behavioral comparison of layer and broiler fowl - measuring fear responese.pdf

8/14/2019 behavioral comparison of layer and broiler fowl - measuring fear responese.pdf

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ELSEVIER Applied A nimal Behaviour Science 49 (1996) 321-333

PPLIED NIM LBEH VIOUR

SCIENCE

Behavioural comparison of layer and broiler fowl:measuring fear responses

S. Keer-Keer, B.O . Hughes * P.M . Hocking, R.B. JonesRoslin Institute Edinburgh), Roslin EH25 9PS, UK

Accepted 27 February 1996

bstract

Broilers and White Leghorns have different temperaments; White Leghorns are regarded asflighty and broilers as docile. This difference in temperament is sometimes interpreted as adifference between the strains in underlying fearfulness. Five experiments were carried out tocompare fear responses of the two strains. All experimental birds were fed a medium-energy(breeder) replacement diet to reduce strain differences in body weight and locomotor activitywhich accom pany provision of standard broiler grower diets. The nature of the test stimuli, the testsituation and the age of the bird were varied betw een tests. In three of the experim ents, differencesin fear response between strains were minimal or absent. These included: exposure of isolatedIO-day-old chicks to a person situated at one end of a novel arena (Experiment l), exposure ofindividually caged -week-old birds to a person approaching from 1 m away (Experiment 31, andexposure of the same birds to a novel object placed at the front of the home cage (Experiment 4).In two experiments, strain differences were apparent. These were: exposure of 3-week-old chicks,placed in pairs in a novel cage, to a person approaching from 4 m away (Experiment 2) andexposure of 16-week-old birds, in groups of seven, to a large novel object (road hazard cone)placed in the test pen (Experiment 5). In both cases the Leghorns showed more marked avoidanceresponses than broilers. Legho rns physical response is often more vigorou s than that of broilers,and it was difficult to separate putative strain differences in the type of behavioural strategyadopte d u pon exposure to threat from the effects of unde rlying fearfulness. Results indicate eitherthat there is no difference in fear between the two strains, or that Leghorns are more fearful than

* Corresponding author. Tel.: (0131) 5 27-4200; fax: (0131) 440 0434.016% 159 1/96 / 15.00 Copyright 0 199 6 Elsevier Science B.V. All rights reserved.PII SOl68-1591(96)01055-6


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broilers, but strain differences only become apparent in a social situation or when the levels of fearevoked by the test are moderate.Keywor ds: Chicken; Fearful behaviour; Genetics

1 Introduction

The UK Farm Animal Welfare Council have identified five freedom s as beingimportant for safeguarding animal w elfare (Webster and Nicol, 1988 ). One of these isfreedom from fear. Fearfulness can be described as a propensity to be easily frightenedby a variety of potentially alarming situations (Jones and Waddington, 1992; Jones,1996). Dom estication has produc ed animals which seem to show lower fearfulness thantheir progenitors but there is still pronounced variation within and between strains.

There has long been a consensus (Murph y, 1977; Murp hy and Woo d-Gush, 1978;Duncan, 1985; Jones, 1987 a) that breeds, stocks and strains show consistent differencesin temperam ent (distinct nature and character). One of the most obvious traits isflightiness, which manifests as rapid movement or flight away from a recogniseddisturbing stimulus. Stock s selected for meat production are regarde d as less flighty thanthose selected for egg production (Siegel, 1984; Appleby et al., 1992 ). Strain differencesin flightiness have been interpreted in terms of differences in underlying fearfulness oremotionality (Murp hy and Woo d-Gush, 1978; Appleby et al., 1992 ).

There have been numerous comparisons of fear between light- and medium-hybridlaying fowl (Gallup et al., 1976; Jones, 1977; Mu rphy, 1977; Jones and Mills, 1983 1, butfew in which White Leg horns and broiler chickens were directly comp ared. This paucityof information may reflect the difficulty in developing a reliable and appropriatemethod ology. Fear is recognised by behavioural changes which include diverse forms ofdefensive behaviour such as passive avoidance, freezing, tonic immobility, withdraw aland vigorous escape (Kruijt, 1964; Duncan, 1985; Jones, 1987b ). How ever, there arelarge differences between stocks in their inherent level of locomo tor activity. Som e, likeLegho rns, are active, while others, like broilers, a re lethargic (although the locomo toractivity of broilers is greatly increased when they are restricted fed; Hocking et al.,1993 ). Pronounced differences in locomotion mak e it difficult to use activity-basedmeasu res as indices of fear when comp aring stocks. Wh ite Leghorns and broilers in thepresent study were fed a medium-energy (breeder) replacement diet; this would havereduced , tho ugh not eliminated, differences in body weight and locomo tor activity whichwould otherwise have accomp anied the provision of standard broiler grower d iets.

Duncan (1981 ) suggested that although fear is a hypothetical intervening variable, itis still possib le to define it operationally. Fear ideally functions to prot ect the animalfrom danger (Toates, 1980; Jones, 1987b) and because it takes precedence over andinhibits all other behaviour systems (Jones, 1987b; Jones, 1996 1, it is argued that theextent to which a test stimulus is avoided reflects the birds fear of it.

Several factors are known to induce or influence fearfulness in dom estic fowl;separation from conspecifics, exposu re to a novel environment or to an unfamiliarobject, approa ch of or proximity to a human being. The objective of the series of


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experiments described in this paper was to examine systematically the withdrawal/avoi-dance response of a Wh ite Leghorn and a broiler line in a number of tests in which thesefactors differed considerably.

2. General methodsThe comparisons were between both sexes of two parent-stock pure lines: a comm er-

cial male-line broiler (R oss Breeder L td., New bridge, UK) and a White Legh orn linemaintained as unselected stock for six generations at the Roslin Institute. The birds werehoused at 1 day of age in single-sex, single-strain groups of 25, in eight pens (2.44m X 1.52 ml containing wo od shavings. The pens were arranged in a systematic order tocontrol for possible environmental effects. At 7 wee ks of age the birds in each pen weresplit into two groups, one group was removed to a new pen, creating a total of 16 pens.All birds were fed a standard replacement (breeder) medium-energy diet ad libitum.Water w as provided ad libitum in suspended bell-shaped drinkers, one per pen.

3 Experiment 1: Box plus experimenter testThis test (Jones and Waddington, 1992 ) measures the approach/avo idance responses

of chicks to a human visible behind a wire wall, at the end of an unfamiliar arena.Becau se withdraw al is thought to be a functional fear behaviour (Toates, 1980 ), mark edavoidance in this test situation is considered to reflect increased fear of human beings.Chicks will view a stimulus either w ith the left or right eye according to its nature ornovelty value (Dharm aretnam and Andrew, 1994; Vallortigara and Andrew , 1994 ) andthey may use this strategy to self regulate their state (R.J. Andrew , personal communica-tion, 1995 ). Therefo re, lateralisation of viewing the experimenter, was also recorde d.3.1. Method

The chicks were tested on successive days when 10 or 11 days old; approximatelyhalf of each strain were tested on each day. Twenty-eight Legho rns (15 females, 13males) and 28 broilers (14 females, 14 males) were caught individually at random fromsuccessive pens (all pens represented) and carried to a nearby empty pen. Fourindividual Legho rns were tested, followed by four individual broilers. Each chick wasplaced in the centre of a rectangular box of 62 cm X 4 cm X 30 cm (length X width Xheight), successive chicks alternately facing the left or right side of the box. The box hadthree wood en walls and one of wire mesh (m esh size 1.5 cm>, the floor was covered inwo od shavings. The observer (S. K-K) sat directly in front of and facing the wire meshwall, with head and upper torso visible to the chick and approximately 30 cm away fromthe box. The box was divided widthw ays into four imaginary areas 15 cm X 4 cm(length X width), and the chicks position recorde d every 15 s during the 5 min testperiod. At each scan the chick scored 1 if it was in the area closest to the experimenter,through 2 and 3, to 4 at the far end. The total sco red (avoidance) by each c hick was the


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Table IExperiment I: means (f SE) scores of Leghorn and broiler chicks in box plus experimenter test (N = 28)

Leghorn Broiler Significance (P 1Avoidance 2.84 + 0.077 3.00*0.091 NSLateralisation 0.39 + 1.05 - 1.00+ 1.14 NSNo. of jumps 10.36f 1.51 3.29 + 0.56 0.001

mean o f 20 scans; high scores reflected high avoidance. While the position of each chickwas recorded, the eye with which it appeared to be observing the experimenter wassimultaneously noted. A lateralisation of viewing score was derived by calculating thetotal number of times the chick wa s recorde d viewing with the right eye minus thenumber of times it was recorde d viewing with the left. The number of jumps made byeach chick during the 5 min test period was also recorded.3.1.1. Statistical analysis

The effects of sex, strain, initial position and test day, and their interactions, wereanalysed using an AN OV A. Num bers of jumps by strains were com pared using theMann-Whitney U-test.3.2. Resul t s

The results are shown in Table 1. Neither the avoidance nor the lateralisation ofviewing scores differed between strains, but Leghorns jumped significantly more oftenthan broilers.

An almost significant interaction of sex and strain (P = 0.054) suggested that maleLegho rns show ed greater avoidance than females, whe reas male and female broilers hada similar avoidance score to each other. Gender exerted no detectable influence onlateralisation of viewing or jumping.

4. Experiment 2: Avoidance response to an approaching human corridor test)

This experiment measures the behavioural response of a bird to a human approachingalong a corridor and is based on metho ds described by Jones et al. (1981 1, Hem sworthand Bam ett (1989 ) and Bam ett et al. (1992). Chicks were tested in pairs in thisexperiment because pilot trials suggested that increased fear levels associated withisolation could mask responses to the approaching human.4.1. Materi al s and met hods4.1 .I. Birds

Birds wer e tested in random order when 3 week s old as same-sex , same-strain pairs;they were different individuals to those used in Experiment 1. Eight pairs (four male,


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S. Keer-Keer et al. / Applied Animal BehauiourScience 49 1996)321-333 325four female) of each strain we re tested, each pair once only. They were caugh t manuallyin their home pens and transported (a 5 min journey) as test pairs in a closed box.4.1.2. Testing environment

This was a separate room , lit by moderate-intensity (120 lux) fluorescent lights andmaintained at a temperature of 24C. Four cages of 40 cm X 60 cm X 68 cm (width Xlength X height) w ere used; they had plywood sides, 2-cm wire-mesh fronts, tops andbacks, and flat, littered floors. A cage wa s placed on a lOO-cm-high table 30 cm fromthe end of each o f four sep arate parallel corridors (5.3 m X 1.0 m; length X width), thewalls and one end (opposite end to the cage) of which were form ed of pale beige, cottonmaterial suspended on wires, like a curtain. A video came ra (Panasonic S-VH S 62 5,wide-angle lens), placed behind each cage, recorde d the birds behaviour; the approac h-ing human was also visible in the field of view.4.1.3. Procedure

Each pair was left to acclimatise in the test cage for l-2.5 h, mean acclimatisationtime was the same for both lines. Thirty minutes before testing, the video ca mera wasplaced behind the cage. The cam era was switched on remotely 5 s prior to testing. At thestart of the test the experimenter (S. K-K) em erged from behind the curtain at the end ofthe corridor at a distance of 4.3 m from the cage front. She advanced slowly, pausing fora 10 s interval at 3.5, 2 .5 and 1.5 m, and fo r 5 s at 1.0, 0.5 and 0 m, before finallyplacing a hand over the top of the cage. The behaviour of the birds was recorde d onvideotape and analysed. Their flight and avoidance reactions were scored on a three-pointscale (see Table 2). High scores reflect increased agitation. In almost all cases both birdswere visible and both were engaged in the same activity. Wh ere birds we re engaged indifferent activities both were scored and a mean value w as calculated. Wh ere only onebird could be seen clearly only its score wa s taken.4.1.4. Statistical analysis

Avoidance scores were com pared betw een strains using the Mann-Whitney U-test.The distribution of number of birds showing their first category 3 (flight) response byappro ach stage, was analysed using an extended Fisher ex act test. The effect of pre-testacclimatisation time and different test corridor w ere analysed using AN OV A.4.2. Results

The mean avoidance behaviour scores of both strains a t each stage are summ arised inFig. 1 . At all positions from 2.5 m onwards the Legho rns scored more highly (greater

Table 2Experiment 2: behavioural categories and their associated scoresscore Description

Sit, alert (head movements), stand stillMajor body movement away from stimulus

2 Flight response: agitated movements at rear of cage, sudden crouch, jump, panic, frantic mMing


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21 roilerH Leghorn

4.3 3.5 2.5 1.5 1.0 0.5 0.0 0.0aApproach stage (m)

Fig. 1. Experiment 2: mean ( + SE) avoidance behaviour scores of broilers and Leghorns in response to anapproaching human. At Oa m the experimenters hand was placed on top of the cage.

agitation) than the broilers, and the mean sco res overall were significantly higher(P = 0.004) for Leghorn s (1.80) than for broilers (1.27). The Leghorn s show ed a panicor flight response at an earlier stage in the appro ach (mean distance 1.2 m> than thebroilers (mean distance 0 m), and the distribution of first flight response by appro achstage (Table 3) was significantly different between lines (P < 0.004). Corridor used andpre-test acclimatisation time were not found to have an effect on mean behaviouralscore. No sex by strain interactions were detected.

5. Experiment 3: Home cage approach

In this test, like the previous one, we measured the responses of birds to humanapproa ch. How ever, here the birds were tested individually in a hom e c age at 11 wee ks

Table 3Experiment 2: numbers of bird pairs showing category 2 (flight response) at successive stages of approach(N = 8). At Oa m, the experimenters hand was placed on top of the cage

Distance of approaching person from birds (m) No response4.3 3.5 2.5 1.5 1.0 0.5 0 Oa

Leghorns 0 0 2 2 2 0 1 0Broilers 0 0 0 0 0 0 3 3 2


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old, and the human approa ched from a distance of 1 m in 20 s. The test was based onone described by Bam ett et al. (1992).5.1. Method

When the birds were 10.5 weeks old, 12 males of each strain were removed fromtheir hom e pens (three from each pen) and transferred to individual cages in the top andmiddle tier of a battery, measuring 40 cm X 48 cm X 58 cm (width X length X height)and 30 cm X 48 cm X 51 cm, respectively. The cages were allocated according to ablocking design to control for possible environmental effects such as tier or cage size.There were three blocks (two in the top tier and one in the middle tier) with eight birds(four of each strain) per block. Broilers and Legho rns were housed in alternate cagesbecause of a requirement of a subsequent experiment. The photop eriod ran from 08:30to 23:OO h. The birds h ad 1 wee k of acclimatisation in the cages before testing. Birdswere selected in random order for testing, with the proviso that the bird was not in acage adjacent to that used in the previous test. All birds in the experiment were tested onthe same day. The experimenter (S. K-K) assum ed a position directly opposite and 1 maway from the cage o f the bird being tested, with her face at cage level, then app roache din three stages:1. stood motionless at 1 m distance for 10 s, keeping her hands by her side;2. moved forwa rd to 0.5 m from the cage, and held the position for 10 s;3. moved forward to 0 m from the cage, placed a gloved hand and face (protected with

goggles) on the bars of the cage front.This procedure was achieved for top tier birds by stepping on stools.The orientation of the bird wa s recorde d on a five-point scale at 5 s intervals, that is,twice at each of the three distances. The scoring system was a modified version of the

novel object scoring system (H ughes and Black, 1974a ; Sefton, 1976 ). The scoring w asas follows: 0, head out of the front o f the cage; 1, head within the cage with birdoriented toward s front; 2 , bird facing the sides of the cage; 3, bird oriented towa rds therear of the cage; 4, bird exhibiting escape behaviour, usually at the back o f the cage. T hetotal orientation score w as the mean of the scores at the three stages: higher scoresrepresent an increasing degre e of fear/avoidance. Mean avoidance scores were com-pared between strains using a one-way AN OV A.

5.2. ResultsThe mean ( f SE) avoidance scores w ere 2.17 f 0.08 for Leghorns and 2.05 f 0.20

for broilers; they we re not significantly differen t.

6. Experiment 4: Response to a novel objectThis test, based on one first described by Hug hes and Black (197 4a), measures the

avoidance response of birds to a brightly coloured novel object placed in the food troughof their home cage.


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6 Method

The birds tested h ere were the same as those used in Experiment 3 and were testedthe day after Experiment 3. Birds w ere selected in random order fo r testing and all testswere completed on the same day. The novel object was a wooden rod 34 cm X 2.5 cm(height X width) rising vertically from a 10 cm X 15 cm square base. The rod wascovered with five different colours of 2-cm-wide plastic tape forming a multicolouredseries of bands. It was placed vertically in the centre of the food troug h, at the front ofthe cage. The observer stood 3 m to the side of the cage. T he birds response to theobject was recorded at 10-s intervals over a 3-min period (a total of 18 observations).The responses were scored as described in Experiment 3. The total scored by each birdwas the mean of 18 scans. Mean avoidance scores were compared between strains usinga one-way ANO VA.

6.2. Resul tsThe mean ( f SE) avoidance scores were 2.21 + 0.09 for Leghorns and 2.3 1 f 0.08

for broilers; they we re not significantly differen t.

7. Experiment 5: Pen and cone testIn this test the responses of Leghorn s and broilers to a novel object were again

measured . How ever, here the birds were tested in groups (of seven) in pens andavoidance of the novel object was measure d by calculating the distance of each birdfrom the object. T he test was based on one described by Jones (1 987c ). The responses ofthe birds were recorde d using video came ras.7.1. Method

The four test pens (two pairs) w ere in the same hut as the birds were housed. Eachpen (2.44 m X 1.53 m) contained a food hopper and bell water drinker; they weresimilar to the hom e pens exc ept that the litter w as fresh. A black and white cam era(Panasonic CC TV) was suspended above the centre of the pen, and the birds behaviourwas videotaped. Two tests were filmed simultaneously, tests took place between 14:00and 16:30 h, and four tests were filmed on each of four test days.

Twenty-four hours before testing (at 16 wee ks of age), four (same-strain, same-sex )groups of seven birds were removed from pre-selected pens and transferred to the fourtest pens. Immediately prior to testing, the food and water w ere removed from the firsttwo pens and the came ra suspended above the pen. The experimenter then left the room .For the next 30 min (pre-cone session) the birds mo ved freely around the test pens.The experimenter returned after 30 min, placed a red road hazard cone (0.45 m high,0.26 m diameter base) in the centre of each pen, and left the birds for a further 30 min(with-cone session). The experimenter then returned and repeated the procedu re for theother tw o test pens. The video tapes w ere analysed at a later date.


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330 S . Ke e r - K e e r e t n l . /A p p l i e d A n im n l B e h a v i o u r S c i e n c e 4 9 1 9 9 6 ) 3 2 1 -3 3 3

Pre-cone Leghorn

0 Pre-cone broiler

IlO-Cone A Cone Leghorn

0 Cone broiler

loo-

= 90-ES85D 80-._n

Pre-cone session Cone session

Time period (mins)Fig. 2. Experiment 5: the mean distance of broilers and White Leghorns from the centre of the pen duringpre-cone and cone sessions of the pen and cone test. Points represent means of previous five scans. Linesfitted: broiler, pre-cone y = - 0.091 x + 7 1.692, with-cone y = -0.459.x + 85.477; Leghorn, pre-cone y =0.594~ + 63.724, with-cone y = - 0.272 x + 97.35 1. Maximum possible distance from centre, 120 cm; meandistance predicted by chance, 75 cm.

havioural inhibition may have reduced jumping in the broilers. Neither of theseexplanations is convincing, given the lack of difference in avoidance scores. Thirdly,chicks of both strains may have been equally frightened but social reinstatementmotivation may have been greater in the Leghorn s. Lastly, the difference may havereflected early line divergence in locomo tor ability o r motivation.

In the hom e cage approach and novel object tests (Experiments 3 and 4) there was nodetectable strain difference in avoidance. Becau se individual Leghorns and broilers inthese tests were housed alternately, the influence of neighbouring birds, through amechanism such as cultural transmission, on their fear behaviour should be considered.How ever, previously docume nted effects of mixing strains on their behaviour orperformance were found to be slight (Hugh es and Black, 1974b; Savory, 1975 ). Thesetwo experiments used the same individual birds and this may have produc ed a greatersimilarity in result between them than between other experiments which used differentindividuals.


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The two experiments (2 and 5) whe re a strain difference in fear was detected;corridor and pen and cone, were those where th e subjects had one or moreconspecifics present. Strain differences in fear may only becom e apparent in social testsituations and it is conceivable that Leghorn s are more sensitive to the transmission ofalarm from conspecifics.In the pen and cone tests fear of the cone may have motivated avoidance of it orattraction to the walls. T here is evidence in the literature suggesting that the positions ofbirds in a pen is influenced by the pen walls (Newberry and Hall, 1990; Pamm ent et al.,1982 ). This wall seeking behaviour is thought to be shelter or escape seekingbehaviour, motivated by fear.

Sex by strain interactions apparent in Experiments 1 and 5 suggested that maleLegho rns were more fearful than female Legho rns, whe reas male and female broilersbehaved similarly to each other. The effect of gender on fear behaviour of fowl isreviewed in Jones (1987b ) and whe re sex differences are reported results suggested thatmales were more fearful than females.In these experimen ts we cannot discount the effects of age on fear: Brake et al.(1994 ) found an increase in the duration of tonic immobility with age in broiler breederpullets and Candland et al. (1963 ) found th at freezing increased in White L eghorns up tothe age of 20-45 days and then declined.

It could be argued that the shorter flight distance and the greater avoidance of anapproaching human and of the cone shown by Leghorn s reflected a strain difference inthe type of behavioural strategy adop ted upon alarm. In other word s, Leghorn s may notbe more fearful than broilers but they may react to the same stimuli in a different(flighty) way. For examp le, Duncan and Filshie (197 9) expo sed W hite Leghorns andbroilers to frightening stimuli w hilst simultaneously measuring the heart rate of the birdusing a subcutaneous radio telemetry device. They found the behavioural reactions ofthe two strains followe d a predictable trend, with Leghorn s showing extrem e panicbehaviour and broilers a less violent alarm reaction. They also found that the heart rateof the Legho rns reache d a higher maximum than the broilers, but the broilers heart ratetook longer to return to resting levels. Both trends are associated with increased fear.They concluded that some reappraisal of the flighty or docile classification isrequired, since docile birds may be as frightened as flighty birds in physiological terms.

Conversely, the results of Experiments 2 and 5 might represen t a real straindifference in fearfulness, rather than just a difference in behavioural strategy. Thus, thefindings present us with a contradiction; in two experiments a clear difference in fearresponse was demonstrable between the two strains, wh ereas in the other three nodifference could be shown.

It is possible that the experiments whe re no strain difference was detected inducedparticularly high (1) or low (3 and 4) levels of fear and those whe re a difference wasdetected (2 and 5), may have induced mod erate levels of fear. This proposition could betested by presenting birds with different stimulus intensities within a given experiment.Murphy and Wood-Gush (1978) suggested that certain procedures produce too high alevel of fear to reveal strain differences and Jones and Faure (1982 ) found that increasednovelty of the test environment abolished sex differences in chicks open field be-haviour.


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The problems inherent in measuring fear have been addressed by Jones (1987b) andJones (1987~) and although methodologies have been developed which detect feardifferences in birds of the same strain, they may be less useful, or may requireadaptation, when comparing fear between very different strains of birds.

AcknowledgementsThis work was supported by Ministry of Agriculture, Fisheries and Food. W e thank

Dave Waddington for statistical advice. Broiler ch icks were kindly don ated by Ros sBreeders Ltd., Newbridge, UK.

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