Aus dem Institut für Tierzucht und Vererbungsforschung
der Tierärztlichen Hochschule Hannover
Evaluation of small group systems with elevated perches, furnished cages
and an aviary system for laying hens with respect to bone strength, keel
bone status, stress perception and egg quality parameters
INAUGURAL-DISSERTATION
zur Erlangung des Grades einer
DOKTORIN DER VETERINÄRMEDIZIN
(Dr. med. vet.)
durch die Tierärztliche Hochschule Hannover
Vorgelegt von
Britta Scholz aus Arnsberg
Hannover 2007
Scientific supervisor: Univ.-Prof. Dr. Dr. habil. O. Distl
1. Examiner: Univ.-Prof. Dr. Dr. habil. O. Distl
2. Co-examiner: PD Dr. Dr. habil. H. Salisch
Oral examination: 26.11.2007
To my family
Parts of this work have been submitted, are in review or have been accepted for publication in
the following journals:
Archiv für Tierzucht
Archiv für Geflügelkunde
Berliner Münchener Tierärztliche Wochenschrift
Züchtungskunde
Table of contents
Chapter I
Introduction ................................................................................................................................ 1
Chapter II
Evaluation of bone strength, keel bone deformity and egg quality of laying hens housed in
small group housing systems and furnished cages in comparison to an aviary system. ............ 5
Chapter III
Bone strength, keel bone deformities and egg quality of Lohmann Silver layers kept in small
group systems with modified perch positions in direct comparison to an aviary housing
system and furnished cages. ..................................................................................................... 19
Chapter IV
Bone strength and keel bone status of two layer strains kept in furnished small group systems
with different perch configurations and group sizes. ............................................................... 47
Chapter V
Effect of housing system, group size and perch position on H/L-ratio in laying hens. ........... 65
Chapter VI
Keel bone condition in laying hens: a histological evaluation of macroscopically assessed keel
bones......................................................................................................................................... 81
Chapter VII
Meta-analysis of welfare, egg quality, production and selected behavioural traits to evaluate
small group housing systems for laying hens........................................................................... 97
Chapter VIII
Summary ................................................................................................................................ 117
Chapter IX
Erweiterte Zusammenfassung ................................................................................................ 121
Appendix ................................................................................................................................ 131
Acknowledgements
List of abbreviations
AP Aviplus
b linear regression coefficent
BE back perch elevated
BFD bone fragment dislocation
BW body weight
CB cortical bone
CI confidence interval
cm centimetre
comp compartment
et al. et alteri
EU European Union
EV Eurovent
FC furnished cages
FCM fracture callus material
FE front perch elevated
g gram
GR group size
H/L-ratio heterophil/lymphocyte ratio
LB Lohmann Brown
LL layer line
LIN layer line
LS Lohmann Silver
LSL Lohmann Selected Leghorn
LSM least square means
LSMlog logarithmised least square means
LT Lohmann Tradition
max maximum
min minimum
MJ mega Joule
mm millimetre
MON laying month
n number
N Newton
NE non-elevated
NS not significant
p error probability
PE periostal ectostosis
PP perch position
Q1/Q3 25%/75%-quantiles
SAS Statistical Analysis System
SD standard deviation
SE standard error
SG small group system
ST stepped position of perches
SYS housing system
x mean
x~ median
Chapter I
Introduction
Chapter I: Introduction
Introduction Laying hen husbandry has always been a focal point in the discussion on ensuring animal
welfare and protection on the one hand and considering economic aspects, such as
competitive market capability in the laying hen industry on the other hand. Comprising the
period from 1995 to 2004, changes in German laying hen husbandry have clearly occurred
towards housing systems that are more appropriate to hens. Whereas in 1995 a proportion of
93.7 % of hens were kept in conventional cages, followed by floor keeping (4.6 %) and free
range husbandry systems (1.6 %), the percentage of keeping hens in conventional cages was
reduced to 77.4 % in 2004 and floor keeping and free range husbandry nearly equalled out to
11.7 % and 10.9 % respectively (STATISTISCHES BUNDESAMT, 2005). These changes
are primarily due to continuous, legal alterations on laying hen husbandry systems.
Conventional cages, offering hens 550 cm² space per layer and providing poor environmental
conditions due to limited floor space and lack of cage enrichments, have always been heavily
criticised. Inactivity osteoporosis in hens and resulting bone fractures is one of the major
welfare problems attributed to these types of housing systems. Increased criticism of animal
welfare activists and the consumer of egg products on keeping hens in conventional cages has
finally led to the EU Council directive 1999/74/EC, which was passed on July 19th, 1999.
The directive sets out minimum standards for the protection of laying hens within member
countries of the EU and brings about major changes in laying hen husbandry, particularly
from 2012.
In the EU, conventional cages will have to be completely phased out by the end of December
2011 and replaced by furnished cages, small group housing systems or alternative housing
systems. In contrast to conventional cages, furnished cages provide an enlarged floor space
(750 cm²/hen) and are enriched with perches, nest boxes, dust baths and devices to shorten
claws. The provision of cage enrichment, particularly perches, is supposed to enhance layers’
bone strengths by offering increased stimulus to move and jump. Small group housing
systems are further advancements of furnished cages. They are designed to keep group sizes
of up to 60 layers per compartment, thus offering hens a larger general floor space area and
therefore increased possibilities to move within their individual compartments.
The implementation of the EU directive 1999/74/EC into national law has confronted the
German laying hen industry with legal requirements far beyond the demands of the EU
directive. In Germany, conventional cages will have to be entirely banned by the end of 2008
already and furthermore, furnished cages will only be accepted until the end of 2020. Only
recently, the German legislation has approved the so called small aviary housing system as an
2
Chapter I: Introduction
adequate replacement for the use of furnished cages. So far, data on keeping hens in small
aviary housing systems is lacking and at the same time mandatory for a successful
implementation of these systems in the future. One of the major advancements of the small
aviary housing system compared to the small group system is the incorporation of perches at
two different heights within individual compartments. In addition, small aviary systems are
supposed to offer an enlarged floor space per hen (800 cm²) and enhanced compartment
heights (60 cm). These modifications aim at offering hens more opportunities to perform
natural behavioural traits and thus trying to combine increased animal welfare and high
hygienic standards, which are related to husbandry systems that are well protected from
outside environmental influences.
Alternative housing systems, such as aviary systems, are designed to keep very large groups
of layers in littered compartments and provide optional outdoor access. Aviary systems
demand more labour-intensive management skills and in addition, layers are permanently
faced with increased risk of infection due to contact with excrements and outdoor
environmental impacts. The occurrence of bird flu in a variety of European and non-European
countries in 2006 will certainly push forward the idea of improved protection of laying hen
flocks against outside environmental effects and strongly suggest the use of indoor husbandry
systems rather than aviaries with outdoor access or free range systems. Therefore, the recent
development of small aviary systems will most probably play a major in the German laying
hen industry in the near future.
The objective of the current study was to evaluate different types of house keeping systems
for laying hens with respect to layers’ welfare and health status, egg quality traits and
production parameters at two different experimental farms, comprising four different layer
lines. For the first time, perches within compartments of the small group system were
incorporated at different heights, thus meeting the legal requirements on the currently
approved small aviary system in this respect. Keeping hens in small group systems with
modified perch positions was directly compared to layers housed in small group systems with
non-elevated perches, furnished cages and an aviary system.
As the study was very comprehensive, it was split into two single dissertation projects.
Results deriving from the individual investigations together with data which had been
collected at the same trial farms from 1999-2004 and published by different authors, were
jointly analysed and discussed in the meta-analysis of this work. Table 1 provides a survey of
the different housing systems, perch positions and layer lines tested over two laying periods at
the two different experimental farms and refers to the main focal points analysed in the
3
Chapter I: Introduction
4
different chapters of this work. Chapter II provides an analysis of bone strength, keel bone
status and egg characteristics of Lohmann Silver and Lohmann Tradition hybrids kept in
furnished cages and small group systems with non-elevated perches in comparison to an
aviary system. In Chapter III, the effect of small group systems with elevated perch
configurations on bone traits, egg quality and production parameters in LS layers was
evaluated. Chapter IV illuminates the impact of different perch configurations and group sizes
within modified small group systems and furnished cages in Lohmann Brown and Lohmann
Selected Leghorn layers on humerus and tibia bone strength. In Chapter V, heterophil to
lymphocyte ratio (H/L-ratio), which reflects a measure of stress perception in laying hens was
analysed in LS layers. Chapter VI provides an analysis of a macroscopic and histological
assessment of keel bone. The general discussion is conducted in form of a meta-analysis in
Chapter VII. A summary of this work is provided in Chapter VIII, followed by an extended
German summary in Chapter IX.
Table 1: Brief overview of the experimental design of this study and the main focal points analysed in the different chapters of this work
Comparison of six housing systems for laying hens Evaluation of effects Aviplus
(FC) EV 625a-EU
(SG) EV 625A-EU
(FC) Natura
(Aviary) Conventional
cages Intensive free range
Farm A First laying period
Perch positions original original - original
LS/LT layers: Humerus and tibia strength, keel bone status, egg quality traits (Chapter II)
Farm A Second laying period
Perch positions original modified - original
LS layers: Humerus strength, tibia strength, keel bone status, egg quality traits, laying performance (Chapter III); Stress perception (heterophil/lymphocyte ratio) (Chapter V)
Farm B First and second laying period
Perch positions original modified modified -
LSL/LB layers (first laying period) and LSL layers (second laying period): Humerus strength, tibia strength, keel bone status, laying performance (Chapter IV)
Former experimental data included in a meta-analysis with special focus on: Humerus and tibia bone strength, keel bone status, plumage condition, food pad health, egg shell strength, laying performance, mortality and behaviour (Chapter VII)
Farm A and B All laying periods tested
LS/LT/LSL/LB layers: histological evaluation of keel bone (Chapter VI) FC: furnished cages, SG: small group system, LS: Lohmann Silver, LT: Lohmann Tradition, LSL: Lohmann Selected Leghorn, LB: Lohmann Brown
Chapter II
Evaluation of bone strength, keel bone deformity and egg quality
of laying hens housed in small group housing systems and
furnished cages in comparison to an aviary housing system.
B. Scholz, S. Rönchen, H. Hamann and O. Distl
Archiv für Tierzucht
Chapter II: Bone strength, keel bone status and egg quality in LSL and LB layers
Institute for Animal Breeding and Genetics, University of Veterinary Medicine Hannover,
Bünteweg 17p, 30559 Hannover, Germany
Britta Scholz, Swaantje Rönchen, Henning Hamann and Ottmar Distl
Evaluation of bone strength, keel bone deformity and egg quality of laying hens housed
in small group housing systems and furnished cages in comparison to an aviary housing
system
Evaluierung des Einflusses von Kleingruppenhaltung und ausgestaltetem Käfig im
Vergleich zu einer Volierenhaltung auf Knochenfestigkeit, Brustbeinstatus und
Eiqualität bei Legehennen
6
Chapter II: Bone strength, keel bone status and egg quality in LSL and LB layers
Abstract
The objective of the study was to assess bone breaking strength, keel bone status and egg
quality parameters of Lohmann Silver (LS) and Lohmann Tradition (LT) layers housed in
small group systems (SG) and furnished cages (FC) in comparison to an aviary system. At the
end of the 3rd, 6th, 9th and 11th laying month, approximately 40 hens were randomly chosen
from each housing system and slaughtered (478 hens in total). Humerus and tibia strengths
were analysed using a three-point-bending machine. Keel bone status was evaluated on a
scale from 1 (severe) to 4 (no deformity). Shell breaking strength was measured every four
weeks, totalling 4,887 eggs. Statistical analyses were performed using the MIXED procedure
of SAS. Humerus and tibia strengths of LS layers housed in SG were significantly higher
compared to LS hens kept in FC. Bone breaking strengths of humerus and tibia in LS and LT
layers were highest in the aviary system and the differences to the other housing systems were
significant. No significant differences in tibia and humerus bone breaking strengths were
found between SG and FC for LT hens. Keel bone status was not significantly influenced by
housing system or laying strain. For both hybrids, shell breaking strength was significantly
lower in SG compared to FC and aviary system. The results showed that SG systems can
significantly enhance bone breaking strength for LS layers in comparison to hens kept in FC.
The lower shell breaking strength of eggs in SG might slightly impair economic aspects.
Key Words: laying hens, bone strength, keel bone status, egg quality, housing systems
Zusammenfassung
Ziel der vorliegenden Studie war es, Humerus- und Tibiabruchfestigkeiten, Brustbeinstatus
sowie ausgewählte Parameter zur Eiqualität der Legelinien Lohmann Silver (LS) und
Lohmann Brown (LB) aus ausgestaltetem Käfig (FC) und Kleingruppenhaltung (SG) im
Vergleich zu einer Volierenhaltung zu untersuchen. Am Ende des 3., 6., 9. und 11.
Legemonats wurden jeweils 40 Hennen aus den drei Haltungssystemen entnommen und
geschlachtet (insgesamt 478 Tiere). Die Knochenbruchfestigkeiten wurden mittels einer
Materialprüfmaschine gemessen. Der Brustbeinstatus wurde anhand einer Skala von 1
(hochgradig verändert) bis 4 (ohne besonderen Befund) beurteilt. Untersuchungen zur
Eiqualität wurden während der Legeperiode in einem Abstand von vier Wochen durchgeführt
(insgesamt 4.887 Eier). Die statistische Auswertung erfolgte mit der Prozedur MIXED von
SAS. Humerus- und Tibiafestigkeiten der LS Hennen aus SG waren signifikant höher im
Vergleich zu LS Hennen aus FC. Für beide Legelinien erwiesen sich die in der
7
Chapter II: Bone strength, keel bone status and egg quality in LSL and LB layers
Volierenhaltung gemessenen Humerus- und Tibiafestigkeiten im Vergleich zu den zwei
übrigen Haltungsformen signifikant am höchsten. Für die LT Hennen konnte kein
signifikanter Unterschied in der Humerus- und Tibiaknochenfestigkeit zwischen SG und FC
ermittelt werden. Der Brustbeinstatus wurde nicht signifikant von Haltungssystem oder
Legelinie beeinflusst. Die Eischalenfestigkeit war für beide Legelinien in SG signifikant
niedriger verglichen zu FC und Volierenhaltung. Die Ergebnisse zeigten, dass die
Kleingruppenhaltung die Knochenfestigkeit von LS Hennen im Vergleich zu Hennen aus
ausgestaltetem Käfig signifikant verbessern konnte. Die niedrigere Schalenfestigkeit aus SG
könnte sich möglicherweise negativ auf die Wirtschaftlichkeit dieses Haltungssystems
auswirken.
Schlüsselwörter: Legehennen, Knochenfestigkeit, Brustbeinstatus, Eiqualität,
Haltungssysteme
Introduction
Since animal welfare plays an increasing role for the consumer, political decisions on laying
hen husbandry have become a focal point in the European Union. Due to current legal
regulations, conventional cages have to be replaced by alternative housing systems or
furnished cages by the end of 2011 in all European countries. In Germany, conventional cages
will be forbidden after 2008 and furthermore, furnished cages will be abandoned after 2011
also. Research is strongly required to test small group housing systems, which are currently
discussed to replace furnished cages by the end of 2011, thus offering an option to alternative
housing systems. Small group systems are designed to house larger groups of hens per
compartment and to provide an enriched environment with help of perches, nest box, sand
bath and devices to shorten claws. They aim to combine improved animal welfare with the
positive hygienic aspects, such as reduced risk of zoonoses and infections that are related to
house keeping systems which are well protected from outside environmental influences. So
far, health and welfare issues of hens housed in small group systems have not been directly
compared to layers housed in an aviary system. The objective of the present investigation was
to assess bone breaking strength, keel bone deformity and egg quality of Lohmann Silver (LS)
and Lohmann Tradition (LT) laying hens housed in a small group housing system (Eurovent
625a-EU) and furnished cages (Aviplus) in direct comparison to an aviary housing system
(Aviary “Natura”).
8
Chapter II: Bone strength, keel bone status and egg quality in LSL and LB layers
Materials and methods
All three housing systems examined (provided by Big Dutchman, Vechta, Germany) were
established within separate rooms of one experimental building. The furnished cage system
Aviplus (FC) consisted of a three-tier block of double-sided cages with solid side and rear
partitions. Group sizes comprised 10 layers (bottom tier), 20 layers (second tier) and 30 hens
(top tier). The small group housing system Eurovent 625a-EU (SG) was built without a centre
partition and accommodated group sizes of 40 and 60 laying hens which were evenly
distributed over the three levels. In both systems, each compartment was equipped with
perches, litter bath, nest box and claw shortening devices. Perches were incorporated in
parallel position to the length of each compartment. In SG, the central tube for the automatic
distribution of the dust bathing substrate served as additional perching space. The cage
surface area provided was 750 cm² per hen. The EU legislative standards on keeping laying
hens (EU directive 1999/74/EG) were fully met (Tab. 1). The aviary system (model “Natura”)
was equipped with a three tier central block and provided access to a covered outdoor area. It
consisted of two compartments, each containing 1,215 laying hens. Perches were installed in
front of the second level and above the top level. Family nest boxes were attached on the
walls opposite the central block. They were connected via footboards with the medium level
of the system.
Table 1 Brief description of the three different housing systems tested FC SG Aviary Group size 10 20 30 40 60 1215 Floor space (mm x mm)
1,206 x 625
2,412 x 625
3,618 x 625
2,412 x 1,250
3,618 x 1,250
7,050 x 18,386
Height (mm) 450 450 450 450 450 2,350 (c.b.) Space/hen (cm²) 756 756 756 750 750 approx. 1,067
FC: furnished cage system Aviplus; SG: small group system Eurovent 625a-EU; c.b.: central block of aviary system.
The trial investigated started in July 2004 and ended in July 2005. Two floor-reared, brown
layer lines (Lohmann Tradition (LT) and Lohmann Silver (LS)) were transferred to the three
housing systems at the age of 18 weeks. Each system tested contained approximately 1,500
layers. All laying hens were subjected to identical management conditions. A common 2-
phase diet for laying hens (Bela-Mühle, Vechta, Germany) was fed 3 to 4 times a day. On
average, food contained 10.8 MJ ME, 3.53 % calcium and 0.49 % total phosphorus. Water
was supplied ad libitum via nipple drinkers. In all three housing systems tested, the light
9
Chapter II: Bone strength, keel bone status and egg quality in LSL and LB layers
period was gradually stepped up from 10.5 h (week 18) up to 14 h (week 26 until the end of
the laying cycle).
At the end of the 3rd, 6th, 9th and 11th laying month approximately 40 hens were randomly
chosen from each housing system (considering layer strain and group size to equal numbers)
and slaughtered (478 hens in total). Humerus and tibia bones were removed from muscles and
tendons and stored for one day (+ 4°C) until bone strength analysis. Bone breaking strength
(N) was measured by using a three-point-bending machine (“Zwick/Z2,5/TNIS”, Zwick-
Roell, Ulm, Germany). Bone ends were placed on two supports and a constant, perpendicular
force was applied until bone fracture.
The keel bone status of the layers was evaluated visually and per palpation after removal of
the skin. It was recorded on a scale from 1 to 4 (1 = severe deformity, 2 = moderate
deformity, 3 = slight deformity, 4 = no deformity).
With begin of the third laying month, every four weeks a sample of approximately 150 and
every 12 weeks a sample of approximately 300 eggs (totalling 4,887) was collected. Shell
breaking strength (N) was assessed using the test machine “Zwick/Z2,5/TNIS”. Eggshell
thickness (µm) was defined using a micrometer (QCT from TSS, York, UK). Eggshell density
(mg/cm²) was calculated by dividing shell weight by surface area. Albumen height (mm) was
measured with help of a semi-automatic device (QCH from TSS, York, UK) and converted to
Haugh Units. Results were recorded separately for housing system, layer line, group size and
compartment (SG).
Statistical analyses were performed using the MIXED procedure of the SAS package, version
9.1.3 (Statistical Analysis System Institute Inc., Cary, NC, USA, 2006). Traits were analysed
for the fixed effects of housing system, layer line, group size and laying month. Two-way and
three-way interactions were also tested. The interaction between laying month and individual
compartment was treated as a randomly distributed effect. The model for keel bone status and
bone breaking strength included body weight of the hens as a linear covariate.
Model for bone breaking strength
Yijklmno = µ + SYSi + LLj + GR(SYS)ik + MONl + SYS*LLij + SYS*MONil + LL*GR(SYS)ijk
+ b x BW(LL*MON)jlm + MON*COMP(LL*GR(SYS))ijkln + eijklmno
Yijklmno humerus or tibia bone breaking strength
µ model constant
SYSi fixed effect of housing system (i = 1-3)
10
Chapter II: Bone strength, keel bone status and egg quality in LSL and LB layers
LLj fixed effect of layer line (j = 1-2)
GR(SYS)ik fixed effect of group size within housing system (k = 1-6)
MONl fixed effect of laying months tested (l = 1-4)
SYS*LLij fixed effect of the interaction between housing system and layer line
SYS*MONil fixed effect of the interaction between housing system and laying month
LL*GR(SYS)ijk fixed effect of the interaction between layer line and group size within
housing system
b linear regression coefficient
BW body weight of hens before slaughter
MON*COMP(LL*GR(SYS))ijkln random effect of interaction between laying month and
compartment of housing system within layer line, group size and
housing system eijklmn random error
Model for keel bone status
Yijklmno = µ + SYSi + LLj + GR(SYS)ik + MONl + SYS*LLij + SYS*MONil + b x
BW(LL*MON)jlm + MON*COMP(LL*GR(SYS))ijkln + eijklmno
Model for egg quality traits
Yijklmn = µ + SYSi + LLj + GR(SYS)ik + MONl + SYS*LLij + SYS*MONil +
MON*COMP(LL*GR(SYS))ijklm + eijklmn
Yijklmn egg quality traits: shell breaking strength, shell thickness, shell density,
Haugh Units, egg weight
Results
Table 2 illustrates the least square means (LSM), standard errors (SE) and error probabilities
of variance analysis of bone breaking strength and keel bone status of hens housed in the three
different housing systems.
11
Chapter II: Bone strength, keel bone status and egg quality in LSL and LB layers
Table 2 Least square means (LSM) and their standard errors (SE) for bone breaking strength and keel bone status for the different housing systems and error probabilities (p) between housing systems
FC (I) SG (II) Aviary (III) p Trait LSM SE LSM SE LSM SE I-II I-III II-III
Humerus (N) 170.9 4.7 185.7 4.8 287.6 9.0 * *** *** Tibia (N) 115.8 2.0 121.9 2.0 156.5 3.4 * *** *** Keel bone (1-4) 3.54 0.06 3.51 0.06 3.43 0.09 n.s. n.s. n.s.
FC: furnished cage system Aviplus; SG: small group system Eurovent 625a-EU; n.s.: not significant, p > 0.05; *: p ≤ 0.05; ***: p ≤ 0.001.
Tibia and humerus breaking strengths of layers were highest in the aviary system. The
differences to both the furnished and small group housing system were significant. In
comparison to FC, bone breaking strengths of hens kept in SG were significantly higher. Keel
bone status was scored highest in FC, but statistically significant differences could not be
detected between the three different housing systems. Table 3 presents LSM and SE of bone
breakings strengths and keel bone status of the two different laying lines and error
probabilities between housing systems.
Table 3 Least square means (LSM) and their standard errors (SE) for bone breaking strength and keel bone status by different laying lines and housing systems and their error probabilities (p)
FC: furnished cage system Aviplus; SG: small group system Eurovent 625a-EU; LS: Lohmann Silver; LT: Lohmann Tradition; n.s.: not significant, p > 0.05; **: p ≤ 0.01; ***: p ≤ 0.001.
FC (I) SG (II) Aviary (III) p Trait LSM SE LSM SE LSM SE I-II I-III II-III
Humerus LS (N) 159.5 6.6 185.6 6.7 293.8 12.7 ** *** *** Humerus LT (N) 182.3 6.5 185.7 6.7 281.3 12.7 n.s. *** *** Tibia LS (N) 109.1 2.8 120.0 2.8 156.3 4.8 ** *** *** Tibia LT (N) 122.4 2.7 123.8 2.8 156.6 4.9 n.s. *** *** Keel bone LS (1-4) 3.5 0.1 3.4 0.1 3.4 0.1 n.s. n.s. n.s. Keel bone LT (1-4) 3.6 0.1 3.7 0.1 3.5 0.1 n.s. n.s. n.s.
Humerus and tibia breaking strengths of LS layers were significantly higher in SG compared
to the FC. However, bone strengths of hens housed in the aviary system were significantly
higher to both the SG and FC system. No differences in humerus and tibia bone breaking
strengths could be detected for LB layers housed in the SG and FC, whereas differences
between the aviary and the other two systems were significant. Keel bone status within laying
line did not differ significantly between the three housing systems tested. Table 4 presents
LSM and SE of keel bone status of the different laying months tested. Results of keel bone
12
Chapter II: Bone strength, keel bone status and egg quality in LSL and LB layers
status in the 11th laying month differed significantly from findings in the 6th laying month,
thus reflecting an increase of deformities towards the end of the laying period in all housing
systems tested.
Table 4 Least square means (LSM) and their standard errors (SE) for keel bone status of each housing system and laying month and error probabilities (p) among laying months within each housing system
Laying month p Keel bone status (1-4) 3 6 9 11 3-6 3-9 3-11 6-9 6-11 9-11FC 3.8 ± 0.1 3.8 ± 0.1 3.1 ± 0.1 3.4 ± 0.1 n.s. *** n.s. *** * n.s.SG 3.3 ± 0.1 3.8 ± 0.1 3.5 ± 0.1 3.4 ± 0.1 * n.s. n.s. n.s. * n.s.Aviary 3.7 ± 0.2 3.7 ± 0.2 3.2 ± 0.2 3.2 ± 0.2 n.s. n.s. * n.s. * n.s.
FC: furnished cage system Aviplus; SG: small group system Eurovent 625a-EU; n.s.: not significant, p > 0.05; *: p ≤ 0,05; ***: p ≤ 0.001; LS: Lohmann Silver; LT: Lohmann Tradition.
Least square means (LSM) and standard errors (SE) of the egg quality traits investigated for
the different housing systems are presented in table 5.
Table 5 Least square means (LSM) and their standard errors (SE) for egg quality traits and error probabilities (p) between housing systems
FC SG (II) Aviary (III) p Trait LSM SE LSM SE LSM SE I-II I-III II-III
Shell strength (N) 40.7 0.3 39.6 0.2 40.6 0.3 ** n.s. ** Shell thickness (µm) 343.6 0.8 342.3 0.8 346.1 1.3 n.s. n.s. ** Shell density (mg/cm²) 87.9 0.2 86.6 0.2 87.7 0.3 *** n.s. ** Haugh Units 79.4 0.2 80.8 0.2 80.5 0.3 *** ** n.s. Egg weight (g) 64.9 0.1 64.4 0.1 65.2 0.1 ** n.s. *** FC: furnished cage system Aviplus; SG: small group system Eurovent 625a-EU; n.s.: not significant, p > 0.05; **: p ≤ 0.01; ***: p ≤ 0.001.
Shell breaking strength, shell density, shell thickness and egg weight were significantly higher
in the aviary system compared to SG. All egg quality traits presented except shell thickness
turned out to be significantly higher in the FC in comparison to SG. Haugh Units measured in
the aviary and SG did not differ significantly and exceeded Haugh Units recorded in FC.
Discussion
Egg shell breaking strength can be regarded as a trait of major commercial importance. A
high incidence of cracked eggs easily spoils financial gains. Literature findings on egg shell
breaking strength are very diverse. Some authors described an increased shell breaking
13
Chapter II: Bone strength, keel bone status and egg quality in LSL and LB layers
strength in aviary systems, whereas other studies did not detect differences of shell breaking
strength between cage and alternative housing systems (VAN DEN BRAND et al., 2004). In
the present investigation, the lowest shell breaking strength was found in the SG (39.6 N).
Compared to a study by LEYENDECKER et al. (2005), shell breaking strengths of LS hens
kept in an aviary (38.1 N) and furnished cage system (36.6 N) were exceeded by the present
findings. In an investigation by VITS et al. (2005) egg quality of layers housed in two
different small group systems was compared to furnished cages. The small group systems
reflected a tendency to improve egg shell breaking strength. In the present study egg shell
strength could not be increased by layers kept in the SG system, but compared to findings in
earlier investigations, the shell breaking strength measured met a high egg quality standard. In
a study by WHITEHEAD (2004) it is discussed that hens with a favourable predisposition of
stronger bones provide less calcium for egg shell formation. This might be part of an
explanation for the lower shell breaking strength of eggs found in SG compared to the other
two systems. Bone strength of hens in SG was stimulated in comparison to FC. Hence,
calcium might be preferentially used for bone remodelling and conservation rather than for
egg shell composition. Haugh Units serve as a well-known parameter to determine egg
freshness. The value decreases with extended time of storage and rising temperature. In the
present study, Haugh Units turned out to be highest in the SG system. It is difficult to
interpret this result as eggs of the three housing systems were treated under identical
conditions from the point of collection until egg quality tests. Literature references regarding
the impact of housing system on Haugh Units are very few and contradictory. Some authors
reported higher Haugh Units in conventional cages (SCHOLTYSSEK, 1975) compared to
floor keeping systems, whereas other findings stated the opposite. Nevertheless, the present
result underlines the high quality of eggs stemming from LS and LT hens kept in small group
housing systems.
With reference to health and welfare issues, osteoporosis of layers is one of the major
concerns related to conventional cages. In a variety of studies on furnished cages, the
incorporation of perches served to improve bone strength of layers (ABRAHAMSSON et al.,
1993). Small group housing systems are designed to ameliorate bone strength by the provision
of perches together with a larger floor space. VITS et al. (2005) compared bone strengths of
layers kept in a small group housing system and furnished cages. Humerus strength was found
to be higher in the furnished cage system, whereas tibia strength did not differ significantly
between the systems. Bone strengths were clearly increased compared to conventional cages.
In the current investigation, humerus and tibia strengths of LS hens kept in SG significantly
14
Chapter II: Bone strength, keel bone status and egg quality in LSL and LB layers
exceeded bone strengths measured in FC. Humerus and tibia strengths of LT kept in SG
showed a tendency to improved bone strengths compared to FC. Nevertheless, bone strengths
measured in the aviary system were not reached. Humerus bone strength of hens housed in
SG clearly exceeded bone strength reported by LEYENDECKER et al. (2005) for LS layers
kept in furnished cages (129.6N). Tibiae strengths between these two investigations hardly
differed. This result corresponds to other findings in the literature. The impact of a housing
system on tibia bone strength has often been reported to be less distinct compared to humerus
bone strength (VITS et al., 2005; HUGHES et al., 1993). In a study by BISHOP et al. (2000)
the inheritance of bone strength characteristics was revealed. Sole selection on improved bone
strength would have inevitably resulted in increased body weight. In the present study hens in
the aviary system had the strongest bones and showed the lowest mean body weight (1994g)
compared to hens kept in SG (2067g) and FC (2073g). The provision of more space together
with the incorporation of perches in the aviary and small group housing system enabled hens
to perform more movements. As a result, bone strength was stimulated and body weight was
reduced within physiological limits.
The type of housing system does not only influence bone strength but also affects the status of
keel bone. Due to its exposed anatomical location, keel bone is very vulnerable to
deformations. Accidental collisions with compartment equipment, extended perching and the
resulting compression are likely to impact keel bone condition. Deformities seem to be
strongly associated with the incorporation of perches. APPLEBY et al. (1993) described a
significantly higher incidence of keel bone deformations of hens kept in furnished cages
compared to conventional cages. FREIRE et al. (2003) detected old keel fractures in 73% of
birds kept in aviary systems. Thus, hens in aviary systems and furnished cages are mostly
predisposed to produce keel bone alterations. Keel bone deformities become manifest in the
form of twists, osteal proliferations and dorso-ventral compressions. FLEMING et al. (2004)
detected fracture callus material in all cases of deformities. In the present study, keel bone
status of hens in the aviary system tended to be lower scored compared to SG and FC at the
end of the laying period. In SG, the lowest-rated keel bone conditions were recorded in the
3rd and 11th laying month. Keel bone might not have been fully ossified in the 3rd laying
month and therefore being very vulnerable to external influences. Also, it might have taken a
longer time for hens to establish a social ranking within a group size of 40 or 60 hens
compared to the smaller group sizes of FC. This might have led to more agitation, thus
causing collision with perches. A study by KEELING et al. (2003) indicated that intermediate
group sizes between 30 and 60 hens suffer from a high degree of social disruption. In all
15
Chapter II: Bone strength, keel bone status and egg quality in LSL and LB layers
housing systems tested, keel bone status significantly deteriorated from the 9th to the 11th
laying month. No statistically significant differences of keel bone status could be found
between the three housing systems at the end of the laying period.
The current study showed that the development of small group housing systems seems to be a
well suitable option to alternative housing systems. In SG, internal and external egg quality
met a high qualitative standard together with the other two systems tested. For a more
comprehensive evaluation of economic parameters, the amount of dirty and cracked eggs
should be analysed together with data on egg production. With reference to bone strength,
results on improved bone breaking strengths of hens housed in SG compared to layers in FC
are very promising. The provision of more space due to larger group sizes seems to affect
bone strength in a very positive way. Further research would be suggested on cage equipment,
particularly perches. As the incorporation of perches is closely linked with both increased
bone strength and the incidence of keel bone deformities, research should be stimulated in
order to optimise these two parameters.
References
ABRAHAMSSON, P.; TAUSON, R.: Effect of perches at different positions in conventional
cages for laying hens of two different strains. Acta Agric. Scand., Sect. A, Animal Sci. 43
(1993), 228-235
APPLEBY, M.C.; SMITH, S.F.; HUGHES, B.O.: Nesting, dust bathing and perching by
laying hens in cages: effects of design on behaviour and welfare. Br. Poult. Sci. 34 (1993),
835-847
BISHOP, S.C.; FLEMING, R.H.; MCCORMACK, H.A.; FLOCK, D.K.; WHITEHEAD,
C.C.: The inheritance of bone characteristics affecting osteoporosis in laying hens. Poult. Sci.
41 (2000), 33-40
FLEMING, R.H.; MCCORMACK, L.; MCTEIR, L.; WHITEHEAD, C.C.: Incidence,
pathology and prevention of keel bone deformities in the laying hen. Br. Poult. Sci. 45 (2004),
320-330
FREIRE, R.; WILKINS, L.J.; SHORT, F.; NICOL, C.J.: Behaviour and welfare of individual
laying hens in a non-cage system. Br. Poult. Sci. 44 (2003), 22-29
HUGHES B.O.; WILSON, W.; SMITH, S.F.: Comparison of bone volume and strength as
measures of skeletal integrity in caged laying hens with access to perches. Res. Vet. Sci. 54
(1993), 202-206
16
Chapter II: Bone strength, keel bone status and egg quality in LSL and LB layers
17
KEELING, L.J.; ESTEVEZ, I.; NEWBERRY, R.C.; CORREIA, M.G.: Production-related
traits of layers reared in different sized flocks: the concept of problematic intermediate group
sizes. Poult. Sci. 82 (2003), 1393-1396
LEYENDECKER, M.; HAMANN, H.; HARTUNG, J.; KAMPHUES J.; NEUMANN, U.;
SÜRIE, C.; DISTL, O.: Keeping laying hens in furnished cages and an aviary housing system
enhances their bone stability. Br. Poult. Sci. 46 (2005), 536-544
SCHOLTYSSEK, S.: Die Qualität von Eiern aus Käfig- und Bodenhaltung. Arch. Geflügelk.
2 (1975), 59-62
VAN DEN BRAND, H.; PARMENTIER, H.K.; KEMP, B.: Effects of housing system
(outdoor vs cages) and age of laying hens on egg characteristics. Br. Poult. Sci. 45 (2004),
745-752
VITS, A.; WEITZENBÜRGER, D.; HAMANN, H.; DISTL, O.: Production, egg quality,
bone strength, claw length, and keel bone deformities of laying hens housed in furnished
cages with different group sizes. Poult. Sci. 84 (2005), 1511-1519
WHITEHEAD, C.C.: Overview of bone biology in the egg-laying hen. Poult.Sci. 83 (2004),
193-199
Britta Scholz, Swaantje Rönchen, Dr. Henning Hamann, Prof. Dr. Dr. Ottmar Distl*
Institute for Animal Breeding and Genetics, University of Veterinary Medicine Hannover,
Bünteweg 17p, 30559 Hannover, Germany
*Corresponding author: O. Distl
E-mail: [email protected]
Chapter III
Bone Strength, Keel Bone Deformities and Egg Quality of
Lohmann Silver Layers Kept in Small Group Systems with
Modified Perch Positions in Direct Comparison to an Aviary
Housing System and Furnished Cages
B. Scholz, S. Rönchen, H. Hamann and O. Distl
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
LOHMANN SILVER HENS KEPT IN SMALL GROUP SYSTEMS
Bone Strength, Keel Bone Deformities and Egg Quality of Lohmann Silver Layers Kept
in Small Group Systems with Modified Perch Positions in Direct Comparison to an
Aviary Housing System and Furnished Cages
B. Scholz1, S. Rönchen, H. Hamann and O. Distl
Institute of Animal Breeding and Genetics, University of Veterinary Medicine Hannover,
Bünteweg 17p, 30559 Hannover, Germany
1Corresponding author:
Britta Scholz, Insitute of Animal Breeding and Genetics, University of Veterinary Medicine
Hannover, Bünteweg 17p, 30559 Hannover, Germany, Tel.: 0049-511-953-8878; Fax: 0049-
511-953-8582; e-mail: [email protected].
20
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
ABSTRACT The objective of the current investigation was to assess the influence of a small
group housing system (Eurovent (EV) 625a-EU, equipped with elevated perches, group sizes
40, 60 layers), furnished cages (Aviplus, group sizes 10, 20, 30 hens) and an aviary system
(Natura, 2 pens, 1250 hens) on bone strength, keel bone deformities and egg quality traits of
Lohmann Silver (LS) layers under identical management and feeding conditions.
Compartments of EV 625a-EU were equipped with perches at different heights (two variants).
Investigations were carried out in the 3rd, 6th, 9th and 12th laying month, comprising a total
of 432 hens. Humerus bone strength did not differ between EV 625a-EU and Aviplus,
whereas tibia bone strength was significantly stronger in EV 625a-EU compared to Aviplus in
the 12th laying month. Hens kept in the aviary system consistently reflected significantly
stronger humerus and tibia bones. Group sizes within EV 625a-EU and Aviplus had a
significant effect on humerus and tibia bone strength. Hens kept in group sizes of 40 hens (EV
625a-EU) and 20 hens (Aviplus) showed highest bone strengths. The different perch variants
within compartments of EV 625a-EU did not have a significant effect on bone strength. Keel
bone deformities of hens kept in the aviary system were significantly more often registered
compared to hens housed in EV 625a-EU and Aviplus. Layers kept in compartments of EV
625a-EU with the back perches being heightened showed significantly more often deformed
keel bones compared to hens housed in Aviplus. Keel bone condition was not influenced by
different group sizes. Egg quality was spoiled in EV 625a-EU due to significantly higher
percentage of dirty and cracked eggs. The small group system with elevated perches did
improve tibia bone strength of LS hybrids compared to furnished cages even if being not
comparable to hens kept in the aviary system. The unfavorable keel bone status related to
hens kept in aviary systems could be largely prevented.
Key words: Small group system, furnished cages, bone strength, keel bone status, egg
quality.
INTRODUCTION
Due to the EU Council directive 1999/74/EC (CEC, 1999) on laying down minimum
standards for the protection of laying hens, conventional cages will be phased out within the
EU by the end of 2011 and replaced by furnished cages. In contrast to other EU countries, the
German government has put a ban on conventional cages by the end of 2008 already.
Furthermore, furnished cages will have to be substituted by either alternative systems or the
recently approved small group housing systems with elevated perches from January 2012.
Therefore, research on the development of small group housing systems with modified perch
21
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
positions is strongly required as these systems will play an important role in the future of
laying hen husbandry in Germany. Small group housing systems are designed to keep group
sizes of up to 60 laying hens per compartment, thus offering hens a larger floor space and
increased possibilities to increased social interaction. One of the major advancements is the
arrangement of perches on at least two different levels within each individual compartment.
This improvement aims at reducing the risk of inactivity osteoporosis in laying hens, which
has been a great welfare concern (Baxter, 1994) and has brought up discussions on legal
changes in laying hen husbandry. In several studies, the implementation of perches (furnished
cages, small group housing systems, aviary systems) has succeeded in improving bone
strength in layers (Hughes and Appleby, 1989; Barnett et al., 1997; Leyendecker et al., 2005).
Perches installed at different heights are supposed to further increase bone strength in layers
by stimulating movement and performance of natural behavioral traits. In correspondence to
furnished cages, small group housing systems are also enriched with nest boxes, sand baths
and devices to shorten claws. In contrast to alternative housing systems, small group systems
are designed to bring together improved animal welfare with the positive hygienic aspects that
are associated with house keeping systems which are well safeguarded against outside
environmental influences. The objective of the current investigation was to draw a direct
comparison of bone breaking strength, keel bone status, egg quality and production
parameters of Lohmann Silver (LS) layers kept in small group housing systems with two
variants of perch positions, furnished cages and an aviary housing system. Special focus was
put on the different perch arrangements and group sizes of the small group housing system
and their effect on bone characteristics. The study was conducted under entirely identical
management conditions, which assures a high informational value due to a direct comparison
of the three house keeping systems tested. So far, health, welfare and production issues of
hens kept in small group housing systems with elevated perch positions have not been
described and directly compared to an alternative housing system and furnished cages.
MATERIALS AND METHODS
Housing Systems and Layer Line
The three housing systems (provided by Big Dutchman GmbH, Vechta, Germany) were
installed in 3 different rooms within the same experimental building. The small group housing
system Eurovent (EV) 625a-EU was installed over 3 tiers. It accommodated compartments of
40 and 60 laying hens (floor space: 2,412 x 1,250 mm and 3,618 x 1,250 mm), which were
evenly distributed over the 3 levels of the system. Each compartment of EV 625a-EU was
22
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
equipped with 2 next boxes (900 mm x 260 mm (60 hens) and 600 mm x 260 mm (40 hens)).
The furnished cage system Aviplus consisted of a three-tier double-sided block of
compartments with solid side and rear partitions. Group sizes comprised 10 layers (bottom
tier; floor space: 1,206 x 625 mm, 1 nest box per compartment), 20 layers (medium tier; floor
space: 2,412 x 625 mm, 2 nest boxes) and 30 hens (top level; floor space: 3,618 x 625 mm, 3
nest boxes). Compartments of both systems offered a height of 450 mm and were enriched
with perches, sand baths, nest boxes and devices to shorten claws. The aviary system
“Natura” provided a fully littered indoor floor space and consisted of a three-tier central
block, which was divided into 2 pens each containing 1,250 laying hens (floor space: 3,650 x
15,980 mm). Both pens were located within the same room and provided access to 2 separate,
covered outdoor areas (20,980 x 3,400 mm). Each pen of the aviary system was equipped
with 21 family next boxes (1,220 x 440 mm), which were attached alongside the walls
opposite the central block and could be accessed via footboards from the first and second tier
of the system. All 3 systems tested fully conformed to the EU legislative standards on keeping
laying hens (EU directive 1999/74/EC). The investigation comprised one laying period which
lasted from September 15th, 2005 until October 16th, 2006. Lohmann Silver hybrids used in
the study were brown layers, predominantly white-feathered and exhibited higher body
weight compared to more common brown layer lines, such as Lohmann Brown or Lohmann
Tradition.
Perch Positions within Housing Systems
In the small group housing system, 4 perches per pen were incorporated in parallel position to
the length of each compartment. Perches were installed at 2 different heights with either the
back perches being elevated (BE, 200 mm distance to cage floor) or back and front perch
being heightened (200 mm and 275 mm distance to cage floor) and installed in a stepped
position (ST) (figure 1). The central tube for the automatic distribution of dust bathing
substrate served as additional perching space. In EV 625a-EU, 4 compartment variants related
to the different group sizes and perch positions (60 hens, BE, ST and 40 hens BE, ST) with 2
replicates each per tier were tested. In the furnished cage system, back and front perch were
installed on an even level within each individual compartment (90 mm to cage floor).
Compartments tested had 8 replicates (top tier), 12 replicates (medium tier) and 24 replicates
(bottom tier). Perches were oval shaped with a flattened top and underside. They were 30 mm
thick and produced a contact area of 20.1 mm for the layers’ feet. All perches in the Aviplus
were made out of white, polished plastics (PVC, rigid). In EV 625a-EU, elevated perches
23
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
were made out of abraded, galvanized zinc and roundly shaped. In the aviary system, square
shaped wooden bars were incorporated in front of the medium level of the central block (830
mm to ground floor) and three galvanized perches were installed above the top level in a
stepped order (480 and 740 mm distance to top level).
Management and Feeding
All laying hens were subjected to identical management conditions throughout the trial
period. Hens were floor-reared within the same flock, thus ensuring fully identical rearing
conditions. Laying hens were treated according to a commonly accepted immunization
scheme for layers during the rearing and laying period. At the age of 18 weeks, a total number
of 5,500 Lohmann Silver hens was transferred to the experimental building and distributed to
the 3 house keeping systems. The lighting scheme employed comprised a 14 h light period in
all 3 housing systems. In the Aviplus and EV 625a-EU, light was provided from 5 am until 7
pm. The lighting period in the aviary system was adapted to environmental light variations
and comprised four different 14 h lighting periods throughout the trial period. The beginning
of the lighting period varied from 5 am (3rd laying month) up to 7.15 am (12th laying month).
Hens were fed a common 2-phase diet for layers, which was adapted to the stage of the laying
cycle. Food was automatically supplied via food chains 3 to 4 times a day. An analysis of
food components was conducted in regular intervals. On average, food contained 10.9 MJ
ME, 16.5% crude protein, 3.89% calcium and 0.48% total phosphorus. Water was supplied ad
libitum via nipple drinkers.
Analysis of Bone Breaking Strength
At the end of the 3rd, 6th, 9th and 12th laying month, approximately 36 laying hens were
randomly taken out of each housing system, considering group sizes and perch positions (EV
625a-EU) to equal parts. Investigations started at the end of the 3rd laying month in order to
give layers the opportunity to adapt to the different environmental housing conditions and
minimize a direct influence of floor-rearing conditions on the parameters tested. The study
comprised a total of 432 hens. Before slaughter, live weight of hens was measured.
Alternately the left or right humerus and tibia bones were dissected after removal of muscles
and tendons. Bones were stored for one day (+ 4°C) until bone strength analysis. Bone
breaking strength was measured by using a three-point-bending machine
(“Zwick/Z2.5/TNIS”, Zwick-Roell, Ulm, Germany). Bone ends were placed on two supports
24
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
(humerus: 40 mm, tibia: 90 mm distance) and a constant, perpendicular force was applied
until bone fracture. Bone strength was automatically recorded and measured in Newton (N).
Analysis of Keel Bone Status
Keel bone status of hens was macroscopically reported following the dissection of humerus
and tibia bones. After removal of the layers’ breast skin, keel bones were examined visually
and per palpation alongside the keel. According to the severity of deviations, keel bone status
was recorded on a scale from 1 to 4 (1 = severe deformity, 2 = moderate deformity, 3 = slight
deformity, 4 = no deformity). Keel bone deviations were observed in the form of s-shaped
deformities, osteal proliferations and dorso-ventral compressions.
Egg Quality Analysis and Investigation of Production Parameters
With begin of the 3rd laying month egg quality analysis was carried out every 4 weeks on 3
consecutive days. A sample of 120 eggs per housing system was randomly collected
considering group sizes, perch positions and compartments (EV 625a-EU) to equal parts. A
total number of 3,960 eggs was examined. Shell breaking strength was measured using the
test machine “Zwick/Z2.5/TNIS” and automatically recorded in Newton (N). Eggshell
thickness (µm) was reported using a micrometer (QCT from TSS, York, UK). Eggshell weight
(g) was measured after having dried the eggshells in a microwave. Eggshell density (mg/cm²)
was automatically calculated by dividing egg shell weight by egg surface area. Egg surface
area derived from the formula S = 4.67 x G2/3 (S: surface area, G: egg weight). Albumen
height (mm) was reported using a semi-automatic device (QCH from TSS, York, UK) and
automatically converted to Haugh Units (HU). Yolk color was measured on a scale from 1 to
15 using a yolk color fan (Roche, Switzerland). Meat and blood spots were recorded
separately and evaluated on a scale from 0 to 2 (0 = no meat/blood spot, 1 = meat/blood spot
smaller than 2 mm, 2 = meat blood spot larger than 2 mm). Hen egg production and the
number of cracked and dirty eggs were recorded on a daily basis. Daily egg mass was
calculated by multiplying the number of eggs laid per day by corresponding egg weight. Daily
salable egg mass did not include cracked and dirty eggs. Both parameters were related to the
number of hens present.
Statistical Analysis
Statistical analysis of the traits humerus and tibia bone breaking strength, keel bone status,
egg quality and body weight of layers was carried out using the Procedure MIXED of the
25
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
SAS package, version 9.1.3. (Statistical Analysis System Institute Inc., Cary, NC, USA,
2006). Housing system (SYS), group size within housing system (GR(SYS)), laying month
(MON), the interaction between housing system and laying month (SYS*MON) and perch
position (PP) within EV 625a-EU were included as fixed effects. The individual
compartments (comp) within housing systems were employed as randomly distributed effects.
Body weight (BW) within laying month was used as a covariate for the traits bone breaking
strength and keel bone status. F-test was conducted to test the significance of the effects in the
statistical model. A separate statistical analysis of data on the small group housing system was
carried out in order to test the fixed effect PP and results for the fixed and random effects as
parameterized in the model described above did not differ.
Yijklmno = µ + SYSi + GR(SYS)ij + MONk + SYS*MONik + PP(SYS)il + comp(SYS)im + b x
BW(MON)kn + eijklmno
Yijklmno humerus and tibia bone breaking strength/keel bone status
μ model constant
SYSi fixed effect of housing system (i = 1 to 3)
GR(SYS)ij fixed effect of group size within housing system (j = 1 to 6)
MONk fixed effect of laying month (k = 1 to 4)
SYS*MONik fixed effect of housing system and laying month (ik = 1 to 12)
PP(SYS)il perch positions within EV 625a-EU (l = 1 to 2)
comp(SYS)im randomly distributed effect of individual compartments within housing
systems (m = 1 to 70)
b linear regression coefficient
BW(MON)kn body weight of layers within laying month
eijklmno random error variation
Statistical analysis of cracked eggs (%), dirty eggs (%), produced eggs (%, per hen present),
egg mass and salable egg mass (g, per hen present) was carried out with a separate statistical
model in which housing system was included as a fixed effect and each day of lay was used as
a covariate in linear, quadratic, logarithmic and squared logarithmic form. Cracked and dirty
eggs were related to the total number of eggs laid throughout the laying period.
Residual correlations were calculated using the SAS procedure CORR for the residuals of the
traits analyzed with the above mentioned models excluding body weight of layers. Residuals
of traits were directly merged by individual laying hen.
26
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
RESULTS
Housing system had a significant effect on the traits humerus and tibia bone breaking
strength, keel bone status, blood spots, meat spots, egg weight, yolk weight and percentage of
dirty eggs. The different group sizes within housing system significantly impacted humerus
and tibia bone strength, blood spots and egg weight. Egg quality traits were significantly
influenced by laying month and the interaction between laying month and housing system.
(Table 1). Humerus and tibia bone breaking strengths were significantly higher in the aviary
system compared to hens kept in the small group system and furnished cages, whereas no
difference was found between the latter two systems (Table 2). Keel bone status was scored
significantly lower in the aviary system compared to EV 625a-EU and Aviplus. Hens kept in
Aviplus showed keel bones with less deformities compared to laying hens housed in EV
625a-EU, although differences did not achieve a significant level (p= 0.08).
The two different perch positions incorporated in the EV 625a-EU did not have a significant
effect on humerus and tibia bone breaking strengths and keel bone status within the small
group housing system, whereas hens kept in ST compartments of EV 625a-EU showed
significantly higher tibia bone breaking strength compared to hens kept in Aviplus. Keel bone
status of hens kept in the furnished cages was scored significantly higher compared to layers
housed in the small group housing system with perches being incorporated in the BE position
(Table 3).
With relation to the different group sizes, hens kept in Aviplus in pens of 20 layers had
significantly higher humerus and tibia bone strengths compared to hens housed in
compartments of 30 layers (Table 4). Group sizes comprising 10 hens had a significant
positive effect on tibia bone strength compared to the larger groups of 30 hens. In EV 625a-
EU, laying hens housed in compartments accommodating 40 hens had produced significantly
higher humerus bone strengths in comparison to group sizes of 60 layers. No difference
related to group sizes within EV 625a-EU was found for the traits tibia bone strength and keel
bone status.
Humerus and tibia bone strengths did not differ between Aviplus and EV 625a-EU related to
the different laying months tested except the 12th laying month (Table 5). Hens kept in the
EV 625a-EU had significantly higher tibia bone strength compared to Aviplus. In all four
laying months tested, humerus and tibia bone strengths of layers kept in the aviary system
were significantly higher compared to bone strengths of layers kept in Aviplus and EV 625a-
EU. Keel bone status differed between EV 625a-EU and Aviplus in the 9th laying month
when hens kept in the small group system reflected a significantly lower keel bone status
27
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
compared to layers housed in the furnished cage system. Keel bone status of hens kept in the
aviary system was scored significantly lower in the laying months 3 to 9 compared to hens of
Aviplus and significantly differed from hens kept in EV 625a-EU in the laying months 9 and
12.
Within Aviplus and EV 625a-EU, humerus bone strength did not differ among the different
laying months tested, whereas hens kept in the aviary system showed a significant decline in
humerus bone strength from the 3rd to the 12th laying month. Tibia bone breaking strength
did not differ among laying months in Aviplus, whereas a significant increase was observed
in EV 625a-EU and aviary system between the 3rd and 12th and 9th and 12th laying month.
Although the fixed effects MON and SYS*MON did not have an overall significant effect on
keel bone status, keel bone status within housing system was in most cases significantly lower
in the 3rd and 6th laying month when compared to laying month 9 and 12.
Body weight of layers was highest in Aviplus (2,085.9 g), followed by hens kept in the aviary
system (2,052.5 g) and EV 625a-EU (2,036.2 g), but differences did not achieve a significant
level.
A significant positive correlation was detected between residuals of the traits humerus and
tibia bone breaking strength. Residuals of the trait keel bone status reflected a significant
positive correlation with residuals of tibia bone strength, whereas no significant correlation
was found between residuals of keel bone status and humerus bone strength. Residuals of the
trait body weight were also significantly positive correlated with humerus and tibia bone
breaking strength (Table 6).
With relation to egg quality traits, no significant differences between housing systems was
found for the traits shell breaking strength, shell thickness, shell density, shell weight,
albumen height, Haugh units, yolk color and egg mass, whereas egg weight and the incidence
of meat and blood spots was significantly higher in Aviplus and EV 625a-EU compared to the
aviary system (Table 2). Egg and yolk weight were highest and daily salable egg mass was
lowest in EV 625a-EU and the differences to the aviary system (egg weight, daily salable egg
mass) and to the aviary system and Aviplus (yolk weight, daily salable egg mass) were
significant. The percentage of dirty eggs was significantly higher in EV 625a-EU compared to
Aviplus. Hens kept in the aviary system had produced significantly more dirty eggs than
layers housed in Aviplus. The percentage of cracked eggs in EV 625a-EU significantly
exceeded the proportion of cracked eggs in Aviplus and aviary system. Differences between
the latter two housing systems were also significant. Egg production (per hen present) was
significantly higher in the aviary system compared to EV 625a-EU and Aviplus. No
28
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
difference in egg production was found between the small group housing system and
furnished cages.
With relation to the different group sizes, egg weight of hens housed in groups of 10 and 20
layers (Aviplus) was significantly higher compared to groups of 30 layers (Table 4). Egg
quality traits measured in EV 625a-EU did not significantly differ among the group sizes of
40 and 60 layers. No significant differences in egg quality traits were found between the two
different perch positions tested in EV 625a-EU (Table 3).
DISCUSSION
Humerus bone breaking strength of hens kept in the small group system did not increase
compared to Aviplus. Previous studies have shown that the provision of perches at different
heights in non-commercial systems increased bone breaking strength of layers (Abrahamsson
et al., 1996). The results of the present study indicated that the incorporation of perches at
different heights together with larger group sizes in the EV 625a-EU might not have provided
enough stimuli to increase humerus bone strength compared to the furnished cage system. The
influence of the particular layer line LS should be considered when evaluating the results as
more commonly used layer lines might be more responsive to changes in bone strength due to
larger group sizes and variations in perch positions. Studies on hens kept in litter pens have
shown that perches which were incorporated in an elevated position were highly accepted
compared to non-elevated ones (Olsson and Keeling, 2000). In the current study, the design of
perches could have had a negative influence on layers’ perching behavior in EV 625a-EU. In
contrast to perches incorporated in the furnished cage system Aviplus, elevated perches
within compartments of EV 625a-EU were roundly shaped, which might have reduced their
usage. Duncan et al. (1992) described hens being more unstable on circular perches compared
to rectangular shaped ones. Knowles and Broom (1990) found layers kept in conventional
cages exhibiting the fewest limb movements and therefore having the weakest bones. Perches
at different heights within compartments of the EV 625a-EU might have inhibited hens’ limb
movements, particular wing flapping, as the arrangement of perches might have been
hindering. Norgaard-Nielsen (1989) found hens kept in cages being restricted in their wing
movements to a degree that bone strength was reduced. The author emphasized the
importance of height of compartments in order to allow movement in the three dimensions. In
the current study compartment heights of EV 625a-EU did not exceed compartment heights of
the furnished cage Aviplus, although perches had been installed at different heights. In an
investigation by Leyendecker et al. (2005), LS layers kept in furnished cages with group sizes
29
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
of 10 layers per compartment were compared to hens kept in an aviary system and the
differences related to humerus bone breaking strength were significant (furnished cage
system: 129.6 N, aviary system: 247.0 N). In the current study, humerus bone strength of hens
kept in EV 625a-EU (167.5 N) and Aviplus (166.6 N) clearly exceeded humerus bone
strength of LS hens kept in furnished cages measured by Leyendecker et al. (2005). These
results suggest that larger group sizes seem to have a positive impact on humerus bone
strength, although bone strengths of laying hens kept in the aviary system in both
investigations could not be achieved. In the current study, tibia bone strength measured in the
aviary system was significantly higher compared to EV 625a-EU and Aviplus. These results
do not agree with the findings of Taylor and Hurnik (1994), who did not detect differences in
tibia bone breaking strength between hens kept in battery cages and an aviary system.
Although the overall interaction SYS*MON was not significant, tibia bone breaking strength
of layers kept in EV 625a-EU measured in the 12th laying month was significantly higher
compared to hens kept in the furnished cages. These data support the tendency of a positive
impact of EV 625a-EU on tibia bone strength compared to Aviplus. The influence of different
housing systems on tibia bone strength has been described very inconsistently. Hughes and
Appleby (1989) described tibia bone strength being positively influenced by cage design as
soon as perches were long enough to provide perching space for simultaneous
accommodation of hens, whereas Moinard et al. (1998) and Hughes and Wilson (1993) could
not detect differences in tibiotarsal breaking strength due to different cage designs.
Comprising data of all four laying months tested, hens kept in EV 625a-EU with perches
being installed in the ST position had significantly higher tibia bone strength compared to
layers kept in the Aviplus. This result might be due to an increased mechanical loading on
tibia bone while jumping up and down elevated perches. In contrast to humerus bone strength,
tibia bone breaking strength differed within the small group housing system among the
different laying months tested and significantly increased from the 3rd to the 12th laying
month. These results are in correspondence with findings of Leyendecker et al. (2005), who
also detected an increase in tibia bone strength towards the end of the production cycle, while
humerus bone strength remained constant. Leyendecker et al. (2005) suggested an
accumulation of medullary bone in tibia together with little resorption of structural bone as a
possible explanation. Humerus bone strength of layers kept in Aviplus and EV 625a-EU
remained unchanged among the different laying months tested, thus demonstrating that layers
retained a constant level of humerus bone strength until the end of the laying cycle although
high egg production and therefore high Ca-requirements were present. Hens kept in the aviary
30
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
system experienced a significant decline in humerus bone strength between laying months 3
and 12, but humerus bone strength consistently exceeded bone strengths measured in Aviplus
and EV 625a-EU, which underlines the distinct impact of an alternative housing system on
bone breaking strength.
The different group sizes within EV 625a-EU and Aviplus had a significant effect on bone
strength and egg quality traits. Hens kept in the EV 625a-EU in compartments of 40 layers
had significantly higher humerus bone strength compared to pens of 60 hens. These findings
do not correspond with findings of Vits et al. (2005), who did not detect a significant effect of
group size on humerus and tibia bone breaking strengths in Lohmann Brown and Lohmann
Selected Leghorn layers. Keeling et al. (2003) described intermediate group sizes around 30
hens being problematic due to a high degree of social disruption and unstable social hierarchy
compared to group sizes of 15, 60 and 120 hens. In the compartments of 40 layers, unwanted
agitation due to stress and social conflicts might have increased general movements, which
could have resulted in increased humerus bone strength. According to Keeling et al. (2003)
hens kept in group sizes of 15 hens were able to maintain a stable hierarchy and groups of 60
and 120 layers reflected tolerant social behavior, thus exhibiting less social conflicts. A
possible social disruption in pens of 40 layers did not negatively impact egg quality, as no
differences in egg quality traits were found between the different group sizes in EV 625a-EU.
In Aviplus, hens kept in group sizes of 30 layers reflected lower humerus and tibia bone
strength compared to the smaller groups of 20 layers and 10 layers (tibia strength). Due to the
experimental design of the study, group sizes of 30 hens were kept in the third tier of the
Aviplus system. Previous studies have described hens being more fearful in upper tiers of a
housing system compared to lower tiers (Hemsworth and Barnett, 1989). One of the reasons
for lower humerus and tibia bone strength in groups of 30 layers might therefore be an
increased fear behavior in the upper tier, which could have negatively affected hens’ agitation
activities. Light intensity in all three housing systems was set to 20 lux, but its intensity
differed between the three tiers of Aviplus and EV 625a-EU with light being darker in the
bottom tier and brightest in the top tier. Although hens were observed to be more active with
higher light intensities (Boshouwers and Nicaise, 1987) and light is generally known to have a
positive impact on bone characteristics, the effect of a higher light intensity in the top tier of
Aviplus could not prevent a lower humerus and tibia bone breaking strength compared to the
medium and bottom tier of the system. The lower egg weight measured in groups of 30 layers
compared to compartments of 10 and 20 hens might have also been influenced by the
31
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
different tiers of the Aviplus system. Vits et al. (2006) reported lighter egg weight in upper
tiers of housing systems compared to medium levels.
With relation to keel bone status, a decline throughout the laying period, which was observed
in all three housing systems tested, was described by a variety of authors (Nicol et al., 2006;
Weitzenbürger et al., 2006a). Findings on inferior keel bone status of layers kept in the aviary
system agreed with previous studies. Freire et al. (2003) found a high number of keel bone
deviations in hens kept in perchery systems. In a study by Elson and Croxall (2006), keel
bone lesions were mostly prevalent in multi-tier aviary systems compared to conventional and
furnished cages. Accidental flight and landing collisions with perches were seen to be the
major reasons for keel bone deformities in aviary systems (Gregory et al., 1991). In a study on
furnished cages and furnished small group systems by Weitzenbürger et al. (2006a),
approximately 33 % of hens exhibited keel bone deformities during the laying period.
Abrahamsson and Tauson (1993) could relate the provision of perches to inferior keel bone
condition. In the present study, keel bone status of layers kept in EV 625a-EU did not differ
from layers kept in Aviplus except in the 9th laying month, when keel bone deformities were
significantly more often registered in the small group system. Fleming et al. (2004) found keel
bone deformities of hens being associated with a generally weaker skeleton. Although hens
kept in the small group system were offered a higher degree of movement and perching
stimulus, layers’ keel bone in general might be too weak and therefore not capable of being
positively influenced by different housing systems. The same applies to layers kept in the
aviary system. Hens exhibited a significantly unfavorable keel bone status compared to EV
625a-EU in the laying months 9 and 12. Tibia bone strength and keel bone status were
positively correlated in the present study, but neither the small group system nor the aviary
system did succeed in strengthening layers’ keel bone to an extent that it would withstand
accidental collisions with perches or mechanical pressure during perching activities.
Wahlström et al. (2001) made long-term perching activities together with increased
mechanical pressure on the keel responsible for a high incidence of keel bone deviations. As
hens kept in the small group system with perches being incorporated in the BE position even
exhibited a significantly poorer keel bone status compared to layers housed in Aviplus, a high
acceptance of elevated back and non-elevated front perch together with perching activities on
the central tube could have led to increased pressure on the keel bone. Perching on the
elevated back perch allowed hens to perch secludedly in the back of the compartment
compared to the elevated front perch of the ST perch variant. Frequent use of the round back
perch might have contributed to increased local pressure resulting in keel bone deformities,
32
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
which would be in correspondence with findings of Tauson and Abrahamsson (1994). As the
round perches incorporated in the ST position did not lead to unfavorable keel bone status
compared to Aviplus, the usage of the more exposed, elevated front perch might have been
less frequent and hens spent more time standing on the wire floor, thus relieving pressure on
their keel bone. In a study by Weitzenbürger et al. (2006b), hens kept in an Aviplus system
spent more time standing on the wire floor rather than using perches compared to layers kept
in two different Eurovent systems with perches at an even height. In the present study, layers
kept in Aviplus were also lacking the central tube as additional perching space. Therefore,
less perching activities in the furnished cage system could have explained the superior keel
bone status of hens kept in Aviplus compared to hens in the BE compartments of the small
group system. The arrangement of perches at different heights in a relatively high stocking
density (750 cm²/hen) could have also led to increased accidental collisions with perches. In
addition, elevated perches were of a darker color compared to the non-elevated ones in
Aviplus, which might have caused difficulties to approach perches properly. According to a
study on adequate perch distances within housing systems (Scott et al., 1997), perches should
be incorporated with minimized horizontal and vertical distances, thus ensuring a move
between perches without failures. The implementation of perches in the small group housing
system should have enabled hens to negotiate distances provided properly as maximum perch
distances from the cage floor did not exceed 275 mm.
With reference to egg quality parameters, a significant influence of housing system was
detected for the traits egg weight, yolk weight, percentage of dirty eggs, meat spots and blood
spots. Hens in the Aviplus and EV 625a-EU produced significantly heavier eggs compared to
layers kept in the aviary system. These results do not agree with findings of Van den Brand et
al. (2004). The authors found eggs from outdoor layers being relatively broader than eggs
from hens kept in cages, but indicated the problem of maintaining constant egg quality in
outdoor housing systems compared to battery cages. Taylor and Hurnik (1996) did not detect
differences in egg weight between hens kept in aviaries and conventional cages, thus
supporting the inconsistency on findings related to egg weight in previous studies. In the
current investigation, egg yolk weight might have accounted for the higher egg weight of hens
kept in the Aviplus and EV 625a-EU as these hens had produced eggs with significantly
higher yolk weights compared to layers kept in the aviary system. De Ketelaere et al. (2002)
found evidence that higher egg weight was not related to inferior egg shell breaking force. In
the current study, no significant influence of housing system on egg shell breaking force was
found, whereas egg weight significantly differed among the different systems. Related to the
33
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
different laying months of the investigation, the interaction SYS*MON showed a decrease in
shell breaking strength and increase in egg weight from laying month 3 to 12 within each
housing system tested. These findings corresponded to results of previous studies on egg shell
quality where increased egg size was accompanied by inferior egg shell quality and reduced
egg shell breaking strength due to constant egg shell mass and decreased capability of layers
to absorb calcium in the course of the laying period (Cordts et al., 2001). Although a decrease
of shell strength was observed in the present study, shell quality traits such as shell thickness,
shell density and shell weight increased from laying month 3 to 12.
The significantly lower number of meat spots in eggs stemming from hens kept in the aviary
system agreed with findings of Leyendecker et al. (2001), who detected a significantly lower
number of meat spots in eggs stemming from Lohmann Tradition free range and aviary layers
compared to caged layers, whereas the number of blood spots did not differ between the
different housing systems. According to Campo and Garcia Gil (1998), increased exposure to
stress was related to an increased incidence of internal egg inclusions. Hens kept in the aviary
system might have had more possibilities to perform natural behavioral traits, thus
experiencing less stress exposure compared to layers kept in Aviplus and EV 625a-EU.
With relation to the percentage of dirty and cracked eggs, hens kept in EV 625a-EU had
produced higher numbers of downgraded eggs compared to layers housed in the aviary
system and Aviplus. A high number of dirty and cracked eggs due to mislaid eggs in dust
baths was found to be problematic in furnished cages as downgraded eggs contribute to a rise
in production costs (Appleby et al., 2002). An increased number of cracked eggs (Duncan et
al., 1992) and dirty eggs (Guesdon and Faure, 2004; Mallet et al., 2006) was associated with
the incorporation of perches. Duncan et al. (1992) observed hens laying their eggs from
perches. In the current investigation, hens kept in the EV 625a-EU might have mislaid a high
number of eggs due to only 2 nest boxes per compartment, which did not provide enough
space for simultaneous use of all layers. Mallet et al. (2006) suggested that an improved
equipment of housing system would succeed in reducing the number of mislaid and therefore
dirty eggs if nest laying possibilities were enhanced. In the current study, elevated perches in
the EV 625a-EU might have provided the potential of laying eggs from perches, thus
increasing the number of cracked eggs. Also, eggs laid in nest boxes easily accumulated when
they rolled onto the egg belt due to the high number of hens per nest box. This might have
been primarily responsible for the high percentage of cracked eggs. Egg shell breaking
strength of eggs stemming from EV 625a-EU was not found to be responsible for the high
incidence of cracked eggs in the small group system as no differences in egg shell strength
34
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
could be detected between the three housing systems tested. An increased number of cracked
eggs in furnished cages was also described by Guesdon et al. (2006). In contrast, egg quality
in furnished cages and small group systems measured by Vits et al. (2005) met the high
qualitative standards related to conventional cages. Findings on significantly higher egg
production in the aviary system compared to EV 625a-EU and Aviplus have to be interpreted
carefully as high egg production can easily be spoiled by a large amount of downgraded eggs.
Daily egg mass did not differ among the three different housing systems tested, but the
number of dirty and cracked eggs detected in the aviary system significantly reduced the daily
salable egg mass compared to Aviplus. Due to the high incidence of downgraded eggs in EV
625a-EU, the small group system yielded the lowest daily salable egg mass per hen housed
compared to the other two housing systems.
The results of the present investigation showed that the elevated perches and enlarged group
sizes of the small group housing system did not provide enough stimuli to ameliorate humerus
bone strength of layers compared to furnished cages. However, a positive impact on tibia
bone strength of the ST perch variant was detected. Furthermore, hens in the small group
system had exhibited superior tibia bone strength at the end of the laying period compared to
Aviplus. At all times of the investigation, the aviary system was found to have a decisive
impact on humerus and tibia bone strength. Although tibia bone strength and keel bone
condition were positively correlated, an unfavorable keel bone status of layers kept in the
aviary system could not be prevented. In addition, perches in the BE position of EV 625a-EU
were found to have a negative impact on keel bone status compared to Aviplus, which was
primarily related to extended perching activities.
Egg shell quality parameters, except the percentage of cracked and dirty eggs, did not differ
between the 3 different housing systems tested. Although the small group system yielded
highest egg and yolk weights together with a sound egg production rate, the high number of
cracked and dirty eggs spoiled results on egg quality and resulted in the lowest daily salable
egg mass among the different housing systems tested.
ACKNOWLEDGEMENTS
The authors would like to thank Big Dutchman GmbH, Lohmann Tierzucht GmbH and
Deutsche Frühstücksei GmbH for financial support of this scientific project.
35
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
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38
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
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39
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
TABLE 1. Analysis of variance for the traits humerus and tibia bone strength, keel bone
status, egg quality traits and egg production, daily egg mass and daily salable egg mass per
hen present
SYS GR(SYS) MON SYS*MON PP(SYS) Trait F-
value P F-
valueP F-
valueP F-
valueP F-
value P
Humerus strength (N) 255.2 *** 3.5 * 0.9 NS 2.3 * 0.2 NS Tibia strength (N) 82.0 *** 4.8 ** 1.2 NS 0.7 NS 2.0 NS Keel bone status (1-4) 17.5 *** 1.0 NS 1.8 NS 0.9 NS 1.4 NS Shell strength (N) 0.1 NS 0.3 NS 63.9 *** 1.7 * 0.6 NS Shell thickness (µm) 0.1 NS 0.7 NS 3.2 *** 2.6 *** 0.01 NS Shell density (mg/cm3) 0.4 NS 0.6 NS 17.1 *** 4.6 *** 0.01 NS Shell weight (g) 0.6 NS 0.9 NS 65.5 *** 4.6 *** 0.01 NS Haugh units 1.0 NS 0.8 NS 173.7 *** 5.1 *** 2.1 NS Blood spots (1-2) 6.4 ** 2.6 * 1.3 NS 1.1 NS 0.1 NS Meat spots (1-2) 9.2 *** 0.8 NS 0.9 NS 1.7 * 0.3 NS Albumen height (mm) 0.4 NS 0.5 NS 165.7 *** 5.0 *** 1.5 NS Yolk weight (g) 32.2 *** 2.0 NS 358.3 *** 3.7 *** 0.01 NS Yolk color (1-15) 0.2 NS 0.9 NS 16.7 *** 2.4 *** 2.1 NS Egg weight (g) 10.8 *** 5.4 *** 111.8 *** 2.8 *** 0.4 NS Dirty eggs (%) 11.7 *** - - - - - - - - Cracked eggs (%) 1.9 NS - - - - - - - - Egg production (%) 1.9 NS - - - - - - - - Egg mass (g) 0.9 NS - - - - - - - - Salable egg mass (g) 2.5 NS - - - - - - - - SYS: housing system; GR(SYS): group size within housing system; MON: laying month;
SYS*MON: interaction between housing system and laying month; PP(SYS): perch position
variant; * P ≤ 0.05, ** P ≤ 0.01, *** P ≤ 0.001.
40
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
TABLE 2. LS-means (LSM), their standard errors (SE) and significant differences between
housing systems for humerus and tibia bone strength, keel bone status, egg quality traits and
egg production, daily egg mass and daily salable egg mass per hen present
Aviplus (I) EV 625a-EU (II) Aviary system (III) Trait LSM SE LSM SE LSM SE
Humerus strength (N) 166.6B 4.2 167.5B 4.4 284.2A 4.1 Tibia strength (N) 120.9B 2.3 126.5B 2.4 159.0A 2.2 Keel bone status (1-4) 3.66B 0.1 3.52B 0.1 3.21A 0.1 Shell strength (N) 43.0a 0.8 42.9a 0.4 42.5a 1.0 Shell thickness (µm) 343.7a 1.9 343.6a 1.0 344.7a 2.3 Shell density (mg/cm3) 86.1a 0.6 85.5a 0.3 85.5a 0.8 Shell weight (g) 6.2a <0.1 6.2a <0.1 6.2a 0.1 Haugh units 81.7a 0.4 81.9a 0.2 82.6a 0.5 Blood spots (1-2) 0.13A <0.01 0.14A <0.01 0.09B <0.01 Meat spots (1-2) 0.86A <0.1 0.89A <0.1 0.81B <0.1 Albumen height (mm) 6.9a 0.1 7.0a <0.1 7.0a 0.1 Yolk weight (g) 17.1B <0.1 17.3A <0.1 16.8C 0.1 Yolk color (1-15) 12.7a 0.1 12.7a <0.1 12.6a 0.1 Egg weight (g) 61.0B 0.1 61.3B 0.1 60.4A 0.1 Dirty eggs (%) 1.62B <0.01 2.04A <0.01 1.99A <0.01 Cracked eggs (%) 1.32Bb <0.01 3.50A <0.01 1.52Cc <0.01 Egg production (%) 86.0B <0.01 86.2B <0.01 88.8A <0.01 Egg mass (g) 51.9a <0.01 51.7a <0.01 51.4a <0.01 Salable egg mass (g) 50.4Aa <0.01 48.8B <0.01 49.7Cc <0.01 EV: Eurovent; means within a row lacking a common superscript differ (P ≤ 0.05).
41
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
TABLE 3. LS-Means (LSM), their standard errors (SE) and significant differences of bone
breaking strength (N) and keel bone status between the two variants of perch positions in EV
625a-EU (EV) and Aviplus
EV ST (I) EV BE (II) Aviplus (III) Trait LSM SE LSM SE LSM SE
Humerus strength (N) 165.7a 6.0 169.3a 6.2 166.6a 4.2 Tibia strength (N) 129.6a 3.2 123.4ab 3.3 120.9b 2.3 Keel bone status (1-4) 3.58ab 0.08 3.46b 0.08 3.66a 0.1 Shell breaking strength (N) 43.2a 0.5 42.6a 0.5 43.0a 0.8 Shell thickness (µm) 343.6a 1.4 343.7a 1.4 343.7a 1.9 Shell density (mg/cm3) 85.6a 0.4 85.5a 0.4 86.1a 0.6 Shell weight (g) 6.2a 0.03 6.2a 0.03 6.2a 0.05 Haugh units 81.6a 0.4 82.3a 0.4 81.7a 0.4 Blood spots (1-2) 0.13a 0.01 0.14a 0.01 0.10a 0.01 Meat spots (1-2) 0.89a 0.02 0.88a 0.02 0.86a 0.01 Albumen height (mm) 6.9a 0.1 7.0a 0.1 6.9a 0.1 Yolk weight (g) 17.3A 0.1 17.3A 0.1 17.1B 0.1 Yolk color (1-15) 12.6a 0.04 12.7a 0.04 12.7a 0.06 Egg weight (g) 61.2a 0.2 61.4a 0.2 61.0a 0.1 ST: perches in stepped position, BE: back perch elevated; means within a row lacking a
common superscript differ (P ≤ 0.05).
42
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
TABLE 4. LS-means (LSM), their standard errors (SE) and significant differences between
group sizes within housing system for humerus and tibia bone strength, keel bone status and
selected egg quality traits
Aviplus P EV 625a-EU P Trait 10 (I) 20 (II) 30 (III) I-II I-III II-III 40 (I) 60 (II) I-II
Humerus strength (N)
170.8 ± 7.2
175.1 ± 7.2
154.0 ± 7.2
NS NS * 177.2 ± 6.2
157.8 ± 6.0
*
Tibia strength (N)
126.2 ± 3.9
126.7 ± 3.9
109.9 ± 3.9
NS ** ** 129.6 ± 3.3
123.3 ± 3.2
NS
Keel bone status (1-4)
3.64 ± 0.09
3.78 ± 0.09
3.56 ± 0.10
NS NS NS 3.54 ± 0.08
3.50 ± 0.08
NS
Blood spots (1-2)
0.11 ± 0.02
0.17 ± 0.02
0.11 ± 0.02
* NS * 0.14 ± 0.01
0.14 ± 0.01
NS
Egg weight (g) 61.2 ± 0.2
61.5 ± 0.2
60.4 ± 0.2
NS * *** 61.1 ± 0.2
61.5 ± 0.2
NS
EV: Eurovent, * P ≤ 0.05, ** P ≤ 0.01, *** P ≤ 0.001.
43
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
TABLE 5. LS-means (LSM), their standard errors (SE) and significant differences between
housing systems and laying months for humerus and tibia bone strength and keel bone status
Aviplus (I) EV 625a-EU (II) Aviary system (III) Laying Months LSM SE LSM SE LSM SE Humerus strength (N) 3 174.6B 8.8 167.5B 9.8 311.7A 8.2 6 165.9B 8.2 176.0B 9.1 298.1A 8.2 9 160.8B 8.4 159.9B 9.0 270.2A 8.2 12 165.2B 8.4 166.7B 7.5 256.7A 8.2 Tibia strength (N) 3 120.4B 4.8 121.2B 5.3 155.8A 4.4 6 123.7B 4.4 123.6B 4.9 159.6A 4.4 9 115.6B 4.5 121.7B 4.7 151.9A 4.4 12 124.1C 4.6 139.4B 4.0 168.8A 4.4 Keel bone status (1-4) 3 3.84a 0.12 3.78ab 0.13 3.49b 0.11 6 3.83A 0.11 3.66AB 0.12 3.42B 0.11 9 3.55A 0.11 3.22b 0.11 2.81C 0.11 12 3.41ab 0.11 3.43a 0.10 3.11b 0.11 EV: Eurovent; means within a row lacking a common superscript differ (P ≤ 0.05).
44
Chapter III: Bone traits and egg quality in small group, furnished and aviary system
45
TABLE 6. Correlation coefficients (below the diagonal) and their error probabilities (above
the diagonal) between humerus and tibia bone breaking strength, keel bone status and body
weight of layers
Trait Bone strength Humerus
Bone strength tibia
Keel bone status Body weight of layers
Bone strength Humerus
- <0.001 0.154 <0.001
Bone strength tibia
0.408 - <0.001 <0.001
Keel bone status
0.069 0.271 - 0.770
Body weight of layers
0.182 0.368 0.014 -
Figure 1. Cross-section of the elevated perch
positions BE (back perch (BP) elevated) and ST
(stepped position with back and front perch (FP)
elevated) and of the central tube (CT) within
Eurovent 625a-EU compartments
Chapter IV
Bone strength and keel bone status of two layer strains kept in
furnished small group systems with different perch configurations
and group sizes
B. Scholz, S. Rönchen, H. Hamann and O. Distl
Chapter IV: Influence of different perch positions on bone strength and keel bone status
Bone strength and keel bone status of two layer strains kept in furnished
small group systems with different perch configurations and group sizes
B. SCHOLZ, S. RÖNCHEN, H. HAMANN and O. DISTL
Institute for Animal Breeding and Genetics, University of Veterinary Medicine Hannover,
Foundation, Hannover, Germany1
Abstract 1. The objective of the present study was to investigate whether an arrangement of
perches at two different heights within individual compartments of small group housing
systems (back perch elevated (BE), front perch elevated (FE) or both perches heightened
(ST)) combined with an enlarged group size would increase humerus and tibia bone breaking
strength and impact keel bone status.
2. Bone strength and keel bone status of two layer strains (Lohmann Selected Leghorn (LSL),
Lohmann Brown (LB)) kept in small group systems (SG 40-60 (groups of 40 and 60 hens),
SG 20-30 (20 and 30 hens)) with different perch configurations and furnished cages (FC, 10
and 20 hens, perches on an even height) were compared in two experimental trials under
identical management conditions.
3. Investigations were carried out at the end of the 6th and 12th laying month, comprising a
total of 576 hens. Layers were caged during rearing and transferred to the three housing
systems at the age of 18 weeks.
4. When all compartments of SG 40-60 had been incorporated with perches at two different
heights, humerus and tibia bone breaking strength in LSL layers significantly increased
compared to FC, whereas keel bone status was negatively impacted.
5. Within SG 40-60, the perch configurations BE and FE significantly increased humerus
bone strength of LSL layers compared to the ST perch position.
6. LB layers showed significantly higher bone strength in pens of 20 hens compared to
compartments of 30 hens in SG 20-30, whereas no effect of group size was detected for LSL
layers within the three housing systems tested.
7. Keeping hens in SG 40-60 with modified perch configurations was associated with
increased bone breaking strength of layers but brought about the problem of inferior keel bone
1Correspondence to: Professor O. Distl, Institute for Animal Breeding and Genetics, University of Veterinary Medicine Hannover (Foundation), Bünteweg 17p, 30559 Hannover, Germany, Phone: +49-511-9538875, Fax: +49-511-9538582. E-mail: [email protected]
48
Chapter IV: Influence of different perch positions on bone strength and keel bone status
status, presumably due to a high compression load on the keel during perching activities and
accidental perch collisions with keel bone.
INTRODUCTION The national implementation of the EU Council directive 1999/74/EC (19 July 1999) on
laying down minimum standards for the protection of laying hens has induced major changes
in laying hen husbandry. The German government has put a ban on furnished cages and
intends to replace these systems either by alternative housing systems or furnished small
group systems which have only recently been approved of as adequate substitutes. In
Germany, conventional cages will be entirely abandoned by the end of 2008. In
correspondence to the legal regulations, most EU countries will stick to conventional cages
until the end of 2011 and then replace them by the use of furnished cages. In several studies,
developments on conventional cages towards furnished house keeping systems have led to
positive achievements in bone breaking strength (Hughes and Appleby, 1989; Abrahamsson
and Tauson, 1993). So far, only very few data exists on furnished small group systems which
are further advancements of furnished cages. Furnished small group systems are designed to
keep group sizes of up to 60 laying hens per compartment and offer increased possibilities to
move due to a larger floor space. In correspondence to furnished cages, small group housing
systems are also equipped with perches, nest box, pecking and scratching area and devices to
shorten claws and provide a cage surface area of 750cm² per hen. Vits et al. (2005) analysed
humerus and tibia bone strengths of LSL layers kept in furnished cages and furnished small
group systems and found tibia bone strengths being comparable to bone strengths of hens kept
in an aviary system measured by Leyendecker et al. (2005). Due to the different designs of
the studies a fully matching comparison can only be carefully drawn. In an investigation by
Weitzenbürger et al. (2006), approximately 33% of layers kept in furnished cages and small
group housing systems experienced keel bone deformities throughout the laying period. These
alterations were supposed to be due to mechanical pressure on the keel bone, which occurred
during perching activities and was primarily influenced by general bone breaking strength.
Currently, furnished small group systems with modified perch configurations, which will be
implemented with the beginning of 2012, reflect the most advanced developments in laying
hen husbandry in Germany. In addition to furnished small group systems, these housing
systems are equipped with perches which are installed at two different heights within each
individual compartment. The modified perch positions aim to increase bone strength by
stimulating movements of layers, thus trying to minimise the problem of inactivity
49
Chapter IV: Influence of different perch positions on bone strength and keel bone status
osteoporosis. Small group systems and particularly small group systems with modified perch
positions were designed to meet the requirements of improved animal welfare and high
hygienic standards that are related to systems which are well protected from outside
environmental influences. In the course of developing such a laying hen husbandry system we
analysed bone breaking strength and keel bone status of Lohmann Selected Leghorn (LSL)
and Lohmann Brown (LB) layers kept in three different housing systems. For the first time
the effect of modified small group systems on bone strength and keel bone status was
measured and directly compared to furnished cages and furnished small group systems under
identical management conditions. Particular emphasis will be put on the influence of different
kinds of perch modifications within individual compartments and the influence of enlarged
group sizes.
MATERIALS AND METHODS Housing systems, trials and layer lines
The three housing systems tested (all provided by Big Dutchman, Vechta, Germany) were
located in parallel position to each other within the same experimental building (Farm
Wesselkamp, Ankum). All housing systems tested were built over four tiers and fully met the
EU legislative standards on keeping laying hens. The furnished cage system Aviplus (FC) and
the small group system (SG) Eurovent 625A-EU (SG 20-30) consisted of a block of double-
sided cages with solid side and solid (FC) rear partitions. Group sizes in FC comprised 10 and
20 layers (cage floor 1206 x 625 mm and 2412 x 625 mm respectively). In SG 20-30 pens of
20 and 30 hens were kept (2412 x 625 mm and 3618 x 625 mm). The small group system
Eurovent 625a-EU (SG 40-60) was built without a centre partition and accommodated group
sizes of 40 and 60 laying hens per compartment (2412 x 1250 mm and 3618 x 1250 mm).
Although group sizes differed, compartment height (450 - 525 mm) and space per hen (750
cm²) was identical for all compartments within the three housing systems tested. Two
experimental trials were investigated which comprised the period August 2004 to October
2006. In the first trial, approx. 4,500 Lohmann Selected Leghorn (LSL) and 4,500 Lohmann
Brown (LB) layers were kept, which were evenly distributed over the three systems. In SG
20-30 and SG 40-60, each tier of the housing systems tested contained three to four
successive compartments of LSL and LB hens, which were arranged in alternate order. In FC,
nine successive compartments of LSL and LB hens alternated. In the second trial, only LSL
hens were used (approx. 9,000). All laying hens included in the investigation were cage-
reared and transferred to the three housing systems at the age of 18 weeks.
50
Chapter IV: Influence of different perch positions on bone strength and keel bone status
Perch positions and perch design
Compartments of both the SG 20-30 and FC were equipped with a front and back perch. Four
perches per compartment were installed in the SG 40-60 respectively. Perches were
incorporated in parallel position to the length of each compartment, allowing each hen 150
mm perch of its disposal. With reference to perch positions, a certain number of
compartments of SG 20-30 and SG 40-60 were modified according to the legal demands on
the modified small group system in each trial. One of the major requirements is the
incorporation of perches at two different heights within each compartment. Perch positions in
the systems tested comprised perches installed on an even level (NE, not elevated, 90 mm
distance to cage floor), the front perch being elevated (FE, 200 mm distance to cage floor), the
back perch being heightened (BE, 200 mm distance to cage floor) or both perches being
elevated and incorporated in a stepped position (ST, 200 and 275 mm distance to cage floor)
(Figure 1). In SG 20-30 compartments, the perch modifications NE, BE and FE were tested.
In SG 40-60 compartments the effect of all four types of perch modifications was analysed
(Table 1). In addition to the other two housing systems, the central tube for the automatic
distribution of the dust bathing substrate in SG 40-60 served as additional perching space.
Perches in FC were installed on an even level in both trials. All perches were made out of
white, polished plastics (RAL9010, PVC, rigid) and had a thickness of 30 mm. They were
oval shaped with a flattened top and underside. The contact area for the layers’ feet was 20.1
mm. Front and back parts of the perch were formed in a convex shape. Perches in SG 40-60,
which were modified in their position were roundly shaped and their surface was made out of
abraded, galvanised zinc.
Management, feeding and laying performance
During both trials laying hens were subjected to identical management conditions.
Throughout the rearing period, hens received a prophylactic treatment according to a
commonly accepted vaccination scheme for laying hens. In addition, layers were vaccinated
against coccidiosis, E. coli, pox and pneumovirus infection. During the laying period, hens
were vaccinated against Newcastle disease and infectious bronchitis in regular intervals. An
identical lighting scheme was employed for all three housing systems tested. The lighting
period was gradually stepped up to 14 h per day. Hens were given a standard diet for laying
hens which was distributed three to four times per day per automatic food chain. An analysis
of food components was conducted in regular intervals, thus monitoring and ensuring the
nutritional value of the diet fed. Water was supplied ad libitum per nipple drinkers. The
incorporated pecking and scratching area (610 x 210 mm in FC, 600 x 260 mm in SG 20-30
51
Chapter IV: Influence of different perch positions on bone strength and keel bone status
and SG 40-60) was automatically supplied with a dust bathing substrate once a day. In SG 20-
30 and SG 40-60, two pecking and scratching areas were incorporated within each
compartment and arranged at opposite sides of the next boxes. In FC, one pecking and
scratching area was located right beside the nest box and a metal gate limited the access to
11am until 3pm. Production performance per housing system was recorded on a daily basis.
Analysis of bone breaking strength
At the end of the 6th and 12th laying month of both experimental trials 48 hens were
randomly chosen from each housing system, considering layer strain (first trial) and group
size within each housing system to equal numbers (576 hens in total). Before slaughter, body
weight of hens was recorded. Alternately the left or right humerus and tibia bones were
removed from muscles and tendons, dissected and stored for one day (+ 4°C) until bone
strength analysis. Bone breaking strength was measured by using a three-point-bending
machine (“Zwick/Z2,5/TNIS”, Zwick-Roell, Ulm, Germany). Bone ends were placed on two
supports (humerus: 40 mm, tibia: 90 mm distance) and a constant, perpendicular force was
applied until bone fracture. Bone strength was automatically recorded and measured in
Newton (N).
Evaluation of keel bone status
Reporting of keel bone status was carried out following the dissection of humerus and tibia
bones. After removal of the skin, keel bones of layers were evaluated visually and per
palpation. According to the severity of deviations (s-shaped deformities, osteal proliferations
and dorso-ventral compressions), keel bone status was recorded on a scale from 1 to 4 (1 =
severe deformity, 2 = moderate deformity, 3 = slight deformity, 4 = no deformity).
Statistical analysis
Statistical analysis was carried out using Residual Maximum Likelihood (REML) with the
MIXED procedure of SAS, version 9.1.3. (Statistical Analysis System Institute Inc., Cary,
NC, USA, 2006). For the first trial, housing system, layer line, group size within housing
system, laying month and perch position (PP) within housing system and layer line were
employed as fixed effects. The effect of PP was also tested within housing system, layer line
and group size and did not have a significant effect. The interactions between layer line and
housing system and layer line and group size within housing system were also included in the
model. The individual compartments (comp) within housing system, layer line and group
52
Chapter IV: Influence of different perch positions on bone strength and keel bone status
sizes were treated as a randomly distributed effect. Body weight (bw) of the layers within
layer line was a linear covariate. Each laying trial was analysed separately. The model was
reduced by the fixed effect layer line (LIN) and its interactions for statistical analysis of the
second trial.
Yijklmnop = µ + SYSi + LINj + GR(SYS)ik + LIN*SYSij + LIN*GR(SYS)ijk + MONl +
PP(LIN*SYS)ijm + compn + b x bw(LIN)jo + eijklmnop
Yijklmnop humerus and tibia bone breaking strength/keel bone status (first trial)
μ model constant
SYSi fixed effect of housing system (i=1 to 3)
LINj fixed effect of layer line (j=1 to 2)
GR(SYS)ik fixed effect of group size within housing system (k=1 to 5)
LIN*SYSij fixed effect of the interaction between layer line and housing system
(ij=1 to 6)
LIN*GR(SYS)ijk fixed effect of the interaction between layer line and group size within
housing system (ijk=1 to 12)
MONl fixed effect of laying month (l=1 to 2)
PP(SYS*LIN)ijm perch positions within housing system and layer line (ijm=1 to 12)
compn randomly distributed effect of individual compartments within housing
systems (n=1 to 91)
b linear regression coefficient
bw(LIN)jo body weight of layers within layer line
eijklmnop random error variation
Results of variance analysis were regarded significant when the error probability was less
than 5% (p< 0.05). Statistical analysis was also carried out by excluding data of the furnished
cage system Aviplus from the model and furthermore, by entirely excluding the fixed effect
SYS and statistically evaluating the effect of perch positions within each EV system
separately. The results did not differ from the statistical model described above.
53
Chapter IV: Influence of different perch positions on bone strength and keel bone status
RESULTS For both trial periods, the overall probability levels of the effects SYS, PP(SYS*LIN) and
GR(SYS) for humerus and tibia bone strength and keel bone status are given in Table 2. The
least square means (LSM), standard errors (SE) and error probabilities of analysis of variance
for bone breaking strength and keel bone status by housing system and layer line are
presented in table 3. In the first trial, no significant difference in humerus and tibia bone
strength could be detected between the three different housing systems tested although
humerus and tibia bone strength of both layer lines measured in the SG systems tended to be
higher compared to FC. In the second trial, when all perch positions within compartments of
SG 40-60 had been modified according to the demands on the modified small group system,
tibia and humerus bone strengths of LSL layers were found to be significantly higher in
comparison to FC. The tendency of a higher bone breaking strength of hens kept in SG 20-30
in the first trial compared to FC was confirmed in the second trial. LSL layers in SG 20-30
had a significantly higher humerus and tibia bone strength compared to FC although the
percentage of compartments with perch modifications had not differed in SG 20-30 between
the two trials. In correspondence to the first trial, no significant difference between humerus
and tibia bone strength was found between the two SG systems in the second trial. Keel bone
status did not differ significantly between housing systems in the first trial. In the second trial,
keel bone status of layers kept in SG 40-60 (all perches in modified positions) was scored
almost significantly lower than hens kept in the SG 20-30 (p = 0.058).
With reference to perch position varieties in SG 40-60, no significant difference in bone
breaking strength could be detected between the variants NE and BE for both layer lines in
the first trial. Although the overall probability level for the effect PP (SYS*LIN) was still not
significant for humerus bone strength (p = 0.14) in the second trial, hens kept in
compartments with the BE and FE positions had significantly higher humerus bone breaking
strength compared to layers housed in compartments with perches in the ST position, whereas
no significant influence of perch positions on tibia bone strength was found (Table 4). Keel
bone status did not differ between the different perch modifications in both trials. Results of
variance analysis for perch varieties of hens kept in SG 20-30 are illustrated in table 5. In the
first trial, no significant difference could be detected between the three kinds of perch
modifications except for tibia bone strength of LSL layers. Tibia bone strength was found
significantly higher in the NE position compared to FE. This finding could not be repeated in
the second trial as hens kept in compartments with FE modification showed significantly
higher tibia bone strength in comparison to layers kept in NE compartments. In
54
Chapter IV: Influence of different perch positions on bone strength and keel bone status
correspondence to SG 40-60, keel bone status did not differ between the different perch
positions within SG 20-30. The effect of group size within housing system did not prove a
significant influence on LSL bone strength, whereas LB layers produced a significantly
higher humerus and tibia bone strength in compartments of 20 hens compared to pens of 30
layers in SG 20-30 (Table 6). No effect of group size on keel bone status could be detected.
Residual correlations between humerus and tibia bone strength, keel bone status and body
weight of hens showed a significant positive residual correlation between humerus and tibia
bone breaking strength and between these two traits and keel bone status, whereas residuals of
body weight did not significantly correlate with residuals of the traits bone strength and keel
bone status.
In the first trial period, layers showed a laying performance (% hen day) of 88.7 in SG 40-60
and 88.4 in SG 20-30 and FC. In the second experimental trial, egg production rate was 89.2
(SG 40-60), 90.5 (SG 20-30) and 88.8 (FC). All standard errors related to the egg production
rates given were 0.002.
DISCUSSION Several investigations on laying hen bone strength have clearly stated that osteoporosis in
layers is due to lack of physical movement resulting from environmental constraints of the
housing system and its equipment (Baxter, 1994; Webster, 2004) together with a switch from
structural to medullary bone, which occurs when a hen reaches sexual maturity (Whitehead
and Fleming, 2000). The incorporation of perches on an even level had proved being
successful in increasing bone strength in a variety of studies compared to conventional cages
(Barnett et al., 1997; Leyendecker et al., 2002). In the first experimental trial hens kept in the
SG systems reflected a tendency of increased bone strength within layer line compared to the
FC system. This result might have been less distinct for LSL layers compared to findings of
the second trial, as the number of hens per observation was reduced due to the two layer
strains used in trial one. In addition, less compartments of SG 40-60 were equipped with
perch modifications in the first trial. In the second experimental trial, humerus and tibia bone
strengths of LSL layers kept in SG 40-60 with all perches being installed at two different
heights were found to be significantly higher compared to hens kept in FC. Elevated perches
together with an enlarged floor space in SG 40-60 seemed to have served as a strong stimulus
to movement. In a study by Olsson and Keeling (2000) layers kept in litter pens preferred
perches at heights of 63 cm compared to lower perches and showed a very high acceptance.
Abrahamsson et al. (1996) found increased humerus bone strength of layers kept in get-away
55
Chapter IV: Influence of different perch positions on bone strength and keel bone status
cages with perches at different levels, thus proving a positive effect of perch arrangements at
different heights. Vits et al. (2005) analysed bone strength of LSL and LB layers kept in a
furnished small group system (Eurovent 625a-EU) with perches incorporated on an even
level. The results of humerus bone strength of LSL layers kept in SG 40-60 in the second trial
(191.7 N) clearly exceeded bone strength measured by Vits et al. (2005). The authors reported
humerus bone strength of 185.3 N pooled for both layer lines and found LB hens having
stronger humerus bones than LSL layers. Tibia bone strength between these two
investigations hardly differed. In SG 40-60, humerus bone strength of LSL layers kept in
compartments with BE and FE perch positions was significantly higher compared to the ST
position. Duncan et al. (1992) analysed the effect of perch arrangement and design on tibia
bone strength. The authors discovered that hens more frequently used perches of rectangular
cross-section compared to round ones and indicated that hens were more unstable on circular
perches. Perches incorporated in the ST position were roundly shaped. This might have
reduced the stimulus to agitation due to less perch acceptance. The colour of perches in the
ST position (dark grey) compared to only the elevated perch being of dark grey colour in the
FE and BE position might have also influenced perching activities. Taylor et al. (2003)
detected hens’ movements between perches in non-cage systems be inhibited when perches
were of dark colour compared to white coloured perches. They suggested altering perch
colours in order to make perches more visible and to provide a better approach. Lower
humerus bone strength of layers kept in compartments with the ST position might have also
been due to less effect of exercise resulting from a closer vertical distance between back and
front perch perches (75 mm) in comparison to the BE and FE modifications (110 mm vertical
distance). Tibia bone strength was not affected by different modifications of perch
arrangements in SG 40-60. Hens kept in SG 20-30 showed very inconsistent reactions
towards the different perch positions regarding tibia bone strength. The effect of the two
variants NE and FE in the first trial was completely reversed in the second trial. This result is
difficult to explain. Some authors found both humerus and tibia bone strength be positively
affected by different cage designs or housing systems (Knowles and Broom, 1990;
Leyendecker et al., 2001), whereas others could not state any effects on tibia bone strength
(Hughes and Wilson, 1993; Abrahamsson and Tauson, 1997; Moinard et al., 1998). In this
context, tibia bone strength does not seem a very reliable indicator of responding to
modifications in cage equipment. Effects on tibia bone strength can be rather diverse. A study
by Fleming et al. (1994) pointed out that humerus is the bone which shows the largest
responses to different husbandry systems. Therefore, effects on tibia bone strength should be
56
Chapter IV: Influence of different perch positions on bone strength and keel bone status
interpreted rather carefully and might not easily be reproduced, as the results of trial one and
two have clearly shown. Differences in group sizes did not produce significant effects on LSL
bone strength in both trials. This result corresponds to findings of Vits et al. (2005). In their
investigation, no differences related to bone breaking strength could be detected between
layers housed in small group pens with varying group sizes. In the current study, LB layers
kept in SG 20-30 reflected significantly higher humerus and tibia bone strength in
compartments of 20 layers compared to pens of 30 hens. The smaller floor space of hens kept
in compartments of 20 hens having a positive influence on bone strength of LB layers is
difficult to explain. Perch arrangement and space per hen (750 cm² per hen) was identical for
both group sizes. As group sizes of 30 hens can reflect a high degree of social disruption
(Keeling et al., 2003), LB hens in the smaller compartments (20 hens) might have been less
displaced when stepping up on elevated perches and exhibiting perching activities. In
addition, the performance of more weight bearing exercise for a longer time when using
elevated perches without disturbance could have contributed to an increase in bone strength.
The equipment of housing systems does not only influence bone strength but also has an
impact on keel bone, which is very vulnerable due to its exposed anatomical location. Keel
bone status was found to be negatively associated with house keeping systems which are
equipped with perches (Appleby et al., 1993; Abrahamsson et al., 1996). Findings in previous
studies have suggested that hens kept in aviary housing systems are predisposed to suffer
from keel bone deviations due to accidental flight and landing collisions with perches
(Gregory et al., 1991). Considering data on keel bone status of a European study (Elson and
Croxall, 2006), conventional and furnished cages were found to be more favourable housing
systems compared to aviaries. In comparison to the first trial, when 33 % of compartments
were equipped with elevated perch variants in SG 40-60, all compartments were incorporated
with perches in modified configurations in the second trial and hens experienced an almost
significantly lower keel bone status compared to hens kept in SG 20-30. The provision of
perches at two different heights in SG 40-60 seemed to have had a negative impact on the
keel. The results of increased bone strength in SG 40-60 compared to FC suggested a high
acceptance of perches in the former system. Long-term perching activities have been
described to produce keel bone deviations due to inadequate mechanical pressure on the keel
(Wahlström et al., 2001). Elevated perches in SG 40-60 were roundly shaped, which might
have led to increased local pressure on keel bone while perching. Tauson and Abrahamsson
(1994) found the incidence of keel bone lesions clearly affected by perches with a round
design. An inadequate arrangement of perches has also been described to cause keel bone
57
Chapter IV: Influence of different perch positions on bone strength and keel bone status
deviations. Scott et al. (1997) suggested a minimised horizontal and vertical distance of
perches at different heights in order to support hens moving downwards without failures. In
the current study the maximal vertical distance between perch and cage floor was 275 mm
(ST), which should not have born a risk of injury while accessing perches. Moinard et al.
(2004) suggested perch distances not to exceed 600 mm in extensive housing systems in order
to avoid injuries through missing perches. The horizontal distance of perches was
approximately 150 mm, which should have provided hens an easy move between perches.
Inferior keel bone status of layers kept in SG 40-60 might therefore primarily be due to
extended perching pressure on keel bone. Also, disruptive reactions in the stocking
environment provided (750 cm² space per hen) together with a great proportion of dark
coloured perches might have contributed to accidental collisions of keel bone with perches.
As regards the perch arrangement, hens should have very well been able to negotiate the
distances provided in SG 40-60 properly. Keel bone status was not influenced by group size,
which is in agreement with findings of VITS et al. (2005). In the present study, bone strength
and keel bone status were positively correlated which corresponds to a study by Bishop et al.
(2000). Also in agreement with Bishop et al. (2000), strength of tibia showed higher
correlations with keel bone status than strength of humerus. As bone strength characteristics
respond rapidly to environmental changes allowing more freely moving of layers,
improvements in housing systems in this respect should increase the strength of the whole
skeleton.
The results of the current study showed that the incorporation of perches at different heights
in the SG systems positively impacted bone strength of humerus and tibia. In SG 40-60, the
variants FE and BE were found to be favourable perch positions compared to the ST
configuration with relation to humerus bone strength. The influence of group size was found
to be less distinct. Although the study demonstrated positive correlations between humerus
and tibia bone strength and keel bone status, keel bone in SG 40-60 with modified perches did
not improve as much that it could withstand extended pressure from perching activities and
possible perch collisions.
ACKNOWLEDGEMENTS The authors would like to thank Big Dutchman GmbH, Lohmann Tierzucht GmbH and
Deutsche Frühstücksei GmbH for financial support of this scientific project.
58
Chapter IV: Influence of different perch positions on bone strength and keel bone status
REFERENCES ABRAHAMSSON, P. & TAUSON, R. (1993) Effect of perches at different positions in
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ABRAHAMSSON, P., TAUSON, R. & APPLEBY, M.C. (1996) Behaviour, Health and Integument
of Four Hybrids of Laying Hens in Modified and Conventional Cages. British Poultry
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ABRAHAMSSON, P. & TAUSON, R. (1997) Effects of group size on performance, health and
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APPLEBY, M.C., SMITH, S.F. & HUGHES, B.O. (1993) Nesting, dust bathing and perching by
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BARNETT, J.L., GLATZ, P.C., NEWMAN, E.A. & CRONIN, G.M. (1997) Effects of modifying
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Australian Journal of Experimental Agriculture, 37: 523-529.
BAXTER, M.R. (1994) The welfare problems of laying hens in battery cages. Veterinary
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BISHOP, S.C., FLEMING, R.H., MCCORMACK, H.A., FLOCK, D.K. & WHITEHEAD, C.C. (2000)
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DUNCAN, E.T., APPLEBY, M.C. & HUGHES, B.O. (1992) Effect of perches in laying cages on
welfare and production of hens. British Poultry Science, 33: 25-35.
ELSON, H.A. & CROXALL, R. (2006) European study on the comparative welfare of laying
hens in cage and non-cage systems. Archiv für Geflügelkunde, 70: 194-198.
FLEMING, R.H., WHITEHEAD, C.C., ALVEY, D., GREGORY, N.G. & WILKINS, L.J. (1994) Bone
structure and breaking strength in laying hens housed in different husbandry systems.
British Poultry Science, 35: 651-662.
GREGORY, N.G., WILKINS, L.J., KESTIN, S.C., BELYAVIN, C.G., & ALVEY, D.M. (1991) Effect
of husbandry system on broken bones and bone strength in hens. Veterinary Record, 128:
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HUGHES, B.O. & APPLEBY, M.C. (1989) Increase in bone strength of spent laying hens
housed in modified cages with perches. Veterinary Record, 124: 483-484.
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Chapter IV: Influence of different perch positions on bone strength and keel bone status
HUGHES, B.O. & WILSON, S. (1993) Comparison of bone volume and strength as measures of
skeletal integrity in caged laying hens with access to perches. Research in Veterinary
Science, 54: 202-206.
KEELING, L.J., ESTEVEZ, I., NEWBERRY, R.C. & CORREIA, M.G. (2003) Production-related
traits of layers reared in different sized flocks: the concept of problematic intermediate
group sizes. Poultry Science, 82: 1393-1396.
KNOWLES, T.G. & BROOM, D.M. (1990) Limb bone strength and movement in laying hens
from different housing systems. Veterinary Record, 126: 354-356.
LEYENDECKER, M., HAMANN, H., HARTUNG, J., KAMPHUES, J., RING, C., GLÜNDER, G.,
AHLERS, C., SANDER, I., NEUMANN, U. & DISTL, O. (2001) Analyse von Genotyp-Umwelt-
Interaktionen zwischen Legehennenhybriden und Haltungssystemen in der Legeleistung,
Eiqualität und Knochenfestigkeit. 3. Mitteilung: Knochenfestigkeit. Züchtungskunde, 73:
387-323.
LEYENDECKER, M., HAMANN, H., HARTUNG, J., GLÜNDER, G., NOGOSSEK, M., NEUMANN, U.,
SÜRIE, C., KAMPHUES, J. & DISTL, O. (2002) Untersuchungen zur Schalenfestigkeit und
Knochenstabilität von Legehennen in drei verschiedenen Haltungssystemen.
Züchtungskunde, 74: 144-155.
LEYENDECKER, M., HAMANN, H. HARTUNG, J., KAMPHUES, J., NEUMANN, U., SÜRIE, C. &
DISTL, O. (2005) Keeping laying hens in furnished cages and an aviary housing system
enhances their bone stability. British Poultry Science, 46: 536-544.
MOINARD, C., MORISSE, J.P. & FAURE, J.M. (1998) Effect of cage area, cage height and
perches on feather condition, bone breakage and mortality of laying hens. British Poultry
Science, 39: 198-202.
MOINARD, C., STATHAM, P. & GREEN, P.R. (2004) Control of landing flight by laying hens:
implications for the design of extensive housing systems. British Poultry Science, 45: 578-
584.
OLSSON, I.A. & KEELING, L.J. (2000) Night-time roosting in laying hens and the effect of
thwarting access to perches. Applied Animal Behaviour Science, 68: 243-256.
SAS INSTITUTE (2006) Statistical Analysis System, Version 9.1.3, SAS Institute Inc., Cary,
NC, USA.
SCOTT, G.B., LAMBE, N.R. & HITCHCOCK, D. (1997) Ability of laying hens to negotiate
horizontal perches at different heights, separated by different angles. British Poultry
Science, 38: 48-54.
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Chapter IV: Influence of different perch positions on bone strength and keel bone status
TAUSON, R. & ABRAHAMSSON, P. (1994) Foot and skeletal disorders in laying hens. Acta
Agriculturae Scandinavica, 44: 110-119.
TAYLOR, P.E., SCOTT, G.B. & ROSE, S.P. (2003) Ability of laying hens to negotiate jumps
between horizontal perches: effects of light intensity and perch colour. British Poultry
Science, 44 (Supplement 1): 32-33.
VITS, A., WEITZENBÜRGER, D., HAMANN, H. & DISTL, O. (2005) Production, egg quality,
bone strength, claw length and keel bone deformities of laying hens housed in furnished
cages with different group sizes. Poultry Science, 84: 1511-1519.
WAHLSTRÖM, A., TAUSON, R. & ELWINGER, K. (2001) Plumage condition and health of
aviary-kept hens fed mash or crumbled pellets. Poultry Science, 80: 266-271.
WEBSTER, A.B. (2004) Welfare implications of avian osteoporosis. Poultry Science, 83: 184-
192.
WEITZENBÜRGER, D., VITS, A., HAMANN, H. & DISTL, O. (2006) Evaluation of small group
housing systems and furnished cages concerning keel bone deformities, plumage condition,
claw length and body weight in layer strains Lohmann Selected Leghorn and Lohmann
Brown. Archiv für Tierzucht, 49: 89-102.
WHITEHEAD, C.C. & FLEMING, R.H. (2000) Osteoporosis in cage layers. Poultry Science, 79:
1033-1041.
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Chapter IV: Influence of different perch positions on bone strength and keel bone status
Figure 1. Perch positions of the small group system Eurovent 625a-EU (SG 40-60)
NE
4
3 2 1
1. central tube for supply of dust bathing substrate 2. back perch 3. front perch 4. nipple drinker
FE ST BE NE: perches not elevated; FE: front perch elevated; ST: perches in a stepped position; BE: back perch elevated; non-elevated perches were made out of white plastics; surfaces of elevated perches were made out of galvanised zinc. Table 1. Number of compartments, number of hens per treatment and percentage of perch positions tested by housing system FC SG 20-30 SG 40-60 Perch configuration NE NE BE FE NE BE - Trial 1 Number of compartments 36 20 4 8 16 7 - Number of hens per treatment 96 56 16 24 64 32 - Percentage of perch positions 100 58 17 25 67 33 - NE NE BE FE ST BE FE Trial 2 Number of compartments 36 14 4 6 8 8 8 Number of hens per treatment 96 56 16 24 32 32 32 Percentage of perch positions 100 58 17 25 33 33 33 NE: perches not elevated; FE: front perch elevated; ST: perches in a stepped position; BE: back perch elevated.
Table 2. Overall probability level (p) of the effects housing system (SYS), perch position within housing system and layer line (PP(SYS*LIN)) and group size (GR(SYS)) for humerus and tibia bone strength and keel bone status Humerus Tibia Keel bone Humerus Tibia Keel bone Trial 1 Trial 2 SYS 0.20 0.41 0.98
*** * 0.16
PP(SYS*LIN) 0.71 0.29 0.86 0.14 0.17 0.83 GR(SYS) 0.22 * 0.54 0.88 0.54 0.28 T1: Trial 1; T2: Trial 2; *: p ≤ 0.05; ***: p ≤ 0.001.
62
Chapter IV: Influence of different perch positions on bone strength and keel bone status
Table 3. LS-means (LSM), their standard errors (SE) and significant differences between housing systems for humerus and tibia bone strength [N] and keel bone status
FC (I) SG 20-30 (II) SG 40-60 (III) I-II I-III II-IIITrait LSM SE LSM SE LSM SE p p p
Trial 1 Humerus LSL 159.1 7.1 172.3 7.8 172.8 7.4 0.16 0.13 0.96 Humerus LB 226.7 7.1 235.7 7.6 230.1 6.7 0.34 0.71 0.57 Tibia LSL 136.5 4.4 141.5 4.8 140.2 4.6 0.39 0.51 0.84 Tibia LB 135.2 4.4 139.7 4.7 140.3 4.2 0.43 0.37 0.93 Keel bone LSL 3.39 0.1 3.47 0.1 3.44 0.1 0.59 0.71 0.86 Keel bone LB 3.59 0.1 3.47 0.1 3.52 0.1 0.42 0.62 0.76
Trial 2 Humerus LSL 171.0 3.6 183.7 4.2 191.7 3.6 * *** 0.15 Tibia LSL 137.6 2.4 147.1 2.8 145.6 2.4 * * 0.68 Keel bone LSL 3.55 0.1 3.66 0.1 3.48 0.1 0.22 0.47 0.058*: p ≤ 0.05; ***: p ≤ 0.001.
Table 4. LS-means (LSM), their standard errors (SE) and significant differences between perch positions of SG 40-60 for humerus and tibia bone strength [N] and keel bone status
BE (I) ST (II) FE (III) NE (IV) I-IV Trait LSM SE - - LSM SE p
Trial 1 Humerus LSL 168.0 11.2 - - 177.5 8.4 0.47 Humerus LB 220.1 10.7 - - 240.1 7.8 0.13 Tibia LSL 138.7 7.1 - - 141.8 5.2 0.71 Tibia LB 143.1 6.7 - - 137.5 4.9 0.50 Keel bone LSL 3.48 0.18 - - 3.41 0.14 0.74 Keel bone LB 3.51 0.17 - - 3.52 0.13 0.98
BE (I) ST (II) FE (III) I-II I-III II-IIITrait LSM SE LSM SE LSM SE p p p
Trial 2 Humerus LSL 199.4 6.3 178.4 6.3 197.3 6.3 * 0.81 * Tibia LSL 147.9 4.2 146.3 4.2 142.6 4.2 0.79 0.37 0.53 Keel bone LSL 3.40 0.1 3.51 0.1 3.54 0.1 0.67 0.81 0.82 BE: Back perch elevated; ST: stepped position; FE: front perch elevated; NE: perches not elevated; *: p ≤ 0.05.
63
Chapter IV: Influence of different perch positions on bone strength and keel bone status
64
Table 5. LS-means (LSM), their standard errors (SE) and significant differences between perch positions of SG 20-30 for humerus and tibia bone strength [N] and keel bone status
NE (I) BE (II) FE (III) I-II I-III II-IIITrait LSM SE LSM SE LSM SE p p p
Trial 1 Humerus LSL 179.0 8.9 167.8 15.5 170.0 2.6 0.52 0.54 0.91 Humerus LB 234.0 8.4 242.3 15.7 230.7 2.5 0.63 0.82 0.56 Tibia LSL 151.1 5.5 142.2 9.7 131.2 7.8 0.41 * 0.37 Tibia LB 134.8 5.2 136.5 9.8 147.8 7.8 0.87 0.16 0.36 Keel bone LSL 3.29 0.1 3.72 0.3 3.39 0.2 0.12 0.67 0.30 Keel bone LB 3.45 0.1 3.48 0.3 3.48 0.2 0.91 0.92 0.98
Trial 2 Humerus LSL 183.3 4.8 181.3 8.9 186.4 7.3 0.84 0.72 0.67 Tibia LSL 142.0 3.2 143.8 5.9 155.5 4.8 0.80 * 0.12 Keel bone LSL 3.70 0.1 3.59 0.2 3.70 0.1 0.51 0.98 0.55 NE: perches not elevated: BE: back perch elevated; FE: front perch elevated; *: p ≤ 0.05.
Table 6. LS-means (LSM), their standard errors (SE) and significant differences between group sizes within housing system for humerus and tibia bone strength [N] and keel bone status
FC SG 20-30 SG 40-60 Trait 10 20 p 20 30 p 40 60 p
Trial 1 Humerus LSL 158.7
± 9.5 159.4 ± 9.3
0.96 175.6 ± 10.3
169.0 ± 9.6
0.60 176.7 ± 9.6
168.8 ± 9.7
0.52
Humerus LB 219.6 ± 9.3
233.7 ± 9.5
0.26 248.5 ± 9.6
222.8 ± 10.1
* 220.5 ± 9.2
239.8 ± 9.0
0.12
Tibia LSL 142.1 ± 5.8
130.9 ± 5.8
0.14 145.7 ± 6.4
137.2 ± 6.0
0.28 139.4 ± 6.0
141.0 ± 6.1
0.84
Tibia LB 133.1 ± 5.7
137.3 ± 5.9
0.58 150.0 ± 6.0
129.4 ± 6.2
** 135.1 ± 5.7
145.5 ± 5.7
0.18
Keel bone LSL 3.3 ± 0.2
3.5 ± 0.2
0.39 3.3 ± 0.2
3.6 ± 0.2
0.19 3.4 ± 0.2
3.5 ± 0.2
0.67
Keel bone LB 3.6 ± 0.2
3.6 ± 0.2
0.97 3.5 ± 0.2
3.5 ± 0.2
0.99 3.4 ± 0.1
3.6 ± 0.1
0.37
Trial 2 Humerus LSL 171.1
± 4.9 171.0 ± 5.1
0.98 180.7 ± 5.5
186.6 ± 5.5
0.42 191.6 ± 5.1
191.8 ± 5.1
0.98
Tibia LSL 139.2 ± 3.4
136.0 ± 3.4
0.50 145.9 ± 3.7
148.2 ± 3.6
0.63 142.6 ± 3.4
148.5 ± 3.4
0.22
Keel bone LSL 3.5 ± 0.1
3.6 ± 0.1
0.32 3.6 ± 0.1
3.7 ± 0.1
0.16 3.4 ± 0.1
3.5 ± 0.1
0.34
*: p ≤ 0.05; **: p ≤ 0.01.
Chapter V
Effect of housing system, group size and perch position on H/L-
ratio in laying hens
B. Scholz, S. Rönchen, H. Hamann, H. Pendl and O. Distl
Archiv für Geflügelkunde
Chapter V: Stress perception in laying hens
H/L-ratio in laying hens
Effect of housing system, group size and perch position on H/L-ratio in laying hens
Einfluss von Haltungssystem, Gruppengröße und Sitzstangenposition auf den H/L-Ratio
bei Legehennen
BRITTA SCHOLZ1, SWAANTJE RÖNCHEN1, H. HAMANN1, HELENE PENDL2 and O. DISTL1
1 Institute of Animal Breeding and Genetics, University of Veterinary Medicine Hannover, Hannover, Germany
2 PendLab, Avian Diagnostic Microscopy, Steinhausen, Switzerland
66
Chapter V: Stress perception in laying hens
Introduction
Due to the EU Council directive 1999/74/EC on laying down minimum standards for the
protection of laying hens, major changes in laying hen husbandry will occur in the near
future. Conventional cages will have to be replaced by furnished cages or small group
housing systems by the end of 2011 in all European countries. Furthermore, the German
government has banned the use of furnished cages after 2011 and has only recently approved
a small group housing system with elevated perch positions as an adequate substitute together
with other alternative housing systems. Compartments of the small group housing system are
equipped with perches at 2 different heights and provide space to house 40 or more hens.
These systems are supposed to combine increased animal welfare with high hygienic and
economic standards that are related to cage keeping systems. The level of stress which is
experienced by laying hens throughout the laying period is an important welfare criterion,
which not only affects layers’ health and resistance against diseases but also impacts
production performance (AL-MURRANY et al., 2006). A well recognized parameter to measure
the amount of stress imposed on layers is the heterophil to lymphocyte (H/L) ratio, which was
described by GROSS and SIEGEL (1983). An increased H/L ratio in response to stressors
reflects a reliable measure of the bird’s perception of environmental stress. Only very few
data exists on the effect of housing system or cage design on the H/L ratio in laying hens.
CAMPO et al. (2005) found a significant decrease of the H/L ratio in hens kept in cages
equipped with perches compared to those without. In a study by ELSTON et al. (2000) the cage
type preference (solid vs open cages) for layers was analysed and a decrease in the H/L ratio
in open cages, which were preferred by hens, was found. These findings provide evidence that
housing systems and particularly cage designs which meet layers’ needs can very well reduce
the level of chronic stress in hens. The purpose of the present investigation was to compare
the H/L ratio of laying hens kept under identical management and feeding conditions in 3
different housing systems (small group housing system with elevated perches, furnished
cages, aviary housing system) and for the first time to analyse the degree of stress imposed on
layers by the different housing environments in a direct comparison. Also, the effect of
different group sizes and perch positions on the H/L ratio of layers kept in small group
housing systems was tested. Perch positions and group sizes are strongly discussed
parameters in the current development of the small group housing system.
67
Chapter V: Stress perception in laying hens
Materials and Methods
Housing Systems
The 3 housing systems examined (provided by Big Dutchman, Vechta, Germany) were
established in parallel position to each other in 3 different rooms of the same experimental
building. The small group housing system Eurovent (EV) 625a-EU consisted of a three-tier
block of compartments without centre partitions. Pens were separated by solid side partitions
and comprised group sizes of 40 and 60 layers to equal shares. Compartments of EV were
evenly distributed over the 3 levels of the system. The floor space provided was 2,412 x 1,250
mm (40 hens) and 3,618 x 1,250 mm (60 hens) respectively. Four perches per compartment
were installed in parallel position to the length of each compartment, offering each laying hen
15 cm perching space. Perches were either installed with the back perches being elevated
(BE) or both front and back perches being heightened and incorporated in a stepped position
(ST). The central tube for the automatic distribution of dust bathing substrate served as
additional perching space. The furnished cage system Aviplus was implemented as a three-
tier block of double-sided cages with solid side and rear partitions. Compartments comprised
group sizes of 10 layers (bottom tier, 1,206 x 625 mm floor space), 20 layers (medium tier,
2,412 x 625 mm) and 30 layers (top tier, 3,618 x 625 mm). Each compartment contained 2
parallel perches, which were installed on an even level. EV and Aviplus system were
equipped with nest boxes, dust baths, devices to shorten claws and provided layers with a
cage surface area of 750 cm² per hen. The EU legislative standards on keeping laying hens
(EU directive 1999/74/EG) were fully met. The aviary housing system (model “Natura”) was
equipped with a three-tier central block within a fully littered indoor floor space. It was
divided into 2 compartments, which were located within the same room (floor space per pen:
3,650 x 15,980 mm). Each compartment contained 1,250 laying hens and had direct access to
a separate, covered outdoor area. The 2 separate outdoor areas contained litter and were
provided with occupational material (hay) once a day (floor space per outdoor area: 3,400 x
20,980 mm). The aviary system was equipped with family nest boxes, which were attached on
the walls opposite the central block. Nest boxes were connected via footboards with the
medium level of the system. Furthermore, perches were installed in front of the second and
above the top level.
Trial Period, Layer Strain and Management
The experimental trial investigated started in September 2005 and ended in September 2006.
A total number of 5,500 floor-reared Lohmann Silver laying hens was transferred to the
68
Chapter V: Stress perception in laying hens
particular housing system at the age of 18 weeks. Hens were reared within the same flock,
thus ensuring fully identical rearing conditions. Hens were subjected to fully identical
management and feeding conditions. A commonly accepted immunisation scheme for laying
hens was employed throughout the rearing and laying period. Hens received a common two-
phase layer diet, which was automatically provided via food chains 3 to 4 times per day. Food
components were analyzed in regular intervals. The nutritional value averaged out at 10.9 MJ
ME, 16.5% crude protein, 3.89% calcium and 0.48% total phosphorus. Water was supplied ad
libitum from nipple drinkers. Hens in all 3 housing systems tested were given 14 hours of
artificial light per day (20 lux). The light scheme in the indoor part of the aviary system was
adapted to seasonal daylight fluctuations and the beginning of the light period varied from
5am (3rd laying month) up to 7.15am (12th laying month). Access to the outdoor areas was
only provided within the 14 hours light period. In the 8th laying month, 3 treatments against
the red mite (Dermanyssus gallinae) with Intermitox (Propoxur) were conducted in all 3
housing systems tested within a period of 13 days.
Evaluation of White Blood Cell Numbers and Heterophil to Lymphocyte (H/L) Ratio
In the 3rd, 6th, 9th and 12th laying month approximately 36 laying hens were randomly
chosen from each housing system, considering group sizes and perch position (small group
housing system) to equal parts (430 hens in total). In EV 625a-EU, 4 compartment variants
related to the different group sizes and perch positions (60 hens, BE, ST and 40 hens BE, ST)
with 2 replicates each per tier were tested. In Aviplus, compartments tested had 8 replicates
(top tier), 12 replicates (medium tier) and 24 replicates (bottom tier). Hens were carried to a
separate room and blood was immediately taken from a wing vein. At least 2 blood smears
per hen were prepared within 30 minutes following blood sampling. Blood smears were fixed
in methanol (70 %) and stained using Wright-Giemsa stains. An average number of 480
leucocytes, including heterophils, lymphocytes, monocytes, eosinophils and basophils was
counted on each slide and proportions of white blood cells were calculated. The H/L ratio was
calculated by dividing the relative numbers of heterophils by the relative numbers of
lymphocytes. In addition, hematocrit and layers’ body weight were measured.
Statistical Analysis
Statistical analysis was carried out using the procedure MIXED of SAS, version 9.1.3.
(Statistical Analysis System Institute Inc., Cary, NC, USA, 2006). According to Dixon and
Tukey (1968), a total of six outlier observations for the H/L ratio, which were located at both
69
Chapter V: Stress perception in laying hens
tails of the distribution, were identified and removed from the data set. After logarithmic
transformation of observed data values, Shapiro-Wilk and Kolmogorov-Smirnow test proved
data to be normally distributed (PROC UNIVARIATE). In the statistical model, housing
system (SYS), group size and perch position (EV) within housing system GR_PP(SYS),
laying month (MON) and the interaction between housing system and laying month
(SYS*MON) were included as fixed effects. Additionally, the interaction
MON*GR_PP(SYS) was included in an extended model to show the differences between
housing systems in the course of the H/L ratio during the laying period. The interaction
between individual compartment within housing system and laying month
(comp(SYS)*MON) was used as randomly distributed effect. Body weight (BW) within
laying month was employed as a covariate. F-test was conducted to test the significance of the
effects in the statistical model. Results of variance analysis were regarded significant when
the error probability was less than 5 % (P < 0.05).
Log-Yijklmn = µ + SYSi + GR_PP(SYS)ij + MONk + SYS*MONik + comp(SYS)*MONikl + b x
BW(MON)km + eijklmn
Log-Yijklmn h/l-ratio or relative proportion of leucocytes
μ model constant
SYSi fixed effect of housing system (i = 1 to 3)
GR_PP(SYS)ij fixed effect of group size and perch position (EV) within housing
system (ij = 1 to 8)
MONk fixed effect of laying month (k = 1 to 4)
SYS*MONik fixed effect of housing system and laying month (ik = 1 to 12)
comp(SYS)*MONikl randomly distributed effect of interaction between individual
compartment within housing system and laying month
b linear regression coefficient
BW(MON)km body weight of layers within laying month
eijklmn random error variation
Results
H/L-ratio and relative numbers of heterophils significantly differed among the 3 different
housing systems tested (Table 1). H/L-ratio was significantly lower in hens kept in the small
group system compared to layers housed in furnished cages. Hens in Aviplus had higher H/L-
ratios compared to the aviary system, although differences were not significant (P = 0.075).
70
Chapter V: Stress perception in laying hens
No differences in H/L-ratio could be detected between layers housed in the aviary system and
EV. Relative numbers of heterophils were significantly higher in hens kept in Aviplus
compared to EV and aviary system, whereas no difference was detected between EV and
aviary system. The corresponding relative number of lymphocytes did not differ among the 3
different housing systems tested. With relation to the different group sizes and perch positions
tested, H/L-ratio was found to be lowest in layers kept in compartments of 40 hens and
perches incorporated in the BE position (EV) and significantly differed from hens kept in
groups of 10, 20 and 30 hens (Aviplus) and from layers kept in compartments of 40 and 60
hens with perches incorporated in the ST position (EV) (Table 1). Furthermore, H/L-ratio in
hens kept in compartments of 40 layers with perches in the BE position was significantly
lower (P = 0.046) compared to hens kept in the aviary system, when the interaction
MON*GR_PP(SYS) was included in the extended statistical model. No differences in H/L-
ratio were found among the different group sizes of layers kept in Aviplus. In EV,
compartments of 40 and 60 layers with perches incorporated in the BE position did not differ
in H/L-ratio and no differences were found between the 2 group sizes and perches installed in
the ST position. H/L-ratio significantly increased from laying month 3 to 12 and 9 to 12. In
the 9th laying month, hens reflected the lowest H/L-ratio of all 4 laying months tested.
Relative numbers of heterophils significantly increased and relative numbers of lymphocytes
significantly decreased from the 3rd to the 12th laying month (Table 1). It was interesting to
note that relative number of eosinophils was highest in layers kept in Aviplus and aviary
system and significantly differed from hens housed in EV. In addition, relative numbers of
eosinophils were significantly lower in compartments of 40 layers with perches in the BE
position compared to layers kept in the aviary system, in the different groups of Aviplus (10,
20, 30 hens) and in compartments of 60 hens with perches incorporated in the BE position.
Discussion
Hens kept in EV showed significantly lower H/L-ratios compared to layers housed in Aviplus.
Layers in EV manifested significant heteropenia and corresponding non-significant
lymphophilia. These results provided evidence that keeping layers in the small group housing
system with elevated perches imposed less environmental stress on hens compared to the
furnished cage system. In contrast to BARNETT et al. (1997a), ELSTON et al. (2000) described
higher H/L-ratios in layers kept in solid-sided cages compared to open-sided cages and traced
these findings back to a possible preference of layers to experience greater visual access to
their surroundings. In both the Aviplus and EV system, compartments were separated by solid
71
Chapter V: Stress perception in laying hens
side partitions. As compartments of Aviplus were also equipped with solid centre partitions,
this could have contributed to an increased level of stress as visual access was limited. The
level of stress experienced by hens kept in EV (H/L-ratio: 0.269) was comparable to layers
kept in the aviary system (H/L-ratios: 0.267). So far, data on H/L-ratios of layers kept in
aviary systems is very rare. NICOL et al. (2006) analyzed the effect of flock size and stocking
density in a single-tier aviary system but could not detect clear effects on the H/L ratio
between the different treatments, except an increase in H/L-ratio towards the end of the laying
period. As the H/L-ratio is a highly heritable trait (AL MURRANI et al., 1997) and NICOL et al.
(2006) used a different layer line in their investigation, data on H/L-ratio values are not
comparable with the present study. Differences in H/L-ratio between layers kept in Aviplus
and aviary system nearly reached a significant level with hens kept in the furnished cage
system experiencing increased levels of stress. A reduced level of stress in layers kept in the
aviary system compared to Aviplus had been expected, but it was a rather unexpected finding
that differences between EV and Aviplus occurred to an even greater extent. Hens in the
aviary system were provided with occupational material and were given access to a littered
outdoor-area. Increased opportunities to perform natural behavioral traits are certainly an
explanation for less perception of stress. The impact of occupational material was studied by
EL-LETHEY et al. (2000) who detected a reduced H/L ratio in hens kept with straw. The effect
of group size on H/L-ratio was significant between compartments of 10, 20, 30 hens (Aviplus)
and 40 layers (perch position BE, EV) with hens in the smaller pens and not-elevated perches
experiencing a higher stress exposure. KEELING et al. (2003) suggested that hierarchical social
structures in small groups, which bear the potential of social conflicts, break down in larger
groups so that birds develop a tolerant social system. A group of 40 hens might be large
enough to develop non-aggressive social behaviour. Layers kept in compartments of 60 hens
(perch position BE) also showed lower H/L-ratio (0.26) compared to the smaller group sizes
of Aviplus (0.32, 0.30, 0.31), although differences did not achieve a significant level. Apart
from the group size, the different perch positions tested in EV seemed to have a significant
effect on layers’ stress perception. Hens kept in groups of 40 and 60 layers with perches in the
ST position did not differ in H/L-ratios compared to the smaller group sizes of Aviplus.
Perches incorporated in the BE position in groups of 40 hens were found to reduce levels of
stress compared to groups of 40 and 60 hens with perches in the ST position and compared to
hens kept in groups of Aviplus. A possible explanation could be that hens were given
opportunities to perch more secludedly in the back of the compartments, which might have
been favourable. Perches incorporated in the ST position could have led to increased
72
Chapter V: Stress perception in laying hens
accidental collisions with perches as elevated front and back perches might have been
hindering in layers’ movements. Accidental collisions with perches as a result of social
disruptions could have increased the level of stress due to pain experience. BARNETT et al.
(1997b) analysed H/L-ratios in hens kept in cages equipped with perches and those without
and could not prove any differences, whereas CAMPO et al. (2005) found hens being less
stressed and reflecting lower H/L-ratios when perches were provided compared to cages
without perches. The perch position seemed to play an important role in reducing layers’
stress perception particularly towards the end of the laying period and elevated perches in the
BE variant seemed to prevent best the increase of the H/L ratio in the second half of the
laying period. Generally, hens in groups of 40 (BE, EV) showed lower stress perception in the
second half of the trial period compared to Aviplus and aviary system. Significant differences
between EV (group size 40, BE) and the aviary system were primarily caused by the increase
of the H/L ratio in hens kept in the aviary system towards the end of the laying period. DAVIS
et al. (2000) also described an increase in H/L-value with age related to the egg production
cycle and NICOL et al. (2006) found an increase in H/L-ratio by the end of the lay in hens kept
in single-tier aviaries due to poorer welfare status of layers. Treatment against the red mite
(Dermanyssus gallinae) in the 8th laying month could have contributed to a lower H/L-ratio
in the 9th laying month compared to laying month 6 provided that the infestation had
contributed to stress exposure. Hematocrit of layers did not differ among the different housing
systems and group sizes, suggesting that infestation with the red mite did not accumulate in
any of the systems or group sizes tested. Small group housing systems with elevated perches
are supposed to combine the needs of high hygienic standards that are related to systems
which are well protected from outside environmental influences and improved animal
welfare. Interestingly, we found a significantly lower number of eosinophils in hens kept in
EV compared to the aviary system, which could be an indicator of a generally lower parasitic
exposure as hens in the EV did not have any outdoor access. As hens in Aviplus and EV were
equally protected from external influences, the higher relative number of eosinophils in
Aviplus compared to EV was difficult to explain. Hens in groups of 10, 20 and 30 layers of
Aviplus might have been subjected to increased dust exposure as the smaller compartment
sizes could have led to less air ventilation compared to the larger group sizes of EV. One of
the reasons for increased relative numbers of eosinophils in layers kept in Aviplus might be
due to allergic reactions as a response to dust exposure.
The findings of the current investigation showed that stress levels in layers were strongly
influenced by different housing environments, group sizes, perch positions and laying month.
73
Chapter V: Stress perception in laying hens
The greatest perception of stress was experienced by layers kept in the furnished cage system.
Keeping laying hens in the small group housing system in groups of 40 layers together with
the back perches being incorporated in an elevated position indicated to impose the least
environmental stress on hens among the different housing environments tested.
Summary
The objective of the present study was to assess the level of stress imposed on Lohmann
Silver laying hens kept in a small group housing system with elevated perches (Eurovent (EV)
625a-EU, group sizes 40, 60 hens, 4 perches with 2 different heights) compared to furnished
cages (Aviplus, group sizes 10, 20, 30 hens) and an aviary housing system (Natura, 2 pens,
1,250 hens) under identical management and feeding conditions. Each 2 perches within
compartments of EV were either incorporated in a stepped position (ST, front and back
perches heightened) or with only the back perches being elevated (BE). In the 3rd, 6th, 9th
and 12th laying month, approximately 36 hens were randomly chosen from each housing
system (430 hens in total) and heterophil to lymphocyte (H/L) ratio was determined. Laying
hens kept in EV had significantly lower H/L ratio compared to hens housed in Aviplus,
whereas no difference was detected between EV and aviary system. Hens kept in groups of 40
layers in compartments with perches in the BE position showed significantly lower H/L-ratios
compared to hens kept in groups of 10, 20, 30 layers (Aviplus) and groups of 40 and 60 hens
with perches incorporated in the ST position. Differences between group size 40 (BE) and the
aviary system nearly achieved the significance level (P = 0.054). Hens kept in furnished cages
reflected the greatest stress exposure. Group sizes of 40 hens together with elevated back
perches were associated with lowest levels of H/L ratios and these ratios were even lower
than in hens kept in the aviary system. Keeping hens in groups of 40 layers together with
perches incorporated in the BE position indicated to be most favourable in terms of imposing
the least environmental stress on layers.
Key words H/L-ratio, stress, furnished cages, small group system with elevated perches,
laying hens
Zusammenfassung
Das Ziel dieser Studie war es, erstmalig die Stressbelastung bei LS Hybriden in
Kleingruppenhaltung mit erhöhten Sitzstangenpositionen (EV 625a-EU, Gruppengrößen 40
und 60 Hennen, hintere Sitzstangen erhöht (HH), vordere und hintere Sitzstangen erhöht und
74
Chapter V: Stress perception in laying hens
stufig installiert (ST)), ausgestalteten Käfigen (Aviplus, Gruppengrößen 10, 20 und 30
Hennen) und einer Volierenhaltung (Natura, zwei Großgruppen zu je 1,250 Hennen) unter
identischen Managementbedingungen anhand des H/L-Ratios vergleichend zu ermitteln. Am
Ende des 3., 6., 9. und 12. Legemonats wurden jeweils 36 Hennen pro Haltungssystem
zufällig entnommen (insgesamt 430 Hennen) und eine Bestimmung des H/L-Ratios
durchgeführt. Hennen aus Aviplus wiesen einen im Vergleich zur Kleingruppe signifikant
höheren und im Vergleich zur Voliere annähernd signifikant höheren (P = 0,075) H/L-Ratio
auf. Zwischen Tieren aus Volierenhaltung und Kleingruppe hingegen konnte kein
Unterschied im H/L-Ratio festgestellt werden. Hennen aus Kleingruppen (40 Tiere, HH
Variante) zeigten einen signifikant niedrigeren H/L-Ratio im Vergleich zu Hennen aus
Kleingruppen (ST Variante) und zu Hennen aus ausgestalteten Käfigen (10, 20 und 30 Tiere).
Die Unterschiede im H/L-Ration von Tieren aus der Kleingruppe (40 Hennen, Variante HH)
im Vergleich zum Volierenhaltungssystem erreichten annähernd Signifikanz (P = 0,054). Bei
einer Erweiterung des statistischen Modells wiesen Hennen aus der Kleingruppe
(Gruppengröße 40, Variante HH) gegen Ende der Legeperiode einen signifikant niedrigeren
H/L-Ratio auf als Tiere aus Volierenhaltung. In allen drei Haltungssystemen wurde ein
signifikanter Anstieg des H/L-Ratios vom 3. zum 12. Legemonat festgestellt. Hennen aus
Kleingruppen (Gruppengröße 40, Variante HH) zeigten insbesondere gegen Ende der
Legeperiode einen geringeren H/L-Ratio. Die Sitzstangenvariante HH (40 Hennen) schien
einen sehr positiven Einfluss auf eine ungestörte Sitzstangennutzung auszuüben und der in
diesem Haltungssystem gemessene niedrigere H/L-Ratio deutet auf eine geringere
Stressbelastung hin.
Stichworte H/L-Ratio, Stress, ausgestalteter Käfig, Kleingruppenhaltung mit erhöhten
Sitzstangen, Legehennen
75
Chapter V: Stress perception in laying hens
References
AL-MURRANI, W. K., A. KASSAB, H. Z. AL-SAM and A. M. AL-ATHARI, 1997:
Heterophil/lymphocyte ratio as a selection criterion for heat resistance in domestic fowls.
Br. Poult. Sci. 38, 159-163.
AL-MURRANI, W. K., A. J. AL-RAWI, M. F. AL-HADITHI and B. AL-TIKRITI, 2006: Association
between heterophil/lymphocyte ratio, a marker of ‘resistance’ to stress and some
production and fitness traits in chickens. Br. Poult. Sci. 47, 443-448.
BARNETT, J. L., P. C. GLATZ, E. A. NEWMAN and G. M. CRONIN, 1997a: Effects of modifying
layer cages with solid sides on stress physiology, plumage, pecking and bone strength of
hens. Austr. J. Exp. Agric. 37, 11-18.
BARNETT, J. L., P. C. GLATZ, E. A. NEWMAN and G. M. CRONIN, 1997b: Effects of modifying
layer cages with perches on stress physiology, plumage, pecking and bone strength of hens.
Austr. J. Exp. Agric. 37, 523-529.
CAMPO, J. L., M. G. GIL, S. G. DÁVILA and I. MUÑOZ, 2005: Influence of perches and footpad
dermatitis on tonic immobility and heterophil to lymphocyte ratio of chickens. Poult. Sci.
84, 1004-1009.
DAVIS, G. S., K. E. ANDERSON and A. S. CARROLL, 2000: The effects of long-term caging and
molt of single comb white leghorn hens on heterophil to lymphocyte ratios, corticosterone
and thyroid hormones. Poult. Sci. 79, 514-518.
DIXON, W. J. and J. W. TUKEY, 1968: Approximate behavior of the distribution of Winsorized
t: Trimming/Winsorization II. Technometrics 10, 83.
EL-LETHEY, H., V. AERNI, T. W. JUNGI and B. WECHSLER, 2000: Stress and feather pecking in
laying hens in relation to housing conditions. Br. Poult. Sci. 41, 22-28.
ELSTON, J. J., M. BECK, M. A. ALODAN and V. VEGA-MURILLO, 2000: Laying hen behaviour
2. Cage type preference and heterophil to lymphocyte ratios. Poult. Sci. 79, 477-482.
GROSS, W. B. and H. S. SIEGEL, 1983: Evaluation of the heterophil/lymphocyte ratio as a
measure of stress in chickens. Avian Dis. 27, 972-979.
KEELING, L. J., I. ESTEVEZ, R. C. NEWBERRY and M. G. CORREIA, 2003: Production-related
traits of layers reared in different sized flocks: the concept of problematic intermediate
group sizes. Poult. Sci. 82, 1393-1396.
NICOL, C. J., S. N. BROWN, E. GLEN, S. J. POPE, F. J. SHORT, P. D. WARRISS, P. H. ZIMMERMAN
and L. J. WILKINS, 2006: Effects of stocking density, flock size and management on the
welfare of laying hens in single-tier aviaries. Br. Poult. Sci. 47, 135-146.
76
Chapter V: Stress perception in laying hens
SAS, 2006: Statistical Analysis System, Version 9.1.3, SAS Institute Inc., Cary, North
Carolina, USA.
Correspondence:
Ottmar Distl, Insitute of Animal Breeding and Genetics, University of Veterinary Medicine
Hannover, Bünteweg 17p, 30559 Hannover, Germany, Tel.: 0049-511-953-8875; Fax: 0049-
511-953-8582; e-mail: [email protected].
77
Chapter V: Stress perception in laying hens
Table 1. Logarithmized LS-Means (LSMlog), their standard errors (SElog), LSMlog re-
transformed (LSM), their 95% confidence intervals (CI95) and significant differences between
the different housing systems, group sizes, perch positions (Eurovent (EV) 625a-EU) and
laying months for H/L ratios and relative proportions of heterophils, lymphocytes and
eosinophils (%).
Logarithmierte LS-Mittelwerte (LSMlog), ihre Standardfehler (SElog), rücktransformierte LSMlog
(LSM), ihre 95% Konfidenzintervalle (CI95) und signifikante Unterschiede zwischen den
verschiedenen Haltungssystemen, Gruppengrößen, Sitzstangenpositionen (Eurovent (EV) 625a-
EU) und Legemonaten für den H/L-Ratio und prozentuale Anteile der heterophilen
Granulozyten, Lymphozyten und eosinophilen Granulozyten (%).
H/L ratio Heterophils (%) Lymphocytes (%) Eosinophils (%) Trait LSMlog SElog
LSM CI95
LSMlog SElog
LSM CI95
LSMlog SElog
LSM CI95
LSMlog SElog
LSM CI95
Housing systems Aviplus -1.18a
0.05 0.31
0.28-0.34 3.04a
0.04 21.0
19.5-22.54.22a 0.01
68.1 66.3-70.0
-0.04A 0.07
1.0 0.8-1.1
EV -1.31b 0.05
0.27 0.24-0.30
2.94b 0.04
18.9 17.5-20.3
4.25a 0.01
70.3 68.3-72.3
-0.32B 0.07
0.7 0.6-0.8
Aviary -1.32ab 0.06
0.27 0.24-0.30
2.93b
0.05 18.6
17.0-20.44.25a 0.02
69.8 67.4-72.3
-0.10a 0.08
0.9 0.8-1.1
Group sizes in Aviplus (10, 20, 30), EV (40-BE, 40-ST, 60-BE, 60-ST) and Aviary system 10
-1.15A 0.08
0.32 0.27-0.37
3.06A 0.06
21.3 18.9-23.9
4.21A 0.02
67.1 64.2-70.2
-0.02A 0.12
1.0 0.8-1.2
20
-1.21AB 0.08
0.30 0.25-0.35
3.03AB 0.06
20.6 18.3-23.3
4.24ab 0.02
69.5 66.3-72.7
0.04A 0.12
1.0 0.8-1.3
30
-1.17AB 0.09
0.31 0.26-0.37
3.05AB 0.06
21.0 18.6-23.8
4.22a 0.02
67.7 64.5-71.0
-0.13a 0.11
0.9 0.7-1.1
40-BE
-1.55C
0.10 0.21
0.17-0.26 2.75C 0.07
15.7 13.5-18.1
4.31B 0.03
74.1 70.0-78.4
-0.57B 0.14
0.6 0.4-0.7
40-ST
-1.21a 0.10
0.30 0.25-0.36
3.02A 0.07
20.5 17.7-23.7
4.23ab 0.03
68.6 64.9-72.5
-0.24ab 0.13
0.8 0.6-1.0
60-BE -1.34ac 0.10
0.26 0.21-0.32
2.92ac 0.07
18.6 16.1-21.6
4.26ab 0.03
70.9 67.0-75.0
-0.15ac 0.14
0.9 0.7-1.1
60-ST -1.16A 0.10
0.31 0.26-0.38
3.05A 0.07
21.2 18.3-24.4
4.22a 0.03
67.7 64.1-71.6
-0.31ab 0.14
0.7 0.6-1.0
1,250 (Aviary)
-1.32ac 0.06
0.27 0.24-0.30
2.93a 0.05
18.6 17.0-20.4
4.25ab 0.02
69.8 67.4-72.3
-0.10A 0.08
0.9 0.8-1.1
Laying month 3
-1.31b 0.07
0.27 0.23-0.31
2.94b 0.05
19.0 17.1-21.0
4.26a 0.02
70.7 68.0-73.5
-0.36B 0.10
0.70 0.58-0.84
6
-1.25ab 0.06
0.29 0.25-0.32
2.98ab 0.05
19.6 17.9-21.5
4.23ab 0.02
68.9 66.5-71.3
-0.20ab 0.08
0.82 0.70-0.97
78
Chapter V: Stress perception in laying hens
79
Table 1 continued.
H/L ratio Heterophils (%) Lymphocytes (%) Eosinophils (%) Trait LSMlog
SElog LSM CI95
LSMlog SElog
LSM CI95
LSMlog SElog
LSM CI95
LSMlog SElog
LSM CI95
Laying month 9
-1.41B 0.06
0.24 0.22-0.28
2.85B 0.05
17.4 15.8-19.0
4.27a 0.02
71.3 68.8-73.9
-0.01A 0.09
0.99 0.83-1.17
12
-1.10aA 0.06
0.33 0.29-0.38
3.10aA 0.04
22.2 20.4-24.3
4.20b 0.02
66.8 64.6-69.1
-0.03a 0.08
0.97 0.83-1.13
ST: both perches heightened and in stepped position; BE: back perch elevated; means within a
column with no common supercscipts differ (lowercase superscripts: P < 0.05; uppercase
superscripts: P < 0.01).
ST: beide Sitzstangen erhöht, stufige Position; BE: hintere Sitzstange erhöht; LS-Mittelwerte
innerhalb einer Spalte ohne gemeinsamen Index unterscheiden sich signifikant
(Kleinbuchstabe: P < 0.05; Großbuchstabe: P < 0.01).
Chapter VI
Keel bone condition in laying hens: a histological evaluation of
macroscopically assessed keel bones
B. Scholz, S. Rönchen, H. Hamann, M. Hewicker-Trautwein and O. Distl
Berliner Münchener Tierärztliche Wochenschrift
Chapter VI: Histological evaluation of keel bone
Britta Scholz1, Swaantje Rönchen1, Henning Hamann1, Marion Hewicker-Trautwein2 and
Ottmar Distl1
1Institute for Animal Breeding and Genetics, 2Institute for Pathology, University of
Veterinary Medicine Hannover (Foundation), Hannover, Germany
Keel bone condition in laying hens: a histological evaluation of
macroscopically assessed keel bones Brustbeinstatus bei Legehennen: eine histologische Untersuchung makroskopisch beurteilter
Brustbeine
Running title: Histological evaluation of keel bone
Laufende Überschrift: Histologische Untersuchung des Brustbeins
Corresponding author: Ottmar Distl, Institute for Animal Breeding and Genetics, University
of Veterinary Medicine Hannover (Foundation), Bünteweg 17p, 30559 Hannover, Germany,
Tel.: +49 511 953 8875; Fax: +49 511 953 8582; E-mail: [email protected]
82
Chapter VI: Histological evaluation of keel bone
Summary
The objective of the present study was to conduct a corresponding histological analysis of 162
macroscopically assessed keel bones (1: severe, 2: moderate, 3: slight, 4: no deformity). Four
layer lines were used and hens were kept in furnished cages, small group systems (both
allowing more activities due to the provision of perches) and an aviary system, which fully
conformed to the EU standards. Investigations were carried out in the 3rd, 6th, 9th and 12th
laying month of two experimental trials. In 97.9 % of grade 4 keel bones, no histological
deviations were found, whereas in keel bones manifesting deformities of grade 1 and 2, the
predominant histological observation was the incidence of fracture callus material (FCM) and
new bone in the form of woven bone. FCM was also detected in 50.9 % of grade 3 keel bones,
whereas in 40.7 %, only s-shaped deviations of keel bones were found, which were related to
extended pressure loading while perching activities rather than short-duration trauma.
Histological analysis showed that keel bones of grade 1 and 2 were mainly attributed to
traumatic origin and therefore associated with pain experience in layers. Grade 3 keel bones
manifested either FCM as a result of trauma or adaptational deformities without any evidence
of a preceding fracture in response to mechanical pressure loading and were most likely not
associated with pain. Therefore, histological analysis was found to be a mandatory tool when
evaluating grade 3 keel bones with respect to layers’ welfare.
Key words: Keel bone condition, laying hen, histological evaluation, welfare
Zusammenfassung
Ziel dieser Studie war es, bei 162 makroskopisch beurteilten Brustbeinen (1 = hochgradig, 2 =
mittelgradig, 3 = geringgradig verändert, 4 = ohne besonderen Befund) von Legehennen, die
in mit Sitzstangen ausgestatteten, ausgestalteten Käfigen, Kleingruppen- und Volierenhaltung
gehalten wurden, eine überprüfende, histologische Untersuchung durchzuführen. Es wurden
vier Legelinien verwendet und die Untersuchungen erfolgten im 3., 6., 9. und 12. Legemonat.
In 97.9 % der mit Grad 4 beurteilten Brustbeine konnten auch histologisch keine
Abweichungen gefunden werden, während Brustbeine mit Deformationen von Grad 1 und 2
überwiegend Frakturkallus (FK) und Knochenneubildung (Geflechtknochen) aufwiesen. FK
wurde auch in 50.9 % der mit Grad 3 beurteilten Brustbeine gefunden, während 40.7 % nur s-
förmige Verbiegungen, vermutlich als Anpassungsreaktion des Knochens auf kontinuierliche,
mechanische Belastung während der Sitzstangennutzung, aufwiesen. Die histologische Studie
zeigte, dass deformierte Brustbeine von Grad 1 und 2 in erster Linie traumatischer Genese
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Chapter VI: Histological evaluation of keel bone
waren. Brustbeine von Grad 3 hingegen wiesen entweder traumatisch bedingten FK oder
lediglich Formänderungen in der Knochenstruktur auf, die vermutlich nicht akuter,
schmerzhafter Natur waren. Die makroskopische Beurteilung von geringgradig veränderten
Brustbeinen im Hinblick auf Wohlergehen, insbesondere Schmerzempfindung, bei Hennen
wurde ohne histologische Untersuchung als unzureichend angesehen.
Schlüsselwörter: Brustbeinstatus, Legehennen, histologische Beurteilung, Wohlergehen
Introduction
Increased awareness of laying hen welfare has led to major changes in policies on laying hen
husbandry. Due to the EU directive passed in 1999 (CEC, 1999) conventional cages have to
be replaced by furnished cages or alternative housing systems by the end of 2011 in all
European countries. As the German legislation has put through the abolition of furnished
cages after 2011, research on housing systems that are appropriate to layers is strongly
required. In the process of developing advanced husbandry systems, evaluation of layers’ keel
bone is an important criterion, which has been included in a variety of studies on welfare of
laying hens kept in a particular housing system. The provision of increased possibilities to
move is a major issue in newly-developed house keeping systems as movement is supposed to
strengthen layers’ skeleton, thus reducing the risk of osteoporosis. Keel bone of layers is not
only affected by general inactivity osteoporosis but is also very vulnerable to deformities and
fractures due to its exposed anatomical location. In a variety of ongoing studies on evaluating
keel bone condition of layers kept in different house keeping systems (Elson and Croxall,
2006; LayWel EU-project, 2006), only macroscopic findings on keel bone status have been
included. Applying macroscopic evaluation techniques on assessing keel bone, studies have
shown that keel bone condition is a widely-spread problem in laying hen husbandry. In a
study by Freire et al. (2003), 73 % of hens housed in an aviary system produced keel bone
deformities at the end of the laying period. Furnished cages with incorporated perches are
more likely to produce keel bone deformities in layers than conventional cages. Vits et al.
(2005) found keel bone deformities in 33% of hens kept in furnished cages, thus
demonstrating a prevalent welfare problem related to this type of housing system. A scoring
scheme for macroscopic evaluation of keel bone ranging from score 1 (severe deformity) to 4
(no deformity) has been used in a variety of investigations (Elson and Croxall, 2006; Vits et
al., 2005; Weitzenbürger et al., 2006). So far, no data exist on the severity code of keel bone
deformities (no deformity, slight, moderate, severe deformity) and the underlying histological
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Chapter VI: Histological evaluation of keel bone
findings of layers kept in housing systems which fully conformed to the EU legislative
standards on keeping laying hens. In a study by Fleming et al. (2004) fracture callus material
and development of new bone was detected in all cases of macroscopically deviated keel
bones in ISA, Hy-line and LSL White Leghorn hybrids kept in battery or free-range systems,
thus proving a traumatic cause. The aim of the present study was to analyse the histological
appearance of keel bone deformities representing the different macroscopically reported
severity codes. The study comprised four different commonly used layer lines (Lohmann
Silver, Lohmann Tradition, Lohmann Selected Leghorn, Lohmann Brown), which were kept
in furnished cages, small group systems and an aviary system.
Materials and Methods
Farms, housing systems and layer lines
The study was conducted over two experimental trials, each comprising a period of 12
months. Laying hens were kept in six different house keeping systems (Big Dutchman,
Vechta, Germany), which were located at two experimental farms. A three-tier, double-sided
furnished cage system (Aviplus, groups of 10, 20 and 30 layers, non-elevated perches), a
three-tier small group housing system (Eurovent (EV) 625a-EU (EVa), groups of 40 and 60
hens) and an aviary housing system with connected outdoor area (model Natura, three-tier
central block, 2 groups, 1,250 layers) were installed at farm A. In the first trial, layer lines
used were Lohmann Silver (LS) and Lohmann Tradition (LT). In the second trial, only LS
were used. Farm B contained two four-tier, double-sided furnished cage systems (Aviplus,
groups of 10 and 20 hens, non-elevated perches; EV 625A-EU (EVA), 20 and 30 layers) and
a four-tier small group housing system (EVa, 40 and 60 hens). Laying strains kept were
Lohmann Selected Leghorn (LSL) and Lohmann Brown (LB) in the first trial and LSL in the
second trial. A total number of approximately 5,500 hens (Farm A) and 9,000 layers (Farm B)
was kept per trial. All systems tested in the present study fully met the EU legislative
standards on keeping laying hens (EU directive 1999/74/EG). Compartments of Aviplus and
EV systems were equipped with perches, nest boxes, dust bathing areas, devices to shorten
claws and provided 750 cm² space/hen. Unlike the aviary system, Aviplus and EV systems
did not provide outdoor access. Perches within a certain percentage of EVa and EVA
compartments were incorporated at two different heights, thus meeting the legal requirements
on the currently approved small aviary system. In compartments of EVA, either back or front
perches were heightened, whereas in compartments of EVa, either back, front or both perches
were incorporated in an elevated position (Fig.1).
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Chapter VI: Histological evaluation of keel bone
Perch design
Perches in Aviplus and EV systems were made out of white, polished plastics (PVC, rigid)
and produced a thickness of 30 mm. They were oval shaped with a flattened top and
underside and provided a contact area of 20.1 mm for the layers’ feet. Front and back part
were formed in a convex shape. In EV 625a-EU systems, perches which were modified in
their height, were roundly shaped and made out of abraded, galvanised zinc.
Management and feeding
Hens were subjected to identical management and feeding conditions within each farm.
Layers of farm A (floor reared) and farm B (reared in cages) were transferred to the particular
farm and housing system at the age of 18 weeks. At both farms, a standard diet for laying
hens was provided. Analysis of food components was conducted in regular intervals in order
to monitor the nutritional value of the diet. Layers were subjected to a commonly accepted
prophylactic immunisation scheme for laying hens.
Macroscopic and histological examination of keel bone
On farm A, keel bone status was examined in the 3rd, 6th, 9th and 12th laying month of both
trials. Considering layer strain (first trial) and housing system to approximately equal parts, a
total number of 910 layers was randomly chosen and slaughtered. On farm B, keel bone status
was recorded in the 6th and 12th laying month and 576 hens were included in the study from
farm B (192 hens per each housing system). In total, 1,486 macroscopically examined keel
bones provided the pool for selecting samples for histological analysis. Keel bone of layers
was evaluated visually and per palpation alongside the keel after removal of the skin and its
macroscopic appearance was classified using the following scoring scheme: score 4 = no
deformity, score 3 = slight, score 2 = moderate and score 1 = severe deformity. In the first
trial, histological samples of keel bone were taken in laying month 6, 9, 12 (Farm A) and
laying month 6, 12 (Farm B). In the second trial, samples were taken in all 4 laying months
tested (Farm A) and in laying month 6 and 12 (Farm B). Samples were chosen to cover the
whole range of macroscopic findings on keel bone status to approximately equal parts.
Sampling did not consider layer strain or housing system. A total of 162 samples was taken
for histological analysis. Table 1 provides the numbers of histological samples taken for
analysis by severity code and the random distribution on housing system and layer line within
each farm. Keel bones were removed of breast muscle and tendons and with help of two
transversal cuts through corpus sterni, a 3 mm thick sample of keel bone was excised. The
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Chapter VI: Histological evaluation of keel bone
location of sampling unaltered keel bones was about 1 cm caudal of the pilae carinae and apex
sterni. Samples of keel bones exhibiting deformities were taken out of the particular area
affected. Tissue samples were fixed for at least 24 hours in formalin (10 %). After
decalcification in HNO3 (5 %) solution for 20 minutes, samples were dewatered and
incorporated into paraffin wax. Histological sections (2-3 µm) were produced using a rotation
microtom (Reichert-Jung 2030, Biocut) and stained with haematoxylin and eosin. Histological
sections were examined and categorised using the following scheme:
0: No evidence of fracture callus material or development of new bone (woven bone)
1: Periostal ectostosis appearing as a thin layer alongside the bone without evidence of a
preceding fracture
2: Appearance of new bone (woven bone) with the keel bone either showing a continous
compacta or a disordered integration of compacta and woven bone, suggesting a preceding
incidence of bone fracture
3: Fracture callus material (woven bone) as a result of bone fracture, still representing a clear
dislocation of bone fragments.
Statistical analysis
Fisher’s exact test (SAS, 2006) was performed in order to determine the significance of the
association between macroscopic scoring of keel bone and related histological findings.
Results
The results of histological findings related to the different severity codes of keel bone
deformities are presented in Table 2. Results of Fisher’s exact test showed significant
differences between macroscopic scoring and histological findings on keel bone (P < 0.001).
In 97.92 % of keel bones evaluated with score 4, pathological deviations in keel bone
structure could not be detected in corresponding histological analysis (Fig. 2a) and in only
one keel bone (2.08 %), development of periostal ectostosis (PE) appearing as a thin layer
alongside the cortical bone, was found (Fig. 3). In 40.68 % of slightly deformed keel bones
(Fig. 5) no evidence of fracture callus material (FCM) or development of new bone (woven
bone) could be observed, whereas deformities in shape without occurrence of new bone
(woven bone) were present (Fig. 2b). In 50.85 % of keel bones scored with 3, either FCM
together with clearly-defined dislocation of bone fragments (10.17 %) (Fig. 5) or appearance
of FCM and new bone, suggesting a preceding bone fracture (40.68 %) could be detected. In
8.47 % of slightly deformed keel bones, cortical bone was accompanied by PE. Histological
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Chapter VI: Histological evaluation of keel bone
analysis of keel bones evaluated with score 2 (Fig. 4) revealed new bone (woven bone) and
FCM in 80 % of keels. PE and keel bones without any development of new bone (woven
bone) or FCM were detected in 10 % of keel bones in each case. In all keel bones reflecting
severe deformities, appearance of new bone (73.33 %) or new bone together with FCM still
representing the dislocation of bone fragments, was found (26.67 %).
Discussion
Macroscopic evaluation of keel bone according to the applied scoring scheme from 1 to 4 was
found to be a reliable method related to keel bones reflecting either no deformities or modest
to severe deviations. In keel bones scored with 4, histological analysis mirrored very well the
macroscopic findings as the incidence of FCM and development of new bone (woven bone)
could not be observed. In very few cases, cortical bone was found to be extended and in one
keel bone, new bone in the form of PE, which appeared as a thin layer alongside the cortical
bone, was found. In contrast to mammals, birds preferably develop endosteal callus instead of
periostal callus after having stabilized bone lesions (Schmidt et al., 2003). Therefore, the
incidence of PE without visible endosteal callus formation most probably represented a
process of providing structural support to the cortical bone without a preceding bone fracture.
As it is generally known that skeletal tissue represents a very reactive tissue, bone formations
such as cortical bone broadening and thin PE are most probably physiological responses of
bone tissue to external mechanical forces. In contradiction to Fleming et al. (2004), FCM and
development of new bone could not be detected in all cases of macroscopically deformed keel
bones. Histological analysis of keel bones reflecting slight deformities either manifested the
incidence of FCM or did not provide any evidence of FCM or PE development and revealed
s-shaped deformities without any osteal proliferation in the form of new bone (woven bone).
These findings were detected in keel bones of all four laying strains tested, thus suggesting
that the different layer strains did not have an influence on these histological observations.
Laying hens investigated by Fleming et al. (2004) were either kept in battery cages with no
access to perches or in free range systems. Therefore, hens could not have experienced long-
term pressure on the keel bone due to extended perching activities and all kinds of deformed
keel bones observed by Fleming et al. (2004) were related to traumatic origin. In the present
study, histological keel bone analysis of hens kept in housing systems which allow more
activities was conducted for the first time and findings seemed to be strongly impacted by the
provision of perches. Keel bone tissue most probably adapted to extended pressure loading
resulting from frequent use of perches and s-shaped deformities were developed without
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Chapter VI: Histological evaluation of keel bone
incidence of bone fracture in 40.68 % of layers reflecting slight keel bone deformities and in
10 % of layers exhibiting moderate deformations. As the corpus sterni was found to be very
thin and therefore rather bendable in some layers, it was difficult to describe the extent of the
s-shaped deformities observed in histological analysis to a more precise extent. Keel bone in
all four layer strains supposedly differed in its consistency due to the hens’ age and degree of
keel bone calcification, with keel bones in younger hens being more flexible. This might have
contributed to a gradual adoption of deformities in layers’ keel bone shape as a response to
extended perching activities and pressure loading. Palmer (1993) described the final molding
of a bone’s shape being subservient to the demands of function and directed by pressure and
tension. As a result, abnormal stressors on a growing bone lead to changes in a bone’s shape.
Most observations of slightly deformed keel bones without evidence of FCM were detected in
laying month 12, thus showing that changes in the shape of keel bone seemed to be a
protracted process. Wahlström et al. (2001) made extended perching activities and the long-
term pressure on keel bone responsible for deformities occurring in hens kept in furnished
cages, but so far, histological proof on the nature of these deformities had not been provided.
Fleming et al. (2004) examined keel bones solely at the end of the lay (70 weeks) and found
evidence of FCM in all cases of keel bones reflecting less severe deviations. These results
supported the idea that the present histological findings on deformed keel bones without
evidence of FCM were closely related to the provision of perches and would not have
occurred if layers had been kept in conventional cages or free range systems. However, in
50.85 % of layers exhibiting slightly deformed keels, FCM was observed, thus reflecting a
traumatic origin. Gentle (2001) found evidence of complex pain perception in chickens and
traumatic fractures are strongly related to pain experience in layers. The incorporation of
perches, particularly perches installed at two different heights, could have born an increased
risk of accidental collision with keel bone and therefore led to the high incidence of keel bone
fractures observed in histological analysis, rather than the incidence of general osteoporosis.
In a study by Appleby et al. (1993), 43% of hens kept in furnished cages suffered from keel
bone alterations in comparison to 4% of their counterparts kept in conventional cages, thus
providing evidence of a high frequency of deformed keels in cages with perches. Fleming et
al. (2004) found keel bone fractures in hens kept without provision of perches and related
these findings to the onset of osteoporosis and therefore loss of bone with age. In the present
study, hens were kept in enriched housing systems which fully conformed to the EU
legislative standards on keeping laying hens and were therefore offered more possibilities to
move. Increased movement supposedly contributed to strengthen layers’ skeleton in general,
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Chapter VI: Histological evaluation of keel bone
which could have alleviated the incidence of osteoporosis in the present study and therefore
the occurrence of keel bone fractures to an even greater extent in slightly deformed keel
bones. As keel bone is very vulnerable due to its exposed anatomical location, lean shape and
mechanical pressure loading, both furnished and small group systems did not succeed in
strengthening layers’ skeleton to an extent that alterations in keel bone’s shape could be fully
prevented. However, a great part of deformities found in slightly deformed keel bones might
not have caused pain in layers due to its non-traumatic origin.
A number of 8 % of slightly and 10 % of moderately deformed keel bones exhibited PE,
which occurred as a thin layer alongside the cortical bone without evidence of a preceding
fracture. It was interesting to note, that PE mainly appeared in slight and moderate keel bone
deformities and were nearly solely found in LSL layers, except in one case of LB hybrid. LSL
layers are of a lighter body weight compared to the other laying strains used in the
investigation. Therefore, LSL layers might be genetically predisposed to develop these kinds
of bone proliferations more frequently in order to structurally support their keel bone. In
addition, 80 % of PE findings occurred in keel bones sampled in laying month 12 and 20 % of
PE findings resulted from keels sampled in laying month 6, thus suggesting an extended
period of time for these formations to develop. In 80 % of keel bones exhibiting moderate and
in all keel bones reflecting severe deformities, development of new bone (woven bone) or
FCM was detected. Keel bone deformities classified as ‘severe’ generally occurred to a less
extent compared to moderate or slight deviations. Samples for histological analysis were
randomly selected according to the macroscopic findings present in the particular laying
month and did not consider layer line or housing system. Most severely deformed keel bones
derived from hens kept in the aviary system and keels reflected FCM or woven bone in all
cases. Histological findings on severely deformed keel bones were therefore primarily related
to traumatic fractures due to flight and landing accidents in the aviary system or perch
collisions and inability to negotiate perches properly in the furnished cages and small group
systems.
The findings of the present study showed that histological analysis of keel bone well agreed to
the macroscopic evaluation related to the grades 4, 2 and 1. In approximately 40 % of slightly
deformed keel bones (grade 3), deviations without development of FCM were observed.
These findings seemed to be strongly related to mechanical pressure loading on the keel bone
due to extended perching activities in furnished and small group housing systems and most
probably did not result from short duration trauma. Unlike traumatic fractures, these bone
remodelling processes in keel bone might not necessarily have produced pain in layers. As
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Chapter VI: Histological evaluation of keel bone
approximately 50 % of slightly deformed keel bones showed clear incidence of FCM in
histological analysis, it was found impossible to draw a conclusion on slightly deformed keel
bones with respect to layers’ welfare without a corresponding histological analysis.
Acknowledgement
The authors would like to thank Big Dutchman GmbH, Lohmann Tierzucht GmbH and
Deutsche Frühstücksei GmbH for financial support of this scientific project.
References
Appleby, M., S.F. Smith, B.O. Hughes (1993): Nesting, dust bathing and perching by laying
hens in cages: effects of design on behaviour and welfare. Br. Poult. Sci. 34, 835-847.
CEC (1999) Richtlinie 1999/74/EG des Rates vom 19. Juli 1999 zur Festlegung von
Mindestanforderungen zum Schutz von Legehennen, ABl. EG Nr. L 203, 53.
Elson, H.A., R. Croxall (2006): European study on the comparative welfare of laying hens in
cage and non-cage systems. Arch. Geflügelk. 70, 194-198.
Fleming, R.H., H.A. McCormack, L. McTeir, C.C. Whitehead (2004): Incidence, pathology
and prevention of keel bone deformities in the laying hen. Br. Poult. Sci. 35, 651-662.
Freire, R., L.J. Wilkins, F. Short C.J. Nicol (2003): Behaviour and welfare of individual
laying hens in a non-cage system. Br. Poult. Sci. 44, 22-29.
Gentle, M.J. (2001): Attentional shifts alter pain perception in the chicken. Anim. Welf. 10,
187-194.
LayWel EU-project (2006): Welfare implications of changes in production systems for laying
hens: a European project. [Work package 3]. www.laywel.eu.
Palmer, N. (1993): Bones and joints. In Jubb, K.V.F., Kennedy, P.C., Palmer, N., eds.
Pathology of domestic animals. San Diego: Academic Press, 24-26.
SAS Institute (2006): Statistical Analysis System, Version 9.1.3, SAS Institute Inc., Cary,
NC, USA.
Schmidt, R.E., D.R. Reavill, D.N. Phalen, eds. (2003): Pathology of pet and aviary birds.
Ames: Iowa State Press 154.
Vits, A., D. Weitzenbürger, H. Hamann, O. Distl (2005): Production, egg quality, bone
strength, claw length and keel bone deformities of laying hens housed in furnished cages
with different group sizes. Poult. Sci. 84, 1511-1519.
Wahlström, A., R. Tauson, K. Elwinger (2001): Plumage condition and health of aviary-kept
hens fed mash or crumbled pellets. Poult. Sci. 80, 266-271.
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Chapter VI: Histological evaluation of keel bone
Weitzenbürger, D., A. Vits, H. Hamann, O. Distl (2006): Evaluierung von
Kleingruppenhaltungssystemen und ausgestalteten Käfigen hinsichtlich
Brustbeindeformationen, Gefiederstatus, Krallenlänge und Körpermasse bei den
Legelinien Lohmann Selected Leghorn und Lohmann Brown. Arch. Tierz. 46, 89-102.
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Chapter VI: Histological evaluation of keel bone
Table 1. Numbers of keel bone samples taken for histological analysis by macroscopic
severity code, farm, layer line and housing system
n No deformity Slight Moderate Severe Farm A 103 EVa-LS 32 10 13 9 0 EVa-LT 7 2 4 0 1 Aviplus-LS 23 10 9 2 2 Aviplus-LT 11 4 2 4 1 Aviary Natura-LS 27 3 10 8 6 Aviary Natura-LT 3 1 0 0 2 Farm B 59 EVa-LSL 20 5 5 10 0 EVa-LB 2 0 0 0 2 Aviplus-LSL 19 8 9 2 0 Aviplus-LB 7 3 2 2 0 EVA-LSL 6 1 3 2 0 EVA-LB 5 1 2 1 1 EVa = Eurovent 625a-EU; EVA = Eurovent 625A-EU; LS = Lohmann Silver; LT = Lohmann
Tradition; LSL = Lohmann Selected Leghorn; LB = Lohmann Brown
Table 2. Results of histological findings (%) related to macroscopic severity code of keel
bone deformity
Histological findings Macroscopic evaluation n 0 1 2 3 No deformity 48 97.92 2.08 0.00 0.00 Slight 59 40.68 8.47 40.68 10.17 Moderate 40 10.00 10.00 42.50 37.50 Severe 15 0.00 0.00 73.33 26.67 0: No evidence of fracture callus material or development of new bone (woven bone); 1:
Periostal ectostosis appearing as a thin layer alongside the bone without evidence of a
preceding fracture; 2: Appearance of new bone (woven bone) with the keel bone either
showing a continous compacta or a disordered integration of compacta and woven bone,
suggesting a preceding incidence of bone fracture; 3: Fracture callus material (woven bone)
as a result of bone fracture, still representing a clear dislocation of bone fragments
93
Chapter VI: Histological evaluation of keel bone
Figure 1. Cross section of perch positions within the small group systems Eurovent 625a-EU
NE
4
3 2
1
1. central tube for supply of dust bathing substrate 2. back perch 3. front perch 4. nipple drinker
FE ST BE NE: non-elevated perches; FE: front perch elevated; ST: perches in a stepped position; BE: back perch elevated.
Figure 2a. Cross-section of keel bone excised 1 cm caudal of
pilae carinae and apex sterni without evidence of histological
deviation.
94
Chapter VI: Histological evaluation of keel bone
Figure 2b. Keel bone revealing an s-shaped deformity without
evidence of fracture callus material or development of new bone
(woven bone).
Figure 3. Periostal ectostosis appearing as a thin layer
alongside the keel bone (cortical bone) without evidence of
a preceding fracture.
CB: Cortical bone; PE: Periostal ectostosis.
95
Chapter VI: Histological evaluation of keel bone
96
Figure 4. Fracture callus material (woven bone) as a result
of keel bone fracture, still representing a clear dislocation of
bone fragments.
CB: cortical bone; FCM: fracture callus material; BFD: bone
fragment dislocation.
Figure 5. Slightly (grade 3, left) and moderately
(grade 2, right) deformed keel bones.
Chapter VII
Meta-analysis of welfare, egg quality, production and selected
behavioural traits to evaluate small group housing systems for
laying hens
B. Scholz, S. Rönchen, H. Hamann and O. Distl
Züchtungskunde
Chapter VII: Meta-analysis of selected welfare, production and behavioural traits
Meta-Analyse von Gesundheits-, Eiqualitäts- Leistungs- und Verhaltensmerkmalen zur
Beurteilung von Kleingruppenhaltungssystemen für Legehennen
BRITTA SCHOLZ, SWAANTJE RÖNCHEN, H. HAMANN UND O. DISTL1
Institut für Tierzucht und Vererbungsforschung der Stiftung Tierärztliche Hochschule Hannover, Bünteweg 17p, D-30559 Hannover; 1Korrespondierender Autor: [email protected]
98
Chapter VII: Meta-analysis of selected welfare, production and behavioural traits
1 Einleitung
Mit Umsetzung der EU-Richtlinie 1999/74/EG zur „Festlegung von Mindestanforderungen
zum Schutz von Legehennen“ in nationales Recht wird in Deutschland die konventionelle
Käfighaltung von Legehennen ab 2008 gänzlich verboten sein. In den übrigen EU-Ländern
dürfen konventionelle Käfige bis 2012 genutzt werden und müssen dann durch ausgestaltete
Käfige oder alternative Haltungssysteme ersetzt werden. Während die deutsche Gesetzgebung
darüber hinaus die Nutzung ausgestalteter Käfige bis 2020 befristet hat, wird derzeit vermehrt
die Entwicklung und praktische Erprobung sogenannter Kleingruppenhaltungen gefördert und
deren Eignung für die Legehennenhaltung untersucht. Die Kleingruppenhaltung stellt zum
jetzigen Zeitpunkt neben der Freiland- und Bodenhaltung ein Haltungssystem dar, welches
den Hennen innerhalb eines geschlossenen Systems einen größtmöglichen
Bewegungsspielraum bietet und somit einen positiven Einfluss auf Gesundheits- und
Leistungsmerkmale erwarten lässt. Kleingruppenhaltungen sowie Bodenhaltungen sind in
Deutschland unbefristet zur Nutzung zugelassen.
Im Rahmen dieser Studie wurde eine Meta-Analyse aus bereits veröffentlichten Studien sowie
eigenen Daten von insgesamt zehn untersuchten Legedurchgängen (Gesamtzahl untersuchter
Hennen: 4.553) und mehreren Legelinien, wie Lohmann Selected Leghorn (LSL), Lohmann
Brown (LB) und Lohmann Silver (LS), durchgeführt. Dabei wurden verschiedene
Haltungssysteme, angefangen von der konventionellen Käfighaltung bis zu der aktuell
diskutierten Kleingruppengruppenhaltung, sowie eine Volierenhaltung, hinsichtlich
ausgewählter gesundheits- und leistungsbezogener Merkmale der Hennen verglichen. Ziel
dieser Studie war es, in einer umfassenden Auswertung darzustellen, inwieweit Einflüsse
durch die technische Weiterentwicklung von ausgestalteten Käfigen zu
Kleingruppenhaltungssystemen auf die ausgewählten Merkmale feststellbar waren und
welche positiven Effekte auf Gesundheit und Leistung der Hennen erzielt werden konnten.
Als Referenzsystem diente eine Volierenhaltung mit Kaltscharrraum bzw. mit zusätzlichem
Auslauf (intensive Auslaufhaltung).
2 Material und Methoden
2.1 Legedurchgänge und Datenherkunft
Die in die Meta-Analyse einbezogenen Untersuchungsdaten wurden im Zeitraum 1999 bis
2006 im Legehennenstall des Lehr- und Forschungsgutes (LuFG) Ruthe der Stiftung
Tierärztliche Hochschule Hannover sowie im Versuchsstall (VS) Wesselkamp der Deutschen
Frühstücksei GmbH in Ankum, Kreis Osnabrück, erhoben. Die Meta-Analyse beinhaltete
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Chapter VII: Meta-analysis of selected welfare, production and behavioural traits
insgesamt zehn Legedurchgänge (LD) und eine Gesamtzahl von 4.553 untersuchten Hennen
unter Einbezug der Studien von LEYENDECKER et al. (2001a; 2001b; 2005; unveröffentlichte
Daten (2002/2003)), VITS et al. (2005), WEITZENBÜRGER et al. (2005; 2006a; 2006b), SCHOLZ
et al. (2006) (sowie zur Veröffentlichung eingereichte Daten (LD 2005/2006)) und RÖNCHEN
et al. (2006) (sowie zur Veröffentlichung eingereichte Daten der LD 2004/2005 und
2005/2006) (Tab. 1). Auf dem LuFG Ruthe erfolgten für alle untersuchten Legeperioden pro
Legedurchgang stichprobenweise Entnahmen von im Mittel 518 Legehennen im 3., 6., 9. und
12. Legemonat. Im VS Wesselkamp wurden pro Legedurchgang im Mittel 360 Hennen zu
den oben genannten Untersuchungszeitpunkten bzw. nur im 6. und 12. Legemonat (LD
2004/2005 und 2005/2006) zur Untersuchung entnommen. Haltungssysteme, Legelinien und
Untersuchungszeitpunkte wurden jeweils anteilsmäßig mit gleichen Anzahlen untersuchter
Legehennen berücksichtigt. Detaillierte Beschreibungen der untersuchten Haltungssysteme
der in Tab. 1 angeführten Autoren sind den jeweiligen Studien zu entnehmen. Eigene Studien
wurden über zwei LD (2004 bis 2006) jeweils zeitgleich auf dem LuFG Ruthe und VS
Wesselkamp durchgeführt.
2.2 Haltungssysteme und Legelinien der LD 2004 bis 2006
In beiden Versuchsställen waren jeweils drei verschiedene Haltungssysteme für Legehennen
(Hersteller Fa. Big Dutchman, Vechta, Deutschland) installiert. Die Systeme Aviplus (AP)
und Eurovent (EV) 625A-EU stellten zwei Varianten eines ausgestalteten Käfigs dar. Im AP
wurden Gruppengrößen von 10, 20 und 30 Tieren (LuFG Ruthe) bzw. 10 und 20 Tieren (VS
Wesselkamp) gehalten. Der ausgestaltete Käfig Eurovent (EV) 625A-EU war für 20 und 30
Hennen pro Abteil ausgelegt. Das Haltungssystem EV 625a-EU stellte eine
Kleingruppenhaltung für Gruppen von 40 und 60 Hennen dar. Alle untersuchten
Haltungssysteme boten den Hennen eine Grundfläche von mindestens 750 cm2 pro Tier und
erfüllten durch die Ausstattung mit Sitzstangen, Legenestern, Sandbädern und
Krallenabriebsflächen in allen Punkten die erforderlichen Kriterien der EU-Richtlinie 1999/74
für die Haltung von Legehennen. In beiden LD (VS Wesselkamp) sowie im zweiten LD
(LuFG Ruthe) wurden die Sitzstangen innerhalb der Abteile des EV 625a-EU und EV 625A-
EU auf zwei verschiedenen Höhen installiert, um den Hennen zusätzlichen Bewegungsanreiz
und die Möglichkeit des Aufbaumens zu bieten.
Auf dem LuFG Ruthe waren die dreietagig montierten Systeme AP (doppelreihig), Eurovent
625a-EU sowie eine dreietagige Volierenanlage „Natura“ installiert. Die Volierenhaltung
bestand aus zwei Abteilen mit jeweils 1.215 Legehennen (3,650 x 15,980 mm Grundfläche
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pro Abteil) und separaten, angegliederten Außenscharrräumen (20.980 x 3.400 mm
Grundfläche). Die im ersten LD eingestallten 5.430 Legehennen setzten sich zu gleichen
Teilen aus den Legelinien Lohmann Silver (LS) und Lohmann Tradition (LT) zusammen. Im
zweiten LD wurden nur LS eingestallt. Im VS Wesselkamp standen die über vier Etagen
installierten Systeme AP, EV 625A-EU (beide doppelreihig) sowie EV 625a-EU zur
Verfügung. Im ersten LD wurden etwa 4.500 Lohmann Selected Leghorn (LSL) und 4.500
Lohmann Brown (LB) eingestallt. Im zweiten LD wurden bei gleicher Tierzahl nur LSL
verwendet.
2.3 Gesundheitsmerkmale der LD 1999 bis 2006
Zur Bestimmung des Gesundheitsstatus der Legehennen wurden die Merkmale Humerus- und
Tibiaknochenfestigkeit, Brustbein-, Fußballen- und Gefiederstatus berücksichtigt. Während
der gesamten Versuchsdauer wurden alle Merkmale von den jeweiligen Autoren mit
identischen Geräten (Knochenbruchfestigkeit) sowie anhand identischer
Untersuchungsprotokolle (Brustbein, Fußballen, Gefieder) erhoben. Die Bestimmung der
Humerus- und Tibiaknochenfestigkeit erfolgte bei allen Autoren mit der
Materialprüfmaschine vom Typ „Zwick/Z2.5/TNIS” (Zwick-Roell, Ulm, Deutschland) und
wurde in Newton (N) angegeben. Die Materialprüfmaschine wurde jährlich geeicht und auf
ihre Präzision bei der Messung hin überprüft. Der Brustbeinstatus der Legehennen wurde von
den Autoren anhand einer vierstufigen Punkteskala ermittelt (Note 4 = unverändertes
Brustbein, Note 3 = geringgradige, Note 2 = mittelgradige und Note 1 = hochgradige
Deformation). Zur Beurteilung des Fußballenstatus (Sohle) wurden von jeder Legehenne
beide Füße makroskopisch untersucht. Dabei wurden Hyperkeratosen und Epithelläsionen
getrennt voneinander erfasst. Der Schweregrad des Fußpaares richtete sich nach der
Veränderung mit der stärksten Ausprägung. Zur Befunderhebung wurde ein einheitliches
Beurteilungsschema mit den Schweregraden 1 (keine Hyperkeratose, Epithel intakt, keine
Verdickung des Ballens) bis 4 (großflächige, tiefgreifende Läsionen, Ballen hochgradig
verdickt) bzw. 5 (höchstgradige Hyperkeratose) verwendet. Der Befiederungsstatus wurde
von allen Autoren für die Körperregionen Kopf, Hals, Brust, Bauch, Rücken, Flügel und
Schwanz separat anhand einer Bewertungsskala von 1 (gravierende Gefiederschäden,
federlose Stellen) bis 4 (sehr gutes, vollständiges Gefieder mit nur wenig deformierten oder
beschädigten Federn) bewertet. Zur Ermittlung des Gesamtgefiederstatus wurden die für die
jeweiligen Körperregionen vergebenen Punkte im Anschluss zu einer Gesamtsumme
aufaddiert (max. 28, min. 7 Punkte).
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2.4 Leistungsmerkmale, Eischalenbruchfestigkeit und Mortalität der LD 1999-2006
Neben dem Leistungsmerkmal Legeleistung pro Bestandshenne wurden die Merkmale
Eischalenbruchfestigkeit und Mortalität der Hennen in die Untersuchung einbezogen. Die
Legeleistung der Hennen sowie die Anzahl der verendeten Tiere wurden in beiden
Versuchsställen täglich durch die Tierbetreuer erfasst. Bei allen Autoren erfolgten die
Untersuchungen zur Messung der Eischalenbruchfestigkeit über den gesamten
Versuchszeitraum mit der Materialprüfmaschine vom Typ „Zwick/Z2.5/TNIS”. Die
Untersuchungen wurden einmal pro LM durchgeführt. In den LD 2004-2006 (Ruthe) wurde
jeweils eine Stichprobe von im Mittel 4.389 Eiern, gleichmäßig auf die jeweils zu
untersuchenden Haltungssysteme aufgeteilt, untersucht. Die Anzahl der untersuchten Eier der
Autoren VITS et al. (2005) und LEYENDECKER et al. (2005) sind den angegebenen
Publikationen zu entnehmen.
2.5 Verhaltensmerkmale der LD 2002-2006
Die Verhaltensmerkmale Stehen auf dem Drahtboden, Gehen auf dem Drahtboden,
Aufenthalt auf den Sitzstangen (Stehen und Sitzen), Ruhen auf den Sitzstangen, Sandbaden
auf dem Drahtboden, Pickaktivität im Sandbad, auf Objekte gerichtete Pickaktivität (z.B.
Einrichtungselemente, Drahtboden) und Federpicken wurden während der Lichtphase mittels
Direktbeobachtung und Momentaufnahme erfasst. Zur Methodik der Datenerfassung siehe
WEITZENBÜRGER et al. (2006b). Eigene Verhaltensbeobachtungen erfolgten im 3., 6., 9. und
12. LM (2. LD, LuFG Ruthe), im 6. und 12. LM (1. LD) sowie im 3., 6. und 12. LM (2.LD)
(VS Wesselkamp).
2.6 Statistische Auswertung
Für die Meta-Analyse wurden die LSM aus jedem Legedurchgang pro Ort der Untersuchung,
Haltungssystem und Legelinie (soweit mehrere LL eingesetzt wurden) für Humerus- und
Tibiabruchfestigkeit, Brustbein-, Fußballen- und Gefiederstatus, Legeleistung pro
Bestandshenne, Mortalität, Eischalenbruchfestigkeit sowie für die Verhaltensmerkmale
verwendet. Die dazu gehörigen Studien sind in Tab. 1 angeführt.
Die Meta-Analyse erfolgte anhand eines linearen Weighted Least Square Modells (Prozedur
GLM von SAS mit der Option „weight“). Als Gewichtung wurden die Reziprokwerte der
quadrierten Standardfehler (SE) der zugehörigen LSM verwendet. Die Anzahl der LSM, die
den gewichteten LSM der einzelnen Merkmale jeweils zugrunde liegen, sind in der Legende
zu unten angegebener Formel aufgeführt. Aufgrund einer unterschiedlichen genetischen
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Herkunft der Legelinie Lohmann Silver wurden dem fixen Effekt LIN in dem statistischen
Modell die drei Ausprägungen Braunleger (Lohmann Brown, Lohmann Tradition), Weißleger
(Lohmann Selected Leghorn) und Lohmann Silver zugewiesen. Das Haltungssystem (SYS),
der Ort der Untersuchungen (LuFG Ruthe, VS Wesselkamp) innerhalb des Haltungssystems
(ORT(SYS)), sowie die Legelinie innerhalb des Haltungssystems (LIN(SYS)) wurden als fixe
Effekte in das Modell einbezogen. Insgesamt wurden sechs verschiedene Haltungssysteme
unterschieden. Aufgrund der Datenstruktur wurde für die Auswertung der Mortalität und der
Verhaltensmerkmale die Legelinie LIN(SYS) nicht mit in das Modell einbezogen. Für die
Verhaltensmerkmale waren Legelinie und Ort der Untersuchung miteinander verknüpft. Für
das Merkmal Legeleistung wurde aufgrund der Datenstruktur der ORT(SYS) nicht in das
Modell aufgenommen.
Yijkl = µ + SYSi + ORT(SYS)ij + LIN(SYS)ik + eijkl
Yijkl LSM für die Merkmale Humerus- und Tibiabruchfestigkeit (jeweils n =
36), Brustbeinstatus (n = 24), Fußballenstatus (n = 21), Gefiederstatus
(n = 21), Legeleistung pro Bestandshenne (n = 30), Mortalität (n = 36),
Eischalenbruchfestigkeit (n = 24) sowie für die Verhaltensmerkmale (n
= 14)
μ Modellkonstante
eijkl zufälliger Restfehler
3 Ergebnisse
Die Ergebnisse der Varianzanalyse zeigten, dass der fixe Effekt des Haltungssystems einen
signifikanten Einfluss auf die Merkmale Humerus- und Tibiabruchfestigkeit,
Sohlenhyperkeratose, Legeleistung, Mortalität und Sandbaden auf dem Drahtboden hatte
(Tab. 2), während er sich für die Merkmale Brustbeinstatus, Epithelläsion der Sohle,
Gefiederstatus, Eischalenfestigkeit sowie für die übrigen ausgewählten Verhaltensmerkmale
als nicht signifikant erwies. Ein signifikanter Einfluss des Untersuchungsortes wurde für die
Merkmale Tibiabruchfestigkeit, Gefiederstatus, Mortalität, Picken im Sandbad, Federpicken,
Aufenthalt auf den Sitzstangen (Stehen/Sitzen) und Sandbaden auf dem Boden festgestellt.
Der fixe Effekt der Legelinie erwies sich ausschließlich für die Legeleistung als signifikant.
Hennen in konventioneller Käfighaltung wiesen im Vergleich zu allen übrigen
Haltungssystemen eine geringere Humerus- und Tibiabruchfestigkeit auf. Weiterhin zeigten
Hennen aus beiden Varianten des ausgestalteten Käfigs und der Kleingruppenhaltung eine
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geringere Humerus- und Tibiafestigkeit im Vergleich zur Volierenhaltung, mit Ausnahme der
in EV 625A-EU gehaltenen Hennen, welche eine mit der Volierenhaltung vergleichbare
Tibiafestigkeit und somit auch eine signifikant günstigere Tibiafestigkeit als Hennen im
ausgestalteten Käfig Aviplus und in der Kleingruppenhaltung aufwiesen. Die
Humerusfestigkeit von Hennen aus Kleingruppenhaltung und ausgestalteten Käfigen
unterschied sich nicht signifikant voneinander.
Hennen aus dem Aviplus (AP) zeigten eine geringere Humerus- und Tibiafestigkeit
verglichen mit Tieren aus der intensiven Auslaufhaltung. Zwischen den beiden untersuchten
EV Systemen und der intensiven Auslaufhaltung konnten keine Unterschiede in der
Humerusfestigkeit beobachtet werden. Für Hennen aus Kleingruppenhaltung zeigte sich im
Vergleich zur intensiven Auslaufhaltung eine niedrigere Tibiafestigkeit.
Hennen im EV 625a-EU zeigten vermehrt hyperkeratotische Veränderungen an den Sohlen
im Vergleich zu Hennen aus AP, während sich die übrigen Haltungssysteme in diesem
Merkmal nicht voneinander unterschieden.
Die Legeleistung der Hennen aus konventioneller Haltung unterschied sich nicht von Tieren
aus den übrigen Haltungssystemen. Hennen aus AP, EV 625A-EU und EV 625a-EU erzielten
eine höhere Legeleistung im Vergleich zur Volieren- und intensiven Auslaufhaltung. Darüber
hinaus zeigten Hennen aus EV 625A-EU eine höhere Legeleistung als Tiere aus AP und EV
625a-EU. Hennen aus der Volierenhaltung zeigten die höchste Mortalitätsrate und die
Unterschiede zu den Systemen AP, EV 625A und EV 625a-EU erwiesen sich als signifikant.
Keine Unterschiede in der Mortalitätsrate zeigte sich zwischen Hennen aus Volierenhaltung,
intensiver Auslaufhaltung und konventioneller Käfighaltung.
Hennen aus AP zeigten signifikant häufigeres Sandbadeverhalten auf dem Drahtboden im
Vergleich zu Hennen aus EV 625a-EU und EV 625A-EU, während Hennen aus den beiden
letztgenannten Systemen sich in diesem Merkmal nicht voneinander unterschieden.
Obwohl der fixe Effekt des Haltungssystems für den Brustbein- und Gefiederstatus sowie für
das Merkmal Aufenthalt auf den Sitzstangen (Stehen/Sitzen) nicht signifikant war, zeigten
sich bei einzelnen Vergleichen der Systeme signifikante Unterschiede. So wiesen Hennen aus
Volierenhaltung einen ungünstigeren Brustbeinstatus im Vergleich zu EV 625a-EU auf,
unterschieden sich jedoch nicht von Hennen aus EV 625A-EU und AP. Weiterhin wurde bei
Hennen aus der Volierenhaltung ein signifikant günstigerer Gefiederstatus verglichen mit
Tieren aus ausgestalteten Käfigen und Kleingruppenhaltung beobachtet. Hinsichtlich der
Verhaltensmerkmale hielten sich im AP signifikant mehr Hennen auf den Sitzstangen auf
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(Stehen, Sitzen) als Hennen aus EV 625A-EU, während Hennen aus EV 625a-EU die
Sitzstangen signifikant häufiger zum Stehen und Sitzen nutzten als Hennen aus EV 625A-EU.
4 Diskussion
Die Meta-Analyse erbrachte in mehrerer Hinsicht bemerkenswerte Ergebnisse. Nur wenige
Merkmale zeigten signifikante Unterschiede zwischen den sechs untersuchten
Haltungssystemen. Im Haltungssystem EV 625A-EU war die Mortalität am geringsten, die
Legeleistung pro Bestandshenne und damit auch pro Anfangshenne am höchsten und die
Gesundheitsmerkmale am ausgewogensten. Die Hyperkeratosen der Sohle waren niedrig und
der Brustbeinstatus zeigte keinen Unterschied im Vergleich zu den anderen untersuchten
Haltungsformen. Die Tibiaknochenfestigkeit war mit den in der Voliere gemessenen Werten
vergleichbar und sowohl Humerus- als auch Tibiafestigkeit unterschieden sich nicht von
Werten aus der intensiven Auslaufhaltung. Im Vergleich zur konventionellen Käfighaltung
wurde in allen untersuchten Haltungssystemen eine bessere Humerus- und
Tibiaknochenfestigkeit erzielt. Die in dieser Untersuchung festgestellte Verbesserung der
Humerus- und Tibiafestigkeiten von Hennen aus ausgestalteten Käfigen und
Kleingruppenhaltungen im Vergleich zur konventionellen Käfighaltung kann neben der
Sitzstangennutzung auch durch den sogenannten „Omnibuseffekt“ hervorgerufen worden
sein, der den Hennen das Zurücklegen größerer Distanzen (insbesondere in der
Kleingruppenhaltung) innerhalb eines Abteils ermöglichte und sich somit in erster Linie
positiv auf die Tibiafestigkeit ausgewirkt haben könnte. Ebenfalls kann eine Aufteilung der
Haltungseinheiten in Sandbad-, Sitzstangen- und Nestbereich und eine hohe Akzeptanz der
verschiedenen Bereiche, dazu beigetragen haben, dass die Hennen angeregt wurden, sich
zwischen den genannten Arealen zu bewegen. Die in der Volierenhaltung erzielten hohen
Knochenfestigkeiten konnten jedoch nicht für Legehennen im Aviplus System und in der
Kleingruppenhaltung ermittelt werden und wurden auch nicht durch die intensive
Auslaufhaltung übertroffen. Das Nutzen des Etagenelementes und des angegliederten
Kaltscharrraumes bot den Hennen in der Voliere eine Vielzahl an Bewegungsmöglichkeiten,
welche sich positiv auf eine Erhöhung der Knochenfestigkeit ausgewirkt hat. Die im EV
625A-EU ermittelte und mit der Volierenhaltung vergleichbare Tibiafestigkeit lässt sich in
diesem Zusammenhang schwer erklären. Da im Gegensatz zum Aviplus System die
Sitzstangen im EV 625A-EU teilweise auf verschiedenen Ebenen installiert waren, könnte
sich dies sehr positiv auf die Tibiafestigkeit in diesem System ausgewirkt haben. In einer
Untersuchung von BISHOP et al. (2000) wurde eine positive Korrelation zwischen Humerus-
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und Tibiafestigkeit sowie dem Brustbeinstatus beschrieben. Trotz hoher Humerus- und
Tibiaknochenfestigkeit in der Volierenhaltung wurde in diesem System jedoch ein
ungünstiger Brustbeinstatus im Vergleich zur Kleingruppenhaltung beobachtet. In einer
umfassenden Studie von ELSON und CROXALL (2006) wurde ebenfalls ein verminderter
Brustbeinstatus bei Hennen in Volieren festgestellt. GREGORY et al. (1990) beschrieben als
einen prädisponierenden Faktor für Brustbeinveränderungen ein hohes Kollisionsrisiko durch
fehlerhaftes Anfliegen von Sitzstangen bei Hennen in Volierenhaltung. Ursache für ein
vermehrtes Unfallrisiko könnte eine ungünstige Sitzstangenpositionierung sein. Laut einer
Studie von MOINARD et al. (2004) sollten Sitzstangen einen Abstand von 600 mm nicht
überschreiten, um den Hennen eine problemlose Nutzung zu gewährleisten. Die in der Voliere
installierten Sitzstangen hatten einen Abstand von 830 mm zum Boden und 480 bzw. 740 mm
Abstand zu der obersten Etage des Volierenelementes. Dies könnte möglicherweise mit einem
höheren Kollisionsrisiko assoziiert gewesen sein. BESSEI (1997) wies ebenfalls darauf hin,
dass Anflugsitzstangen optimal positioniert sein müssen, um das Risiko von Frakturen zu
minimieren. Obwohl der Brustbeinstatus in den ausgestalteten Käfigen sich nicht von den
Werten der Volierenhaltung unterschied, war zwischen letzterem System und der
Kleingruppenhaltung ein signifikanter Unterschied zu verzeichnen. KEELING et al. (2003)
stellten bei Hennen in Abteilen mit Gruppengrößen um die 30 Hennen eine vermehrte Unruhe
aufgrund einer instabilen sozialen Hierarchie fest. In diesem Zusammenhang könnten die
teilweise auf verschiedenen Ebenen positionierten Sitzstangen in den 30-er Abteilen des EV
625A-EU vermehrt zu ungewollten Kollisionen mit dem Brustbein geführt haben, während in
den größeren Gruppen der Kleingruppenhaltung eine tolerantes Sozialverhalten auftrat, dass
mit weniger Unruhe verbunden war. In einer Studie von WAHLSTRÖM et al. (2001) wurden die
in ausgestalteten Käfigen beschriebenen Brustbeinveränderungen auf starke mechanische
Belastung bei der Sitzstangennutzung zurückgeführt. In der vorliegenden Studie führte nur die
Nutzung der Sitzstangen in der Kleingruppenhaltung weniger stark zu Deformationen des
Brustbeins als die Haltungsbedingungen im untersuchten Volierensystem. GENTLE (2001)
konnte in einer Studie eindeutige Hinweise auf komplexe Vorgänge der
Schmerzwahrnehmung bei Geflügel nachweisen, so dass die in der Voliere auftretenden
Brustbeindeformationen durchaus kritisch zu bewerten sind.
Legehennen im den untersuchten Kleingruppenhaltungssystemen waren stärker von
hyperkeratotischen Veränderungen der Sohlenballen betroffen. Hierzu könnte eine
unterschiedlich frequente Nutzung der Sitzstangen beigetragen haben. Darüber hinaus wird
der Fußballenstatus durch das Design der angebotenen Sitzstangen maßgeblich beeinflusst
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(SIEGWART, 1991; OESTER, 1994; TAUSON und ABRAHAMSSON, 1994). Form und
Oberflächenbeschaffenheit der in der Kleingruppenhaltung installierten Sitzgelegenheiten
unterschieden sich teilweise von denen der ausgestalteten Käfige. In allen untersuchten LD
war den Hennen im Kleingruppenhaltungssystem das Nutzen des Zuleitungsrohres der
Sandbadbefüllung als Sitzgelegenheit möglich. Durch seine runde Form und die
vergleichsweise raue Oberfläche, könnte eine vermehrte Proliferation der Sohlenballenhaut
hervorgerufen worden sein (WEITZENBÜRGER et al, 2005). In Studien von SIEGWART (1991)
und WEITZENBÜRGER et al. (2005) werden als Ursache des Entstehens von
Sohlenballenhyperkeratose vor allem die Nutzung von Sitzstangen angesehen. Läsionen und
Entzündungen werden am häufigsten in alternativen Haltungssystemen beobachtet (KEUTGEN
et al., 1999). So begünstigt eine feuchte und durch Exkremente verunreinigte Einstreu (WANG
et al., 1998) sowie mangelnde Sauberkeit von Sitzstangen (ELSON und CROXALL, 2006)
entzündliche Veränderungen der Fußballen. Entgegen Blokhuis et al. (2007) konnte in der
vorliegenden Studie jedoch kein vermehrtes Auftreten von Sohlenballenläsionen in der
Volierenhaltung im Vergleich zu den ausgestalteten Käfigen und Kleingruppenhaltungen
beobachtet werden. Dies könnte auf guten hygienischen Zustand des verwendeten
Einstreumaterials zurückgeführt werden.
Ein intaktes Gefieder trägt maßgeblich zum Wohlbefinden der Hennen bei. Gefiederschäden
können sowohl durch Einrichtungselemente in Käfighaltungssystemen (FREIRE et al., 1999)
als auch durch einen gegenseitigen Abrieb zwischen Hennen bei hoher Besatzdichte
verursacht werden (APPLEBY et al., 2002). Diese Faktoren könnten den in den ausgestalteten
Käfigen und Kleingruppenhaltungen beobachteten ungünstigeren Gesamtgefiederstatus der
Hennen im Vergleich zur Volierenhaltung hervorgerufen haben. Federpicken stellt ebenfalls
eine wichtige Ursache für das Auftreten von Gefiederschäden dar (BILČÍK und KEELING,
1999). Die durchgeführten Untersuchungen zum Verhalten zeigten jedoch keine Unterschiede
hinsichtlich des Auftretens von Federpicken in Kleingruppenhaltung und den ausgestalteten
Käfigen. Verhaltensbeobachtungen in der vorliegenden Studie umfassten die Untersuchung
von Merkmalen, die Rückschlüsse auf die Raumnutzung sowie Akzeptanz der
Einrichtungselemente der Haltungseinheiten zuließen. Obwohl die Kleingruppenhaltung
aufgrund der größeren Grundfläche der Abteile Möglichkeit zu mehr Fortbewegung bot,
konnte kein Unterschied in der Häufigkeit der Fortbewegung (Gehen auf Drahtboden) zum
ausgestalteten Käfig ermittelt werden. Ebenso konnten keine Abweichungen zwischen den
Haltungssystemen für die Merkmale Ruhen auf den Sitzstangen und Aufenthalt (Stehen) auf
dem Drahtgitterboden ermittelt werden. Hennen aus EV 625a-EU nutzten Sitzstangen im
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Vergleich zum EV 625A-EU zum Sitzen/Stehen vermutlich häufiger, da ihnen durch das
Zuleitungsrohr zur Sandbadbefüllung eine zusätzliche Möglichkeit der Sitzstangennutzung
zur Verfügung stand. Sandbaden stellt ein wichtiges Element des Komfortverhaltens dar. In
neuartigen Haltungssystemen, in denen durch Ausgestaltung der Abteile mit
Sandbadevorrichtungen den Legehennen die Ausübung des Sandbadens ermöglicht wird, ist
dieser Bereich jedoch noch immer als eine Schwachstelle anzusehen (BUCHENAUER, 2005).
So kritisierten WEITZENBÜRGER et al. (2006b) unter anderem die Größe der angebotenen
Staubbäder, die das von Hennen bevorzugte Sandbaden in der Gruppe nur eingeschränkt
zuließ. In der vorliegenden Studie wurde Sandbadeaktivität auf dem Drahtboden signifikant
häufiger im AP beobachtet im Vergleich zur Kleingruppenhaltung und EV 625A-EU. Dies
könnte möglicherweise auf ungünstigere Lichtverhältnisse in den Sandbadevorrichtungen des
AP zurückgeführt werden. Aufgrund der zentralen, lichtundurchlässigen Trennwand war die
Lichtintensität in diesen Bereichen im Vergleich zur Kleingruppenhaltung (ohne Trennwand)
und dem EV 625A-EU (Trennwand zur Hälfte aus Gitterdraht) geringer. BUCHENAUER (2005)
konnte das Ausüben des Sandbadeverhaltens oftmals auf dem Drahtboden in Nähe einer
Lichtquelle beobachten, da die Sandbadevorrichtungen nicht genügend ausgeleuchtet waren
und somit der wichtige Schlüsselreiz des Lichtes fehlte. Auch die im Vergleich zu EV 625a
und EV 625A zeitlich limitierte Verfügbarkeit des Sandbads im AP wird als Grund einer
erhöhten Sandbadeaktivität auf dem Drahtboden angesehen, da die Hennen nur unzureichend
Möglichkeiten hatten, ihr Sandbadeverhalten während des begrenzten Zugangs zu der
Sandbadevorrichtung auszuüben. Pickaktivitäten werden zum Funktionskreis des
Erkundungs- und Nahrungsaufnahmeverhaltens gezählt. WEITZENBÜRGER et al. (2006b)
erwähnten einen möglichen Zusammenhang zwischen einem gehäuften Auftreten von
Federpicken und gleichzeitig verminderter Pickaktivität im Sandbad in ausgestalteten Käfigen
und führten dies auf einen Mangel an adäquatem Erkundungs- und Beschäftigungsmaterials
zurück, welches die Hennen veranlasste, Pickaktivitäten auf das Gefieder ihrer Artgenossen
zu projizieren. In der vorliegenden Studie konnten für die Verhaltensmerkmale Federpicken,
Pickaktivität im Sandbad sowie gegen Objekte gerichtetes Picken keine Unterschiede
zwischen ausgestalteten Käfigen und der Kleingruppenhaltung beobachtet werden. Da alle
aufgeführten Pickaktivitäten in den untersuchten Systemen beobachtet wurden, konnte aus
den vorliegenden Ergebnissen nicht geschlussfolgert werden, ob Menge und Struktur des
angebotenen Scharrmaterials geeignet waren, den Erkundungstrieb der Tiere voll zu
befriedigen. Die in der Volieren- und Auslaufhaltung niedrigere Legeleistung im Vergleich zu
ausgestaltetem Käfig und Kleingruppenhaltung entspricht den Ergebnissen von BLOKHUIS et
108
Chapter VII: Meta-analysis of selected welfare, production and behavioural traits
al. (2007). Nicht vollständig geschlossene Haltungssysteme bergen aufgrund externer
Umwelteinflüsse ein größeres Gesundheitsrisiko für Hennen, welches zusammen mit oftmals
höherem Futteraufwand zu einer größeren, wirtschaftlichen Unsicherheit des Haltungssystems
führen kann. Die in der Volierenhaltung im Vergleich zu ausgestaltetem Käfig und
Kleingruppenhaltung aufgetretene höhere Mortalitätsrate spiegelt diesen Aspekt ebenfalls
wider.
Schlussfolgernd lässt sich sagen, dass sich die technische Weiterentwicklung der
Legehennenhaltungssysteme hin zu ausgestalteten Käfigen und Kleingruppen positiv auf die
erfassten gesundheits- und leistungsbezogenen Merkmale im Vergleich zur konventionellen
Käfighaltung ausgewirkt hat. Die Volierenhaltung konnte in den Merkmalen Humerus- und
Tibiaknochenfestigkeit nicht übertroffen werden, wobei Hennen aus EV 625A-EU eine
vergleichbare Tibiafestigkeit aufwiesen. Hennen aus der Voliere zeichneten sich durch einen
ungünstigeren Brustbeinstatus im Vergleich zur Kleingruppenhaltung aus und wiesen eine
höhere Mortalität und geringere Legeleistung auf. Die Weiterentwicklung der ausgestalteten
Käfige zur Kleingruppenhaltung brachte weitere Verbesserungen in den untersuchten
Gesundheits-, Leistungs- und Verhaltensmerkmalen. Hinsichtlich wirtschaftlicher Aspekte
(Legeleistung, Mortalität) boten ausgestaltete Käfige und Kleingruppenhaltungssysteme
deutliche Vorteile gegenüber der Volierenhaltung. In den untersuchten ausgestalteten Käfigen
sind gegenüber den anderen alternativen Haltungsformen bestimmte Verhaltensweisen stark
eingeschränkt beziehungsweise fehlgeleitet (Sandbadeverhalten auf dem Drahtboden im AP),
so dass auch unter Verhaltensaspekten eine Weiterentwicklung der ausgestalteten Käfige zur
Kleingruppenhaltung notwendig war.
Zusammenfassung
In der vorliegenden Studie wurden mittels Meta-Analyse gesundheits- und leistungsbezogene
Parameter, sowie ausgewählte Verhaltensmerkmale von Legehennen in unterschiedlichen
Haltungssystemen untersucht. Einbezogen wurden eigene Untersuchungsergebnisse sowie
bereits veröffentlichte Daten verschiedener Autoren zu insgesamt zehn Legedurchgängen und
einer Gesamtzahl von 4.553 Hennen. Die getesteten Haltungssysteme waren konventionelle
Käfige, zwei Varianten eines ausgestalteten Käfigs, Kleingruppenhaltungen, ein
Volierensystem, sowie eine intensive Auslaufhaltung. Die Analyse umfasste die LS-
Mittelwerte (LSM) von Humerus- und Tibiaknochenfestigkeit, Brustbein-, Fußballen- und
Gefiederstatus, Legeleistung, Mortalität, Eischalenfestigkeit sowie Verhaltensmerkmale der
Hennen. Die LSM der einbezogenen Studien wurden anhand der Reziprokwerte ihrer
109
Chapter VII: Meta-analysis of selected welfare, production and behavioural traits
quadrierten Standardfehler gewichtet und die Meta-Analyse erfolgte anhand eines linearen
Weighted Least Square Modells. Das Haltungssystem erwies sich für Humerus- und
Tibiabruchfestigkeit, Sohlenballenhyperkeratose, Legeleistung, Mortalität und Sandbaden auf
dem Drahtboden als signifikant. Im Vergleich zu den ausgestalteten Käfigen und der
Kleingruppenhaltung erzielten die in der Voliere gehaltenen Hennen die höchsten
Knochenfestigkeiten, zeigten jedoch einen ungünstigeren Brustbeinstatus verglichen mit den
ausgestalteten Käfigen, sowie eine geringere Legeleistung und höhere Mortalität.
Hyperkeratotische Veränderungen der Sohlenballen traten am häufigsten in der
Kleingruppenhaltung auf. Für die Merkmale Humerusbruchfestigkeit, Brustbein- und
Gefiederstatus, Eischalenfestigkeit, Mortalität sowie für die ausgewählten
Verhaltensmerkmale, mit Ausnahme der Sandbadeaktivität auf dem Drahtboden und des
Aufenthaltes auf den Sitzstangen (Stehen und Sitzen), konnten keine Unterschiede zwischen
ausgestaltetem Käfig und Kleingruppenhaltung festgestellt werden.
Schlüsselwörter: Meta-Analyse, Legehennen, Gesundheitszustand, Verhalten,
Haltungssysteme
110
Chapter VII: Meta-analysis of selected welfare, production and behavioural traits
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LEYENDECKER, M., H. HAMANN, J. HARTUNG, J. KAMPHUES, C. RING, G. GLÜNDER, C.
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WAHLSTRÖM, A., R. TAUSON and K. ELWINGER (2001): Plumage condition and health of
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WEITZENBÜRGER, D., A. VITS, H. HAMANN und O. DISTL (2006a): Evaluierung von
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WEITZENBÜRGER, D., A. VITS, H. HAMANN und O. DISTL (2006b): Evaluierung von
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Danksagung
Die Autoren danken der Big Dutchman GmbH, der Lohmann Tierzucht GmbH und der
Deutschen Frühstücksei GmbH für die finanzielle Unterstützung des Forschungsprojektes.
Meta-analysis of welfare, egg quality, production and selected behavioural traits to
evaluate small group housing systems for laying hens
Abstract
The objective of the current investigation was to employ the tool of meta-analysis in order to
assess selected welfare, behavioural and production traits of four different layer strains kept in
different types of housing systems. The study was carried out from 1999 to 2006 at two
experimental farms and included data of ten laying periods, comprising 4,553 hens in total.
Data was collected by the different authors employing fully identical methods. Housing
systems tested were conventional cages, two types of furnished cages, small group systems,
an aviary housing system and an intensive free range system. Least square means (LSM) of
the traits bone strength, keel bone status, foot pad health, plumage condition, egg shell
strength, production, mortality and selected behavioural patterns were chosen for meta-
analysis. LSM given by the included studies were weighted with their squared, reciprocal
113
Chapter VII: Meta-analysis of selected welfare, production and behavioural traits
standard errors and meta-analysis was carried out using a linear Weighted Least Square
Model. Housing system had a significant effect on humerus and tibia bone strength,
hyperkeratosis of sole pad, production, mortality rate and dustbathing on wire floor. At the
expense of inferior keel bone status compared to furnished cages and unfavourable production
and mortality rate, bone strength of hens kept in the aviary system could not be exceeded by
any other type of housing system tested. Foot pad health of hens kept in the aviary was not
found to be unfavourable although litter had been provided and hyperkeratosis of sole pad
was found to be mostly prevalent in the small group systems. Highest production and lowest
mortality rates were detected in furnished cages and small group systems. Humerus bone
strength, keel bone status, plumage condition, eggshell strength, mortality rate and the
selected behavioural patterns, except the traits dust bathing on wire floor and standing/sitting
on perch, did not differ between hens kept in furnished cages and small group systems.
Key words: meta-analysis, laying hen, welfare, behaviour, housing system
114
Chapter VII: Meta-analysis of selected welfare, production and behavioural traits
Tab. 1. In die Meta-Analyse einbezogene Studien, deren Untersuchungszeiträume (LD),
Versuchsfarmen, Haltungssysteme, verwendete Legelinien (LIN), Anzahl untersuchter
Hennen (n) und Anfangsbestand (AB) der jeweils in dem Versuchsstall eingestallten Hennen.
Studies included in the meta-analysis, their investigation periods (LD), trial farms, housing
systems, layer lines (LIN), number of hens (n) examined and total number of hens housed.
LuFG Ruthe VS Wesselkamp LD
Studien, Systeme LIN n AB Studien, Systeme LIN n
AB
1999-2000
Leyendecker et al. (2001a, 2001b)
KK, Voliere, AH
LSLLT
300 4.500 - - -
2000-2001
Leyendecker et al. (2005)
KK, AP, Voliere LS 600
5.211 - - -
2001-2002
Leyendecker et al. (2005)
KK, AP, Voliere LS 675
4.882 - - -
2002-2003
Leyendecker, unveröffentlicht LS 628
5.410
Vits et al. (2005), Weitzenbürger et al. (2005, 2006a, 2006b)
AP, EV 625A-EU, EV 625a-EU
LB LSL
432 8.640
2003-2004 - - -
Vits et al. (2005), Weitzenbürger et al. (2005, 2006a, 2006b)
AP, EV 625A-EU, EV 625a-EU LSL 432
8.640
2004-2005
Scholz et al. (2006) Rönchen et al. (2006),*
AP, EV 625aEU, Voliere
LS LT
478 5.490
Scholz/Rönchen* AP, EV 625A-EU, EV 625a-EU
LB LSL
288 ca.
9.000
2005-2006
Scholz/Rönchen* AP, EV 625a-EU,
Voliere LS 432
5.560Scholz/Rönchen*
AP, EV 625A-EU, EV 625a-EU LSL 288 ca.
9.000 KK: konventioneller Käfig; AP: AP; AH: intensive Auslaufhaltung; EV: Eurovent; LD:
Legedurchgang; LIN: Legelinie; LSL: Lohmann Selected Leghorn, LT: Lohmann Tradition;
LS: Lohmann Silver; LB: Lohmann Brown; *: zur Veröffentlichung eingereicht
115
Chapter VII: Meta-analysis of selected welfare, production and behavioural traits
116
Tab. 2. Signifikante Unterschiede der Meta-Analyse zwischen den verschiedenen Haltungssystemen
bezogen auf die Merkmale Humerus- und Tibiabruchfestigkeit, Hyperkeratose der Sohle (HypS),
Legeleistung pro Bestandshenne (LL), Mortalitätsrate (Mort) und Sandbadeaktivität auf dem
Drahtboden (Sb Draht)
Significant differences of meta-analysis among the different housing systems tested related to the
traits humerus- and tibia bone strength, sole pad hyperkeratosis (HypS), production rate per hen
present (LL), mortality rate (Mort) and dustbathing on wire floor (Sb Draht)
Humerus (N)
Tibia (N)
HypS (1-5)
LL (%)
Mort (%)
Sb Draht (%) Sys
LSM SE LSM SE LSM SE LSM SE LSM CIu CIo LSM SE
KK 107,98a 15,74 107,34a 4,45 - - 81,20abcd22,69 11,1ab 0,07 0,16 - - AP 169,83b 8,09 129,98b 1,98 1,83a 0,04 87,57a 0,22 5,86c 0,04 0,08 0,96a 0,07EVA 195,23bc 12,81 143,44c 3,53 1,88ab 0,08 88,75b 0,15 3,74c 0,02 0,06 0,61b 0,09EVa 184,42bc 9,72 133,67b 2,23 2,04b 0,04 87,88a 0,22 5,51ac 0,03 0,09 0,52b 0,06VOL 237,14d 14,85 153,26c 3,95 2,02ab 0,12 79,50c 0,60 12,23b 0,09 0,16 - - AH 231,90cd 23,10 153,25c 6,52 - - 74,21d 0,85 9,68abc 0,04 0,21 - - Sys: Haltungssystem; KK: konventioneller Käfig; AP: AP; EVA: EV 625A-EU; EVa: EV 625a-EU;
VOL: Voliere; AH: intensive Auslaufhaltung; verschiedene Buchstaben (a, b, c, d) innerhalb einer
Spalte kennzeichnen signifikante Differenzen (p < 0,05) zwischen den Haltungssystemen für das
jeweilige Merkmal
Chapter VIII
Summary
Chapter VIII: Summary
Summary
by Britta Scholz (2007)
Evaluation of small group systems with elevated perches, furnished cages and an aviary
system for laying hens with respect to bone strength, keel bone status, stress perception
and egg quality parameters.
The objective of the present investigation was to assess different kinds of house keeping
systems for laying hens with respect to humerus and tibia bone breaking strength,
macroscopic and histological keel bone condition, layers’ stress exposure and selected
internal and external egg quality traits. Special focus was put on the only currently approved
small group system with elevated perch positions and the influence of the different perch
configurations and group sizes on laying hens’ welfare and production traits.
Small group systems with non-elevated perches could increase humerus and tibia bone
strengths in LS layers compared to hens housed in furnished cages, whereas bone strength of
LT layers was not positively affected. The aviary system showed a decisive impact on bone
characteristics of LS and LT hybrids. Bone strength was significantly increased, whereas keel
bone status tended to be inferior. For both layer lines, egg shell breaking strength was lower
in the small group system compared to furnished cages and aviary system. A favourable
predisposition of stronger bones, particularly related to LS layers, might have led to
preferential use of calcium for bone remodelling processes at the expense of calcium
provision for egg shell formation.
The small group system with elevated perches did not lead to increased humerus strength in
LS layers in comparison to the furnished cage system, whereas tibia strength was positively
influenced towards the end of the laying period. In addition, hens kept in small group
compartments with perches incorporated in the stepped position showed significantly higher
tibia bone strength compared to furnished cages. With relation to the different group sizes,
increased humerus strength was found in groups of 40 layers compared to groups of 60 hens.
Hens kept in the modified small group system showed an unfavourable keel bone status
compared to layers housed in furnished cages, thus suggesting a negative impact of elevated
perches on layers’ keel bone. However, a lower H/L-ratio in LS hens kept in the small group
system with modified perches suggested a lower stress exposition in comparison to hens kept
in the furnished cage system. The number of dirty and broken eggs recorded in the modified
118
Chapter VIII: Summary
119
small group system was significantly higher compared to furnished cages and aviary system.
Egg accumulation in front of nest boxes due to a high number of hens per nest box and risk of
laying eggs from elevated perches could have been responsible for the high number of
downgraded eggs.
In LSL layers, which are of a lighter body weight, elevated perches did succeed in increasing
humerus and tibia bone strengths in comparison to hens kept in furnished cages. Furthermore,
hens kept in compartments with either the back or front perches incorporated in an elevated
position showed higher humerus bone breaking strength compared to layers housed in
compartments with perches being installed in the stepped position. In LSL layers, perches
incorporated at different heights also led to an unfavourable keel bone condition. Although
humerus and tibia bone strengths were positively correlated with keel bone condition,
improvements in bone strength of LSL layers kept in the small group system with elevated
perches could not prevent keel bone deformities, which might have been caused by accidental
perch collisions or mechanical pressure on keel bone due to extended perching activities.
Histological evaluation of macroscopically assessed keel bone showed that in almost all
samples of unaltered keel bones, no histological deviations were found, whereas in
moderately to severely deformed keel bones, the incidence of fracture callus material was the
predominant histological finding, suggesting a traumatic origin and pain experience. In 50.9
% of sligthly deformed keel bones, fracture callus material was observed, whereas non-
traumatic s-shaped deformities, presumably as a response of layers’ keel bone to mechanical
forces while perching activities, were found in 40.7 % of slightly altered keels. Therefore,
histological analysis was found to be a mandatory tool when evaluating slightly deformed
keel bones with respect to layers’ welfare.
The tool of meta-analysis was employed in order to jointly analyse and discuss selected
welfare, behavioural and production parameters of hens kept in different types of housing
systems over 10 laying periods. These results showed that the technical advancements in the
development of laying hen husbandry systems from conventional cages to furnished cages
and small group systems had a positive influence on a variety of the selected welfare and
production traits. In aviary systems, laying hens’ humerus and tibia bone strengths could not
be exceeded, whereas keel bone status and production parameters (egg production, mortality)
were inferior compared to hens housed in furnished cages and small group systems.
Behavioural traits of hens kept in furnished cages and small group systems are still limited
and advancements in the development of laying hen husbandry systems should concentrate on
constant improvements of environmental housing conditions.
Chapter IX
Erweiterte Zusammenfassung
Chapter IX: Erweiterte Zusammenfassung
122
Erweiterte Zusammenfassung
Britta Scholz
Evaluierung von Kleingruppenhaltungen mit modifizierten Sitzstangenpositionen,
ausgestalteten Käfigen und einer Volierenhaltung für Legehennen im Hinblick auf
Knochenfestigkeiten, Brustbeinstatus, Stressbelastung und Eiqualitätsparameter.
Ziel dieser Untersuchung war es, verschiedene Haltungssysteme für Legehennen hinsichtlich
ihres Einflusses auf Knochenfestigkeit, Brustbeinstatus, Stressbelastung und
Eiqualitätsparameter zu untersuchen und zu beurteilen. Im Zuge der geänderten rechtlichen
Rahmenbedingungen in der Legehennenhaltung wurden in dieser Untersuchung erstmalig
Abteile von Kleingruppenhaltungen derart modifiziert, dass sie in dem Punkt der
Sitzstangenanordnung der von der Bundesregierung beschlossenen sogenannten Kleinvoliere
entsprachen, welche spätestens ab 2020 die bis dahin im Einsatz befindlichen ausgestalteten
Käfige ersetzen soll. Die Studie wurde über zwei Legedurchgänge zeitgleich auf zwei
verschiedenen Betrieben durchgeführt (Legehennenstall des Lehr- und Forschungsgutes
(LuFG) Ruthe der Stiftung Tierärztliche Hochschule Hannover und Versuchsstall (VS)
Wesselkamp der deutschen Frühstücksei GmbH, Ankum, Landkreis Osnabrück). Insgesamt
wurden vier verschiedene Legelinien getestet. Im ersten Legedurchgang wurden auf dem
LuFG Ruthe zu gleichen Teilen Lohmann Silver (LS) und Lohmann Tradition (LT) Hybride
eingestallt. Im zweiten Versuchsdurchgang standen ausschließlich LS zur Verfügung. Auf
dem LuFG Ruthe wurden eine Kleingruppenhaltung (Eurovent (EV) 625a-EU,
Gruppengrößen 40 und 60 Hennen), ein ausgestalteter Käfig (Aviplus, Gruppengrößen 10, 20
und 30 Hennen) sowie eine Volierenhaltung („Natura“, zwei Großgruppen zu je 1.250 Tieren)
installiert. Die Abteile der Kleingruppenhaltung wurden im zweiten Legedurchgang derart in
ihrer Sitzstangenanordnung verändert, dass sie in diesem Punkt den rechtlichen
Anforderungen der Kleinvoliere entsprachen. Die im ersten Durchgang in den jeweiligen
Abteilen des EV 625a-EU auf einer Ebene installierten Sitzstangen wurden hierzu entweder
beide erhöht und in stufiger Position angebracht (Variante ST) bzw. es wurden nur die zur
Abteilmitte hin zeigenden, hinteren Sitzstangen erhöht (Variante HH). Im VS Wesselkamp
standen zwei ausgestaltete Käfige (Aviplus, Gruppengrößen 10, 20 Hennen und EV 625A-
EU, Abteilgrößen 20 und 30 Hennen) und eine Kleingruppenhaltung EV 625a-EU (Abteile
für 40 und 60 Hennen) zur Verfügung. Im Eurovent 625A-EU wurden in beiden
Chapter IX: Erweiterte Zusammenfassung
123
Legedurchgängen etwa 40 % der Abteile mit modifizierten Sitzstangen ausgestattet
(Varianten VH (vordere Sitzstangen erhöht) und Variante HH), während im EV 625a-EU
System im ersten Legedurchgang etwa 33 % der Abteile (Variante HH) und im zweiten
Legedurchgang alle Abteile mit modifizierten Sitzstangen eingerichtet wurden (Varianten ST,
HH und VH). Im ersten Legedurchgang wurden im VS Wesselkamp die Legelinien Lohmann
Selected Legehorn (LSL) und Lohmann Brown (LB) verwendet, im zweiten Legedurchgang
wurden ausschließlich LSL eingestallt. Die Untersuchungen wurden auf dem LuFG Ruthe im
3., 6., 9. und 12. Legemonat vorgenommen, im VS Wesselkamp im 6. und 12. Legemonat. Zu
diesem Zweck wurde jeweils eine bestimmte Anzahl von Legehennen unter gleichmäßiger
Berücksichtigung von Haltungssystem, Legelinie und Gruppengröße zufällig entnommen und
in der Klinik für Geflügel der Stiftung Tierärztliche Hochschule Hannover geschlachtet.
Untersuchungen zur Humerus- und Tibiaknochenfestigkeit wurden jeweils am Folgetag nach
Herauspräparieren der Knochen durchgeführt. Die Beurteilung des Brustbeinstatus erfolgte
sowohl adspektorisch und palpatorisch als auch histologisch an ausgewählten
Brustbeinbefunden. Untersuchungen zur Messung der Stressbelastung wurden nur auf dem
LuFG Ruthe im 2. Legedurchgang durchgeführt. Hierzu wurde den Hennen unmittelbar nach
Entnahme aus dem jeweiligen Haltungssystem venöses Blut entnommen und ein Blutausstrich
zur späteren mikroskopischen Beurteilung des Heterophilen/Lymphozyten (H/L)-Ratios
angefertigt. Untersuchungen zur Eiqualität erfolgten im Abstand von vier Wochen (LuFG
Ruthe) und im Abstand von acht Wochen (VS Wesselkamp).
Hinsichtlich der Knochenfestigkeit konnte auf dem LuFG Ruthe bei den LS Hybriden des
ersten Legedurchganges ein signifikanter Anstieg der Humerus- und Tibiabruchfestigkeit in
der Kleingruppenhaltung EV 625a-EU im Vergleich zum Aviplus gemessen werden. Die
Legelinie LT hingegen zeigte keine Unterschiede in der Knochenfestigkeit zwischen Hennen
aus Kleingruppenhaltung und dem ausgestalteten Käfig. Auffällig für beide Legelinien war
der signifikante Einfluss der Volierenhaltung auf die Humerus- und Tibiabruchfestigkeit.
Vergleichbare Knochenfestigkeiten zu den Tieren aus Volierenhaltung konnten weder im
Aviplus noch in der Kleingruppenhaltung nachgewiesen werden. Im EV 625a-EU konnte
weder für LS noch für LT Hennen ein Unterschied in der Knochenfestigkeit zwischen den
beiden untersuchten Gruppengrößen ermittelt werden, während die Legelinie LT im Aviplus
eine signifikant höhere Humerusbruchfestigkeit in der Gruppengröße 10 im Vergleich zu
Abteilen mit 20 und 30 Hennen aufwies. Der Brustbeinstatus der Hennen unterschied sich
nicht signifikant zwischen den untersuchten Haltungssystemen. Es konnte jedoch für jedes
Chapter IX: Erweiterte Zusammenfassung
124
System eine signifikante Verschlechterung des Brustbeinstatus vom 3. zum 12. Legemonat
beobachtet werden. Die Untersuchungen zeigten, dass die Legelinie LS sehr viel sensibler auf
das vergrößerte Raumangebot in der Kleingruppenhaltung reagierte und bei LS Hennen
dementsprechend eine signifikant höhere Humerus- und Tibiabruchfestigkeit im Vergleich
zum Aviplus erzielt werden konnte. Hennen in der Volierenhaltung zeigten die signifikant
höchsten Knochenbruchfestigkeiten und eine vermutlich allgemeine Stärkung des Skeletts
konnte dazu beitragen, dass der in der Voliere ermittelte Brustbeinstatus sich lediglich
tendenziell, jedoch nicht signifikant negativ von den beiden anderen untersuchten
Haltungssystemen abgrenzte. Hinsichtlich der Untersuchungen zur Eiqualität wurden bei
Hennen aus der Kleingruppenhaltung signifikant geringere Eischalenfestigkeiten im
Vergleich zum ausgestalteten Käfig und der Voliere ermittelt.
Ziel der Untersuchungen im zweiten Legedurchgang auf dem LuFG Ruthe war es, die zu
diesem Zeitpunkt erstmalig in der Praxis erprobte Kleingruppenhaltung mit zwei
verschiedenen Varianten der Sitzstangenmodifikation (modifizierte Kleingruppe)
vergleichend zum Aviplus und zur Volierenhaltung zu untersuchen. Die Ergebnisse dieser
Studie zeigten, dass bei Hennen aus der modifizierten Kleingruppe keine signifikant höhere
Humerusbruchfestigkeit im Vergleich zum ausgestalteten Käfig gemessen werden konnte,
während sich die Tibiabruchfestigkeit im 12. Legemonat signifikant positiv von Tieren aus
dem Aviplus abgrenzte. Analog zu den Ergebnissen des ersten Versuchsdurchganges
unterschied sich die Humerus- und Tibiabruchfestigkeit der Hennen aus der Voliere
signifikant von den beiden anderen untersuchten Haltungssystemen. Bei Hennen, die in der
modifizierten Kleingruppe in Abteilen mit 40 Tieren gehalten wurden, konnte ein
signifikanter Anstieg der Humerusfestigkeit im Vergleich zu Gruppen mit 60 Hennen
nachgewiesen werden. Bei den getesteten Sitzstangenvarianten zeigten sich innerhalb der
Kleingruppe keine Unterschiede in der Knochenfestigkeit. Hennen aus Abteilen mit der
Variante ST wiesen jedoch eine signifikant höhere Tibiabruchfestigkeit im Vergleich zum
ausgestalteten Käfig auf, was auf eine hohe Akzeptanz dieser Sitzstangenmodifikation
hindeutet. Im Gegensatz zum ersten Versuchsdurchgang, der eine Tendenz zu einem
ungünstigeren Brustbeinstatus bei den Tieren aus Volierenhaltung aufzeigte, wurde im
zweiten Legedurchgang bei Hennen aus der Voliere im Vergleich zu den beiden anderen
Haltungssystemen ein signifikant ungünstigerer Brustbeinstatus festgestellt. Darüber hinaus
erwies sich der Brustbeinstatus der Tiere aus der modifizierten Kleingruppe annähernd
signifikant ungünstiger (P = 0,08) im Vergleich zum ausgestalteten Käfig. Dies könnte
Chapter IX: Erweiterte Zusammenfassung
125
möglicherweise auf eine vermehrte Kollision des Brustbeins mit den auf verschiedenen
Ebenen installierten Sitzstangen zurückgeführt werden, sowie auf eine hohe mechanische
Belastung des Brustbeins während der Sitzstangennutzung. Weiterhin zeigte die
Sitzstangenmodifikation HH einen signifikant ungünstigeren Einfluss auf den Brustbeinstatus
im Vergleich zu Hennen aus dem Aviplus. In der Untersuchung wurde eine positive
Korrelation von Residuen der Tibiabruchfestigkeit und Residuen des Merkmals
Brustbeinstatus nachgewiesen, jedoch konnten weder die modifizierte Kleingruppe noch das
Volierenhaltungssystem das Brustbein in seiner Festigkeit derart stärken, dass es Kollisionen
mit Sitzstangen oder vermehrter Druckbelastung standhalten konnte. Für die Legelinie LS
konnten die erhöhten Sitzstangen in der Kleingruppe nicht dazu beitragen, die
Humerusbruchfestigkeit zu verbessern, während positive Ergebnisse auf die
Tibiabruchfestigkeit nachweisbar waren. Der Brustbeinstatus erwies sich insbesondere bei
Tieren aus Volierenhaltung als problematisch und in der modifizierten Kleingruppe zeigten
sich eindeutige Tendenzen hin zu einem ungünstigeren Brustbeinzustand im Vergleich zum
Aviplus. Hinsichtlich der Eiqualitätsuntersuchungen konnten zwischen den untersuchten
Haltungssystemen keine Unterschiede in der Schalenfestigkeit, -dicke- und dichte sowie im
Schalengewicht festgestellt werden. Auffällig war jedoch ein hoher Anteil von Knick-, Bruch-
und Schmutzeiern in der Kleingruppe im Vergleich zu den übrigen zwei Haltungssystemen.
Ursächlich wurde hier ein erhöhter Rückstau und damit Kollisionsgefahr der Eier vor den
Legenestern vermutet, bzw. ein eventuelles Legen der Eier von den erhöhten Sitzstangen.
Das Ziel der Untersuchungen im VS Wesselkamp war es, den Einfluss der
Sitzstangenanordnung und der unterschiedlichen Gruppengrößen auf die oben genannten
Parameter bei den Legelinien LB und LSL zu untersuchen. Bei den LSL Hybriden handelte es
sich um Weißleger, welche sich durch ein geringeres Körpergewicht im Vergleich zu den
übrigen Legelinien auszeichneten. Im ersten Legedurchgang konnte für beide Legelinien kein
signifikanter Unterschied in der Humerus- und Tibiabruchfestigkeit sowie im Brustbeinstatus
zwischen den untersuchten Haltungssystemen festgestellt werden. Die im zweiten
Legedurchgang in der Kleingruppenhaltung EV 625a-EU installierten, drei verschiedenen
Varianten der Sitzstangenerhöhung hingegen übten einen signifikant positiven Einfluss auf
die Humerus- und Tibiabruchfestigkeit aus. Die in der Kleingruppe gemessenen
Knochenfestigkeiten unterschieden sich signifikant von dem ausgestalteten Käfig Aviplus.
Darüber hinaus wiesen Hennen aus Abteilen mit den Sitzstangenvarianten HH und VH eine
signifikant höhere Humerusbruchfestigkeit im Vergleich zu der Variante ST aus, während die
Chapter IX: Erweiterte Zusammenfassung
126
Tibiabruchfestigkeit nicht durch unterschiedliche Sitzstangenanordnungen innerhalb der
Abteile beeinflusst wurde. Im System Eurovent 625A-EU, welches in den beiden
untersuchten Legedurchgängen eine identische Sitzstangenanordnung hatte, zeigten Hennen
im zweiten Versuchsdurchgang eine signifikant höhere Humerus- und Tibiafestigkeit im
Vergleich zum Aviplus, was die im ersten Durchgang beobachtete Tendenz verifizierte.
Die auf verschiedenen Ebenen installierten Sitzstangen im EV 625a-EU schienen analog zu
den Beobachtungen auf dem LuFG Ruthe einen ungünstigen Einfluss auf den Brustbeinstatus
der LSL Hennen zu haben. Hennen zeigten einen nahezu signifikant ungünstigeren
Brustbeinstatus (P = 0,058) im Vergleich zum EV 625A-EU, wenn alle Abteile des EV 625a-
EU mit Sitzstangen auf zwei verschiedenen Ebenen ausgestattet waren. Die Gruppengrößen
übten keinen entscheidenden Einfluss auf die Knochenfestigkeit und den Brustbeinstatus der
LSL Hennen aus.
Zusammenfassend lässt sich sagen, dass die Sitzstangenmodifikationen im EV 625a-EU die
Humerus- und Tibiaknochenfestigkeit bei LSL Hennen positiv beeinflusste, während für die
Gruppengröße kein entscheidender Einfluss auf die Knochenfestigkeit nachgewiesen werden
konnte. Insbesondere die Sitzstangenanordnungen HH und VH im EV 625a-EU erwiesen sich
gegenüber der Variante ST als vorteilhaft. Obwohl die Knochenfestigkeit und der
Brustbeinstatus positiv korreliert waren, konnte die positive Beeinflussung der
Knochenfestigkeit durch das EV 625a-EU System jedoch nicht dazu beitragen, das Brustbein
vor Veränderungen durch Kollisionen oder lang anhaltender mechanischer Druckbelastung
durch Sitzstangennutzung zu schützen. In der Untersuchung wurde ein negativer Einfluss der
Kleingruppenhaltung mit modifizierten Sitzstangenhöhen auf den Brustbeinstatus manifest.
In einer weiteren Untersuchung wurde erstmalig die Stressbelastung bei LS Hybriden in
Kleingruppen mit modifizierten Sitzstangenpositionen (EV 625a-EU), ausgestalteten Käfigen
und einer Volierenhaltung (LuFG Ruthe) anhand des H/L-Ratios vergleichend ermittelt. Die
Ergebnisse dieser Studie zeigten, dass die in ausgestalteten Käfigen gehaltenen Hennen einer
im Vergleich zur Kleingruppe signifikant höheren und im Vergleich zur Voliere annähernd
signifikant höheren (P = 0,075) Stressbelastung unterworfen waren. Zwischen Tieren aus
Volierenhaltung und Kleingruppe hingegen konnte kein Unterschied im H/L-Ratio festgestellt
werden. Hennen, die im EV 625a-EU in Abteilen von 40 Tieren verbunden mit Sitzstangen in
der HH Variante gehalten wurden, zeigten einen signifikant niedrigeren H/L-Ratio und somit
eine geringere Stressbelastung im Vergleich zu Hennen in Abteilen von 10, 20 und 30 Tieren
aus dem Aviplus und vergleichend zu Hennen aus Abteilen des EV 625a-EU mit Sitzstangen
Chapter IX: Erweiterte Zusammenfassung
127
in der ST Variante. Die Unterschiede in der Stressbelastung der Tiere aus den 40-er Abteilen
der Kleingruppe (Variante HH) zum Volierenhaltungssystem erreichten annähernd
Signifikanz (P = 0,054). Bei einer Erweiterung des angewandten statistischen Modells konnte
gezeigt werden, dass Hennen aus der Kleingruppe (Gruppengröße 40, Variante HH) gegen
Ende der Legeperiode einen signifikant niedrigeren H/L-Ratio aufwiesen als Tiere aus
Volierenhaltung. In allen drei Haltungssystemen wurde ein signifikanter Anstieg des H/L-
Ratios vom 3. zum 12. Legemonat festgestellt. Die Ergebnisse zeigten, dass Hennen in
Kleingruppen (Gruppengröße 40, Variante HH) insbesondere gegen Ende der Legeperiode im
Vergleich zu den beiden anderen untersuchten Haltungssystemen der geringsten
Stressbelastung unterworfen waren. Die im hinteren Bereich der Abteile erhöhten Sitzstangen
des EV 625a-EU schienen einen sehr positiven Einfluss auf eine ungestörte
Sitzstangennutzung auszuüben und konnten somit in Verbindung mit einer Gruppengröße von
40 Hennen durch die geringste Stressbelastung das Wohlbefinden der Tiere steigern.
Ergänzend zur makroskopischen Beurteilung des Brustbeinstatus wurde in einer weiteren
Studie eine histologische Untersuchung ausgewählter Brustbeinpräparate durchgeführt. Ziel
dieser Untersuchung war es, die in einer Vielzahl von Untersuchungen zum Brustbeinstatus
angewandte makroskopische Klassifizierung anhand einer Notenskala von 1 bis 4 (1 =
hochgradig verändert, 2 = mittelgradig verändert, 3 = geringgradig verändert, 4 = ohne
besonderen Befund) histologisch zu überprüfen. Für die Untersuchung wurden Brustbeine
von allen vier der in dieser Studie verwendeten Legelinien untersucht. Die Probenahme
erfolgte zufällig und richtete sich ausschließlich nach Art der makroskopischen Bewertung.
Die Ergebnisse der Studie zeigten, dass Brustbeine, die makroskopisch als unauffällig
beurteilt wurden in 97,9 % der Fälle auch in der histologischen Untersuchung keinen
besonderen Befund aufwiesen. Bei 2,1 % der Präparate konnten histologisch schmale
periostale Exostosen entlang der intakten Kompakta nachgewiesen werden. Diese wurden als
natürliche Reaktion des Knochengewebes auf vermehrte mechanische Belastung gedeutet, um
die Knochenstruktur zu stützen. Bei mittelgradig veränderten Brustbeinen wurde in insgesamt
80,0 % der Fälle eine umfangreiche Geflechtknochenbildung beobachtet. Davon konnte bei
37,5 % der Tiere zusätzlich eine eindeutige Dislokation der Frakturenden (Kompakta)
festgestellt werden. Eine Ausbildung von Geflechtknochen ist stets ein Indikator für eine
vorangegangene Knochenfraktur, welche mit Schmerzen für das betreffende Tier verbunden
ist. In 10,0 % der Fälle mittelgradig deformierter Brustbeine wurden schmale, periostale
Exostosen entlang der Kompakta nachgewiesen und in weiteren 10,0 % der Fälle war das
Chapter IX: Erweiterte Zusammenfassung
128
Brustbein histologisch unauffällig bzw. wies eine leichte s-förmige Verbiegung auf, jedoch
ohne Ausbildung von Frakturkallus. Bei makroskopisch hochgradig veränderten Brustbeinen
wurden histologisch ausschließlich Veränderungen an der Knochenstruktur festgestellt.
Geflechtknochenbildung wurde in 73,3 % der Fälle beobachtet und in weiteren 26,7 %
wurden zusätzlich deutlich sichtbare Dislokationen der Frakturenden beobachtet.
Geringgradig veränderte Brustbeine stellten sich bei der makroskopischen Beurteilung und
der anschließenden histologischen Befundung sehr uneinheitlich dar. Während in 40,7 % der
Fälle histologisch entweder keine Veränderung bzw. lediglich eine Verbiegung des
Brustbeins ohne eine Ausbildung von Geflechtknochengewebe beobachtet wurde, traten bei
40,7 % der untersuchten Präparate Geflechtknochenbildungen. In 10,2 % der Fälle wurde
neben der Ausbildung von Geflechtknochen zusätzlich eine deutlich sichtbare Dislokation der
Frakturenden gefunden. Bei 8 % der makroskopisch unveränderten Präparate konnten
schmale periostale Ektostosen entlang der intakten Kompakta nachgewiesen werden. Die
Ergebnisse dieser Studie zeigten, dass die histologische Befundung des Brustbeins die
makroskopische Beurteilung hinsichtlich der Noten 4, 2 und 1 sehr gut widerspiegelt.
Geringgradig veränderte Brustbeine zeigten zu etwa gleichen Teilen eine durch vermehrte
Druckbelastung bei der Sitzstangennutzung entstandene Adaption des Brustbeins, welche
vermutlich nicht mit Schmerzen für das betroffenen Tier verbunden war, beziehungsweise
eine traumatisch bedingte, und somit mit Schmerzen verbundene, Ausbildung von
Geflechtknochengewebe. Die makroskopische Beurteilung von geringgradig veränderten
Brustbeinen im Hinblick auf Wohlergehen und insbesondere Schmerzempfindung bei Hennen
wurde ohne begleitende histologische Untersuchung als unzureichend angesehen.
Aufgrund der Komplexität des Gesamtprojektes, wurden die zu erhebenden Daten zu Beginn
der Untersuchung auf zwei Dissertationen, die jeweils in kumulativer Form verfasst worden
sind, aufgeteilt. In der abschließenden Meta-Analyse und Diskussion ausgewählter
gesundheits-, verhaltens- und leistungsbezogener Parameter wurden die Daten beider
Dissertationen zusammen geführt. Darüber hinaus wurden bereits veröffentlichte Daten
früherer Autoren, deren Studien mit identischer Methodik ebenfalls auf dem LuFG Ruthe und
im VS Wesselkamp durchgeführt worden sind, in die Meta-Analyse einbezogen. Diese
umfasst somit eine Gesamtauswertung von insgesamt zehn untersuchten Legedurchgängen
innerhalb des Zeitraumes 1999-2006. Für die Meta-Analyse wurden die LS-Mittelwerte aus
jedem Legedurchgang pro Ort der Untersuchung, Haltungssystem und Legelinie für
Humerus- und Tibiaknochenfestigkeit, Brustbein-, Gefieder- und Fußballenstatus
Chapter IX: Erweiterte Zusammenfassung
129
(Sohlenballenhyperkeratose, Sohlenballenläsion), Legeleistung, Mortalität,
Eischalenfestigkeit sowie für bestimmte in ausgestaltetem Käfig und Kleingruppenhaltung
erfasste Verhaltensmerkmale der Hennen ausgewählt. Die untersuchten Haltungssysteme
waren konventionelle Käfige, zwei Varianten eines ausgestalteten Käfigs (Aviplus, EV 625A-
EU), Kleingruppenhaltungen (EV 625a-EU), ein Volierensystem (Voliere „Natura“), sowie
eine intensive Auslaufhaltung. Die Meta-Analyse erfolgte anhand eines linearen Weighted
Least Square Modells (Prozedur GLM von SAS, Option „weight“), wobei die Reziprokwerte
der zugehörigen quadrierten Standardfehler (SE) als Gewichtung verwandt wurden. Das
Haltungssystem, der Untersuchungsort innerhalb des Haltungssystems, sowie die Legelinie
wurden als fixe Effekte berücksichtigt. Das Haltungssystem übte einen signifikanten Einfluss
auf die Merkmale Humerus- und Tibiabruchfestigkeit, Sohlenballenhyperkeratose,
Legeleistung, Mortalität und Sandbaden auf dem Drahtboden aus, während für die Merkmale
Brustbeinstatus, Sohlenballenläsion, Gefiederstatus, Eischalenfestigkeit sowie für die übrigen,
ausgewählten Verhaltensparameter kein signifikanter Einfluß des Haltungssystems beobachtet
werden konnte. Hennen aus konventioneller Käfighaltung zeigten im Vergleich zu allen
übrigen Haltungssystemen eine geringere Humerus- und Tibiafestigkeit. Bei den in der
Voliere gehaltenen Hennen konnte eine höhere Humerus- und Tibiabruchfestigkeit im
Vergleich zu Hennen aus den beiden Varianten des ausgestalteten Käfigs und der
Kleingruppenhaltung nachgewiesen werden. Eine Ausnahme bildeten Hennen aus EV 625A-
EU, welche eine mit der Volierenhaltung vergleichbare Tibiafestigkeit aufwiesen und sich in
diesem Merkmal signifikant von Hennen aus Aviplus und der Kleingruppenhaltung
abgrenzten. Hennen aus Volierenhaltung zeichneten sich durch einen ungünstigeren
Brustbeinstatus im Vergleich zur Kleingruppenhaltung aus, sowie durch eine geringere
Legeleistung und höhere Mortalitätsrate. Hennen in der Kleingruppe wiesen vermehrt
hyperkeratotische Veränderungen am Sohlenballen im Vergleich zum Aviplus System auf,
während sich Hennen aus den übrigen Haltungsformen in diesem Merkmal nicht voneinander
unterschieden. Die höchste Legeleistung und die geringsten Mortalitätsraten wurden in den
beiden Varianten des ausgestalteten Käfigs und in der Kleingruppenhaltung erzielt. Die
Legeleistung der Hennen aus Volierenhaltung war geringer im Vergleich zu den
ausgestalteten Käfigen und der Kleingruppenhaltung, jedoch höher verglichen mit der
intensiven Auslaufhaltung. Die Ergebnisse der Meta-Analyse zeigten dass sich die technische
Weiterentwicklung der Legehennenhaltungssysteme von der konventionellen Käfighaltung
hin zu ausgestalteten Käfigen und Kleingruppen positiv auf die erfassten gesundheits- und
leistungsbezogenen Merkmale ausgewirkt hat. Die Volierenhaltung konnte in den Merkmalen
Chapter IX: Erweiterte Zusammenfassung
130
Humerus- und Tibiaknochenfestigkeit nicht übertroffen werden, wobei Hennen aus EV 625A-
EU eine vergleichbare Tibiafestigkeit aufweisen konnten. Gegenüber alternativen
Haltungsformen sind in den ausgestalteten Käfigen und Kleingruppensystemen bestimmte
Verhaltensweisen immer noch stark eingeschränkt beziehungsweise werden fehlgeleitet, wie
zum Beispiel das vermehrt bei Hennen im Aviplus beobachtete Sandbadeverhalten auf dem
Drahtboden, so dass eine stetige Weiterentwicklung hinsichtlich artgerechter Tierhaltung bei
gleichbleibender Wirtschaftlichkeit erforderlich ist.
Appendix
Appendix
Non-elevated perches (NE) Front perch elevated (FE)
Back perch elevated (BE) Stepped position (ST) Figure 1: Schematic cross-section of perch positions within
compartments of small group systems; 1: supply pipe for dust
bathing substrate; 2: back perch; 3: front perch; 4; nipple drinkers.
Figure 2: Cross-section of three-tier small group housing system
Eurovent 625a-EU with non-elevated perches.
4
3 2 1
Big Dutchman, Vechta, Germany
131
Appendix
Figure 3: Compartment of small group housing system Eurovent 625a-EU (60 hens) with
elevated back perches.
Nest box
Front perch Elevated back perch
Dust bath
Dust bath
Back perch
Elevated front perch
Next box
Big Dutchman, Vechta, Germany, modified
Big Dutchman, Vechta, Germany, modified
Figure 4: Compartment of small group housing system Eurovent 625a-EU (40 hens) with
elevated front perches.
132
Appendix
Figure 5: Lohmann Silver laying hens kept in a compartment of
Eurovent 625a-EU with elevated front perches.
Big Dutchman, Vechta, Germany
Figure 6: Compartment of the furnished cage system Aviplus (10 hens).
133
Appendix
Compartment 01 02 03 04 05 06 07 08 09 10 Group size 40 60 60 60 40 40 40 40 60 60 Perch variant NE NE NE NE NE NE NE NE NE NE
Tier 3 LM 3 2 3 LT 3 LT 2 2 LT 3 LM 6 3 LT 2 2 LT 3 LM 9 2 3 3 2 LT LT 2 LT 3 LM 12 3 2 LT LT 2 3
Tier 2 LM 3 3 3 2 LT 2 3 LT
LM 6 2 LT 3 2 LT 2 3 LT LM 9 3 3 3 2 LT 2 LT
LM 12 2 LT 2 LT 2 3 LT 3 Tier 1
LM 3 3 LT 2 2 LT 3 LM 6 2 3 LT 3 LT 2 2 LT 3 LM 9 3 2 2 3 LT LT
LM 12 2 3 LT 3 LT 2 2 LT 3 Figure 7: Number of hens (Lohmann Silver, Lohmann TraditionLT) taken out of
compartments of Eurovent 625a-EU in laying month (LM) 3, 6, 9 and 12 of laying trial
004/2005, Farm Ruthe; NE: perches non-elevated. 2
Compartment 01 02 03 04 05 06 07 08 09 10 Group size 60 40 60 60 40 40 40 40 60 60 Perch variant ST ST BE B BE FE ST ST ST E BE
Tier 3 LM 3 2 2 2 2 LM 6 2 2 2 2 LM 9 2 2 2 2 LM 12 6 6 6 6
Tier 2 LM 3 3 3 3 3 LM 6 3 3 3 3 LM 9 3 3 3 3 LM 12 3 3 3 3
Tier 1 LM 3 3 3 3 3 LM 6 3 3 3 3 LM 9 3 3 3 3 LM 12 3 3 3 3 Figure 8: Number of hens (Lohmann Silver) taken out of compartments of Eurovent 625a-
EU in laying month (LM) 3, 6, 9 and 12 of laying trial 2005/2006, Farm Ruthe; ST: stepped
osition; BE: back perch elevated; FE: front perch elevated. p
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Appendix
Compartment 01 02 03 04 05 06 07 08 09 10 11 12 13 14 15 Group size 60 60 60 60 60 60 40 40 40 40 40 40 40 40 40
T ei r 4 Perch variant NE NE NE NE NE N N NE NE NE N NENE E E NE NE ELM 6 2 2 2 LB 2 LB 2 2 2 LB 2 LB LM 12 2 2 2 LB 2 LB 2 2 2 LB 2 LB
Tier 3 Perch variant N N NE N NE NE N NE NE NE NENE NE E E E NE NE ELM 6 2 LB 2 LB 2 2 2 LB 2 LB 2 2 LM 12 2 LB LB B LB2 2 2 2 L 2 2 2
T ei r 2 Perch variant BE NE BE NE BE NE BE NE BE NE BE NE BE NE BELM 6 LM 12
T ei r 1 Perch variant B B B BE BE BE B BE BE BE BEBE BE E E E BE BE ELM 6 2 2 4 2 2 2 2 LB LB LB LB
LM 12 2 LB 2 LB 4 2 LB 2 LB 2 2 Figure 9: Number of hens (Lohmann Selected Leghorn, Lohmann BrownLB) taken out of
compartments of Eurovent 625a-EU in laying month (LM) 6 and 12 of laying trial
004/2005, Farm Wesselkamp; NE: non-elevated; BE: back perch elevated. 2
Compartment 01 02 03 04 05 06 07 08 09 10 11 12 13 14 15 Group size 60 60 60 60 60 60 40 40 40 40 40 40 40 40 40 Perch variant ST ST FE FE BE S ST FE F FE BE B BEB SE T T E E
Tier 4 LM 6 2 2 2 2 2 2 LM 12 2 2 2 2 2 2
T er 3i LM 6 2 2 2 2 2 2 LM 12 2 2 2 2 2 2
Tier 2 LM 6 2 2 2 2 2 2 LM 12 2 2 2 2 2 2
T er 1i LM 6 2 2 2 2 2 2 LM 12 2 2 2 2 2 2 Figure 10: Number of hens (Lohmann Selected Leghorn) taken out of compartments of
Eurovent 625a-EU in laying month (LM) 6 and 12 of laying trial 2005/2006, Farm
esselkamp; ST: stepped position; FE: front perch elevated; BE: back perch elevated. W
135
Appendix
136
t
Compartmen 01 02 03 04 05 06 07 08 09 10 11 12 13 14 15 Group size 30 30 30 30 30 30 20 20 20 20 20 20 20 20 20
Tier 4 Perch variant N N NE NE N N NE NE NE E NE NE NE NE E NE NE E ELM 6 2R 1L * 2R* 1L* 2R 1L * 2R* 1L* * * LM 12 2R 1L * 2R* 1L* 2R 1L * 2R* 1L* * *
Tier 3 Perch variant F F F F FE FE FE FE FEFE FE E E FE FE E FE FE ELM 6 2R* 1L* * 2R 1L * 2R* 1L* * 2R 1L LM 12 2R* 1L* * 2R 1L * 2R* 1L* * 2R 1L
Tier 2 Perch variant B F BE FE B F BBE FE E E BE FE BE FE E E BE FE ELM 6 2L 1R * 2R* 1L* 2L 1R * * 2L* 1R* * LM 12 2L 1R * 2R* 1L* 2L 1R * * 2L* 1R* *
Tier 1 Perch variant NE NE NE NE NE N NE N NENE NE NE NE E NE NE ELM 6 * 2R* 1L* 2R 1L 2R* 1L* * 2R 1L LM 12 * 2R* 1L* 2R 1L 2R* 1L* * 2R 1L Figure 11: Number of hens (Lohmann Selected Leghorn, Lohmann Brown*) taken out of
compartments of Eurovent 625A-EU in laying month (LM) 6 and 12 of laying trial
2004/2005, Farm Wesselkamp; NE: non-elevated; FE: front perch elevated; BE: back perch
levated.
t
e
Compartmen 01 02 03 04 05 06 07 08 09 10 11 12 13 14 15 Group size 30 30 30 30 30 30 20 20 20 20 20 20 20 20 20
Tier 4 Perch variant NE NE NE NE NE NE NE NE N NENE NE NE NE NE ELM 6 2R 2R 2L 2R 2R 2L LM 12 2R 2R 2L 2R 2R 2L
T ei r 3 Perch variant F F FE FE FE FE FE FE FE FEFE FE E E FE FE FELM 6 2R 2L 2R 2R 2L 2R LM 12 2R 2 2RL 2R 2L 2R
Tier 2 Perch variant B B B BBE BE E BE BE E E ELM 6 2L 2L 2R 2L 2L 2R LM 12 2L 2L 2R 2L 2L 2R
Tier 1 Perch variant NE NE NE NE NE NE NE NE N NENE NE NE NE NE ELM 6 2R 2R 2L 2R 2R 2L LM 12 2R 2R 2L 2R 2R 2L Figure 12: Number of hens (Lohmann Selected Leghorn) taken out of compartments of
Eurovent 625A-EU in laying month (LM) 6 and 12 of laying trial 2005/2006, Farm
Wesselkamp; NE: non-elevated; FE: front perch elevated; BE: back perch elevated.
Appendix
137
Appendix
138
Appendix
139
Appendix Appendix
140
140
Appendix
Figure 17: Normal (grade 4, left), slightly deformed (grade 3, middle) and moderately
deformed (grade 2, right) keel bone.
Figure 18: Severely deformed (grade 1) keel bone after removal of
breast muscles.
141
Appendix
Figure19: Heterophil granulocyte surrounded by erythrocytes.
Figure 20: Lymphocyte surrounded by erythrocytes.
Figure 21: Eosinophil granulocyte surrounded by erythrocytes.
142
Appendix
50%
60%
70%
80%
90%
100%
0 50 100 150 200 250 300 350
Aviplus - LSL EV 625A-EU - LSL
EV 625a-EU - LSL
Figure 22: Laying performance (%) per hen housed of the layer line Lohmann
Selected Leghorn (LSL), trial period 2004/2005, Farm Wesselkamp.
50%
60%
70%
80%
90%
100%
0 50 100 150 200 250 300 350
Aviplus - LB EV 625A-EU - LB
EV 625a-EU - LB
Figure 23: Laying performance (%) per hen housed of the layer line Lohmann
Brown (LB), trial period 2004/2005, Farm Wesselkamp.
143
Appendix
50%
60%
70%
80%
90%
100%
0 50 100 150 200 250 300 350
Aviplus - LSL EV 625A-EU - LSL
EV 625a-EU - LSL
Figure 24: Laying performance (%) per hen housed of the layer line Lohmann
Selected Leghorn (LSL), trial period 2005/2006, Farm Wesselkamp.
50%
60%
70%
80%
90%
100%
0 50 100 150 200 250 300 350
Aviplus - LS EV 625a-EU - LS
Voliere - LS
Figure 25: Laying performance (%) per hen housed of the layer line Lohmann
Silver (LS), trial period 2005/2006, Farm Ruthe.
144
Appendix
100,0 Aviplus - LSL
99,5 EV 625A-EU
99,0 LSL
98,5 EV 625a-EU -LSL
98,0 Aviplus - LSL
97,5 EV 625A-EU -LSL 97,0
96,5 EV 625a-EU -LSL
96,0
95,5
95,0 0 50 100 150 400 200 250 300 350
Figure 26: Survival rate (%) of the layer line Lohmann Selected Leghorn (LSL),
trial period 2004/2005, Farm Wesselkamp.
Figure 27: Survival rate (%) of the layer line Lohmann Brown (LB), trial period
2004/2005, Farm Wesselkamp.
97,0
97,5
98,0
98,5
99,0
99,5
100,0 Av
EA
Ea
Aviplus - LB
EV 625A-EU -LB
EV 625a-EU -LB
0 50 100 150 400 200 250 300 350
145
Appendix
92,0
93,0
94,0
95,0
96,0
97,0
98,0
99,0
100,0
0 50 100 150 200 250 300 350 400
Ea
Avi
Vol
EV 625a-EU - LS
Aviplus - LS
Voliere - LS
Figure 28: Survival rate (%) of the layer line Lohmann Silver (LS), trial period
2005/2006, Farm Ruthe.
146
Appendix
147
Table 1: Number (n), mean ( x ), standard deviation (SD), range (min/max), median ( x~ ) and
25%/75%-quantiles (Q1/Q3) of humerus and tibia bone strength [N], keel bone status, egg
quality traits and egg production per hen present (Farm Ruthe, 2nd trial period, chapter 3).
Trait n x SD min max x~ Q1 Q3 Humerus bone strength (N) 428 205.1 76.2 77.2 511.1 185.4 148.3 256.8 Tibia bone strength (N) 432 135.3 34.2 61.2 284.9 135.9 114.7 153.0 Keel bone status (1-4) 430 3.5 0.7 1 4 - - - Shell breaking strength (N) 3892 42.8 9.3 6.5 71.4 43.6 37.4 49.0 Shell thickness (µm) 3893 344.0 26.5 131 463 344 327 361 Shell density (mg/cm²) 3893 85.7 6.1 51.3 122.2 85.7 81.8 89.5 Shell weight (g) 3893 6.2 0.6 3.3 9.0 6.2 5.8 6.6 Haugh units 3893 82.1 9.2 5.1 107.7 83.2 77.3 88.2 Blood spots (1-2) 3893 0.1 0.3 0 2 - - - Meat spots (1-2) 3893 0.9 0.4 0 2 - - - Albumen height (mm) 3893 7.0 1.3 1.8 11.7 7.0 6.2 7.8 Yolk weight (g) 3891 17.1 1.9 10.0 32.0 17.2 15.9 18.4 Yolk color (1-15) 3893 12.6 0.8 9 15 13 12 13 Egg weight (g) 3893 60.9 4.9 43.5 92.7 60.8 57.5 64.0 Egg production (%) 1152 87.0 0.2 - - - - -
Acknowledgements
Firstly, I sincerely and very gratefully wish to thank Prof. Dr. Dr. habil. Ottmar Distl who
gave me the opportunity to work on this interesting scientific project and who very kindly
provided continous support and help during the preparation of this dissertation.
I am very grateful to my colleague Swaantje Rönchen for providing an excellent working
atmosphere and for bringing up many useful discussions and inspirations, which fruitfully
contributed to the outcome of this thesis.
A special thank goes to Dr. Henning Hamann who guided me throughout the process of
statistical analysis with an excellent knowledge, patience and always in a very friendly
manner.
I would like to thank Deutsche Frühstücksei GmbH, Big Dutchman GmbH and Lohmann
Tierzucht GmbH for their financial support of this project.
I would like to acknowledge Prof. Dr. Ulrich Neumann, PD Dr. Gerhard Glünder and Dr.
Martin Ryll for their scientific and organisational support throughout the trial periods.
I am very glad to mention Sonja Bernhard who was an essential help in conducting laying
hens’ autopsies. Without her very kind support, experiments on these particular trial days
would not have been feasible.
I am very grateful to Harald Ulbrich. He very kindly and encouragingly assisted in bone
dissections and blood sampling.
I would like to thank Mrs Cornelia Mrusek and Mrs Doris Böhm for their kind support in all
kinds of organisational issues. I would also like to mention Jörn Wrede who kindly provided
help in all matters of computing problems.
I am very grateful to Julian Sander and Johanna Siemen for their excellent support in
preparing blood smears and conducting laying hens’ autopsies.
A special thank goes to Dr. Anne Vits and Dr. Daniela Weitzenbürger. They very kindly and
thoroughly introduced my colleague and me to this scientific project, while providing an
excellent working environment.
I would also like to thank Prof. Dr. Marion Hewicker-Trautwein and Dr. Martin Peters for
being an excellent source of advice in helping me evaluate histological keel bone samples.
I am glad to mention Bettina Buck and I would like to thank her for her very friendly and kind
support in preparing histological samples.
I wish to thank Mr Brinkmann for his continous and very reliable support in collecting data at
the trial farm Wesselkamp, Ankum.
I am also grateful to Dr. Christian Sürie for his advice and kind support in all kinds of issues
related to the trial farm Ruthe.
My family deserves a very special acknowledgement for their continous support and care.
Without their help, the preparation of this dissertation thesis would not have been possible.