ISRAEL JOURNAL OF

VETERINARY MEDICINE
VOLUME 55 (3), 2000
REVIEW:

HANDLING AND TRANSPORTATION OF BROILERS - WELFARE, STRESS, FEAR AND MEAT QUALITY. PART III: FEAR; DEFINITIONS, ITS RELATION TO STRESS, CAUSES OF FEAR, RESPONSES OF FEAR AND MEASUREMENT OF FEAR
K. Elrom
The Technion - Israel Institute of Technology, Faculty of Food Engineering & Biotechnology, 32000 Haifa, Israel

Abstract The process of domestication aimed at modifying animal behavior, anatomy and physiology and at mans specific needs, has accelerated markedly in poultry. Since the middle of the eighteenth century poultry rearing has been kept for egg and meat production, rather for fighting skills. Although fear is adaptive in ideal circumstances, in reality it can seriously harm the welfare and performance of poultry and other farm animals, particularly if its arousal is sudden, intense, prolonged or inescapable. Fear is a very important behavioral trait, which may lead, if not evaluated properly, to high economic losses. Without doubt the domestic fowl now shows reduced fear as a result of long-term genetic selection.

Fear
Fear is a major stressor, that is widely regarded as an undesirable state of suffering by many people, the scientific community, welfare and policy groups, as well as a growing numbers of farmers (1). In ideal conditions fear is adaptive behavioral functioning, whose biological role is to protect the animal from injury. Both acute and chronic fear can seriously harm the welfare and the performance of poultry. Fear responses are seen as escape or panic reactions, which are inappropriate in intensive rearing systems and can cause injury, pain or even death. Jones, (1) claims that the most efficient ways of reducing fearfulness and increasing adaptability in poultry (at least in laboratory conditions) are: environmental enrichment, regular handling or related treatments, vitamin C (ascorbic acid) supplementation to the diet or the drinking water and genetic selection. He cites a few definitions of fear: peril, painful emotion excited by danger, a state of alarm or dread and more. Fear is usually listed among the emotions as love, hate, and anger and is regarded as an emotional - psychophysiological response to perceived danger. In ideal circumstances fear is an adaptive state, fear behavior acts to protect the animal from psychochemical damage and injury. High levels of fear will decrease plumage condition, egg production, egg shell quality, growth and feed conversion efficiency. Fear will impair the adaptability of the birds to environmental changes, will

decrease their ability to interact between themselves and between the poultry-man. In poultry the most frightening events encountered by poultry are sudden changes in their physical or social environment and exposure to humans.

How fear is related to stress

Fear may contribute to overall stress, particularly if the stimulation is intense or prolonged. Fear is a powerful stressor, that can seriously damage the welfare, management and performance of poultry. Fear is important particularly in the present farming systems when birds are housed in systems which prevent or restrict the expression of appropriate or adaptive responses to threatening stimuli so leading to a more sever outcome. Today the scientific and farming communities support the view that fear is not only a state of suffering but is a powerful and potentially damaging stressor. (1,2,3,4). The intensity of the fear response is influenced by several cognitive, physiological and physical factors such as previous experience, assessment of the opportunity to escape, hormonal status and the size of a threatening animal or object. There are varieties of fear responses and the bird will respond appropriately for coping with a particular danger. A higher level of fear caused by major environmental change or by a potential threat or predator, might elicit flight, fight or immobility responses. The immobility response of crouching or freezing might reduce the chances that the predator sees the bird from a distance while flight or fight response promotes escape from the threatening factor (1). Animals which are characterized as fearful, are more likely to show exaggerated fear responses to a wide variety of alarming stimuli than are less fearful ones. Poultry may experience a similar behavioral condition to fear, which is defined as Anxiety. Anxiety is a diffuse state of tension which magnifies and even causes the illusion of external danger, without pointing to appropriate defense strategies.

The causes of fear in poultry

Many factors are known to be fearful for birds, some of which will be dealt with in this section. Chickens often perceive contact with humans as an alarming predatory encounter. Two of the commonest and most potentially frightening events for domestic fowl are sudden changes in their social or physical environment and exposure to people, and that is why gathering, crating and transportation of broilers are probably the most fearful events in their life. 1. Transport from one place to another, e.g. from hatchery to brooding house. 2. Large open areas (Neophobia) are considered as fearful since domestic fowl are descended from Red Jungle fowl whose natural habitat is dense rainforest. Chicken may feel exposed and vulnerable to attack by predators in open areas. 3. Exposure to unfamiliar stimuli: object, food, noise or odor, are all potentially frightening. Examples are changes in diet formulation, lighting, thunder, sonic booms and banging of metal buckets (1). 4. Visual, auditory and / or physical contact with people may be threatening to birds that are unaccustomed to their presence or have unpleasant experiences with them (5). Birds may panic if untrained people enter the poultry house (6). Also sudden changes in the clothes (e.g. color and style) of the poultry-man may elicit fear and panic. The quality of the contact is also important where inversion and suspension by the legs is more frightening than being held upright. 5. Rapid approaching objects (humans, animals and machinery) are fear-provoking stimuli. These may be sensed at distances of 25 m or more by layers.

6. Unpredicted appearance and movement of animate and inanimate objects (e.g. other birds, people etc.) regardless of how familiar these may be. 7. Disruption of the social environment: Common changes are separation of familiar companions, presence of strangers or exposure to a strange group, destabilization of an established hierarchy, aggressive encounters, alarm vocalizations and displays (1,7). 8. Exposure to potential predators or predator-related stimuli. It is interesting to stress out that cockerels show alarming behavior when they are presented with computerized predator simulators such as views of raccoon and flying hawks. Though feather pecking and cannibalism are induced by sight of blood, it was suggests that domestic chicks and pheasants avoid conspecific blood, when presented in small dishes (1). 9. Large fast-moving stimuli; many poultry producers report serious losses when their birds are frightened by low flying aircraft. 10. Husbandry procedures (such as dust cleaning, preventive treatment against external parasites). 11. The transportation of poultry from the farm to the slaughterhouse is a multi-factorial process, which embraces a number of potentially traumatic events. Harvesting, loading, disruption of social environment, motion, sudden acceleration and deceleration, exposure to unfamiliar environments; birds and noises, climatic changes, pre-slaughter processing and many other stressful factors (4,7,8). Transportation arouses relatively high levels of fear in broilers and layers, and is related to the duration of the journey (4,7,9-13). Also social, genetic and environmental backgrounds such as group size, stocking density, social stability, genome, housing system, the shape, dimensions and position of cages(1,7). Domestication has produced birds which show lower levels of fear of humans. The domestic fowl is thought to be one domestic species that was initially bred primarily for aggressiveness rather than tameness; only since the middle of the eighteenth century has it been kept for egg and meat production, rather for fighting skills. Birds are very sensitive to threatening stimuli such that if the bird gives up trying to find an alternative and suitable coping strategy, or if it learns that none is available, it could enter the dangerous state of hopelessness, learned helplessness and behavioral depression. Such failure to cope could eventually produce psychosomatic symptoms and eventually death through the breakdown of internal homeostatic mechanisms. Summary of potential deleterious consequences of fear responses and heightened fear in poultry: (1) Energy wastage Injury (lesions, broken bones), pain or death Feather pecking, feather damage and loss Inhibition of other motivational systems, reduced adaptability Management problems and economic losses Egg shell abnormalities, compromised hatchability Downgrading of eggs and carcasses Reduced egg production Decreased growth and food conversion efficiency Delayed maturation

The responses to fear

Responses which, in normal circumstances may be appropriate, tend to be devastating in intensive rearing systems. During catching before transportation to the slaughterhouse, panic, hysteria and violent attempts to escape may lead to a waste of energy, injury, pain or even death of birds. The injuries caused directly or indirectly by the elicitation of acute fear state represent a major welfare problem because they lead to chronic pain, infection, physical disability, and undesirable behavioral symptoms such as social withdrawal. Moreover, they also cause reduced profitability through the downgrading of carcasses at slaughter as well as through increased D.O.A rate (1). Exploratory pecking, feeding, social and sexual behavior would all be suppressed in frightened birds. Such suppression would dramatically reduce the birds ability to adapt to environmental changes and to react appropriately. Birds which tend to be more fearful than others are much predisposed to panic responses in environmental disturbances. It is interesting to note that in an experiment conducted across 22 commercial broiler units, it was recorded that broilers with greater avoidance of people had lower conversion efficiencies (1). No disputable explanation was found for the negative relationship between the fear of humans and the feed conversion efficiency. Fear was estimated by counting the number of broilers that remain close to or approach the experimenter as he walked slowly through the poultry shed. It is reasonable that fearful birds will be more influenced by the presence of man and other surrounding stimulation, which will excite the birds during the growing period. It is known that during stress blood is deviated from organs such as the G.I.T (by activation of a adrenoceptors) though catecholamines in the blood and so decreases the absorbance of metabolites from the intestines. Catecholamines also decrease peristaltic contraction of the avian intestines by relaxing the smooth muscle (through activation of a 2 and b adrenoceptors) and contracting the sphincters (through the activation of a adrenoceptors) (14). Gastrointestinal ulceration is one of the consequence of long term exposure to high levels of corticosteroids during stress (chronic stress) and definitely harms the efficiency of the GIT (7).

Measurement of fear
A full discussion can be found in Joness review (1) in which he stresses that neither the fear state nor underlying fearfulness can be measured directly in any species, including man. The following behavioral fear-ranking tests have been frequently used to measure fear in poultry. Some of the tests are controversial within the research community. 1) The open field or novel environment - Birds are observed in a novel and generally barren enclosure which is often larger and more brightly lit than the home cage, after removal from their home environment and placed in sudden insulation. Silent, inactive birds are considered to be more frightened than those which vocalized, ambulate, eat, or explore the environment. 2) Emergence or hole-in-wall test - Based on the conception that a frightened bird will avoid emergence from a sheltered area, through a doorway, into an exposed brightly lit unfamiliar area than a less fearful one. 3) Home cage avoidance test - This test may be done without removing the bird from its cage. A stimulus such as nearby humans, or an object (e.g. pencils, metronomes, colored rods), which is placed in the feeder (trough), is estimated for its ability to cause the birds withdrawal. This test is controversial since fear function to protect the organism from a harmful stimuli and so the avoidance, in this case, may not reflect the birds fear of the stimuli. 4) Box plus experimenter - Used in the laboratory to score the approach or avoidance tendencies of chicks towards a visible human seated behind a wire mesh (net) at one end of an unfamiliar room. High avoidance is considered to reflect high fear of people. It is noted that in this case, regular handling of the birds may influence the results of the test.

5) Approaching human test - The number of broilers that remain close to or approach the experimenter as he walks slowly through the poultry shed estimates fear of human. This has been shown to be an important limiting factor of productivity in broilers. The experimenter can use a video camera so video tapes can be analyzed later. 6) Tonic immobility (TI) - This relates to an unlearned response, which is easily induced by light manual restraint. The bird is held down on its back or side for approximately 15 seconds and then released. At first when fixed, the bird struggles and attempts to escape but soon it adopts an immobile posture, which may last from a few seconds to several hours. The state is characterized by temporary motor inhibition, rigidity and loss of righting response, which according to Blood and Studdert (15), is the return of an animal to sternal recumbancy after being placed on its back or side. This postural reaction turns a falling animal in space so its feet or paws are pointed at the ground. The normal reaction is dependent on normal vestibular, visual and proprioceptive functions. TI is an indicator of fear and stress during transportation (6,8,10). Additional characters of the state of TI are slow-wave deactivated Electroencephalogram (EEG) pattern, sympathetic nervous activity and reduced overt responsiveness to external stimulation. This is an anti-predator reaction in which the more frightened bird will show a longer TI reaction.

References
1) Jones, R. B.: Fear and adaptability in poultry: insights, implications and imperatives. Worlds Poult. Sci. J., 52: 131-173, (1996). 2) Craig, J.V. and Adams, A.W.: Behavior and well-being of hens (Gallus domesticus) in alternative housing environments. Worlds Poult. Sci. J., 40: 221-240, (1984). 3) Jones, R.B.: The assessment of fear in the domestic fowl. In: Zayan, R. and Duncan, I.J.H. (Editors): Congestive Aspects of Social Behavior in the domestic Fowl. Elsevier, Amsterdam, pp. 40-81, 1987. 4) Nicol, C.J. and Scot, G.B.: Pre-slaughter handling and transport of broiler chickens. Appl. Anim. Behav. Sci. 28: 57-73, 1990. 5) Duncan, I.J.H.: The assessment of welfare during handling and transport of broilers. In: rd Faure, J.M. and Mills, A.D. (Editors): Proceedings of the 3 European Symposium on Poultry Welfare. Worlds Poult. Sci. Assoc., French Branch, pp. 93-107, 1989. 6) Jones, R. B.: The nature of handling immediately prior to test affects tonic immobility fear reactions in laying hens and broilers. Appl. Anim. Behav. Sci. 34: 247-254, 1992. 7) Elrom, K.: Stress in Broilers due to pre-slaughter handling and transportation. D.V.M. thesis. University of Veterinary Medicine in Kosice, The Slovak Republic. 1999. 8) Knowles, T. G. and D. M. Broom: The handling and transport of broilers and spent hens. Appl. Anim. Behav. Sci., 28: 75-91, 1990. 9) Bayliss, P.A. and Hinton M. H.: Transportation of broilers with special reference to mortality rates. Appl. Anim. Behav. Sci. 28: 93-118, 1990.

10) Frazer, A.F. and Broom, D.M.: Farm Animal Behaviour and Welfare. Baillier Tindall, London, pp.266-391, 1990. 11) Scot, B. G.: Effects of short-term whole body vibration on animals with particular reference to poultry. Worlds Poult. Sci. J., 50: 25-37, 1994.

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