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Short- and long-term effects of conventional and artificial rearing
strategies on the health and performance of growing lambs
A. Belanche
1,2†
, J. Cooke
3
, E. Jones
1
, H. J. Worgan
1
and C. J. Newbold
1,4
1
IBERS, Aberystwyth University, Aberystwyth SY23 3DA, UK;
2
Estacion Experimental del Zaidín (CSIC), Profesor Albareda, 1, 18008 Granada, Spain;
3
Volac
International Ltd., Orwell, Cambridgeshire, Royston SG8 5QX, UK;
4
Scotland’s Rural College, Peter Wilson Building, King’s Buildings, Edinburgh EH9 3JG, UK
(Received 26 September 2017; Accepted 17 July 2018)
Artificial rearing of young animals represents a challenge in modern ruminant production systems. This work aims to evaluate the
short- and long-term effects of the type of rearing on the animal’s health, growth, feed utilization and carcass performance. A total
of 24 pregnant ewes carrying triplets were used. Within each triplet set, lambs were randomly allocated to one experimental
treatment: natural rearing on the ewe (NN); ewe colostrum for 24 h followed by artificial rearing with milk replacer (NA) and 50 g
of colostrum alternative supplementation followed by artificial rearing (AA). Milk replacer, ryegrass hay and creep feed were
offered
ad libitum
, and each experimental group was kept in independent pens until weaning at 45 days of age. After weaning all
lambs were placed together on the same pasture for fattening for 4 months. Blood samples were taken at 24 h after birth, at
weaning and at the end of the fattening period (23 weeks). Results showed that no failure in the passive immune transfer was
detected across treatments. Although artificially reared lambs at weaning had lower plasma levels of
β
-hydroxy-butyrate (−62%),
high-density lipoproteins (−13%) and amylase (−25%), and higher levels of low-density lipoproteins (+38%) and alkaline
phosphatase (+30%), these differences disappeared during the fattening period. Only the greater levels of calcium and the lower
levels of haemoglobin and white blood cells detected at weaning in artificially reared lambs (+7.2%, −2.8% and −17.8%)
persisted by the end of the fattening period (+4.3%, −3.3% and −9.5%, respectively). Minor diarrheal events from weeks 2 to 5
were recorded with artificial rearing, leading to lower growth rates during the 1
st
month. However, these artificially reared lambs
caught up towards the end of the milk feeding period and reached similar weaning weights to NN lambs. During the fattening
period NN lambs had a greater growth rate (+16%) possibly as a result of their greater early rumen development, which allowed a
higher feed digestibility during the fattening period in comparison to NA lambs (+5.9%). As a result, NN lambs had heavier final
BWs (+7.0%), but tended to have lower dressing percentage (−5.7%) than artificially reared lambs, thus no differences were
noted in either carcass weight or in carcass conformation across treatments. In conclusion, the use of a colostrum alternative and
milk replacer facilitated the successful rearing of lambs, reaching similar productive parameters; however, special care must be
taken to maximize the rumen development before weaning.
Keywords: animal performance, colostrum, health, milk replacer, weaning
Implications
This study revealed that artificial rearing of lambs with
colostrum alternative and milk replacer represents an appro-
priate strategy to maximize the number of lambs weaned per
ewe with a similar final BW achieved to lambs reared on the
ewe. However, direct contact with the ewe provided a
competitive advantage in naturally reared lambs allowing
them to better develop their immune system and rumen
function, which led to increased BW gain during the fatten-
ing period.
Introduction
Two main systems exist for rearing offspring in ruminant
production: in commercial dairy systems, or when dam milk
is not available in sufficient amount or sanitary condition,
newborns are separated from their dams within the first
hours after birth and fed either milk replacer or whole milk; in
contrast, in meat production systems, newborn animals gen-
erally remain with their dams until weaning. A recent study
has reported that goat kids reared with their dams had greater
rumen development than their twins fed on milk replacer and
isolated from adult animals, despite both groups having
access to the same solid feed (Abecia
et al
., 2014). However, it
†
E-mail: a.belanche@csic.es
Animal
, page 1 of 10 © The Animal Consortium 2018
doi:10.1017/S1751731118002100
animal
1
remains unknown whether these differences are transitory or if
they persist later in life during the fattening period.
Lambs are born hypogammaglobulinemic due to the
complexity of the synepitheliochorial ruminant placenta,
which does not allow sufficient transfer of immunoglobulins
from the dam to the foetus (Hernández-Castellano
et al
.,
2014; Hernández-Castellano
et al
., 2015), thus immunoglo-
bulin G (IgG) transfer from colostrum is vital for the neonatal
health (Arguello
et al
., 2004b). Insufficient neonatal absorp-
tion of colostral immunoglobulins within the 1
st
day of life
has been associated with failure of passive immunitytransfer,
which is indicated when serum IgG levels are below a certain
threshold (generally 10 mg/ml in calves, 12 mg/ml in goats
and 15 mg/ml in lambs) leading to increased risk for neonatal
diseases, mortality and with a negative effect on adult health,
longevity and performance (DeNise
et al
., 1989; Arguello
et al
., 2004a, Faber
et al
., 2005; Alves
et al
., 2015). As a
result, higher morbidity and mortality rates have been
observed in colostrum-deprived lambs (80% and 67%) than
colostrum-fed lambs (20% and 13%) (Hodgson
et al
., 1992).
In addition, there is increasing evidence showing that nutri-
tional management in the pre-weaning period determines to
a great extent the potential for milk production during sub-
sequent lactations: several studies have indicated that those
heifers fed with a greater volume of the same high-quality
colostrum (Faber
et al
., 2005) and those with a greater
plasma concentration of IgG shortly after birth (DeNise
et al
.,
1989) had higher milk yield than their counterpart control
animals during their productive life. Moreover, it has been
noted that increased growth rate before weaning results in
positive effects on milk yield in cattle (Soberon
et al
., 2012).
Thus, the general recommendation is to actively feed lambs
with colostrum from a freshly lambed ewe in order to max-
imize passive immunity transfer. However, when ewe colos-
trum is scarce the supplementation of lambs with colostrum
alternatives may represent a strategy to maximize the num-
ber of lambs weaned. Nevertheless, it remains unknown
whether these early life interventions in lambs could have
similar long-lasting consequences to those described in
cattle.
In this study we hypothesized that nutritional interven-
tions early in the life of the lambs could have immediate
effects on the animal’s health and performance, with some
effects persistent later in life under conventional production
systems. These nutritional interventions during the pre-
weaning period consisted of (1) lambs remained with the
ewe (natural rearing) (NN), (2) ewe colostrum followed by
artificial rearing with milk replacer (NA) and (3) colostrum
alternative supplementation and artificial rearing (AA).
Material and methods
Animals and diets
Triplet sibling lambs were used to provide similar genetic
background, gestation environment and ewe colostrum in
order to minimize the inter-animal variation across treatments.
Thus, after pregnancy scanning, 24 pregnant Aberdale ewes
carrying triplets were selected from the Aberystwyth University
commercial flock. A total of 72 Aberdale-texel crossbreed
lambs were born within an 8-day period (14–22 April). At
birth, umbilical cords were disinfected with iodine and lambs
were weighed. One sibling of each triplet set was randomly
allocated to one of three experimental treatments. During this
allocation process sex and initial BW of the lambs was con-
sidered resulting in similar sex distribution (average 13 males
and 11 females per group) and birth weights (3.8 ± 0.8 kg)
across treatments. All three sibling lambs were kept with their
mother in an individual pen during the first 24 h after birth.
Two siblings (NN and NA) were encouraged to suckle ewe
colostrum by connecting them to an ewe’s teat four times over
the first 24h (1, 2, 4 and 6 h after birth) until the gut filling was
evident in order to ensure a high colostrum intake. Then, one
of those siblings (NN) remained with its mother suckling ewe
milk from birth to weaning, whereas the second sibling (NA)
was separated from its dam after 24h and artificially reared
with milk replacer. On the contrary, the third sibling (AA) was
not encouraged to suckle ewe colostrum; instead, it was
immediately fed with 50 g of colostrum alternatively divided
into two equal doses at 1 and 6h after birth followed by
artificial rearing with milk replacer. In this latter group, no
obvious signs of gut filling with ewe colostrum were noted
suggesting a minimal intake of it. Colostrum alternative was
freshly prepared by mixing 25g of product (Lamb Volostrum;
Volar Ltd, Lampeter, UK) in 50ml of water at 30°C and pro-
vided by a stomach tube at each time (1 and 6 h after birth).
Milk replacer was prepared by mixing 200 g of milk powder
(Lamlac Instant; Volar Ltd) with water to make up 1 l of
reconstituted milk following the manufacturer instructions.
During their 1
st
week of life all lambs had access to heat lamps
and warm milk replacer (39°C) offered
ad libitum
using
temperature-controlled feeders (Ewe 2 Feeder; Volar Ltd).
Lambs that did not suckle were stomach tubed and trained to
suck from a teat connected to the milk feeder. After 1 week of
age all lambs were able to suckle and milk replacer was
offered
ad libitum
at room temperature (average 12°C) using
two buckets connected to four teats for each experimental
group. These milk buckets were emptied twice a day and
thoroughly cleaned and rinsed, using soap and hot water.
At 24 h after birth, blood was sampled (see below), and all
animals were tagged and intramuscularly injected with 1 ml
of AD
3
E (NAPHA Veterinary, Ho Chi Minh City, Vietnam) to
prevent vitamin deficiency. Then, all lambs from the same
treatment were placed together in a single pen (10 ×12 m)
with clean and dry barley straw bedding and
ad libitum
access to creep feed (NuGro CCF, Aberystwyth, UK), ryegrass
hay and water (chemical composition described in Supple-
mentary Table S1). During the milk feeding stage all three
groups of animals were physically separated from each other
(1 m gap) but kept in the same building with an average
temperature of 12°C, relative humidity of 86% and an
average of 10 h of day light. Treatments NA and AA also had
free access to milk replacer which was freshly prepared twice
a day at 0900 and 1700 h. Lambs from treatment NN shared
Belanche, Cooke, Jones, Worgan and Newbold
2
a pen with their mothers that were fed twice a day with the
same ryegrass hay and commercial concentrate (Wynnstay;
High Production Ewes, Llanidloes, UK). Ewes were physically
separated from the NN lambs for 10 min during the con-
centrate feeding. Group intakes of milk replacer and creep
feed were recorded daily until weaning. Animals were
inspected daily for signs of disease. The severity of diarrheal
events was recorded based on the following score index
(Bentounsi
et al
., 2012): 1 corresponds to normal lamb fae-
ces in pellets, 2 corresponds to ‘soft’faeces (similar to cow
pat), 3 corresponds to mild diarrhoea with semi-liquid faeces
and 4 corresponds to profuse diarrhoea with liquid faeces.
Animals with a score equal or above 3 received a single dose
of intramuscular antibiotic treatment (Pen-Strep; Norbrook
Laboratories Ltd, Newry, Northern Ireland). Lambs were
weekly weighed using a digital balance to determine their
growth during the entire duration of the experiment.
Animals were weaned at 45 days of age by abrupt
weaning and kept in the same building with the same solid
feed for a further week. When lambs were on average
8 weeks of age, all experimental lambs were grouped toge-
ther on the same ryegrass pasture (
Lolium perenne
) with free
access to creep feed until 10 weeks of age but not thereafter.
Thus, all lambs grazed the same pasture over 5 months (from
June to November). Animals belonging to the same sibling
set were always sampled and weighed at the same time.
Moreover, when the average BW of a given set of siblings
reached the optimum slaughter weight (~40 kg and between
23 and 31 weeks of age), all three lambs were slaughtered in
a commercial abattoir. Carcass weight and performance was
assessed at an official abattoir according to the EUROP
classification (Johansen
et al
., 2006).
Sampling and analyses
Blood samples (5 ml) were collected from the jugular vein
at 24 h after birth for IgG and blood cells measurements.
Moreover, blood samples were also taken when animals
reached 45 days of age (weaning) and at 23 weeks of age
(near the end of the fattening period). One blood sub-
sample (2 ml) was placed in a tube with anticoagulant
(K
3
-ethylenediaminetetraacetic acid) mixed by inversion
10 times, kept at 4°C and immediately analysed for haematology
using a Mythic 18 Vet Haematology Analyser (Woodley Equip-
ment Company Ltd, Horwich, UK). This analysis determined the
levels of the main blood cells and their morphotypes (see below).
A second subsample (3 ml) was placed in a tube without antic-
oagulant; serum was harvested by centrifugation at 2000 ×gfor
15 min and stored at −20°C until analysis. Serum metabolites
were determined using RX Daytona
+
equipment (Randox
Laboratories Ltd, Crumlin, UK).
Colostrum (10 ml) and milk (50 ml) samples were obtained
by hand milking from each ewe at 24 h after the birth of the
first lamb and at 45 days postpartum, respectively. Samples
were kept frozen, and milk and colostrum composition
(Table 1) was determined using a milk analyser (LactoScope
Advance FTIR; Delta Instruments, Drachten, The Nether-
lands). Concentration of IgG in serum and colostrum was
determined using the Sheep IgG ELISA 96-well plate kit
(reference GWB-OVI374; GenWay Biotech Inc, San Diego,
CA, USA) after dilution (4 ×10
−4
and 4 ×10
−6
for serum and
colostrum, respectively) and absorbance determination at
450 nm using a plate reader (PowerWave XS2; BioTek,
Swindow, UK). Concentration of IgG was also estimated
based on the serum density: Temperature corrected density
(
nD
TC
) in serum samples (100 µl) was measured in triplicate
using an automatic digital refractometer (Reichert AR200 Ver
1.8, Ametek, Germany) and the estimated serum IgG
concentration was obtained based on the regression
equations described by Morril (2011): IgG (mg/
ml) =5919.1 ×
nD
TC
−7946.1.
Faecal analysis
At 23 weeks of age, faecal grab samples were collected
from each animal on 2 non-consecutive days, frozen and
pooled by animal (30 g dry matter (DM) approximately). On
the same day as faecal sampling, ryegrass pasture was cut
to 5 cm above soil level from four different locations of the
field and immediately frozen for further analysis. The effect
of the experimental treatments on pasture digestibility was
estimated using the acid insoluble ash as an internal mar-
ker (Thonney
et al
., 1979). For feed and faeces analyses,
DM content was determined by drying in an oven at 105°C
for 24 h. Organic matter (OM) concentration was deter-
mined by heating at 550°C for 6 h in a muffle furnace.
Nitrogen and carbon concentration was measured by the
Dumas combustion method (Elementar analyser; Vario
MAX cube, Langenselbold, Germany). Neutral-detergent
fibre and ADF were determined using an automated fibre
analyser (ANKOM 2000; Ankom Technology, Macedon, NY,
USA) using heat stable amylase and sodium sulphide.
For faecal fingerprint analysis, samples were analysed as
previously reported (Belanche
et al
., 2017). Briefly, freeze dry
samples were ground to a fine powder (IKA Analytical Mill,
Staufer, Germany) and analysed by attenuated total reflec-
tance (ATR) from 4000 to 600 cm
−1
using an Equinox 55
Fourier transformed IR (FTIR) spectrophotometer (Bruker Ltd,
Table 1
Colostrum and milk composition from sheep
Colostrum Milk
Natural
1
Alternative
2
Natural
1
Replacer
3
Crude protein (%) 22.6 22.1 4.35 4.77
Fat (%) 15.5 4.52 5.51 4.84
Lactose (%) 2.79 2.82 4.90 7.33
Solids (%) 40.9 30.5 15.4 17.4
Solids non-fat (%) 27.2 27.9 10.4 13.1
Immunoglobulin G (g/l) 42.2 32.1
1
Natural colostrum and milk sampled at 24 h and 45 days after parturition,
respectively.
2
Values after mixing 25 g of colostrum alternative with 50 ml of water. Figures
obtained experimentally which may differ from the declared composition.
3
After mixing 200 g of milk replacer with water to make up 1 l of reconstituted
milk. Figures obtained experimentally which may differ from the declared
composition.
Effects of artificial rearing of lambs
3
Coventry, UK), and scanned using the Golden Gate ATR
accessory (Specac Ltd, Slough, UK). Infrared settings and
data collection were conducted as previously reported
(Belanche
et al
., 2014). Fourier transformed IR spectra were
imported into Matlab (version 2007b; The MathWorks Inc.,
Natick, MA, USA), averaged, transformed to the first
Savitzky–Golay derivative to smooth baseline noise and
improve spectral resolution using a 13-point window, and
then mean centre normalized (mean =1, standard devia-
tion =1). Data were then analysed by non-parametric per-
mutational multi-variate analysis of variance using
PRIMER-6 software (PRIMER-E Ltd, Plymouth, UK). Statis-
tical signification was calculated after 999 random permu-
tations of residuals under a reduced model using the
Monte-Carlo test. For graphical interpretation, principal
component analysis was conducted and a canonical variate
analysiswasperformedbasedonthedatacompiledinthe
main principal components (Genstat 18
th
Edition, VSN
International, Hemel Hempstead, UK).
Calculations and statistical analysis
Haematological analysis determined the levels of red blood
cells, haemoglobin, haematocrit, mean corpuscular volume
(MCV), mean corpuscular haemoglobin (MCH), mean corpus-
cular haemoglobin concentration (MCHC), red blood cell dis-
tribution width (RBCDW), white blood cells and its morphotype
percentages, platelets, mean platelets volume (MPV), throm-
bocrit and platelet distribution width (PDW). Although the
plasma metabolic analysis measured: calcium, glucose, β-
hydroxybutyrate (BHB), cholesterol, triglycerides, high-density
lipoproteins (HDL), low-density lipoproteins (LDL), albumin,
creatinine, urea, ammonia, L-lactate dehydrogenase and alka-
line phosphatase levels, globulins and LDL concentrations in
plasma were mathematically calculated:
Globulins =Total proteins Albumin
LDL =Cholesterol HDL Triglycerides=5ðÞ
To evaluate the effect of experimental treatments on blood
parameters, data were analysed using a repeated measures
procedure (residual maximum likelihood) using Genstat 18
th
edition (VSN International, Hemel Hempstead, UK) as fol-
lows:
Yijk =μ+Ri+Tj+RTij +Tk+Al+eijkl
where
Y
ijk
is the dependent, continuous variable (
n
=24),
µ
the overall mean,
M
i
the fixed effect of the type of rearing
(
i
=NN
v
.NA
v
. AA),
T
j
the fixed effect of the animal age
(
j
=weaning v. fattening),
FV
ij
is their interaction,
S
k
the
random effect of the triplet set used as a block (
k
=1–24),
A
l
the random effect of the animal (
j
=1–72) and
e
ijkl
is the
residual error. For animal weight, growth and carcass per-
formance data, the term sex (male
v
. females) was also
included as a fixed effect. When significant effects were
detected across treatments, means were compared by Fish-
er’s protected LSD test. Significant effects were declared at
P
<0.05.
Results
Animal health
At 24 h after birth all animals remained in good health and
no haematological differences were observed across treat-
ments (Table 2). Alternative supplementation followed by
artificial rearing lambs tended to have lower plasma IgG
concentrations at 24 h of age in comparison to NN and NA
lambs when measured by refractometry (
P
=0.075) but did
not reach statistical significance when measured with ELISA
(
P
=0.135). Animals artificially reared (NA and AA) suffered
a greater incidence of diarrhoea episodes than NN lambs
from 2 to 5 weeks of age but this effect disappeared there-
after. Antibiotic usage was also higher for NA and AA lambs
than for NN lambs (
P
<0.001) and the number of animals
with recurrent diarrhoea which required more than two
antibiotic doses were 0, 6 and 9 for NN, NA and AA lambs,
respectively. No antibiotic treatment was required for any
lamb from week 5 onwards.
The age of the lambs exerted a major effect on the blood
cell distribution (Table 3) and the concentration of most
plasma metabolites (Table 4). At weaning animals had a
greater concentration of red blood cells, haemoglobin,
RBCDW, lymphocytes, platelets, thrombocrit and plasma
levels of calcium, glucose, cholesterol, triglycerides, HDL,
LDL, albumin, creatinine, amylase and alkaline phosphatase
than animals at fattening (
P
<0.01). On the contrary, at
fattening animals had a greater concentration of white blood
cells, monocytes, granulocytes, MPV, PDW and plasma levels
of BHB, total proteins, globulins and urea (
P
<0.001).
Table 2
Effect of colostrum alternative and artificial rearing on plasma
immunoglobulin G (IgG) levels and haematology at 24 h after birth and
incidence of diarrhoea in lambs
Types of rearing NN NA AA SED
P
-value
Red blood cells (10
6
/µl) 8.20 7.77 8.01 0.221 0.152
White blood cells
(10
3
/µl)
6.48 5.82 6.01 0.539 0.461
Platelets (10
3
/µl) 630
a
502
b
575
ab
48.8 0.041
Haematocrit (%) 38.0 36.2 37.3 1.14 0.276
ELISA IgG2 (mg/ml) 40.1 45.6 37.1 4.19 0.135
Refractometer IgG
(mg/ml)
38.3 38.3 32.5 2.88 0.075
Diarrhoea score
1
Week 2 1.13
b
1.83
a
2.04
a
0.229 <0.001
Week 3 1.29
b
1.96
a
2.33
a
0.269 0.001
Week 4 1.08
b
1.96
a
1.92
a
0.252 0.001
Week 5 1.04
b
1.58
a
1.96
a
0.227 <0.001
Week 6 1.04 1.08 1.25 0.121 0.201
Week 7 1.04 1.04 1.17 0.108 0.415
Antibiotic usage
(doses/lamb)
2
0.08
b
0.96
a
1.42
a
0.333 <0.001
IgG =Immunoglobulin G; NN =natural rearing; NA =ewe colostrum and arti-
ficial milk feeding; AA =colostrum alternative and artificial milk feeding;
SED =Standard error of the difference among means.
a,b
Within a row means without a common superscript differ (
P
<0.05).
1
Diarrhoea score: 1, absence, 2, very mild, 3, moderate and 4, severe.
2
Intramuscular penicillin–streptomycin.
Belanche, Cooke, Jones, Worgan and Newbold
4
However, artificial rearing also had some mid- and long-term
effects on the animals’health (Table 3). Independently of the
age considered, NN lambs had a greater haemoglobin
(
P
=0.029), haematocrit (
P
=0.070), white blood cells
(
P
=0.009) and calcium levels than NA and AA lambs.
Moreover, a significant interaction was observed for several
metabolites and haematological parameters: at weaning NN
lambs had greater RBCDW (
P
>0.001), BHB (
P
<0.001), HDL
(
P
=0.025) and amylase plasma levels (
P
<0.001), as well as
lower MCHC (
P
=0.012), PDW (
P
=0.013), LDL (
P
=0.009)
and alkaline phosphatase (
P=
0.002) were observed in NN
lambs than in NA or AA, but no such differences were
observed at fattening.
Animal performance
Average group intake of milk replacer remained constant
until week 3 (300 g DM/day per lamb) and linearly increased
thereafter reaching 550 g DM/day at weaning for AA and NA
groups, while milk intake in NN lambs was not recorded.
Group intake of creep feed also remained low and constant
until week 4 across treatments, and increased linearly
thereafter reaching an average of 256, 137 and 96 g DM/day
at weaning for treatments NN, NA and AA, respectively. No
differences in BW were observed at birth across treatments,
but NN lambs had a greater BW than NA and AA lambs from
week 2 to 5. These differences disappeared during the
weaning stage and reappeared from week 11 onwards
(Figure 1). No differences in the average daily gain (ADG)
were observed before weaning (Table 5), but NN lambs had a
greater ADG during the fattening period calculated from
weaning to 23 weeks of age (
P
<0.001). In terms of carcass
composition, NN lambs had a higher slaughter weight than
NA and AA lambs (
P
<0.001), but NN lambs tend to have a
lower dressing percentage resulting in similar carcass weight
and conformation across treatments. Male lambs tended to
have a greater BW at birth and ADG during the fattening
period (
P
=0.047); however, no differences were observed in
carcass conformation.
Pasture utilization
The chemical structure of the faecal samples tended to differ
(
P
=0.079) between treatments based on the PERMANOVA
analysis of the FTIR spectral data (Supplementary Table S2).
Canonical variate analysis (Figure 2) compiling the informa-
tion of the first 15 principal components (representing 98.1%
of the total variance) showed that these differences were
more obvious between NA and the other two experimental
groups. In terms of pasture digestibility (Table 6), values
were always highest for NN lambs: NN and AA lambs had
higher digestibility for DM (
P
<0.001), C (
P
<0.001) and
N
(
P
=0.003) than NA lambs, whereas no differences were
observed in NDF and ADF digestibility.
Discussion
Effect of colostrum alternative
Colostrum products have been shown to provide a degree of
passive immunity transfer (Seymour
et al
., 1995; Castro
et al
., 2007), although the results vary greatly depending on
the product used, colostrum preservation methods, dosage
techniques and inter-animal variation (Arguello
et al
.,
2004b). As a result, colostrum products that typically contain
lacteal-derived or plasma-derived IgG are classified as either
colostrum replacers or colostrum supplements depending on
their ability to raise serum IgG concentration above a certain
Table 3
Effect of colostrum alternative and artificial rearing on haematology and blood metabolites in lambs
Weaning (45 days) Fattening (23 weeks)
P
-value
Types of rearing NN NA AA NN NA AA SED Rearing Age R ×A
Red blood cells (10
6
/µl) 11.4 11.4 11.7 11.3 10.9 11.1 0.233 0.357 0.002 0.323
Haemoglobin (g/dl) 11.5 11.0 11.3 11.1 10.6 10.8 0.176 0.029 0.002 0.982
Haematocrit (%) 38.3 35.8 36.7 36.2 34.6 37.5 1.441 0.07 0.401 0.417
MCV (fL) 33.6 31.5 32.1 32.1 31.9 34.0 1.448 0.305 0.723 0.299
MCH (pg) 10.1 9.72 9.77 9.83 9.74 9.78 0.201 0.241 0.555 0.577
MCHC (%) 30.0
b
30.8
a
30.8
a
30.6
a
30.6
a
30.7
a
0.211 0.006 0.448 0.012
RBCDW (%) 25.4
a
20.0
b
20.7
b
17.9
c
18.2
c
17.9
c
0.523 <0.001 <0.001 <0.001
White blood cells (10
3
/µl) 7.95 6.31 6.76 8.91 8.40 7.73 0.571 0.009 <0.001 0.273
Lymphocytes (%) 56.5 56.9 54.4 53.2 47.6 51.1 2.398 0.355 <0.001 0.121
Monocytes (%) 11.6 11.9 10.9 13.7 14.7 14.4 0.620 0.371 <0.001 0.181
Granulocytes (%) 31.9 31.2 34.7 33.1 37.6 34.5 2.114 0.352 0.043 0.066
Platelets (10
3
/µl) 1982
a
1419
b
1695
ab
548
c
616
c
639
c
182.7 0.129 <0.001 0.054
MPV (fl) 5.20 4.90 4.71 5.71 5.98 5.75 0.363 0.662 <0.001 0.419
Thrombocrit 1.10 0.72 0.82 0.29 0.33 0.62 0.197 0.265 <0.001 0.078
PDW (%) 30.1
d
36.0
c
34.9
c
46.0
a
42.1
b
44.0
ab
2.437 0.678 <0.001 0.013
NN =natural rearing; NA =ewe colostrum and artificial milk feeding; AA =colostrum alternative and artificial milk feeding; SED =Standard error of the difference
among means; R ×A=Interaction rearing system and age; MCV =mean corpuscular volume; MCH =mean corpuscular haemoglobin; MCHC =mean corpuscular
haemoglobin concentration; RBCDW =red blood cell distribution width; MPV =mean platelets volume; PDW =platelet distribution width.
a,b
Within a row means without a common superscript differ (
P
<0.05).
Effects of artificial rearing of lambs
5
threshold (typically 15 mg/ml in lambs) (Alves
et al
., 2015).
Colostrum supplements (as in our study) can be used to
increase the amount of IgG fed to lambs when only low or
medium quality/quantity colostrum is available. However,
supplements cannot replace high-quality colostrum, which is
still considered the gold standard for feeding newborn lambs
(Jones
et al
., 2004). Our study aimed to simulate two real
scenarios in the artificial rearing of lambs: one (NN and NA
lambs) consisting of maximizing colostrum intake by
encouraging lambs to suckle for at least four times from the
ewe; and an alternative strategy (AA lambs) based on
colostrum alternative supplementation of lambs with an
insufficient intake of ewe colostrum. To achieve this later
situation, AA lambs were not encouraged to suckle and had
to compete with their two siblings for the remaining ewe
colostrum.
A rapid change in the colostrum composition to transi-
tional milk has been described during the post-partum period
(Alves
et al
., 2015). In our study, despite the late sampling of
ewe colostrum (24 h after the first lamb was born), the IgG
concentrations (average 42.2 g/l) were comparable to pub-
lished literature (from 15.7 to 65 g/l) in which the samples
were collected just after parturition (Vatankhah, 2013; Alves
et al
., 2015; Hernández-Castellano
et al
., 2015), possibly as a
result of a higher colostrum production in high prolific ewes.
As a result, only one lamb had an IgG concentration below
15 mg/ml at 24 h after birth suggesting effective overall
passive immunity transfer across treatments (Alves
et al
.,
2015). This may explain the lack of differences in terms of
growth, haematology parameters and blood metabolites
levels between NA and AA lambs, as well as the absence of
deaths before weaning. Moreover, the high level of easily
digestible energy and protein in the colostrum alternative
Table 4
Effect of colostrum alternative and artificial rearing on blood metabolites in lambs
Weaning (45 days) Fattening (23 weeks)
P
-value
Items
1
NN NA AA NN NA AA SED
1
Rearing Age
R
×
A
Calcium (mM) 2.33 2.52 2.48 1.84 1.92 1.93 0.122 0.067 <0.001 0.832
Energy
Glucose (mM) 5.47 5.89 5.75 3.50 3.56 3.56 0.319 0.438 <0.001 0.732
BHB (µM) 265
b
100
c
100
c
342
a
372
a
394
a
30.56 <0.001 <0.001 <0.001
Lipids (mM)
Cholesterol 2.82 2.91 2.79 1.27 1.31 1.23 0.163 0.683 <0.001 1
Triglycerides
2
0.78 0.72 0.75 0.24 0.21 0.24 0.063 0.512 <0.001 0.909
HDL 1.91
a
1.65
b
1.66
b
0.62
c
0.65
c
0.61
c
0.092 0.16 <0.001 0.025
LDL
1
0.76
b
1.11
a
0.98
a
0.60
c
0.61
c
0.57
c
0.090 0.032 <0.001 0.009
Proteins (g/l)
Total proteins 45.4 46.7 46.3 65.3 67.3 66.6 2.646 0.659 <0.001 0.986
Albumin 32.9 33.5 33.3 30.2 31.1 31.2 1.061 0.55 <0.001 0.919
Globulin
1
12.5 13.3 13.0 35.1 36.2 35.4 1.803 0.771 <0.001 0.985
Creatinine (µM) 83.0 85.8 87.9 78.3 80.4 78.5 4.802 0.597 0.029 0.811
Urea (mM) 3.85 3.95 3.82 9.98 9.85 10.1 0.357 0.96 <0.001 0.756
Ammonia (µM) 83.6 81.9 85.2 84.9 86.0 89.7 5.704 0.593 0.306 0.928
Enzymes (U/l)
Amylase 25.7
a
20.3
b
18.3
b
12.5
c
10.8
c
12.6
c
1.676 0.021 <0.001 <0.001
L-lactate dehydrogenase 1171 1238 1112 1163 1093 1098 64.69 0.302 0.136 0.248
Alkaline phosphatase 637
b
841
a
819
a
177
c
184
c
183
c
43.39 0.002 <0.001 0.002
NN =natural rearing; NA =ewe colostrum and artificial milk feeding; AA =colostrum alternative and artificial milk feeding; SED =Standard error of the difference
among means;
R
×
A
=Interaction rearing system and age; BHB =beta-hydroxybutyrate; HDL =high-density lipoproteins; LDL =low-density lipoproteins.
a,b,c
Within a row means without a common superscript differ (
P
<0.05).
1
Mathematically calculated: LDL =Cholesterol −HDL −(Triglycerides/5); Globulin =Total proteins −Albumin.
0
5
10
15
20
25
30
35
40
0123456789
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
Body weight (kg)
Age (weeks)
NN
NA
AA
Weaning
Lactation Fattening
**
ns
ns ns
ns
ns
ns
*
**
**
*
**
**
**
** **
**
Figure 1 Effect of colostrum alternative and artificial rearing on lamb’s
growth. NN, natural rearing; NA, ewe colostrum and artificial milk
feeding; AA, colostrum alternative and artificial milk feeding. Standard
error of the mean level of signification is depicted: ns, not significant,
*
P
<0.05, **
P
<0.01.
Belanche, Cooke, Jones, Worgan and Newbold
6
also seems to represent an important source of nutrients for
the lambs during its first hours of life to maintain body
temperature and good health (Jones
et al
., 2004). Thus, the
supply of colostrum alternative after birth can be considered
an appropriate strategy to prevent health problems and
maximize the number of lambs weaned per ewe when ewe
colostrum is insufficient.
Effect of artificial rearing on lamb’s health
This study does not attempt a direct comparison of the
effects of milk replacer
v
. maternal milk since artificial
rearing involves the replacement of the contributions made
by the ewe which are essential to the growth and develop-
ment of the lamb. This not only includes the feed supply but
also the warmth, shelter and ‘mothering’normally provided
by the ewe. Our experiment showed a greater incidence of
diarrhoea events in artificially reared lambs than those
reared on the ewe. These diarrhoea episodes appeared from
week 2 to week 5; they were very mild (<2.0 scored) and
required an average of 1.2 antibiotic doses per lamb, whilst
antibiotic usage in NN lambs was negligible. Although these
diarrheal events did not trigger any deaths, they could
explain the lower ADG for NA and AA lambs during the first
5 weeks. Similar diarrhoea events starting at 2 weeks of age
have been described in calves and various pathogens com-
patible with enteric infections have been identified in the
necropsy (i.e.
Salmonella
,
Cryptosporidium parvum
,
Escher-
ichia coli
and coronavirus) (Quigley
et al
., 2006). None of the
lambs required the use of antibiotics from week 5 onwards,
and the study of the rumen microbial community showed no
residual antibiotic effects at 45 days and 23 weeks of age
(data not shown). Thus, the potential long-term effect of
antibiotics on blood metabolites and animal performance
seems to be negligible under our experimental conditions.
Table 5
Effect of colostrum alternative and artificial rearing on animal and carcass performances in lambs
Type of lactation Sex
P
-value
Items NN NA AA Males Females SED
1
Rearing Sex
Animal performance
BW at birth (kg) 3.81 3.89 3.88 4.07 3.56 0.124 0.794 0.005
BW at weaning, 45 days (kg) 18.5 18.9 18.3 19.1 18.0 0.572 0.583 0.001
BW at fattening, 23 weeks (kg) 38.6
a
37.2
b
35.3
b
38.7 35.2 1.022 0.004 0.035
ADG from 0 to 45 days (g/day) 325 332 318 332 319 5.110 0.568 0.444
ADG from 45d to 23 weeks (g/day) 176
a
153
b
150
b
170 150 5.050 <0.001 0.047
Carcass performance
Final BW (kg) 42.3
a
40.4
b
38.7
b
41.4 39.5 0.754 <0.001 0.155
Warm carcass weight (kg) 18.3 18.2 17.6 18.6 17.4 0.532 0.624 0.490
Dressing percentage (%) 43.1
b
45.3
a
46.2
a
45.3 44.2 1.390 0.052 0.311
Conformation
1
3.78 3.63 3.61 3.82 3.52 0.167 0.750 0.853
Fatness
1
2.72 2.74 2.76 2.76 2.76 0.166 0.971 0.495
NN =natural rearing; NA =ewe colostrum and artificial milk feeding; AA =colostrum alternative and artificial milk feeding; ADG =average daily gain; SED =standard
error of the difference among means.
1
EUROP classification. Conformation: E =5, U =4, R =3, O =2, P =1. Fatness: 1 =1, 2 =2, 3 L =3, 3 H =3.5, 4 L =4, 4 H =4.5, 5 =5.
2
0
-2
32
10
-1
-1
1
-3
-2
Canonical variate 1
Canonical variate 2
NN
NA
AA
AA
NN
NA
Figure 2 Canonical variate analysis illustrating the impact of nutritional
intervention in early life on the faecal Fourier-transform infrared spectra
from lambs of 23 weeks of age. NN, natural rearing (
circles
); NA, ewe
colostrum and artificial milk feeding (
crosses
); AA, colostrum alternative
and artificial milk feeding (
triangles
). Big circles indicate the 99%
confidence interval of the mean for each treatment.
Table 6
Effect of artificial rearing on total tract digestibility (% in dry
matter (DM) basis) in grazing lambs (23 weeks of age)
Items NN NA AA SED
P
-value
DM 66.3
a
62.6
b
65.0
a
0.83 <0.001
Carbon 61.7
a
56.8
b
60.3
a
1.02 <0.001
Nitrogen 75.5
a
73.2
b
75.1
a
0.69 0.003
NDF 51.7 50.7 53.8 1.36 0.143
ADF 38.4 34.2 36.5 2.47 0.327
NN =natural rearing; NA =ewe colostrum and artificial milk feeding; AA =
colostrum alternative and artificial milk feeding; SED =Standard error of the
difference among means.
a,b
Within a row means without a common superscript differ (
P
<0.05).
Effects of artificial rearing of lambs
7
Various studies have investigated the effect of different
artificial milk feeding strategies to prevent diarrheal events
and to improve animal performance: Jasper and Weary
(2002) concluded that
ad libitum
nipple feeding of whole
milk to dairy calves v. restricted can increase weight gain
with no diarrheal problems nor detrimental effects on feed
intake after weaning. Quigley (2006) observed calves that
fed a variable amount of milk replacer (peaking at 3 weeks of
age with 908 g/day) had not only greater ADG but also
increased incidence of diarrhoea which required added
veterinary treatment in comparison to those fed a fixed
amount (454 g/day). Thus, it seems that our artificial rearing
strategy based on the
ad libitum
access to milk replacer
might not only explain the incidence of moderate diarrhoea
but also did help to prevent feed competition between
lambs, because lambs in contrast to calves tend to be reared
in groups with a large number of animals. More research is
needed to assess whether these diarrheal events could be
minimized by using alternative rearing systems such as
automatic feeding machines.
Although most lambs remained in good health from birth
to slaughter, the haematological analysis revealed that NN
lambs had higher levels of white blood cell at weaning in
comparison to artificially reared lambs (+21.6%), and those
differences persisted during the fattening period (+10.5%). It
has been shown that colostrum and milk have viable cells,
including neutrophils and macrophages, which secrete a
range of immune-related components (Stelwagen
et al
.,
2009). Our findings are in line with this observation and
suggest that direct contact with adult animals in NN may
also represent an important exposure to antigens, which may
help in the immune system development of young lambs
with long-lasting effects on the levels of white blood cells.
Moreover, artificially reared lambs had lower haemoglobin
levels (−2.8%) and haematocrit (−5.3%) at weaning in
comparison to NN lambs. The variation in the size of red cells
(anisocytosis) provided an insight of the potential reasons of
slight signs of anaemia. Since neither the size of the red
blood cells (MCV) nor the amount of haemoglobin per cell
(MCH) were affected, it seems that the normocytic anaemia
was very mild and partially compensated by a greater
amount of haemoglobin per unit of volume (MCHC +2.6%).
Despite this lack of severity, artificially reared lambs still had
lower levels of haemoglobin (−3.3%) and haematocrit
(−0.4%) during the fattening period suggesting a small but
long-term effect of the type of rearing strategy on the ani-
mals’health. On the contrary, NN lambs had a higher coef-
ficient of variation in RBCDW (+20.0%), which is compatible
with early stages of iron deficiency at weaning in animals
having limited amounts of milk (Blaxter
et al
., 1957), possibly
as a result of a lower milk intake and lower iron content in
the ewe milk in comparison to lambs fed milk replacer
ad
libitum
. This observation was supported by the lower blood
calcium concentration in NN lambs at weaning (−6.7%) and
fattening (−4.2%). Increases in plasma glucose and urea
concentrations have been associated with higher artificial
milk intake in calves (Quigley
et al
., 2006). However, in our
study all experimental treatments had similar glucose, urea
and total protein levels at weaning, possibly because a lower
milk intake in NN lambs during late milk feeding period in
comparison to those fed milk replacer was compensated by a
greater creep feed intake (256
v
. 116 g/day). Our experiment
indicates that protein and energy sources included in the milk
replacer were highly digestible since no differences in the
plasma concentration of metabolites related with the protein
(total proteins, albumin, globulin, creatinine, urea and
ammonia) and energy (glucose) metabolism were detected
across treatments. These findings agree with the similar
content of urea nitrogen, total protein, albumin and globulin
in the serum of lambs fed milk replacers made up of milk
protein or other protein sources (Huang
et al
., 2015). Most of
the milk bypasses the rumen through the oesophageal
groove, thus high milk intake in artificially reared lambs may
increase the amino acid flow to the small intestine leading to
an increase in the deamination processes occurring in the
liver as was reflected by increased levels of alkaline phos-
phatase (+30%) as an indicator of the liver stress (Reichling
and Kaplan, 1988). On the contrary, solid feed (carbohy-
drates and proteins) is fermented in the rumen producing
volatile fatty acids and ammonia as the main fermentation
end product. Thus, the increased levels of
β
-hydroxybutyrate
in NN at weaning (+2.6-fold times) suggest a greater phy-
siological and fermentative development of the rumen.
Although cholesterol and triglyceride concentrations were
unaffected by the experimental treatments, artificially reared
lambs had lower levels of HDL (−13%) and higher levels of
LDL (+38%) at weaning than NN lambs. Increased blood
levels of LDL are considered a circulatory risk factor, which
can be mainly determined by diet, physical activity, genetics,
sex and age (Sigurdardottir
et al
., 2002). Overall, our data
also showed that most of the haematological and metabolite
differences observed at weaning were transient and tended
to disappear later in life with no further effects on the ani-
mal’s health.
Effect of artificial rearing on productive performance
This study revealed that in comparison with artificially reared
lambs, NN lambs had a higher neonatal growth, suggesting
that the ewe mothering instinct helps lambs to suckle more
efficiently during the 1
st
days of life. Moreover, this compe-
titive advantage was maintained until 3 weeks after birth,
when NN lambs reached the greatest differences in BW
(+10.5%), corresponding with the peak in the lactation
curve described for crossbred ewes rearing lambs (Cardellino
and Benson, 2002). However, these differences tended to
disappear as weaning approached, possibly due to the
increased milk intake recorded for the artificially reared
lambs (average 2.9 l/day), resulting in similar BW at weaning
across treatments. This observation agrees with the lack of
differences in weaning weights reported for Comisana lambs
reared artificially or conventionally (Napolitano
et al
., 2002).
However, differences in BW gain reappeared after wean-
ing despite all lambs being grazed together on the same
pasture. As a result, NN lambs had a greater growth during
Belanche, Cooke, Jones, Worgan and Newbold
8
the fattening period (+16%) and higher BW from week 13
onwards. Several reasons could explain these findings: (i) The
greater solid feed intake observed in NN lambs at weaning
(256
v
. 116 g DM/day) has been described as a key factor
which promotes the rumen physiological development in
calves and facilitates a smooth transition to the solid diet
(Khan
et al
., 2011). (ii) The direct contact with adult animals
represents a source of microbes (i.e. bacteria, protozoa,
methanogens, anaerobic fungi) which are crucial for the
development of the symbiotic rumen microbiota (Belanche
et al
., 2010; Belanche
et al
., 2011). (iii) Adult animals teach
young animals in terms of feeding behaviour since the pre-
sence of adult companions has been reported to increase
solid feed intake and performance of calves before and after
weaning (Vieira
et al
., 2012) as was noted in our experiment.
Our findings also suggest that the greater BW gain in NN
lambs during the fattening period may in part be explained
by greater feed DM digestibility (+5.9%) in comparison to
NA lambs, although differences were less obvious (+2.0%)
when compared with AA lambs. These differences in forage
utilization were also observed based on the fingerprint ana-
lysis of faecal samples using FTIR spectroscopy. As a result,
NN lambs reached a greater final BW (+7.0%) at slaughter
but they performed substantially worse in dressing percen-
tage (−5.7%) leading to similar carcass weight, carcass
confirmation and fatness. This observation indicates that NN
lambs may have a greater rumen size, slower rumen transit
time or greater wool yield all of which could reduce the
killing out percentage. These findings support previous
observations which suggest that rearing lambs on the ewe,
and the early intake of solid feed are important drivers not
only for the rumen anatomical enlargement but also for the
physiological and microbiological development (Yáñez-Ruiz
et al
., 2015). Thus, more research is needed based on a better
description of the rumen dynamics of feed utilization, rumen
microbiota and animal behavioural studies to elucidate
which factor plays a greater role on animal resilience and
productivity during the post-weaning processes as well as
later in life.
Acknowledgements
This work has been supported by the European Regional
Development Fund Program through the Welsh Government
(WISE Network) and Volac International Ltd. The authors thank
D. R. Yáñez-Ruiz for his contribution to the paper preparation.
Declaration of interest
There is not conflict of interests.
Ethical standards
All animal procedures were carried out according to the Home
Office Scientific Procedures, Act 1986 and protocols were
approved by the Aberystwyth University Ethics Committee (PLL
40/3653; PIL 40/9798).
Software and data repository resources
None of the data were deposited in an official repository
Supplementary material
To view supplementary material for this article, please visit
https://doi.org/10.1017/S1751731118002100
References
Abecia L, Ramos-Morales E, Martínez-Fernandez G, Arco A, Martín-García A,
Newbold C and Yáñez-Ruiz D 2014. Feeding management in early life influences
microbial colonisation and fermentation in the rumen of newborn goat kids.
Animal Production Science 54, 1449–1454.
Alves AC, Alves NG, Ascari IJ, Junqueira FB, Coutinho AS, Lima RR, Pérez JRO, De
Paula SO, Furusho-Garcia IF and Abreu LR 2015. Colostrum composition of
Santa Inês sheep and passive transfer of immunity to lambs. Journal of Dairy
Science 98, 3706–3716.
Arguello A, Castro N, Capote J, Tyler JW and Holloway NM 2004. Effect of
colostrum administration practices on serum IgG in goat kids. Livestock Pro-
duction Science 90, 235–239.
Arguello A, Castro N, Zamorano MJ, Castroalonso A and Capote J 2004. Passive
transfer of immunity in kid goats fed refrigerated and frozen goat colostrum and
commercial sheep colostrum. Small Ruminant Research 54, 237–241.
Belanche A, Abecia L, Holtrop G, Guada JA, Castrillo C, de la Fuente G and
Balcells J 2011. Study of the effect of presence or absence of protozoa on rumen
fermentation and microbial protein contribution to the chyme. Journal of Animal
Science 89, 4163–4174.
Belanche A, Balcells J, de la Fuente G, Yanez-Ruiz DR, Fondevila M and Calleja L
2010. Description of development of rumen ecosystem by PCR assay in milk-fed,
weaned and finished lambs in an intensive fattening system. Journal of Animal
Physiology and Animal Nutrition 94, 648–658.
Belanche A, Newbold CJ, Lin W, Stevens PR and Kingston-Smith AH 2017. A
systems biology approach reveals differences in the dynamics of colonization
and degradation of grass vs. hay by rumen microbes with minor effects of
vitamin e supplementation. Frontiers in Microbiology 8, 1–18.
Belanche A, Weisbjerg MR, Allison GG, Newbold CJ and Moorby JM 2014.
Measurement of rumen dry matter and neutral detergent fiber debradability of
feeds by Fourier-transform infrared spectroscopy. Journal of Dairy Sciences 97,
2361–2375.
Bentounsi B, Meradi S and Cabaret J 2012. Towards finding effective indicators
(diarrhoea and anaemia scores and weight gains) for the implementation of
targeted selective treatment against the gastro-intestinal nematodes in lambs in
a steppic environment. Veterinary Parasitology 1, 275–279.
Blaxter KL, Sharman GAM and MacDonald AM 1957. Iron-deficiency anaemia
in calves. British Journal of Nutrition 11, 234–246.
Cardellino R and Benson M 2002. Lactation curves of commercial ewes
rearing lambs. Journal of Animal Science 80, 23–27.
Castro N, Capote J, Morales L, Quesada E, Briggs H and Argüello A 2007. Short
communication: addition of milk replacer to colostrum whey: effect on immu-
noglobulin G passive transfer in Majorera kids. Journal of Dairy Science 90,
2347–2349.
DeNise S, Robison J, Stott G and Armstrong D 1989. Effects of passive immunity on
subsequent production in dairy heifers 1. Journal of Dairy Science 72, 552–554.
Faber S, Faber N, McCauley T and Ax R 2005. Case study: effects of colostrum
ingestion on lactational performance 1. The Professional Animal Scientist 21,
420–425.
Hernández-Castellano LE, Almeida AM, Castro N and Arguello A 2014. The colostrum
proteome, ruminant nutrition and immunity: a review. Current Protein and Peptide
Science 15, 64–74.
Hernández-Castellano LE, Suárez-Trujillo A, Martell-Jaizme D, Cugno G, Argüello
A and Castro N 2015. The effect of colostrum period management on BW and
immune system in lambs: from birth to weaning. Animal 9, 672–1679.
Hodgson JC, Moon GM, Hay LA and Quirie M 1992. Effectiveness of substitute
colostrum in preventing disease in newborn lambs. Occasional Publication-BSAP
15, 163–165.
Huang K, Tu Y, Si B, Xu G, Guo J, Guo F, Yang C and Diao Q 2015. Effects of
protein sources for milk replacers on growth performance and serum biochem-
ical indexes of suckling calves. Animal Nutrition 1, 349–355.
Jasper J and Weary DM 2002. Effects of ad libitum milk intake on dairy calves.
Journal of Dairy Science 85, 3054–3058.
Effects of artificial rearing of lambs
9
Johansen J, Aastveit AH, Egelandsdal B, Kvaal K and Røe M 2006. Validation of
the EUROP system for lamb classification in Norway; repeatability and accuracy
of visual assessment and prediction of lamb carcass composition. Meat Science
74, 497–509.
Jones C, James R, Quigley J and McGilliard M 2004. Influence of pooled colostrum
or colostrum replacement on IgG and evaluation of animal plasma in milk replacer.
Journal of Dairy Science 87, 1806–1814.
Khan M, Weary D and Von Keyserlingk M 2011. Hay intake improves perfor-
mance and rumen development of calves fed higher quantities of milk. Journal
of Dairy Science 94, 3547–3553.
Morril KM 2011. Modifying current laboratory methods for rapid determination
of colostral IgG concentration and colostral IgG absorption in the neonate.
Thesis, Iowa State University, Ames, IA, USA.
Napolitano F, Cifuni G, Pacelli C, Riviezzi A and Girolami A 2002. Effect of
artificial rearing on lamb welfare and meat quality. Meat Science 60, 307–315.
Quigley JD, Wolfe TA and Elsasser TH 2006. Effects of additional milk replacer
feeding on calf health, growth, and selected blood metabolites in calves. Journal
of Dairy Science 89, 207–216.
Reichling JJ and Kaplan MM 1988. Clinical use of serum enzymes in liver disease.
Digestive Diseases and Sciences 33, 1601–1614.
Seymour W, Nocek J and Siciliano-Jones J 1995. Effects of a colostrum substitute
and of dietary brewer’s yeast on the health and performance of dairy calves.
Journal of Dairy Science 78, 412–420.
Sigurdardottir V, Fagerberg B and Hulthe J 2002. Circulating oxidized low‐density
lipoprotein (LDL) is associatedwith risk factors of the metabolic syndrome and LDL
size in clinically healthy 58‐year‐old men (AIR study). Journal of Internal Medicine
252, 440–447.
Soberon F, Raffrenato E, Everett RW and Van Amburgh ME 2012. Preweaning
milk replacer intake and effects on long-term productivity of dairy calves. Journal
of Dairy Science 95, 783–793.
Stelwagen K, Carpenter E, Haigh B, Hodgkinson A and Wheeler TT 2009.
Immune components of bovine colostrum and milk. Journal of Animal Science
87, 3–9.
Thonney M, Duhaime D, Moe P and Reid J 1979. Acid insoluble ash and per-
manganate lignin as indicators to determine digestibility of cattle rations.
Journal of Animal Science 49, 1112–1116.
Vatankhah M 2013. Relationship between immunoglobulin concentrations in
the ewe’s serum and colostrum, and lamb’s serum in Lori-Bakhtiari sheep. Ira-
nian Journal of Applied Animal Sciences 3, 539–544.
Vieira ADP, Von Keyserlingk M and Weary D 2012. Presence of an older weaned
companion influences feeding behavior and improves performance of dairy
calves before and after weaning from milk. Journal of Dairy Science 95,
3218–3224.
Yáñez-Ruiz DR, Abecia L and Newbold CJ 2015. Manipulating rumen micro-
biome and fermentation through interventions during early life: a review.
Frontiers in Microbiology 6, 1–12.
Belanche, Cooke, Jones, Worgan and Newbold
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