The impact of early life nutrition and housing on growth and reproduction in dairy cattle
The impact of early life nutrition and housing on growth and reproduction in dairy cattle
G. Curtis 0 1 2
C. McGregor Argo 0 2
D. Jones 0 2
D. Grove-White 0 2
☯ These authors contributed equally to this work. 0 2
0 Knowledge Transfer Partnership between Tesco Plc and University of Liverpool; Funders: Biotechnology and Biological Sciences Research Council, Innovate UK and Tesco Plc. Volac, For Farmers. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript
1 Department of Obesity and Endocrinology, Institute of Ageing and Chronic Disease, University of Liverpool , Leahurst Campus, Neston, Wirral , United Kingdom , 2 School of Veterinary Medicine, University of Surrey , Guilford , United Kingdom , 3 Institute of Veterinary Science, University of Liverpool , Leahurst Campus, Neston, Wirral , United Kingdom
2 Editor: Juan J Loor, University of Illinois , UNITED STATES
Contentious issues in calf rearing include milk feeding practices and single versus group housing. The current study was performed on a high producing 170 Holstein cow dairy farm, to investigate the impact of nutrition and housing on growth and reproduction. Heifer calves (n = 100) were allocated in birth order to one of two commonly used management strategies. All calves received 3±4 litres of dam specific colostrum within 6 hours of birth. Group A calves were group housed from birth and fed milk replacer (MR) ad libitum via a computerised machine utilising a single teat, with weaning commencing at 63 days of age. Group R calves were initially housed in individual pens and received 2.5 litres of MR twice daily via a bucket until 21 days of age when they were group housed and fed 3 litres of MR twice daily via a group trough with weaning commencing at 56 days. From 12 weeks of age onwards, calves in both dietary groups were subject to common nutritional and husbandry protocols. All breeding of heifers was via artificial insemination with no hormonal intervention. Calves were weighed, body condition scored and morphometric measures recorded weekly up till 12 weeks of age then monthly until conception. Pre-weaning growth rates (kg/day) were significantly higher in Group A calves compared to Group R (0.89, 95% CI 0.86±0.93 vs 0.57, 95% CI 0.54±0.6 kg/day P < 0.001) with the most marked differences observed during the first three weeks of life (0.72, 95% CI 0.61±0.82 vs 0.17, 95% CI 0.08±0.26 P < 0.001). Whilst Group A calves gained body condition score (BCS) throughout the pre-weaning phase, Group R calves lost BCS during the first 4 weeks of life. Data suggested that Group R calves supported skeletal growth during this period by catabolising body tissue. Group A calves had a greater risk of disease than group R calves during the pre-weaning phase (diarrhoea: odds ratio 3.86, 95% CI 1.67±8.9; pneumonia: odds ratio 5.80, 95% CI 2.33±14.44) although no calves died during this period. Whilst pneumonia had a significant impact on growth during the study duration (P = 0.008), this was not the case for diarrhoea. Whilst univariate analysis failed to show any statistically significant group differences (P > 0.050) in any of the mean values of measured reproductive parameters, multivariable Cox regression suggested that there was a weak trend (P = 0.072) for Group A animals to achieve first service earlier than their Group R counterparts (62.6 weeks versus 65.3 weeks). Irrespective of dietary group, the hazard for achievement of all measured reproductive parameters, apart
Competing interests: The authors have declared
that no competing interests exist. Whilst funding
from time to puberty, was 20±40% less for heifers borne from multiparous dams compared
to heifers from primiparous dams.
Dairy heifer rearing involves significant financial input accounting for approximately 20% of
total on farm costs [1±3]. Published data recommend that the optimal age at first calving
(AFC) is 24 months [4±6]. Below this age, heifers are considered unlikely to have sufficient
body size to support their genetic potential for lifetime milk production or to easily deliver a
healthy calf [
]. Conversely, rearing costs will be increased for animals with a greater AFC [
Achieving this optimal AFC depends largely on early life management and nutrition [7±10]
ensuring that animals are sufficiently well grown to receive their first insemination at 12±13
months. Whilst the optimal AFC is 24 months, there is debate as to the ideal weight and height
targets for first service in Holstein heifers, with a paucity of peer reviewed recommendations.
This is attributable in part to the increase in mature body size of the Holstein cow over the past
10±20 years, with animals becoming heavier and taller in stature [
]. Current targets
commonly used in the UK dairy industry are weight at 1st service of between 380±400 kg and a
minimum withers height of 125cm [
The provision of restricted amounts of milk or milk replacer (MR) for pre-weaned dairy
calves is commonplace on U.K. dairy farms [
], despite concerns that this practice may result
in calves receiving a sub-optimal supply of nutrients for growth and development [
practice is justified by anecdotal or short-term evidence , coupled with the requirement for
maximal rumen development at weaning [
]. Studies which evaluated rumen characteristics
of veal calves fed large volumes of milk reported minimal rumen development at weaning
]. Early transition from MR to cheaper solid feedstuffs has traditionally been considered
an important economic objective for dairy producers. However, restricting MR provision, in
order to encourage early transition to solid food, may deprive the calf of sufficient dietary
energy to support growth in early life . There is increasing evidence that growth rates and
MR intake prior to weaning are positively associated with increased productivity in later life
], suggesting that restricting MR provision in early life may constrain long term production
Post-weaning, heifers should be provided with a diet that allows growth at a sufficient rate
without fattening: a growth rate of between 0.8±0.9 kg per day is considered optimal [
terms of body composition and ensuring animals reach an adequate size and weight for service
(55% of mature bodyweight) to calve down at 24 months of age. Furthermore, age of onset of
puberty has been shown to be affected by plane of nutrition in a study where dairy heifers
(aged 4.5±9.5 months) fed an accelerated (1000g/day weight gain) feeding regime reached
puberty at least one month earlier than animals fed a standard diet (700g/day weight gain)
The present study compared data from calves subjected to one of two pre-weaning
management strategies: 1) restricted milk replacer (twice daily bucket feeding) with individual
penning for the first 21 days of life followed by group housing or 2) ad libitum access to milk
replacer with group housing from birth. The objectives were to describe growth and
reproductive parameters of heifers from birth until attainment of first pregnancy.
2 / 20
Materials and methods
This study was performed in compliance with Home Office (Animal Scientific Procedures
Act, 1986) legislation and was approved by the University of Liverpool Animal Welfare
Committee. The study was performed between April 2011 and April 2014 at the University of
Liverpool's Wood Park Dairy Farm, Neston, Wirral, U.K. (53ÊN). All healthy singleton heifer calves
born between January 2011 and November 2012 were recruited at birth into either an ad
libitum (Group A, n = 50) or restricted (Group R, n = 50) MR feeding cohort for the first 12 weeks
Calves were born into group calving accommodation with between 5 and 15 cows present.
If born between 08:00 and 18:00 hours, calves were removed from their mothers within 4
hours of birth and taken to calf accommodation; if born between 18:00 and 08:00 hours, calves
remained with their dam for up to 12 hours before being transferred to the calf house. Dam
parity was recorded and calves were assigned to one of the two MR feeding strategies on arrival
at the calf house in alternate groups of 6, such that each group or pen of calves had an age
range of no more than 14 days (Table 1).
Between 3 and 4 litres of calves own dam's colostrum (collected as soon as possible after
birth) was administered to each calf via an oesophageal feeder at the earliest opportunity after
birth. Freshly-collected, dam-specific colostrum meals i.e. ªtransition milkº were then fed
twice daily via individual buckets (2 litres per feed) for four days at which time MR feeding
was introduced to Group R calves. The composition of the MR was 96.97% DM, 7% ash, ME
21.570 MJ/kgDM, pH 5.96, 18% Oil, 23% Protein based on fat filled whey protein phospholipid
concentrate, with a small proportion of hydrolysed wheat gluten (10%), additives (1.3%), and
synthetic amino acids (Volac International Ltd, UK). The specific gravity of the initial
colostrum meal was assessed with a Brix refractometer (Animal Reproduction Systems, CA, U.S.
A.). For Group A calves, familiarisation and training for use of the automatic computerised
teat feeder (Vario feeder, Forster Technik, Germany) from which ad libitum MR was
dispensed began on entry to the calf house. Calves in this group were able to access MR from
birth in addition to the 4 day dam specific colostrum meals. Milk replacer powder was
thoroughly mixed with water (125g MR/litre, 37ÊC) immediately prior to feeding for both dietary
groups. The age and timing of weaning from MR differed between the 2 dietary groups.
Weaning commenced in Group R calves at 56 days and was completed by day 63, whilst in Group A
calves it commenced at 63 days and was completed by day 84 (Table 1).
Milk replacer intakes for individual calves in Group A were recorded daily from the
computerised feeder (± 0.1litres). Concentrate feed (Primestart coarse mix, 86.2% DM, 18% crude
protein, 8% crude fibre, 9.5% ash, 3.5% oil, ME 14.459 MJ/kgDM, BOCM Pauls Ltd U.K.) was
supplied daily on an ad libitum basis up to 2.5 kg per head from birth. Individual intakes could
Stepwise restriction of daily MR Group housed from
allowance over 21 days (0.7L birth
restriction/day). Completed by day (n 6)
50% reduction of MR allowance
over 7 days prior to stopping milk
feeding. Completed by day 63
until 21 days then
Ad libitum access to grass hay
and up to 2.5kg concentrate
feed (coarse mix) daily
Ad libitum access to grass hay
and up to 2.5kg concentrate
feed (coarse mix) daily
Ad libitum access from birth until
5L daily from day 4 until day 21, Individual bucket to
then 6L daily until day 56 (provided day 21, thereafter
as 2 equal meals, 09:00 & 17:00hrs) group trough fed
Milk Replacer feeding
Automatic teat feeder
not be measured for group penned calves; however mean group intakes were recorded for a
subset of calves: 2 pens of Group A calves (n = 9) and 2 pens of Group R calves (n = 7) between
April and September 2012.
Calves in Group R were housed individually in metal gated pens (1m x 2m) over raised slatted
flooring bedded with wheat straw from birth until 21 days of age. At 21 days of age, Group R
calves were moved to deep wheat straw-bedded group pens (5m x 6m, n 6, age range 14
days). Calves in Group A were grouped by age (range 14 days, n 6) and were directly
introduced to identical group pens on entry into the calf house. All calves had ad libitum access
to forage (grass hay 85% DM, 8.5% crude protein, 8% crude fibre, 7.4% ash, ME 8.4 MJ/
kgDM), fresh water and coarse mix concentrate feed, up to a maximum of 2.5 kg per head
From 12 weeks of age onwards, calves in both dietary groups were subject to common
nutritional and husbandry protocols. Irrespective of pre-weaning dietary group, at 4 months
of age all calves were transferred to follow-on accommodation (indoor straw yards 18m x 6m,
approximately n = 12 per group). Calves in the straw yards were fed along the front (18m) of
each yard ensuring adequate bunk space. However from 9 months of age until conception was
confirmed, heifers were housed in free-stall accommodation with 31 free-stalls (1.93m x
1.14m), total available bunk space/feed barrier was 35.3 metres.
From 3 to 5 months of age, the diet consisted of a maximum of 2.5 kg of concentrate feed
per head (86.20% DM, 18.00% crude protein, 4.00% oil, 9.50% ash, 12.50% crude fibre, ME
14.551 MJ/kg Super Rearer 18 nuts, BOCM Pauls, U.K.). Grass hay and fresh water were freely
available at all times.
In accordance with standard farm practice, nutrition from 5 months onwards was highly
variable consisting largely of refusals from the total mixed rations fed to the lactating, far off
dry and transition dry cows. However, depending on the quantity of refusals available each
day, additional maize silage or grass silage was added to the diet. Whilst no precise rationing
was performed, approximately 12 kg on a fresh weight basis (dry matter ~ 50%) was supplied
per head daily. It was not possible to estimate individual feed intakes since animals ranged in
body weight from approximately 200±400 kg.
A target body weight of 380kg and withers height of 125cm were set by the farm
management as minimum standards which animals were to achieve before first service. All heifers
were served via artificial insemination of selected semen following once per day visual heat
detection (no synchronisation or other heat detection methods were employed).
The body weight of each calf was recorded within 12 hours of birth (Ritchey Ltd, North
Yorkshire, U.K., ± 0.5kg). During the following 36 hours, measures of the height at the highest
point of the withers and loin (±0.1cm, wooden measuring stick, I&D Smallwood, U.K.),
circumference of the heart girth (immediately caudal to the elbow) and belly girth (widest
part of the belly) (± 1cm), crown to rump length (CRL) (± 1cm) and hock-fetlock length
(HFL) (± 1cm, plasticised tape measure) were recorded and body condition score (BCS) was
recorded in accordance with the system presented by Edmonson et al [
] (1 = emaciated
5 = obese). All body weight, morphometric and BCS measures were repeated weekly to 12
weeks of age, then every 4 weeks until attainment of pregnancy.
4 / 20
Heparinised blood samples (7ml) were collected from all calves within 48 hours of birth and
weekly from 28 weeks of age until puberty was confirmed. Samples were stored on ice prior to
harvesting plasma, which was stored atÐ20ÊC for up to 3 months pending analyses. Adequacy
of passive transfer of Immunoglobulin (Ig) was assessed by measuring calf plasma total protein
(PTP) concentrations at 48 hours of age using a refractometer (Clinical refractometer, Hayes,
U.K.) taking a cut-off of 56 g/l as indicative of failure of passive transfer (FPT) of Ig [
28 weeks of age onwards `pregnane metabolites' were measured in triplicate as a proxy for
progesterone concentrations using a previously validated ELISA test . The minimum
detectable concentration was 0.08 ng/ml, intra and inter-assay variation were 8.3 and 14%
respectively. Animals were classified as pubertal when plasma pregnane metabolite
concentrations of 2.00 ng/ml were recorded for 2 consecutive weeks.
All pre-weaned calves were examined twice daily for signs of illness by the researchers.
Diarrhoea was diagnosed on the basis of a faecal score > 2 [
]. Pneumonia was diagnosed
on the basis of the presence of one or more of the following signs, accompanied by a rectal
temperature > 39.4Ê C: nasal discharge, ocular discharge, coughing, increased respiratory rate
]. Cases of diarrhoea received 2L twice daily of oral rehydration solution (Effydral: Zoetis)
by bucket and teat or oesophageal feeder if no suck reflex was present. Rehydration therapy
was continued for at least 3 days. Diarrhoeic calves were not removed from their
accommodation and continued being offered MR at the same rate as their healthy counterparts, although
they did not always consume their full allocation. Cases of pneumonia were treated once with
sub-cutaneous injections of tulathromycin (Draxin, Zoetis) at a dose rate of 2.5 mg / kg and
Meloxicam (Metacam, Boehringer Ingleheim) at a dose rate of 0.5 mg / kg.
All data were initially entered into an Excel spreadsheet (Microsoft Corp, USA) and exported
to STATA 13 (StataCorp, Texas, USA) for analysis.
Heifer calves at birth. Simple univariable analyses using linear regression and Students t
tests were carried out initially to investigate possible associations between the measured
variables. Outcome variables of interest were, birth weight, colostrum quality and plasma total
protein concentration at 48 hours.
Heifer calves from birth until pregnancy. Daily changes of body weight and other mor
phometric measures from birth to 108 weeks of age were calculated for discrete time periods
throughout the study. Student's t tests were used to compare the mean measurements at
different time points between calves in Group A and Group R.
Random effects linear regression models were then fitted using backward stepwise selection
for all morphometric measures from birth until pregnancy. All remaining covariates were
included in the initial model. A backwards, stepwise model-building strategy [
employed whereby a full model was built and then each variable removed in turn, a likelihood
ratio test performed and the resultant P value noted. The variable with the highest P value was
then omitted and the process repeated. This process was repeated until only variables with
P<0.2 remained in the model. The omitted variables were then added back in turn, starting
with the lowest P value, a likelihood ratio test performed after each addition, and the variable
retained if P<0.2. This process was continued until no further variables could be added, to
produce the final model. Calf identity was included as a random effect to account for clustering
in all models.
5 / 20
The following explanatory variables were initially offered to the full body weight model:
pre-weaning dietary group (ad libitum or restricted MR), age in weeks, an age diet interaction
term, dam parity (primiparous v multiparous), plasma TP and occurrence of diarrhoea and/or
pneumonia during the first 12 weeks. Other interaction terms were offered if considered
biologically feasible and retained if their inclusion improved model fit.
The final explanatory variables for the body weight model were forced into models for the
other morphometric measures (withers and loin height, heart and belly girth, CRL, HFL and
BCS). Predicted marginal means were estimated from multivariable models and plotted
graphically where appropriate.
Survival analysis was employed to assess the impact of pre-weaning diet on the age at
puberty onset, first service and age at conception. Since the age at first service and age at
conception are in part affected by management practices such as heat detection, survival analysis
was used to investigate the age at which animals reached pre-determined height (125 cm
withers height) and weight (380 kg) targets after which they were eligible for insemination. Kaplan
Meier survival curves were plotted for Group A and R separately. Multivariable Cox
proportional hazard models were fitted for all outcomes to assess the hazard ratio for potential
explanatory variables. Variable selection for final models was by backwards stepwise removal
taking a P value < 0.200 (log likelihood test) for retention of a variable. The following
explanatory variables were offered to all models: Birth weight, dam parity (primiparous v
multiparous), plasma TP and occurrence of diarrhoea and/or pneumonia during the first 12 weeks.
Dietary group was forced into all models. Proportional hazard assumptions for Cox's
regression were checked using Schoenfeld residuals and were accepted if P > 0.050.
The mean birth weight of heifer calves (n = 100) was 41.78 kg (95% CI 40.66±42.90). Birth
weight was positively associated with dam parity (primiparous: n = 43, mean 38.4 kg, 95% CI
37.1±39.8; multiparous: n = 57, mean 44.3 kg, 95% CI 42.9±45.7, P < 0.001).
Time from birth to first colostrum ingestion was similar for calves in both dietary groups
(Group R: 3.29 hours, range 0.50±11 hours, Group A: 3.27 hours, range 0.25±9.50, P = 0.974).
The specific gravity of peri-partum colostrum was comparable between dietary groups (23.5%,
95% CI 22.5±24.5) and was not influenced by dam parity. Calves born to primiparous dams
consumed less colostrum in their first meal (primiparous: 2.96 L, 95% CI 2.77±3.15 L;
multiparous: 3.26 L, 95% CI 3.11±3.40 L, P = 0.006). However, when data were normalised for calf
body weight, initial colostrum intakes were similar for all calves (primiparous dams: 0.077
litres/kg BM; multiparous dams: 0.075 litres/kg BM, P = 0.337). Mean PTP (sd) concentration
was 68.9 g/L (0.81) with no dietary group (P = 0.76) or dam parity associated (P = 0.91)
differences. Taking a PTP cut-off of 56.0 g/L as indicative of adequate passive transfer, 5 (5.0%)
calves were classified as having FPT. There were no associations between occurrence of FPT
and calf group (P = 1.000) or dam parity (P = 0.650).
All calves consumed all transitional milk offered during the first 4 days of life. Group A
calves consumed considerably more MR (mean 914 litres, 95% CI 873±947) than Group R
animals (315 litres) over the entire pre-weaning period (Fig 1a). Voluntary daily MR intakes in
Group A calves increased rapidly to reach 7.6 L/day (95% CI 6.5±8.7) by day 5 and increased
linearly to reach 13.3 L (95% CI 12.4±14.2) by day 26 before the rate of increase slowed to peak
at 15.3 litres per day (95% CI 14.2±16.4) near the onset of gradual weaning on day 64. The
maximum daily MR intake recorded for any calf was 25.5 litres. In Group A, MR intakes
declined at a pre-programmed rate of 0.7 L daily (Fig 1a) over a 21 day period, whilst Group R
calves had a 50% reduction in MR supply for one week prior to weaning at 63 days of age.
6 / 20
Fig 1. Milk replacer and calf concentrate consumption for Group A and Group R calves. a) Mean (95%CI) daily
MR consumption for heifer calves in Group A (blue), and MR allowance for Group R animals (red) and b) mean
weekly concentrate intakes (kg) for a subset of calves in Group A (blue, n = 9) and Group R (red, n = 7) from birth
until 12 weeks of age.
When data were corrected for body weight and ME, the maximum mean energy provision
from MR at 3 weeks of age for calves in Group A was 0.54 MJ/kg body weight/day compared
to 0.34 MJ/ kg body weight/day in Group R.
Concentrate feed intakes were negligible (< 50g) for calves in both dietary groups from
birth to 3 weeks. After this time, voluntary intakes of concentrate feed for Group R calves
gradually increased to approximately 1.0 kg daily by 7 weeks of age. Conversely, concentrate
intakes were relatively less for Group A calves and had only attained < 0.5 kg/head daily by
the onset of weaning at week 8 (Fig 1b). However, mean intakes were similar in both groups of
calves at 12 weeks of age i.e at completion of weaning.
There was a high incidence of disease in both groups of calves. In total, 80 (80%) calves
suffered from at least one incident of disease during the period from birth to 12 weeks. Group A
calves had a greater risk of disease than group R calves (diarrhoea: OR 3.86, 95% CI 1.67 to 8.9;
pneumonia: OR 5.80, 95% CI 2.33 to 14.44) [
]. However, no animals died during the
preweaning period. Of the 100 heifer calves which entered the study, 98 animals remained within
the cohort at the end of the study period (68.9 weeks, 95% CI 66.6±71.3). Two animals, one
from each dietary group, died post-weaning prior to reaching eligibility for first service
(accidental death), these animals were excluded from further analyses.
Overall, pre-weaning growth rates (kg/day) (Table 2) were significantly higher in Group A
calves (0.89 kg/day, 95% CI 0.86±0.93: measured over 12 weeks) compared to Group R (0.57
7 / 20
kg/day, 95% CI 0.54±0.6: measured over 9 weeks) such that at 12 weeks of age, when weaning
was complete in both groups, there was a significant difference (P <0.0001) in mean body
weight between the 2 groups (Group R: 103.88 kg, 95% CI 100.55±107.21, Group A: 116.80 kg
95%CI 113.45±120.15). However, mean daily growth rates showed temporal variation between
the 2 groups during the pre-weaning period. The most marked differences were observed
during the first three weeks of life (Group A 0.72 kg/day, 95% CI 0.61±0.82, Group R 0.17 kg/day,
95% CI 0.08±0.26, P < 0.001). Conversely, between 9 and 12 weeks of age when Group A were
undergoing gradual weaning, growth rates were greater in Group R (Group R: 1.04 kg/day,
95% CI 0.97±1.11, Group A: 0.84 kg/day, 95% CI 0.74±0.93, P < 0.001).
Multivariable modelling (Tables 3 and 4, Fig 2) suggested the following explanatory
variables were associated with body weight change over the first 12 weeks of life: pre-weaning
dietary group (ad libitum or restricted MR) with an interaction with age in weeks, dam parity,
plasma TP, the presence of diarrhoea in the first 12 weeks and presence of pneumonia in the
first 12 weeks. A plot of the model-derived predicted marginal means for body weight (Fig 2a)
indicated that the impact of dietary group was most marked during the first 3 weeks of life
when increase in body weight was minimal for Group R animals. Beyond this time, rate of
change in body weight were broadly similar between pre-weaning dietary groups. Early
constraints on growth therefore resulted in a right shift of the growth curve for Group R.
There were marked dietary group differences in BCS change during the first four weeks of
life (Fig 2a), with Group A calves gaining BCS at a rate 0.0053 (sd 0.0190) units per day
95% Confidence Intervals
8 / 20
Fig 2. Predicted marginal means (95% CI) for morphometric measures. a) body weight (kg), b) BCS c) belly girth
(cm), and d) heart girth (cm) for calves in Group A (blue) and R (red) from birth until 12 weeks of age. Full models are
presented in S1 supporting information.
compared to Group R calves who lost BCS at a rate 0.0149 (sd 0.0207) units per day (P <0.001)
during this period. From 3 weeks onwards, BCS increased for both dietary groups.
With the exception of belly girth, all other morphometric measures (withers and loin
height, heart girth, CRL and HFL) had broadly similar dietary group differences in rates of
change over time during the first 12 weeks of life, although group differences in predicted
withers height and other skeletal measures were only apparent after 3 weeks of age (Fig 3).
Mean average daily weight gain from 12 to 60 weeks (Group R, n = 49; Group A, n = 49)
was 0.837 kg daily (95% CI, 0.815±0.860) with no dietary group differences (P = 0.771). For all
other morphometric measures including body weight, Group A calves had higher recorded
values than Group R calves from 12±60 weeks, but these differences were not statistically
significant at every time point. There was a trend for pre-weaning diet-associated differences to
decrease over time, such that by the end of the study there were no differences attributed to
pre-weaning dietary group in any of the morphometric measures with the exception of body
weight. Although mean BCS remained higher in Group A than Group R animals throughout
the study period, there was a trend for BCS to increase in both dietary groups from
approximately 36 weeks of age onwards (S2 supporting information).
The mean age at which animals reached 380 kg (pre-defined as the minimum weight for
insemination) was 57.4 (95% CI 55.4±59.4) weeks for Group A calves and 60.4 (95% CI 58.2±
62.7) weeks for Group R calves (P = 0.043) (Fig 4). However, the mean age at which animals
reached 125 cm height at the withers (pre-defined as the minimum withers height for
insemination) was 46.5 (95% CI 45.1±47.8) weeks with no dietary group difference (P = 0.230) (Fig
4). The mean age at the onset of puberty was 41.6 (95% CI 39.2±44.1) weeks for Group A calves
and 43.8 (95% CI 41.6±46.0) weeks for Group R calves (P = 0.167) and was not affected by
disease (diarrhoea or pneumonia) during the pre-weaning period (P = 0.469). The mean age at
first service was 62.6 weeks (95% CI 61.4±63.8) for Group A and 65.3 (95% CI 62.6±68.0)
weeks for Group R (P = 0.068) and the age at conception was 67.7 (95% CI 64.5±70.8) weeks
9 / 20
Fig 3. Predicted marginal means (95% CI) for skeletal morphometric measures. a) withers height (cm), b) loin
height (cm) c) crown-rump length (cm), and d) hock-fetlock length (cm) for calves in Group A (blue) and R (red)
from birth until 12 weeks of age. Full models are presented in S1 supporting information.
for Group A and 70.1 (95% CI 66.6±73.6) weeks for Group R (P = 0.305) (Fig 5). Based on a
285 day gestation period, predicted calving ages for heifers from Group A was 25.3 months
(95% CI 24.6±26.0), and Group R animals was 25.8 months (95% CI 25.0±26.7). Neither age at
first service or conception were affected by disease during the pre-weaning period. Forty-nine
animals in Group A and 46 animals in Group R conceived.
The mean number of services required to achieve conception was similar between dietary
groups (2.02; 95% CI 1.66±2.38, P = 0.998). Fifty seven percent of group A and 51% of Group
R animals became pregnant after the first service (P = 0.550). There were no dietary group
differences in body weight, withers height or BCS at the onset of puberty, first service and
conception (P > 0.050) (Table 5).
Multivariable Cox regression (Table 6) suggested that in the case of time to achievement of
380 kg target weight there was a significant association with dietary group (Hazard ratio 1.7
95% CI 1.08±2.67, P = 0.021) but this was not the case with withers height (P = 0.330). In the
case of time to achievement of puberty there were statistically weak associations with dietary
Fig 4. Kaplan- Meier survival curves for morphometric measures relating to first service parameters. Proportion
of heifers not yet reaching a) 380 kg and b) 125cm withers height in Group A (blue line) and Group R (red line).
10 / 20
Fig 5. Kaplan- Meier survival curves for measured KPI's. Proportion of heifers not yet reaching a) puberty, b) first
service and c) conception in Group A (blue line) and Group R (red line).
group (Hazard ratio 1.14, 95% CI 0.88±2.26, P = 0.157) and occurrence of pneumonia during
the pre-weaning period (Hazard ratio 0.70 95% CI 0.43±1.14, P = 0.147). However, time to
first service was associated with dietary group (Hazard ratio 1.47, 95% CI 0.97±2.24,
P = 0.072), birth weight (Hazard ratio 1.08 95% CI 1.03±1.14 P = 0.001), plasma total protein
concentration measured at 48 hours of age (Hazard ratio 1.43 95% CI 1.09±1.87 P = 0.009).
Time to conception was weakly associated with dietary group (Hazard ratio 1.39, 95% CI 0.93±
2.1, P = 0.109) and significantly associated with birth weight (Hazard ratio 1.09, 95% CI 1.04±
11 / 20
1.15, P < 0.001) (Table 6). In the case of all outcomes apart from time to puberty, there was a
significant and consistent negative impact of having a multiparous dam with hazard ratios
ranging from 0.44±0.67.
This study was designed to investigate the impact of ad libitum milk replacer (MR) feeding
and group housing from birth (n 6/group) on the growth and performance of Holstein
dairy calves under commercial conditions. For comparison, a control group of calves fed
restricted amounts of MR housed from birth until 3 weeks and thereafter grouped (n 6) and
fed restricted MR according to current U.K. practices was also studied. The decision to base
the intervention on ad libitum MR feeding rather than increased volumes was made on the
basis that it was important to understand the growth potential of Holstein calves with access to
unlimited MR. It was not the intention of the study to provide a novel ªoff the shelfº feeding
strategy for adoption by the farming industry.
The present study provides valuable information regarding impact of feeding and housing
systems on growth and future reproductive performance, despite there being implicit study
limitations which must be acknowledged. Firstly, calves were not randomly allocated to
intervention arm. This was dictated by the farm size and calving rate, coupled with the requirement
to produce groups of up to six calves with no more than 14 days' age difference between them.
Secondly, due to the standard farm policy for housing calves individually during the first 3
weeks of life, there is implicit confounding of feeding system by housing and vice versa thus
not allowing differences to be attributed absolutely to either feeding system or housing system.
Another shortcoming of the study is the relatively small sample size, dictated by the study farm
12 / 20
size. This reduces the statistical power and ability to detect differences at the P < 0.05 level. In
fact, post-hoc power calculations suggest that whilst the sample size (n = 100) is adequate
(> 80% power) to detect differences in body weight and growth rates during the study period,
it is insufficient to detect significant differences in achieving specific reproductive or growth
targets; having a power of 53% to detect a hazard ratio of 1.5, with only a 17% power to detect
a 10% difference in e.g. conception rates. For this reason we present actual P values allowing
the reader to judge the validity of conclusions reached.
There is an increasing body of evidence in support of increased milk or MR feeding of dairy
calves during early life with the majority reporting benefits in terms of increased daily live
weight gain (DLWG) during the pre-weaning period [14,29±31]. Current targets for DLWG
for the entire pre-weaning phase are 0.8±0.9 kg/day [
]. In the current study, all calves were
weighed and measured weekly affording the opportunity to investigate in depth morphometric
changes during the pre-weaning phase. Overall, mean pre-weaning growth rates were more
than 1.5 times greater in Group A calves (0.89 kg/day, 95% CI 0.86±0.93: measured over 12
weeks) compared to Group R (0.57 kg/day, 95% CI 0.54±6.00: measured over 9 weeks), such
that at 12 weeks of age, when weaning was complete for all calves, Group A calves were 13 kg
(12%) heavier on average compared to their Group R counterparts. The most dramatic
differences in growth rates were observed during the first 3 weeks of life when DLWG was 0.72 kg
(95% CI 0.61±0.82) per day in the ad libitum MR fed, group housed calves compared to 0.17
kg (95% CI 0.08±0.26) per day in the restricted MR fed, individually penned calves, a four-fold
difference, during this period. Similar findings have been reported previously [
minimal growth in the restricted MR fed calves was accompanied by a considerable loss in BCS of
nearly 0.5 BCS points over the first 4 weeks, comparable to that of an adult lactating cow
during the first 8 to 10 weeks post-partum. In contrast, a consistent increase in BCS from birth was
recorded in the ad libitum MR fed animals. In addition to the differences in body weight gain,
other morphometric measures of growth differed between dietary groups during the
preweaning period. In the case of skeletal measures namely withers and loin height, heart girth,
crown to rump length and hock-fetlock length, there was no dietary group difference in the
first 3 weeks of life, in contrast to body weight. However from 4±6 weeks of age ad libitum fed
calves demonstrated significantly increased skeletal growth compared to their restricted fed
counterparts. This observation, together with the BCS changes observed in early life in the
restricted fed calves, would suggest that skeletal growth is prioritised at the expense of soft
tissue growth during the first 3 weeks of life.
After three weeks of age solid food intake increased in the restricted MR fed calves
coincident with an increased growth rate comparable to that of the ad libitum MR fed calves.
However their body weights remained lower with no compensatory growth observed throughout
the pre-weaning period. The ability for `catch-up' or `compensatory' growth following a period
of limited nutrient availability is well documented for various mammalian species [33,34].
Abdalla et al [
] demonstrated that compensatory growth occurred in Holstein calves, aged at
least 8 weeks at recruitment, that underwent a period of restriction of protein and energy
intake sufficient to reduce daily live weight gain by 50% for between 112 and 154 days. In the
present study, nutritional restriction was applied to the restricted fed calves from birth,
supporting the hypothesis that compensatory growth cannot occur if dietary restriction is
imposed during very early life [
As previously mentioned, the effect of dietary intake during the first 3 weeks of life is
confounded by housing as calves fed restricted volumes of MR were single penned in contrast to
the ad libitum fed calves which were group housed from birth. It has been clearly shown that
growth, solid feed intake and social development of calves are all improved by group housing
13 / 20
calves compared to individual penning [
]. Thus it could be concluded that group housing in
combination with unrestricted MR feeding affords both welfare and financial benefit.
Rates of both diarrhoea and pneumonia were significantly higher in the Group A compared
to Group R calves. In the case of diarrhoea, all cases occurred during the first 3 weeks of life
when Group R calves were individually penned compared to their Group A counterparts who
were group penned. Diarrhoeic calves were not removed from group pens, so it is likely that
the higher rates observed were a reflection, in part, of a greater pathogen transmission
potential. However it is recognised that feeding increased amounts of milk or MR will result in
greater volumes of looser faeces. Thus it is also possible that since diagnosis of diarrhoea was
solely on the basis of a faecal score > 2 that some calves in Group A were mis-classified as
suffering from diarrhoea when in fact they were not, further adding to the number of cases
observed in this group. In fact, there is little evidence regarding any deleterious impact per se
of a high plane of nutrition on risk of diarrhoea [
], whilst there is evidence that increased
plane of nutrition can mitigate the severity of experimentally induced diarrhoea associated
with Cryptosporidium parvum infection . However the increased risks of disease
transmission in group housed animals are well recognised [
]. In the case of pneumonia, all episodes
were observed in calves over 3 weeks of age. All calves were housed in a common air space
which suffered from high humidity and wide temperature fluctuations, coupled with poor
drainage; all of which are well recognised risks for pneumonia. We hypothesise that the
increased pneumonia risk in the ad libitum milk fed calves was likely associated primarily with
the sharing of a common teat facilitating transmission of respiratory viruses via saliva and
nasal secretions [
]. A further factor could be the increased volumes of urine produced
associated with increased fluid intakes leading to increased bed wetness. Disease risk in the present
study is the topic of a previous publication to which the reader is referred for further details
]. The published work on the impact of group housing on disease risk is contradictory with
some studies [41±43] showing increased disease risk associated with group housing, whilst
others have reported improved health in group housed calves [
]. Increasing group size
 and continual introduction of calves into the group versus an all inÐall out stable
grouping system [
] are both associated with increased disease risk. In the present study, group size
was equal to or less than 6 with no more than 14 days age difference and all groups were stable,
thus mitigating these latter risks.
Restricted feeding of milk or MR has traditionally been justified on the basis of promoting
early rumen development associated with consumption of concentrate feed at an early age
]. New born calves are mono-gastric with undeveloped rumens thus are incapable of
utilising solid foods until the establishment of a rumen microflora and rumen villous growth has
occurred. Concentrate intakes during the first 3 weeks of life were minimal in calves of both
dietary groups (Fig 1) corresponding to this so-called pre-ruminant phase [
], during which
the calf is dependent on MR for almost all its nutritional requirements. This inability of the
young calf (< 3 weeks old) to utilise solid feeds will accentuate the energy deficits associated
with restricted MR feeding and contribute to the loss in BCS observed in these calves. This
would imply that under-feeding of MR at this stage is not compatible with the concept of a
ªsuitable dietº as stipulated by their five needs [
A concern raised with regards to feeding increased volumes of milk or MR is that calves
will have poor rumen development at the time of weaning due to insufficient consumption of
concentrate feed [51±53]. In the present study, a three week step-down weaning strategy was
adopted for the ad libitum MR fed calves in order to minimise this risk. Concentrate intakes in
ad libitum MR fed animals was relatively low prior to the onset of weaning, but increased
rapidly to that of restricted MR fed calves by the end of the pre-weaned period with no apparent
adverse effects on health.
14 / 20
Plasma total protein concentration at 48 hours of age had a significant positive impact on
growth up to the time of conception, although this was not apparent during the first 12 weeks
of life. The impact of PTP on long term growth was such that it remained an explanatory
variable in the Cox regression model for time to first service. These findings suggest that colostrum
intake impacts not only on the immune status of the calf via transfer of immunoglobulins, but
has other, at present poorly described, roles affecting future growth. Similar findings have
been shown by other groups and it is likely that these findings illustrate a further mechanism
by which early life colostrum intake has a long term impact on animal lifetime production
Whilst the intervention was applied during the pre-weaning period, data collection
continued until conception, as confirmed by ultrasound examination. In terms of body weight, there
was no clear evidence of any catch-up growth in the restricted MR fed group as demonstrated
by the earlier age at which Group A animals achieved a target weight of 380 kg. Interestingly,
differences in other morphometric measures between the 2 dietary groups disappeared over
time such that there were no group differences in age of achievement of the 125 cm withers
height target. This suggests a degree of catch up growth occured in respect of skeletal measures.
It is unclear why catch-up growth occurred with respect to morphometric measures (which
included measures of skeletal growth) but not for body weight.
While the feeding regime for study animals during the pre-weaning and early post-weaning
phases were highly controlled, this was not the case from 5 months of age onwards when all
heifers were fed `left-over' Total Mixed Ration (TMR) from the adult lactating and dry cow
diets which will have likely varied considerably in composition especially with respect to
dietary starch levels. Due to this variablility it is not possible to accurately state what the likely
energy density or protein content of the diet was: however the lactating cow diet fed had an
approximate energy density of 12 MJ ME/ kg DM which is considerably higher than required
for growing dairy heifers at this stage of life, which is in the region of 9.5±10.5 MJ/kg DM [
This may have contributed to the increase in BCS observed in both groups from 4 months of
One major Key Performance Indicator (KPI) associated with dairy heifer rearing is age at
first calving (AFC). Most published studies suggest an optimal AFC of 23 to 24 months [
although a recent study based on over 400,000 animals in the UK suggest that an AFC of 22±
23 months may be associated with increased lifetime productivity [
]. In the present study,
predicted AFC was sub-optimal in both groups of animals at 25.3 months for Group A
compared to 25.9 months for Group R. However irrespective of dietary group mean weight at first
service was 414 kg i.e. 34 kg over the 380 kg target. Assuming an average daily weight gain of
0.85 kg per dayÐthis would imply that heifers were first served on average 40 days after
reaching their target weight. This would suggest that improved heat detection would dramatically
reduce AFC by an average of 40 days. Prior to commencement of the current study, a
consensus was reached that there were 2 targets to be met prior to first service, namely attainment of
a body weight of 380 kg and a withers height of 125cm. These targets were intended to be
employed on the farm for the duration of the study. However, farm staff failed to utilise weight
and height data collected by the researcher for decision making regarding breeding. This likely
had a deleterious impact on the achievement of optimal age at conception. When
retrospectively evaluating final morphometric measures from study heifers it was interesting to find that
only 40 out of the 100 heifers reached the 2 targets simultaneously. Generally, the height target
was reached earlier than the body weight measure; survival curves presented (Fig 4) suggest
there was up to 4 weeks difference between achievement of the 2 targets. This raises the
question: which is the best KPI measure for timing of first serviceÐbody weight or withers height?
15 / 20
There were statistically non-significant trends for ad libitum MR fed animals to reach all
reproductive KPIs (age at puberty, age at first service and age at conception) earlier than
restricted MR fed animals. The ad libitum MR fed heifers achieved targets approximately 2±3
weeks earlier than their restricted MR fed counterparts, suggesting significant financial
benefits could accrue from the increased feeding regime. Although not statistically significant, ad
libitum MR fed heifers had a higher conception rate (57%) than restricted MR fed heifers
(51%). This lack of statistical signifcance may be a reflection of the relatively small sample size
(n = 50 per group). Although the ad libitum MR fed heifers reached the pre-defined target
weight of 380kg earlier than their restricted fed counterparts, the target AFC of 24 months was
not met by either group as discussed above due to delay in serving heifers on achievement of
their target weight. It is imperative that if the benefits of improved early life growth are to be
realised, farm management practices must be optimised to ensure heifers are served as early as
possible after becoming eligible. The target should be that all heifers are served within 21 days
of achieving target weight or height. This requires both regular monitoring of height and/or
body weight of heifers and active heat detection. A recent trend has been the development of
hormonal interventions to allow fixed time insemination thereby eliminating the need for
oestrus detection [
Multivariable cox regression was performed to investigate factors associated with time to
achievement of the pre-determined morphometric measures and reproductive parameters.
Whilst caution must be taken in interpretation of these models due to the small sample size, it
is interesting to note that for all outcomes, except ªtime to pubertyº there was a negative
association (hazard ratio less than 1) with the binary variable ªparityº having adjusted for
birthweight. This suggested that the hazard for heifers born from multiparous dams was 20±40%
less than for those from primiparous dams for achievement of these targets. This finding is in
contrast to the impact of dam parity on weight over the study period as shown by the positive
coefficient (7.69 Table 3). However this is likely to be a proxy for the heavier birthweight of
calves born from multiparous dams compared to those from primiparous dams (44.3 vs 38.4
kg in the present study). This observation is in agreement with those of Swali & Wathes [
who also found time to conception was significantly less in heifers born to primiparous dams.
Two hypotheses can be generated regarding this finding; firstly it is associated with in utero
nutrition either via a direct effect on ovarian development [
] or indirectly via unknown
epigenetic mechanisms. Alternatively it could be associated with differences between colostrum
derived from primiparous compared to multiparous dams. A recent study [
] highlighted the
reduced microbial richness in multiparous dam colostrum compared to primiparous
colostrum, suggesting this may be a consequence of routine intra-mammary antimicrobial
treatment of lactating cows at the end of lactation (dry cow therapy). Furthermore it is recognised
that the colostrum microbiome will contribute to the calf intestinal microbiome, the
composition of which can impact on gut health and early life growth [
In the current study, ad libitum MR fed heifers reached conception and therefore predicted
first calving 2.3 weeks earlier than restricted MR fed heifers. Based on current estimates of the
financial losses associated with a delayed AFC (£2.87/day [
]), this equates to an accrued
financial benefit of £46.21 per ad libitum fed heifer. However the approximate additional cost
of ad libitum feeding for 12 weeks compared to restricted MR feeding and weaning at 9 weeks
was £84 (£187 versus £103), suggesting that in this study, at least, the financial benefits of a
reduced AFC did not justify the increased rearing costs associated with ad libitum MR feeding
and weaning at 12 weeks of age. Thus, this study demonstrated clear benefits of ad libitum
feeding on growth and by extension calf welfare during the first 3 weeks of life but failed to
demonstrate a clear financial benefit. However since the study ended when animals achieved
pregnancy, no data regarding future health or production is available. There is an increasing
16 / 20
body of evidence reporting reported the benefits of increased liquid milk feeding for at least
the first 5 weeks of life on lifetime performance [
With this in mind, future studies should investigate the impact of shorter ad libitum MR
feeding periods. The present data would suggest that if, for example, ad libitum MR was fed for
3±4 weeks of life with a subsequent gradual weaning period of 3 weeks, then growth and
welfare benefits would still be realised albeit with a reduced financial investment. Whatever the
length of the ad libitum MR fed period, the associated costs should be considered as an
investment in the future of the dairy herd rather than an increase in rearing cost.
S1 File. Multivariable regression models for the association between morphometric mea
sures and pre-weaning dietary group from 0 to 108 weeks, including potential
confounders. Calf was included as a random effect. Coefficients for time (in weeks) and interaction
terms are omitted for clarity.
S2 File. Marginal means (95% CI) of predicted morphometric measures by dietary group for calves from birth until 80 weeks of life.
The authors thank Prof Robert Smith, John Cameron and Andrew Parkinson for facilitating
the study at Wood Park Farm. They also thank Linda Cameron for caring for the calves during
Conceptualization: C. McGregor Argo.
Data curation: G. Curtis, C. McGregor Argo, D. Grove-White.
Formal analysis: G. Curtis, C. McGregor Argo, D. Grove-White.
Funding acquisition: C. McGregor Argo, D. Grove-White.
Investigation: G. Curtis, C. McGregor Argo, D. Jones, D. Grove-White.
Methodology: G. Curtis, C. McGregor Argo, D. Grove-White.
Project administration: G. Curtis, C. McGregor Argo.
Resources: C. McGregor Argo.
Supervision: C. McGregor Argo, D. Grove-White.
Writing ± original draft: G. Curtis, C. McGregor Argo, D. Grove-White.
Writing ± review & editing: G. Curtis, C. McGregor Argo, D. Grove-White.
17 / 20
southern Ontario. Prev Vet Med 83: 11±23. https://doi.org/10.1016/j.prevetmed.2007.03.001 PMID:
18 / 20
19 / 20
1. Gabler MT , Tozer P , Heinrichs AJ ( 2000 ) Development of a cost analysis spreadsheet for calculating the cost to raise a replacement dairy heifer . Journal of Dairy Science 83 : 1104 ± 1109 . PMID: 10821586
2. Trotz-Williams LA , Martin SW , Leslie KE , Duffield T , Nydam DV , et al. ( 2008 ) Association between management practices and within-herd prevalence of Cryptosporidium parvum shedding on dairy farms in
3. Dairy C ( 2011 ) Cost of rearing heifers . PD+ Fertility handbook for farmers.
4. Trotz-Williams LA , Wayne Martin S , Leslie KE , Duffield T , Nydam DV , et al. ( 2007 ) Calf-level risk factors for neonatal diarrhea and shedding of Cryptosporidium parvum in Ontario dairy calves . Prev Vet Med 82 : 12 ± 28 . https://doi.org/10.1016/j.prevetmed. 2007 . 05 .003 PMID: 17602767
5. Ettema JF , Santos JE ( 2004 ) Impact of age at first calving on lactation, reproduction, health and income in first-parity Holsteins on commercial farms . Journal of Dairy Science 87 : 2730 ± 2742 . https://doi.org/ 10.3168/jds.S0022- 0302 ( 04 ) 73400 - 1 PMID: 15328299
6. Haworth GM , Tranter WP , Chuck JN , Cheng Z , Wathes DC ( 2008 ) Relationships between age at first calving and first lactation milk yield, and lifetime productivity and longevity in dairy cows . The Veterinary Record 162 : 643 ± 647 . PMID: 18487583
7. Brickell JS , Bourne N , McGowan MM , Wathes DC ( 2009 ) Effect of growth and development during the rearing period on the subsequent fertility of nulliparous Holstein-Friesian heifers . Theriogenology 72 : 408 ± 416 . https://doi.org/10.1016/j.theriogenology. 2009 . 03 .015 PMID: 19481791
8. Morrison SJ , Wicks HCF , Carson AF , Fallon RJ , Twigge J , et al. ( 2012 ) The effect of calf nutrition on the performance of dairy herd replacements . Animal: an International Journal of Animal Bioscience 6 : 909 ± 919 .
Waltner-Toews D , Martin SW , Meek AH ( 1986 ) The Effect of Early Calfhood Health Status on Survivorship and Age at First Calving Canadian Veterinary Journal 50 : 314 .
Wathes DC , Swali A , Cheng Z , Brickell JS , Bourne NE ( 2008 ) Factors influencing heifer survival and fertility on commercial dairy farms [electronic resource] . Animal: an international journal of animal bioscience 2: 1135 ± 1143 .
11. Bermingham M , Berry D , Cromie A ( 2006 ) Change in the conformation of Irish Holstein-Friesian dairy cows over the past decade . Moorepark production Research centre.
12. Dairy A ( 2010 ) Heifer rearing myths .
13. Johnson KF , Chancellor N , Burn CC , Wathes DC ( 2017 ) Analysis of pre-weaning feed policies and other risk factors influencing growth rates in calves on 11 commercial dairy farms . Animal: 1 ± 11 .
14. Jasper J , Weary DM ( 2002 ) Effects of Ad Libitum Milk Intake on Dairy Calves . Journal of Dairy Science 85 : 3054 ± 3058 . https://doi.org/10.3168/jds.S0022- 0302 ( 02 ) 74391 - 9 PMID: 12487471
15. Van Amburgh ME , Soberon F , Raffrenato E , Karzses J , Everett RW ( 2011 ) Taking the long view: treat them nice as babies and they will be better adults . AABP Proceedings 44 : 79 ± 87 .
16. Anderson NG ( 2011 ) Practical aspects of accelerated feeding of dairy calves . AABP Proceedings 44 : 88 ± 100 .
17. Khan MA , Bach A , Weary DM , von Keyserlingk MAG ( 2016 ) Invited review: Transitioning from milk to solid feed in dairy heifers . Journal of Dairy Science 99 : 885 ± 902 . https://doi.org/10.3168/jds.2015-9975 PMID: 26709160
18. Baldwin RL , McLeod KR , Klotz JL , Heitmann RN ( 2004 ) Rumen development, intestinal growth and hepatic metabolism in the pre-and post-weaning ruuminant . Journal of Dairy Science 87 : E55± E65 .
19. Heinrichs AJ , Lesmeister KE ( 2005 ) Rumen development in the dairy calf . Nottingham: Nottingham University Press. pp. 53 ± 66 .
20. Soberon F , Raffrenato E , Everett RW , Van Amburgh ME ( 2012 ) Preweaning milk replacer intake and effects on long-term productivity of dairy calves . J Dairy Sci 95 : 783 ± 793 . https://doi.org/10.3168/jds. 2011-4391 PMID: 22281343
21. Drackley JK ( 2008 ) Calf nutrition from birth to breeding . Vet clin food anim 24 : 55± 86 .
22. Lammers BP , Heinrichs AJ , Kensinger RS ( 1999 ) The effects of accelerated growth rates and estrogen implants in prepubertal Holstein heifers on growth, feed efficiency, and blood parameters . Journal of Dairy Science 82 : 1746 ± 1752 . https://doi.org/10.3168/jds.S0022- 0302 ( 99 ) 75405 - 6 PMID: 10480101
23. Edmonson AJ , Farver T , Webster G , Lean IJ , Weaver LD ( 1989 ) A body condition scoring chart for holstein dairy cows . Journal of Dairy Science 72 : 68 ± 78 .
24. MacFarlane JA , Grove-White DH , Royal MD , Smith RF ( 2014 ) Use of plasma samples to assess passive transfer in calves using refractometry: comparison with serum and clinical cut-off point . Veterinary Record 174 .
Walker SL , Smith RF , Jones DN , Routly JE , Dobson H ( 2008 ) Chronic stress, hormone profiles and estrus intensity in dairy cattle . Hormones and Behavior 53 : 493 ± 501 . https://doi.org/10.1016/j.yhbeh.
2007 . 12 .003 PMID: 18206887
26. McGuirk SM ( 2008 ) Disease management of dairy calves and heifers . Veterinary Clinics of North America-Food Animal Practice 24 : 139 ±+.
27. Kirkwood BR , Sterne JAC ( 2003 ) Essential Medical Statistics. Oxford: Blackwell Science.
28. Curtis GC , Argo CM , Jones D , Grove-White DH ( 2016 ) Impact of feeding and housing systems on disease incidence in dairy calves . Veterinary Record 179 : 512 ±U550. https://doi.org/10.1136/vr.103895 PMID: 27803374
29. Appleby MC , Weary DM , Chua B ( 2001 ) Performance and feeding behaviour of calves on ad libitum milk from artificial teats . Applied Animal Behaviour Science 74 : 191 ± 201 .
30. Drackley JK , Pollard BC , Dann HM , Stamey JA ( 2007 ) First lactation milk production for cows fed control or intensified milk replacer programs as calves . Journal of Dairy Science 90 : 614 (Abstr.).
31. Kiezebrink DJ , Edwards AM , Wright TC , Cant JP , Osborne VR ( 2015 ) Effect of enhanced whole-milk feeding in calves on subsequent first-lactation performance . Journal of Dairy Science 98 : 349 ± 356 . https://doi.org/10.3168/jds.2014-7959 PMID: 25468697
32. Dairy A ( 2016 ) Calf Management .
Tanner JM ( 1981 ) Catch-up growth in man . British Medical Bulletin 37 : 233 ± 238 . PMID: 7034846
Wilson P , Osbourn D ( 1960 ) Compensatory growth after undernutrition in mammals and birds . Biological Reviews 35 : 324 ± 361 . PMID: 13785698
35. Abdalla HO , Fox DG , Thonney ML ( 1988 ) Compensatory gain by Holstein calves after underfeeding protein . Journal of Animal Science 66 : 2687 ± 2695 .
36. Lawrence TLJ , Fowler VR , Novakofski JE ( 2012 ) Growth of farm animals: CABI.
37. Costa JHC , von Keyserlingk MAG , Weary DM ( 2016 ) Invited review: Effacts of group housing of dairy calves on behavior, cognition, performance and health Journal of Dairy Science 99 : 2453 ± 2467 . https://doi.org/10.3168/jds.2015-10144 PMID: 26874423
38. Ollivett TL , Nydam DV , Linden TC , Bowman DD , Van Amburgh ME ( 2012 ) Effect of nutritional plane on health and performance in dairy calves after experimental infection with Cryptosporidium parvum . J Am Vet Med Assoc 241 : 1514 ± 1520 . https://doi.org/10.2460/javma.241.11.1514 PMID: 23176246
39. Klein-Jobstl D , Iwersen M , Drillich M ( 2014 ) Farm characteristics and calf management practices on dairy farms with and without diarrhea: A case-control study to investigate risk factors for calf diarrhea . Journal of Dairy Science 97 : 5110 ± 5119 . https://doi.org/10.3168/jds.2013-7695 PMID: 24881793
40. Hepola H ( 2003 ) Milk feeding systems for dairy calves in groups: effects on feed intake, growth and health . Applied Animal Behaviour Science 80 : 233 ± 243 .
41. Maatje K , Verhoeff J , Kremer WD , Cruijsen AL , van den Ingh TS ( 1993 ) Automated feeding of milk replacer and health control of group-housed veal calves . The Veterinary Record 133 : 266 ± 270 . PMID: 8236650
Warnick VD , Arave CW , Mickelsen CH ( 1977 ) Effects of group, individual and isolated rearing of calves on weight gain and behaviour . Journal of Dairy Science 60 : 947 ± 953 .
43. Gulliksen SM , Lie KI , Loken T , Osteras O ( 2009 ) Calf mortality in Norwegian dairy herds . Journal of Dairy Science 92 : 2782 ± 2795 . https://doi.org/10.3168/jds.2008-1807 PMID: 19448012
44. Hanninen L , Hepola H , Rushen J , de Passille AM , Pursaiainen P , et al. ( 2002 ) Resting behaviour, growth and diarrhoea incidence rate of young dairy calves housed individually or in groups in warm or cold buildings . Acta Agriculturae Scandinavica Section a-Animal Science 53.
45. Babu LK , Pandey HN , Patra RC , Sahoo A ( 2009 ) Hemato-biochemical changes, disease incidence and live weight gain in individual versus group reared calves fed on different levels of milk and skim milk . Animal Science 80 : 149 ± 156 .
46. Losinger WC , Heinrichs AJ ( 1997 ) Management practices associated with high mortality among preweaned dairy heifers . Journal of Dairy Research 64 : 1± 11 . PMID: 9120071
47. Pedersen RE , Sørensen JT , Skjøth F. , Hindhede J. , Nielsen TR ( 2009 ) How milk-fed dairy calves perform in stable versus dynamic groups . Livestock Science 121 : 215 ± 218 .
48. Quigley JD , III, Heitmann RN , Sinks GD , Caldwell LA ( 1991 ) Changes in blood glucose, nonesterified fatty acids, and ketones in response to weaning and feed intake in young calves . Journal of Dairy Science 74 : 250 ± 257 . https://doi.org/10.3168/jds.S0022- 0302 ( 91 ) 78167 - 8 PMID: 2030170
Webster AJ ( 2001 ) Farm animal welfare: the five freedoms and the free market . Vet J 161 : 229 ± 237 .
https://doi.org/10.1053/tvjl. 2000 .0563 PMID: 11352481
50. DEFRA ( 2006 ) Animal Welfare Act . In: DEFRA, editor.
51. Grove-White D ( 2010 ) Prevention and Treatment of Neonatal Calf DiarrhoeaÐA Personal Overview . CATTLE PRACTICE 18: 220 ± 223 .
52. Quigley JD , Wolfe TA , 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 . https://doi.org/ 10.3168/jds.S0022- 0302 ( 06 ) 72085 - 9 PMID: 16357284
53. Jensen MB , Budde M ( 2006 ) The Effects of Milk Feeding Method and Group Size on Feeding Behavior and Cross-Sucking in Group-Housed Dairy Calves . American Dairy Science Association 89 : 4778 ± 4783 .
54. Faber SN , Faber PNE , McCauley TC , AX RL ( 2005 ) CASE STUDY: Effects of Colostrum Ingestion on Lactational Performance . The professional animal scientist 21 : 420± 425 .
55. Marsh S ( 2009 ) Heifer Management at Harper Adams . UK: Holstein UK.
56. Pirlo G , Miglior F , Speroni M ( 2000 ) Effect of age at first calving on production traits and on difference between milk yield returns and rearing costs in Italian Holsteins . Journal of Dairy Science 83 : 603 ± 608 . https://doi.org/10.3168/jds.S0022- 0302 ( 00 ) 74919 - 8 PMID: 10750118
57. Eastham N , Coates A , Cripps P , Richardson H , Smith RF , et al. Associations between age at first calving and subsequesnt performance in UK Holstein and Holstein-Friesian dairy heifers; 2017; UK .
58. Lima FS , Ribeiro ES , Bisinotto RS , Greco LF , Martinez N , et al. ( 2013 ) Hormonal manipulations in the 5-day timed artificial insemination protocol to optimize estrous cycle synchrony and fertility in dairy heifers . J Dairy Sci 96 : 7054 ± 7065 . https://doi.org/10.3168/jds.2013-7093 PMID: 24011941
59. Swali A , Wathes DC ( 2007 ) Influence of primiparity on size at birth, growth, the somatotrophic axis and fertility in dairy heifers . Animal Reproduction Science 102 : 122 ± 136 . https://doi.org/10.1016/j. anireprosci. 2006 . 10 .012 PMID: 17097838
60. da Silva P , Aitken RP , Rhind SM , Racey PA , Wallace JM ( 2003 ) Effect of maternal overnutrition during pregnancy on pituitary gonadotrophin gene expression and gonadal morphology in female and male sheep at day 103 of gestation . Placenta 24 : 248 ± 257 . PMID: 12566252
61. Lima SF , Teixeira AG , Lima FS , Ganda EK , Higgins CH , et al. ( 2017 ) The bovine colostrum microbiome and its association with clinical mastitis . Journal of Dairy Science 100 : 3031 ± 3042 . https://doi.org/10. 3168/jds.2016-11604 PMID: 28161185
62. Oikonomou G , Teixeira AG , Foditsch C , Bicalho ML , Machado VS , et al. ( 2013 ) Fecal microbial diversity in pre-weaned dairy calves as described by pyrosequencing of metagenomic 16S rDNA. Associations of faecalibacterium species with health and growth . PLoS One 8 : e63157 . https://doi.org/10.1371/ journal.pone. 0063157 PMID: 23646192
63. Soberon F , Van Amburgh ME ( 2013 ) The effect of nutrient intake from milk or milk rep;acer of preweaned dairy calves on lactation milk yield as adults: a meta-analysis of current data . Journal of Animal Science.