The effect of periconceptional undernutrition of sheep on
the cognitive/emotional response and oocyte quality of
offspring at 30 days of age
J. A. Abecia
1
*, A. Casao
2
, M. Pascual-Alonso
1
, S. Lobón
1
, L. A. Aguayo-Ulloa
1
, A. Meikle
3
, F. Forcada
1
, C. Sosa
4
,
R. H. Marín
5
, M. A. Silva
1
and G. A. Maria
1
1
Dept de Producción Animal y Ciencia de los Alimentos, Facultad de Veterinaria, Zaragoza, Spain
2
Depart de Bioquímica y Biología Molecular y Celular, Facultad de Veterinaria, Zaragoza, Spain
3
Laboratorio de Técnicas Nucleares, Universidad de la República, Montevideo, Uruguay
4
Dept de Anatomía Patológica, Medicina Legal y Forense y Toxicología, Universidad de Zaragoza, Facultad de Veterinaria, Zaragoza, Spain
5
Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de Córdoba, Argentina
Maternal periconceptional undernutrition is associated with altered development and increased risks of adverse outcomes in the offspring.
This circumstance is normal in flocks under extensive farming systems, which depend on natural forage resources. The aim of this study was to
determine the effect of periconceptional undernutrition in sheep on behavioral and reproductive aspects of the offspring. Eighty ewes were
synchronized in estrus and allocated to two groups (n = 40) to be fed diets that provided 1.5 (C) or 0.5 (L) times the requirements for
maintenance. Ewes were mated and 7 days later fed the control diet until lambing. One month after lambing, 32 lambs were exposed to tests to
determine their cognitive and emotional responses. Six ewe lambs were euthanized and in vitro maturation and fertilization procedures were
performed. L ewes presented a significant reduction in prolificacy and fecundity (P < 0.05) in comparison with C ewes. Mean LW at lambing of
L lambs was significantly higher than C lambs (C: 3.80 ± 0.11; L: 4.24 ± 0.15 kg, P < 0.05). Lambs born from C ewes spent more time walking
than L lambs (P < 0.05) in the isolation test, revealing a decrease in the locomotor activity of lambs born from undernourished ewes around
conception. Ewe lambs from the undernourished ewes presented a total population of oocytes 2.3 times higher than ovaries from control ewe
lambs (60.0 ± 7.8 v. 140.0 ± 18.5 oocytes; P < 0.05). In conclusion, periconceptional undernutrition is able to produce an increment in the body
weight and the oocyte population, and an alteration of the locomotor activity of the offspring.
Received 31 October 2013; Revised 4 December 2013; Accepted 10 January 2014; First published online 11 February 2014
Key words: offspring, periconceptional, sheep, undernutrition
Introduction
The expression ‘developmental programming’ is described as
the programming of various bodily systems and processes by a
stressor of the maternal system during pregnancy or during the
neonatal period.
1
It has also been termed as ‘Fetal Program-
ming’, ‘The Barker Hypothesis’, or ‘developmental origins of
health and disease’.
2
The effects of this process are evident at
the offspring level in changes in litter size, sex ratios, fetal or
neonatal development, and in key organ systems and functions,
especially reproductive capacity, health and behavior.
3
One
of these stressors is maternal nutrition, especially around
conception, which is known as the ‘periconceptional period’. In
a recent review,
4
it has been indicated that maternal peri-
conceptional undernutrition is related to altered development
and an enlarged danger of adverse neurodevelopmental and
metabolic consequences in childhood and later life, suggesting
that environmental signals acting during early development may
result in epigenetic changes, which may play a role in the rela-
tionship between early life vulnerability and adult phenotype.
The importance of nutrition during certain windows of physio-
logical processes, in the context of the livestock industry, have led
to create the term ‘focus feeding’, which is based on using short
periods of nutritional supplements that are precisely timed and
specifically designed for stages of the reproductive process.
5
The accessibility to pasturage resources in a particular year can
produce situations of deprivation and subnutrition, a circum-
stance that is normal in sheep flocks under extensive farming
systems such as those found in the Mediterranean area that
extensively rely on natural forage resources. It has been widely
demonstrated that undernutrition affects sheep reproduction,
6
so that together with season, undernutrition becomes one of
the main environmental factors affecting lamb production.
Maternal undernutrition around conception has numerous
effects on several aspects of the physiology of offspring. A low
level of nutrition from -45 days to 6 days after conception is
sufficient to change the amount of key factors regulating cardiac
growth and metabolism and this may increase the capacity to
develop cardiovascular diseases in later life,
7
or cause a suppres-
sion of the pituitary glucocorticoid receptor expression at the end
*Address for correspondence: J. A. Abecia, Departamento de Producción
Animal y Ciencia de los Alimentos, Facultad de Veterinaria, Miguel Servet,
177, 50013 Zaragoza, Spain.
(Email alf@unizar.es)
Journal of Developmental Origins of Health and Disease (2014), 5(2), 79–87.
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2014
ORIGINAL ARTICLE
doi:10.1017/S2040174414000051