DEPARTMENT for ENVIRONMENT, FOOD and RURAL AFFAIRS
Research and Development
CSG 15
Final Project Report
(Not to be used for LINK projects)
Two hard copies of this form should be returned to:
Research Policy and International Division, Final Reports Unit
DEFRA, Area 301
Cromwell House, Dean Stanley Street, London, SW1P 3JH.
An electronic version should be e-mailed to [email protected]
Project title
Stocking density and welfare in broilers
DEFRA project code
AW0219
Contractor organisation
and location
Department of Zoology
University of Oxford
South Parks Road
Oxford
OX1 3PS
Total DEFRA project costs
Project start date
£ 249,435
01/04/00
Project end date
31/03/03
Executive summary (maximum 2 sides A4)
Background
While there is major public concern over the welfare of broiler chickens, particularly at high stocking densities,
up until now there has been no unequivocal and universally accepted evidence that reducing stocking density
would significantly increase bird welfare. This study examined the effect of experimentally manipulating
stocking density on broiler welfare, including health, hormonal and behavioural measures at five different
maximum stocking densities: 30,34,38,42 and 46 kg/m2. The study was carried out entirely on commercial
farms, with the full cooperation of the broiler industry. It covers a wide range of broiler housing, from small
older houses to large modern ones and involved whole-house experimental manipulation of stocking density.
Objectives
1. To document the effect of stocking density on the behaviour, physical health and productivity of broilers
within the range 30-46 kg/m2 by experimental manipulation of stocking density on commercial farms
2. To document the effect of season (temperature) on stocking density by conducting the same
experimental manipulation of stocking density in summer and again in winter.
3. To identify commercially relevant factors that modify the effect of stocking density by conducting the
same experimental manipulation on farms belonging to thirteen different commercial broiler companies
at present using a wide range of management and husbandry systems.
CSG 15 (Rev. 6/02)
1
Project
title
Stocking density and welfare in broilers
DEFRA
project code
AW0219
Methods
A total of 114 chicken houses on 20 farms involving 2.7 million chickens were studied between August 2000
and November 2002. Two trials were conducted in Northern Ireland, one in Denmark, eight in England and
one in Scotland. A wide range of housing systems (different ages and sizes of house) were included in the
study.
Stocking density was manipulated by altering the number of day old chicks placed in each house, with
maximum final stocking density predicted from average company growth rates and mortality against a
company-specific required bird weight at a particular age (normally 37/38 days). The ‘target’ stocking density
was the maximum stocking density that would be experienced by the birds during their lives. This was either
just before clearance or, where thinning occurred, just before thinning. Each company was asked to set aside
two whole houses for each of five stocking densities but otherwise not to change its normal practice. A large
number of management and husbandry variables as well as environmental correlates were then measured.
Bird welfare was assessed through a variety of measures including mortality, downgrades, gait, leg health,
faecal corticosterone levels and behaviour.
Results and conclusions
1. Experimental manipulation of stocking density of broiler chickens between 30kg/m2 and 46 kg/m2
resulted in a depression of growth rate, an increase in the incidence of birds jostling each other and, at
the two highest stocking densities, a decrease in birds with the best gaits. Some other behaviours such
as lying stretched out and wing stretching were also affected by stocking density.
2. The effects of stocking density were, however, overshadowed by much larger differences between
companies, suggesting that husbandry and management factors are, within limits, more important than
stocking density per se.
3. There were differences between birds reared in summer and those reared in winter. In winter, there
were higher levels of mortality and birds showed higher levels of faecal corticosterone and a higher
incidence of pad dermatitis and dirty pads.
4. Husbandry and management factors that appear to be important include those that affect the litter
moisture levels and temperature and humidity during the birds’ growth. These in turn can be related to
drinker type, number of drinkers/bird and season of the year. ‘Good management’, however, consists of
more than just controlling temperature and humidity since there are many other factors that have
significant effects such as the number of stockmen and the number of visits they make each day.
5. The differences between companies in how well they ‘coped’ with higher stocking densities shows the
importance of carrying out commercial scale trials with more than one company and not relying on
small scale trials that may give misleading results.
6. Legislation to improve broiler welfare should not be directed solely to limiting stocking density as this
will detract attention from other more important factors such as improving the birds’ environment and
their genetics.
7. Reliance on single measures of welfare such as foot pad dermatitis can be misleading and a variety of
different measures are needed to assess welfare, Including physical health and behaviour.
CSG 15 (Rev. 6/02)
2
Stocking density and welfare in broilers
Project
title
DEFRA
project code
AW0219
Scientific report (maximum 20 sides A4)
Introduction
Worldwide, 20 billion meat chickens (broilers) are killed every year1, over 900 million in the UK alone and 2.2
billion in the US, where almost 90% of animals eaten are chickens. Commercial pressures to produce cheap
meat have led to intensification of broiler production, commonly involving large, environment-controlled houses
containing 5,000-50,000 birds and selection for rapid growth so that birds reach a slaughter weight of 2-3 kg at
39-42 days of age. There is widespread concern about the welfare of these birds2-4 , particularly their lack of
space, but only in Sweden and Switzerland is there any specific legislation about how much space each bird
should be given1. In the rest of the world, there are no legal limits on how crowded birds can be and there are
now calls for legislation to limit bird density in the UK and elsewhere1,4. Such legislation would have major
implications for the competitiveness and viability of broiler production in countries adopting it unilaterally. The
key question for policy makers is, therefore, whether giving each chicken more space would genuinely improve
welfare. If welfare benefits are demonstrable, then the case for legislation to regulate space allowances would
be clear even in the face of economic costs. But if the welfare benefits cannot be demonstrated, then imposing
an arbitrary upper limit on stocking density will hinder genuine improvements in bird welfare by deflecting
attention from more effective measures, such as improving environment, management, nutrition or genetics.
Animal welfare includes both physical health and mental well-being5,6 but current evidence is contradictory 1,7-9
and does not answer even the basic question of whether the physical health of broilers is improved by giving
them more space. Inconsistencies arise because many studies are conducted on a small scale and so do not
accurately reflect the conditions of large commercial broiler houses9-11 , are concerned with only a limited
range of conditions in which broilers are kept12, measure only limited aspects of welfare such as foot
condition13 or use correlation rather than experimental manipulation 12,13. We here describe a study that for the
first time supplies policy makers with the standard of evidence necessary for rational decisions about stocking
density and welfare of broiler chickens. The study involved 2.7 million chickens belonging to 10 major broiler
producers in the UK and Denmark, and included both large modern houses and smaller older ones. In an
unprecedented experimental collaboration, each company stocked whole houses of broilers to five different
maximum final stocking densities: 30, 34, 38, 42 and 46 kgm2, with at least two houses at each stocking
density, a total of 114 houses were included in the study. By recording a range of welfare measures, plus a
large number of environmental and management variables, we provide an evidence base for policy makers
seeking to improve bird welfare.
Objectives
The scientific objectives of this project were:
1) To document the effect of stocking density on the behaviour, physical health and productivity of broilers
within the range 30-46 kg/m2 by experimental manipulation of stocking density on commercial farms
2) To document the effect of season (temperature) on stocking density by conducting the same
experimental manipulation of stocking density in summer and again in winter.
3) To identify commercially relevant factors that modify the effect of stocking density by conducting the
same experimental manipulation on farms belonging to thirteen different commercial broiler companies
at present using a wide range of management and husbandry systems.
Methods
Companies:
Initially, there were 13 broiler producing companies participating in this project (Objective 3) but by the time the
contract had been signed, one (Marshall’s) had been taken over by Grampian and soon after, Webbs were
taken over by Faccendas and Skovsgaard were taken over by Rose Poultry. Subsequently, Premier Poultry
became part of the 2 Sisters group. This left 9 independent companies (which now represented an even
greater proportion of the industry than before) but both 2 Sisters and Faccendas agreed that we could do trials
on farms that had been part of their original companies as well as those that were part of the company just
taken over, giving us 11 ‘companies’. These were: Dove Valley, Banhams, Padleys, Moy Park, O’Kane’s, Rose
CSG 15 (Rev. 6/02)
3
Project
title
Stocking density and welfare in broilers
DEFRA
project code
AW0219
Poultry (Denmark), Grampian, 2 Sisters (previously Premier), 2 Sisters (previously not Premier), Faccendas
(always Faccendas) and Faccendas (previously Webbs). An outbreak of disease in the Faccenda (previously
Webbs) trial prevented us from carrying out this trial but as by this time the previously Webbs farms had been
fully integrated into the Faccenda management system, there was no substantive difference between a
previously Webbs farm and a farm that had always been part of Faccendas, so that this trial would not have
contributed greatly to the ‘between company’ effects reported below. In addition, we carried out two ‘seasonal
repeat’ trials – that is, we carried out the experimental manipulation of stocking density with the same stocking
densities in the same 10 houses once in winter and once in summer (Objective 2). These seasonal repeat
trials were carried out on a 2 Sisters (previously Premier farm) and a Faccenda (always Faccenda) farm.
Treatments and replication:
Ten major broiler producing companies were each asked to stock whole houses of broilers to five different
target maximum stocking densities: 30, 34, 38, 42, and 46 kg/m2, and two houses at each stocking density.
Seasonal repeats were conducted with two companies. In total, 114 chicken houses on 20 farms involving 2.7
million chickens were studied between August 2000 and November 2002. Two trials were conducted in
Northern Ireland, one in Denmark, eight in England and one in Scotland.
The range in densities covered the Freedom Food recommendation15 of 30 kg/m2, the Farm Animal Welfare
Council recommendation of 34 kg/m2 and current practice in the UK and EU1, which can be as high as
42.5kg/m2. At the insistence of MAFF (now Defra), the higher stocking density of 46kg/m 2 was included in the
study, but as this was beyond normal commercial practice in the UK, companies were given the opportunity for
not including it; three companies declined to include this density on welfare grounds.
Target stocking density, which was the maximum density experienced by the birds either just before clearance
or where thinning occurred, just before thinning, was manipulated by altering the number of day old chicks
placed in each house, predicted from average company growth rates and mortality against a company-specific
required bird weight at a particular age (usually 37/38 days). Houses within a company were randomly
assigned to a given stocking density (one density per house) before the eggs were incubated, to ensure the
right number of chicks for a given size house. With five companies, all 10 houses (and therefore stocking
densities and replicates) were on one farm, with three companies the trial was split between two sites (with
one replicate of each stocking density at each site), and with two companies the houses were split between
three and six farms. On the whole, houses used within a company were similar where as houses between
companies were diverse.
Manipulating stocking density was the only change we asked the companies to make; normal procedures were
conducted in all other respects (e.g. sexing chicks or using as hatched, light schedule, feed etc.), and were
recorded in detail.
Management and husbandry variables:
We recorded: company assessment of performance of house, age of house, ownership (company or contract
grower), size, orientation, fabric, light pattern, light source, dawn dusk dimming, percent wheat in the finishing
ration, feeder type, number of feeders, drinker type, number of drinkers, heater type and number and position
in house, type of ventilation system and control, use of misting systems, floor and litter type, number of
stockmen and number of visits per house, vaccination programme, feed withdrawal and thinning/clearance
programme.
Environmental variables:
To obtain continuous information about the bird’s environment during their lives, we fitted four randomly (see
Appendix 1) positioned Tiny Talk Data loggers in each house at a height of 60cm, recording temperature and
humidity every hour. In addition, when target stocking density had been reached, we recorded levels of
atmospheric ammonia (Gastec pumpset GV-100s), and light at bird height (ISO-Tech digital light meter), and
litter moisture content ({weight difference in sample after drying/sample weight}*100)
CSG 15 (1/00)
4
Stocking density and welfare in broilers
Project
title
DEFRA
project code
AW0219
Animals:
Chicks arrived on farm as day-olds from whatever source the company normally used. We recorded: source,
date, time, position of modules on lorry (front, middle, back), number of trays per house, number of chicks per
tray, type of vehicle (rigid or artic), ventilation (fans, vents, and position on container) and on board
temperature at time of arrival. We counted the numbers of chicks in at least five trays as a check and
estimated the number of birds placed in each house. Information on breed, numbers per breed, sex (as
hatched, male, female), and age of parent flock per house were provided by the company.
Leg Health:
Gait score: A single bird was chosen at random from each of 10 grid points (see Appendix 1) in each house.
The bird was chosen by viewing the grid through a clear acetate sheet with a pre-chosen point. By
approaching the bird slowly and in a circular path, the bird was observed to walk unhindered by other birds, for
at least 10 paces and the gait recorded as follows:
0
1
2
birds walks with ease, is well balanced and has regular and even strides
bird walks with irregular and uneven strides and appears unbalanced
bird is reluctant to move and unable to walk many strides before sitting down
Ten birds were recorded per house, so that in total 1140 birds were recorded for gait.
Hockburn, pad dermatitis and leg deviation: Lights were dimmed in the house, so that the birds would not
move as researchers moved through the house. Groups of 10 birds were caught in a triangular frame at four
previously chosen random grid points (see Appendix 1) per house for further visual inspection of leg health (40
birds per house). Individuals were lifted and supported under the breast during inspection of the hocks and
pads. They were then inverted (ventral side facing handler) and held by the legs with the handler’s thumbs
just below the inter-tarsal joint, pointing upwards with no rotation. Healthy legs are parallel, with foot pads
facing directly away from the handler and the middle toes pointing straight up. Deviations were scored as
shown in Table 1; the bird was then weighed (Welltech International with sling) and released. In total 4370
birds were weighed and their legs inspected.
Table 1. Scoring system for hockburn, pad dermatitis and leg deviations.
Foot pads**
Angle – in
0
No discoloration or
lesions
No lesions
Legs straight
Angle – out
Legs straight
Hocks*
Rotation
Toes
Legs straight, pads
facing away from
handler
Straight toes
1
<10% hock with
lesion
<5mm lesion on pad
Inward bow at intertarsal joint so that
the two legs meet
>220
Outward twist at
inter-tarsal joint with
300 or more
between the legs
Rotation of the tibia
shaft so that pads
face each other
>150
One or more toes
twisted in the medial
or lateral direction
* Pink hocks in score 0 were also recorded
** Dirty and swollen pads were also recorded
CSG 15 (1/00)
5
2
>10% hock with
lesion
>5mm lesion on pad
Project
title
Stocking density and welfare in broilers
DEFRA
project code
AW0219
Corticosteroid levels and disease status:
The first fresh faecal sample observed in each of five random grids (see Appendix 1) was collected and
uniquely labelled. Swabs were taken and sent to the laboratory for the following tests: Salmonella, E.coli,
Campylobacter, Clostridia and Coccidia. Faecal samples were dried at 400C and sent to the laboratory for
corticosteroid analysis14.15,16.
Behaviour:
Prior to chick placement we installed four cameras and their operating batteries (supplied by Tracksys Ltd
Nottingham, UK) in each house at a height of 155cm according to the randomised grid (see Appendix 1).
Each camera battery had a unique switch code and sent a radio signal to a receiver linked to a VCR and
switch gear positioned in the ante room of the house. Adjacent houses operated at different radio signals to
prevent interference, and the view from cameras at the same location in each house was standardised as
much as possible. The cameras were switched on close to maximum stocking density and video records of
the birds were made between 10.00am and 12 noon. In total 80 minutes of video was recorded per house in
eight 10 minute sequential switches between each camera for two switching cycles. The birds were not
disturbed by the stockman or researchers during the recording period.
For analysis, one focal bird was chosen at random from each camera and each switch cycle (eight birds per
house), via a transparency over the monitor with a predetermined point; the following behaviours were
recorded for five minutes: the frequency and duration of stand, lie, feed, drink, preen, rest (eyes closed), lie
stretched out; the frequency of walk (including the number of strides), run (including the number of strides),
peck litter, peck other bird, scratch litter, scratch head, stretch head, stretch wing, stretch leg, shake body,
shake head, dust bathe, wing flap, aggressive interactions, and perch. We also recorded the number of times
the bird changed posture (up/down), jostled by or through other birds, was disturbed, was facilitated in its
behaviour, and walked-on other birds, or was walked-on by another bird. In total records were obtained from
107 houses and 741 birds.
Production data:
From audited company records: we analysed: mortality (numbers of birds found dead plus the numbers of
birds culled due to illness or leg problems), feed conversion ratio, water intake, date, numbers and weights of
birds removed from the house (thinned or cleared), and information on birds subsequently rejected at the
processing plant.
Bird weight, growth rate and calculated stocking density: Individual bird weight was taken at the time of leg
inspection and growth rate subsequently calculated ({individual weight – average chick weight}/number of
days). Stocking density at the time of bird weighinga (target) and immediately prior to thinning or clearanceb
(maximum) was calculated ({average weight at a or b * number of birds in house at a or b}/area of house). All
measures were later correlated to hock burn, pad dermatitis and leg deviation.
Post-mortem analysis:
On thinning or clearance, we followed the birds to the processing plant and collected 10 birds per house off the
processing line immediately pre-evisceration, at randomly predetermined times. The birds were chilled and
sent to the laboratory for external, abdominal and thoracic examination, as well as for bacteriological and
parasitological analysis (as for the faecal samples previous). Birds were not sent from three companies and in
total 807 birds were analysed.
Standard Protocol:
Our measurements outlined above were taken as close to target stocking density and hence thinning or
clearance, as possible. Since the decision to remove birds from each house was determined by each
company, often with little notice, a judgement of when to take our measures was taken to ensure no loss of
data; this sometimes resulted in our measures being taken a few days prior to clearance/thinning.
CSG 15 (1/00)
6
Project
title
Stocking density and welfare in broilers
DEFRA
project code
AW0219
A strict protocol was followed on farm, to ensure minimum disturbance to the birds and so allow for collection
of base line corticosteroid levels and natural behaviour for example. The protocol was as follows: Sample 1
(between 2pm and 5pm, day 1). Enter house and slowly move to the sample grids collecting gait score,
atmospheric ammonia and light data, and collecting litter and faecal samples. Video records (10am – 12pm
day 2). Enter house and switch on batteries. Allow 15 minutes for birds to settle before commencing
recording. Sample 2 (afternoon day 2). Dim lights and enter house moving to the sample grids. Catch birds
in frame and inspect legs and weigh.
Statistical analysis
Initially variables were analysed for the effects of target density and company by analysis of variance (general
linear model). Where target effects were shown, the effects of actual stocking density was tested by
regression analysis (fitted line model). For the behavioural variables, angular transformation was applied to
proportional data, and the numbers of incidents of behaviour were square root transformed.
Later, univariate linear correlations were examined between outcome variables and predictors that could be
treated as continuous variables. Multivariate linear models were constructed using a stepwise model selection
procedure (starting from a model with no predictors) with possible predictors including those continuous
predictors with substantial linear correlations (<-0.2 or >0.2) as well as categorical predictors.
Results
Management and husbandry:
A wide range of housing was used in the study. On average houses were 19 years old (5-40 years) and
1144m2 (455-1901m2). Resource was divided almost 50:50 between pan and chain feeders, nipple and nipple
with cup drinkers, whilst kerosene powered space heaters were most common (present in 82 percent of all
houses). The environment was mostly controlled automatically (82 percent), and litter was in the form of
woodshavings, straw or a woodshave/straw mix in 49, 33 and 17 percent of houses respectively. Full details
of management data are given in Appendix 2.
Animals:
Chick numbers placed for each target stocking density is given in Table 2 whilst details of the chicks placed
are given in Appendix 3. Most flocks were Ross breed (75 percent) from an average 2.7 parent flocks at 35.3
weeks of age. Audits of numbers into and out of the house (mortality and at processing) were made where
possible. Average potential discrepancies of chicks in to the house were 6 birds (n=56 SE31.2 range -639 to
+634) and out of the house -24 (n=103 SE 30.5 range -1864 to 672).
Table 2. Chicks placed per target stocking density (one density per house)
Target SD
Mean
Minimum
Maximum
30
18,939
7,500
35,922
34
21,491
8,550
42,500
38
24,130
9,600
45,200
42
26,235
10,500
48,300
46
29,615
11,550
53,051
Environmental variables:
Details of mean temperature and humidity and the percent of time these variables were out of range
(according to the Ross broiler manual), as well as the percent variation explained by company, week and other
factors, are given in Appendix 4. Company differences were large and there were some target density effects
on humidity variables.
Average weekly temperature fell from 29.6oC in week 1 to 20.3oC in week 6, and was not affected by target
stocking density. Approximately 85 percent of the variation was explained by week, company, drinker type,
CSG 15 (1/00)
7
Project
title
Stocking density and welfare in broilers
DEFRA
project code
AW0219
season and drinker ratio. The percent time temperature was out of range varied from an average 26.9 to 71.6
across the weeks, and 49.6 percent of the variation was explained by week, company, control, number of
stockmen and season.
Average humidity increased through out the growth cycle from 49.9 to 71.5 percent, and was significantly
affected by target stocking density in weeks 1, 3, and 5. Seventy one percent of the variation was explained
by week, company and drinker ratio. The percent of time humidity was out of range varied from 20.6 to 62
percent across the growth cycle and 29.9 percent of the variation was explained by week and company. The
number of visits made to the house, litter type and age of house helped to explain some of the variation
between companies.
Average moisture (given in Table 3 and detailed in Appendices 5 and 7) was significantly affected by target
density, so that levels were greater in densities of 38 and 42kg/m2 (19.75 percent compared to ~17.7 percent).
Fifty six percent of the variation was explained by company and covariate effects (drinker ratio, position of
heaters, control, and calculated stocking density). Average ammonia levels were not affected by target
density and averaged 10.4 ppm (Table 3).
Table 3 presents average figures for the measures taken (except behaviour) along with the uni-variate
analysis for the effects of target stocking density, company and calculated stocking density. Effects of
stocking density were few (detailed below and further in Appendix 5), whilst effects of company were plentiful
and large. Correlations between variables and details of the explanatory statistics are given in Appendices 6
and 7 respectively.
Leg health:
Gait score:
Across all densities and on average, approximately three quarters of the birds examined were awarded a gait
score zero. Gait zero was significantly affected by target stocking density, actual stocking density and
company, and fell from 81 percent of examined birds in target density 30kg/m2 to 68 and 61 percent in target
densities 42 and 46kg/m2, respectively. It also fell linearly with increasing actual density (slope -1.27,
R2=11.7% p<0.0001). Graphs of gait deviation (scores 1+2) are given by target density and company in
Figures 1 and 2 below. Gaits attaining score 2 which were considered a welfare problem were on average
less than one percent of examined birds, and was not affected by density or company.
Figure 1. Average gait deviation (with 95 percent confidence levels) by target stocking density
Percentage gait deviation
60
Percent incidence
50
40
38.9
30
32.5
26.4
20
23.9
19.2
10
0
30
34
38
Target stocking density
CSG 15 (1/00)
8
42
46
Project
title
Stocking density and welfare in broilers
DEFRA
project code
AW0219
Table 3. The effect of experimental manipulation of stocking density (target), actual achieved density, and
differences between companies, on leg health, faecal corticosteroid, important production parameters, litter
moisture and ammonia levels.
Mean
SE
Range
Company
10-100
Target
density
p=0.027
p<0.0001
Actual
density
p=0.002
Gait 0 %
72.6
2.0
Gait 2 %
0.9
0.3
0-20
ns
ns
ns
Hock 0 %
80.6
1.7
20-100
ns
p<0.0001
ns
Hock 2 %
1.5
0.5
0-47.5
ns
p=0.0003
ns
Pad 0 %
81.2
2.1
12.5-100
ns
p<0.0001
ns
Pad 2 %
2.8
0.7
0-47.5
ns
ns
ns
Angle-in %
12.3
0.7
0-35
ns
p<0.0028
ns
Angle-out %
3.5
0.4
0-17.5
ns
p<0.0001
ns
Rotation %
6.9
0.7
0-47.5
ns
p<0.0001
ns
Crooked toe %
0.6
0.1
0-7.5
ns
p<0.0001
ns
Total leg
deviation %
Corticosterone
ng/ml
Calculated
growth rate
(g/d)
Total mortality
%
Leg cull
%
Other cull
%
Dead birds
%
Downgrades
%
Litter moisture
%
Ammonia
levels
ppm
23.3
1.2
0-62.5
ns
p<0.0001
ns
18.9
1.1
3.5 – 50.4
ns
p<0.0001
ns
49.4
0.4
39.1–57.9
p=0.011
p<0.0001
ns
4.1
0.2
1.4 – 14.7
ns
p<0.0001
ns
0.6
0.1
0 - 2.4
ns
p<0.0001
ns
1.5
0.1
0.4 – 4.7
ns
p<0.0001
ns
2.0
0.1
0.6 – 4.8
ns
p<0.0001
ns
0.9
0.1
0 – 4.24
ns
p<0.0001
ns
18.3
0.4
10.7–32.5
p=0.05
p<0.0001
ns
10.4
0.7
1.3 – 29.8
ns
p<0.0001
ns
CSG 15 (1/00)
9
Project
title
Stocking density and welfare in broilers
DEFRA
project code
AW0219
Figure 2. Average gait deviation by target density and company.
Gait deviation by trial
100
A
percent G1+
90
B
80
C
70
D
60
E
F
50
G
40
H
30
I
20
J
10
K
L
0
30
34
38
42
46
Target stocking density
Gait 0 was negatively correlated to a wide range of variables. Interestingly ‘normal’ gait fell with increasing
light levels, more birds in the house, more visits by the stockman, and the more time temperature was out of
range in weeks 1 and 4. It also decreased as the incidence of rotation, pad dermatitis 2 and jostling increased.
It was positively correlated to hockburn 0 and average temperature in week 1. Fifty two percent of the
variation seen in gait score 0 was explained by company and covariate effects.
Hockburn, pad dermatitis, and leg deviation:
Zero scores for hockburn and pad dermatitis were on average awarded to 81 percent for all birds examined.
There was no effect of target or actual density, but a significant effect of company on both measures. Hocks
and pads attaining score 2 were low and averaged 1.5 and 2.8 percent respectively. Neither were affected by
target density, but company significantly affected hock score 2. On average 25 percent of birds examined had
dirty pads (SE 2.57 range 0-95 percent), and 11.5 percent had swollen pads (SE 1.89 range 0-90 percent).
Almost a quarter of all birds examined had some form of leg deviation. The most common deviation was
angle-in, representing 12 percent of birds examined, rotation was intermediate at 7 percent, whilst angle-out
and twisted toes represented 3.5 and 0.6 percent respectively. There was a significant effect of company but
no effect of stocking density on leg variables.
Corticosteroids and faecal bacteriology and parasitology:
Average faecal corticosteroid levels were 18.9 ng/ml and were not affected by target or actual stocking
density, but were affected by company. There was no effect of density on disease status of the birds. E.coli
and Clostridia were isolated from 13.6 and 10.7 percent of faecal swab samples whilst Salmonella and
Campylobacter were isolated in 2.1 and 1.9 percent of samples respectively; no coccidian were isolated.
Average faecal corticosteroid was negatively correlated to many temperature and relative humidity readings,
and average levels of ammonia and litter moisture. It was strongly positively correlated to mortality levels and
percent time temperature was out of range in week 1. Approximately 84 percent of the variation in faecal
corticosteroid levels was explained by company and covariate effects.
Behaviour:
On average birds spent 72 percent of the observation period lying down and just less than half of that time was
spent resting (eyes closed head down). The proportion of the observation period spent in various activities is
CSG 15 (1/00)
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title
Stocking density and welfare in broilers
DEFRA
project code
AW0219
shown in Figure 3. One fifth of the time was spent feeding, drinking and preening, whilst 45 percent of the
observation period was spent alert; during this time birds were performing small body movements (stretching
head, shaking body etc.), walking, or remaining stationary but watchful. There was no effect of density on the
proportion of time spent in these various activities, the length of the activity bout or the number of behaviour
incidents per minute. Detailed results of the behaviour analysis are given in Appendix 8.
Figure 3. Percentage time observed birds spent feeding, drinking, resting,
lying fully stretched out, and alert.
Bird activity (percent time)
8.6
7.2
Feed
Drink
Rest
45.5
Preen
LSO
Alert
34
0.5 4.2
Apart from jostle and stretch leg, there was no effect of density the incident rate of behaviours. On average
birds changed position 0.54 times per minute, pecked at the litter 0.81 times per minute, and stretched head,
shook head and dust-bathed 0.12, 0.08 and 0.001 times per minute respectively.
The incidence of birds jostling increased from 0.32 per minute at 30 kg/m2 to 0.57 and 0.62 per minute at 42
and 46kg/m2, respectively and is shown in Figure 4. Jostle rate was also significantly affected by actual
stocking density and increased with increasing density (Jostle = -0.3613 + 0.0232 density, R2=19.2% F=22.2
p<0.0001). In addition to jostling, birds were also disturbed in their behaviour at an average rate of 0.16 per
minute, which was not affected by density.
Jostle rate was negatively correlated to gait score 0 and leg cull percentage, and positively correlated to pink
hocks (or worse), rotation and angle-out leg deviations, total numbers of birds in the house, various
temperature and humidity readings and litter moisture. In total 35.2 percent of the variation in jostle rate was
explained by company and co-variate effects.
On average birds performed a walking bout 0.43 times per minute which was not affected by target density.
The number of strides taken per walking bout was affected by target density, however, and fell from an
average 5 strides at 30 and 34kg/m2 to 3.6 strides at 46kg/m2. The rate of leg stretching decreased from 0.056
incidents per minute at 30kg/m2 to 0.028 at 42kg/m2. The following incidents of behaviours were also affected
by density in the mixed general linear models: drink (target density p=0.034), lie stretched out (maximum
density at thinning p=0.03), shake head (actual density p=0.007), and stretch wing (actual density p=0.038).
CSG 15 (1/00)
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Project
title
Stocking density and welfare in broilers
DEFRA
project code
AW0219
Figure 4. Average jostle rate of focal birds by target stocking density
(with 95 percent confidence bars)
Jostle rate
0.9
0.8
Incidenst/minute
0.7
0.6
0.618
0.5
0.5655
0.4
0.4553
0.4314
0.3
0.2
0.3163
0.1
0
1
2
3
4
5
Target stocking density
Production data:
Growth rate:
Growth rate was significantly affected by target stocking density, so that birds grew faster at densities of 30
kg/m2 than at 46kg/m2(50.3g/d over the whole growth cycle compared to 47.7g/d, respectively). Growth rates
by target density and company are given in Figures 5 and 6 respectively. On average birds were 1.784kg (SE
0.014 range 1.49-2.27) at 35 days (range 32-40) when weighed prior to thinning or clearance.
Growth rate was negatively correlated with humidity in week 1, dirty pads and litter moisture, and positively
correlated with flock age, hock and pad scores zero, and the number of visits made per day by the stockman.
In total 65.8 percent of the variation see in growth rate was observed by company and co-variate effects.
Figure 5. The effect of target stocking density on average growth rate over the crop cycle (with 95
percent confidence bars).
Average growth rate
53
52
51
g/d
50
49
50.26
49.9
49.7
48.9
48
47.8
47
46
45
30
34
38
Taregt stocking density
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42
46
Project
title
Stocking density and welfare in broilers
DEFRA
project code
AW0219
Figure 6. Average growth rate over the crop cycle by company and target stocking density.
Average growth rate
60
55
g/d
50
45
40
35
30
30
34
38
42
46
Taregt stocking density
Stocking density:
Stocking density was calculated at the time of bird weighing and immediately prior to the first birds leaving the
house for processing, and is shown in Table 4 below. Both were highly correlated to target density (0.77 and
0.81 p<0.0001, respectively).
Table 4. Actual and maximum densities in kg/m2 (calculated at weighing/leg health inspection and
immediately prior to birds leaving the house, respectively) by target density.
30
28.42
(0.54)
34
32.32
(0.52)
38
35.39
(0.83)
42
38.47
(0.75)
46
40.40
(1.4)
24.6 – 32.4
32.2
(0.97)
26.5 – 35.9
35.69
(0.81)
22.2 – 39.8
37.65
(0.57)
32.0 – 43.4
41.75
(0.48)
24.6 – 46.7
44.83
(0.58)
Range
26.4 – 42.3
(standard error)
31.5 – 49.8
32.3 – 43.6
37.5 – 45.5
39.7 – 49.1
Actual
density (at
weigh)
Range
Maximum
density
Mortality:
Total mortality across all densities averaged 4.1 percent (range 1.4 to 14.7 percent) and was not affected by
target density, shown in Figure 7, or actual density; mortality was affected by company and is shown in Figure
8. For some companies mortality was highest at the higher densities, whereas with others the highest
mortality occurred at the lower densities or was not affected by density.
Causes of mortality were mostly due to birds found dead (average 2 percent of all birds) or culled for reasons
other than leg problems (average 1.5 percent of all birds); overall leg culls were small and represented on
average 0.6 percent of all birds.
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title
Stocking density and welfare in broilers
DEFRA
project code
AW0219
Figure 7. Average bird mortality by target stocking density
Average total mortality
7
6
Percent
5
4
3
4.16
3.69
30
34
4.45
4.78
42
46
3.79
2
1
0
38
Target stocking density
Figure 8. Bird mortality by company and target density
Total mortality
Percent
10
9
A
8
B
7
C
D
6
E
5
F
4
G
3
H
2
I
1
J
K
0
30
34
38
42
46
L
Target stocking density
Mortality was negatively correlated with ammonia levels, actual stocking density, age of house, and pink hocks
or worse percent. It was positively correlated to relative humidity deviation in weeks 3, 4 and 5, and
temperature deviation in week 5, as well as number of birds placed, corticosterone levels, and the number of
stockmen on the unit. Forty four percent of the variation in mortality was explained by company and co-variate
effects.
Downgrades at processing plant:
Less than 1 percent of birds (range 0-4.2 percent; 17.5K out of 1.89million birds) were downgraded or rejected
at the processing plant. Stocking density did not affect the rate of downgrades, where as company did. The
reject categories recorded differed between companies making comparisons between categories difficult.
However, where categories were recorded 11.2, 14.2, 12.6, and 13.6 percent of rejects were due to ascities,
E.coli, Septicaemia, and skin lesions respectively, where as 3, 0.8, and 1.2 percent were attributed to
Staphylococci infection, emaciation, and abnormal colouring, respectively. ‘Others’ accounted for 43 percent
of rejects.
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title
Stocking density and welfare in broilers
DEFRA
project code
AW0219
Post-mortem analysis:
There was no effect of stocking density on the post mortem findings of the birds sent to the laboratory. Twenty
three percent of the birds had hock burn, whilst the incidence of breast blisters, abdominal cavity (what) and
thoracic cavity (what) were low at 1.5, 0.7 and 0.1 percent, respectively.
There was no effect of density on disease status of the birds. E.coli was most prevalent and was isolated from
29 percent of post mortem birds. Campylobacter, Clostridia, and Salmonella were isolated from 7.6, 8.2 and
0.6 percent of birds. A single egg of coccidian was isolated.
Seasonal effects:
Detailed results for the seasonal trials with two companies are given in Appendix 9. There was a significant
effect of season on pad dermatitis score 0, dirty pads, rotation, total leg deviation, faecal corticosterone levels,
leg culls, dead birds and total mortality.
Fewer birds attained pad score 0 in winter than summer (71.6 compared to 88.9 percent respectively) and
more birds (30.3 percent compared to 8.8 percent) had dirty pads in winter.
Fewer birds had rotational leg deviation in winter than summer (3.3 versus 5.8 percent respectively) and
overall leg deviation was lower in winter (14.9 compared to 19.6 percent). Leg cull was higher in winter than
summer (1.3 versus 0.9 percent) and birds found dead were also higher in winter (2.2 compared to 1.7
percent); total mortality was therefore higher in winter (5.3 versus 4.2 percent).
Corticosterone levels were higher in winter (36.2ng/ml) than in summer (8.6ng/ml).
Mortality data from 2002 relating to the farms and houses used in the stocking density trial was analysed for a
further two companies, to increase the numbers of seasonal comparisons outside the main database, and is
given in detail in Appendix 10.
First company: Mortality was significantly affected by farm (F=8.01 p=0.006) and crop (F=8.98 p<0.0001).
Least mortality occurred in crops placed in March, May, August and October (average range 2.77-3.89
percent); most mortality occurred in crops placed in December, February, and June.
Second company: Total mortality was significantly affected by crop (F=12.7 p<0.001) and parent flock age
(F=22.6 p<0.001); cull mortality was also affected by crop (F= 19.8 p<0.001) and parent flock age (F=8.3
p<0.001), and birds found dead was significantly affected by crop (F=20.7 p<0.001). There was no effect of
house, sex or breed on mortality.
Least mortality occurred in the crop placed in July (3.26 percent) and most occurred in the crop placed in May
(6.1 percent). Mortality decreased with increasing parent flock age (F=6.6, R2 = 10.1 p<0.05).
Discussion
Objective 1: To document the effect of stocking density on the behaviour, physical health and productivity of
broilers within the range 30-46 kg/m2 by experimental manipulation of stocking density on commercial farms.
The most striking overall result of this study was that, while there were detectable effects of experimentally
manipulating the stocking density of meat chickens on a number of the variables we measured, these were
overshadowed by the much larger and more consistent differences between companies. Growth rate and the
number of birds with the best gaits were related to target stocking density (Table 3) as were some behaviours
such as jostling and leg stretching (Appendix 8). However, on almost all measures, the way in which the birds
responded to the different stocking densities was modified by which company a trial was carried out with.
Some companies appeared to ‘cope’ with high stocking densities much better than others, as judged by
welfare indicators such as mortality, leg health and downgrades.
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Project
title
Stocking density and welfare in broilers
DEFRA
project code
AW0219
This result has two important implications. Firstly, it shows that studying the effects of stocking density on
broiler chickens can be very misleading if the study covers only a limited set of environmental conditions.
Small scale, laboratory manipulations of stocking density provide useful baseline information but it is
impossible to reproduce the relevant conditions of a commercial farm under non-commercial conditions so that
any conclusions that can be drawn from them are strictly limited. Even commercial trials carried out with just
one company could be misleading since they would not necessarily represent conditions in the rest of the
industry. For example, our results show (Figure 8) that by picking out different company’s results, it would be
possible to conclude that mortality increased with stocking density, that mortality decreased with stocking
density or that mortality was unaffected by stocking density. This dependence of the effects of stocking density
on the precise conditions in which it is studied probably accounts for the diversity of previous findings and their
lack of consensus on the welfare implications of stocking density for meat chickens1,7-9.We hope that this study
will set new standards for the use of scientific information as the basis of legislation that affects a whole
industry by involving the industry itself and studying the range of conditions found commercially.
Secondly, this result shows that bird welfare is greatly affected by factors other than stocking density and so
concentration by legislators on stocking density could mean that other more effective ways of improving bird
welfare – such as improving the environment or the genetics – are overlooked. Changes in stocking density
are relatively easy to legislate: from a legislators point of view, one number rather than another is inserted into
a sentence and a producer conforms by falling below rather than above this figure. Our results show that such
a simplistic view of stocking density is not in the best interests of bird welfare. Factors other than stocking
density have, within limits, more effect on bird health welfare and should form part of any future legislation. Our
study has, as discussed below, gone some way to identifying what those factors are, but what makes for ‘good
management’ is, as we point out, inconveniently complex.
We must not, however, conclude that stocking density is unimportant. At the two highest stocking densities (42
kg/m2 and 46 kg/m2), there were fewer birds with the very best gaits and, as culling rates were not sufficiently
greater, this suggests that leg health was compromised above 42 kg/m2. It is noticeable that some behaviours
such as jostling and leg stretching were significantly affected by stocking density and we are in process of
examining these effects and their relationship to bird health in more detail by further analysis of the
videotapes. We are developing the use of these non-invasive ‘behavioural indicators’ of welfare for use in
commercial situations, but as this was not an objective of this project, a detailed report is not included here.
Furthermore, the multivariate analysis (discussed under Objective 3) showed that there were significant
correlations between actual stocking density and a number of other measures such as drinking, head shaking
and wing stretching.
In this study, we used a variety of different measures of bird welfare. Some of these were obvious and
universally accepted measures such as mortality, some were indirect (downgrades) and others behavioural
(gait score, ethograms). We also used a new method of assessing corticosteroid levels from freshly collected
faeces and, in conjunction with Ross (now Aviagen) developed a measure of leg health that involved several
different features of the state of the feet and legs. It is clear from the results that different measures are
affected both by stocking density and by company in different ways – in other words, the different measures do
not always correlate with each other. This reinforces the now well established view that there is no single
measure of welfare5,6. Animal welfare is multi-faceted and assessing bird welfare on single variables such as
foot pad dermatitis, as has been proposed13 could be misleading.
Objective 2 To document the effect of season (temperature) on stocking density by conducting the same
experimental manipulation of stocking density in summer and again in winter.
There were some significant differences between trials conducted at different seasons. Total mortality and
faecal corticosterone were higher in winter than in summer (Appendix 9). Pad dermatitis and dirty were also
higher in winter. Leg deviations were higher in summer but this was possibly due to the fact that there were
more leg culls in winter. The temperature and humidity inside the houses is clearly of crucial importance
(Appendix 4) and environmental control is a widely recognized by the industry as very important. It is striking,
however, that producers monitor temperature but not humidity within the houses.
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title
Stocking density and welfare in broilers
DEFRA
project code
AW0219
Objective 3. To identify commercially relevant factors that modify the effect of stocking density by conducting
the same experimental manipulation on farms belonging to thirteen different broiler producers at present using
a wide range of management and husbandry systems
The large and highly significant differences between companies we detected on almost all our measures show
that the effects of stocking density can be greatly modified by the birds’ environment. Some features of
housing, management or husbandry or a combination of all three clearly has a major effect on bird welfare.
The very large numbers of measurements we took of how companies operated and the effects of what they
did (for example how good their environmental control was) enabled us to ask what it was that correlated best
with the different welfare measures. In view of the need to take different measures of ‘welfare’, we were
particularly concerned to pick out company features that consistently affected several different welfare
measures.
One problem we encountered in analysing this data was that different companies tended each to have their
own ‘package’ of management and husbandry practices – a particular lighting regime, temperature profile
during development, feed composition etc - and so the different environmental factors tended to vary in
clusters, rather than independently. This is an inevitable feature of a correlational as opposed to an
experimental approach. Whereas the stocking density results (Objective 1) are based on experimental
manipulation of just one factor the effect of which can therefore be clearly identified, a correlational approach
(Objective 3) can only point to variables that co-vary and to the possibility that they are causally related. A
second problem was of our own making – the very large number of variables we measured. For example, the
fact that we had data on how humidity varied hourly throughout the birds’ lives as well as litter moisture just
before clearance means that the analysis of how humidity interacts with stocking density could be carried out
in a large number of ways, such as humidity on Day 34, mean humidity in each week of the bird’s life, amount
of time humidity was outside the recommended (Ross) levels, interaction with temperature and so on. This
analysis and its interpretation are still in progress and we believe it will be a very valuable guide to the
important environmental variables in a chick’s life. What we are reporting here are the results that meet
Objective 3 – namely, the factors that modify the effects of stocking density. We therefore concentrate on the
variables that we found to be most affected by stocking density (gait score 0, growth rate and jostle rate) or
season (faecal corticosterone). Because of its importance as both a welfare and production indicator, we also
included mortality. It was clear from this analysis (Appendix 6) that factors relating to the temperature, air
humidity and litter moisture are among most important predictors for these variables. The extent to which
companies are able to control this aspect of their birds’ environment is thus one of the explanations for the
major between-company differences apparent throughout this study. Components of variation in humidity and
temperature include drinker type and the numbers of drinkers/bird (Appendix 4), as well as season of the year.
However, it would be a mistake to conclude that control of temperature and humidity are the only management
factors that can modify the effects of stocking density. For example, the number of stockmen in charge of a
site and the number of visits per day made to each house also recur as predictors of the variables most
affected by manipulation of stocking density.
Summary and Conclusions
1. Experimental manipulation of stocking density of broiler chickens between 30kg/m2 and 46 kg/m2
resulted in a depression of growth rate, an increase in the incidence of birds jostling each other and, at
the two highest stocking densities, a decrease in birds with the best gaits. Some other behaviours such
as lying stretched out and wing stretching were also affected by stocking density.
2. The effects of stocking density were, however, overshadowed by much larger differences between
companies, suggesting that husbandry and management factors are, within limits, more important than
stocking density per se.
3. There were differences between birds reared in summer and those reared in winter. In winter, there
were higher levels of mortality and birds showed higher levels of faecal corticosterone and a higher
incidence of pad dermatitis and dirty pads.
4. Husbandry and management factors that appear to be important include those that affect the litter
moisture levels and temperature and humidity during the birds’ growth. These in turn can be related to
drinker type, number of drinkers/bird and season of the year. ‘Good management’, however, consists of
more than just controlling temperature and humidity since there are many other factors that have
significant effects such as the number of stockmen and the number of visits they make each day.
CSG 15 (1/00)
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Project
title
Stocking density and welfare in broilers
DEFRA
project code
AW0219
5. The differences between companies in how well they ‘coped’ with higher stocking densities shows the
importance of carrying out commercial scale trials with more than one company and not relying on
small scale trials that may give misleading results.
6. Legislation to improve broiler welfare should not be directed solely to limiting stocking density as this
will detract attention from other more important factors such as improving the birds’ environment and
their genetics.
7. Reliance on single measures of welfare such as foot pad dermatitis can be misleading and a variety of
different measures are needed to assess welfare, including physical health and behaviour.
Knowledge transfer
We intend to publish the results in high quality scientific journals, in the popular farming press (e.g. Poultry
World) and for a more general audience (e.g. New Scientist).
The following papers are planned:
1. The main findings will be submitted shortly to Nature or another rapid publication journal.
2. At least two papers are planned on the behaviour of the birds, one to Animal Behaviour, the other to
Applied Animal Behaviour Science.
3. A paper on the role of environmental factors, particularly temperature and humidity, will follow further
analysis of the data set.
References
1. European Commission (2000) The welfare of chickens kept for meat production (broilers). Report of the
Scientific Committee on Animal Health and Animal Welfare.
2. Webster J. (1994) Animal Welfare: A cool eye towards Eden. Blackwell Scientific, Oxford.
3. Farm Animal Welfare Council (1992) Report on the Welfare of Broiler Chickens. FAWC, Tolworth,
Surrey.
4. Stevenson, P. (1995) The Welfare of Broiler Chickens. Compassion in World Farming. Petersfield,
Hants.
5. Broom, D.M. (1986) Indicators of poor welfare. British Veterinary Journal 142: 5246. Dawkins, M.S. (2001) How can we recognize and assess good welfare? In: Coping with Challenge:
Welfare in Animals including Humans ed. D.M. Broom. Dahlem University Press, Berlin. Pp 63-78.
7. Hall, A. (2001) The effect of stocking density on the welfare and behaviour of broiler chickens reared
commercially. Animal Welfare 10: 23-40.
8. Grashorn, & Kutritz (1991) Effect of stocking density on performance of modern broiler breeds. Arch
Geflugelk 55: 84-90.
9. McLean, J.A., Savory, C.J. & Sparks, N.H.C. (2002) Welfare of male and female broiler chickens in
relation to stocking density, as indicated by performance, health and behaviour. Animal Welfare 11:
55-73.
10. Sørensen, P., Su, G. & Kestin, S.C. (2000) Effects of age and stocking density on leg weakness in
broiler chickens. Poultry Science 79: 864-870.
11. Feddes, J.J.R., Emmanuel, E.J. & Ziudhoff, M.J. (2002) Broiler performance, body weight variance,
feed and water intake and carcass quality at different stocking densities. Poultry Science 81: 774-9
(small pens).
12. Heier, B.T., Hogasen, H.R. and Jarp, J. (2002) Factors associated with cumulative mortality in
Norwegian broiler flocks. Preventive Veterinary Medicine 53: 147-165.
13. Martrenchar, A., Boilletot, E., Huoinnic, D. & Pol, F. (2002) Risk factors for foot-pad dermatitis in
chicken and turkey broilers in France. Preventative Veterinary Medicine 52: 213-226
14. Cockrem, J.F. & Rounce, J.R. (1994) Faecal measurements of oestradial and testosterone allow noninvasive estimation of plasma steroid concentrations in the domestic fowl. Bristish Poultry Science
35: 433-443.
15. Lord, A (2001) D. Phil. Thesis, Oxford.
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16. Denhard, M., Schreer, A., Krone, O., Jewgenow, K., Krause, M. & R. Grossmann (2003) Measurement
of plasma corticosterone and fecal glucocorticoid metabolites in the chicken (Gallus domesticus), the
great cormorant (Phalacrocorax carbo), and the goshawk (Accipiter gentilis). General and Comparative
Endocrinology 131: 345-352.
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