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Effects of specific noise and music stimuli on stress
and fear levels of laying hens of several breeds
J.L. Campo*, M.G. Gil, S.G. Da
´vila
Departamento de Gene
´tica Animal, Instituto Nacional de Investigacio
´n y Tecnologı
´a
Agraria y Alimentaria, Apartado 8.111, 28080 Madrid, Spain
Accepted 12 August 2004
Abstract
The purpose of the present study was to analyze the effects of specific sound stimuli on heterophil
to lymphocyte ratio and tonic immobility duration of laying hens. There were two different
experiments. The first experiment (216 birds) measured heterophil to lymphocyte ratio and tonic
immobility duration in 36-week-old hens of four Spanish breeds of chickens (Castellana, Villa-
franquina, Vasca, and Prat) exposed to specific noise stimuli of 65 dB (background chicken
vocalizations and fans, control) or 90 dB (background noises plus truck, train, and aircraft noises)
for 60 min, between 8.00 and 9.00 once. There was significant difference for the heterophil to
lymphocyte ratio between noise treatments (P<0.01), the ratio of hens treated with noise being
higher than that of control hens. Treated hens had significant heterophilia (P<0.01). There was
significant difference for the duration of tonic immobility between treatments (P<0.001), tonic
immobility duration being significantly longer in the group of hens treated with noise. Thus, hens
exposed to 90 dB noise were more stressed and fearful than control hens, as indicated by the
heterophil to lymphocyte ratio and the tonic immobility duration, respectively. Results were
consistent across the breeds. The second experiment (108 birds) measured heterophil to lymphocyte
ratio and tonic immobility duration in 36-week-old hens of two different Spanish breeds of chickens
(Leonesa and Andaluza) exposed to background noises (65 dB) or to specific classical music stimulus
plus background noises (75 dB) between 9.00 and 14.00 for three days. There was no significant
effect of music treatment on the heterophil to lymphocyte ratio, its numerator or its denominator,
whereas there was significant effect for the tonic immobility duration (P<0.001), tonic immobility
of hens treated with music being longer than that of control hens. Thus, hens exposed to specific
music stimulus were more fearful than control hens. The results of the present study indicate that
www.elsevier.com/locate/applanim
Applied Animal Behaviour Science 91 (2005) 75–84
* Corresponding author. Tel.: +34 91 3476743; fax: +34 91 3572293.
E-mail address: jlcampo@inia.es (J.L. Campo).
0168-1591/$ – see front matter #2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.applanim.2004.08.028
specific noise stimulus (90 dB versus 65 dB) causes stress and fear in laying hens and specific
classical music stimulus (75 dB versus 65 dB) has a negative influence on their fearfulness.
#2004 Elsevier B.V. All rights reserved.
Keywords: Noise; Music; Stress; Fear; Laying hens
1. Introduction
Noise is a potential stressor to animals and has an important psychologic component, so
it is a potential source of fear for animals. Algers et al. (1978) reported the significant
negative impact of continuous noise on animal health. It has been shown that noise is a
stressor in pigs (Bond et al., 1963; Forsling et al., 1984; Stephens et al., 1985; Talling et al.,
1996; Talling et al., 1998), cattle (Forsling et al., 1984; Elridge, 1988; Francesco et al.,
1990; Arave et al., 1991; Grandin, 1996; Waynert et al., 1999), and people (Molino, 1979;
Melamed and Bruhis, 1996).
Noise as a stressor in fowls has been little investigated, although it seems that can
adversely affect the productive performance and behavior of the birds. Stadelman (1958a)
found that sound intensities of 96 dB had no effect on hatchability or quality of chicks
produced, although he reported that sound intensities of 115 dB were effective in
interrupting brooding of hens. Stadelman (1958b) found no effect on growth when young
chickens were exposed to noises of 80–118 dB, even though he reported violent behavioral
response (crowding) to intermittent sound exposure at 100–118 dB. Hamm (1967) showed
that a single short stress due to aircraft noise did not affect poultry egg production, but
longer periods of stress (three or more days) reduced egg production. He attributed the loss
to a change in behavior (hens kept away from feed and water due to noise stress), not to a
physiological change. McFarlane et al. (1989a) found that noise did not influence weight
gain, feed intake, or behavioral traits in broiler chicks. Lynch and Speake (1978) concluded
that sonic booms did not initiate abnormal behavior that would result in decreased
productivity in wild turkeys. Book and Bradley (1990) found panic and aggression in
turkeys were higher in the noise group of animals. Two hours exposure to auditory
stimulation (80 dB) during the last three days of incubation accelerated the hatching of
Japanese quail (Woolf et al., 1976).
The relationship between noise and indicators of stress in fowls has been less studied,
and there are no previous studies on the relationship between noise and indicators of fear.
McFarlane and Curtis (1989) found that continuous noise for seven days (80 or 95 dB) did
not have significant effect on the heterophil to lymphocyte ratio or the plasma
corticosterone concentration of broiler chicks. A slow increase in baseline steroid level
was observed in white leghorns exposed to noise (Borg, 1981). McFarlane et al. (1989b)
reported that monocyte percentage and duodenal lesion severity caused by coccidiosis
was increased by continuous noise at 80 or 95 dB. Gross (1990) found that when chickens
were subjected to a sound of 104 dB for 30 s, heterophil to lymphocyte ratios begin to rise
18 h later, reaching their maximum value in 20 h and returning to pre-stress values after
30 h. The pre-stress sound level was 70 dB, and it was caused by fans and chicken
vocalizations.
J.L. Campo et al. / Applied Animal Behaviour Science 91 (2005) 75–8476
On the other hand, the positive physiological and psychological effects of music on
humans are well known (Standley, 1986; Snyder and Chan, 1999). Its effect on animals,
however, has not been well studied, although music can be played as environmental
enrichment for farm animals or to mask disruptive noises. Reports that music calms the
animals and improves productivity appear in commercial journals (for example
Anonymous, 1994). Previous results looking at the effects of this practice on animal
productivity and behavior have been contradictory. Uetake et al. (1997) showed a
stimulatory effect of music (background noise + music: 70 dB versus background noise:
60 dB) on the voluntary approach of dairy cows to an automatic milking system. On the
contrary, Cloutier et al. (2000) suggested that playing music (between 70 and 80 dB)
provides no improvement in conditions for piglets during handling and weaning; indeed,
music tended to increase distress after weaning.
Christensen and Knight (1975) exposed meat type chicks to two different levels (70 and
85 dB) and kinds (rock and roll and dinner) of continuous (12 h each day) music but did not
find any significant results on feed consumption. McAdie et al. (1993) studied four
different sounds (music, water-hose, poultry, and train) at a range of 90–100 dB, music
being the least aversive for domestic hens; however, they reported that hens chosen to
spend more time in a noise-reduced environment, when given the option. The relationship
between music and indicators of stress or fear in fowls has been little studied. Gvaryahu et
al. (1989) studied the combined effects of music, environmental enrichment, and filial
imprinting. Low-level classical music (Vivaldi’s Four Seasons) was used intermittently
(1 h on/1 h off). Control chicks were exposed to an ambient noise level of 65 dB (fans and
chick noises), whereas chicks in the experimental groups were exposed to a maximum of
75 dB (background noises plus music). They reported that treated chicks were less fearful
(less tonic immobility duration) and fed and weighted significantly more than controls.
Ladd et al. (1992) reported that regular exposure to music (country or classical/jazz during
8 h) reduces heterophil to lymphocyte ratio and grooming (in excess indicates stress),
whereas it stimulate feeding and head shaking in laying hens.
The purposes of the present study were to define the effect of specific noise and music
stimuli, from a human point of view, on heterophil to lymphocyte ratio, the best indicator of
stress in poultry (Gross and Siegel, 1983), and on tonic immobility duration,a frequently used
measurement of fear reaction (Gallup, 1979), in laying hens of different breeds. It would be
hypothesized that noise would increase the stress and fear levels of birds, whereas music
would decrease both these levels. The current study relative to the existing literature analyze
for the first time the relationship between noise and fear, and complement the scarce previous
experiments with meat animals to analyze the relationship between noise and stress (two
experiments), music and fear (one experiment), or music and stress (one experiment). It is
necessary to indicate that type and duration of exposition to sound stimuli as well as the
genetic make up of the birds are important when making comparisons across studies.
2. Materials and methods
In both experiments, hens from each breed were housed at 20 weeks of age in different
pens with a raised slatted floor covering a droppings pit and straw litter on the rest of the
J.L. Campo et al. / Applied Animal Behaviour Science 91 (2005) 75–84 77
floor; the slatted area occupied one third of the floor. Bird density was four hens/m
2
. Hens
were fed standard layer diet, containing 16% CP, 2700 kcal ME/kg, 3.5% Ca, and 0.5%
available P. Feed and water were supplied for ad libitum consumption. The lighting regimen
was 14 h light: 10 h darkness (light from 7.00 to 21.00) and room temperature was 16–
20 8C. Feeders, drinkers, and nest boxes were in the slatted floor area. To broadcast the
sounds, a Denon stereo component system H-1 with two speakers was put at housing in each
experiment. They were hanged above the hens at housing. Results for response to sound
stimuli are probably not confounded with response to a novel visual object (speakers)
because habituation is probably occurred from housing to age of testing (36 weeks).
The first experiment measured heterophil to lymphocyte ratio and duration of tonic
immobility in four different Spanish breeds of chickens (Black Castellana, Red
Villafranquina, Barred Red Vasca, and Buff Prat) exposed to two different noise levels
(90 and 65 dB). The breeds were selected according to their different genetic background.
Castellana is a white-shelled egg layer, whereas Prat is a tinted shell egg layer; Vasca and
Villafranquina lay brown- and dark brown-shelled eggs, respectively. Castellana and Prat
are light breeds, and Vasca and Villafranquina are heavy breeds. All these breeds are
maintained at the experimental station of El Encı
´n (Madrid, Spain) in a conservation
program of genetic resources started in 1975 (Campo and Orozco, 1982) and have been
described by Campo (1998). Data were collected from different replicate groups in
different rooms. There were six rooms in the experiment (two per replicate: one for the
noise treatment and one for the control) and 24 pens (four per room). Three replicates
(hatches) separated seven days were used. The treated group consisted of 108 hens (27 hens
of each breed, in three replicates of nine hens) exposed to the specific sound stimulus of a
tape with a mix of three different noises (truck, train, and aircraft) for 60 min (between 8.00
and 9.00 once), in addition to the background noises, in a total noise level of 90 dB
maximum (ranging from 85 to 90 dB; treated group). The age of the birds when exposed to
the noise stimulus was 1 day before testing at 36 weeks. The control group consisted of 108
additional hens (27 hens of each breed, in three replicates of nine hens) housed in a noise
level of 65 dB maximum (ranging from 60 to 65 dB). In this group, the main sources of
noise were animal voices and fans (in this order). Decibel levels in the rooms were
determined with a Cesva type 2 integrating averaging sound level meter (Dicesva Acoustic
Instruments Ltd., Barcelona, Spain).
The second experiment measured heterophil to lymphocyte ratio and duration of tonic
immobility in two different Spanish breeds of chickens (Birchen Leonesa, and Black–red
Andaluza) exposed to two different sound treatments (music and control). Andaluza is a
white-shelled egg layer, whereas Leonesa is a tinted shell egg layer. Data were collected
from different replicate groups in different rooms. There were six rooms in the experiment
(two per replicate: one for the music treatment and one for the control) and 12 pens (two per
room). Three replicates (hatches) separated seven days were used. The treated group
consisted of 54 hens (27 hens of each breed, in three replicates of nine hens) exposed to the
specific sound stimulus of a 60 min tape with classical music (Mozart’s String Quartettes K
428 and K 458) between 9.00 and 14.00 for three days; the sound level was 75 dB
maximum (ranging from 70 to 75 dB; background noises plus music). The age of the birds
when exposed to the music stimulus was 3 days before testing at 36 weeks. The control
group consisted of 54 additional hens (27 hens of each breed, in three replicates of 9 hens)
J.L. Campo et al. / Applied Animal Behaviour Science 91 (2005) 75–8478
housed without music; the sound level was 65 dB maximum (ranging from 60 to 65 dB;
chickens and fans noises) in this group.
On two different days, birds were tested for heterophil to lymphocyte ratio and tonic
immobility duration. The age of the birds used as controls were the same as that of the
experimental birds. They were tested on the same days as the experimental birds. The
heterophil to lymphocyte ratio was tested at 36 weeks for all birds. To obtain the heterophil
to lymphocyte ratio, birds were randomly sampled and carried to a separate room, and
collection of blood was made immediately after the noise or music treatment. Two drops of
blood were taken from a small puncture in the comb of each bird, one drop being smeared
on each of two glass slides. The smears were stained using May–Gru
¨nwald and Giemsa
stains (Lucas and Jamroz, 1961), approximately 2–4 h after preparation with methyl
alcohol fixation. One hundred leukocytes, including granular (heterophils, eosinophils, and
basophils) and non-granular (lymphocytes and monocytes), were counted on one slide of
each bird, and the heterophil to lymphocyte ratio was calculated.
All birds were tested for tonic immobility in a separate room on the day following the
test for blood sampling. Tonic immobility was induced, as soon as a bird was randomly
sampled and caught, by placing the animal on its back with the head hanging in a U-shaped
wooden cradle (Jones and Faure, 1981). The bird was restrained for 10 s. The observer sat
in full view of the bird, about 1 m away, and fixed his eyes on the bird because of the fear-
inducing properties of eye contact. If the bird remained immobile for 10 s after the
experimenter removed his hands, a stopwatch was started to record latencies until the bird
righted itself. If the bird righted itself in less than 10 s, then it was considered that tonic
immobility had not been induced, and the restraint procedure was repeated (three times
maximum). If the bird did not show a righting response over the 10 min test period, a
maximum score of 600 s was given for righting time.
A three-way analysis of variance (Sokal and Rohlf, 1981) was used according to the
following model: x
ijkl
=m+T
i
+B
j
+TxB
ij
+R
k
+TxR
ik
+BxR
jk
+TxBxR
ijk
+e
ijkl
.In
this model, x
ijkl
is the analyzed measurement (heterophil to lymphocyte ratio, heterophil
number, lymphocyte number, or tonic immobility duration), mthe overall mean, T
i
the
effect of the sound treatment (i=1,..., 2), B
j
the effect of breed (j=1,..., 4, and j=1,...,
2 in experiments 1 and 2, respectively), TxB
ij
the interaction of breed and sound treatment,
R
k
the effect of replicate (k=1,..., 3), and e
ijkl
the residual (l=1,..., 9). Sound treatment
and breed were considered fixed effects and replicates were assumed to be a random effect.
Significant differences among breeds in Experiment 1 were evaluated using the Student–
Newman–Keuls’multiple range test (Snedecor and Cochran, 1980). Square root
(heterophil to lymphocyte ratio) or logarithmic (tonic immobility duration) transforma-
tions were used for analyses of variance, but actual mean values are presented. Individual
birds were not identified and correlation between heterophil to lymphocyte ratio and tonic
immobility duration was not calculated.
3. Results
Replicates (confounded with hatches), replicate by treatment (confounded with rooms),
replicate by breed, or replicate by treatment by breed (confounded with pens) interactions
J.L. Campo et al. / Applied Animal Behaviour Science 91 (2005) 75–84 79
were not significant for either experiment, and they were pooled with the residual to give a
two-way factorial model of treatment and breed effects (x
ijk
=m+T
i
+B
j
+TB
ij
+e
ijk
).
Mean values indicating the effect of specific noise treatment and breed on stress and fear
measurements (Experiment 1) are summarized in Table 1. There was a significant
difference between noise levels for the heterophil to lymphocyte ratio (P<0.01); the ratio
of hens treated with noise was higher than that of control hens. In hens treated with noise,
there was a significant (P<0.01) increase in heterophil number, without a significant
decrease in lymphocytes. Results were consistent across the breeds, as there was no
significant noise treatment by breed interaction for heterophil to lymphocyte ratio,
heterophil number or lymphocyte number. There were significant differences among
breeds in terms of heterophil to lymphocyte ratio (P<0.001), heterophil number
(P<0.001), and lymphocyte number (P<0.05). Ratio and heterophil number were
smaller for the Villafranquina breed than for the other breeds used in this study, whereas
lymphocyte number was significantly greater in that breed.
The tonic immobility duration was significantly longer within the group of hens treated
with noise than within the control group of hens (Table 1;P<0.001). Noise treatment by
breed interaction was not significant, indicating consistent differences between treated and
control hens. There were significant differences among breeds (P<0.05), hens from the
Vasca breed showing longer tonic immobility duration than hens from the other breeds.
The number of inductions required to achieve the tonic immobility reaction was similar in
both groups (1.05 0.02 and 1.11 0.03 in the treated and control groups, respectively),
with 5.55% (treated) and 11.11% (control) of hens requiring two inductions.
Results from Experiment 2 show that there was no significant effect of specific music
treatment on blood heterophil to lymphocyte ratio, and its numerator or denominator
(Table 2). Breed and treatment by breed interaction were not significant for either analyzed
measurement. There was significant difference between sound treatments for the tonic
immobility duration (Table 2;P<0.001). Tonic immobility of hens treated with music
was longer than that of control hens. Neither breed nor treatment by breed effects were
J.L. Campo et al. / Applied Animal Behaviour Science 91 (2005) 75–8480
Table 1
Mean heterophil:lymphocyte ratio, number of heterophils, number of lymphocytes, and tonic immobility
duration(s) with two specific noise levels in hens from four Spanish breeds (n= 216) (Experiment 1)
Effect Heterophil:lymphocyte
ratio
Heterophil
number
Lymphocyte
number
Tonic immobility
duration
Noise level
90 dB 0.47
a
26.80
a
61.19
a
363.81
a
65 dB 0.40
b
23.90
b
63.47
a
165.21
b
S.E.M. 0.02 0.54 0.87 15.19
Breed
Castellana 0.45
a
25.98
a
61.96
b
238.41
b
Villafranquina 0.34
b
21.45
b
65.75
a
235.09
b
Vasca 0.48
a
27.17
a
60.92
b
337.76
a
Prat 0.47
a
26.76
a
60.70
b
246.80
b
S.E.M. 0.03 1.08 1.23 21.49
Means within the same effect and column with no common superscript (a, b) differ (P<0.05).
significant, the changes in tonic immobility duration being similar in both breeds. The
number of inductions was similar in both groups. The mean value was 1.20 0.07 in the
music treated group, with 12.96% of hens requiring two inductions and 3.70% of hens
requiring three inductions; the mean number of inductions was 1.30 0.07 in the control
group with 22.22 and 3.70% of hens requiring two and three inductions, respectively.
4. Discussion
The difference in heterophil to lymphocyte ratio between hens housed with two specific
noise levels (90 dB versus 65 dB) was significant (Experiment 1). Hens exposed to an
ambient noise of 90 dB (between 8.00 and 9.00 once) showed higher ratio than those that
were exposed to an ambient noise level of 65 dB (control group), hens in the noised group
having significant heterophilia, although corresponding lymphopenia was not significant.
Thus, hens exposed to noise were more stressed than control hens. This result confirms the
finding of Gross (1990) that the heterophil to lymphocyte ratio in White Leghorns 6-week-
old is affected by noise level (104 dB for 30 s and 70 dB). Although the timing of the
response was very different in our experiment, it might be possible to get an immediate
heterophil to lymphocyte ratio change in response to a specific noise stimulus of 90 dB for
60 min. It also agrees with the change in several behavioral traits indicated in previous
works: brooding and crowding (Stadelman, 1958a, b), feeding and drinking (Hamm, 1967),
and panic and aggression (Book and Bradley, 1990). However, the result in the current
study disagrees with that of McFarlane and Curtis (1989), who reported that heterophil to
lymphocyte ratio was unaffected by continuous noise for seven days (95 dB versus 80 dB)
in broiler chicks 2-week-old. Similarly, McFarlane et al. (1989a) indicated that behavioral
traits (standing, lying, drinking, and eating) were not influenced by noise, although
McFarlane et al. (1989b) showed that noise affected pathologic traits, suggesting that it
may be detrimental to the bird’s health even though behavioral measures do not show any
obvious adverse effects.
Although, as far as the authors know, the relationship between the noise level and
duration of tonic immobility has not been previously studied, the significant increase for
J.L. Campo et al. / Applied Animal Behaviour Science 91 (2005) 75–84 81
Table 2
Mean heterophil:lymphocyte ratio, number of heterophils, number of lymphocytes, and tonic immobility
duration(s) with two specific sound treatments in hens from two Spanish breeds (n= 108) (Experiment 2)
Effect Heterophil: lymphocyte
ratio
Heterophil
number
Lymphocyte
number
Tonic immobility
duration
Treatment
Music 0.46
a
26.82
a
61.51
a
309.52
a
Control 0.51
a
27.29
a
61.91
a
168.89
b
Breed
Leonesa 0.49
a
27.33
a
60.04
a
246.93
a
Andaluza 0.47
a
26.78
a
63.41
a
231.48
a
S.E.M. 0.04 1.40 1.53 22.67
Means within the same effect and column with no common superscript (a, b) differ (P<0.05).
this trait found in hens treated with noise is consistent with that reported for the heterophil
to lymphocyte ratio, suggesting that treated hens were more fearful than control hens and
that noise can be regarded as aversive. Birds in the noise treatment groups were frightened
by the sound from the tape, most of the birds piling up in the corners far from the cassette
player or laying flat on the floor.
There was no evidence of a change of stress response, as judged by heterophil to
lymphocyte ratio, in hens exposed to a specific music treatment (between 9.00 and 14.00
for three days; Experiment 2), but there was evidence of a significant increased fear
response as judged by tonic immobility duration. Birds in the music treatment group laid in
the corner far from the cassette player. The control group of hens had only 54% of the tonic
immobility duration of the group with music treatment. Thus, hens exposed to music were
more fearful than control hens, suggesting that it negatively affected bird welfare, even
though stress measures did not show any obvious positive or negative effects. Although it is
difficult to come to a general conclusion across experiments from different authors, as
music differs widely with regard to rhythm, instruments, and frequency, it may be
interesting for the comparison with previous experimental results. The findings in the
current study disagree with results reported by other authors, who found an association
between music treatment and less stressfulness or fearfulness. Ladd et al. (1992) reported
that the heterophil to lymphocyte ratio was higher in the control group than in hens, who
listened to a country station during 8 h, although it was similar in the control group and in
hens that listened to a classical/jazz station. Similarly, Gvaryahu et al. (1989) reported that
intermittent music (1 h on/1 h off) at 75 dB (versus 65 dB), in combination with
environmental enrichment and filial imprinting, had a decreasing effect on fearfulness in
broiler chicks 1- or 8-week-old. Tonic immobility duration was less in their study 1 (46 s
versus 180 s) and in Experiment 1 of their study 2 (136 s versus 246 s), although it was
similar in Experiment 2 of their study 2 (51 and 84 s, respectively).
On the contrary, the results agree with the findings by other authors with regard to the no
significant or negative association between music treatment and animal welfare.
Christensen and Knight (1975) did not indicate any significant tranquilizing effect
associated with high (85 dB) or low (70 dB) music levels for 12 h each day. Birds in the
music treatments were frightened initially, although this reaction gradually decreased
through the first week and was not observed after that time. McAdie et al. (1993) reported
that the sound of hens in a commercial poultry house at 100 dB was associated with the
highest stress response, and a piece of music at 90 dB was associated with the lowest stress
response, but hens chosen a noise-reduced environment when given the choice, suggesting
that music, as other sounds, may have negative effects on behavior.
With regard to differences in sound levels between experiments 1 and 2, music level
(75 dB) in Experiment 2 was much lower than that of the noise (90 dB) in Experiment 1.
Although the effects of these two specific noise and music stimuli tested are not
comparable, due to differences in duration of sound and the different breeds of hens that
were used in both experiments, it may be suggested that a small change in the sound level
(10 dB) is enough to produce significant changes in the tonic immobility duration
(experiments 1 and 2), whereas it is necessary an extra change in the sound level
(10 + 15 dB) to produce significant change in the heterophil to lymphocyte ratio
(Experiment 1). In conclusion, with the specific sound stimuli of the current study, a
J.L. Campo et al. / Applied Animal Behaviour Science 91 (2005) 75–8482
significant negative influence of noise (90 dB versus 65 dB) on the stressfulness and
fearfulness of hens was reported, whereas the classical music (75 versus 65 dB) did not
affect the level of stress of hens and had an increasing effect on their fearfulness. In this
way, the belief that exposure to noise causes stress in farm animals seems to be true, but the
claim that music can generally help to alleviate stress does not, with these specific sound
stimuli.
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