Maintenance of body temperature in the neonatal lamb: Effects of breed,
birth weight, and litter size1
C. M. Dwyer2 and C. A. Morgan
Sustainable Livestock Systems Group, SAC, West Mains Road, Edinburgh, EH9 3JG, UK
ABSTRACT: To survive, the newborn lamb must be
able to maintain body temperature and to stand and
move to the udder to suck colostrum to fuel heat production. The objective of this study was to investigate
whether neonatal lambs showing slow behavioral progress to standing and sucking also have an impaired
ability to maintain body temperature. The time taken
to stand and suck after birth, rectal temperatures, and
blood samples were collected from 115 newborn single,
twin, and triplet lambs of 2 breeds, Scottish Blackface
and Suffolk, which are known to show variations in
their neonatal behavioral progress. Blood samples were
assayed for thyroid hormones, known to be involved in
heat production, and cortisol, which plays a role in tissue maturation before birth. In addition, colostrum
samples were collected from the 56 ewes that gave birth
to the lambs, and assayed for protein, fat, and vitamin
contents. Heavy lambs (more than 1 SD above the breed
mean), Blackface lambs, and singleton or twin lambs
were quicker to stand and suck from their mothers than
lightweight (more than 1 SD below the breed mean),
Suffolk, or triplet lambs. Low birth weight lambs also
had lower rectal temperatures than heavier lambs (P
< 0.01), as did Suffolk compared with Blackface lambs
(P < 0.001). Lambs that were slow to suck after birth
had lower rectal temperatures than quick lambs, and
this difference persisted for at least 3 d after birth.
Within breed, heavy lambs had greater plasma triiodothyronine and thyroxine immediately after birth than
light lambs. Blackface lambs had greater plasma triiodothyronine and thyroxine than Suffolk lambs but
tended to have less cortisol. Colostrum produced by
Blackface ewes had a greater fat content than that of
Suffolk ewes (P < 0.001). Thus, lambs that are behaviorally slow at birth are also less able to maintain their
body temperature after birth. Although part of their
lower body temperature might be attributable to behavioral influences on thermoregulation, the data also suggest that physiological differences exist between these
animals. These differences may be related to different
degrees of maturity at birth.
Key words: behavior, breed, neonate, sheep, temperature
2006 American Society of Animal Science. All rights reserved.
INTRODUCTION
The worldwide rate of mortality in newborn lambs is
in excess of 15% of lambs born and represents a challenge to sheep production and welfare. The ability to
survive is crucially dependent on the response of the
lamb to the thermal (climatic) environment into which
1
This study was supported by the Scottish Executive Environment
and Rural Affairs Department. We thank the following: N. Scott
and M. Ramsay for the animal husbandry; S. Robson, M. Farish, J.
Donbavand, J. Chirnside, and H. Pickup for technical assistance at
lambing time; A. Thain for cortisol assays, S. Gorrie for thyroid hormone assays, J. Rooke and M. Ewen for analysis of vitamin contents
and immunoglobulin G; E. Brechany and J. Dunsmuir at the Hannah
Research Institute for the colostrum analysis; and C. Theobald and
I. Nevison for statistical advice.
2
Corresponding author: Cathy.Dwyer@sac.ac.uk
Received July 14, 2005.
Accepted November 30, 2005.
J. Anim. Sci. 2006. 84:1093–1101
it is born. Lambs are born, often into cold or wet conditions, with low fat cover and have a high surface area
to BW ratio, which exacerbates heat loss (Alexander,
1970; Stephenson et al., 2001). There is a high energy
demand to maintain body temperature, and this must
be supplied by efficient metabolism of brown adipose
tissue (BAT) and by showing the appropriate standing
and sucking responses to obtain milk. Temperature control at birth is dependent mainly on heat production by
oxidation of fat from BAT by a process under the control
of triiodothyronine (T3; Dauncey, 1990). Triiodothyronine is produced from thyroxine (T4) in BAT by the
enzme 5′-monodeiodinase, the activity of which increases in the last month of pregnancy. Tissue maturation in the fetus is controlled by the increased production of cortisol toward the end of pregnancy (Fowden
et al., 1998; Mellor, 1988). The development of neonatal
behavior and thermoregulatory ability may thus be related to relative maturity at birth. Lambs that are slow
to stand and suck after birth have greater mortality
1093
1094
Dwyer and Morgan
(Dwyer et al., 2001), and lambs with low rectal temperatures are more likely to fail to reach the udder (Slee
and Springbett, 1986). Further, damage to the fetal
central nervous system during delivery causes impaired
sucking and locomotor activity in lambs (Haughey,
1980) and impairs thermoregulation in the neonate
(Eales and Small, 1980; Bellows and Lammoglia, 2000).
Therefore, it seems that neonatal behavior, specifically
success in finding the udder and obtaining colostrum,
is intimately associated with the ability to thermoregulate. In this study we investigated whether lambs showing slow neonatal behavioral progress also have an impaired ability to maintain body temperature.
MATERIALS AND METHODS
Animals
Data were collected from the purebred offspring of
56 ewes [33 Blackface (BF) and 23 Suffolk (S)] over 2
years. Thirteen ewes contributed lamb records in both
years. The ewes produced 115 lambs alive at birth (BF:
16 singles, 40 twins, and 13 triplets; S: 11 singles, 20
twins, and 14 triplets). Lambs were sired by 1 of 10
rams (4 BF and 6 S).
Ewes were estrous-synchronized using progesterone
vaginal sponges (Veramix; Upjohn Ltd, Crawley, UK)
and artificially inseminated with fresh semen. At approximately midgestation, the ewes were brought indoors into large straw-bedded pens (7 × 7 m) in groups
of approximately 10 ewes and given access to hay and
fresh drinking water ad libitum. Concentrates (locally
milled ewe nuts; 218 g of CP per kg of DM) were provided from wk 14 of gestation, at a ration of 300 gⴢ
ewe−1ⴢd−1 (S) or 200 gⴢewe−1ⴢd−1 (BF). The rations were
doubled every 2 wk until wk 18 of gestation and then
maintained at this level. The ewes were vaccinated with
a clostridial vaccine (Covexin-8, Mallinckrodt, Middlesex, UK) in wk 17.
In the weeks immediately before parturition, the
ewes were habituated to the presence of observers in
the central walkways between pens. Approximately 3
d before the expected parturition dates (parturition occurs on average at d 145 of gestation), the ewes were
kept under 24-h video surveillance. In addition, at least
1 observer was present at all times once lambing had
begun. As far as possible, the ewes were allowed to give
birth to and care for their lambs unaided. However,
lambing assistance (n = 30 lambs) was given if the ewe
had failed to progress through a time schedule of events;
that is, 1 h after the appearance of fluids but no appearance of parts of the lamb, and/or 2 h after parts of the
lamb were seen at the vulva with no other obvious
progress being made. In all cases, intervention was kept
to a minimum and mainly involved correcting lamb
presentation before the ewe continued the birth process
unaided. Once the lamb had been born, it was allowed
3 h to achieve a successful sucking unaided. Lambs that
had not sucked after this time were assisted to suck.
Lamb weight, crown-rump (CR) length, and sex were
recorded within 24 h of birth. Lambs were marked with
the identity number of their mothers and also for birth
order using paint brands. The ewes remained in the
lambing pens until 3 d after birth, when they and their
lambs were moved outside to pasture. The lambs were
born and maintained throughout at ambient temperature (mean temperature at birth = 7.4°C; range = −2
to 18°C).
Data Recording
The time of birth, the overt length of labor (calculated
from the appearance of fluids until birth of the last
lamb), the interval between littermates in multiple litters, and the degree of assistance required were recorded for all ewes and lambs. Birthing difficulty was
assessed on a score of 1 to 3, with 1 indicating no assistance required, 2 indicating that presentation only was
corrected or minor assistance was given, and 3 indicating that the lamb was delivered manually. Lamb presentation at delivery was also recorded whenever possible. A correct presentation was recorded when the lamb
was presented forefeet first with the nose lying along
the forelegs. Any other presentation at birth (head first
with 1 or both forelegs retracted, head back, 2 lambs
together, backwards, or breech) was recorded.
Behavior. Data on lamb behavioral latencies were
collected on handheld Psion Workabout computers during the 2 h after the birth of each lamb using Observer
data recording software (Noldus Information Technology, Wageningen, The Netherlands; Noldus et al.,
2000). The time from birth to successful standing
(standing on all 4 extended legs for more than 5 s) and
successful sucking (teat held in mouth, lamb still and in
parallel-inverse position with tail wagging for at least
5 s, confirmed by palpation of the abdomen at 2 h)
was recorded.
Physiology. Between 30 and 50 min (mean = 45 min)
after birth, the lamb was caught and a 2-mL blood
sample was taken by jugular venipuncture into heparinized vacutainers. Rectal temperature was also recorded at this time using digital probes (Digital thermometers, Boots, Nottingham, UK). To minimize the
disruption to ewe and lamb bonding, all samples were
collected within the home pen of the animal, which
allowed the ewe to continue to interact with the lamb
during sampling, and all samples were collected within
2 min of entering the pen. The blood sampling and
temperature recording procedures were repeated at 24
and 72 h after birth. Blood samples were stored on ice
until centrifugation (20 min, 1,000 × g). The resultant
plasma was separated and stored at −80°C until assayed for cortisol, T3, and T4 concentrations. At 2 h
after birth, a 15-mL sample of colostrum was taken
from each ewe. Five milliliters was frozen at −20°C for
subsequent analysis of immunoglobulin G, vitamin A,
and vitamin E contents. The remaining 10 mL was
stored in a tube with preservative (8 mg of Bronopol,
1095
Temperature maintenance in the neonatal lamb
Broad-Spectrum Microtabs II, D&F Control Systems
Inc., Dublin, CA) at 4°C until protein and fat contents
were determined.
Assay Procedures
Cortisol. Samples for cortisol analysis were extracted from 100 ␮L of plasma with diethyl ether, and
the concentrations were measured using RIA of the
extracted steroid, as previously described (Duncan et
al., 1990). Single samples were extracted and then assayed in duplicate. The intra- and interassay CV were
9.1 and 10.2% respectively, and the minimum detectable level of the assay was 0.23 ngⴢmL−1.
Thyroid Hormones. Concentrations of thyroid hormones were determined using a solid phase, competitive chemiluminescent enzyme immunoassay system
[Immulite, Diagnostic Products Corporation (DPC),
California]. Concentrations were determined using
kits, controls, monoclonal mouse antibodies, and reagents supplied by DPC. The intra- and interassay CV
were 7.6 and 8.6% for T3 and 8.9 and 10.8% for T4. The
minimum detectable levels of the assays were 0.29 and
3.9 nmol/L for T3 and T4, respectively.
Vitamin Content of Colostrum. Colostrum was deproteinized with ethanol, and the vitamins were extracted into hexane (Hoehler et al., 1998). The resulting
hexane extracts were analyzed by HPLC (Kontron 400,
Kontron Instruments, Watford, UK) with programmed
fluorescence detection and by reference to internal and
external standards (Williams, 1985). The mobile phase
was 1% ethanol in hexane at a flow rate of 2 mL/min
isocratic using a Waters Spherisorb Silica 250 × 4.6mm column with integral guard (Waters Ltd., Elstree,
Herts., UK.
Protein and Fat Contents of Colostrum. Ewe colostrum samples were diluted with water, and the protein
and fat contents were determined by near-infrared reflectance using a Milkoscan 50 (Foss, Hillerød, Denmark). The instrument was first calibrated using bovine
milk samples and a number of sheep samples analyzed
by a modified Kjeldahl nitrogen method [protein:
BS1741, part 5, section 5.2 (1996)] and a modified Rose
Gottlieb method [fat: BSEN IS01211 (2001)].
temperatures, and plasma cortisol concentrations were
not normally distributed in the neonatal lambs. The
behavioral and cortisol data could be normalized by
natural logarithm transformations, but the temperature data could not be normalized. Total cortisol over
the first 3 d of life was calculated as the area under the
curve by integration. This variable was not normally
distributed and could not be normalized by transformation. Therefore, the nonparametric Kruskal-Wallis test
in Minitab (Release 12.1; Minitab Inc., State College,
PA) was used to investigate temperature and total cortisol. The effect of time on cortisol concentrations in lamb
plasma was determined by Wilcoxon matched-pairs
analysis.
To investigate the relationship between lamb behavior and rectal temperature, lambs were divided into
groups based on the time taken for them to stand and
suck, and the group was used as a factor in the analysis.
For other lamb behavioral and physiological variables,
the effects of birth difficulty, birth weight, litter size,
lamb sex, lamb breed, and ewe parity and age were
fitted as fixed effects to the model using the REML
procedure (Patterson and Thompson, 1971) in Genstat
7.0 (Lawes Agricultural Trust, Rothamsted Experimental Station, UK), after checking for interactions among
the variables. The potentially confounding effects of
birth weight and litter size were addressed by fitting
birth weight as a covariate and running the model twice
by alternating the order of the explanatory variables.
Year and ewe identity were fitted as random factors in
the analysis, as ewes produced more than 1 lamb in
the data set. This test procedure approximated to an
ANOVA when the data were balanced but was capable
of also handling unbalanced data. It was deemed the
most appropriate test for these data, as they were unbalanced with respect to most of the fixed effects. For
categorical data (birth difficulty score and sucking failure), significant differences were determined by χ2
tests.
RESULTS
There were no significant effects of lamb sex or ewe
age and parity on the data; thus these factors will not
be discussed further.
Statistical Analysis
As lamb breeds differed markedly in their birth
weights (BF = 3.96 ± 0.08 kg; S = 4.93 ± 0.20 kg), within
breed lamb weights were divided into light weight
lambs (>1 SD below the breed mean; n = 20), medium
weight lambs (weighing within 1 SD of the breed mean;
n = 77), and heavy weight lambs (>1 SD greater than
the breed mean; n = 16). This weight code was used in
subsequent analysis of birth weight on the data that
were not normally distributed. The effect of birth
weight on normally distributed neonatal physiological
variables (thyroid hormones) was assessed by regression within breed. The behavioral data, lamb rectal
Breed Effects
Gestation length (P < 0.001), lamb birth weight (P <
0.001), and lamb CR length (P = 0.007) were affected
by breed (Table 1). Blackface lambs were born following
a gestation of approximately 1.5 d less than S lambs,
and were lighter and shorter than S lambs. Blackface
lambs required less assistance at delivery than S lambs
(respectively 14.7 and 43.5%, χ2 = 11.71, df = 1, P <
0.001) and were less likely to be incorrectly presented
at birth (21.1 and 41.3% respectively, χ2 = 7.50, df = 1,
P = 0.006). Suffolk lambs were slower than BF lambs
to stand (P < 0.001) and suck (P < 0.001; Table 1).
1096
Dwyer and Morgan
Table 1. The effects of breed and litter size on gestation length, lamb weights and neonatal lamb behavior1
Breed
Litter size
Blackface
lamb
Suffolk
lamb
69
143.5 ± 0.17
46
144.9 ± 0.26
Birth weight, kg
3.96 ± 0.08
4.93 ± 0.20
CR length,4 cm
42.0 ± 0.4
43.5 ± 0.6
13.58
(10.23 – 19.67)
80
(43 – 110)
25.13
(15.30 – 45.87)
144
(944 – 200)
Item
n
Gestation length, d
Stand latency,5 min
Suck latency,6 min
Statistic
2
18.65,
P < 0.001
55.09,
P < 0.001
7.4,
P = 0.007
30.67,
P < 0.001
13.77,
P < 0.001
Single
Twin
Triplet
27
144.7 ± 0.37
61
144.3 ± 0.19
27
142.9 ± 0.27
5.35 ± 0.19
4.25 ± 0.10
3.55 ± 0.20
45.1 ± 0.7
42.1 ± 0.4
41.2 ± 0.7
21.60
(13.90 – 34.82)
71
(52 – 131)
13.38
(10.62 – 20.08)
89
(43 – 123)
20.15
(14.00 – 29.60)
130
(89 – 200)
Statistic3
8.12,
P = 0.017
75.46,
P < 0.001
21.05,
P < 0.001
18.41,
P < 0.001
9.80,
P = 0.007
1
Values are means with SE or 95% confidence intervals for back-transformed means (behaviors only).
Values are Wald statistics determined by REML analysis and approximate to a χ2 distribution; df = 1 throughout.
3
Values are Wald statistics determined by REML analysis; df = 2 throughout.
4
Crown-rump length.
5
Time from birth until the lamb was seen to stand unsupported for 5 s.
6
Time from birth until the lamb was seen to suck successfully from the udder.
2
Additionally, a greater proportion of S lambs failed to
suck during the recording period (sucking failure: S =
57.1%, BF = 2.9%, χ2 = 42.94, df = 1, P < 0.001).
There was no relationship between ambient temperature at birth and lamb rectal temperature over the first
3 d of life (Spearmans rank order correlation = 0.002,
P = 0.985), nor was there any relationship between
assistance given with delivery and rectal temperature
(Kruskal Wallis H = 1.76, df = 2, P = 0.415). Blackface
lambs had greater body temperatures than S lambs
throughout the first 3 d of life (P < 0.001; Table 2).
Plasma cortisol concentrations were high in newborn
lambs and declined with age over the first 3 d of life
(Wilcoxon matched pairs, t = 271, n = 88, P < 0.001;
Figure 1). There was no significant effect of lamb breed
at any sampling time after delivery. However, the total
amount of cortisol in S plasma over the first 3 d of life
(calculated as the area under the curve) tended to be
greater than in BF lambs (plasma cortisol (ng/mL: medians with interquartile ranges): BF = 193.7 (151.3 −
267.9), S = 253.2 (164.1 − 331.7), Kruskal Wallis H =
3.64, df = 1, P = 0.057).
There was a significant effect of lamb breed on both
thyroid hormones (Table 3). Throughout the recording
period BF lambs had greater circulating concentrations
of both T3 and T4 than S lambs. The ratio of T3/T4 was
equal in both breeds immediately after birth and at 72
h, but tended to be greater in Suffolk lambs 24 h after
birth (mean ratio: BF = 0.046, S = 0.050, SED = 0.002,
Wald = 3.27, df = 1, P = 0.07).
Blackface ewes had a greater concentration of fat (P
< 0.001) but not of protein (P = 0.271) in their colostrum
than S ewes (Table 4). There were no significant effects
of breed on the immunoglobulin G content of the colostrum (P = 0.15), but as might be expected from the
greater fat content, BF colostrum had a greater concentration of vitamin E (P = 0.021) and tended to have
greater vitamin A concentration (P = 0.079) than S colostrum.
Litter Size Effects
Gestation length (P = 0.017), lamb birth weight (P <
0.001), and lamb CR length (P < 0.001) were affected
Table 2. The effects of breed and litter size on lamb rectal temperatures (in °C) measured over the first 3 d of life1
Time
after
birth, h
Breed
Litter size
Blackface lamb
Suffolk lamb
Statistic2
Single
Twin
Triplet
Statistic3
<1
40.0 (39.6 – 40.3)
39.4 (38.2 – 39.7)
39.8 (39.4 – 40.3)
39.8 (39.4 – 40.2)
39.4 (38.0 – 39.9)
24
39.3 (39.1 – 39.6)
39.1 (38.7 – 39.3)
39.3 (39.1 – 39.6)
39.2 (39.0 – 39.6)
39.0 (38.6 – 39.2)
72
39.4 (39.2 – 39.6)
39.2 (38.9 – 39.5)
23.85,
P < 0.001
14.63,
P < 0.001
8.64,
P = 0.003
39.3 (39.2 – 39.5)
39.4 (39.1 – 39.6)
39.2 (39.1 – 39.7)
10.04,
P = 0.007
9.88,
P = 0.007
0.06,
P = 0.972
1
Values are medians with interquartile ranges, numbers of animals in each group as in Table 1.
Significance was determined by Kruskal Wallis tests; df = 1 throughout.
Values are Kruskal Wallis H; df = 2.
2
3
Temperature maintenance in the neonatal lamb
1097
P = 0.313; T4: Wald = 2.03, df = 2, P = 0.362). Ewes had
increasing amounts of fat content in their colostrum
with each increase in litter size (P = 0.008; Table 4).
Litter size also had an impact on protein content with
triplet-bearing ewes producing colostrum with a reduced protein content compared with single- or twinbearing ewes (P = 0.005). Colostrum of twin-bearing
ewes had a greater vitamin E content than other litter
sizes (P = 0.021), but there was no effect on vitamin A
content (P = 0.534).
Birth Weight Effects
Figure 1. The effect of lamb age on plasma cortisol
concentrations for Blackface (solid symbols and solid
lines) and Suffolk lambs (open symbols and broken lines)
over the first 3 d of life. Values are medians with interquartile ranges. Plasma cortisol declined with increasing
lamb age (P < 0.001) and tended to be greater in Suffolk
lambs compared with Blackface over the first 3 d of life
(P = 0.057).
by litter size (Table 1). Triplet pregnancies were shorter
than singleton or twin pregnancies. Lamb birth weight
and CR length declined with each increase in lamb
number in the litter. There were no effects of litter size
on assistance at delivery (χ2 = 4.26, df = 2, P = 0.119)
or lamb presentation (χ2 = 1.60, df = 2, P = 0.449). There
was an effect of litter size (Table 1) on lamb neonatal
behaviors that was not attributable to birth weight.
Triplet lambs were slower to suck than single and twin
lambs (P = 0.007), and both triplet and single lambs
were slower to stand than twin lambs (P < 0.001). Triplet lambs had lower temperatures than single or twin
lambs immediately after birth (P = 0.007) and at 24 h
of age (P = 0.007) but not by 72 h (P = 0.972; Table 2).
There were no significant effects of litter size on
plasma cortisol concentrations (Wald = 2.84, df = 2, P =
0.242). In addition, there were no significant effects
of litter size on the thyroid hormones that were not
accounted for by birth weight (T3: Wald = 2.32, df = 2,
Table 3. The effect of lamb breed on plasma T3 and T4
(nmol/L) over the first 3 d of life1
Item
n
T3
T3
T3
T4
T4
T4
at
at
at
at
at
at
1
<1h
24 h
72 h
< 1h
24 h
72 h
Blackface
lamb
Suffolk
lamb
Pooled
SED
69
6.25
7.51
6.79
149.5
175.2
144.8
46
5.50
6.67
5.62
131.4
132.6
119.9
0.39
0.29
0.35
10.45
8.84
7.42
T3 = triiodothyronine. T4 = thyroxine.
Values are Wald statistics; df = 1.
2
Statistic2
3.84,
8.46,
11.27,
2.97,
23.21,
11.26,
P = 0.05
P = 0.004
P < 0.001
P = 0.085
P < 0.001
P < 0.001
Heavy lambs were quicker to suck than light lambs
(P = 0.047; Table 5), although there was no effect on
time to stand (P = 0.33). Lamb birth weight relative to
the breed mean had a significant impact on lamb rectal
temperature (Figure 2); light lambs had lower temperatures than heavier lambs at 1 h (P = 0.045), 24 h (P =
0.001), and 72 h after birth (P = 0.016). Heavy lambs
tended to be more likely to need assistance at delivery
than light lambs (percentage of lambs requiring assistance: light = 20.0%, medium = 23.7%, heavy = 50.0%,
χ2 = 5.24, df = 2, P = 0.073).
There were no effects of birth weight on plasma cortisol concentrations (Wald = 0.70, d.f. = 1, P = 0.402).
However, lambs that had been assisted at delivery had
greater plasma cortisol than unassisted lambs at both
24 and 72 h after birth [plasma cortisol (ng/mL; mean
values with 95% confidence intervals): 24 h—unassisted lambs = 40.8 (31.7 − 52.5); partly assisted lambs =
37.3 (29.0 − 48.0); assisted lambs = 74.8 (58.1 − 96.4),
Wald = 10.47, df = 2, P = 0.005; 72 h—unassisted
lambs = 17.8 (12.9 − 24.7), partly assisted lambs = 29.2
(21.1 − 40.4), assisted lambs = 40.0 (28.9 − 55.3), Wald =
9.21, df = 2, P = 0.01)].
Plasma T3 was significantly related to birth weight,
in both breeds of lamb, for the first 24 h of life but not
thereafter (Table 6). In the BF breed, birth weight had
an effect on plasma T4 immediately after birth only (P =
0.001), whereas, for S lambs, plasma T4 was related to
birthweight for the first 24 h of life (P = 0.017), and
there was still a tendency for birth weight to influence
T4 72 h after birth (P = 0.076; Table 6).
Relationship Between Lamb Behavior
and Rectal Temperature
Lambs that were slow to stand had lower rectal temperatures within 1 h of birth (P < 0.001) and at 24 h
after birth (P = 0.045) than lambs that stood quickly
(Figure 3a). This relationship had disappeared by 72 h
after birth (P = 0.08). Lambs that were slow to suck,
or failed to suck successfully within the recording period
and needed assistance to suck also had lower temperatures than lambs that were quick to suck after birth
over the first 3 d of life (P = 0.027; Figure 3b).
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Dwyer and Morgan
Table 4. The effects of breed and litter size on colostrum content of ewes1
Breed
Litter size
Item
Blackface
ewe
Suffolk
ewe
Statistic2
Single-bearing
ewe
Twin-bearing
ewe
Triplet-bearing
ewe
n
% fat
39
16.53 ± 0.74
26
13.26 ± 0.86
12.25 P < 0.001
26
12.91 ± 0.97
32
15.05 ± 0.85
7
16.93 ± 0.74
% protein
15.54 ± 0.67
14.19 ± 1.16
1.42 P = 0.271
15.22 ± 0.93
17.21 ± 0.72
12.17 ± 2.51
45.08
(39.29 – 51.26)
7.89
(6.99 – 8.86)
5.52
(4.97 – 6.10)
54.09
(47.73 – 60.86)
6.35
(5.54 – 7.21)
4.24
(3.76 – 4.75)
2.07
P = 0.15
5.93 P = 0.021
55.80
(46.87 – 65.51)
6.60
(5.49 – 7.82)
4.67
(3.96 – 5.43)
53.88
(45.10 – 63.43)
8.76
(7.47 – 10.16)
5.20
(4.45 – 6.01)
39.56
(32.10 – 47.80)
6.15
(5.08 – 7.33)
4.75
(4.04 – 5.53)
Immunoglobulin
G, mg/mL
Vitamin E, ␮g/mL
Vitamin A, ␮g/mL
3.09 P = 0.079
Statistics3
9.56
P = 0.008
10.62
P = 0.005
2.74
P = 0.222
7.70
P = 0.021
1.14
P = 0.534
1
Values are means and SE (fat and protein content) or means with 95% confidence intervals.
Values are Wald statistics; df = 1.
3
Values are Wald statistics; df = 2.
2
DISCUSSION
This experiment has confirmed our previous observations of differences between BF and S breeds in neonatal behavior (Dwyer and Lawrence, 2000; Dwyer, 2003).
The data also demonstrate that the BF lambs, in addition to standing and sucking quickly, have greater rectal temperatures than S lambs, and greater plasma T3
and T4 over the first 3 d of life. Plasma cortisol tends
to be greater in S lambs compared with BF. Our data
also support previous observations (Dwyer, 2003) that
low birth weight lambs within breed show slower behavioral progress after birth. In addition, this experiment has shown that lightweight lambs have lower
body temperatures over the first days of life, and have
less T3 and T4 at birth than heavier lambs. Triplet
lambs were slower to stand and suck at birth than other
litter sizes as seen previously (Dwyer, 2003), and this
effect was in addition to their lower birth weight. Triplet
lambs also had lower temperatures over the first days
of life, but there were no influences of litter size on
neonatal concentrations of cortisol or T3 and T4. The
data therefore suggest that lamb thermoregulatory
ability at birth can be influenced by genetic factors
(lamb breed) and by environmental factors (such as
prenatal nutrition and litter size) influencing birth
weight. In both cases, lambs that are behaviorally slow
at birth also have difficulty maintaining their body temperature.
Lambs are known to maintain body temperatures
greater than those of adult ewes for the first month of
life (Symonds et al., 1989; Clarke et al., 1997; Bird et
al., 2001) and with a blunted nocturnal rhythm compared with ewes (Faurie et al., 2004). Lambs have a
high metabolic turnover immediately after birth, which
may increase body temperature (Symonds et al., 1995).
Behavioral competence and body temperature appear
to be linked; lambs with a low rectal temperature are
more likely to fail to reach the udder after birth than
those with normal temperatures (Slee and Springbett,
1986). Thus, behavioral mechanisms may operate to
prevent falls in temperature. Standing rapidly after
birth helps to reduce convective heat loss of the wet
lamb to the ground, and sucking bouts or feeding raise
body temperature (Bird et al., 2001). Thus the rapid
behavioral progress of the BF lambs compared with S
lambs and of the heavier lambs compared with low
birth weight lambs seen in the current study will have
contributed directly to their greater temperatures. In
addition, neonatal huddling with other lambs or sleeping close to the ewe could prevent falls in core temperature. Our previous data demonstrate that BF lambs
and ewes maintain closer spatial relationships than S
lambs and ewes (Dwyer and Lawrence, 2000), sug-
Table 5. Relationship between lamb birth weight and neonatal behavioral progress to standing and sucking1
Behavior
Stand latency (min)4
Suck latency (min)5
1
Light2
Medium2
Heavy2
Statistic3
20.15 (12.88 – 46.37)
127.5 (74.15 – 180)
14.42 (11.25 – 26.32)
91.27 (54.20 – 135.75)
20.53 (11.92 – 24.15)
54.00 (46.25 – 99.00)
2.24 P = 0.33
6.07 P = 0.047
Values are medians with interquartile ranges.
Lambs were classified as light (more than 1 SD lighter than the breed mean), medium (within 1 SD of the breed mean), and heavy (more
than 1 SD heavier than the breed mean).
3
Values are Kruskal Wallis H with 2 df.
4
Time from birth until the lamb was seen to stand unsupported for 5 s.
5
Time from birth until the lamb was seen to suck successfully from the udder.
2
Temperature maintenance in the neonatal lamb
1099
Figure 2. The relationship between lamb birth weight
and rectal temperature recorded within 1 h, at 24, and at
72 h after birth. Values are medians with upper interquartile ranges. Light lambs (weighing more than 1 SD
less than the breed mean; n = 20) had significantly lower
temperatures than heavy lambs (weighing more than 1
SD greater than the breed mean; n = 16) at <1 h after
birth (P = 0.045), at 24 h after birth (P = 0.001), and at 72
h after birth (P = 0.016). a,bBars with different letters are
significantly different.
gesting that this may be an additional mechanism by
which BF lambs are able to maintain greater temperatures than S lambs.
Breed differences in ability to maintain body temperature at birth and genetic variation in this trait within
breed have been observed before (Sykes et al., 1976;
Slee and Springbett, 1986; Slee et al., 1991). Blackface
lambs are smaller than S lambs and would be expected
to lose heat more quickly and to be energetically disadvantaged. However, BF lambs were more successful at
maintaining body temperature than S lambs, at least
over the first 3 d of life. This indicates that the BF were
either more efficient at conserving heat through better
coat or tissue insulation or were more efficient at producing heat than S lambs, or both. Differences in coat
insulation at birth are small immediately after delivery
when the lambs are wet with birth fluids (Sykes et al.,
1976), which is when the first breed difference in body
Table 6. Correlation of lamb birth weight with T3 and
T4 concentrations in plasma from Blackface and Suffolk
lambs collected over the first 3 d of life1
Item
<1
24
72
<1
24
72
T3
T3
T3
T4
T4
T4
1
Blackface lamb
h
h
h
h
h
h
after
after
after
after
after
after
birth
birth
birth
birth
birth
birth
b2 = 0.438,
b = 0.268,
b = −0.054,
b = 0.350,
b = 0.136,
b = −0.109,
P
P
P
P
P
P
=
=
=
=
=
=
0.001
0.038
0.678
0.012
0.300
0.40
T3 = triiodothyronine. T4 = thyroxine.
b = correlation coefficient.
2
Suffolk lamb
b = 0.469,
b = 0.318,
b = −0.018,
b = 0.534,
b = 0.367,
b = 0.284,
P
P
P
P
P
P
= 0.002
= 0.040
= 0.912
< 0.001
= 0.017
= 0.076
Figure 3. The relationship between lamb rectal temperatures and behavioral progress after birth. (a) Median
time to stand after birth (with upper interquartile ranges);
groups are lambs that stood within 15 min of birth (n =
52); lambs that stood between 15 and 30 min after birth
(n = 40); lambs that stood between 30 and 60 min after
birth (n = 8); and lambs that stood more than 1 h after
birth (n = 9). Differences are significant at <1 h after birth
(P < 0.001) and 24 h after birth (P = 0.045) but not at 72
h (P = 0.08). (b) Median time to suck after birth (with
upper interquartile ranges); groups are lambs that sucked
within 30 min of birth (n = 19); lambs that sucked between
30 and 60 min after birth (n = 36); lambs that sucked
between 1 and 2 h after birth (n = 20); and lambs that
took longer than 2 h or required assistance to suck (n =
31). Differences are significant at <1 h after birth (P =
0.002), 24 h after birth (P = 0.005), and 72 h after birth
(P = 0.027). a,bBars with different letters are significantly different.
temperature was recorded in the current study. Thereafter BF lambs have a thicker birth coat than S lambs,
and phenotypic correlations with coat depth and cold
resistance have been reported in BF lambs (Stott and
Slee, 1987). However, Slee (1978) demonstrated a breed
difference in cold resistance in clipped lambs, suggesting that birth coat is at most only a contributory
factor to breed differences in thermoregulation. With
respect to the degree of tissue insulation, Sykes et al.
(1976) concluded that differences between breeds would
be too small to account for the large differences in temperature regulation. Thus it is likely that the differ-
1100
Dwyer and Morgan
ences in ability to maintain body temperature between
the BF and S breeds seen here, in addition to behavioral
mechanisms mentioned previously, were a result of differences in the rate of development of cold thermogenesis after birth (Sykes et al., 1976).
Cold thermogenesis in the newborn lamb occurs
largely in BAT, which can rapidly generate heat by
nonshivering thermogenesis (Stephenson et al., 2001).
The prenatal development and subsequent neonatal responses of BAT are influenced by the thyroid hormones,
particularly through actions on BAT iodothyronine 5′
monodeiodinase (which converts T4 to T3) and mitochondrial uncoupling protein (UCP1; reviewed by Polk,
1988). The greater concentrations of plasma T3 and T4
seen in BF lambs suggest that both their thyroid and
BAT was more active than in S lambs and thus cold
thermogenesis was more efficient in BF lambs. Symonds et al. (1989) showed that lambs with low plasma
T3 concentrations (below 1.73 nmol/L) relied more on
shivering thermogenesis in response to cold exposure
than lambs with greater concentrations of T3 (>2.06
nmol/L), which had a greater contribution from nonshivering thermogenesis. The minimum plasma T3 concentrations recorded here in both breeds of lamb were
considerably greater than 2.06 nmol/L; thus it is likely
that nonshivering thermogenesis predominated. The
ratio of T3/T4 in the plasma was similar for both breeds
except at 24 h old, when it tended to be greater in S
lambs. Thus, a behavioral delay and reduced thermogenesis in S lambs appear to contribute to their lower
rectal temperatures during the neonatal period in comparison with BF lambs.
Cortisol is an important regulator of fetal maturation
and increases the production of T3 in the fetus in preparation for the increase in metabolic rate and thermogenesis that occurs at birth (reviewed by Liggins, 1994).
Brown adipose tissue UCP1 is increased in the fetal
lamb by infusion of cortisol (Mostyn et al., 2003), which
also increases fetal T3. Given the greater concentration
of thyroid hormones in BF lambs in the current study,
it was surprising that greater plasma cortisol concentration was measured in the neonatal S lambs compared with BF lambs. It is possible that this represents
a delay in neonatal maturity in the S lambs, and a
more frequent sampling regimen might have shown
a difference in the rate of decline of plasma cortisol
concentration over the first days of neonatal life.
Whether this breed difference is also present in the
fetus or whether BF fetal lambs have greater plasma
cortisol concentrations than S fetuses requires further investigation.
The lesser ability of low birth weight and triplet
lambs to maintain body temperature after birth can be
at least partly attributed to their small body size and
therefore greater relative surface area for heat loss. In
addition they were slower to stand and suck so were
less able to make use of behavioral strategies to maintain body temperature. Low birth weight lambs will
have experienced some degree of undernutrition in
utero (for example, through being part of a triplet litter),
and fetal adipose tissue development is known to be
sensitive to fetal nutrition (Budge et al., 2003). Fetuses
subjected to low nutrition in late gestation have less
adipose tissue and reduced abundance of UCP1 mRNA
in that tissue (Budge et al., 2004). In the current study,
plasma concentrations of plasma T3 and T4 were reduced at birth in low birth weight lambs in comparison
with heavier lambs as has been shown before (Cabello
and Levieux, 1981; Wrutniak et al., 1990). This suggests that these animals were also compromised in their
ability to produce heat by nonshivering thermogenesis
immediately after birth.
The supply of nutrients in colostrum is important for
the production of heat by the lamb as neonatal reserves
are rapidly exhausted. The supply to the lamb will be
the product of colostrum composition and yield and
lamb sucking behavior and ingestion. Colostrum yield
was not measured in the present experiment, but our
previous (unpublished) data have shown that the yield
for the 2 breeds is similar. Likewise, other studies suggest that, although differences are apparent between
meat- and milk-type sheep (Pattinson and Thomas,
2004), there are no breed differences in colostrum yield
between breeds of a similar type (Snowder and Glimp,
1991; Pattinson and Thomas, 2004). However, the fat
content of the colostrum of BF ewes was greater than
that in the S and thus, once the lambs had obtained
the colostrum, the BF lambs would have had a greater
nutrient supply for thermoregulation. This may have
contributed to their greater body temperature at 24 h
after birth. In addition, the increase in litter size also
resulted in increased fat content of colostrum as has
been shown before (Snowder and Glimp, 1991), although protein content was reduced in triplet-bearing
ewes. This increase in fat content may have partly compensated larger litter sizes for their reduced intake of
colostrum.
In conclusion, our data show that lambs that are
active at birth (BF lambs and heavier lambs) are better
able to maintain their body temperature than slower
lambs (S lambs and light weight lambs). This may be
partly attributable to behavioral means of thermoregulation, but BF and heavier lambs also have greater
plasma concentrations of T3 and T4, suggesting they
are better able to generate heat, and a better colostral
nutrient supply to fuel thermoregulation. These differences may suggest a causal relationship, where physiological development underpins behavioral competency,
or be related to different degrees of maturity at birth.
Further investigation of neonatal lamb BAT to assess
activity of 5′ deiodinase and UCP would help to determine the relationships of genotype, litter size, and birth
weight with thermoregulatory ability.
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