Theriogenology 63 (2005) 1092–1110

www.journals.elsevierhealth.com/periodicals/the

Breed, litter and parity effects on placental weight

and placentome number, and consequences
for the neonatal behaviour of the lamb
C.M. Dwyer*, S.K. Calvert, M. Farish,
J. Donbavand, H.E. Pickup
Animal Behaviour and Welfare, Sustainable Livestock Systems Group, SAC,
West Mains Road, Edinburgh, EH93JG Scotland, UK
Received 13 March 2004; received in revised form 3 June 2004; accepted 6 June 2004

Abstract

Lamb survival is impaired in low birth weight lambs, and those that are slow to stand and suck.
Many of the factors that influence lamb vigour, such as parity, litter size, and breed, may exert their
effects, at least partially, before birth by influencing placenta development. Our hypothesis was that
retarded lamb behavioural development was due to differences in placentation in these animals. Data
were collected from Blackface and Suffolk lambs in the first 2 h after birth and placentas were
collected when delivered. Suffolk lambs, which were behaviourally slower and had lower rectal
temperatures than Blackface lambs, were associated with larger but less efficient placentas (placental
efficiency defined as foetal weight supported per g placenta) with fewer foetal cotyledons than
Blackface placentas. Triplet lambs were significantly slower than twin or single lambs to suck and
had lower rectal temperatures. Although placenta efficiency increased with litter size, placenta and
cotyledon weight, and cotyledon number increased with twinning but not thereafter. It seemed likely
that triplet lambs suffered some placental insufficiency in comparison to other litter sizes. Lambs
born to first parity mothers were slower to stand and reach the udder than lambs of more experienced
ewes, and first parity ewes also had smaller and less efficient placentas although cotyledon number
was not affected. Male lambs tended to be slower than female lambs for most behaviours, although
rectal temperatures were not affected. The sire of the lamb also influenced lamb behaviour and rectal

* Corresponding author. Present address: Animal Behaviour and Welfare, Sustainable Livestock Systems
Group, SAC, Sir Stephen Watson Building, Bush Estate, Penicuik, Midlothian, EH260PH Scotland, UK.
Tel.: +44 1315353228; fax: +44 1315353121.
E-mail address: c.dwyer@ed.sac.ac.uk (C.M. Dwyer).

0093-691X/$ – see front matter # 2004 Elsevier Inc. All rights reserved.
doi:10.1016/j.theriogenology.2004.06.003
 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110 1093

temperature. Both lamb sex and lamb sire influenced the average weight of placental cotyledons, thus
some of the sire effect on the behaviour and birth weight of his progeny might be mediated through
placental development. Lamb neonatal vigour was correlated with placental efficiency suggesting
that lamb behaviour immediately after birth is related to placental development and function.
# 2004 Elsevier Inc. All rights reserved.

Keywords: Lamb; Neonatal behaviour; Placenta; Breed; Litter; Parity

1. Introduction

Many studies have shown that lamb survival is impaired in low birth weight lambs [1–
7], and in lambs that are slow to stand and suck after [8–11]. Poor lamb vigour is associated
with both environmental factors (e.g. litter size, ewe parity, maternal nutrition: [12,13]) and
genetic effects [11,14–17]. In general, lambs of hill and mountain breeds are quicker to
stand and suck than lowland lambs (e.g. [14]). However, we have also shown that hill and
mountain ewes carry heavier foetuses as a proportion of their own body weight than do
lowland ewes [17]. This suggests that hill ewes are more efficient at partitioning nutrients
to their developing foetuses than lowland animals, and this may function as an adaptation to
deal with the impoverished nutritional conditions encountered in hill environments.
Alternatively, the lowland breeds tend to have received greater artificial selection pressure
for growth characteristics, which may lead the ewes to partition nutrients more to their own
bodily reserves and less to their foetuses. Thus, the apparent breed effect seen in lamb
behaviour might be partially a consequence of altered nutritional partitioning to the foetus.
Similarly, the effects of litter size and ewe parity on lamb behaviour may be a consequence
of inadequate nutrition reaching the foetuses, through placental constraint, even in well-fed
ewes.
In the last third of pregnancy ovine foetal growth is affected by maternal nutrient supply
[18], by uterine blood flow to the placenta [19] and by the placental capacity for nutrient
transport [20]. The weight of the placenta becomes increasingly important in explaining the
variation in foetal weight in late gestation compared to mid pregnancy [21], demonstrating
the importance of placental function for sustaining the growth of the foetus in late
gestation. In addition to its effects on growth rate, placental insufficiency (induced by
carunclectomy of ewes prior to conception) is known to affect the development of the foetal
brain, influencing the development and complexity of brain structures [22]. Placental
insufficiency can lead to a reduction in cell numbers and myelination of axons, and to
decreased synaptogenesis in the hippocampus [23–27]. These effects may be the cause of
the impaired neuromotor development demonstrated in prenatally undernourished young
in several species (sheep: [13]; humans: [28]; rodents: [29–31]; cats: [32]). These studies
show that undernutrition impairs both vigour and the ability to carry out complex
behaviours. Thus, the placenta plays a pivotal role not only in ensuring good foetal
growth in late gestation, but also in the development of the foetal brain, with likely
consequences for neonatal behaviour.
The ovine placenta is polycotyledonary, consisting of placentomes composed of
maternal and foetal tissues where exchange between the maternal and foetal circulations
occurs. Foetal attachment to the uterine wall and the development of foetal cotyledons
1094 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110

occurs at the endometrial thickenings, termed maternal caruncles. Thus, placental

exchange in the ovine placenta is dependent on the number and size of the placentomes,
which may be influenced by both maternal and foetal factors [33]. Foetal growth and the
placental capacity for glucose transport are greatly influenced by the number of caruncles
and the number of placentomes that develop [34–36]. In the present study, as we wished to
record the behaviour of the live neonatal lambs, the placental tissue analysed consisted of
the delivered portion, that is the chorioallantois and its attached foetal cotyledons. Previous
studies [37] have suggested that litter size and weight affect placenta weight and surface
area of cotyledons. We hypothesised that differences in placental development would occur
between breeds, in larger litter sizes or in first parity ewes. If these differences result in
placenta insufficiency then, from the effects described above, this would contribute to the
impaired behaviour seen in lambs born in these groups. Thus, the objective of this study
was to investigate the relationships between placental weight, morphology and efficiency
and lamb behavioural development in the first two hours after birth.

2. Materials and methods

2.1. Animals

The study involved 61 ewes aged between 2 and 4 years over 2 consecutive years. Ewes
were either Scottish Blackface (n = 35) or Suffolk (n = 26) and were pregnant to one of 9
rams (5 Blackface, 4 Suffolk) of the same breed as themselves. All ewes were pregnant by
artificial insemination (AI) and were in parities 1–3. Parity 1 animals were either 2 or 3
years old, parity 2 ewes were 3 or 4 years old and parity 3 ewes were all aged 4 years. Data
were collected from 32 ewes in both years of the study and from 29 ewes in one year only.
There were 38 singleton, 46 twin and 9 triplet pregnancies. The distribution of ewes by
breed, parity and litter size is shown in Table 1. Ewes were weighed and condition scored (a
measurement of relative fat and muscle over the lumbar vertebrae, determined by hand, on
a scale from 0 (emaciated) to 5 (obese)) prior to AI, and then at housing and parturition.
Ewes weighed 53.97  1.05 kg (Blackfaces) and 84.85  1.38 kg (Suffolks) before
pregnancy. Ewes were ultrasonically scanned to determine litter size at mid gestation
(approximately day 70). Ewe condition scores did not differ by breed before conception
and averaged 3.67  0.043. At approximately mid-gestation (January) ewes were brought

Table 1
The distribution of ewes (or placentas) by breed, parity and litter size
Litter size Parity 1 Parity 2 Parity 3 Total
Blackface Suffolk Blackface Suffolk Blackface Suffolk
Single 13 6 10 4 3 2 38
Twin 9 6 13 9 6 3 46
Triplet 0 0 3 5 0 1 9
Total 22 12 26 18 9 6 93
Total (parity) 34 44 15
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indoors into large straw-bedded pens (7 m  7 m), in groups of approximately 10 ewes, and
given access to hay and fresh drinking water ad libitum. Concentrates (ewe nuts, 218 g
crude protein per kg dry matter, energy 12.5 MJ ME/kg dry matter) were provided from
week 14 of gestation, at levels appropriate for the ewe bodyweight, litter size and stage of
gestation. Ewes were vaccinated with a clostridial vaccine (Heptavac, Intervet UK Ltd.) in
week 17. Ewes remained in the lambing pens until 3 days after birth, when they and their
lambs were moved outside to pasture. From approximately one day before the expected
parturition dates, ewes were kept under 24-h surveillance. Ewes were accustomed to the
presence of observers in the walkways between pens in the weeks before parturition, and
were clearly identified by paint-brands to facilitate recognition.

2.2. Data collection

Length of parturition for each ewe was determined as the interval between first
appearance of fluids or membranes at the vulva until full expulsion of the lamb. Birth
was considered to have occurred once the lamb had been expelled beyond the hips, even if
the rest of the lamb’s hind legs had not been fully expelled. This coincided with the last
contraction made by the ewe. After parturition the behavioural progress of the neonatal
lambs to standing and sucking was recorded for the first 2 h after delivery using handheld
Psion Workabout computers running Observer software [38]. The definitions of behaviours
recorded are as in previous studies [12] and given in Table 2. For all lamb neonatal
behaviours, the latency of each behaviour (the time that these behaviours first occurred
after birth) was recorded. If lambs had not achieved a particular behaviour within the 2 h
recording period a value of 2 h was assigned to that latency for the lamb. After 2 h any
lambs that had not sucked were assisted to suck and value of 2 h was recorded for latency to
suck for these animals. Lamb rectal temperatures were recorded at approximately 45 min
after delivery. Lambs were weighed, sexed and crown-rump length measured at 12–24 h
after birth. Relative litter weight (weight of litter/maternal pre-pregnancy body weight) and
lamb ponderal indices (PI: birth weight/crown-rump length3) were calculated for each ewe
and lambs.
Placentas were collected immediately after delivery (approximately 2 h after the birth of
the last lamb) and stored at 4 8C until analysis (within 24 h of delivery). Each placenta was

Table 2
Definitions of behaviours recorded for each lamb
Behaviour Definition
Shakes head Lamb raises and shakes head
To knees Lamb rolls onto chest, gathers legs under it and pushed front half
of the body up off the ground
Attempts to stand Lamb supports body weight on at least one foot
Stands Lamb stands unsupported on all four feet for >5 s
Reaches udder Lamb approaches ewe and nudges her in the udder region
Unsuccessful suck Lamb places head under ewe in contact with the udder but either fails to
grasp the teat or releases it without sucking
Sucks Lamb holds teat in its mouth and appears to be sucking with appropriate mouth
and head movements, may be tail-wagging, remains in this position for >5 s
1096 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110

carefully washed and blotted dry before being weighed. Individual placental cotyledons
were dissected from the chorioallantois and sub-divided by size (small <1 cm diameter;
medium between 1 and 5 cm; large >5 cm). The number and weight of cotyledons in each
size class was recorded. In total 93 placentas were collected and dissected over the two
years. As placentas were collected after delivery (as lamb behavioural data was also
recorded) we were unable to determine placental characteristics per lamb in litters except
for singleton pregnancies. Data are therefore reported for entire litters. Placental efficiency
(defined as gram of lamb produced per gram of placenta) was calculated for each ewe.

2.3. Statistical methods

The effects of ewe age and parity, ewe condition score, litter size, lamb sex, breed and
sire on placental parameters and lamb and litter weights were investigated by using the
restricted maximum likelihood procedure (REML, [39]) as the data were unbalanced with
respect to these effects. These factors were fitted sequentially as fixed effects, as was the
year in which the data was collected, and ewe identity fitted as a random factor as some
ewes appeared in the data set twice. Direct comparisons of the same ewes across parities
were carried out by paired t-tests. Lamb neonatal behavioural latencies were assessed in the
137 lambs with complete behavioural records, and temperature data were analysed for 147
lambs. These data were not normally distributed so were transformed by exponential (lamb
rectal temperature), square root (time for the lamb to suck) or natural logarithm trans-
formations. Data were first checked for linearity by plotting residuals from regression
analyses against the explanatory variables. The data were then analysed by REML using
the same fixed and random factors as for weights and placental parameters but including
lamb birthweight and length of parturition as covariates. In addition, the number of lambs
in various classes that needed assistance to suck was investigated by chi-squared tests. The
relationship between placental parameters, lamb vigour (nlog time to stand) and lamb
temperature were investigated by regression analysis in singleton pregnancies. GenStat
statistical packages were used throughout.

3. Results

3.1. Ewe, lamb and litter weights

Before conception ewe weights were affected by ewe breed and, within each breed, by
parity (mean weight (kg): Blackface: parity 1 = 57.33, parity 2 = 54.15, parity 3 = 49.30,
S.E.D. = 2.90, Wald x2 = 11.40, d.f. = 2, P < 0.005; Suffolk: parity 1 = 87.54, parity 2 =
83.99, parity 3 = 85.91, S.E.D. = 4.07, Wald x2 = 8.12, d.f. = 2, P < 0.05), and ewe age
(mean weight (kg): Blackface: 2 years = 44.04, 3 years = 54.09, 4 years = 62.65, S.E.D. =
2.79, Wald x2 = 27.34, d.f. = 2, P < 0.001; Suffolk: 2 years = 75.11, 3 years = 88.40, 4 years
= 93.93, S.E.D. = 5.42, Wald x2 = 23.31, d.f. = 2, P < 0.001). Within breed, first parity
ewes gained less weight in pregnancy than multiparous ewes (maternal weight gain (kg):
Blackface: parity 1 = 4.55, parity 2 = 5.65, parity 3 = 6.41, S.E.D. = 1.90, Wald x2 = 5.65,
d.f. = 2, P = 0.06; Suffolk: parity 1 = 0.22, parity 2 = 10.42, parity 3 = 13.81, S.E.D. = 4.39,
 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110 1097

Wald x2 = 11.07, d.f. = 2, P < 0.005). Younger ewes had lower condition score (CS) values
before conception (mean CS: 2-year-old ewes = 3.46, 3-year-old ewes = 3.94, 4-year-old
ewes = 3.90, S.E.D. = 0.17, Wald x2 = 9.53, d.f. = 2, P < 0.01), but there was no consistent
effect of ewe parity. There were no significant effects on the amount of CS ewes lost or
gained during gestation.
Lamb birth weight declined by approximately 1 kg for each increase in lamb number in
the litter (Table 3). First parity mothers produced lighter litters than more experienced ewes
(Table 4), and female lambs were lighter than their male counterparts (mean birth weight
(kg): males = 4.46, females = 4.15, S.E.D. = 0.13; Wald x2 = 5.22, d.f. = 1, P < 0.05). In
addition, Blackface lambs were lighter than Suffolk lambs (Table 5). Lamb ponderal
indices (PI) were affected in a similar way by litter size (mean PI: single = 2.68, twin =
2.07, triplet = 1.52, S.E.D. = 0.12, Wald x2 = 82.56, d.f. = 2, P < 0.001), parity (parity 1 =
1.94, parity 2 = 2.08, parity 3 = 2.25, S.E.D. = 0.15, Wald x2 = 7.22, d.f. = 2, P < 0.05) and
breed (Blackface = 2.01, Suffolk = 2.16, S.E.D. = 0.17, Wald x2 = 4.54, d.f. = 1, P < 0.05),
but not by lamb sex.
Litters born were equivalent to the scanned litter size, indicating no foetal mortality
occurred after day 70. Litter size clearly affects total litter weight with an average increase
of 3.34 kg with twins and 5.49 kg with triplets over single litters (Table 3; P < 0.001).
However, litter weight was also affected by ewe age (2-year-old ewes produced lighter
litters than older ewes: 2-year old = 7.69 kg, 3-year old = 8.54, 4-year old = 8.30, S.E.D. =
0.56; Wald x2 = 87.09, d.f. = 2, P < 0.001), ewe parity (Table 4), the gender of the litter (all
male litters heavier than all female or mixed sex litters: litter weights = 8.64, 8.03 and 7.86,
respectively, S.E.D. = 0.28; Wald x2 = 8.72, d.f. = 2, P < 0.05), ewe breed (Table 5) and the
sire of the litter (Wald x2 = 14.01, d.f. = 7, P < 0.05). When litter weight was expressed as a
percentage of the maternal pre-pregnancy bodyweight it appeared that, although younger
ewes carried a relatively heavier litter than older ewes (2-year old = 12.89%, 3-year old =
12.05%, 4-year old = 10.38%, S.E.D. = 0.82, Wald x2 = 28.03, d.f. = 2, P < 0.001),
increasing parity increased the relative litter weight carried by ewes (Table 4). In addition
to their greater absolute weight, all male litters were also relatively heavier than all female

Table 3
The effect of litter size on lamb, litter and placenta weights, and placental components
Single Twin Triplet S.E.D. Test statistic and P
Number of litters 38 46 9
Lamb birthweight (kg) 5.29a 4.39b 3.25c 0.19 Wald x2 = 90.64, d.f. = 2, P < 0.001
a b
Litter weight (kg) 5.08 9.08 11.41c 0.40 Wald x2 = 289.98, d.f. = 2, P < 0.001
Litter weight % ewe weight 8.45a 13.39b 15.24c 0.60 Wald x2 = 173.69, d.f. = 2, P < 0.001
Placenta weight (g) 418.5a 604.1b 519.2ab 58.64 Wald x2 = 30.53, d.f. = 2, P < 0.001
Placental efficiency 12.81a 15.77a 24.74b 1.96 Wald x2 = 20.87, d.f. = 2, P < 0.001
No. cotyledons per placenta 75.28a 90.14b 85.63ab 9.08 Wald x2 = 6.86, d.f. = 2, P < 0.05
Average cotyledon weight (g) 1.67a 1.92b 1.95b 0.16 Wald x2 = 17.44, d.f. = 2, P < 0.001
No. of small cotyledons 19.21 17.56 13.58 3.77 NS
No. of medium cotyledons 50.85a 65.08b 62.06ab 6.81 Wald x2 = 11.59, d.f. = 2, P < 0.005
No. large cotyldeons 2.11a 4.76a 8.35b 1.94 Wald x2 = 13.54, d.f. = 2, P < 0.001
Values are means with pooled standard errors. Within rows values with differing superscripts are significantly
different.
1098 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110

Table 4
The effect of ewe parity on lamb, litter and placenta weights, and placental components
Parity 1 Parity 2 Parity 3 S.E.D. Test statistic and P
Number 34 44 15
Lamb birthweight (kg) 3.95 4.45 4.52 0.23 Wald x2 = 8.31, d.f. = 2, P < 0.05
Litter weight (kg) 7.52a 7.96a 9.06b 0.49 Wald x2 = 21.63, d.f. = 2, P < 0.001
Litter weight % ewe weight 10.28a 11.68b 13.36c 0.72 Wald x2 = 15.07, d.f. = 2, P < 0.001
Placenta weight (g) 400.8a 536.5ab 647.6b 73.11 Wald x2 = 9.61, d.f. = 2, P < 0.01
Placental efficiency 15.02a 17.47ab 20.83b 2.35 Wald x2 = 6.52, d.f. = 2, P < 0.05
No. of cotyledons per placenta 89.75 82.47 78.82 10.80 NS
Average cotyledon weight (g) 1.35a 1.83b 2.26c 0.21 Wald x2 = 12.84, d.f. = 2, P < 0.005
Values are means with pooled standard errors. Within rows values with differing superscripts are significantly
different.

or mixed sex litters (all male: 12.34%, all female: 11.65%, mixed: 11.34%, S.E.D. = 0.42;
Wald x2 = 8.01, d.f. = 2, P < 0.05). Although Suffolk litters were heavier than Blackface
litters, Blackface ewes carried a relatively heavier litter than Suffolk ewes (Table 5). Sire of
the litter also influenced the relative litter weight (Wald x2 = 22.14, d.f. = 7, P < 0.005).

3.2. Placenta weights

Placenta weight tended to be affected by the same factors that influenced litter weight,
although neither the gender nor the sire of the litter had a significant impact on placenta
weight. Placenta weight increased with ewe age (placenta weights (g): 2-year old = 385.1,
3-year old = 518.5, 4-year old = 655.3; S.E.D. = 75.85, Wald x2 = 14.55, d.f. = 2, P < 0.05),
with ewe parity (Table 4) and with twins and triplets over singles (Table 3). However,
placenta weight per lamb declined with each increase in lamb number in the litter (mean
placenta weight per lamb (g): singles: 396.9, twins: 281.4, triplets: 124.0, S.E.D. = 31.98,
Wald x2 = 54.81, d.f. = 2, P < 0.001). The condition score of the ewe before conception, or
at lambing, was also negatively related to placental weight (effect = 15.69 and 56.60 for
before conception and at lambing, Wald x2 = 5.27 and 5.82 respectively, d.f. = 1, P < 0.05

Table 5
The effects of ewe breed on lamb, litter and placenta weights, and placental components
Blackface Suffolk S.E.D. P
Number 57 36
Lamb birth weight (kg) 3.94 4.68 0.24 Wald x2 = 8.04, d.f. = 1, P < 0.001
Litter weight (kg) 7.36 8.99 0.43 Wald x2 = 58.60, d.f. = 1, P < 0.001
Litter weight % ewe weight 13.52 10.02 0.65 Wald x2 = 36.68, d.f. = 1, P < 0.001
Placenta weight (g) 455.9 583.4 68.43 Wald x2 = 28.15, d.f. = 1, P < 0.001
Placental efficiency 19.16 16.39 2.32 Wald x2 = 4.92, d.f. = 1, P < 0.05
No. of cotyledons per placenta 93.53 73.83 10.72 Wald x2 = 4.93, d.f. = 1, P < 0.05
Average cotyledon weight (g) 1.42 2.28 0.19 Wald x2 = 66.53, d.f. = 1, P < 0.001
No. of small cotyledons 22.07 16.30 4.51 Wald x2 = 4.82, d.f. = 1, P < 0.05
No. of medium cotyledons 69.67 48.99 8.04 Wald x2 = 10.64, d.f. = 1, P < 0.001
No. of large cotyledons 1.70 8.46 2.29 Wald x2 = 20.53, d.f. = 1, P < 0.001
Values are means with pooled standard errors.
 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110 1099

Fig. 1. Correlation of placental weight per ewe with the weight of the litter for 93 pregnancies for Blackface (solid
symbols) and Suffolk ewes (open symbols).

for both) although the amount of condition gained or lost by the ewe during pregnancy did
not have an influence on placenta weight. There was a significant effect of ewe breed on
placenta weight, with Suffolk ewes having heavier placentas than Blackface ewes, as with
litter weight (Table 5). There was a significant positive correlation between placenta weight
and litter weight (r2 = 44.6, F1,85 = 70.29, P < 0.001; Fig. 1). Placentas became
increasingly efficient as litter size increased (Table 3). There was no significant effect
of ewe age on placental efficiency, but efficiency increased with increasing parity (Table 4).
The placentas of Blackface ewes were also significantly more efficient than those of
Suffolk ewes (Table 5). There were no other significant effects on placental efficiency.

3.3. Analysis of placental components

There were no significant effects of ewe age or parity (Table 4), gender composition of
the litter or sire of the lamb on the number of placental cotyledons. There was, however, a
significant increase in cotyledon number with twins or triplets over singleton pregnancies
(Table 3), and in Blackface ewes compared to Suffolks (Table 5). Whether the effect of
litter size on the number of cotyledons was due to increased recruitment of caruncles
during placental development in multiple pregnancies was investigated by comparing 11
ewes which gave birth to single and twin litters in consecutive pregnancies. This
demonstrated an increase in cotyledon number in the twin pregnancies over singletons
in the same ewes (mean number of cotyledons: singleton pregnancy = 61.73, twin
pregnancy = 90.91, paired T = 3.39, n = 11, P < 0.01). There was no corresponding
1100 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110

change in 12 animals which gave birth to the same litter size in subsequent parities (mean
number of cotyledons: first recorded pregnancy = 90.42, second = 91.42, paired T = 0.12,
n = 12, NS).
Average cotyledon weight increased with increasing ewe age (average weight (g): 2-
year old = 1.45, 3-year old = 1.89, 4-year old = 2.22, S.E.D. = 0.22, Wald x2 = 12.36, d.f. =
2, P < 0.005) and parity (Table 4). Twin or triplet pregnancies were associated with an
increase in cotyledon weight compared to singleton pregnancies (Table 3). Total cotyledon
weight per lamb, however, declined with each increase in lamb number in the litter (mean
cotyledon weight per lamb (g): singles = 103.66, twins = 74.71, triplets = 40.62, S.E.D. =
11.49, Wald x2 = 28.37, d.f. = 2, P < 0.001). All male litters were associated with heavier
cotyledons than all female litters, mixed sex litters were intermediate (average weight (g):
all male = 1.92, all female = 1.79, mixed = 1.84, S.E.D. = 0.14, Wald x2 = 10.73, d.f. = 2, P
< 0.05). The average weight of cotyledons was also affected by both ewe breed (Table 5)
and the sire of the lamb (Wald x2 = 22.79, d.f. = 7, P < 0.005).
Most changes in average cotyledon weight seemed to be due to a shift in the frequency
of different size classes of cotyledons. Blackface placentas had a higher number of small
and medium sized cotyledons compared to Suffolks, but fewer large cotyledons (Table 5).
Similarly, twin and triplets placentas had greater numbers of medium and large cotyledons
in comparison to singleton placentas (Table 3).

3.4. Lamb neonatal behaviour and thermoregulation

The behaviour of individual lambs was affected predominantly by ewe parity, litter size,
lamb breed and the sire of the lamb, although the importance of these factors varied
depending on the behaviour (see Table 6). There were no significant effects of the length of
parturition on any behavioural latencies. Lamb birth weight had a significant positive effect
only on the time taken by the lamb to reach the udder (Wald x2 = 7.44, d.f. = 1, P < 0.01).
Early righting behaviour, for example the time from birth to the first time the lamb reached
sternal recumbancy and began to develop standing movements (to knees, see Table 2), was
slower in lambs from younger ewes (Table 6). Thereafter, ewe age had no significant effect
on lamb behaviours, although lambs of 4-year-old ewes needed less assistance to suck.
However, lambs of first parity mothers were consistently slower than more experienced
mothers for all other behaviours, except latency to suck (Table 6). The offspring of most
experienced ewes, however, were less likely to require assistance to suck. Twin lambs
tended to be quicker than both single and triplet lambs in their initial behaviours, thereafter
triplet lambs were significantly slower than other litter sizes and fewer of these lambs
sucked unaided. Male lambs compared to female were slower to rise to their knees (mean
latency in minutes (with 95% confidence intervals): males: 6.47 (5.64–7.43); females: 4.75
(4.14–5.45), Wald x2 = 5.59, d.f. = 1, P < 0.05) and tended to be slower to attempt to suck
(mean latency (with 95% confidence intervals): males: 46.05 (41.15–51.52); females:
37.96 (33.93–42.48); Wald x2 = 3.34, d.f. = 1, P = 0.07). Suffolk lambs compared to
Blackface were consistently slower for all behaviours (Table 6), and fewer Suffolk lambs
managed to suck unaided in 2 h compared to Blackface lambs. The sire of the lamb had a
significant influence on most lamb behaviours, particularly those behaviours relating to
sucking requiring co-ordination, and this effect was most pronounced in Suffolks (Table 6).
Table 6
The effect of ewe age, parity, litter size, ewe breed and sire on the latency of neonatal behaviours (in minutes), and on the percentage of lambs sucking unaided within 2 h of
birth
Latencies To knees To stand To reach udder To attempt to suck To suck Percent sucking unaided
(mins from birth)
Ewe age
2-year old 9.78 (7.24–13.23) NS NS NS NS 83.33%
3-year old 4.00 (2.95–5.41) 69.51%

C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110

4-year old 4.35 (3.22–5.88) 90.48%
Wald x2 = 14.59, x2 = 7.40, d.f. = 2,
d.f. = 2, P < 0.001 P < 0.05
Ewe parity
1st parity NS 27.98 (22.27–35.17) 35.68 (25.60–49.74) 67.40 (54.10–83.98) NS 75.61%
2nd parity 20.84 (15.58–26.19) 21.34 (15.31–29.75) 30.65 (24.60–38.19) 71.79%
3rd parity 12.50 (9.94–15.71) 17.44 (12.51–24.31) 35.40 (28.41–44.10) 100%
Wald x2 = 9.76, Wald x2 = 8.67, Wald x2 = 7.84, x2 = 8.54, d.f. = 2,
d.f. = 2, P < 0.01 d.f. = 2, P < 0.05 d.f. = 2, P < 0.05 P < 0.05
Litter size
Single NS 20.08 (16.19–24.90) 23.37 (17.53–31.16) 30.84 (25.04–37.96) 85.23 (71.78–99.83) 88.24%
Twin 17.20 (13.87–21.32) 20.38 (15.29–27.17) 31.97 (25.96–39.36) 97.18 (82.78–112.73) 77.38%
Triplet 21.11 (17.02–26.18 27.90 (20.93–37.20) 74.26 (60.32–91.48) 126.21 (109.72–143.85) 64.00%
Wald x2 = 19.49, Wald x2 = 7.37, Wald x2 = 55.18, Wald x2 = 27.69, x2 = 5.86, d.f. = 2,
d.f. = 2, P < 0.001 d.f. = 2, P < 0.05 d.f. = 2, P < 0.001 d.f. = 2, P < 0.001 P = 0.053
Breed
Blackface 5.11 (3.94–6.63) 14.15 (10.86–18.43) 18.78 (12.94–27.25) 36.26 (28.10–46.78) 94.08 (77.20–112.61) 93.90%
Suffolk 6.01 (4.63–7.80) 26.57 (20.40–34.60) 29.86 (20.58–43.34) 48.21 (37.37–62.21) 110.62 (92.26–130.66) 55.74%
Wald x2 = 2.85, Wald x2 = 27.46, Wald x2 = 12.62, Wald x2 = 18.11, Wald x2 = 12.98, x2 = 29.33, d.f. = 1,
d.f. = 1, P = 0.091 d.f. = 1, P < 0.001 d.f. = 1, P < 0.001 d.f. = 1, P < 0.001 d.f. = 1, P < 0.001 P < 0.001
Sire Wald x2 = 12.96, Wald x2 = 14.17, NS Wald x2 = 19.40, Wald x2 = 15.20, Blackface sires:
d.f. = 7, P = 0.073 d.f. = 7, P < 0.05 d.f. = 7, P < 0.01 d.f. = 7, P < 0.05 88.89%, 86.96%,
100%, 100%, 100%, NS
Suffolk sires: 45.54%,
100%, 66.67%, 44.44%,

1101
x2 = 7.36, d.f. = 3, P = 0.06
Values are means (with 95% confidence intervals).
1102 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110

Fig. 2. Box and whisker plots of lamb rectal temperatures recorded within 1 h of birth showing the variation by (a)
litter size and (b) breed. Values are medians (bar within the box) and upper and lower quartile ranges (borders of
the box) with 5 and 95 percentiles shown as the error bars.

Lamb rectal temperatures were not significantly affected by length of parturition, lamb
birth weight, ewe age or parity, or by lamb sex. Triplet lambs had lower temperatures than
singles or twins (Fig. 2a; Wald x2 = 18.60, d.f. = 2, P < 0.001), and Blackface lambs had
higher temperatures than Suffolk lambs (Fig. 2b; Wald x2 = 18.65, d.f. = 1, P < 0.001). The
sire of the lamb also had a significant impact on the ability of the lamb to maintain rectal
temperature in the first hour after birth (Wald x2 = 15.46, d.f. = 7, P < 0.05). Lamb birth
weight was fitted first in the model (although its effects were not significant), therefore
these effects could not be attributed to birth weight.
 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110 1103

3.5. Relationship of placental components to lamb behaviour

To avoid confounds where the placenta may not have been shared equally between
lambs in multiple litters, the relationship between lamb behaviours and placental compo-
nents was examined in the 38 ewes that gave birth to single lambs. As with litter weight,
there was a significant positive correlation between lamb weight and placenta weight (r2 =
52.2, F1,33 = 34.90, P < 0.001), and between lamb length and placenta weight (r2 = 33.4,
F1,33 = 16.04, P < 0.001). Placenta weight was also correlated with lamb PI (r2 = 50.3, F1,33
= 32.39, P < 0.001).
Placenta weight was the best single predictor of lamb birth weight, however both
average cotyledon weight (r2 = 36.0, F1,33 = 19.46, P < 0.001) and total cotyledon weight
(r2 = 43.0, F1,33 = 25.39, P < 0.001) were also significantly correlated with lamb birth
weight. There was no relationship between placental efficiency or the total number of
cotyledons in the placenta and lamb birth weight.
Placenta weight was positively correlated with the time taken by the lamb to stand after
birth (b = 0.483, r2 = 20.4, F1,27 = 7.93, P < 0.01), as was average cotyledon weight (b =
0.566, r2 = 29.4, F1,27 = 12.26, P < 0.005). Lamb stand latency was also positively
correlated with total cotyledon weight (b = 0.415, r2 = 13.9, F1,26 = 5.19, P < 0.05), that is
the lambs that took longest to stand were associated with the heaviest placentas and
cotyledons. However, lamb time to stand was negatively correlated with placental
efficiency (b = 0.413, r2 = 13.9, F1,27 = 5.35, P < 0.05), demonstrating that lambs
associated with efficient placentas stood more quickly. There was no relationship between
the number of placental cotyledons and lamb behaviour. The placenta variables were better
predictors of lamb behaviour than lamb birth weight, although this was positively
correlated with lamb behaviour (b = 0.393, r2 = 12.3, F1,28 = 4.94, P < 0.05), thus heavy
singleton lambs took longer to stand than lighter weight lambs. There was, however, no
correlation between any measures of the placenta and its components and lamb rectal
temperature, or between lamb birth weight and temperature.

4. Discussion

The relationship between placenta weight and litter and lamb birth weight seen in this
study is similar to previous studies (e.g. [21]). However, the data suggest that differences
exist by breed, litter size and parity in placental morphology and efficiency, which may
have consequences for the neonatal lamb. The behaviours of the neonatal lambs recorded in
this study are similar to our previous results in a different population of lambs [12]. In
summary, lambs are slow to show neonatal behavioural progress if born to first parity
mothers compared to more experienced ewes, if they are triplet lambs compared to singles
or twins, if they are male, if they are Suffolk rather than Blackface and if they are sired by
particular rams. The ability of the newborn lamb to maintain rectal temperature in the first
few hours after birth is also reduced in triplet lambs and Suffolks, and influenced by sire,
but is not affected by ewe parity or by lamb gender.
In common with our previous results [17] the data show that, although Suffolk lambs
and litters are significantly heavier than Blackface in absolute weights, when scaled for the
1104 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110

difference in maternal body size between the breeds Blackface ewes carry a relatively
heavier litter. Blackface ewes appear to be more efficient at transferring nutrients to the
foetus than Suffolk ewes as each gram of Blackface placenta supported a greater foetal
mass than did the placentas of Suffolks. Uteroplacental tissues of ruminants consume up to
70% of glucose taken up by the placenta and foetus [40] and whilst some of this is then
transferred to the foetus as lactate and fructose [41], the fate of a substantial proportion of
this glucose is unknown. The placenta also influences the amount and composition of
amino acids reaching the foetus [40]. Conceivably very large placentas consume relatively
more nutrients, and transfer relatively less to the foetus, than do smaller but more efficient
placentas.
Our data demonstrate that, despite differences in placenta weight, Blackface placentas
contain significantly more foetal cotyledons than do those of Suffolks. A reduced number
of placentomes has been shown to be associated with growth retardation of lambs in studies
where the numbers of caruncles were reduced before mating, with differences in caruncle
occupancy due to seasonal differences or due to the natural variation between ewes
[21,34,36,42]. This difference in cotyledon number by breed, therefore, may be an
explanation for the ability of Blackface ewes to carry relatively heavier lambs than Suffolk
ewes. Whether the differing number of cotyledons is due to breed differences in the number
of uterine caruncles or to differences in caruncle occupancy is unknown. The cotyledons
taken from Suffolk placentas do, however, show evidence of increased growth in
comparison to those of Blackface placentas. The average and total cotyledon weight is
greater in Suffolks, and this seems to be due primarily to an increase in the number of very
large cotyledons. Breed differences in the transport capacity of the placenta, relating both
to expansion in the size of the exchange surface areas and to expression of specific transport
proteins [40], may also exist.
Increasing maternal parity is associated with both absolute and relatively heavier litters
and heavier placentas. Although placental efficiency also increased with increasing parity
there was no increase in the number of foetal cotyledons, unlike the breed differences. The
main reason for the increase in both weight and placental efficiency appeared to be the
increase in cotyledon weight with parity. As ewe age was included in the model these
effects could not be explained by the age and growth stage of the ewe, which has been
shown to have a considerable impact on placentation [43], but were due to the reproductive
maturity of the animals. Several studies have shown that primiparous mothers produce
smaller offspring than multiparae (humans: [44]; sheep: [9,10,45,46]; cattle: [47]), and the
placenta data and maternal weight gain in pregnancy seen in this study are consistent with
these results. In addition, a similar effect of primiparity on placenta and foetal weight, and
on exchange surface area, has been reported in mares [48,49]. Primiparous females show
physiological and neuroendocrinological immaturity in their responses compared to
mothers with previous experience of pregnancy. For example, primiparous mothers have
a lower milk yield and lactation is energetically inefficient [50,51]. The lactational
response to exogenous oestradiol and progesterone is also reduced in nulliparous ewes
compared to ewes that have previously experienced pregnancy [52], and the parturition-
associated elevation of oxytocin in the ovine olfactory bulb is greater in multiparous than
primiparous ewes [53]. Primiparous ewes may also partition nutrients less efficiently to the
gravid uterus than multiparas [54]. Thus reduced growth of the placenta and cotyledons
 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110 1105

may be another example of the immature responsiveness of primiparae to pregnancy. For

many mammals the uterus does not return to its original size following involution after the
first pregnancy, and may remain more vascularised than the nulligravid uterus [55].
Increases in placental weight between primiparous and multiparous ewes, therefore,
may be due to the increased size and vascularisation of the uterus as the placenta develops.
Twinning increased placenta weight, the number of cotyledons per placenta and the
average placenta weight above singleton pregnancies, although there was no additional
increase with triplets. As can be inferred from our data, and shown by Stegeman [55], each
twin or triplet is associated with fewer cotyledons than singles, and triplets fewer than
twins. Placenta efficiency, however, increased with each increase in litter size, and this may
have been achieved by the compensatory increase in large cotyledons in the triplet
pregnancies. However, previous studies have suggested that compensatory increases in
the exchange surface area with triplets are insufficient to meet all the foetal requirements,
particularly in the rapid growth phase of late pregnancy, as the exchange surface area per
foetus declines with litter size [37]. Similarly in our data, although cotyledon weight and
placenta weight increased with litter size, the mass of cotyledons or placenta associated
with each lamb declined markedly with increases in litter size. It is likely, therefore, that
triplet foetuses experience some degree of placental insufficiency in comparison to single
and twin lambs. This may have been due to the inability of triplet foetuses to recruit
sufficient caruncles for cotyledon development. The increase in cotyledon number with
multiple births may arise because ewes with a low number of caruncles in the uterus are
incapable of carrying more than singleton foetuses, or because of differences in cotyledon
recruitment with litter size. Studies of seasonal changes in placentation suggest that
caruncle occupancy can vary between 79 and 88% of available sites [36]. Comparison of
the same ewes with differing litter sizes in consecutive years in the present study
demonstrated that the placentas of the same ewes have a third more foetal cotyledons
with twins than singles. This suggests that increase in caruncle occupancy with increasing
litter size is the most likely explanation for the increase in cotyledon number seen in
pregnancies of twin and triplet litters. Our data suggested that there was no foetal mortality
after mid gestation, although we cannot rule out the possibility that embryo mortality
occurred early in gestation. It is possible that early embryo mortality may alter the
relationship between litter size seen at birth and placental development. However, this
seems unlikely to have played a major role in our results since these concur with other data
on the relationship between litter size and placentation, and suggest an increase in placental
weight and cotyledon number with an increase in foetuses carried to term.
In addition to the substantial effects of breed, parity and litter size on placentation, our
data also demonstrate that both lamb gender and the sire of the lamb can influence lamb
birth weight and cotyledon weight. These effects on lamb birth weight must be pre-
dominantly through the increase in the average weight of cotyledons as placental efficiency
and the numbers of foetal cotyledons were unaffected. As lamb gender and sire influenced
litter weight this suggests a potential mechanism for the increased foetal growth. The effect
of sire on the average weight of foetal cotyledons suggests that, if this is related to an
increased exchange surface area, individual sires can influence the nutrient partitioning of
the mother to their offspring. This concurs with current understanding of the role of
paternally imprinted genes, such as Igf2, acting on placental structure and function [56].
1106 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110

Paternally expressed genes are thought to act in the placenta to influence the supply of
maternal nutrients to the foetus and hence to increase foetal growth [57]. Thus, the effect of
sire on placental development and litter weight seen here may be mediated via individual
differences in paternally imprinted genes.
Placental insufficiency (induced experimentally) is known to cause a number of deficits
in the foetal brain, including decreased neuronal numbers and connections in the
hippocampus and cerebellum [22,27] and reduced myelination and synaptogenesis at
term [58,59]. These deficits are believed to have functional consequences for the newborn,
particularly affecting neurological processing and behaviour [27,59,60]. Thus, we specu-
lated that naturally occurring variation in placental sufficiency and function, as seen in the
current study, may be associated with behavioural deficits in newborn lambs. The
behavioural data demonstrate that triplet lambs are clearly compromised in comparison
with single or twin lambs, and this is most evident in the more co-ordinated behaviours of
finding the udder and sucking. In addition, triplet lambs have lower rectal temperatures
than singles or twins, which was in addition to any influence of their lower birth weight.
The placenta data support the hypothesis that behavioural impairments in triplet lambs are
due to the inability of the placenta to transport adequate nutrients to triplet lambs in late
gestation, resulting in brain function deficits [22] that have behavioural consequences for
the newborn lamb. In addition, foetal adipose tissue development has been shown to be
very sensitive to nutritional manipulations in late gestation [61]. Lambs associated with
light placenta and cotyledon weights had less adipose tissue, smaller organ weights and
were less able to maintain body temperature in a cold environment [62]. Thus, the lower
temperatures of the triplet lambs may also be a consequence of placental insufficiency in
late gestation, particularly affecting their ability to show non-shivering thermogenesis.
Lambs born to first parity ewes also showed behavioural deficits in comparison to the
lambs of older ewes, as we have previously demonstrated [12], although their ability to
maintain temperature after birth was unaffected. Suffolk lambs were considerably slower
than Blackface lambs, and also had a reduced ability to maintain rectal temperatures after
birth. Some of the behavioural deficits, particularly udder seeking and sucking, may have
been influenced by variation in maternal care as both first parity ewes and Suffolks are
known to show a greater degree of moving away as the lambs attempt to suck [17,46].
Additionally genetic differences in lamb responses may exist that are unrelated to prenatal
development. However, the placental data suggest that, as differences in placental
efficiency and morphology exist by both breed and parity, prenatal mechanisms relating
to placental insufficiency may also be operating.
The direct comparison between placenta variables and lamb behaviour must necessarily
be treated as a pilot study as this data set only included singleton lambs, and thus ignored
some of the categories where lamb behaviour is affected, particularly triplet lambs. With
the need to collect behavioural data from live lambs, however, in order to address our
hypothesis, it was not possible to determine placental characteristics associated with each
lamb within larger litters. However, the data from singleton lambs did reveal a relationship
between placental efficiency and lamb vigour. Thus, the ability of the placenta to transfer
nutrients to the developing foetus in late gestation may influence brain development and
functional behaviour at birth. Measures of placenta weight and lamb weight were, however,
negatively related to lamb vigour. Lamb birth weight is known to have a U-shaped
 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110 1107

relationship with lamb behavioural progress at birth, and a heavy birth weight has an
indirect effect on lamb behaviour through its influence on length of labour and birth
difficulty [12]. Thus, it is possible that the negative relationship between placenta weight
and lamb vigour reflected longer labour in heavy birth weight lambs.
In conclusion, our data show significant differences in placental morphology with breed,
parity and litter size, which partially reflect variations in neonatal lamb behaviour. The data
from multiple litters supports the idea that triplet lambs are behaviourally slow and show
poor homeothermy because of prenatal compromise, through placental insufficiency, that
may have impaired neurological development. These effects appear to be in addition to any
impact of placental function on birth weight. Lambs born to first parity mothers, and
Suffolk lambs compared to Blackface lambs, are also behaviourally slow and show
evidence of altered placental development. Suffolk lambs, which also showed reduced
rectal temperatures, were associated with placentas with fewer cotyledons and with
reduced placental efficiency, which from the analysis of single lamb data, appeared to
be correlated with poor lamb postnatal vigour. The slower behaviour of the lambs of first
parity mothers may have been due to the immature reproductive responsiveness of
primiparae affecting placental growth. However, there is likely to be an additional impact
on lamb behaviour from maternal care, particularly immature responses to lamb sucking
behaviour, which is known to occur with primiparous ewes. Finally the data demonstrate a
genetic effect on cotyledon growth through the impact of different sires on cotyledon
weights. As sire identity also influences the behaviour of their offspring, this suggests that
part of this mechanism may occur prenatally through its effect on placental growth and
hence nutrient transfer to the foetus.

Acknowledgements

The authors thank Simon Cotham and Joan Chirnside for technical assistance during the
project, Mark Ramsay and Alex Moir for animal husbandry and Dr. Linda Mitchell for
helpful discussions about the placental analysis. This study was supported by the Scottish
Executive Environment and Rural Affairs Department.

References

[1] Dalton DC, Knight TW, Johnson DL. Lamb survival in sheep breeds on New Zealand hill country. New Zeal
J Agric Res 1980;23:167–73.
[2] Hinch GN, Kelly RW, Owens JL, Crosbie SF. Patterns of lamb survival in high fecundity Booroola flocks. In:
Proceedings of the New Zealand Society of Animal Production, vol. 43. 1983. p. 29–32.
[3] Elving L, Grommers FJ, van Eldik P. Parturition difficulties and perinatal mortality in Texel and Milksheep.
In: Factors affecting the survival of newborn lambs. A seminar in the CEC programme of coordination of
agricultural research held in Brussels; 1985. p. 115–22.
[4] Lindsay DR, Nowak R, Putu IG, McNeill D. Behavioural interactions between the ewe and her young at
parturition: A vital step for the lamb. In: Reproductive physiology of merino sheep – concepts and
consequences. University of Western Australia, Perth, 1990. p. 191–205.
[5] Gama LT, Dickerson GE, Young LD, Leymaster KA. Effects of breed, heterosis, age of dam, litter size, and
birth weight on lamb mortality. J Anim Sci 1991;69:2727–43.
1108 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110

[6] Yapi CV, Boylan WJ, Robinson RA. Effect of genetic and environmental factors on lamb mortality. World
Rev Anim Prod 1992;27:35–41.
[7] Fogarty NM, Hopkins DL, van de Ven R. Lamb production from diverse genotypes 1. Lamb growth and
survival and ewe performance. Anim Sci 2000;70:135–45.
[8] Alexander G. Behaviour of newly born lambs. Proc Aust Soc Anim Prod 1958;2:123–5.
[9] Owens JL, Bindon BM, Edey TN, Piper LR. Behaviour at parturition and lamb survival of Booroola Merino
sheep. Livest Prod Sci 1985;13:359–72.
[10] Cloete SW... Observations on neonatal progress of Dormer and South African Mutton Merino lambs. South
Afr J Anim Sci 1993;23:38–42.
[11] Dwyer CM, Lawrence AB, Bishop SC. Effects of selection for lean tissue content on maternal and neonatal
lamb behaviours in Scottish Blackface sheep. Anim Sci 2001;72:555–71.
[12] Dwyer CM. Behavioural development in the neonatal lamb: effect of maternal and birth-related factors.
Theriogenology 2003;59:1027–50.
[13] Dwyer CM, Lawrence AB, Bishop SC, Lewis M. Ewe-lamb bonding behaviours at birth are affected by
maternal undernutrition in pregnancy. Br J Nutr 2003;89:123–36.
[14] Slee J, Springbett A. Early postnatal behaviour in lambs of ten breeds. Appl Anim Behav Sci 1986;15:229–
40.
[15] Dwyer CM, Lawrence AB, Brown HE, Simm G. Effect of ewe and lamb genotype on gestation length,
lambing ease and neonatal behaviour in lambs. Reprod Fertil Dev 1996;8:1123–9.
[16] Cloete SWP. Scholtz AJ. Lamb survival in relation to lambing and neonatal behaviour in medium wool
Merino lines divergently selected for multiple rearing ability. Aust J Exp Agric 1998;38:801–11.
[17] Dwyer CM, Lawrence AB. Variability in the in expression of maternal behaviour in primiparous sheep:
effects of genotype and litter size. Appl Anim Behav Sci 1998;58:311–30.
[18] Mellor DJ. Nutritional and placental determinants of foetal growth rate in sheep and consequences for the
newborn lamb. Br Vet J 1983;139:307–24.
[19] Lang U, Baker RS, Braems G, Zygmunt M, Kunzel W, Clark KE. Uterine blood flow—a determinant of fetal
growth. Eur J Obstet Gynaecol Reprod Biol 2003;110:S55–61.
[20] Bell AW. Consequences of severe heat stress for fetal development. Amsterdam: Elsevier; 1987.
[21] Greenwood PL, Slepetis RM, Bell AW. Influences on fetal and placental weights during mid to late gestation
in prolific ewes well nourished throughout pregnancy. Reprod Fertil Dev 2000;12:149–56.
[22] Rees S, Mallard C, Breen S, Stringer M, Cock M, Harding R. Fetal brain injury following prolonged
hypoxemia and placental insufficiency: a review. Compar Biochem Physiol 1998;653–60.
[23] Morgane PJ, Austin-LaFrance R, Bronzino J, Tonkiss J, Diaz-Cintra S, Cintra L, Kemper T, Galler JR.
Prenatal malnutrition and development of the brain. Neurosci Biobehav Rev 1993;17:91–128.
[24] Rees S, Bocking AD, Harding R. Structure of the fetal sheep brain in experimental growth retardation. J Dev
Physiol 1988;10:211–25.
[25] Rees S, Harding R. The effects of intrauterine growth retardation on the development of the Purkinje cell
dendritic tree in the cerebellar cortex of fetal sheep: a note on he ontogeny of the Purkinje cell. Int J Dev
Neurosci 1988;6:461–9.
[26] Dauncey MJ. Bicknell RJ Nutrition and neurodevelopment: mechanisms of developmental dysfunction and
disease in later life. Nutr Res Rev 1999;12:231–53.
[27] Mallard C, Loeliger M, Copolov D, Rees S. Reduced number of neurons in the hippocampus and the
cerebellum in the postnatal guinea-pig following intrauterine growth-restriction. Neuroscience
2000;100:327–33.
[28] Grantham-McGregor SM, Walker SP, Chang S. Nutritional deficiencies and later behavioural development.
Proc Nutr Soc 2000;59:47–54.
[29] Hsueh AM, Simonson M, Hanson HM, Chow BF. Protein supplementation to pregnant rats during third
trimester and the growth and behaviour of offspring. Nutr Rep Int 1974;9:31–45.
[30] Bush M, Leatherwood PD. Effect of different regimens of early malnutrition on behavioural development
and adult avoidance learning in Swiss white mice. Br J Nutr 1975;33:373–85.
[31] Gramsbergen A, Westerga J. Locomotor development in undernourished rats. Behav Brain Res 1992;48:57–64.
[32] Smith BA, Jansen GR. Maternal undernutrition in the feline: behavioural sequelae. Nutr Rep Int 1997;16:
513–526.
 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110 1109

[33] Alexander G. Studies on the placenta of the sheep (ovis aries): placental size. J Reprod Fertil 1964;7:289–
305.
[34] Alexander G. Studies on the placenta of the sheep (ovis aries): effect of surgical reduction in the number of
caruncles. J Reprod Fertil 1964;7:307–22.
[35] Owens JA, Falconer J, Robinson JS. Effect of restriction of placental growth on fetal and utero-placental
metabolism. J Dev Physiol 1987;9:225–38.
[36] Jenkinson CMC. Peterson SW, Mackenzie DDS. McDonald MF, McCutcheon SN. Seasonal effects on birth
weight in sheep are associated with changes in placental development. New Zeal J Agric Res 1995;38:337–
45.
[37] Kaulfuss KH, Schramm D, Berttram M. Effects of genotype, dams age, litter size, birth weight and ram on
morphological parameters of the placenta in sheep. Deutsche Tierarztliche Wochenschrift 2000;107:269–75.
[38] Noldus LPJJ. Trienes RJH. Hendriksen AHM. Jansen H, Jansen RG. The Observer Video-Pro: new software
for the collection, management, and presentation of time-structured data from videotapes and digital media
files. Behav Res Methods Instrum Comput 2000;32:197–206.
[39] Patterson HD, Thompson R. Recovery of inter-block information when block sizes are unequal. Biometrika
1971;58:545–54.
[40] Bell AW, Ehrhardt RA. Regulation of placental nutrient transport and implications for foetal growth. Nutr
Res Rev 2002;15:130–211.
[41] Aldoretta PW, Hay WW. Effect of glucose supply on uteroplacental glucose metabolism. Am J Physiol
1999;277:R947–958.
[42] Robinson JS, Kingston EJ, Jones CT, Thorburn GD. Studies on experimental growth retardation in sheep.
The effect of removal of endometrial caruncles on fetal size and metabolism. J Dev Physiol 1979;1:379–98.
[43] Wallace, JM. Nutrient partitioning during pregnancy: adverse gestational outcome in overnourished
adolescent dams. Proc Nutr Soc 2000;59:107–17.
[44] Goldstein H. Factors related to birth weight and perinatal mortality. Br Med Bull 1981;37:259–64.
[45] Smith GM. Factors affecting birth weight, dystocia and preweaning survival in sheep. J Anim Sci
1977;44:745–53.
[46] Dwyer CM, Lawrence AB. Maternal behaviour in domestic sheep (Ovis aries): constancy and change with
maternal experience. Behaviour 2000;137:1391–413.
[47] Bellows RA, Short RE, Richardson GV. Effects of sire, age of dam and gestation feed level on dystocia and
postpartum reproduction. J Anim Sci 1982;55:18–27.
[48] Wilsher S, Allen WR. The influence of maternal size, age and parity on placental and fetal development in
the horse. Theriogenology 2002;58:833–5.
[49] Wilsher S, Allen WR. The effects of maternal age and parity on placental and fetal development in the mare.
Eq Vet J 2003;35:476–83.
[50] Doreau M, Boulot S, Martin-Rosset W. Effects of parity and physiological state on intake, milk production
and blood parameters in lactating mares differing in body size. Anim Prod 1991;53:111–8.
[51] Kunkele J, Kenagy GJ. Inefficiency of lactation in primiparous rats: the costs of first reproduction. Physiol
Zool 1997;70:571–7.
[52] Dwyer CM, Lawrence AB. Induction of maternal behaviour in non-pregnant, hormone-primed ewes. Anim
Sci 1997;65:403–8.
[53] Lévy F, Kendrick KM, Goode JA, Guevara-Guzman R, Keverne EB. Oxytocin and vasopressin release in the
olfactory bulb of parturient ewes—changes with maternal experience and effects of acetylcholine, K-butyric
acid, glutamate, and noradrenaline release. Brain Res 1995;669:197–206.
[54] Kelly RW, Speijers EJ, Ralph IG, Newnham JP. Lambing performances and wool production of maiden and
adult Merino ewes fed different amounts of lupin seed in mid-pregnancy. Aust J Agric Res 1992;43:339–54.
[55] Stegeman JH... Placental development in the sheep and its relationship to fetal development. Bijdragen tot de
Dierkunde 1974;44:1–72.
[56] Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet 2001;2:
21–32.
[57] Constãncia M, Hemberger M, Hughes J, Dean W, Ferguson-Smith A, Fundele R, Stewart F, Kelsey G,
Fowden A, Sibley C, Reik W. Placenta-specific IGF-II is a major modulator of placental and fetal growth.
Nature 2002;417:945–8.
1110 C.M. Dwyer et al. / Theriogenology 63 (2005) 1092–1110

[58] Rees S, Harding R. Effects of experimentally induced placental insufficiency on prenatal brain development.
Dev Brain Dysfunc 1995;8:152–65.
[59] Mallard EC, Rees S, Stringer M, Cock ML, Harding R. Effects of chronic placental insufficiency on brain
development in fetal sheep. Pediat Res 1998;43:262–70.
[60] Rees S, Breen S, Loeliger M, McCrabb G, Harding R. Hypoxemia near mid-gestation has long-term effects
on fetal brain development. J Neuropathol Exp Neurol 1999;58:932–45.
[61] Budge H, Dandrea J, Mostyn A, Evens Y, Watkins R, Sullivan C, Ingleton P, Stephenson T, Symonds ME.
Differential effects of fetal number and maternal nutrition in late gestation on prolactin receptor abundance
and adipose tissue development in the neonatal lamb. Pediat Res 2003;53:302–8.
[62] Clarke L, Yakubu DP, Symonds ME. Influence of maternal bodyweight on size, conformation and survival of
newborn lambs. Reprod Fertil Dev 1997;9:509–14.