Hostname: page-component-76fb5796d-45l2p Total loading time: 0 Render date: 2024-04-26T09:45:18.676Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of periconceptional undernutrition of sheep on the cognitive/emotional response and oocyte quality of offspring at 30 days of age

Published online by Cambridge University Press:  11 February 2014

J. A. Abecia ,
A. Casao ,
M. Pascual-Alonso ,
S. Lobón ,
L. A. Aguayo-Ulloa ,
A. Meikle ,
F. Forcada ,
C. Sosa ,
R. H. Marín  and
M. A. Silva
...Show all authors
J. A. Abecia*
Affiliation:
Dept de Producción Animal y Ciencia de los Alimentos, Facultad de Veterinaria, Zaragoza, Spain
A. Casao
Affiliation:
Depart de Bioquímica y Biología Molecular y Celular, Facultad de Veterinaria, Zaragoza, Spain
M. Pascual-Alonso
Affiliation:
Dept de Producción Animal y Ciencia de los Alimentos, Facultad de Veterinaria, Zaragoza, Spain
S. Lobón
Affiliation:
Dept de Producción Animal y Ciencia de los Alimentos, Facultad de Veterinaria, Zaragoza, Spain
L. A. Aguayo-Ulloa
Affiliation:
Dept de Producción Animal y Ciencia de los Alimentos, Facultad de Veterinaria, Zaragoza, Spain
A. Meikle
Affiliation:
Laboratorio de Técnicas Nucleares, Universidad de la República, Montevideo, Uruguay
F. Forcada
Affiliation:
Dept de Producción Animal y Ciencia de los Alimentos, Facultad de Veterinaria, Zaragoza, Spain
C. Sosa
Affiliation:
Dept de Anatomía Patológica, Medicina Legal y Forense y Toxicología, Universidad de Zaragoza, Facultad de Veterinaria, Zaragoza, Spain
R. H. Marín
Affiliation:
Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de Córdoba, Argentina
M. A. Silva
Affiliation:
Dept de Producción Animal y Ciencia de los Alimentos, Facultad de Veterinaria, Zaragoza, Spain
G. A. Maria
Affiliation:
Dept de Producción Animal y Ciencia de los Alimentos, Facultad de Veterinaria, Zaragoza, Spain
*
*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)
Get access Rights & Permissions [Opens in a new window]

Abstract

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.

Keywords

offspringpericonceptionalsheepundernutrition
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 5 , Issue 2 , April 2014 , pp. 79 - 87
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Reynolds, LP, Borowicz, PP, Caton, JS, et al. Developmental programming: the concept, large animal models, and the key role of uteroplacental vascular development. J Anim Sci. 2010; 88, 61–72.CrossRefGoogle ScholarPubMed
2. Caton, JS, Hess, BW. Maternal plane of nutrition: impacts on fetal outcomes and postnatal offspring responses. Invited Review. In Proceedings of 4th Grazing Livestock Nutrition Conference (eds. Hess W, Delcurto T, Bowman JGP, Waterman RC), 2010; pp. 104–122. West Sect Am Soc Anim Sci, Champaign, IL.Google Scholar
3. Ashworth, CJ, Toma, LM, Hunter, MG. Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability. Phil Trans R Soc B. 2009; 364, 3351–3361.CrossRefGoogle ScholarPubMed
4. Bloomfield, FH. Epigenetic modifications may play a role in the developmental consequences of early life events. J Neurodev Disord. 2011; 3, 348–355.CrossRefGoogle ScholarPubMed
5. Martin, GB, Rodger, J, Blache, D, et al. Nutritional and environmental effects on reproduction in small ruminants. Reprod Fertil Dev. 2004; 16, 491–501.CrossRefGoogle ScholarPubMed
6. Forcada, F, Abecia, JA. The effect of nutrition on the seasonality of reproduction in ewes. Reprod Nutr Dev. 2006; 46, 355–365.CrossRefGoogle ScholarPubMed
7. Lie, S, Sim, M, McMillen, IC, et al. Maternal undernutrition around the time of conception and embryo number each impact on the abundance of key regulators of cardiac growth and metabolism in the fetal sheep heart. J Dev Orig Health Dis. 2013; 4, 377–390.CrossRefGoogle ScholarPubMed
8. Zhang, S, Williams-Wyss, O, MacLaughlin, SM, et al. Maternal undernutrition during the first week after conception results in decreased expression of glucocorticoid receptor mRNA in the absence of GR exon 17 hypermethylation in the fetal pituitary in late gestation. J Dev Orig Health Dis. 2013; 4, 391–401.CrossRefGoogle ScholarPubMed
9. Rae, MT, Palassio, S, Kyle, CE, et al. Effect of maternal undernutrition during pregnancy on early ovarian development and subsequent follicular development in sheep fetuses. Reproduction. 2001; 122, 915–922.CrossRefGoogle ScholarPubMed
10. Donovan, EL, Hernandez, CE, Matthews, LR, et al. Periconceptional undernutrition in sheep leads to decreased locomotor activity in a natural environment. J Dev Orig Health Dis. 2013; 4, 296–299.CrossRefGoogle Scholar
11. Hernandez, CE, Matthews, LR, Oliver, MH, Bloomfield, FH, Harding, JE. Effects of sex, litter size and periconceptional ewe nutrition on offspring behavioural and physiological response to isolation. Physiol Behav. 2010; 101, 588–594.CrossRefGoogle ScholarPubMed
12. Oliver, MH, Bloomfield, FH, Jaquiery, AL, et al. Periconceptional undernutrition suppresses cortisol response to arginine vasopressin and corticotropin-releasing hormone challenge in adult sheep offspring. J Dev Orig Health Dis. 2012; 3, 52–58.CrossRefGoogle ScholarPubMed
13. Mitchell, LM, Robinson, J, Watt, RG, et al. Effects of cobalt/vitamin B12 status in ewes on ovum development and lamb viability at birth. Reprod Fertil Dev. 2007; 19, 553–562.CrossRefGoogle ScholarPubMed
14. Erhard, HW, Boissy, A, Rae, MT, et al. Effects of prenatal undernutrition on emotional reactivity and cognitive flexibility in adult sheep. Behav Brain Res. 2004; 151, 25–35.CrossRefGoogle ScholarPubMed
15. Forcada, F, Abecia, JA, Sierra, I. Seasonal changes in oestrous activity and ovulation rate in Rasa Aragonesa ewes maintained at two different body condition levels. Small Rumin Res. 1992; 8, 313–324.CrossRefGoogle Scholar
16. Russel, AJF, Doney, JM, Gunn, RG. Subjective assessment of body fat in live sheep. J Agric Sci. 1969; 72, 451–454.CrossRefGoogle Scholar
17. Marín, RH, Arce, A, Martijena, ID. T-maze performance and body weight relationship in broiler chicks. Appl Anim Behav Sci. 1997; 55, 197–205.CrossRefGoogle Scholar
18. Gilbert, DT. Thinking lightly about others: automatic components of the social inference process. In Unintended Thought (eds. Uleman JS, Bargh JA), 1989; pp. 189– 211. Guilford: New York.Google Scholar
19. Marin, RH, Arce, A. Benzodiazepine receptors increase induced by stress and maze-learning performance in chick forebrain. Pharmacol Biochem Behav. 1996; 53, 581–584.CrossRefGoogle ScholarPubMed
20. Ortiz-Plata, C, De Lucas-Tron, J, Miranda-de la Lama, GC. Breed identity and leadership in a mixed flock of sheep. J Vet Behav. 2012; 7, 94–98.CrossRefGoogle Scholar
21. Briefer, EF, McElligott, AG. Social effects on vocal ontogeny in an ungulate, the goat (Capra hircus). Anim Behav. 2012; 83, 991–1000.CrossRefGoogle Scholar
22. Langbein, J. Investigations on training, recall and reversal learning of a Y-maze by dwarf goats (Capra hircus): the impact of lateralization. Behav Process. 2012; 89, 304–310.CrossRefGoogle Scholar
23. Forcada, F, Buffoni, A, Abecia, JA, et al. Maximising embryo production in endangered sheep breeds: in vitro procedures that complement in vivo techniques. J App Anim Res. 2011; 39, 412–417.CrossRefGoogle Scholar
24. Chacón, G, Garcia-Belenguer, S, Illera, JC, Palacio, J. Validation of an EIA technique for the determination of salivary cortisol in cattle. Spanish J Agric Res. 2004; 2, 45–51.CrossRefGoogle Scholar
25. Kelly, JM, Kleemann, DO, Walker, SK. The effect of nutrition during pregnancy on the in vitro production of embryos from resulting lambs. Theriogenology. 2005; 63, 2020–2031.CrossRefGoogle ScholarPubMed
26. Borwick, SC, Rhind, SM, McMillen, SR, Racey, PA. Effect of undernutrition of ewes from the time of mating on fetal ovarian development in mid gestation. Reprod Fertil Dev. 1997; 9, 711–715.CrossRefGoogle ScholarPubMed
27. Sosa, C, Abecia, JA, Forcada, F, et al. Effect of undernutrition on uterine progesterone and oestrogen receptors and on endocrine profiles during the ovine oestrous cycle. Reprod Fertil Dev. 2006; 18, 447–458.CrossRefGoogle ScholarPubMed
28. Sosa, C, Abecia, JA, Carriquiry, M, et al. Early pregnancy alters the metabolic responses to restricted nutrition in sheep. Domest Anim Endocrinol. 2009; 36, 13–23.CrossRefGoogle ScholarPubMed
29. Abecia, JA, Forcada, F, Palacín, I, et al. Undernutrition affects embryo quality of superovulated ewes. Zygote. 2013; doi:10.1017/S096719941300035X.CrossRefGoogle Scholar
30. Bispham, J, Gopalakrishnan, GS, Dandrea, J, et al. Maternal endocrine adaptation throughout pregnancy to nutritional manipulation: consequences for maternal plasma leptin and cortisol and the programming of fetal adipose tissue development. Endocrinology. 2003; 144, 3575–3585.CrossRefGoogle ScholarPubMed
31. Gardner, DS, Tingey, K, Van Bon, BWM, et al. Programming of glucoseinsulin metabolism in adult sheep after maternal nutrition. Am J Physiol Regul Integr Comp Physiol. 2005; 289, 947–954.CrossRefGoogle Scholar
32. Ford, SP, Hess, BW, Schwope, MM, et al. Maternal undernutrition during early to mid- gestation in the ewe results in altered growth, adiposity, and glucose tolerance in male offspring. J Anim Sci. 2007; 85, 1285–1294.CrossRefGoogle ScholarPubMed
33. Jaquiery, AL, Oliver, MH, Honeyfield-Ross, M, et al. Periconceptional undernutrition in sheep affects adult phenotype only in males. J Nutr Metab. 2012; 2012, 123610.Google Scholar
34. Young, LE, Sinclair, KD, Wilmut, I. Large offspring syndrome in cattle and sheep. Rev Reprod. 1998; 3, 155–163.CrossRefGoogle ScholarPubMed
35. Wilmut, I, Sales, DI, Ashworth, CJ. Physiological criteria for embryo mortality: is asynchrony between embryo and ewe a significant factor? In Genetics of Reproduction in Sheep (eds. Land RB, Robinson DW), 1985; pp. 275–289. Butterworths: London.CrossRefGoogle Scholar
36. Walker, SK, Hartwich, KM, Seamark, RF. The production of unusually large offspring following embryo manipulation: concepts and challenges. Theriogenology. 1996; 45, 111–120.CrossRefGoogle Scholar
37. Lozano, JM, Abecia, JA, Forcada, F, Zarazaga, L, Alfaro, B. Effect of undernutrition on the distribution of progesterone in the uterus of ewes during the luteal phase of the oestrous cycle. Theriogenology. 1998; 49, 539–546.CrossRefGoogle Scholar
38. McEvoy, TG, Robinson, JJ, Findley, PA, Aitken, RP, Robertson, IS. Dietary excesses of urea influence the viability and metabolism of preimplantation sheep embryos and may affect fetal growth among the survivors. Anim Reprod Sci. 1997; 47, 71–90.CrossRefGoogle ScholarPubMed
39. Rosenfeld, CS, Roberts, RM. Maternal diet and other factors affecting offspring sex ratio: a review. Biol Reprod. 2004; 71, 1063–1070.CrossRefGoogle ScholarPubMed
40. Simitzis, PE, Charismiadou, MA, Kotsampasi, B, et al. Influence of maternal undernutrition on the behaviour of juvenile lambs. Appl Anim Behav Sci. 2009; 116, 191–197.CrossRefGoogle Scholar