Emotions in farm animals.pdf

Behavioural Processes 60 (2002) 165 / 180

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Emotions in farm animals:

a new approach to animal welfare in applied ethology

Lara D´sir´, Alain Boissy * , Isabelle Veissier

Unit´ de Recherche sur les Herbivores, INRA Clermont-Ferrand/Theix, F-63122 Saint-Gen`s-Champanelle, France

Received 1 November 2001; accepted 25 February 2002

Abstract

One of the major topics of applied ethology is the welfare of animals reared by humans. Welfare can be defined as a

state of harmony between an individual and its environment. Any marked deviation from this state, if perceived by the

individual, results in a welfare deficit due to negative emotional experiences. In humans, verbal language helps to assess

emotional experiences. In animals, only behavioural and physiological measurements help to detect emotions.

However, how to interpret these responses in terms of emotional experiences remains an open question. The

information on the cognitive abilities of farm animals, which are available but scattered, could help the understanding

of their emotions. We propose a behavioural approach based on cognitive psychology: emotions can be investigated in

farm animals in terms of the individual’s appraisal of the situation. This evaluative process depends on: (a) the intrinsic

characteristics of the eliciting event (suddenness, novelty, pleasantness); (b) the degree of conflict of that event with the

individual’s needs or expectations; and (c) the individual’s coping possibilities offered by the environment. The result of

such an evaluation determines the negative versus positive emotions. We propose an analysis of the emotional

repertoire of farm animals in terms of the relationship between the evaluative process of the event on the one hand and

the behavioural and physiological responses on the other hand.

Keywords: Cognition; Emotion; Farm animal; Welfare

1. Introduction

standards. For example, the Council of Europe

adopted a Convention for the protection of

animals kept for farming purposes in 1976 ( Coun-

cil of Europe, 1976 ). The concern for animal

welfare is strongly associated with the attribution

of mental states to animals ( Dawkins, 1990 ).

Welfare is fulfilled when the animals do not feel

any long lasting negative emotions and when they

can experience positive emotions ( Dawkins, 1983;

Fraser, 1995 ). Nevertheless, what emotions exactly

farm animals can feel is not clear.

Animal welfare is becoming a major topic in

applied ethology. Applied ethology deals with

behaviour of animals reared by humans. Humans,

being responsible for the living conditions of the

animals, have the duty to ensure minimal welfare

* Corresponding author. Tel.: / 33-473-62-4298

E-mail address: boissy@clermont.inra.fr (A. Boissy).

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L. D´sir´ et al. / Behavioural Processes 60 (2002) 165 / 180

Emotional responses are generally assessed by

behavioural tests, which are often experimentally

using events that animals can face in farming. For

example, Hargreaves and Hutson (1990) studied

the emotional response of wethers in five routine

handling treatments namely shearing, crutching,

drenching, dipping and drafting. In such tests, the

tendency of an animal to react more or less to

negativeevents is called ‘emotionality’ or ‘reactiv-

ity’ or so-called ‘temperament’ ( Wolff et al., 1997;

Boissy, 1998 ). Emotional states are used as post-

hoc variables to try to understand the animal’s

reaction to the test. Words like ‘fear’ or ‘frustra-

tion’ are often used to describe what the animal

experiences when faced with a new or sudden

situation, or one associated beforehand with

punishment ( Gray, 1987 ). Hence, fear is highly

adaptive, it prevents the animal from interacting

with potentially dangerous elements. The term of

frustration describes the emotional state arising

when the animal fails to achieve some gratification

where it is expected ( LeDoux, 1995 ). Exposure to

sudden stimuli, to the presence of a human or a

novel object or environment are classically used to

induce fear in order to study the effect of breed or

rearing conditions on reactivity of animals from

various species, such as sheep ( Romeyer and

Bouissou, 1992 ) and cattle ( Boissy and Bouissou,

1995 ). In addition, preventing the access to a

substrate that allows performance of highly moti-

vated behaviour results in emotional responses,

which are believed to express frustration. For

instance, Mason et al. (2001) used the word

‘frustration’ to explain the increased cortisol blood

levels in minks denied the access to a pool where

they used to swim. But in most other cases, tests

are not set up to address the question of emotions

of animals and no comparison between different

emotional states can be made.

In behavioural tests, the measures are mainly

based on ‘gross’ behaviour: approach or avoidance

of a stimulus, locomotion during a test, interaction

with an object or a person are generally measured

( Boissy et al., 2001 ). These might not allow us to

distinguish between different emotions. For exam-

ple, locomotor activity of sheep is increased in fear

eliciting situations such as the presence of a novel

object or in an open-field ( Romeyer and Bouissou,

1992 ). However, locomotor activity is also en-

hanced in response to a sexually frustrating situa-

tion ( Bishop et al., 1999 ). In humans, emotions can

be distinguished via facial expressions even when

the general behaviour of the person looks the same

( Ekman and Friesen, 1971 ). Because the aim of

most experiments related to emotions in farm

animals was to characterise their ‘reactivity’, such

distinctions are not looked for.

Although it is claimed that farm animals are

sentient creatures, it is paradoxical that there is no

exact knowledge of what their subjective experi-

ences are about. This gap in knowledge could

result from a lack of a theoretical framework for

the study of emotions in animals. Recent develop-

ments in human psychology could help us to

overcome this problem. In this paper, we first

present a series of arguments in favour of the

existence of emotions in farm animals. On the

basis of current knowledge, we show that these

animals are able to build mental representations to

support their subjective experiences. Then, after a

brief presentation of the different theories of

emotion developed in human psychology, we

propose a framework for an approach of emotions

in animals. This paper will focus on birds and

mammals, which are used in farming, and which

will be referred to as ‘farm animals’.

2. Existence of emotional experiences in animals

An emotion is an intense but short-living

affective response to an event (the duration of

emotion is a much debated question but briefness

seems widely accepted), and is materialised in

specific body changes. An emotion is classically

described through a behavioural component (a

posture or an activity), an autonomic component

(visceral and endocrine responses) and a subjective

component (emotional experience or feeling) (for

review see Dantzer, 1988 ). In addition, the sub-

jective component, which corresponds at least in

humans to the perception of the emotion in

relation to the eliciting situation, leads to subse-

quent adjustment of the behavioural and auto-

nomic response.

L. D´sir´ et al. / Behavioural Processes 60 (2002) 165 / 180

167

The existence of emotions in animals is a

controversial issue both in psychology and biol-

ogy. Rollin (1989) calls attention to the following

paradox: scientists are shy of attributing mental

states to animals, such as the ability to feel fear,

anxiety or suffering, yet at the same time con-

siderable experimental work is manifestly being

done to stop pain or to relieve anxiety in animals.

From an adaptation perspective the ability to

perceive its own emotions enables an individual

to detect and assess a discrepancy between its

requirements and environmental conditions. In

addition, the etymology of the word ‘emotion’ is

‘movement outwards’: the ability to express emo-

tions enables an individual to give information to

other

tive emotions such as fear act as negative reinfor-

cers in the sense that the animal learns to avoid an

action if fear is the consequence of that action. For

instance, fear is supposed to produce running and

hiding in reaction to a perceived danger. However,

at that stage, we cannot be sure that the reaction is

based on an emotional experience since some

plants ‘approach’ light by turning their branches,

although they do not have a nervous system to feel

emotions. Nevertheless, animals do not just react

to existing challenges; they are also able to

anticipate a challenge. For instance, Veissier et

al. (1989) conditioned heifers to be frightened by a

visual object by associating it with an aversive

electric shock. Animals react as if they were able to

compare their actual environment to some internal

reference, being what they expect their environ-

ment to be ( Wiepkema, 1987 ). As a matter of fact,

stress responses, which have been defined as non-

specific modifications of the body to an aggression

do not depend directly on the situation to which

the individual is exposed; but rather on the

negative interpretation that the individual makes

of the situation, specially when it is prevented from

meeting its own expectancies or needs ( Lazarus,

1991 ). The importance of mental representations

in animals’ responses to stress was first demon-

strated in primates. Monkeys deprived of food

while their neighbours are normally fed show high

plasma corticoid levels, a sign of stress ( Mason,

1971 ). This reaction disappears when they are fed

non-nutritive pellets or when they are isolated

from the normally fed controls. In this case, it is

not so much the absence of food as the perception

of a deprivation that causes the stress. Similar

effects have been reported in farm animals. Cows

do not react in the same way when they are

exposed to gradual or to sudden temperature

variations. When ambient temperature rises gra-

dually, the plasma corticoid levels fall, enabling

the animal to reduce its own heat production

( Johnson and Vanjonack, 1975 ). However, when

the ambient temperature rises suddenly, there is a

transient rise in corticoid levels before the normal

decreasing ( Fig. 1 ). The corticoid rise may be

interpreted here as a psychological response to the

situation. This psychological response is not linked

to the nature of the situation (exposure to heat),

individuals

help

them

adjust

their

behaviour.

In humans, at least in adults, verbal reports of

emotions can be obtained together with beha-

vioural and physiological responses. In contrast, in

animals, which lack verbal language, behavioural

and physiological criteria are the only available

means* / as a body language* / to determine

whether the animal perceives a situation as emo-

tionally relevant. Since the evolutionary theory of

Darwin (1872) , the phylogenetic continuity and

universality of emotions have often been con-

firmed. There has been extensive research showing

that the neural circuits that underpin experience

and expression of emotions in humans exist in

animals, too. These circuits include subcortical

nervous structures such as the limbic system, the

hypothalamus and the brain stem, which ensure

regulation of the body and survival (for review see

Gray, 1987; LeDoux, 1995 ), and also, at least in

primates, cortical structures such as the frontal

lobe and somatosensory areas where signals from

the body are sent (for review see Damasio, 2001 ).

The existence of a subjective component in

animals is supported by a series of analogies

between emotional manifestations in humans and

behavioural or physiological adaptations reported

in animals ( Wiepkema, 1987 ). Emotions are often

supposed to be the reason why an animal ap-

proaches or rather avoids an eliciting situation

( DeCatanzaro, 1999 ). Rolls (2000) claims that

animals which have the ability to anticipate or

learn to obtain reinforcers, have emotions: nega-

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L. D´sir´ et al. / Behavioural Processes 60 (2002) 165 / 180

Fig. 1. Evolution of plasma cortisol in cows that are individually exposed to an increase (upper histogram) or a decrease (lower

histogram) of room temperature. Changes of temperature are either progressive (dotted line) or sudden (full line). When cows are

exposed to a sudden change in the room temperature, an initial increase of the plasma cortisol is observed which is independent of the

temperature the animal is exposed to. In the case of an exposition to a high temperature, the elevation of plasma cortisol does not serve

a thermoregulatory mechanism since for thermoregulation, a decrease would be more adequate. It seems that the ﬁrst response of the

corticotropic axis to a strong stimulus is a psychological one (response to an acute change) and that the speciﬁc response

(thermoregulation) occurs subsequently (from Johnson and Vanjonack, 1975; Dantzer and Morm`de, 1979 ).

but to its suddenness, which the animal probably

perceives as an aggression ( Dantzer and Morm`de,

1979 ). The apparent ‘non-specificity’ of stress

response seems to come from the common emo-

tion that underlies them ( Mason, 1971 ).

Analogy between human depressive chronic

states and the consequences of repeated stress in

animals argues that animals experience emotional

states that can have long term consequences. In

depressive patients the function of the corticotro-

pic axis is modified: more specifically the stimulat-

ing action of ACTH on corticoids release by the

adrenal glands is increased, and the corticotropic

axis escapes from the feedback control by corti-

coids ( Carroll et al., 1981; Modell et al., 1998;

O’Toole et al., 1998 ). Such modifications of the

functioning of the corticotropic axis are also

observed in farm animals exposed to a chronic

stress. For example increased sensitivity to ACTH

has been observed in calves subjected to frequent

L. D´sir´ et al. / Behavioural Processes 60 (2002) 165 / 180

169

changes of their social partners ( Veissier et al.,

2001 ; Fig. 2 ). Similarly, in pigs subjected to high

social densities, the corticotropic axis escapes from

the feedback control by corticoids ( Meunier-Sal-

aun et al., 1987 ).

The question of emotions in animals does

therefore seem to have a biological basis, because

first, there are homologies between humans and

animals in the nervous system and, second, there

are analogies between humans and animals in

behavioural and physiological modifications ob-

served in emotion-eliciting situations, at least in

extreme situations. However, little is known on

what emotions animals can really feel. Tradition-

ally, the analysis of emotions in animals has

focused on negative emotions, most often fear,

frustration, anger and aversion ( DeCatanzaro,

1999 ). These emotions are often described using

the same behavioural (flight, etc.) and physiologi-

cal responses (activation of the corticotropic axis,

or of the autonomic nervous system, etc.) making

it difficult to distinguish them on the behavioural

and physiological level. By contrast to laboratory

animals, emotions of a positive nature, such as joy

or pleasure, are seldom mentioned in farm ani-

mals. Very few tests use positive situations

although it could help to improve handling as

shown by Hutson (1985) who observed that food

rewards might improve sheep handling. Just as

flight, attack or behavioural inhibition elicited by

a situation, are thought to result from fear, pursuit

of a stimulus (approach, choice, etc.) is interpreted

as a preference for a pleasant situation.

3. Diversity of approaches of emotion in psychology

Emotions have been extensively studied in

psychology. A brief review of this wide research

could help to clarify what emotion is and may be

Fig. 2. Response of the adrenal cortex to an injection of dexamethasone and ACTH in calves that were either repeatedly changed of

partner and of pen (regrouped animals n / 8) or were maintained in stable pairs (controls n / 8). The area under the curve, that

represents the overall cortisol response to ACTH injection, is higher in regrouped animals than in controls (6.688 vs. 5.508 ng min/ml,

F / 8.76, P B / 0.01). This higher sensitivity of the adrenals to ACTH may be explained, in this gregarious species, by chronic stress

induced by the repeated loss of the partner and mixing with a new one. This modiﬁcation is similar to the one observed in humans who

suffer from depression. This homology gives support to the existence of negative experiences in calves that might, to a certain extent, be

similar to those reported by depressive patients (from Veissier et al., 2001 ).

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