming, especially the pig industry (to a large extent run with low paid, low- status workers). Their conclusions are that it is possible to change the attitudes of stockmen and thus obtain more positive behavior towards farm animals and better animal welfare. They have also done encouraging work to put this into practice, developing training procedures for stockmen.

Practical consequences

Human action is of great importance for the animal. Research has indicated that human handling may even ease the effects of a bad environment. This leaves the stockman with a great responsibility in the daily work with farm animals. Current knowledge of animal behavior should be applied in all handling of animals. Information and education of stockmen is thus crucial, and the work done by the Hemsworth group shows that this can change daily routines and improve animal welfare and production.

From this literature study some practical conclusions can be drawn regarding human behavior towards the farm animals.

Daily interaction and routines

Consequent pleasant handling is the key to good husbandry. It should be performed in an atmosphere of confidence and stability and characterized by good stockmanship e.g. as described by Seabrook in table 9. Consistent action should be pointed out as especially important since it provides predictability. The effects of inconsistent handling may be similar to those of negative handling (Hemsworth et al. 1987a).

The hand, arm and vocal interaction (discussed by Seabrook 1995) should consistently be of positive nature. There are several studies performed regarding the first type of interaction, the work done by the Hemsworth group giving some of the major contributions in this field. The vocal interaction is much less studied. As mentioned earlier, the last type of interaction distinguished by Seabrook, the holistic empathetic interaction, is hardly studied at all which is a drawback when defining good daily interactions and routines. In several of his articles Seabrook has identified the correct actions of the stockman in order to create a good stable interaction on the basis of relevant scientific research. (Such actions are summarized in table 7 and 8.)

Seabrook (1988) suggests that the human should adopt stimuli used in the social communication between animals, to establish social bonds with the animal. The stockman’s role in the herd can be supported by the use of social communication signals (boss animal, mother substitute, social object etc). This technique is also described from indigenous, cattle rearing people, and it is also used more or less consciously by skilled stockmen. However, the technique should be further studied and made fully conscious, in order to make it a useful tool in the human – animal interaction. It must of course be adapted to species differences – the chicken views the world differently than a pig, and behavior that might be perceived as threatening for a chicken is not necessarily so for the pig.

A question arising is: should the stockman strive for omitting negative action or should he/she strive for positive handling? An interesting fact in this context is that although the presence of an aversive handler depressed the daily milk yield in dairy cows, the presence of a gentle handler did not increase milk yield (Rushen 1997).

However, the attitude to just omit negative action is incompatible with an empathetic stockmanship of the kind described by Seabrook (1988; Seabrook and Bartle 1992b). The limits for positive handling would then only be where the animals get too tame for handling; a situation which is not very likely in modern animal husbandry where one stockman is responsible for large herds.

There is strong evidence for the beneficial effects of positive handling. Pedersen et al. (1998) showed in a study of tethered pregnant sows that a positive human – animal relationship obviated some of the negative effects of being tethered, by lowering the physiological stress level and by strengthening the immunity system of the animals. It has been shown that some positive handling, not just an absence of aversive handling, is required for calves to discriminate between handlers and to overcome a generalized fear of people resulting from aversive handling (de Passillé et al. 1996). Gonyou et al. (1986) found that increased amounts of positive contact may improve the ease of handling.

Minimize fear of humans through habituation

There are many benefits if farm animals do not display fear of humans. Tame animals are much easier to handle and pose less risk of harm onto themselves or to the handler. It is also a question of animal welfare, since the chronic stress responses caused by fear of humans may cause animal suffering. Also, this stress response has effects on animal productivity. Much effort has been made to examine these relations scientifically.

It will give economic benefits to habituate the animal to human presence and reduce stress. The habituation should be accomplished through optimal use of any period in the animal’s life during which it is more prone to bond to humans.

This literature study shows many indications of the existence of such sensitive periods. The study of the species’ natural behavior could increase our understanding further of this phenomenon. For example, the fact that handling of new born calves does not increase their openness for human contact later in life may be due to that they naturally do not socialize with others during this first period of life (Boivin et al. 1992a). Handling performed a few weeks later may have much bigger effect, since this is a period when the calf naturally seeks contact and establishes bonds to others. In fact, in cattle sensitive periods seem to be a few weeks after birth, at weaning and at first calving. Hemsworth et al. (1986b) found that human handling of pigs early in their life (during the 0-3 week period) can influence the subsequent response towards humans. However Pedersen (1997) found that the best effect for socialization in pigs is the period around puberty.

It can be noted that just restricting the animals by tying them up has no effect on their fear of humans (Boivin et al. 1995). It is important that animals become used to the specific type of handling of which they will be exposed. Sato et al. (1984) showed that although calves display low levels of fear for humans after being regularly caressed, 62

they still showed great resistance towards being lead with a halter. Le Neindre et al. (1993) suggest that the animals should have an active role if the handling is to improve the relationship.

Young animals reared in isolation seem to bond more easily to the human caretaker. This is clearly demonstrated in the experiments done by Krohn (1996): Heifers reared in closed single boxes without any contact with their conspecifics showed least fear of humans, whereas heifers reared with their mothers were very reserved towards humans. Arave et al. (1985) found that calves reared in isolation yield more milk. This opens up for an ethical dilemma: Should we allow the animal a natural behavior including the identification with its own species, although this might mean that the animal becomes more stressed when handled by humans later in life? The solution might be in finding the optimal degree of imprinting or conditioning. Animals that are too tame could also cause problems since they attempt to force human attention and may be more difficult to handle as compared with animals displaying a certain amount of respect for the human caretaker (Waran 1995).

Minimize the effects of unavoidable negative handling

It is difficult to avoid all handling perceived negatively by the animal, e.g. medical treatments. However, knowledge gained in applied ethology can be used to minimize the negative effects of this type of actions.

Aversive action may be perceived as less aversive if it is predictable and/or controllable (Hemsworth et al. 1993a). The use of clear signals regarding what type of handling to expect will provide a more predictable environment for the animals. The use of special coloring clothing (Rushen 1997) or special treatment pens during aversive management procedures is one way to reduce the development of fear of the handlers. For example, de Passillé et al. (1996) showed that aversive treatments carried out in a special place are less likely to lead to a generalized fear of people than would be apparent in other places. Thus applying these procedures in special places outside the animal’s home pen would help in minimizing the effect of negative handling.

An enriched environment, such as housing in enriched pens or outdoor housing, reduces fear of humans (Pearce et al. 1989; Seabrook and Bartle 1992a). This also includes social organization, which enables members of a group to sustain emotional stimulation more efficiently (Arnone and Dantzer 1980). This indicates that animals become less stressed if handling is performed in the presence of group mates rather than in separation from their peers. It raises the question of the importance of a natural behavior. Animals prevented from expressing a natural behavior suffer from stress and will in certain situations probably be less likely to bond to humans. However, in a situation when the stress comes from social isolation especially young animals will be more likely to bond to the human caretaker.

Food awards are very effective as operant conditioning to minimize the negative effects of aversive handling that can not be avoided (Seabrook and Mount 1993). In studies of 63

pigs it was found that these not only result in pigs being less fearful of a specific human but the animals could also generalize to other humans (Hemsworth et al. 1996b). This ability for generalization seems to be true also for cattle and poultry.

Assessment of animal individuality ("temperament")

Individual responses by different animals to different stimuli are the norm and not the exception. This individuality of the animal – termed "temperament" by Seabrook and Bartle (1992a) – must be assessed and taken into consideration by the handler when interacting with the animal. The stockman must be able to match the individual requirements of individual animals. This is the essence of good stockmanship. Seabrook and Bartle (1992a) state that it is possible to isolate behaviors like the perceptive skills and to adopt or train these. This is confirmed by Ledin and Lema (1996). The ability to assess animal temperament is one of the key features of people possessing "an eye for the animals". These people have a finely attuned perceptive capacity of the individual animal. The authors state that although this ability to some extent is made up by a hereditary component, there is also an experiential component that can be trained. However, this kind of personal competence can not be transferred to other persons through description only, but has to be learned through example. To obtain a personal integration of this type of "silent knowledge" impossible to describe, transfer of knowledge should be made in the environment where the knowledge is to be used, that is in a herd together with a skilled and interested stockman.

The effects of modern technology

When new technology is developed, it is crucial that ethological and veterinary knowledge is applied in order to adapt technology to the biological prerequisites of the animals and what we know about the interaction between the stockman and the farm animal.

Modern technology cannot per se be said to have decisive positive or negative effects on the relation between the human and the farm animal. Thus, some authors suggest that the technique will allow a better contact since much routine work can be omitted through the technical development (Albright 1993), while others think that modern technique has deceased both time and closeness in the relation (Seabrook 1984a; Knierim and Waran 1993).

Instead of the technology, it might rather be factors outside the farm and particularly the economic pressure exerted on farms today that creates problems, resulting from increasing demands on high productivity per man-hour. This means that the stockman in intensive systems is not allowed time enough to develop a relation to the individual animal. This may put animal welfare at danger. The research performed by the Hemsworth group implies that fear of humans, due to lack of close contact between the farm animal and the caretaker, is a serious problem at least in large units.

To some extent the problem of fear of humans may be avoided through the use of machines instead of hand labor, as for example when harvesting broilers (Duncan et al. 1986). However, when animal welfare is considered machines are not as good as manual catching when a relatively careful method of manual catching is used (Ekstrand 1998). There are authors advocating technical systems to be developed which minimize human effect on the animals (Schlichting and Schmidt 1986). Robot milking would be one step in this direction.

However, it will never be possible to completely omit human contact in any system for animal husbandry. Thus, the importance of a positive relation between human and animal remains also in modern large scale systems for animal husbandry with extended use of modern technique. The daily contact also provides the caretaker with indispensable information regarding health status and any aberrations that may occur to the individual animal. This means that the behavior of the human will still be important in any system. In large scale animal husbandry the impact of any stockman behavior will actually be much bigger than in small scale systems, since one person affects many more animals.

Conclusions

The conclusion drawn from this literature study is that the human – animal relation depends on different factors related to the human part as well as to the animal part, and that the relation can be manipulated in several ways. Using current knowledge it is possible to substantially improve the relationship in order to improve animal and human welfare. These improvements need not always cost a lot to implement, rather they can pay off well due to increased human and animal productivity. There is however need for additional scientific studies in order to further broaden and deepen our knowledge in this important field. These should e.g. concern the fine-tuned interaction between the stockman and the farm animal, the different components of stockmanship and how these can be taught to people working in animal husbandry. Another interesting question is how important a bonding relation is to the human and to the animal: Do interspecies interactions fulfill more needs than prescribed within the practical agricultural context and, if so, how should they be valued?

Summary

The human – animal relationship is a complex one, depending on many factors. So far it has been studied scientifically only briefly. The research performed has focused on the animal, e.g. animal fear and reactions to different types of handling. Some pioneering work has also been done (in interdisciplinary co-operation with social scientists and psychologists) regarding the human component of the relationship, e.g. the effects of stockman personality and attitudes. Both research areas are beset with many methodological and epistemological problems. However, there is an increasing scientific interest in the field. It is clear that both animal and human can have great benefits from an improved relationship, e.g. better animal welfare as well as higher production. It has been shown that fear of humans due to too little human contact and/or too much negative handling is a significant cause of distress in farm animals, causing low production. The stockman has a key role and should attempt to create a stable, consistent and caring environment. Empathy appears a crucial component of stockmanship.

The relationship can be improved through minimizing fear of humans and effects of negative handling that can’t be avoided. This can be done in several ways. To minimize fear, critical times for habituation should be used to habituate the individual animal to handling. There are indications of such periods, but this need to be further researched. Also breeding and selection of suitable breeds are of some importance.

There is strong evidence for the beneficial effects of consequent pleasant handling, such as patting and talking gently with the animal. Food awards should be used as operant conditioning to minimize negative effects of aversive handling that can’t be avoided, and this type of handling should be performed so that the animal can predict it. This can be done through the use of special clothing or performing it in special places.

It will never be possible to completely omit human contact in any system for animal husbandry. Thus, the importance of a positive relation between human and animal remains also in modern large scale systems for animal husbandry with extended use of modern technique.

Acknowledgements

This project has been funded by the Swedish Council for Forestry and Agricultural Research.

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