assessment of stress during handling and transport

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T GrandinAssessment of stress during handling and transport.

1997, 75:249-257. J ANIM SCI

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1Presented a t a sympos ium t i t led Effects of S t ress in FarmAnimals at the ASAS 87th Annu. Mtg., Orlando, FL, July 26, 1995

2T h e a u t h or w ou ld l ik e t o t h a n k M a r k D ee sin g a n d J u l ieSt ru thers for ass is tance with l ib ra ry research .

Received August 25, 1995.Accepted February 2 , 1996.

Assessment of Stress During Handling and Transport 1,2

T. G ra n d i n

Department of Animal Sciences , Colorado Sta te Univers ity, For t Col lins 80523

ABSTRACT: Fear is a very strong stressor, and thehighly variable results of handling and transportations tudies a re likely to be due to d iffe ren t leve ls of psychological stress. Psychological stress is fear stress.Some examples are restraint, contact with people, orexposure to nove lty. In many d iffe ren t an ima ls ,s t im u la t ion of t h e a m ygd a la wit h a n im pla n t edelectrode triggers a complex pattern of behavior andautonomic responses that resemble fear in humans.Both previous experience a nd genetic factors affectingtemperament will interact in complex ways to deter-mine how fearful an animal may become when i t i s

handled or t ransported. Catt le trained and habituatedto a squeeze chute may have baseline cortisol levelsand be behaviorally calm, whereas extensively rearedanimals may have elevated cortisol levels in the samesqueeze chute . The squeeze chute is perceived asneutra l and non-threatening to one a nimal; to anotheranimal, the novel ty of i t may t r igger in tense fear.N ove lt y is a s t ron g s t re ss or w he n a n a n im a l issuddenly confronted with i t . To accurately assess ananimals reaction, a combination of behavioral andphysiological measurements wil l provide the bestoveral l measurement of animal discomfort .

Key Words: Handling, Rest ra int , Welfare , Anxiety, St ress, Slaughter

J . Anim. Sci. 1997. 75:249257

Introduction

Studies to determine the amount of stress on farmanimals during routine handling and transport oftenhave h igh ly va r iab le r e su lt s and a re d ifficu lt t ointerpret from an animal welfare s tandpoint . Thispaper will cover some of the factors that influence how

an animal may react dur ing ha ndling. Much of thevariability between handling studies is l ikely to bedue to different levels of psychological stress. Animalscan be str essed by either psychological stress (re s-t r a in t , hand ling, or novel ty) or phys ica l s t r es ses(hunger , th irst , fatigue, injury, or therma l extrem es).Procedures such as restraint in a squeeze chute do notusua lly cause s ign ifican t pa in , but fea r may be amajor psychological stressor in extensively raisedcattle. Man y a pparen tly conflicting results of differents tudies may be explained i f the varying amounts of psychological stress and physical stress within eachstudy are considered. Fear responses in a particular

situation are difficult to predict because they dependon how the animal perceives the handling or transportexperience. The an ima ls r eactions will be governed by

a complex interaction of genetic factors and previousexper iences . For example, animals with previousexperiences with rough handling will remember it andmay become more stressed when handled in the futurethan animals t hat have had previous experiences withgentle handling. Previous handling experiences mayinteract with genetic factors. Rough handling may be

more detr imental and s t ressful t o animals wi th anexci table t emperament compared to animals with amore placid temperament . For example, Brahman-cross cattle had higher cortisol levels when restrainedin a squeeze chute than English crosses (Zavy et al . ,1992). An a nimals social ra nk within the group canalso affect stress levels. McGlone et al. (1993) foundthat subordinate submissive pigs were more stressedby 4 h of t ranspor t than dominant p igs . This paperwil l only address shor t -term s t ressors such as han-d ling and t r anspor t . The measurement of ch ron icstress imposed by the environment or different hous-ing sys tems is much more complex.

Importance of Fear and Effects of No velty

Fear is a universal emotion in th e a nimal kingdomand motivates animals to avoid predators . Al l ver-tebrates can be fear-conditioned (LeDoux, 1994). Theamygdala in t he brain is probably the centra l fearsystem that is involved in both fear behavior and theacquisition of conditioned fear (Davis , 1992). Davis



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( 1 9 9 2 ) cit ed ove r 20 a n im a l s t ud ie s fr om m a n ydifferent laborator ies that showed that e lect r icals t im u la t ion of t h e a m ygd a la w it h a n im pla n t edelectrode triggers a complex pattern of behaviors andchanges in autonomic responses that resembles fear inhumans . In humans , e lect r ica l s t imula t ion of theam ygdala elicits feelings of fear (Gloor et al., 1981).Studies have also shown that electrical stimulation of

the amygdala will increase plasma corticosterone incats (Setckle iv e t a l ., 1961; Matheson e t a l ., 1971)and in r ats (Redgate and F ahringer, 1973). Lesioningof t he amygdala will block both unconditioned andcondit ioned fear responses (Davis , 1992). Largelesions in the amygdala will r educe emotionality inwild rats as measured by flight distance (Kemble eta l., 1 98 4). Ke mble e t a l. ( 1 9 8 4 ) a ls o n ot ed t h a tlesioning of the amygdala had a taming effect on wildrat s. LeDoux (19 94) explains that fear conditioningt a kes p la ce in a s ubcor t ica l p at h wa y a n d t h atextinguishing a conditioned fear response is difficultbecause i t r equires the animal to suppress the fearmemory via an active learning process. A single, veryaversive event can produce a strong conditioned fearresponse, but extinguishing th is fear response is muchmore difficult.

Observations by the author on cattle ranches haveshown that to prevent cattle and sheep from becomingaverse and fearful of a new squeeze chute or corra lsystem, painful or highly aversive procedures shouldbe avoided the first time the animals enter the facility.The same p r inciple a l so applie s to r a t s . Ra t s tha treceive a strong electrical shock the first t ime theye nt er a n ove l a lle y w ill r efu s e t o e nt er it a ga in(Miller, 1960). However, if the rat is subjected to aseries of shocks of gradually increasing intensity, i twill continue to enter the alley to get a food reward.Therefore, Hutson (1993) recommends that stress insheep during routine handling could be reduced if theanima ls were conditioned gradua lly to handling proce-dures. Less severe procedures should be done first(Stephens and Toner, 1975; Dantzer and Mormede,1983).

Novelty is a very s t rong s t ressor (Stephens andToner, 1975; Moberg and Wood, 1982; Dant zer andMormede, 1983). This is especia lly t r ue when ananimal is suddenly confronted with i t . In the wild,

novelty and strange sights or sounds are often a signof d a nge r (G r a n d in , 1 99 3a ) . Ca t t le w ill ba lk a tsha dows or differences in flooring during movementthrough handling facilities (Grandin, 1980). Pigs thathave been t r a ined to l abora tory p rocedures wil lrespond to deviations in their daily routine with a risein blood pressure (Miller and Twohill , 1983). Reidand Mills (1962) have suggested that livestock can betra ined to accept changes in management rout inesthat would cause a significant increase in physiologi-ca l m ea s ur em en t s in a n im a ls t h a t h a d n ot be entra ined. Gradual exposure of animals to novel ex-per iences enables them to become accustomed to

nonpainful stimuli th at ha d pr eviously evoked a flightreact ion. Grandin e t a l . (1995b) repor ted that t ra in-ing nyala an telope t o cooperat e du ring blood sa mplinghad to be done ve ry s lowly to avoid t r igge r ing amassive flight reaction. The animals are very vigilantand wil l react to any unfamiliar s ights a nd sounds.

There a re some s itua t ions in which nove lty isattractive to animals. Cattle and pigs often approach

and man ipu la te a p iece of paper d ropped on theground. The author has observed that the same pieceof paper will cause animals to balk and jump away if they are being forced to walk toward it. Therefore, thep ap er m a y be p er ceived a s t h rea t en in g in on esituation and non-threatening in another. The authorhas observed that ca t t le in the Phi lippines se ldomreact to cars, tru cks, and other distra ctions when t heygraze on the highway median s t r ip. Cars and t rucksar e no longer novel because they ha ve seen th em sincebir th . In the nyala ante lope, animals born af ter theadults had been trained to blood sampling procedureslearned to cooperate more quickly (Gra ndin e t a l .,

1995b).Cat t le can become accustomed to repeated non-avers ive procedures such as weighing or drawingblood through an indwelling catheter (Peischel et al.,1980; Alam and Dobson, 1986). Sheep, p igs , andgira ffes have been t r a ined to volun ta r ily en ter ares t ra int device (Panepinto , 1983; Wienker, 1986;Grandin, 1989).

However, a nimals do not habituate to procedurest h a t a r e ve ry a ve rs ive (H a rgr e a ve s a n d H u t son ,1990a). A procedure can be h ighly a versive withoutbeing pa in fu l. Fu ll inve r sion to an upside-downposit ion is extremely avers ive to sheep. The t ime

required to dr ive sheep down a race in to a res t ra intdevice that inverted t hem increased th e following year(Hutson, 1985). Cortisol levels did not decrease withexper ience when cat t le were subjected to repeatedtruck t r ips dur ing which they fel l down (Fel l andShut t , 1986) . Hargreaves a nd Hutson (1990a ) foundtha t r epea ted t r ia ls of a sham shea r ing p rocedurefailed to redu ce the s tress response. Sheep also did noth a bit u a t e t o 6 h of r es t ra in t w it h t h eir le gs t ie d(Coppinger e t a l ., 1991).

Apple e t a l . (1995) found tha t in sheep, 6 h of r e st r a int s t r es s caused da rk cu t t ing mea t and ve ryh igh (> 110 ng /mL) leve ls of cor t isol. Ep idura l

blockage with l idocaine, which prevents the animalsfrom contracting their muscles and straining againstthe restraint, failed to inhibit glycogen metabolism.This experiment indicates that psychological stresswas probably a s ignificant factor.

Cattle are very sensitive to the relative aversive-ness of different parts of h andling procedures. Whenthey were handled every 30 d in a squeeze chute and as ingle animal scale, balking a t the scale decreasedwith successive experience and balking at the squeezech u t e in cr ea s ed s ligh t ly (G r a n d in , 1 99 2). T heanimals learned that the scale never caused discom-for t . Cat t le that had been mishandled in a squeeze



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chu te and s t ruck ha rd on the head by the headga tewere more likely to resist entry into the chute in thefuture (Gran din e t a l ., 1994) compared with cat t let h a t h a d n eve r be en h it w it h t h e h ea dga t e.

Effects of Adaptation to Handling on S tress

Tame an imal s tha t a re accus tomed to fr equen tha ndling and close conta ct with people a re u sually lesss t ressed by res t ra int and handling than animals thatseldom see people. Binstead (1977 ), Fordyce et al .( 1 98 5 ), a n d F or dyce ( 1 9 8 7 ) r ep or t t h a t t r a in in gweanling heifer calves produced calmer adult animalstha t were easier to h andle. Training th ese extensivelyraised calves involved walking quietly among them,teaching them to fol low a lead horseman and quie twalking through chutes . How an animal is ha ndledearly in l ife will h ave an effect on its physiologicalr es pon se t o s t re ss or s la t er in life . Ca lve s on aunivers ity exper iment s ta t ion that had become ac-customed to pet t ing by vis itors had lower cor t isolle vels a ft er r es t ra in t t h a n ca lve s t h a t h a d le ssfrequent contact with people (Boan dle et al ., 19 89).Lay e t a l . (1992a) found that res t ra int in a squeezechute was almost as stressful as hot-iron branding forextensively reared beef cattle. In hand-reared dairycows, branding was much more s t ressful than res-t r a in t ( La y e t a l., 1 99 2b ).

Taming may reduce the physiological reactivity of the n ervous system. Hastings et al . (1992 ) found th athand-rea red dee r had lower cor t isol leve ls a ft e rre st r a int compared with fr ee-ranging dee r. Even

though the physiological response to res t ra int waslower in the tame animals, hand-reared deer struggled ju st a s viole nt ly a s free -range de er (H a st in gs et a l.,1992). Associa t ions that animals make seem to behighly specific. Mateo et al . (1991) found that tamesheep approached a person more quickly, but be-havioral measurements of stru ggling indicated thattaming did not generalize to other procedures. Similarfindings by Hargreaves and Hutson (1990a,b) showedtha t gentling and reduction of the sheeps flight zonefailed to reduce aversion to shearing. Tame animalscan sometimes have an extreme flight reaction whensuddenly confronted with novelty that is perceived asa threat . Reports from ranchers and horse t ra inersindicate that horses and cattle that are calm and easyto hand le a t the ir home fa rm somet imes becomeextremely a gitated when confronted with the noveltyof a livestock show or a uction. The a nima ls beh avioralreaction seems to be less likely to generalize to otherprocedures than its physiological reaction. Moberg andWood (198 2) found that experiences during rear inggreatly affected behavior in an open field test but hadl it t le effect on adrenocor t ical response of lambs.Exposing piglets to novel noises for 20 min increasesbot h h ea r t r a te a n d m ot or a ct ivit y. H ea r t r a te

habituated to a recording of abat toi r sounds morequickly than motor activity (Spensley et al . , 1995).

The effects of previous experience on an an imalsfear response may provide one explanat ion for theoft en va r iab le r e su lt s in hand ling and t r anspor tstudies. F or example, extensively ra ised animals mayhave more psychological or fear stress during loadingand unloading for transport compared to more inten-

sively reared animals. Brit ish researchers have foundthat loading and unloading of sheep and calves wasthe most stressful par t of the journey (Tru nkfield andBroom, 1990; Knowles, 1995). Kenney a nd Tarran t( 1 9 8 7 ) r ep or t ed t h a t for I r is h ca t t le , t h e a ct u a l journey wa s more st r es sfu l than loa ding and unloa d-ing. The physical stresses of the trip, such as jiggling,were more stressful than the psychological stresses of loading or unloading. A possible explana tion for thisdiscrepancy between these two s tudies may be theamount of contact the animals had with people. Theremay be a big difference in the degree of fear s t ressbetween U.S. cattle reared on rangeland where theyseldom see people and European pasture-reared cattle.Differences in the degree of psychological stress mayexplain why too many rest stops during long-distancetransport is detrimental to the health of weaner calvesra ised under U.S. condit ions . Cat t le feeders havele ar n ed fr om p r act ica l e xp er ie nce t h a t 200- t o300-kg calves shipped from the southeast to Texas willhave fewer health problems i f they a re t ranspor tedn on -s t op for t h e e nt ir e 32-h ou r t r ip . F or t h es eextensively reared calves, rest stops ma y possibly turninto str ess stops. Research is needed to conclusivelydete rmine wha t factor s cause the r e st s tops to best ressful . Legisla t ing too many res t s tops may bedetrimental to welfare. One possibility is fear stressdur ing loading a nd unloading a t res t s tops and thesecond possibility is tha t the calves become infectedwith diseases a t the res t s top. Many of the calvesshipped on these trips a re not properly vaccinated.There may be an in teract ion between res t s tops anddisease. Frequent rest stops may be more beneficial tofully vaccinated calves.

Genetics

Genet ic factors such as temperament in teract incomplex ways with an animals previous handlingexper iences and learning to determine how i t wil lreact dur ing a par t icular handl ing procedure. Wildspecies are usua lly more rea ctive to novel stimuli th andomest icated animals . Pr ice (1984 ) mainta ins thatthe domest ic phenotype have reduced responses tochanges in the environment . Domest icated animalsa re more s t r es s-resi st an t because they have beenselected for a calm atti tude toward people (Parsons,1988). When deer or antelope are tamed, the fl ightytemperament is masked until they are confronted witha novel s t imulus that i s perceived a s threatening. A



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tame deer or antelope can have an explosive reactionto a novel event . A wild species has a more in tenseflight response because this enables i t to flee frompredators.

Temperament in cattle is a heritable trait that mayaffect t he a nimals rea ction to han dling (L e Neindre etal., 1995). There are differences in temperament bothbetween and within cat t le breeds. Within the Brah-

man breed, temperament is her i table (Hearn shaw etal., 1979; Fordyce et al., 1988). Temperament differ-ences between breeds have a lso been repor ted byStr icklin e t a l . (1980 ) and Tulloh (1961) . Genet icsalso affects an animals response to str ess. Brahm an-cross cattle had higher cortisol levels while restrainedin a squeeze chute compared to English crosses (Zavye t a l., 1992). Recen t r e sea rch by Grand in e t a l .(1995a) and replicated by H. Randle (1995, personalcommun ication, University of Plymouth, U.K.) indi-cated th at the spiral ha ir whorl on a bovines forehea dis an indicator of temperament. Cattle with spiral hairwhorls above the eyes became more agita ted whileres t ra ined tha n animals with hair whorls below theeyes.

Temperament may be under genet ic con t rol inmany different animals. Research with rats has showntha t they can be selected for e ithe r h igh or lowemotionality (Fujita et al., 1994) or for reduced fear-induced aggress iveness toward humans (Popova e tal ., 1993). Phenotypic characteristics are also relatedto temperament . Interestingly, i t seems that differentgenetic factors control fear-induced aggression andintermale aggression. Select ion for reduced fear-induced aggression had no effect on aggressive be-havior toward othe r ma le r a t s .

Temperam ent is a trait that seems to be stable overtime. In European Continental-cross catt le, certainindividuals became extremely agita ted every t imethey were handled in a squeeze chute and others werealways calm (Grandin, 1992) . The agi ta ted animalsfa i led t o adapt to being held in the squeeze chutedur ing four hand ling sess ions spaced 30 d apa r t .Cat t le wi th a very exci table temperament may havegreater d ifficul ty adapt ing to repeated nonpainfulhandling procedures than cattle with a calmer temper-ament. The two types of animals may have differingphysiological and behavioral reactions to the same

procedure . Animals with a calm temperament mayadapt more easi ly and become le ss s t r es sed withrepea ted hand ling t r ea tmen t s and an imals with avery excitable temperament may become increasinglys t r es sed with each repea ted hand ling t r ea tmen t .Lanier et al . (1995) found that some pigs habituatedto a swimming t a sk and main ta ined nea r base linelevels of epinephrine and norepinephrine and otheran imal s fa il ed to hab itua te and never adapted.

At five s laugh te r p lan t s in the Unit ed S ta tes ,Holland, and Ireland, the author has observed increas-ing problems with very excitable pigs and cattle fromcertain genetic lines that become highly agitated. It is

a lmost impossible to dr ive them quiet ly through ahigh-speed slaughter line. These animals seem to havea much stronger startle reaction to novelty, are morelikely to balk at small distractions such as shadows orreflections in the race, and are more likely to bunchtogether. Observations at slaughter plants and reportsfrom ra nchers also indicate tha t excitable cattle arem or e lik ely t o in ju r e t h em s elve s wh en t h ey a r e

confronted with the novel, unfamiliar surroundings of an auction m arket or slaughter plant. The appearanceof greater numbers of more excitable pigs and cattlemay possibly be related to the increasing emphasis of the l ivestock industry on lean beef and pork. In bothcattle and pigs, the author has observed that excessiveexci tabi li ty occurs most often in animals bred forl eanness tha t have a s lender body shape and finebones . Cat t le and pigs bred for large , bulging leanmuscles usually have a calmer temperament. This isa n a r ea t h at n eed s t o be r es ea r ch ed. P r act ica lexperience indicates t hat the excitable an imal pr oblemneeds to be corrected because excessive excitabilitycreates serious animal welfare problems during han-d ling a t auct ion market s and s laugh te r p lan t s .

Cat t le and pig producers need to se lect animalswith a calm temperament, but care must be taken notto over-select for any one par t icular t ra i t . A goodexample of overselect ion for a s ingle t ra i t i s theha lothane gene in p igs . P igs with th is gene haveincreased mea t p roduct ion , bu t the p r ice for th isincreased production is poor meat quality (Pomm ierand Houde, 1993). Over-selection for calm tempera-ment may possibly have detrimental effects on eco-nomically important traits, such as maternal abili ty.Researchers in Russia found that selecting foxes forcalmness over 80 yr produced animals that lost theirseasonal breeding pat tern and had s t range piebaldblack and white colored coats (Belyaev, 1979; Belyaevand Borodin, 1982). The foxes turned into animalsthat acted and looked l ike Border col lies .

Fear Pheromones

Another factor that could confound handling stresss tudies is fear pheromones. Vievi lle-Thomas andSignoret (1992) found that urine from a stressed gilt

caused other gilts to avoid a feed dispenser and urinefrom an unst ressed a nimal had no effect . Both theresults of th is exper iment and observat ions by t heauthor indicate that i t takes 10 to 15 min for the fearpheromone to be secreted. Observations by the authorind ica te tha t ca t t le will volun ta r ily wa lk in to arestraining chute that is covered with blood, but if anan imal becomes ext remely agi t a ted for seve ra lminutes, the other animals refused to enter (Gra ndin,1993b). In a labora tory set t ing p igs witness ingslaughter had no increases in either beta endorphinsor cor t isol . These were ca lm an imals fit t ed with jugu la r ca thet er s (An il et a l., 1995). Eibl -Eibe sfe ldt



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Table 1. Mean cortisol values in cattle during handling

Cor t isol level, ng/m L Breed Sex Study

Baseline

.5 to 2 Fr iesia n Bulls Tennessen et a l., 19842 Fr iesia n Cows Ala m a nd Dobson , 19863 An gu s cross Bull ca lves Henr icks et a l., 19846 An gu s cross Heifer ca lves H en r icks et a l., 19849 Fr iesla nd an d Nuguni Cows Mitchell et a l., 1988

Res t ra in t in headgate

13 Holstein cows Ha nd-r ea red La y et a l., 1992a2 4 (w ea n e d 2 wk b efor e t e s t ) U n kn ow n B rit is h or E u r op ea n We an lin gs , m ixe d s exe s Cr ook sh a n k e t a l., 1 97927 Bra hma n cross Steers Ra y et a l., 197228 Angu s Hereford Steers Za vy et a l., 199230 Simmenta l Hereford Brah-

ma n83% Steer s La y et a l., 1992b

36 Angu s Bra hma n Steers Za vy et a l., 199246 (wea ned day of t es t) Unknown Br it ish or E uropea n Mixed sexes Crooksha nk et a l., 197963 Bra hma n Hereford

AfrikanderSt eer s a nd h eifer s Mitch ell et a l., 1988

Extreme value

93 (in ver ted on ba ck for 103 s ) Unkn own Br it ish or Eu ropea n Mixed Dunn , 1990

(1970 ) observed that i f a r a t i s ins tant ly ki lled by at rap, the t rap wi l l remain effect ive and can be usedagain . Rats wil l avoid a t rap that fa i led t o ins tant lyk ill. Resea rch with r a t s ind ica tes tha t b lood maycon ta in a fea r pheromone (S tevens and Gerzog-Thomas, 1977). Stevens an d Saplikoski (19 73 ) foundthat b lood and muscle t i ssue f rom s t ressed ra ts wasavoided in a choice tes t , whereas brain t i ssue and

water had no effect. Blood from guinea pigs and peoplealso had lit t le effect (Horn buckle a nd Beall , 1974).

Short-Term Stress Measurements

This discussion will be limited to measuring short-term stress induced by ha ndling procedures such a sbeing h eld in a squeeze chute. Assessment of stressand discomfort should conta in both behavioral andphysiological measu res. Behaviora l indicat ors of dis-comfort ar e at tempt ing t o escape, vocalization, kick-ing, or struggling. Other behavioral measures of howan animal perceives a handling procedure are choicetests and aversion tests. Common physiological meas-ures of stress are cortisol, beta endorphin, and heartr a t e . Cor t isol i s a usefu l ind ica tor of shor t -t e rmstresses from handling or husbandry procedures suchas cas t ra t ion. Researchers must remember that cor-tisol is a t ime-dependent measure that takes 10 to 20m in t o r ea ch p ea k va lu es ( La y e t a l., 1 99 2a ) .

A review of many s tudies indicates that cor t isollevels in catt le fall into t hree categories: 1) baseline,2) levels that occur dur ing res t ra int in a headgate ,and 3) extreme s t ress (Table 1) . Cort isol levels are

highly variable and absolute comparisons should notbe ma de between studies, but the figures on Tables 1

and 2 would make it possible to determine whether ahandling or slaughter procedure was either very lows t res s or ve ry h igh s t r es s . One cou ld t en ta t ive lyconclude that a mean value of >70 ng/mL in e ithersteers or cows would possibly be an indicator of eitherrough handling or poor equipment , and low valuesclose to the basel ine values would indicate that aprocedure was e ither low s t ress or was very quick.

Quick procedures would be completed before cortisollevels could rise. Restraint in a headgate for bloodsampling and s laugh te r p roduced s imila r va lues(Tables 1 and 2) . Sexual ly mature bul ls have muchlower cor t isol levels than s teers , cows, or heifers(Tennessen e t a l ., 1984). In one s tudy, there was anextreme m ean of 93 ng/mL for inverting cattle on t heirbacks for 103 s (Dun n, 1990). This very high figure isnot due to differences in assay methods because thissame researcher obtained more reasonable values of 45 ng/mL for upright restraint. Properly performedcat t le s laughter seems to be no more s t ressful thanfa r m r es tr a in t (Ta bl es 1 a n d 2 ).

Less clear cut ranges have been obtained in sheep.Pearson et al . (1977) found that slaughter in a quietresear ch aba ttoir pr oduced lower cort isol levels tha nslaughter in a noisy commercia l p lant . The valueswere 40 vs 61 ng/mL. Values for shearing and otheron-farm handling procedures were 73 ng/mL (Har -greaves and Hutson, 1990c,d) and 72 ng/mL (Kilgoura n d d e La n ge n, 1 97 0). P r olon ge d r es t ra in t a n disolation for 2 h increased cortisol levels up to 100 ng/ m L (Ap p le e t a l., 1 99 3).

Creatine phosphokinase ( CP K ) and l acta t e seemto be u seful m easures for assessing h andling stresses

in p igs (War r i s e t a l ., 1994). War r is e t a l. (1994)found tha t the sound leve l of squea ling p igs in a



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Table 2. Mean cortisol values du ring slaughter

a Conducted in ei ther England or Ir eland with Bos taurus cattle.

Cor t isol level, ng/mL H a ndling m ethods Study

Baseline quiet research a battoir

15 Held in h ea d rest ra in t , shot imm edia tely with ca pt ive bolt Tum e an d Sha w, 1992

Commercial slaughter plant

24 Ha ndled quiet ly in convent iona l stun ning box E wba nk et a l., 1992a32 Unknown Mitchell et a l., 198844 Convent iona l stunning box Tum e a nd Sha w, 199245 Convent iona l stunnin g box Dunn , 1990a51 P oor ly design ed h ea d r est ra in t on ly 14% of ca t t le volu nta r ily en-

te red i tEwbank et al ., 1992a

63 (m e di a n) E lect ric pr od a ll ca tt le, 38% a nim als slipped, con ven tion al st unbox

Cockra m and Corley, 1991a

Ext reme s t ress

93 Inver ted on back for 103 s Dunn, 1990 a

commercial abattoir was highly correlated with CPKmeasurements. White et al . (1995) also reported that

vocalizations in pigs were indicative of stress and werecorrelated with other measures of acute stress, such asheart rat e. Cattle th at become behaviorally agitatedhave higher cortisol levels (Stahringer et al . , 1989).Hear t r a t e in ca t t le dur ing re s t r a in t in a squeezechute was highly correlated with cortisol levels (Laye t a l., 1992a ,b ). S termer e t a l . (1981) found tha trough handling in poorly designed facilities resulted ingr ea t er h ea r t r a t es t h a n qu ie t h a n dlin g in w ell-designed facilities.

Isolation is also a factor in handling stress. Duringrestraint for routine husbandry procedures, animalsare often separated from their conspecifics. Stookey et

al . (1994) found that cattle became less behaviorallyagitated during weighing on a single animal scale if they could see another animal in the chute less tha n 1m away in front of the scale. Agitation was measuredelectronically by measuring movement and jiggling viathe scale load cell sys tem. Numerous s tudies haveshown that i sola t ion from conspecifics wil l ra isecortisol and other physiological measures (Kilgourand deLangen, 1970; Whittlestone et al., 1970; Aravee t a l ., 1974).

Aversion Tests

Aversion to a handling procedure can be m easuredby either choice testing or measuring aversion. Onemeasure of aversion is the t ime r equired t o induce a nanimal to re-enter a chute where i t was previouslyhandled (Rushen , 1986a,b 1995). In a choice t est , theanimals are allowed to choose between two differentchutes that lead to different procedures (Gra ndin etal ., 1986; Rushen and Congdon, 1986a,b). Anotherusefu l measure is the degree of force r equ ired toinduce a n animal to move through a race. In somecases, measuring the degree of force provides a moreaccurat e a ssessment of aversion than time. Examples

of force are the number of pats on the rump or numberof electr ical prods. Experience and genetic factors can

confound a version tests. Rushen (199 6) warns that toaccura te ly measure ave r sion in a r ace , the an imalmust exper ience the avers ive procedure more thanonce. Observations by the author indicate that excita-ble cattle sometimes run through a single fi le chutequickly in an attempt to escape. Research (in progressby Bridget te Voisinet and the au thor) reveals thatbu lls t r a ined to move th rough a r ace to a squeezechute exhibi t no avers ion in the race af ter a s inglenoxious treatm ent. After one aversive treat ment, theycontinued to voluntarily walk th rough the race intothe squeeze chute, but balking and turning back in thecr owd p en a t t h e en t ra n ce t o t h e r a ce gr ea t ly

increased. At th is point , t he animals may perceivethat they may be able to avoid re-entering the r ace. Inaversion studies, balking and other behaviors indica-tive of aversion must be measured in both the singlefile race and in t he pens and a lleys tha t lead up to theentrance of the s ingle fi le race. This is especia llyimportant if the aversive procedure is performed onlyonce. After the animal is forced to enter the chute thatleads to the squeeze, i t may perceive that i t may beable to escape by running quickly through it towardthe squeeze chute. Under certain conditions, choicetests may be unr eliable for m easur ing choices betweenmildly aversive procedures. Research conducted by

Grandin et al . (1994 ) showed that catt le are reluctantto change a p revious ly lea rned choice i f t he twochoices in a choice test are only mildly aversive. Otherresearch showed that sheep immediate ly switchedsides to avoid highly a versive electroimmobilization(Grand in e t a l ., 1986).

Implications

Both researchers and people making decisionsa bou t a n im a l w elfa r e m u st u n de rs t a nd t h a t fe arduring non-painful routine handling and transport can



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vary great ly. Fear is a very s t rong s t ressor. Cat t lethat have been t ra ined and habi tuated to a handl ingprocedure may be completely calm and have baselinecortisol and h eart rat e measur ements during han dlingand rest r a in t . Extensive ly r ea red ca t t le with anexci table disposit ion may have very high cor t isollevels an d show extreme behavioral agitat ion duringthe same procedure. For one animal, a squeeze chute

may be perceived a s n eutral and non-threatening, butto another i t may t r igger an extreme fear response.T he a n im a ls r es pon s e w ill be d et er m in ed b y acomplex interact ion of genet ics and previous ex-per ience. Studies to assess animal welfare dur inghandling and transport should contain both behavioraland physiological measurements.

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