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Performance, Livability, and Carcass Yield of Slow- and Fast-Growing
Chicken Genotypes Fed Low-Nutrient or Standard Diets
and Raised Indoors or with Outdoor Access
A. C. Fanatico,* P. B. Pillai,* P. Y. Hester,† C. Falcone,‡ J. A. Mench,‡ C. M. Owens,* and J. L. Emmert*
1
*Center for Excellence in Poultry Science, University of Arkansas, Fayetteville 72701; †Department of Animal Sciences,
Purdue University, West Lafayette, IN 47907; and ‡Department of Animal Science, University of California, Davis 95616
ABSTRACT Two experiments were conducted to assess
the effect of genotype, production system, and nutrition
on performance and livability of meat chickens for niche
markets. Slow-growing (SG) and fast-growing genotypes
(FG) were raised for 91 and 63 d, respectively, in experi-
ment 1 (females) or 84 and 56 d, respectively, in experi-
ment 2 (males). In each trial, SG were placed before FG
to achieve a similar BW at processing. In experiment 1,
each genotype was assigned to 8 pens of 20 birds each,
with 4 pens within each genotype raised indoors in a
conventional research facility or in a small facility with
outdoor access. All birds were fed a low-nutrient diet. In
experiment 2, genotype assignment to pens was as in
experiment 1; however, 4 pens within each genotype were
fed a low-nutrient diet or a conventional diet, and birds
were raised indoors. Birds were gait-scored and commer-
cially processed; legs were examined for tibial dyschon-
droplasia lesions and scanned for bone mineral density.
Key words: broiler, free range, organic, growth performance, livability
2008 Poultry Science 87:1012–1021
doi:10.3382/ps.2006-00424
INTRODUCTION
Interest in alternative animal production systems and
alternatively produced products has increased at a rapid
rate in recent years. Alternative animal production sys-
tems are typically designed to address a variety of con-
cerns held by consumers and independent producers.
Although alternative poultry production systems vary
greatly in size and composition, most systems are de-
signed to address one of the foremost concerns of some
consumers: access to the outdoors. Products from these
systems are often labeled as free range, which although
not specifically defined by the USDA may be used on
labels after a review process, in which the producer sub-
mits written documentation that describes how outdoor
©2008 Poultry Science Association Inc.
Received December 11, 2006.
Accepted February 8, 2008.
1
Corresponding author: jemmert@uark.edu
1012
In experiment 1, FG gained more weight than SG (P<
0.05) even though they were placed later. Outdoor access
increased feed intake, and feed efficiency was poorer (P
<0.05). Fast-growing genotypes had higher breast meat
yield, whereas SG had higher wing and leg yields (P<
0.05). In experiment 2, the low-nutrient diet reduced (P
<0.05) gain of the SG; FG increased feed intake of the
low-nutrient diet such that their gain was unaffected (P
>0.05). For FG, the low-nutrient diet resulted in a poorer
(P<0.05) feed efficiency. Although weight gain of the
FG was maintained on the low-nutrient diet, breast yield
was reduced (P<0.05). Genotype affected bone health in
both experiments, with SG having better gait scores and
less tibial dyschondroplasia (P<0.05). Outdoor access
and the low-nutrient diet also resulted in better gait score
(P<0.05). These data indicate differences among geno-
types and provide information about the efficiency and
potential for alternative poultry systems.
access is provided (USDA, 2006a). In addition to outdoor
access, many consumers are interested in obtaining or-
ganic poultry products. For organic production, a strict
set of standards must be followed in addition to outdoor
access, including the use of 100% organic feed grown
without synthetic chemicals and without growth promo-
tants or antibiotics (USDA, 2006b). European alternative
production systems are typically governed by more com-
prehensive standards, which in some cases even dictate
the genotype and dietary nutrient levels that can be used
(European Union, 1991). The Label Rouge program, for
example, requires the use of slow-growing genotypes and
dictates that a high level of cereal grains be used, thus
limiting the amount of protein that is provided (Ministe
`re
de L’Agriculture, 1996).
As interest in alternative poultry production continues
to grow in the United States; it is possible that more
strictly defined production systems could develop, in
which the use of certain genotypes or specified dietary
nutrient levels is dictated, similar to some European sys-
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ALTERNATIVE PRODUCTION SYSTEM AND GENOTYPE PERFORMANCE 1013
tems. In the United States, the conventional broiler from
a cross of Cornish and White Rock chickens is typically
used in both conventional and alternative poultry produc-
tion; it is an efficient bird that reaches market weight in
42 d. However, it was primarily developed for use in
indoor, climate-controlled conditions. Alternative pro-
duction systems are influenced by concerns about animal
behavior and welfare, which includes the incidence of leg
disorders and livability. A slower-growing genotype that
shows more foraging behavior and has a different body
conformation could be more suitable for production sys-
tems that provide outdoor access.
Very little data about growth performance and carcass
yield are available for slow-growing genotypes. Further-
more, the effect of feeding low-nutrient diets, similar to
those fed in the Label Rouge program, on growth perfor-
mance in alternative and conventional chicken genotypes
has not been assessed in alternative production systems in
the United States. Fanatico et al. (2005) described growth
patterns for slow-, medium-, and fast-growing genotypes
fed an industry-type diet, but information about the effect
of outdoor access was limited, and low-nutrient diets
were not tested. The potential use of alternative genotypes
is not strictly a performance-based decision, but as the
alternative market grows in response to increased con-
sumer concerns, there is a need to quantify the effect of
production system and diet on growth performance. This
information would provide producers with realistic data
to use in their production decisions. The objective of this
study was to investigate the effect of production system
(indoor vs. access to outdoors), genotype (fast- vs. slow-
growing), and diet (conventional vs. low-nutrient) on
growth, livability, bone health, and carcass yield of meat-
type chickens.
MATERIALS AND METHODS
Two experiments were conducted at the University of
Arkansas Poultry Research Farm from August to Novem-
ber 2004. All procedures were approved by the University
of Arkansas Institutional Animal Care and Use Commit-
tee. In both experiments, a slow-growing genotype (S &
G Poultry LLC, Clanton, AL) and a typical fast-growing
genotype (Cobb, Siloam Springs, AR) were compared.
Although commercial slow-growing products are widely
available in Europe, there is little availability in the United
States. The companyS&GPoultry recently developed
a slow-growing chicken that requires approximately 12
wk to achieve the typical BW of an 8-wk-old commercial
broiler chicken but with a poorer feed efficiency and
lower breast yield (Fanatico et al., 2005). Because of the
difference in growth rate, chick placement dates in both
experiments were staggered in an attempt to reach a simi-
lar final BW at the time of processing, as previously re-
ported (Fanatico et al., 2005). In both experiments, 4
replicate pens per treatment containing 20 birds per pen
were used. Birds and feed were weighed for the determi-
nation of weight gain, feed intake, and feed efficiency
(adjusted for mortality). Feed and water were freely avail-
able in both trials. The fast-growing birds were gait-
scored at 56 d and the slow-growing at 84 d with the 0
to 5 gait score system of Garner et al. (2002), with a score
of 0 assigned to birds with no obvious gait impairment
and a score of 5 assigned to lame birds that cannot walk
(Garner et al., 2002). Birds were also examined for foot
pad dermatitis usinga0to2score system (Algers and
Berg, 2001), with a score of 0 representing no or very
small and superficial lesions and a score of 2 representing
a severe lesion with ulcers or scabs, signs of hemorrhages,
or a swollen food pad.
At trial termination, all birds were commercially pro-
cessed at the University of Arkansas Pilot Processing
Plant. Feed was withheld for 10 h before slaughter, and
birds were weighed individually at the plant. Automated
equipment was used for stunning, scalding, picking, vent
opening, and evisceration. Birds were electrically stunned
(11 V, 11 mA, 10 s) followed by scalding at 53°C for 120
s. Carcasses were prechilled at 12°C for 15 min and chilled
(immersion) at 1°C for 1 h. After chilling, carcasses were
aged on ice and breast fillets deboned from the carcass
at 4 h postmortem. Weights of breast (boneless, skinless),
wings, legs, and frame (carcass including skin but with
breast, wings, and legs removed) were recorded. Yield
was expressed as a percentage of chilled, ready-to-cook
(RTC) weight.
The incidence of tibial dyschondroplasia (TD) was de-
termined for all birds at the time of processing. The drums
were removed from the thighs at the femoral joint during
cut-up, and the proximal end of the tibiotarsus bone was
cut longitudinally to observe cartilage formation using
the following visual scoring: 0 = normal growth plate
with smooth contour and off-brown tincture; 1 = mild to
moderate with translucent cartilage thickened approxi-
mately to twice the size of normal; and 2 = severe with
opaque white cartilage widened to span more than twice
the size of a normal growth plate, indented or extending
into the metaphyses (Rath et al., 2004). The left wing and
drumstick were collected from an average of 2 birds per
replicate pen per treatment, resulting in a sample size of
6 to 11 observations per treatment. Samples were frozen
and express-mailed in dry ice to Purdue University,
where they were thawed and scanned with muscle and
skin intact using dual-energy x-ray absorptiometry for
determination of bone mineral density (BMD; Hester et
al., 2004).
Experiment 1: Production System
The objective of experiment 1 was to evaluate the effect
of production system (indoor vs. outdoor access) on the
performance of female slow- and fast-growing genotypes,
which were raised for 91 or 63 d, respectively. Birds were
randomly assigned to pens in a conventional indoor facil-
ity or a portable facility with outdoor access. The 4 treat-
ments consisted of slow-growing birds given outdoor
access, slow-growing birds that were confined indoors,
fast-growing birds given outdoor access, and fast-grow-
ing birds that were confined indoors.
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FANATICO ET AL.1014
Table 1. Composition of experimental diets
1
Conventional Low-nutrient
Ingredient Starter Grower I Grower II Finisher Starter Grower I Grower II Finisher
%
Corn 55.06 66.12 72.17 77.48 61.45 64.75 69.85 72.05
Soybean meal 37.18 27.94 22.61 18.08 29.00 21.00 15.00 10.50
Wheat middlings — — — — 6.00 11.00 12.00 14.30
Corn oil 3.96 2.31 2.05 1.29 — — — —
Dicalcium phosphate 1.20 1.30 1.10 1.10 1.40 1.20 1.00 1.00
Limestone 1.60 1.40 1.30 1.30 1.30 1.30 1.40 1.40
NaCl 0.40 0.40 0.30 0.30 0.40 0.30 0.30 0.30
Vitamin mix
2
0.20 0.20 0.20 0.20 0.20 0.20 0.20 0.20
Mineral mix
2
0.10 0.10 0.10 0.10 0.10 0.10 0.10 0.10
CholineⴢCl (60%) 0.10 0.10 0.10 0.10 0.10 0.10 0.10 0.10
DL
-Met 0.1563 0.0815 0.0174 — — — — —
Sacox salinomycin
3
0.05 0.05 0.05 0.05 0.05 0.05 0.05 0.05
Calculated composition
ME, kcal/kg 3,100 3,100 3,150 3,150 2,886 2,902 2,946 2,956
CP, % 22.9 19.4 17.4 15.7 20.5 17.7 15.5 13.9
Digestible Lys, % 1.10 0.89 0.76 0.65 0.94 0.76 0.62 0.52
Digestible Met, % 0.41 0.33 0.28 0.26 0.31 0.27 0.25 0.23
Digestible Cys, % 0.41 0.34 0.29 0.26 0.31 0.28 0.25 0.24
Digestible Thr, % 0.75 0.63 0.53 0.50 0.65 0.55 0.47 0.41
Ca, % 1.00 0.90 0.80 0.80 0.90 0.85 0.80 0.80
Nonphytate P, % 0.45 0.35 0.30 0.30 0.45 0.35 0.30 0.30
Protein:energy, g/kcal 0.74 0.63 0.55 0.50 0.71 0.61 0.53 0.47
1
Conventional diets were fed in experiment 2, whereas low-nutrient diets were fed in experiments 1 and 2.
2
Provided (per kilogram of diet): vitamin A, 7,715 IU (retinyl acetate); cholecalciferol, 2,204 IU; vitamin E, 16.5 IU (
DL
-α-tocopheryl acetate);
thiamin, 1.54 mg; niacin, 38.6 mg; riboflavin, 6.6 mg;
D
-calcium pantothenate, 9.9 mg; vitamin B
12
, 0.013 mg; vitamin B
6
, 2.8 mg;
D
-biotin, 0.07 mg;
folic acid, 0.88 mg; menadione dimethylpyrimidinol bisulfite, 3.30 mg; choline, 400 mg; ethoxyquin, 125 mg; Se, 0.1 mg; MnSO
4
ⴢH
2
O, 308 mg;
FeSO
4
ⴢ7H
2
O, 250 mg; ZnSO
4
ⴢ7H
2
O, 440 mg; CuSO
4
ⴢ5H
2
O, 39.3 mg; MgO, 43.9 mg; Ca(IO
3
)
2
ⴢH
2
O, 3.2 mg.
3
Sacox 60, Hoechst-Roussel Agri-Vet Co., Somerville, NJ. Provided 66 mg/kg of salinomycin activity.
Indoor treatments were grown in floor pens in a con-
ventional poultry research facility that contained a con-
crete floor, side curtains, and fans for ventilation and
cooling. Thermostatically controlled heater and gas
brooders, which extended along the length of the house,
were used to provide additional heat during brooding.
Indoor pens measured 1.8 m ×1.8 m (6.2 birds/m
2
) and
contained 1 bell waterer and hanging tube feeder. New
wood shavings were used as litter. A constant photope-
riod of 24 h was provided.
Birds with outdoor access were grown in a small porta-
ble facility measuring 3.7 m ×5.5 m. The portable facility
was not moved during the trial. The facility was insulated
and naturally ventilated but had no access to power. Pro-
pane space heaters were used to keep nighttime tempera-
tures above 15.5°C inside the house. No artificial lighting
was used, with photoperiod being limited to natural day-
light. The house was subdivided into 8 indoor pens that
opened to 8 separate yards, which were surrounded by
electric net fencing. The indoor area of each pen measured
1.2 m ×1.5 m (11.1 birds/m
2
). All pens allowed outdoor
access to grassy yards through bird exits (0.6-m width ×
0.5-m height). Birds were allowed access to the outdoors
during daytime hours, with the exception of 2 d during
the study period in which the outdoor temperature was
less than 4.4°C. The outdoor portion of each pen had an
area of 9.3 m
2
and was completely covered with grassy
vegetation. The indoor portion of each pen contained 1
fount-type waterer and hanging tube feeder, and the floor
was covered with fresh wood shavings. The outdoor por-
tion of each pen contained 1 waterer and a range-type
tube feeder with a rain shield.
All chicks were brooded in the indoor facility; chicks
in the treatments with outdoor access were moved to the
portable facility after 21 d of age. The temperature inside
the portable house during the study period ranged from a
high of 23.9°C to a low of 13.9°C; the temperature outside
ranged from a high of 22°C to a low of 2°C. There were
30 d of precipitation during the 71-d period when the
birds had access to the outdoors. The total precipitation
was 27.82 cm.
All birds were provided with multistage diets (Tables
1 and 2) that were formulated to be low in protein and
energy, similar to those used in the French Label Rouge
program (Lewis et al., 1997) for slow-growing birds. This
study was not conducted under USDA organic require-
ments, which require the use of 100% organic nonmedi-
cated feed. Although animal by-products were not used,
anticoccidial medication was included in the feed.
Experiment 2: Dietary Nutrient Level
The objective of experiment 2 was to evaluate the effect
of dietary nutrient level (conventional vs. low-nutrient)
on the growth performance and bone health of male slow-
and fast-growing genotypes, which were raised for 84 or
56 d, respectively. Birds in experiment 2 were raised for
a shorter period of time than birds in experiment 1 (con-
ducted concurrently), because processing capacity dic-
tated that the 2 experiments be terminated on different
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ALTERNATIVE PRODUCTION SYSTEM AND GENOTYPE PERFORMANCE 1015
Table 2. Design of dietary treatments (experiments 1 and 2)
Age range when diets were provided (wk) Age at
termination
Experiment Diet type Genotype Starter Grower I Grower II Finisher (wk)
1
1 Low-nutrient Slow-growing 0 to 4 4 to 8 8 to 10 10 to 13 13
1 Low-nutrient Fast-growing 0 to 4 4 to 8 8 to 9 NA
2
9
2 Conventional Slow-growing 0 to 4 4 to 8 8 to 10 10 to 12 12
2 Conventional Fast-growing 0 to 4 4 to 8 NA
2
NA
2
8
2 Low-nutrient Slow-growing 0 to 4 4 to 8 8 to 10 10 to 12 12
2 Low-nutrient Fast-growing 0 to 4 4 to 8 NA
2
NA
2
8
1
The fast-growing genotype was placed at a later date such that there was a single trial termination date.
2
The fast-growing genotype did not receive the finisher diet in experiment 1 or the grower II and finisher
diets in experiment 2.
days. Moreover, because of sex and diet differences, males
used in experiment 2 were expected to grow at a faster
rate than the females used in experiment 1. All birds
were housed in the conventional indoor facility described
above. Birds were randomly assigned to pens according
to experimental diet, which consisted of either a low-
nutrient diet (low in amino acids and energy as used
in experiment 1) or a more conventional diet that was
formulated according to NRC (1994) recommendations
(Table 1). Diets were provided in multiple phases (Table
1), and the 4 treatments consisted of slow-growing birds
fed the low-nutrient diets, slow-growing birds fed the
conventional diets, fast-growing birds fed the low-nutri-
ent diets, and fast-growing birds fed the conventional
diets. Specific ages associated with each diet are shown
in Table 2.
Statistical Analysis
Data were subjected to ANOVA using the GLM proce-
dure (SAS Institute, 2003) appropriate for a completely
randomized design. A factorial arrangement of treat-
ments was used. Treatment means were separated using
Fisher’s protected least significant difference multiple
comparison procedure. The proportions of gait and TD
scores were compared using a χ
2
test for equality of distri-
butions except in those cases in which small expected
counts may have substantially affected the approximate
P-value from the χ
2
. In those cases, Fisher’s exact test
was used (Fleiss, 2003). Because BW as a covariant was
significant, the BMD was analyzed using analysis of co-
variance with the factorial arrangement of treatments and
type of bone (tibia and humerus) as a subplot within the
individual bird (Steel et al., 1997). The mixed procedure
of the SAS system was used in the BMD analysis (SAS
Institute, 2003).
RESULTS AND DISCUSSION
Many factors affect growth performance of poultry in-
cluding genotype, production system, diet, age, sex,
stocking density, photoperiod, temperature, and activity.
Although stocking density, lighting, and temperature
varied and could have affected the results, the analysis
was limited to the controlled factors of interest, namely
genotype (slow- or fast-growing), nutrient level (low or
conventional), and production system.
Growth Performance
The type of production system tested did not affect
weight gain, but weight gain of the fast-growing genotype
exceeded (P<0.05) that of the slow-growing birds, even
though an attempt was made to reach a similar market
BW (Table 3). Previous research (Gordon and Charles,
2002; Fanatico et al., 2005) indicated that 84 to 91 d was
sufficient for the slow-growing birds to reach a live
weight of 2.0 to 2.5 kg, which is a typical live weight for
specialty poultry production. Fast-growing broilers have
been selected for rapid early growth and reach this market
weight in roughly 42 d, depending on diet and growing
conditions. Overall feed intake was not affected (P>0.05)
by genotype. The outdoor access production system in-
creased (P<0.05) feed intake of both genotypes but had
a greater effect on the feed intake of slow-growing birds.
As expected, feed conversion of the fast-growing birds
was better (P<0.05) than that of the slow-growing birds.
Feed conversion was worsened (P<0.05) by outdoor
access in both genotypes, and the effect was more pro-
nounced in the slow-growing birds.
A difference in feed conversion between these geno-
types was previously reported (Fanatico et al., 2005), even
when raised under indoor conditions. Slower-growing
birds would be expected to have a higher maintenance
requirement, which would affect feed conversion. Cold
temperatures are also known to increase feed intake and
worsen feed conversion. Experiment 1 was conducted
from August to November, and birds with outdoor access
were exposed to temperatures as low as 4.4°C during the
latter portion of the trial. Even when they did not venture
outdoors, birds housed in the unit that provided outdoor
access were exposed to a lower average temperature, be-
cause the bird doorways were usually open (except for
2 d when the outdoor temperature was below 4.4°C).
Therefore, temperature could in part explain the effect of
outdoor exposure on feed intake and feed conversion.
Foraging activity and exercise could also conceivably in-
crease feed intake and worsen feed conversion. Nielsen
et al. (2003) reported that slower-growing broilers used
an outdoor area more than faster-growing broilers, and
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FANATICO ET AL.1016
Table 3. Effect of genotype and production system on growth performance, bone health, and mortality (experiment 1)
Weight Feed
gain
2
intake
2
Feed:gain
2
BMD
3
Mortality
2
Genotype
1
Production system (g) (g) (g:g) (g/cm
2
) (%)
Slow-growing Outdoor access 2,254
b
8,459
a
3.75
a
0.193 3
b
Slow-growing Indoor 2,105
b
6,752
c
3.21
b
0.189 0
b
Fast-growing Outdoor access 3,370
a
8,087
a
2.40
c
0.183 11
a
Fast-growing Indoor 3,389
a
7,402
b
2.19
d
0.185 9
a
Pooled SEM 54 172 0.06 0.007 4
P-values
ANOVA
Genotype 0.0010 0.4362 0.0001 0.5283 0.0364
Production system 0.2545 0.0001 0.0001 0.8164 0.5137
Genotype ×production system 0.1451 0.0118 0.0151 0.5576 1.0000
a–d
Means within a column lacking a common superscript differ (P<0.05).
1
Slow- and fast-growing birds were grown for 91 or 63 d, respectively; placement dates were staggered such that there was a single trial
termination date.
2
Values are means of 4 pens of 20 female birds.
3
Bone mineral density (BMD) values (adjusted for BW) represent the mean averaged across the tibia and humerus with 18 to 19 observations
per mean.
in the current study, the slow-growing genotype was
much more active and appeared to forage more, whereas
the fast-growing birds rarely went outside, and when they
did, they grouped around the feeder or rested instead of
foraging. Differences in foraging and activity level likely
contributed to the different degree to which feed intake
and feed conversion of the slow- and fast-growing geno-
types were affected by outdoor access.
Birds of experiment 2 were raised indoors and were
fed a low-nutrient diet or a conventional diet (Table 1).
When compared with the conventional diet, the low-nu-
trient diet did not affect (P>0.05) weight gain of the fast-
growing birds and reduced (P<0.05) weight gain of the
slow-growing genotype (Table 4). Total weight gain of
the slow-growing birds fed the conventional diet was
similar (P>0.05) to that of the fast-growing birds fed
either diet. Weight gain responses are readily explained
by the interaction of diet composition and feed intake.
Fast-growing broilers were able to increase (P<0.05)
consumption of the low-nutrient diet to the extent that
Table 4. Effect of genotype and diet type on growth performance, leg health, and mortality (experiment 2)
Weight Feed
gain
2
intake
2
Feed:gain
2
BMD
3
Mortality
2
Genotype
1
Diet type (g) (g) (g:g) (g/cm
2
) (%)
Slow-growing Low-nutrient 2,593
a
7,994
a
2.96
a
0.192
b
1
b
Slow-growing Conventional 2,888
b
7,959
a
2.76
a
0.204
a
3
b
Fast-growing Low-nutrient 2,888
b
6,404
b
2.22
b
0.183
b
9
a
Fast-growing Conventional 2,808
b
5,546
c
1.97
c
0.203
a
19
a
Pooled SEM 38.0 143.0 0.08 0.007 4
P-values
ANOVA
Genotype 0.0154 0.0001 0.0001 0.4679 0.0123
Diet 0.0159 0.0088 0.0160 0.0439 0.1885
Genotype ×diet 0.0004 0.0139 0.8183 0.6032 0.2995
a–c
Means within a column lacking a common superscript differ (P<0.05).
1
Slow- and fast-growing birds were grown for 84 or 56 d, respectively; placement dates were staggered such
that there was a single trial termination date.
2
Values are means of 4 pens of 20 male birds.
3
Bone mineral density (BMD) values (adjusted for BW) represent the mean averaged across the tibia and
humerus with 18 to 22 observations per mean.
weight gain was maintained, although feed conversion
was worsened (P<0.05). In contrast, slow-growing broil-
ers apparently lacked the ability to increase feed con-
sumption, so that feed conversion worsened, although
not significantly. Overall, the fast-growing broilers exhib-
ited reduced (P<0.05) total feed intake and improved (P
<0.05) feed conversion compared with the slow-grow-
ing genotype.
The ability of fast-growing birds to maintain weight
gain by increasing feed consumption by 15.5% was strik-
ing but perhaps not surprising. In experiment 2, the low-
nutrient diet contained less energy and digestible Lys,
Met, Cys, and Thr, but nutrient:energy ratios were fairly
similar for the conventional and low-nutrient diets
(within period). Therefore, as intake increased in response
to lower energy levels, total nutrient intake did not differ
substantially (data not shown), resulting in similar weight
gain for the fast-growing genotype fed the 2 dietary regi-
mens. In contrast, Lewis et al. (1997) found that a low-
nutrient diet resulted in slower growth for both fast-grow-
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ALTERNATIVE PRODUCTION SYSTEM AND GENOTYPE PERFORMANCE 1017
ing and slow-growing genotypes. However, in that study,
there was more protein relative to energy in the conven-
tional diet than in the low-nutrient diet, and the feed
intake did not increase. Therefore, it is possible that feed
intake did not increase because the energy needs were
being met.
It is clear from experiment 2 that the genotypes re-
sponded differently to diet, thus in part explaining why
final BW of slow- and fast-growing birds in experiment
1 were different. The degree of effect of the low-nutrient
diet on weight gain of the slow-growing birds was some-
what surprising in light of their body composition. As
evident in both experiments and in previous research
(Fanatico et al., 2005), the slow-growing birds are much
less heavily muscled (Tables 7 and 8) than the fast-grow-
ing birds; however, the slow-growing birds appear to
have a greater proportion of feathers relative to their BW,
which could conceivably affect sulfur amino acid re-
quirements.
Fanatico et al. (2005) examined the effect of outdoor
access and showed that similar BW and weight gains
were attained at 11.5 and 7.5 wk of age, respectively,
in slow- and fast-growing birds that had access to the
outdoors. However, a conventional dietary regimen was
fed (Fanatico et al. 2005), which in the current work (ex-
periment 2) was shown to result in similar weight gains
for both genotypes (Table 4). Fanatico et al. (2005) also
reported no effect of outdoor access on feed intake or
feed conversion within genotype. In experiment 1, out-
door access increased feed consumption and worsened
feed conversion. However, the previous research was
conducted during a different time of the year (March to
June), whereas birds of experiment 1 were exposed to
substantially lower temperatures, particularly during the
latter portion of the trial.
Livability
The slow-growing birds had much lower mortality than
the fast-growing genotype (Table 3 and 4). In both experi-
ments, birds became infected with Escherichia coli at ap-
proximately 4 wk of age and were treated with
oxytetracycline administered in water. Although the
USDA prohibits the use of antibiotics in organic produc-
tion, this study was not intended to be conducted under
organic conditions. Slow-growing birds were not affected,
although they presumably received the same exposure
and were given the same antibiotic treatment. Conse-
quently, in both trials, the fast-growing birds had a much
higher mortality. Although the slow-growing birds had
no mortality in experiment 1, the fast-growing birds aver-
aged 10% mortality in experiment 1 and 14% mortality
in experiment 2 (Tables 3 and 4). Although the mortality
was variable within treatment and likely due in part to
the Escherichia coli infection, these data agree with Lewis
et al. (1997), who found no mortality in slow-growing
birds and 11% in fast-growing birds. Slow-growing Label
Rouge birds have been reported to have 3% mortality
compared with 6% mortality of conventional flocks, even
though the slow-growing birds are in production twice
as long (J. M. Faure, Institut National de la Recherche
Agronomique, Nouzilly, France, personal communica-
tion). In addition to the effect on the number of birds
available for processing, livability is a welfare issue of
concern to some consumers and could affect purchasing
decisions and therefore perceived product value.
In experiment 1, there was no effect of genotype on
BMD after adjusting for BW (P>0.05; Table 3). There
was also no effect (P>0.05) of production system on
BMD, even with the slow-growing broilers that foraged
extensively when outdoors. In experiment 2, the conven-
tional diet resulted in a higher BMD (P<0.05) in both
genotypes (Table 4). Calcium and phosphorus levels in
the conventional and low-nutrient diets were similar in
the grower II and finisher diet phases, with Ca being
higher in the conventional diet during the starter and
grower I phases.
The prevalence of bone and joint disorders in broiler
chickens continues to be a concern (Mench, 2004). Both
infectious and noninfectious skeletal conditions are seen
in commercial broilers, but the incidence varies widely
from one flock to another. Among the most common
disorders are bacterial chondronecrosis, angular deformi-
ties (e.g., valgus-varus), and TD. All of these disorders
can impair mobility. Although their causes are complex
and multifactorial, fast growth is certainly a contributing
factor (Mench, 2004). Slower-growing birds have a lower
incidence of bacterial chondronecrosis (McNamee and
Smythe, 2000), and slowing growth in the first 15 to 20
d of life can reduce incidence of angular bone deformity
and dyschondroplasia (Classen and Riddell, 1989). Slow-
growing genotypes are reported to have less varus-valgus
deformity than fast-growing genotypes (Leterrier et al.,
1998).
In the present study, gait scores and incidence rates for
TD showed clear advantages for the slow-growing birds
in both experiments (Tables 5 and 6). In experiment 1,
the slow-growing birds all had gait scores of 0, whereas
the fast-growing birds had higher scores (P<0.05); birds
with gait scores of 4 and 5 were culled for lameness during
the course of the trial. In the fast-growing genotype, birds
in the production system with outdoor access had better
gait scores than the indoor birds (P<0.05). In experiment
2, again the slow-growing birds had much better gait
scores (P<0.05). For both genotypes, the conventional
diet resulted in worse gait scores (P<0.05). The gait score
results could have been affected by genotype differences
in both growth rate and in conformation, because the
larger breast size of fast-growing strains causes their cen-
ter of gravity to shift forward, resulting in a more ineffi-
cient and tiring gait pattern (Corr et al., 2003). The outdoor
access most likely resulted in better gait score due to the
opportunity for exercise; Falcone et al. (2004) found that
the walking ability of broilers can be improved in more
complex environments that promote activity.
Genotype had more effect than production system or
diet on TD incidence (Tables 5 and 6). In experiment 1,
the slow-growing birds all had normal TD scores,
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FANATICO ET AL.1018
Table 5. Distribution of gait scores and tibia dyschondroplasia (TD) scores according to genotype and production
system (experiment 1)
Gait score
1
TD score
Genotype Production system 0 1 2 3 4 5 0 1 2
(%)
Slow-growing Outdoor access 1000000010000
Slow-growing Indoor 1000000010000
Fast-growing
2
Outdoor access 8.3 30.6 52.8 8.3 0 0 85.9 4.7 9.4
Fast-growing
2
Indoor 2.9 8.6 77.1 10 1.4 0 83.9 9.7 6.5
1
Birds with gait scores of 4 or 5 were culled during the course of growout.
2
The gait score proportions (P<0.05) and TD proportions (P>0.05) of fast-growing with outdoor access and
fast-growing indoor treatments were compared for equality of distributions.
whereas the fast-growing birds had a higher incidence
of scores that indicate abnormal cartilage formation (P<
0.05). In the fast-growing birds, production system had
no effect (P>0.05). In experiment 2, again the slow-
growing birds had much better TD scores (P<0.05),
whereas the diet had no effect (P>0.05). Foot pad derma-
titis and hock burn scores were normal for all birds (data
not shown).
Carcass Yield
Carcass weights reflect differences in weight gain, with
the production system with outdoor access having no
effect (P>0.05) on carcass weight and with the fast-
growing birds having higher carcass weights (P<0.05)
than the slow-growing birds (Table 7). Similarly, RTC
yield was higher (P<0.05) for the fast-growing birds.
Interestingly, the overall effect of production system on
RTC yield was significant (P<0.05) because of the effect
on the slow-growing birds, which had a lower RTC yield
when provided outdoor access as compared with the con-
ventional indoor production system. There was no effect
(P>0.05) of outdoor access on breast weight and breast
yield (pectoralis major and pectoralis minor), but both
were affected by genotype, with the fast-growing birds
exhibiting far superior values (P<0.05) in both categories.
Wing yield was reduced and leg yield increased (P<
0.05) by outdoor access; for both parameters, the effect
of outdoor access was greater in the slow-growing birds.
There was a significant genotype effect on wing, leg, and
frame yield; slow-growing broilers had a higher percent-
Table 6. Distribution of gait scores and tibia dyschondroplasia (TD) scores according to genotype and dietary
regimen (experiment 2)
Gait score
1
TD score
Genotype Diet 0 1 2 3 4 5 0 1 2
(%)
Slow-growing Low 98.7 0 1.3 0 0 0 95.7 2.9 1.4
Slow-growing Conventional 89.7 2.6 7.7 0 0 0 97.3 2.7 0
Fast-growing
2
Low 0 1.4 74.7 23.9 0 0 74.2 14.5 11.3
Fast-growing
2
Conventional 0 1.5 54.6 34.9 6.1 3 58.3 15 26.7
1
Birds with gait scores of 4 or 5 were culled during the course of growout.
2
The gait score proportions (P<0.05) and TD proportions (P>0.05) of fast-growing on a low diet and fast-
growing on a conventional diet were compared for equality of distributions.
age (P<0.05) yield in each category, which is reflective
of the large percentage difference in breast yield.
Lewis et al. (1997) found that a low stocking density
increased breast yield compared with a high stocking
density; Fanatico et al. (2005) observed a nonsignificant
increase in breast yield for fast- and slow-growing broilers
provided outdoor access. However, in experiment 1, we
failed to note a similar trend in birds provided outdoor
access, which had a much greater area in which to grow.
Rather, production system had a greater effect on leg yield
of the slow-growing genotype, perhaps due to increased
activity of these birds when provided outdoor access.
The low-nutrient diet reduced the carcass weight of the
slow-growing birds as compared with carcass weights
among birds of other treatment groups (P<0.05; Table
8). The low-nutrient diet reduced RTC yield in fast-grow-
ing, but not slow-growing, birds (genotype ×diet interac-
tion, P<0.05). Similar to experiment 1, in experiment 2,
breast weight and breast yield were affected substantially
by genotype, with the fast-growing birds exhibiting far
superior values (P<0.05) in both categories (Table 8).
Breast weight and breast yield were reduced (P<0.05)
in birds fed the low-nutrient diet, and the effect on breast
yield was more pronounced in the fast-growing broilers.
As in experiment 1, wing and frame yields in experiment
2 were higher (P<0.05) for the slow-growing birds, but
in contrast to the first experiment, there was no effect (P
>0.05) of genotype on leg yield. Dietary regimen (low-
nutrient vs. conventional) had no effect (P>0.05) on wing,
leg, or frame yield (Table 8).
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ALTERNATIVE PRODUCTION SYSTEM AND GENOTYPE PERFORMANCE 1019
Table 7. Effect of genotype and production system on meat yield (experiment 1)
1
Carcass RTC Breast Breast Wing Leg Frame
weight yield
3
weight
4
yield
5
yield
5
yield
5
yield
5,6
Genotype
2
Production system (kg) (%) (g) (%) (%) (%) (%)
Slow-growing Outdoor access 1.65
b
71.5
c
312
b
18.9
b
11.5
b
32.9
a
36.0
a
Slow-growing Indoor 1.57
b
73.4
b
296
b
18.8
b
12.3
a
31.4
b
36.1
a
Fast-growing Outdoor access 2.62
a
76.4
a
792
a
30.1
a
10.6
c
29.7
c
29.2
b
Fast-growing Indoor 2.63
a
76.3
a
800
a
30.5
a
10.8
bc
29.1
c
29.4
b
Pooled SEM 0.01 0.04 26 0.4 0.1 0.3 0.3
P-values
ANOVA
Genotype 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001
Production system 0.5789 0.0424 0.8776 0.7693 0.0005 0.0023 0.7279
Genotype ×production system 0.4236 0.0307 0.6654 0.6068 0.0139 0.0948 0.9454
a–c
Means within a column lacking a common superscript differ (P<0.05).
1
Values are means of 4 pens of 20 female birds.
2
Slow- and fast-growing birds were grown for 91 or 63 d, respectively; placement dates were staggered such
that there was a single trial termination date.
3
Ready-to-cook (RTC) yield represents the chilled carcass weight as a percentage of live BW.
4
Pectoralis major and pectoralis minor (boneless, skinless).
5
Calculated as a percentage of chilled RTC weight.
6
Frame is the carcass including skin but with breast, wings, and legs removed.
Although weight gain of the fast-growing broilers was
maintained on the low-nutrient diet (Table 4), breast yield
was reduced (Table 8). Therefore, although nutrient in-
take was sufficient to maintain overall BW, it appeared
that the nutrient level was insufficient to support maxi-
mum breast yield. Some researchers have suggested that
amino acid needs for maximum breast yield exceed those
needed for maximum growth performance (Sibbald and
Wolynetz, 1986; Moran and Bilgili, 1990; Bilgili et al., 1992;
Schutte and Pack, 1995; Dozier et al., 2000), whereas other
researchers have not reported similar results (Kidd et al.,
1999, 2003, 2004; Garcia et al., 2006). Our data on breast
yield are in agreement with that of Gordon and Charles
(2002), who reported that the reduction in breast meat
yield of broilers fed a low-nutrient diet was not as large
in slow-growing broilers as in fast-growing broilers.
Table 8. Effect of genotype and diet type on meat yield (experiment 2)
1
Carcass RTC Breast Breast Wing Leg Frame
weight yield
3
weight
4
yield
5
yield
5
yield
5
yield
5,6
Genotype
2
Diet (kg) (%) (g) (%) (%) (%) (%)
Slow-growing Low-nutrient 1.95
b
74.1 352
d
18.1
c
12.4
a
33.6 34.7
a
Slow-growing Conventional 2.14
a
73.3 408
c
18.9
c
12.2
a
33.3 34.7
a
Fast-growing Low-nutrient 2.17
a
72.7 544
b
25.1
b
11.6
b
33.9 29.2
b
Fast-growing Conventional 2.13
a
74.1 590
a
27.3
a
11.9
b
33.1 28.7
b
Pooled SEM 0.04 0.47 13 0.37 0.21 0.34 0.31
P-values
ANOVA
Genotype 0.0200 0.5502 0.0001 0.0001 0.0185 0.9073 0.0001
Diet 0.0743 0.5659 0.0024 0.0014 0.7569 0.1474 0.4552
Genotype ×diet 0.0135 0.0379 0.6988 0.0739 0.1946 0.5348 0.4558
a–d
Means within a column lacking a common superscript differ (P<0.05).
1
Values are means of 4 pens of 20 male birds.
2
Slow- and fast-growing birds were grown for 84 or 53 d, respectively; placement dates were staggered such
that there was a single trial termination date.
3
Ready-to-cook (RTC) yield represents the chilled carcass weight as a percentage of live BW.
4
Pectoralis major and pectoralis minor (boneless, skinless).
5
Calculated as a percentage of chilled RTC weight.
6
Frame is the carcass including skin but with breast, wings, and legs removed.
In agreement with the findings of Fanatico et al. (2005),
in which similar genotypes were used, results of both
trials highlight basic growth and carcass differences be-
tween the fast- and slow-growing broilers. Indicative of
their classification, slow-growing broilers had a much
slower and less efficient pattern of growth and were much
less heavily muscled. In particular, there was a striking
difference in breast meat quantity and yield, which re-
flects the years of genetic improvements in breast meat
quantity that have led to the present-day fast-growing
broiler. Although there are differences in trial design, our
results are similar in many ways to those of Havenstein
et al. (1994, 2003), who conducted a series of studies to
assess the effect of genetics and diet on growth perfor-
mance of slower-growing 1957 broilers and faster-grow-
ing 1991 or 2001 broilers. They cited large differences in
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FANATICO ET AL.1020
growth rate, and most of the difference was attributed to
genetics, with 10 to 15% of the difference brought about
through improved diets.
Alternative poultry producers are aware that outdoor
access can affect growth performance and efficiency.
However, an increasing number of consumers are inter-
ested in purchasing poultry products that were produced
in alternative systems that typically provide outdoor ac-
cess; recently, nearly 10% of Americans surveyed re-
ported that they regularly consume organic products
(Hisey, 2004). Consumers must be willing to pay a pre-
mium for alterative poultry products to overcome ineffi-
ciencies in the production system.
In some countries, alternative production systems such
as free-range and organic must adhere to standards that
define stocking density, outdoor access, genotype, and
diet. In the Label Rouge program in France, the use of
slow-growing genotypes and low-nutrient diets is re-
quired (Ministe
`re de L’Agriculture, 1996). Currently, al-
ternative production systems in the United States are not
standardized, and producers have more freedom in defin-
ing their production system. However, the choice of geno-
type in an alternative production system is not a simple
question. It is influenced not only by bird growth and
feed efficiency but also by livability, welfare, behavior,
and consumer preferences. Despite poorer performance
and efficiency, slow-growing birds had better livability
with lower mortality and fewer leg disorders. Further,
from a behavioral standpoint, slow-growing birds may
be more adapted to an alternative production because
they forage more actively, but availability of specialty
slow-growing genetics is currently limited in the
United States.
The issue then is the amount of premium consumers
are willing to pay and the type of product they expect to
receive. Producers that elect to purchase and raise slow-
growing broilers with low-nutrient diets will raise fewer
flocks per year, and resulting broiler carcasses will not
have the meaty appearance of fast-growing commercial
broilers. However, for some consumers, this may be ac-
ceptable and even desirable. For these consumers, the
production system, the genotype, and the diet may all be
part of a total package that is desired. It would seem,
however, for alternative production systems in which
further processing will be conducted, a more heavily mus-
cled genotype could be beneficial. An intermediate-type
bird may be of interest; in France, a medium-growing
genotype that is harvested at 56 d has gained market
share (Beaumont et al., 2004).
In conclusion, the production system with outdoor ac-
cess resulted in increased feed intake and poorer feed
conversion compared with a conventional system. The
fast-growing birds had superior growth performance and
breast yield, whereas the slow-growing birds had less
mortality and improved bone health, which is important
in an alternative system. The use of a low-nutrient diet
improved gait score in fast- and slow-growing birds, al-
though it reduced BW in slow-growing birds and breast
yield in fast-growing broilers. Alternative poultry pro-
ducers need to understand the expectations and willing-
ness of target consumers to pay a premium price to assess
whether it is possible to offset the higher cost of produc-
tion associated with slow-growing genotypes.
ACKNOWLEDGMENTS
We would like to thank the USDA Southern Region
Sustainable Agriculture Research and Education program
and the US Poultry and Egg Association (Tucker, GA)
for providing funding for this research. Funding for this
project was also provided by the National Research Initia-
tive of the USDA Cooperative State Research, Education
and Extension Service, grant number 2001-35204-10800,
to J. A. Mench. We also thank N. C. Rath with the USDA
Agricultural Research Service (Fayetteville, AR) for TD
analysis and P. Talaty (Purdue University, West Lafa-
yette, IN) for technical assistance in use of dual-energy
x-ray absorptiometry.
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