Comparison of performance and carcass composition of a novel

slow-growing crossbred broiler with fast-growing broiler for

chicken meat in Australia

M. Singh,*,1 A. J. Lim,y W. I. Muir,y and P. J. Groves*,z

*Sydney School of Veterinary Science, The University of Sydney, Camden, NSW 2570, Australia; ySchool of Life and
Environmental Science, The University of Sydney, Camden, NSW 2570, Australia; and zBirling Avian Laboratories,
Bringelly, NSW 2556, Australia

ABSTRACT Slow-growing broilers offer differentia- suspension of sheep red blood cells was injected subcu-
tion in the chicken meat market for consumers who have taneously into 8 broilers of each breed to compare their
distinct preferences based on perceived higher welfare antibody response. Birds from both breeds were grown to
indices and willingness to pay a higher price for the a final live weight of 2.0–2.2 kg, before a latency-to-lie
product. Although breeding for slow-growing broilers is (LTL) test, carcass analysis and apparent metaboliz-
relatively advanced in Europe and the United States, it is able energy (AME) assay were performed. The SGB
limited in Australia. Crossbreeding is one of the ap- reached the target weight at 55 d of age compared with
proaches taken to developing slow-growing broiler 32 d in CB. However, SGB stood for longer during LTL,
strains. Thus, the aim of this study was to compare had higher thigh, drumstick, and wing yields (as a per-
performance, immune response, leg health, carcass centage of carcass weight) as well as darker and redder
characteristics, and meat quality of a novel crossbred meat in comparison with the CB. The CB had better feed
slow-growing broiler breed (SGB) with the conventional, conversion efficiency, higher antibody (IgM) production,
fast-growing Cobb 500 broiler (CB) to assess their suit- higher AME, heavier breast yield, and lower meat drip
ability as an alternative for chicken meat production in loss than the SGB. Although fast-growing CB out-
Australia. A total of 236 one-day-old broiler chicks (116 performed the SGB for traditional performance param-
SGB and 120 fast-growing CB) were reared on standard eters, the crossbred in this study was comparable with
commercial diet in an intensive production system. Birds other slow-growing broiler breeds and strains across
and feed were weighed on a weekly basis and feed intake different countries and is thus a suitable candidate for a
and feed conversion ratio calculated. At 21 d of age, a 2% slow-growing alternative in Australia.
Key words: performance, carcass composition, crossbred, slow-growing broiler, chicken meat
2021 Poultry Science 100:100966
https://doi.org/10.1016/j.psj.2020.12.063

INTRODUCTION indicate better welfare such as improved leg health,

adaptability to different rearing conditions, and lower
Selective breeding, efficient production systems, mortality rates (Fanatico et al., 2008; Sirri et al., 2011;
improved diets, and veterinary care have all resulted in Comert et al., 2016; Wilhelmsson et al., 2019). Producers
the exponential growth rates of meat chickens contrib- of slower-growing meat chickens can capitalize on these
uting to their high levels of production (Fanatico et al., attributes by marketing their chickens as a perceived
2007). Although many consumers are driven by lower pri- higher welfare product.
ces of fast-growing meat chickens, some seek additional Slower-growing breeds make up nearly 40% of Dutch
attributes that add apparent value when making choices broiler production, 24% of French broiler production,
about their purchases. The expansion of slow-growing and 11% of production in the United Kingdom
broiler breeds can be attributed to characteristics that (Davies, 2019). One of the most successful specialty
poultry production systems in Europe is the “French La-
bel Rouge” program which uses broilers with a growing
Ó 2020 The Authors. Published by Elsevier Inc. on behalf of Poultry period of at least 81 d. In Poland, certified chickens are
Science Association Inc. This is an open access article under the CC BY- available for pasture-based poultry production, and a
NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Received November 12, 2020.
good example of a free-range rearing program is “kurczak
Accepted December 21, 2020. zagrodowy z Podlasia” (“organically raised chickens of
1
Corresponding author: mini.singh@sydney.edu.au Podlasie”) (Mikulski et al., 2011). Global Animal

1
2 SINGH ET AL.

Partnership (GAP), creator of North America’s most and Australia’s often extreme climate. They also need
comprehensive farm animal welfare standards, has to develop at a rate that allows for all body parts to
announced their intention to replace 100 percent of grow proportionately to perform natural behaviors and
fast-growing chicken breeds with slower-growing breeds movement and be grown as per RSPCA approved
for all levels of its 5-Step Rating Program by the farming scheme standards (RSPCA, 2020). Thus, it is
year 2024. increasingly important for SGB breeds to be locally
As there has been a 10-fold increase in chicken meat developed and their performance and suitability deter-
consumption per capita from 5.9 kg (in 1965) to mined for the Australian market.
47.4 kg (in 2019) and, it has been forecast, to reach The objective of this study was to compare the perfor-
approximately 52 kg per capita by 2022/2023 mance, serological response, leg health, carcass charac-
(Mullumby, 2018), the Australian chicken meat industry teristics, and meat quality of a locally developed novel
needs to continue to increase its production. Contrary to crossbred slow-growing broiler (SGB) with a fast-
most developed countries that have shown some diversi- growing commercial Cobb 500 broiler (CB), both grown
fication in the chicken meat market with slow-growing in identical housing conditions and fed the same diet.
broilers, the predominant chicken meat available in The results of this study provide a better understanding
Australia is from the fast-growing strains including those of the productivity, feed conversion ratio, and meat
grown in free-range production systems. Research sug- quality of a candidate slow-growing broiler breed in an
gests slow-growing broilers may be better suited to Australian context.
free-range and pasture poultry systems than their fast-
growing counterparts (Rack et al., 2009). Some studies MATERIALS AND METHODS
found slow-growing broilers to have better meat quality,
and lower nutrient requirements and cost of rearing Birds, Housing, and Experimental
(Attia et al., 2007, 2009, 2011, 2017). To date, Australia Conditions
has not conducted research into developing any specific
slow-growing broiler breed. Adjusting the amount or All procedures within this study were approved by the
nutritional quality of the feed delivered to the fast- University of Sydney Animal Ethics Committee (2018/
growing broiler strains is not an alternative solution to 1389) and the Birling Animal Ethics Committee
slow their growth rates as it inflicts stress on the birds (BAEC Ref No: 1069).
(Mench, 2002). Thus, there is need to develop a slow- One hundred sixteen one-day-old novel crossbred
growing broiler breed that would provide an option for SGB chicks and 120 fast-growing Cobb 500 chicks
producing a welfare-oriented and differentiated chicken (CB), were vaccinated for Marek’s disease via subcu-
meat market. Furthermore, increased awareness among taneous injection and coarse-sprayed against infectious
Australian consumers about the welfare of production bronchitis and Newcastle disease. The day-old chicks
animals, as reflected by the increased demand for free- were randomly allocated into 8 mixed-sex pens consist-
range poultry products (Scott et al., 2017), presents an ing of either 30 CB or 29 SGB. Each pen was provided
opportunity for the slow-growing broiler breeds to be with 3.5 m2 floor space, 2 tube feeders, a line of nipple
introduced into the market. The consumers who are drinkers, a double-level perch and wood shavings as
interested in other premium labels such as organic, litter. Water was available via fonts in the first 4 d
free-range, pasture poultry, etc., are more likely than and then nipple drinkers for the rest of the trial. A ther-
the average customer to pay the premium price for mostatically controlled gas-fired space heater was used
slow-growing broilers (Fisher, 2017). during brooding, with the shed temperature at 32 C
Slow-growing broilers can either be imported as exist- on day 1 and decreasing by 1 C every second day until
ing genetics from overseas or developed locally through 21 C was reached at 21 d. Artificial lighting for both
domestic breeding programs. Coles Supermarkets groups were provided at 20 Lux with a duration of
Australia Pty Ltd., recently launched “Slow Hills 23 h light for the first 2 d, which was then reduced to
Chicken”, a new special breed of chicken from the poultry 16 h from day 4, 12 h from day 9, 11 h from day 16,
genetics company Hubbard based in France. However, and finally 11.5 h of light from day 22 until day 55.
importation of poultry genetic stock into Australia is Environmental enrichment in the form of perches
not only costly but also requires strict quarantine mea- ((30 cm (l) ! 45 cm (w) ! 15 cm (h)) was provided
sures. Moreover, customers in Australia may have in all pens for the birds from 7 d old.
different requirements regarding performance and char- The same standard broiler diet (Table1) was allocated
acteristics of the chickens, for example, some may prefer to both CB and SGB based on the number and weight of
breast meat while others may prefer the bone portions. birds in a pen. The ration consisted of a starter diet
Furthermore, there are large differences in the environ- (crumble, 500 gm/bird to CB and SGB over first
ments (housing facilities, ambient temperature, altitude, 2 wk), a grower diet (pelleted, 1.2 kg/bird over 1 wk to
available nutritional sources, quality of the water, etc.) CB and over 3 wk to SGB) and a finisher diet (pelleted,
and it might be that chickens of one strain or crossbred 2 kg/bird over 2 wk to the CB and 2.4 kg/bird over 4 wk
producing well in one environment will perform poorly to SGB). All diets contained Maxiban (Elanco Animal
in another (EFSA, 2010). Slow-growing broilers in Health, Australia) at 500 g/tonne for coccidiosis control.
Australia need to be suitable for free-range conditions Birds were grown to a final live weight of 2.0–2.2 kg for
 A NOVEL SLOW-GROWING BROILER FOR AUSTRALIA 3
Table 1. Ingredient and calculated composition of starter, grower, positive result to be recorded. Subsequently, 0.2 M of
and finisher diets fed to both Cobb (CB) and slow-growing broiler 2-mercaptoethanol (2-ME; source: Sigma-Aldrich)
(SGB).
were administered to the serum samples to inactivate
Starter Grower Finisher IgM and determine the IgG antibodies. The IgM titer
Ingredient %
was determined by subtracting the IgG titers from
the total antibody as per protocols described by
Wheat 57.9 61.0 65.4 Haghighi et al. (2005).
Soya meal 31.0 26.4 20.3
Canola meal 5.0 6.0 7.5
Canola oil 1.82 3.32 4.00
L-Lysine HCL 0.274 0.230 0.234
Latency-to-Lie Test
DL-Methionine 0.276 0.219 0.163
L-Threonine 0.119 0.0964 0.0826 Severe leg weakness is a significant issue in commer-
L-Valine 98% 0.0479 0.0183 0.01 cial broiler production and the latency-to-lie (LTL)
Salt 0.136 0.147 0.133 technique, which is based on the chicken’s natural aver-
Sodium bicarbonate 0.161 0.153 0.182
Limestone flour 1.26 1.02 0.86 sion to water (Berg and Sanotra, 2003), is an objective
Dicalcium phosphate 1.60 1.03 0.83 measure used to assess broiler leg strength (Weeks
Xylanase 0.005 0.005 0.005 et al., 2002). Latency-to-lie test was conducted at the
Phytase 0.01 0.01 0.01
Choline chloride 0.08 0.07 0.06 final mean weight of 2.0–2.2 kg, where a total of 60
Vitamin-mineral premix1 0.2 0.2 0.2 male birds (30 each of CB and SGB) were randomly
MaxibanTM (500 g/t)2 0.05 0.05 0.05 selected and individually placed into a tub with 3 cm
BACECO 150TM (267 g/t)3 0.027 0.027 0.027
Calculated composition of tepid water (30 C–33 C) and timed until the bird
DM% 90.4 90.5 90.6 sat down or to a maximum of 5 min. The results (in sec-
ME, kcal/kg 2,892 3,040 3,126 onds) collected from the LTL were compared across the
Digestible CP, % 20.2 18.7 16.9
Digestible Lys, % 1.28 1.15 1.03 2 breeds using Kaplan-Meier survival analysis, with
Digestible Met, % 0.58 0.51 0.44 data for birds that remained standing at 300 s being
Digestible Met 1 Cys, % 0.93 0.85 0.76 censored. Comparisons between the 2 broiler breeds in
Digestible Thr, % 0.84 0.77 0.69
DEB4, Meq/Kg 254 233 207 LTL were performed using the Gehan’s Wilcoxon test
Digestible Ca, % 0.65 0.54 0.48 (Groves and Muir, 2017). Only the male birds were
Available P 0.52 0.43 0.40 compared in the LTL test as the distinction between
1
The vitamin-mineral premix supplied per tonne of feed: [MIU] retinol their LTL time was considered to be more apparent
12, cholecalciferol 5, [g] tocopherol 50, menadione 3, thiamine 3, riboflavin (Groves and Muir, 2017).
9, pyridoxine 5, cobalamin 0.025, niacin 50, pantothenate 18, folate 2,
biotin 0.2, copper 20, iron 40, manganese 110, cobalt 0.25, iodine 1,
molybdenum 2, zinc 90, selenium 0.3.
2
Carcass Analysis
Maxiban (Elanco Australasia Pty Ltd., Australia), provided 40 g of
active ingredients narasin and nicarbazin per tonne of complete feed.
3
BACECO 150 (IAH Sales Pty Ltd., Australia), provided 40 g
A total of 80 broilers (forty (20 female and 20
bacitracin activity per tonne of complete feed. male) each of CB and SGB) were randomly selected
4
Dietary electrolyte balance. at their final weights of 2.0–2.2 kg, for carcass anal-
ysis. After 11 h of fasting the final body weight was
determined and the broilers were slaughtered using
both breeds. Mortality was recorded daily, and postmor- cervical dislocation followed by exsanguination.
tem analysis was conducted to determine the cause of Plucked weight (PW) (weight of whole bird after
death. removal of feathers) was determined. Length of the
duodenum, jejunum, ileum, and caeca, as well as
Weight, Feed Intake, and Performance empty weight of the crop, proventriculus, gizzard,
pancreas, liver, heart, duodenum, jejunum, ileum,
The birds and feed were weighed on a weekly basis. and caeca, were determined as a relative percentage
Feed intake, body weight gain, and feed conversion ratio to plucked weight (%PW). The carcasses were
(FCR) were calculated weekly for the duration of the dissected into breast meat (without skin and adherent
study. fat), thighs, drumsticks, whole wings. Carcass weight
(CW) was determined by adding the weights of the
Antibody Response Test breast, thighs, drumsticks, wings, and rest of carcass
(back 1 rib cage). Length and width of the breast,
At 21 d of age, 2 mL of blood was drawn from a total length of the thigh, drumstick and wing, weight of
of 16 birds (8 each of CB and SGB), randomly selected, the abdominal fat pad, breast, 2 thighs, 2 drumsticks
wing tagged, and injected subcutaneously in the neck and 2 wings were calculated as relative percentage to
with 0.25 mL of a 2% suspension of sheep red blood carcass weight (%CW). The color of the skin on top
cells (SRBC) to evaluate their antibody response of the right pectoralis major was determined at 3 pla-
(Kreukniet et al., 1992; Parmentier et al., 1993; ces with a Konica Minolta Chromameter 400 (Konica
Haghighi et al., 2005). Hemagglutination was used to Minolta Sensing Singapore Pte Ltd.) applying the
evaluate the total antibody response after 7 d. A min- CIE (1978) system color profile of lightness (L*),
imum of 50% SRBC agglutination was required for a redness (a*), and yellowness (b*). Ultimate pH24 of
4 SINGH ET AL.

the right pectoralis major was measured using a pro- RESULTS AND DISCUSSION
fessional portable meat pH meter (Instrument Choice,
Australia) 24 h after slaughter. Samples from left pec- Performance (Body Weight, Feed
toralis major muscle were subjected to drip loss mea- Consumption, Feed Conversion Ratio)
surement by weighing and then storing them on a
suspended net in a plastic container at 4 C on day Day-old body weight of CB (47.3 g) was higher
1, 3, 6, and 10 after slaughter. Drip loss was (P , 0.001) than that of SGB (39.8 g) (Figure 1). Final
expressed as a percentage of the initial muscle weight market weight of 2.0–2.5 kg was achieved on day 32 for
(Fanatico et al., 2005a). CB (2.16 kg) and on day 55 for SGB (2.02 kg) (Figure 1).
Body weight gain on a weekly basis was found to be
significantly higher (P , 0.001) in CB than in SGB, until
Apparent Metabolizable Energy Assay day 32, as would be expected from several previous
studies (Fanatico et al., 2005b, 2008; Mikulski et al.,
At the respective final weights of 2.0–2.2 kg for each 2011; Sarica et al., 2014a; Cano
gulları Do
gan et al.,
breed, a total of 48 birds (24 each of CB and SGB) were 2019), where weight gain of fast-growing broilers
housed in 8 bioassay cages. The total collection of exceeded that of the slow-growing genotype. The lower
excreta and feed intake on a per cage basis over 48 h body weight of SGB in this study on day 32 could be
was measured. Excreta were pooled within a cage, attributed to the genetic effect of the layer strain as
mixed well using a blender, and representative samples one of its parents. However, the number of days needed
per pen were taken. The samples were oven dried and for SGB to achieve market weight of 2–2.5 kg at 55 d was
ground to pass through a 0$5 mm sieve. The gross en- found to be either comparable or better to the commer-
ergy of diets and excreta were determined by bomb cially available slow-growing broiler breeds such as
calorimetry using an adiabatic calorimeter (Parr 1281 Rowan Ranger (Aviagen, 2018) and CobbSasso (Cobb-
bomb calorimeter; Parr Instruments Co. Moline, IL). Vantress, 2007), and many other slow-growing strains
The apparent metabolizable energy (AME) of the diet and breeds investigated in several other studies
was calculated as outlined by Ravindran et al. (2000). (Fanatico et al., 2005b; Sarica et al., 2014b; McCrea
et al., 2014; Cruz et al., 2018; Mueller et al., 2018) that
estimated time to reach market weight at 50 to 105 d.
Statistical Analyses There was a significant difference in the cumulative
weekly feed consumption between genotypes with that
Data were analyzed with a one-way analysis of vari- of the SGB (1.41 kg) being lower than that of CB
ance using Genstat 18th Edition (VSN International (3.04 kg) on day 32 (P , 0.01). While CB consumed
Ltd., UK, 2017) with breed as the main effect and pen nearly 76% more feed than SGB on day 32, the cumula-
as an experimental unit. The least mean squares were tive feed intake to achieve target market weight was
compared using the Tukey–Kramer option and consid- significantly lower for CB (3.04 kg per bird) than for
ered to be significantly different at P , 0.05. SGB (4.03 kg per bird) (P , 0.05) (Figure 2), confirming

Figure 1. Average body weight (kg/bird) on a weekly basis, for Cobb (CB) until day 32 and slow-growing broiler (SGB) until day 55, grown to a
market weight of 2.0–2.2 kg.
 A NOVEL SLOW-GROWING BROILER FOR AUSTRALIA 5

Figure 2. The weekly cumulative feed consumption (kg/bird) of Cobb (CB) until day 33 and slow-growing broiler (SGB) until day 55, grown to a
market weight of 2.0–2.2 kg.

results from previous studies (Fanatico et al., 2005b; requirements due to increased mobility (Gordon and
McCrea et al., 2014; Cano
gulları Dogan et al., 2019). Charles, 2002), thus affecting their feed efficiency
However, in a study by Sarica et al. (2019), total feed (Fanatico et al., 2008). The crossbred SGB in this study
consumption was found to be higher for the fast- performed better with an FCR of 1.98 at day 55 when
growing broiler genotype than for the slow-growing compared with the established commercial slow-
broiler strains, although they were still more efficient. growing CobbSasso, where FCR is expected to be
The cumulative FCR was significantly lower for SGB 2.14 at day 56 (Cobb-Vantress, 2007).
on day 7 (0.681 (CB) vs. 0.207 (SGB); (P , 0.001)) and
day 21 (1.22 (CB) vs. 1.16 (SGB); P , 0.05)). However,
Apparent Metabolizable Energy
SGB had a higher FCR of 1.98 on processing at target
weight, which was 0.54 points higher than the CB at Difference in AME values of 13.62 MJ/kg for CB as
1.44 (Figure 3), and in agreement with earlier findings compared with 13.36 MJ/kg for SGB (P , 0.05) indi-
(Fanatico et al., 2005b, 2008; Mikulski et al., 2011; cated a 1.91% higher AME obtained from the same
McCrea et al., 2014; Sarica et al., 2016). The slow- diet in CB. Apparent metabolizable energy is the energy
growing broilers are believed to have higher maintenance used for growth, reproduction, and metabolic processes.

Figure 3. Weekly cumulative FCR of Cobb (CB) until day 33 and slow-growing broiler (SGB) until day 55, grown to a market weight of 2.0–2.2 kg.
6 SINGH ET AL.

The growth rates of birds are likely to affect the rates of Latency-to-Lie-Test
gastrointestinal development and enzyme production,
consequently, influencing nutrient utilization by the Latency-to-lie test conducted at the target market
birds (Santos et al., 2015). weight of 2.0–2.2 kg resulted in shorter median stand-
The higher body weight gain of CB could be ing time by the CB (200.5 s) than by the SGB (300 s)
attributed to their higher feed intake and thus a (P 5 0.0182) (Figure 4), which could be a consequence
higher AME, resulting in more energy being available of their higher and faster growth rates resulting in the
for growth. Moreover, it is likely that the SGB uti- skeleton and joints still being immature when they are
lized the metabolizable energy to perform increased subjected to the exceptionally heavier weight loads
physical activities thus contributing to their slower (Webster, 2004; Shim et al., 2012; Alves et al., 2016).
and lower weight gain on a weekly basis. The energy Increased sternal load largely increases metabolic and
utilization of SGB (13.36 MJ/kg) was similar to that energetic costs associated with prolonged standing in
of the slow-growing Cobb Sasso (13.31 MJ/kg) re- birds (Tickle et al., 2012, 2013, 2018) and could be
ported in the production manual (Cobb-Vantress, associated to the impact of a larger breast muscle
2007), implying that the results of this study are mass on fast-growing broiler energetics, thus reducing
comparable with slow-growing broiler industry their time to stand. Moreover, the potentially adverse
standards. thermoregulatory effects of rapid growth rate and
body mass increases, contribute to the increased seden-
tary resting and decreased locomotor behavior
Antibody Response Test observed in large broilers as compared with SGB
The antibody response test was designed to expose (Dukic-Stojcic and Bessei, 2011; Tickle and Codd,
the birds to an antigen (SRBC) to which they were 2019). Slow-growing broilers have been reported to
na€v e allowing a robust evaluation of their antibody have higher tibia ash, tibia density, and tibia breaking
(IgM and IgG) response, as assessed by a direct hem- strength than fast-growing broilers which have more
agglutinin reactions (Haghighi et al., 2005). The CB porous bones (Shim et al., 2012) and reduced mineral-
had a significantly higher mean total anti-SRBC anti- ization (Williams, 2000). Tahamtani et al. (2018)
body titer (IgM and IgG) of 13 in comparison with found a high prevalence of impaired walking ability
the SGB titer of 6 (P , 0.05) 7 d after exposure. (measured by gait score) and severe lameness in con-
The CB also had a significantly higher mean IgM ventional fast-growing as compared with organic
titer of 11, compared with 4 for the SGB slow-growing broilers.
(P , 0.05). However, for the 2-mercaptoethanol–
treated serum samples, the IgG titer reported for Carcass Analysis (Carcass Characteristics,
both broiler breeds was 2, indicating undetectable Gastrointestinal Segments, and Offal
levels of anti-SRBC IgG. Weights)
A stronger immune response to SRBC antigen was
observed in the fast-growing CB as compared with Carcass weight of SGB (1.49 kg) was significantly
SGB. This is similar to observations in turkeys lighter than CB (1.62 kg) (P , 0.05) (Table 2). The
(Li et al., 2000), where the subline selected for body and breast were longer and narrower (P , 0.01)
increased 16-wk body weight had higher total anti- and the length of shank, thigh, drumstick, and wing
SRBC, IgM, and IgG titers than the slower-growing was higher (P , 0.001) in SGB as compared with CB.
random bred control line, probably due to the higher Apart from the weight of breast which was 1.53 times
proportion of helper T cells, which promote B cell pro- higher in CB (P , 0.001), the thighs, drumsticks, wings,
liferation and maturation in the faster-growing line in head, and the rest of the carcass, were heavier (P , 0.01)
comparison with the slow-growing. However, it should in SGB (Table 2). Of the gastrointestinal segments and
be noted that the T-cell subpopulation in the birds of offal weights (% PW), crop, proventriculus, jejunum,
the present study was not measured. The variation in ileum, liver, and abdominal fat pad were heavier
the SGB immune response could also be due to the ge- (P , 0.05) in CB, whereas the gizzard, duodenum, and
netic influences of the layer line in the crossbred, as caeca were heavier (P , 0.001) in SGB (Table 3).
Koenen et al. (2002) found higher IgM titers in This study found that genotype was a major factor
response to SRBC in meat chickens indicating a strong impacting carcass weight of broilers with SGB being
short-term humoral response (good IgM response but a nearly 0.13 kg lighter at final market weight with carcass
poor IgG response) in comparison with the layer-line yields being 75.82 and 72.90% for CB and SGB, respec-
chickens. However, contrary to our findings, some tively. Similar effects of genotype on carcass yield have
studies found that chicken lines which were selected been observed in previous studies (Fanatico et al.,
for increased growth had compromised immune func- 2008; Mikulski et al., 2011; Cruz et al., 2018; Mueller
tions (Cheema et al., 2003; van der Most et al., et al., 2018, 2020; Devatkal et al., 2019) that found
2011). Immunization followed by pathogen challenge carcass yield to decrease in slow-growing broiler strains.
would be a more conclusive comparison of immune However, by contrast, Cruz et al. (2018) found carcass
response between SGB and fast-growing chickens, in yields of slow-growing strains could be increased by
future studies. delaying slaughter age to 105 d of age.
 A NOVEL SLOW-GROWING BROILER FOR AUSTRALIA 7
2018; Mueller et al., 2018; Sarica et al., 2019; Jaspal
et al., 2020).
Weight (% PW) of the thighs, drumsticks, and wings
were heavier for SGB in this study. A high leg weight
percentage in the slow-growing genotype has also been
observed by Cano
gulları Do
gan et al. (2019), Sarica
et al. (2014a, 2016), C€omert et al. (2016), Sirri et al.
(2011), and Fanatico et al. (2005b, 2008). The higher
wing yield observed in SGB could be a result of higher
activity levels which promote the bone mass and sup-
porting muscle mass accumulation, compared with CB,
(Gordon and Charles, 2002; Abdullah and Buchtova,
2016). Moreover, it has been found that layer-type males
Figure 4. Kaplan-Meier survival analysis and Gehan’s Wilcoxon test tend to have a higher percentage of leg yield and less
for latency-to-lie (LTL) of male Cobb (CB) and slow-growing broilers value parts of the carcass than broilers (Gerken et al.,
(SGB) timed for 300 s. Total number of birds censored were 14 of 30 2003). This suggests that the higher thigh-drumstick
for CB with a median standing time of 200.5 (SEM: 19.05) s, and 18 of
28 for SGB with a median standing time of 300 (SEM: 20.08) s. yield in SGB in our study could be a result of the layer
strain genotype in the parental cross.
A significantly heavy gizzard (P , 0.0001) in the SGB
The breast weight (% PW) in the present study was
as compared with CB in this study is comparable with
significantly higher in CB (27%) as compared with SGB
observations in studies by Alshamy et al. (2018) and
(17.58%) (P , 0.001), which is possibly a consequence
Mohammadigheisar et al. (2020), where both the body
of intensive selection for this trait in fast-growing
weight and genetic line of bird had a significant influence
broilers and leads to the reduction in the relative yield
on gizzard mass. Reduction in visceral organ weight rela-
of other carcass components (Fanatico et al., 2005b,
tive to body weight has been associated with a higher
2008). Greater breast muscle weight in fast-growing
growth rate in modern broiler breeds (Havenstein
meat chickens has been attributed to the higher
et al., 2003) due to a reduction in maintenance energy
insulin-like growth factor concentrations in the serum
required and therefore increased overall energy utiliza-
and breast muscle as compared with the slow-growing
tion and efficiency (Tallentire et al., 2016).
genotype (Xiao et al., 2017). Higher relative breast
The abdominal fat pad was significantly heavier in
weight in fast-growing broiler strains in comparison
CB than in SGB (P , 0.001). Similarly, Smith et al.
with slow-growing breeds were also observed previously
(2012) reported that a longer growing period resulted
(Fanatico et al., 2008; Mikulski et al., 2011; Cruz et al.,
in a leaner bird. When selecting for lower residual
feed intake, Wen et al. (2018) identified that the weight
and percentage of abdominal fat pad was lower in slow-
Table 2. Carcass characteristics for Cobb (CB) on day 32 and growing birds. This may explain the lower abdominal
slow-growing broiler (SGB) on day 55, grown to a market weight
of 2–2.2 kg.
fat pad weight as a consequence of lower feed intake
of SGB in the present study. By contrast, Quentin
Genotype et al. (2003) and Mikulski et al. (2011) reported that
Carcass characteristics Cobb SGB SEM P-value slow-growing birds provided with dietary energy and
Weight of the bird (BW) 2,143 2,049 42.130 0.117 protein in excess of their nutritional requirements
Plucked weight (PW)1 2,025 1,892 40.247 0.0219 resulted in more abdominal fat.
Carcass weight (CW)2 1,626a 1,495b 32.76 ,0.001
Length of body (cm) 23.53b 30.31a 0.345 ,0.0001
Width of body (cm) 18.84a 17.63b 0.213 0.0001
Length of breast (cm) 17.93b 18.78a 0.196 0.003 Meat Quality (Color, pH, Water-Holding
Width of breast (cm) 15.23a 13.68b 0.145 ,0.0001
Length of shank (cm) 5.79b 7.23a 0.118 ,0.0001 Capacity)
Length of thigh (cm) 9.84b 12.29a 0.152 ,0.0001
Length of drumstick (cm) 9.44b 12.85a 0.190 ,0.0001 The CIE (1978) system color profile of lightness (L*),
Length of wing (cm) 23.10b 29.01a 0.334 ,0.0001 redness (a*), and yellowness (b*) was used to evaluate
Breast weight (% CW3) 27.00a 17.58b 0.205 ,0.0001
Two thighs (% CW) 13.56b 14.53a 0.177 ,0.0001 breast meat color. A lower L* results in redder meat co-
Two drumsticks (% CW) 11.90b 15.16a 0.133 ,0.0001 lor, which is perceived to be an indicator of good meat
Two wings (% CW) 10.38b 12.26a 0.107 ,0.0001 quality and is also often the first trait observed by con-
Rest of carcass (% CW) 37.15b 40.44a 0.256 ,0.0001
Head (% CW) 3.06b 3.76a 0.061 ,0.0001 sumers. Breast meat color of CB was lighter with a
higher L* value (51.93) than that of the SGB (45.39)
a,b
Means within a column lacking a common superscript differ (P , 0.001), whereas SGB showed a higher (P , 0.05)
(P , 0.05).
1
Plucked weight (PW) is the weight of whole bird after removal of redness (a*: 2.64 vs. 2.08) and lower (P , 0.001) yellow-
feathers. ness (b*: 3.84 vs. 4.97) (Table 4). The redder pectoralis
2
Carcass weight (CW) was determined by adding the weights of breast major of SGB found in this study was in agreement
(without skin and adherent fat), thighs, drumsticks, wings, and rest of
carcass (back 1 rib cage). with earlier findings (Berri et al., 2001; Quentin et al.,
3
Percentage of total carcass weight. 2003; Smith et al., 2012; Sarica et al., 2014a) whereby
8 SINGH ET AL.

Table 3. Gastrointestinal sections and offal weights for Cobb (CB) Cano
gulları Do
gan et al., 2019), with the slow-growing
on day 32 and slow-growing broiler (SGB) on day 55, grown to a genotype reporting a lower ultimate pH in comparison
market weight of 2–2.2 kg.
with the fast-growing genotype. Berri et al. (2001)
Organ (%PW) 1 CB SGB SEM P-value concluded that the intense selection for increased growth
Crop 0.34 a
0.29b
0.013 0.0084
rates and breast meat yield of broilers leads to dimin-
Proventriculus 0.45a 0.42b 0.009 0.0196 ished postmortem glycolysis, resulting in less pyruvic
Gizzard 1.57b 2.62a 0.059 ,0.0001 acid being released, leading to a higher ultimate pH.
Duodenum 0.49b 0.58a 0.011 ,0.0001
Jejunum 1.14a 1.07b 0.019 0.0281
However, Henckel (1996) suggested that the muscles of
Ileum 0.93a 0.75b 0.015 ,0.0001 birds subjected to a period of concentrated growth would
Both caeca 0.33b 0.44a 0.010 ,0.0001 likely be in a constant state of hypoxia. Consequently,
Rectum 0.10 0.12 0.027 0.7701
Liver 2.54a 2.06b 0.035 ,0.0001
the demand for energy by the muscle cells leads to anaer-
Pancreas 0.22 0.22 0.005 0.7293 obic glycolysis which converts glycogen into lactate,
Heart 0.61 0.62 0.014 0.9261 lowering the pH. This has been observed in several
Abdominal fat pad 1.58a 1.30b 0.066 0.0047
studies (Sarica et al., 2014a; Hoan and Khoa, 2016;
a,b
Means within a column lacking a common superscript differ Devatkal et al., 2019) which contrasts to observations
(P , 0.05). in this study. Nonetheless, in the present study, given
1
Expressed as a percentage of total plucked weight.
that the 2 broiler breeds were processed at different
ages, the impact of the age on muscle metabolism and
the redness (a*) was higher for the alternative broiler composition must also be considered.
type than for the conventional broilers selected for rapid Fanatico et al. (2007), Hoan and Khoa (2016), and
growth. The varying degree of redness could be a result Devatkal et al. (2019) found breast muscle of slow-
of the difference in slaughter age given that the growing broilers had a lower water-holding capacity
myoglobin content (heme pigment) of the breast meat than the fast-growing breed (P , 0.05), which is in
of broilers increases with age (Berri et al., 2001;
agreement with the present study, where the breast
Gordon and Charles, 2002). The redder breast muscle
weight (% CW) of SGB was lower in comparison with
of SGB can also be explained by the increased blood cir-
the CB, suggesting smaller and thinner breast fillets
culation as a consequence of prolonged wing flapping from SGB. Therefore, SGB are expected to have a larger
associated with slaughter (Berri et al., 2005a,b). By surface area with regards to the muscle mass exposed to
contrast, Fanatico et al. (2005a) and Cano
gulları air, thus, being vulnerable to greater drip loss (Fanatico
Do
gan et al. (2019) found thinner fillets from the slow- et al., 2005a, 2007). However, fillet thickness was not
growing broilers to have higher L* values (lighter) objectively measured in this study and was concluded
than thicker fillets of the commercial fast-growing
based on visual observations only.
genotype.
Berri et al. (2005a) suggested a strong negative corre-
The ultimate pH24 of breast meat was lower
lation between breast muscle pH at 24 h postmortem and
(P , 0.001) in SGB, and the drip loss in pectoralis major drip loss similar to that seen in the current study, where
(calculated as a percentage of initial muscle weight) on SGB were reported to have a higher drip loss correspond-
day 10 after slaughter was higher at 11.21% for SGB in ing to a lower ultimate pH. Because rigor mortis pro-
comparison with 8.58% for CB (P , 0.05) (Table 4). ceeds at a faster rate in the SGB as compared with the
In the event of the conversion of muscle to meat, the fast-growing broilers, the initial rate of pH drop is has-
extent of postmortem pH decline is crucial as it not
tened, thus, leading to poorer water-holding capacity
only affects meat color, but also its water-holding capac-
(Mikulski et al., 2011).
ity and texture (Aberle et al., 2001). The pH findings in
this study were consistent with previous results
(Quentin et al., 2003; Fanatico et al., 2007; CONCLUSION
In this study the SGB were grown for 55 d to reach the
Table 4. Meat quality (color, ultimate pH, and drip loss) of the target weight of 2–2.5 kg, compared with the 32 d for
pectoralis major of Cobb (CB) on day 32 and slow-growing broiler CB. However, SGB showed longer standing times during
(SGB) on day 55, grown to a market weight of 2–2.2 kg.
LTL test, higher thigh, drumstick and wing yields (as a
Meat Quality Attributes Cobb SGB SEM P-value percentage of carcass weight) as well as darker and
Breast color L* (lightness) 51.93a
45.39 b
0.413 ,0.0001 redder meat in comparison with the CB. Although CB
Breast color a* (redness) 2.08b 2.64a 0.166 0.0204 outperformed the SGB for traditional performance pa-
Breast color b* (yellowness) 4.97a 3.84b 0.145 ,0.0001 rameters such as feed conversion ratio, antibody (IgM)
pH241 5.88a 5.74b 0.013 ,0.0001
Drip loss2@ 24 h (%) 2.93b 6.17a 0.400 ,0.001 production, AME, breast yield, and meat with lower
Drip loss @ 3 d (%) 5.78b 9.13a 0.462 ,0.001 drip loss, the crossbred SGB showed comparable out-
Drip loss @ 6 d (%) 8.26b 9.76a 0.473 0.032 comes to other more established slow-growing broiler
Drip loss @ 10 d (%) 8.58b 11.21a 0.468 ,0.001
breeds. The main advantage of the slow-growing geno-
a,b
Means within a column lacking a common superscript differ type is their improved welfare over the fast-growing
(P , 0.05). broilers, as indicated by better leg strength. Moreover,
1
pH at 24 h after processing.
2
Drip loss calculated as a percentage of initial muscle weight at the difference in body conformation between the geno-
processing. types helps to differentiate the slow-growing brand
 A NOVEL SLOW-GROWING BROILER FOR AUSTRALIA 9
from the conventional broiler. However, production Aviagen. 2018. Rowan ranger broiler performance objectives.
costs have been found to be 11–25% per pound higher Accessed Oct. 2020. http://en.aviagen.com/assets/Tech_Center/
Rowan_Range//RowanRanger-Broiler-PO-18-EN.pdf.
for slower-growing breeds than for modern breeds, Berg, C., and G. Sanotra. 2003. Can a modified latency-to-lie test be
depending on the target end point, and consumer will- used to validate gait-scoring results in commercial broiler flocks?
ingness to pay would need to increase by 10.8% to offset Anim. Welf. 12:655–659.
the producer losses. (Lusk et al., 2019). The advantages, Berri, C., M. Debut, V. Sante-Lhoutellier, C. Arnould, B. Boutten,
N. Sellier, E. Baeza, N. Jehl, Y. Jego, and M. Duclos. 2005a.
over and above the higher cost of production arising Variations in chicken breast meat quality: implications of struggle
from the longer growing period, would likely attract a and muscle glycogen content at death. Br. Poult. Sci. 46:572–579.
niche market and be able to fetch premium pricing for Berri, C., E. Le Bihan-Duval, E. Baeza, P. Chartrin, L. Picgirard,
N. Jehl, M. Quentin, M. Picard, and M. J. Duclos. 2005b. Further
the SGB, making it a suitable candidate for a slow- processing characteristics of breast and leg meat from fast-, medium-
growing welfare-oriented alternative for the Australian and slow-growing commercial chickens. Anim. Res. 54:123–134.
market. However, a cost-benefit analysis would be useful Berri, C., N. Wacrenier, N. Millet, and E. Le Bihan-Duval. 2001. Effect
to determine the feasibility of growing SGB in Australia. of selection for improved body composition on muscle and meat
characteristics of broilers from experimental and commercial lines.
Further research is also needed to evaluate meat Poult. Sci. 80:833–838.
nutrient content and taste characteristics of SGB. Cano
gulları Do

gan, S., M. Baylan, A. Bulancak, and T. Ayaşan. 2019.
Differences in performance, carcass characteristics and meat
quality between fast- and slow-growing broiler genotypes. Prog.
ACKNOWLEDGMENTS Nutr. 21:558–565.
Cheema, M., M. Qureshi, and G. Havenstein. 2003. A comparison of
The authors are most grateful for the exemplary ani- the immune response of a 2001 commercial broiler with a 1957
randombred broiler strain when fed representative 1957 and 2001
mal care provided throughout this experiment by broiler diets. Poult. Sci. 82:1519–1529.
Jadranka Velnic of Zootechny Pty Ltd. The research CIE (Commission Internationale de l’Eclairage). 1978. Recommen-
was financially supported by Poultry Research Founda- dations on uniform color spaces-color difference equations, psy-
tion at the Sydney School of Veterinary Science, Univer- chometric color terms, Supplement No. 2 to CIE Publication No.
15 (E-1.3.1) 1971/(TC-1$3), Paris, France.
sity of Sydney, Australia. Cobb-Vantress. 2007. CobbSasso breeder management Supplement.
Accessed Oct. 2020. https://www.cobb-vantress.com/assets/
Cobb-Files/product-guides/6c1436d72b/CobbSasso_Breeder_
Management_Supplement_v1_EN.pdf.
DISCLOSURES Comert, M., Y. Sayan, F. Kirkpinar, O. H. Bayraktar, and
S. Mert. 2016. Comparison of carcass characteristics, meat quality,
The authors declare that they have no conflict of inter- and blood parameters of slow and fast grown female broiler
est and competing interests. chickens raised in organic or conventional production system.
Asian-Australas. J. Anim. Sci. 29:987–997.
Cruz, F. L., L. K. V. Saraiva, G. E. Silva, T. M. Nogueira, A. P. Silva,
and P. B. Faria. 2018. Growth and carcass characteristics of
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