In order to provide cattle with appropriate housing and handling conditions in the research setting, their specific needs for behavioral, emotional, and physical well-being must be met. Only then can the researcher vouch that he/she adhered to basic principles of scientific methodology and ethics in his/her investigations.

Figure 1. Cattle develop friendly relationships with one another that are based on mutual preferences. These two cows, Nanette and Gilla, are not kin-related but preferred each other - over 27 other cows of the herd - as grooming partner and as grazing partner (cf. Figure 5) during a test period of five years (Reinhardt and Reinhardt, 1981).

• Cattle are herd animals. In the wild, the individual cow, bull, or calf is dependent on the presence of other conspecifics for the detection and avoidance of predators. A lone animal has little chance of survival. The members of a herd are tightly integrated in a cohesive social structure. Partners develop enduring, affectionate (Reinhardt and Reinhardt, 1981a; Figure 1), and stable dominance-subordination relationships (Reinhardt, 1980) that make the inter-individual interactions predictable and hence provide a safeguard for a harmonious co-existence as a coherent social group (Reinhardt, 1980). In sharp contrast to intensive housing systems, aggressive conflicts among cattle are rare, and even the presence of long horns poses no risk in a natural, free ranging husbandry system where the animals have enough room for respecting each other's dominance-related spatial privileges thereby avoiding antagonism (Reinhardt, 1980; Figure 2). In the course of a 24-month study of a free-ranging cattle herd consisting of 29 cows, one bull and their offspring, several thousand agonistic interactions were witnessed, but an animal was never injured during such encounters (Reinhardt, 1980). Dominance rank is determined by age, which in turn correlates with horn length. Old animals who are no longer the heaviest and strongest animals of the herd do not lose their high position in the social hierarchy. Their long horns are an effective social weapon that help them retain the respect of younger animals (Reinhardt, 1980). When animals are dehorned, the biological foundation of the hierarchical system is destabilized, leading to alarmingly high rates of overt aggression (Reinhardt and Reinhardt, 1975).

Figure 2. Cattle do not use their horns to injure each other. Subordinate animals avoid overt aggression by moving out of the way of dominant partners. Note the bossy look of the cow at left and the moving-away gesture of the subordinate, cow at right (Drawing by Annie Reinhardt).

In the research context, group-housing is the only acceptable husbandry system for cattle. Social isolation is a serious stressor leading to increased heart rate and plasma cortisol concentration, vocalization, and behavioral signs of frustration and fear (Dantzer and Mormède, 1983; Hopster and Blokhuis, 1994; Munksgaard and Simonsen, 1996; Veissier et al., 1997). Data collected under such circumstances are confounded by stress and, therefore, have little or no scientific value. The intensive need for a social partner can only be met by another cow. Contact with a familiar, empathetic person can ameliorate behavioral stress reactions, but it is not sufficiently comforting to reduce the endocrine response to isolation stress (Rushen et al., 2001).

It is imperative that animals kept in a barn have as little reason as possible for competition. There must be enough feeding space and a sufficiently large bedded area so that all animals can comfortably access the food at the same time or rest in a comfortable recumbent position at the same time. This will foster group harmony (cf. Nielsen et al., 1997). Visual barriers help to buffer agonistic conflicts arising from the inherent spatial constraints of indoor housing (Bouissou, 1970). Sufficient space is necessary so that subordinate animals can yield to dominant partners, thus triggering no overt aggression (cf., Figure 2).

Stable rank relationships are a prerequisite so that there are no undue social tensions or overt conflicts. A group's composition should, therefore, not be altered unless there is a specific veterinary reason. The members of a cattle herd know each other intimately and will show xenophobic behavior towards other cattle (Reinhardt, 1980; cf., Schloeth, 1961; Scheurmann, 1975; Figure 3). To introduce a strange cow into a herd is not a good idea!

Figure 3. A strange cow ([animal at left] submissively approaches another herd and is blocked from proceeding by a cow who displays the broadside-threat gesture (Drawing by Ingrid Schaumburg).

A loose-housing system that is designed to meet the animals' social spacing requirements along with management that respects the animals' hierarchy system and herd-feeling makes the dehorning of cattle unnecessary (Menke et al., 1999). Dehorning is a sign of inadequate husbandry, but it is also a distressing and painful experience for the animals (Taschke, 1995).

The tie-stall is an extremely uncomfortable [hard surface], painful [risk of inflammations of knees and hocks], frustrating [lying down is aversive, but there is a strong urge to rest in recumbence], and boring [restricted or no opportunity for social contact/interaction and foraging] housing environment (Krohn and Munksgaard, 1993; Redbo, 1993; Krohn, 1994; Haley et al., 2000) and, therefore, is not appropriate for cattle who are expected to yield research data that are not confounded by impaired well-being. The inadequacy of the tie-stall is reflected in the frequent occurrence of stereotypical activities [e.g., bar-biting, tongue-rolling], which disappear when the animals are transferred to loose housing or pasture (Redbo, 1992; Krohn, 1994). If circumstances require that a cow is temporarily tethered - e.g., venipuncture, remote sample collection via indwelling catheter - she should be tied by a halter and released as soon as the procedure is completed. A temporarily tied or single-housed animal must always be able to keep at least visual contact with other close-by members of the herd to buffer stress reactions. Under exceptional experimental circumstances lasting less than a day, a mirror may substitute for another conspecific (Piller et al., 1999).

• Long-lasting affiliative relationships exist not only between friends - who prefer each other as grazing, grooming, and resting partners (Reinhardt, 1980; Reinhardt and Reinhardt, 1981a; Reinhardt et al., 1986) - but also between mother and offspring. The bond between cow and calf is not affected by the weaning process - which occurs when the calf is approximately 10 months old (Reinhardt and Reinhardt, 1981b) - but lasts many years, leading to the development of tight-knit family subgroups within the herd (Reinhardt and Reinhardt, 1981a; Reinhardt et al., 1986; Figure 4).

Figure 4. Cow Aida nursing her newborn calf while grooming her 13-month old daughter whom she had weaned four months ago. Aida's mean calving interval was 338 days; she produced 9 calves - who were all allowed to stay with the maternal herd beyond the age of natural weaning - during a test period of 7.5 years (Reinhardt, 1983a).

In the research setting, distress has to be avoided to guarantee the scientific validity of research data. It is, therefore, not justifiable to subject the dam and the calf to the extremely disturbing situation created by premature weaning. Forced weaning distresses both the cow, who will show reduced reproductivity as a result of it (Reinhardt, 1982), and the calf, who will be prone to develop behavioral signs of frustration (Seo et al., 1998) and whose physiological ability to cope with stress will be impaired (Lay et al., 1992). If calves are allowed to stay with their mothers until the natural weaning process has occurred, they will not engage in compulsory substitute sucking, which often leads to health problems associated with the development of bezoars. It is not the substitute sucking that deserves the label "abnormal" (Loberg and Lidfors, 2001) but the human interference with a natural process (Reinhardt and Reinhardt, 1980a).

• Under natural conditions cattle divide the day time into long periods of foraging while moving considerable distances, and long periods of chewing the cud while loafing or resting in a recumbent position (Reinhardt, 1980; Krohn and Munksgaard, 1997). When given the choice, cattle will spend almost all their time on a grass field rather than in a stable with deep bedding (Krohn et al., 1992). The urge to forage is so strong that well-fed cattle will push their way through a fenced area to get access to a meadow where they can graze (Trantham, 2000).

For cattle used in research, a well managed pasture is the most appropriate living environment (Krohn and Munksgaard, 1997; Figure 5). That's were they can graze ad libitum and that's were they can find suitable places to lie down comfortably and rest undisturbed in cattle-specific recumbent positions. The enhanced well-being of cattle on pasture is reflected by a high degree of herd synchrony and the absence of restlessness that typically occurs indoors as a result of spatial restriction (cf., O'Connell et al., 1989; Miller and Wood-Gush, 1991). Rotational grazing is the most suitable management system providing the animals adequate foraging opportunities, while fostering their health (Beetz, 1999).

Figure 5. The grass field is the most appropriate living environment for cattle. Here two friends, Nanette and Gilla, keeping each other's company while grazing (cf., Figure 1).

Cattle seek out shady places during the hottest time of the day because they are very susceptible to heat stress (Kidd, 1993; Silanikove, 2000; Mitlöhner et al., 2001; Figure 6). If the pasture does not include trees or other shade-casting structures, a shademobile should be provided to ensure that the animals can avoid extreme exposure to direct sunlight during hot weather conditions (Salatin, 1991).

Figure 6. Cattle must have access to shaded areas to forestall heat stress.

• Cattle don't like to lie on hard or wet surfaces but prefer dry, relatively soft locations for resting (Irps, 1983; Jensen et al., 1988). It should be remembered that recumbent animals need considerable space in front of them to "swing" up into a standing position (Figure 7; Hoffmann and Rist, 1975).

Figure 7. Cattle need considerable space in front of them to "swing" up into a standing position (Drawing by H. Hoffmann).

Under indoor-housing conditions, cattle should be provided with a dry, well heat-insulated, straw-bedded lying area. They prefer straw over sawdust, mats or slats as floor type (Lowe et al., 2001). Straw not only provides comfort while lying but also resistance to slipping, and opportunity to express natural foraging behavior. Solid concrete and slatted floors, especially when they are slippery, dirty, and wet, create a serious risk of injuries (Anonymous, 2001). All animals must have free access to resting sites that are spacious enough to allow for unrestricted, cattle-specific resting postures and freedom of movement during postural changes. Straw is a cattle-appropriate resting substrate and should be used whenever possible (Krohn and Munksgaard, 1997; Figure 8). Lying mats can be equivalent to straw bedding in terms of cattle resting behavior, but they are less favorable with respect to leg injuries (Wechsler et al., 2000).

Figure 8. Straw is a cattle-appropriate resting substrate and should be used whenever possible (Photo by Hans-Peter Haering).

• Cattle are herbivores. They need rather voluminous fodder with a high fiber content for normal digestion and normal metabolism.

In the research setting, special care must be taken that cattle receive enough roughage to stimulate feeding and ruminating (Graf, 1994). A diet that is too concentrated may lead to metabolic imbalances, indigestion, and the development of behavioral disorders such as tongue rolling and nibbling at objects. Cattle who have ad libitum access to hay or regular access to a pasture do not develop these stereotypies.

Figure 9. Positions in the order of entrance into the milking parlor of two cows – of a 26-animal herd – during the morning and afternoon milking on 31 consecutive days. The order of entrance is correlated with the social hierarchy; cow Kalidel had the social rank place No. 3, cow Kakdie place No. 21 (Reinhardt and Reinhardt, 1980b).

• Cattle develop strong habits in their daily routine. When moving from one location to another - e.g., from the barn to the pasture - or when entering the milking parlor or the chute, they proceed in a predictable order in which each herd member has a well-defined place (Reinhardt, 1973; Reinhardt, 1983b; Andrada et al., 2001; Figure 9). When lying down, individual animals occupy specific resting sites with consistent preference (Schmisseur et al., 1966; Thinès et al., 1975; Reinhardt et al., 1978; Figure 10). These habits introduce a predictable routine in a herd's daily activities that should be respected by personnel. A cow may enter the milking parlor calmly when it is her turn but get obnoxious and stressed when coerced to do so too early. Interference in these habits also has a socially disruptive effect that disturbs not only one selected animal but the whole herd.

Figure 10. Resting positions of the two cows Elsa (left figure) and Alma (right figure) - members of a 29-cow herd [plus calves and one bull] – 30 minutes after darkness in a 20 x 22 m resting area on 318 consecutive days (Reinhardt et al., 1978).

• Cows, calves, but also bulls readily establish a positive relationship with humans. They seem to enjoy being scratched by a trustworthy person no less than being groomed by another conspecific (Figure 11; cf., Norton et al., 2000). At the same time, however, cattle get easily frightened and stressed by a person who is hectic, impatient, or even callous (Kidd, 1994). Research data collected under such circumstances are confounded by stress, and hence have no scientific value.

Figure 11. Cattle enjoy being groomed. Such a friendly interaction fosters a human-animal relationship that is based on trust rather than fear.

Animal caretakers and animal technicians must be knowledgeable of cattle behavior and cattle psychology (Grandin, 1989; Albright and Arave, 1997), and they must be willing and compassionate enough to establish a good relationship with the animals in their charge. Cattle who are well socialized with people are less fearful, grow more quickly, have higher rates of milk production, and show improved immune competence (Mench et al., 1998). Professional, i.e., considerate handling implies that the research subject shows no signs of apprehension when being approached, and no signs of fear, resistance or distress when being held in a stationary position, manipulated [e.g., for blood collection] or moved [e.g., enter an experimental stall]. This type of interaction increases the safety of the handling person, since the animal has no reason to show defense aggression; at the same time it buffers stress reactions, thereby preventing physiological changes that could confound research results. Cattle who have a good relationship with the handling personnel will show reliable baseline values of stress-sensitive parameters during procedures (Karg et al., 1972; Reinhardt and Schams, 1974). A positive human-animal relationship and good knowledge of bovine behavior also make the dehorning of cattle superfluous (Menke et al., 1999).

Cattle are not dumb beasts. They are very sensitive and quickly learn whom they can trust and whom they should avoid. They are not stubborn or aggressive by nature, but a brutal or unskilled person can easily trigger these reactions in them. In their behavioral responses, cattle - like all other confined animals - mirror the attitude of the people whom they are in contact with. When they exhibit so-called undesirable behavior, such as defensive aggression, it is always good advice to ask yourself "What is wrong with the way I treat them?" To blame animals for their reactions to our inappropriate behavior, would reflect a high degree of ethological ignorance (Figure 12).

Figure 12a,b. A young cow warns you with a broadside-threat not to approach her (Figure 12a). If she attacks you (Figure 12b), there is no reason to blame her for a natural behavior reaction that is triggered by your inappropriate behavior. Good knowledge of cattle psychology is one of the basic prerequisites of good stockmanship.

Recommendations

The following provisions are basic requirements for cattle-adequate husbandry in research institutions:
1) Social housing;
2) Sufficient feeding space and straw-bedded lying area for all group members;
3) Stable social relationships;
4) Access to pasture;
5) Positive human-animal relationship;
6) Firm-and-gentle handling.

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Viktor Reinhardt is Laboratory Animal Advisor to the Animal Welfare Institute in Washington, DC. He is a clinical veterinarian and ethologist and did extensive research in reproductive physiology, animal husbandry and ethology in cattle, muskox and bison.

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.

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