Comfortable Quarters for Sheep in Research Institutions Viktor Reinhardt and Annie Reinhardt Animal Welfare Institute, PO Box 3650, Washington, DC 20007, USA

Sheep are probably the most apprehensive animals used in research. They require excellent professional care - including regular monitoring of their behavior - to address stress reactions to the inherently fear-provoking environment of the laboratory. If these stress reactions are not ameliorated or buffered, any research with sheep is questionable because the results are likely to be influenced by an important, yet uncontrolled variable. In the United States approximately 24,000 sheep are used in research (United States Department of Agriculture, 2000).

• Gregariousness is the most outstanding characteristic of sheep. A sheep needs to be with other sheep in order to be in a state of well-being and normative physiology (Figure 1). Sheep will always try to maintain uninterrupted visual contact with at least one other sheep, and they will flock close together at any sign of danger. Individuals show a multitude of endocrine, hematological and biochemical alterations (Kilgour and de Langen, 1970; McNatty and Young, 1973; Bobek et al., 1986; Parrott et al., 1987; Minton et al., 1992; Apple et al., 1993; van Adrichem and Vogt, 1993; Carbajal and Orihuela, 2001), stereotypic behaviors (Done-Currie et al., 1984) and a marked increase in heart rate and respiration rate when isolated from other sheep (Syme and Elphick, 1982; Baldock and Sibly, 1986; Carbajal and Orihuela, 2001). When an ewe is separated from other sheep by a fence, she will stay calm as long as she can see her companions. However, if the fence is solid, the isolated subject will show dramatic stress reactions (Baldock and Sibly, 1990).

Figure 1. Sheep do best in the company of other sheep in naturally structured outdoor enclosures with pasture (©STS, photo by H.P. Haering).

• Like cattle, sheep establish well-defined social relationships with all other group members, and they follow certain leading animals when moving from one location to another (Scott, 1945). The harmony within a flock is based on stable dominance-subordination relationships, which predetermine harmonious interactions between partners. Any change in the group composition - removals or introductions - will destabilize or disrupt these relationships. This will prompt agonistic conflicts leading to the establishment of new rank relationships.
       
• Confined sheep are prone to develop wool pulling behavior. Individuals pick with their mouths strands of wool from the fleece of other - typically subordinate - group members, who in time can become quite denuded. As in captive muskox calves (Ovibos moschatus; Reinhardt and Flood, 1983, Figure 11), rabbits (Maertens and DeGroote, 1994) and nonhuman primates (Elton, 1979; Reinhardt et al., 1986), this seemingly abnormal behavior may reflect difficulties to adjust to abnormal, i.e., species-inadequate, stressful husbandry conditions.
       
• When given the opportunity sheep will spend approximately 8 hours per day grazing (Figure 2; Kilgour and Dalton, 1984) and travel several kilometers (Arnold and Dudzinski, 1978). Although casual observation of well-habituated sheep in small stalls restricting almost all locomotion may not reveal any outward signs of distress, the confined subjects will show a distinct endocrine stress response reflected in increased adrenal activity (Bowers et al., 1993).

Figure 2. The grass-covered paddock is a practicable, species- appropriate housing environment for sheep kept in research institutions (©STS, photo by S. Scherrer).

• Unlike cattle, sheep are very fearful by nature, and any changes in their surroundings make them apprehensive and ready to flee. Novelty is usually an acute stressor for them, a circumstance that makes the research laboratory a particularly unsuited place to collect data that are not tainted by stress. The shape of the human "predator" elicits a specially strong fear response that can only be overcome through patient and compassionate conditioning. Sheep have excellent memory of aversive experiences (Belschner, 1962). The experience of rough handling can make a sheep quasi "useless" for any subsequent experimental procedures.

Probably even more than cattle - who, unlike sheep can easily overcome their fear of people - sheep require social company in order to cope with the circumstances of their domestication. It therefore follows that, in accommodating these animals for purposes of experimentation, their social needs must be given full consideration, on a par with other well-recognized physical needs such as nutrition, hygiene, and shelter (Fraser, 1995; Figure 3). Data collected from a single-housed sheep are not representative of "normal" sheep, that is to say animals in the sheep-characteristic social setting (Bowers et al., 1993).

Figure 3. Social housing of sheep is a fundamental condition of sound scientific research methodology.

Stable social relationships provide the basic condition that the members of a flock will live in a relatively stress-free environment. To remove a sheep or to introduce a strange sheep into a flock is not a good idea because it will destabilize or disrupt dominance-subordination relationships leading to rank determining aggressive conflicts. Such conflicts are counterproductive in the research setting and should therefore be avoided by all means. Lambs should always be allowed to stay with their mother until the age of natural weaning. Premature separation from the ewe is extremely disturbing for the young who will exhibit behavioral and physiological responses indicative of stress, including increased levels of plasma cortisol and impaired immune responses (Price and Thos, 1980; Moberg and Wood, 1981; Napolitano et al., 1995).

Sheep do best in naturally structured outdoor enclosures with pasture (Figure 1). The grass-covered paddock is a practicable, species-appropriate housing environment for sheep kept in research institutions (Figure 2). The floor area per animal must be sufficient to permit adult animals to keep appropriate social distances and hence minimize aggressive conflicts arising from confinement, and to allow young animals to engage in play activities. Feed troughs should be shallow enough so that the animals can maintain visual contact with each other. There must be enough trough space and/or feed rack space so that all animals of the flock can feed at the same time.

Sheep do not adapt to the stress of separation from other sheep (Niezgoda et al., 1987). Individually housed sheep are restless and show an increased heart rate that may persist over many days and account for an increased metabolic rate of up to 15% (van Adrichem and Vogt, 1993). A lone sheep will never be at ease and hence will always be unsuited for research that relies on stress-free data (cf., Done-Currie et al., 1984; Marsden and Wood-Gush, 1986). Not only for scientific but also for ethical reasons, a sheep should not be housed alone unless there is evidence that social housing would jeopardize the animal's health and/or well-being. During experiments that require temporary single-housing - for example in metabolic stalls - provision must be made that the sheep can keep uninterrupted acoustic, visual, and olfactory contact while standing and lying with one or several other sheep kept in the same room in close proximity (cf., Olfert et al., 1993). The presence of mirror panels during isolation can reduce the magnitude but fails to eliminate the physiological responses to this psychologically distressing situation (Parrott et al., 1988). Since sheep treat their own reflection as a strange individual (Parrott, 1983), the mirror image may, actually, be mildly stressful (Franklin and Hutson, 1982). The adjustment to the stress associated with experimental conditions is best buffered by the presence of another familiar conspecific (Pearson and Mellor, 1976; Porter et al., 1995; cf., Lyons et al., 1988). This does not imply that the attending care personnel is unimportant; on the contrary.

Temporary experimental enclosures - such as stalls and crates - for individual animals should be no less than 2 x 1 m so that an adult sheep can freely turn around and make at least a few steps in one direction (Hinch and Lynch, 1997) and that a young sheep can engage in some rudimentary play activities.

A 15 cm layer of straw or coarse [to prevent "balling"] sawdust mixed with wood shavings are recommended as comfortable, species-appropriate bedding (Hinch and Lynch, 1997). When given the choice of floor surface, sheep show a clear preference for straw bedding compared with wooden slats (Gordon and Cockram, 1995; Figure 4). Wooden slats are thought to assist with drying feces and keeping the sheep clean. However, they require regular maintenance to guarantee safe footing and to ensure that there are no irregular gaps and broken surfaces that could injure the animals.

Figure 4. Sheep prefer solid flooring with straw beeding (a; © Archiv STS) over wooden slat flooring (b; Photo by Geoff N. Hinch).

The need to ruminate demands that sheep receive sufficiently bulky food. The overall fiber content of the ingested food should be no less than 40%. A lack of fiber may lead to the development of stereotypical bar chewing and wool pulling (Hinch and Lynch, 1997).

The characteristic neophobia of sheep makes it an imperative that care personnel, which includes not only animal caregivers and technicians but also the attending veterinarian(s) and the principal investigator(s), habituate all animals who are subjected to experimentation to any new, i.e., fear-inducing situations. Frequent gentle handling and familiarization are the key to habituate a ewe, ram, or a lamb so that he or she will accept a potentially aversive situation, such as blood collection (Kilgour, 1987). It goes without saying that a person who does not get along well with animals in general, and with sheep in particular, and lacks understanding in the way sheep perceive their environment and the people in it should not be allowed to handle sheep in the research setting. Such a person will be a source of distress, affecting not only the well-being of the sheep but also the quality of research data collected.

With knowledge of sheep behavior, patience, and gentleness, the inherent fear of the human "predator" can easily be overcome and a relationship between sheep and human handler developed that is based on trust. Stroking sheep and quietly talking to them in the research laboratory setting has nothing to do with sentimentalism but with sound scientific methodology. Tame sheep have more normal cortisol concentrations and heart rates and hence are more reliable research subjects than fearful sheep (Pearson and Mellor, 1976; Hargreaves and Hutson, 1990). It is not an overstatement to say that good care personnel instill qualities in the animals that make them better and more reliable research subjects. Stress, on the other hand, leads to physiological and behavioral changes that increase the variability of the data and decrease the reliability of the results.

The attending caretaker or technician is at the pinnacle of a cascading series of environmental and social influences that determine the well-being of the animals. She or he must strive to develop a social bond with the sheep in her or his charge. This bond will convey to the individual sheep a quiet sense of assurance upon which coping strategies can be developed (Wolfle, 1996). Animal care personnel should be strongly encouraged to establish positive relationships with all the sheep in their charge. This implies that provision has to be made that a certain amount of time is set aside each day of the week, to allow attending personnel to interact with the animals in a manner that fosters a trustful relationship. This extra time investment quickly pays off in better research data, and in a more satisfactory, i.e., humane work environment (cf., Kidd, 1994).

Individual sheep will spontaneously lead others during routine handling procedures, such as weighing and veterinary examination (Hutson, 1993). It is good advice to encourage this leader-following behavior rather than interfere in this biologically natural behavior by coercing the animals to move in an unorganized, usually chaotic fashion. The preferable means for movement is to allow sheep to proceed as a group, away from the handler and follow the leader to the target location. The use of fear stimuli such as dogs or noise must be avoided by all means because they unnecessarily frighten the animals. Taking advantage of voluntary, organized movement minimizes stress responses during handling, thereby enhancing the reliability of research data collected (Hinch and Lynch, 1997).

Positive food reinforcement, such as barley, can help both the sheep and the handling personnel to get the job done more quickly (Hutson, 1985). The important thing to remember is, that low-stress or no-stress handling can only be achieved with sheep who are not forced to move, but who are so confident with the handling personnel and with the environment that they move voluntarily to a designated location and accept a certain procedure. It has been documented that sheep can easily be trained to voluntarily enter a tilt table and accept brief immobilization for a grain reward (Grandin, 1989). Restraint does not have to be a distressing, data-biasing procedure as demonstrated by "fourteen out of sixteen ewes [who] returned for one or more additional passes" (Grandin, 1989, p. 200). Positive reinforcement training techniques to assure voluntary cooperation during such common procedures as blood collection and injection have been described in detail in other medium-size ungulates, namely goats and antelopes (Grandin et al., 1995; Lager, 1998; Phillips et al., 1998). It is recommended that these techniques be applied for sheep. There is no reason to assume that they are not equally useful in this species.

Like all animals in research laboratories, sheep respond best to gentle-and-firm handling. They should be held securely and, if the procedure allows it, kept with all four feet firmly on the ground. Sheep have sensitive skin and, therefore, should not be held by the wool. If it is necessary, a sheep can be made to sit up on his or her hindquarters while the handler holds the forelegs and provides firm-and-gentle support to the head and back region with his or her legs and body. In this position examinations and treatments can be carried out under the condition that they take only a few minutes.

The management of sheep in research institutions must address the following minimum requirements in order to be species-adequate and conducive to reliable research:

• Housing in stable group(s);
• Spacious indoor enclosure(s) with straw bedding;
• Access to spacious outdoor enclosure(s) with pasture;
• Provision of bulky food;
• Gentle familiarization to any new situation;
• Knowledgeable, patient and gentle-and-firm animal care personnel;
• Working with rather than against the animals during procedures.
  

Apple JK, Minton JE, Parson KM, Unruh JA 1993. Influence of repeated restraint and isolation stress and electrolyte administration on pituitary-adreneal secretions, electrolytes, and other blood constituents of sheep. Journal of Animal Science 71, 71-77

Arnold GW, Dudzinski ML 1978. Ethology of free-ranging domestic animals. Elsevier, Amsterdam, Netherlands

Baldock NM, Sibly RM 1990. Effects of handling and transportation on the heart rate and behaviour of sheep. Applied Animal Behaviour Science 28, 15-39

Baldock NM, Sibly RM 1986. Effects of management procedures on heart rate in sheep. Applied Animal Behaviour Science 15, 191

Belschner HG 1962. Sheep Management and Diseases, 7th Edition. Angus and Robertson, Sydney, Australia

Bobek S, Niezgoda J, Pierzchala K, Litynski P, Sechman A 1986. Changes in circulating levels of iodothyronines, cortisol and endogenous thiocyanate in sheep during emotional stress caused by isolation of animals from the flock. Zentralblatt für Veterinärmedizin 33, 698-705

Bowers CL, Friend TH, Grissom KK, Lay DC 1993. Confinement of lambs (Ovis aries) in metabolism stalls increased adrenal function, thyroxine and motivation for movement. Applied Animal Behaviour Science 36, 149-158

Carbajal S, Orihuela A 2001. Minimal number of conspecifics needed to minimize the stress response of isolated mature ewes. Journal of Applied Animal Welfare Science 4, 249-255

Done-Currie JR, Hecker JF, Wodzicka-Tomaszewska, M 1984. Behaviour of sheep transferred from pasture to an animal house. Applied Animal Behaviour Science 12, 121-130

Elton RH 1979. Baboon behavior under crowded conditions. In Captivity and Behavior Erwin J, Maple T, Mitchell G (ed), 125-139. Van Nostrand Reinhold, New York, NY

Franklin JR, Hutson GD 1982. Experiments on attracting sheep to move along a laneway. III. Visual stimuli. Applied Animal Ethology [Applied Animal Behaviour Science] 8, 457-478

Fraser AF 1995. Sheep. In The Experimental Animal in Biomedical Research, Volume II - Care, Husbandry, and Well-Being Rollin BE, Kesel ML (eds), 87-118. CRC Press, Boca Raton, FL

Gordon GDH, Cockram MS 1995. A comparison of wooden slats and straw bedding on the behaviour of sheep. Animal Welfare 4, 131-134

Grandin T 1989. Voluntary acceptance of restraint by sheep. Applied Animal Behaviour Science 23, 257-261

Grandin T, Rooney MB, Phillips M, Cambre RC, Irlbeck NA, Graffam W 1995. Conditioning of nyala (Tragelaphus angasi) to blood sampling in a crate with positive reinforcement. Zoo Biology 14, 261-273

Hargreaves AL, Hutson GD 1990. The effect of gentling on heart rate, flight distance and aversion of sheep to a handling procedure. Applied Animal Behaviour Science 26, 243-252

Hinch GN, Lynch JJ 1997. Comfortable quarters for sheep and goats. In Comfortable Quarters for Laboratory Animals Reinhardt V (ed), 94-100. Animal Welfare Institute, Washington, DC
Full Text: http://www.awionline.org/pubs/cq/sheep.htm

Hutson GD 1993. Behavioral principles of sheep handling. In Livestock Handling and Transport Grandin T (ed), 127-146. CAB International, Wallingford, UK

Hutson GD 1980. The effect of previous experience on sheep movement through yards. Applied Animal Ethology [Applied Animal Behaviour Science] 6, 233-240

Hutson GD 1985. The influence of barley food rewards on sheep movement through a hanndling system. Applied Animal Ethology [Applied Animal Behaviour Science] 14, 263-273

Kidd R 1994. Put away your prod: herd stock with less stress by understanding how they think. The New Farm 16(5), 6-10 & 44

Kilgour R 1987. Learning and the training of farm animals. The Veterinary Clinics of North America 3, 269-284

Kilgour R, Dalton DC 1994. Livestock Behaviour. Westview Press, Boulder, CO

Kilgour R, de Langen H 1970. Stress in sheep resulting from management practices. Proceedings of the New Zealand Society of Animal Production 30, 65-76

Lager K 1998. Apparatus and technique for conditioning goats to repeated blood collection. Lab Animal 27(3), 38-42

Lyons DM, Price EO, Moberg GP 1988. Social modulation of pituitary-adrenal responsiveness and individual differences in behaviour of young domestic goats. Physiology and Behavior 43, 451-458

Maertens L, DeGroote G 1984. Influence of the number of fryer rabbits per cage on their performance. Journal of Applied Rabbit Research 7, 151-155

Marsden MD, Wood-Gush DGM 1986. A note on the behaviour of individually-penned sheep regarding their use for research purposes. Animal Production 42, 157-159

McNatty KP, Young A 1973. Diurnal changes of plasma cortisol levels in sheep adapting to a new environment. Journal of Endocrinology 56, 329-330

Minton JE, Coppinger TR, Reddy PG, Davis WC, Blecha F 1992. Repeated restraint and isolation stress alters adrenal and lymphocyte functions and some leukocyte differentation antigens in lambs. Journal of Animal Science 70, 1126-1132

Moberg GP, Wood VA 1981. Neonatal stress in lambs: behavioral and physiological responses. Developmental Psychobiology 14, 155-162

Napolitano F, Marino V, de Rosa G, Capparelli R, Bordi A 1995. Influence of artificial rearing on behavioral and immune response of lambs. Applied Animal Behaviour Science 45, 245-253

Niezgoda J, Wronska D, Pierzchala K, Bobek S, Kahl S 1987. Lack of adaptation to repeated emotional stress evoked by isolation of sheep. Zentralblatt für Veterinärmedizin 34, 734-739

Olfert ED, Cross BM, McWilliam AA 1993. Guide to the Care and Use of Experimental Animals, Volume 1, 2nd Edition. Canadian Council on Animal Care, Ottawa, Canada
Full Text: http://www.ccac.ca/guides/english/V1_93/chap/chiv.htm#4B2

Parrott RF 1983. A method for the quantification of butting activity in androgen-treated wethers. Applied Animal Ethology [Applied Animal Behaviour Science] 10, 319-324

Parrot RF, Thornton SN, Forsling ML, Delaney E 1987. Endocrine and behavioural factors affecting water balance in sheep subjected to isolation stress. Journal of Endocrinology 112, 305-310

Parrott RF, Houpt KA, Misson BH 1988. Modification of the responses of sheep to isolation stress by the use of mirror panels. Applied Animal Behaviour Science 19, 331-338

Pearson RA, Mellor DJ 1976. Some behavioral and physiological changes in pregnant goats and sheep during adaptation to laboratory conditions. Research in Veterinary Science 20, 215-217

Phillips M, Grandin T, Graffam W, Irlbeck NA, Cambre RC 1997. Crate conditioning of bongo (Tragelaphus eurycerus) for veterinary and husbandry procedures at the Denver Zoological Gardens. Zoo Biology 17, 25-32

Porter R, Nowak R, Orgeur P 1995. Influence of a conspecific agemate on distress bleating by lambs. Applied Animal Behaviour Science 45, 239-244

Price EG, Thos J 1980. Behavioral responses of short-term isolation in sheep and goats. Applied Animal Ethology [Applied Animal Behaviour Science] 6, 331-339

Reinhardt V, Flood PF 1983. Behavioural assessment in muskox calves. Behaviour 87, 1-21

Reinhardt V, Reinhardt A, Houser WD 1986. Hair pulling-and-eating in captive rhesus monkeys. Folia Primatologica 47, 158-164
Full Text: http://www.awionline.org/Lab_animals/biblio/pr14-1.htm

Scott JP 1945. Social Behavior, Organization and Leadership in a Small Flock of Domestic Sheep - Comparative Psychology Monographs, Volume 18, Serial no. 96. Williams & Wilkins, Baltimore, MD

Syme LA, Elphick GR 1982. Heart rate and behaviour of sheep in yards. Applied Animal Ethology [Applied Animal Behaviour Science] 9, 31-35

van Adrichem PWM, Vogt JE 1993. The effect of isolation and separation on the metabolism of sheep. Livestock Production Science 33, 151-159

Wolfle TL 1996. How different species affect the relationship. In The Human/Research Animal Relationship Krulisch L, Mayer S, Simmonds RC (eds), 85-91. Scientists Center for Animal Welfare, Greenbelt, MD

Viktor Reinhardt is Laboratory Animal Advisor to the Animal Welfare Institute in Washington, DC. He is a clinical veterinarian and ethologist and was responsible for the husbandry of sheep assigned to research at the Institute of Animal Husbandry and Hygiene in Bonn, Germany.

Annie Reinhardt is a librarian and manages the databases of the Animal Welfare Institute on Alternative Farming and on Refinement and Environmental Enrichment for Laboratory Animals. Annie has participated in numerous ethological studies conducted in cattle, muskox and bison.

Back to Table of Contents