Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-22T17:27:42.789Z Has data issue: false hasContentIssue false
  • English
  • Français

Impact of maternal stress and nutrition on behavioural and physiological outcomes in young lambs

Published online by Cambridge University Press:  01 January 2023

JA Rooke ,
G Arnott ,
CM Dwyer  and
KMD Rutherford
JA Rooke*
Affiliation:
Beef and Sheep Research Centre, Future Farming Systems, SRUC, West Mains Road, Edinburgh EH9 3JG, UK
G Arnott
Affiliation:
Animal Behaviour and Welfare, Animal and Veterinary Sciences Research Group, SRUC, West Mains Road, Edinburgh EH9 3JG, UK Institute for Global Food Security, School of Biological Sciences, Queen's University Belfast, Medical Biology Centre, 97 Lisburn Road, Belfast BT9 7BL, UK
CM Dwyer
Affiliation:
Animal Behaviour and Welfare, Animal and Veterinary Sciences Research Group, SRUC, West Mains Road, Edinburgh EH9 3JG, UK
KMD Rutherford
Affiliation:
Animal Behaviour and Welfare, Animal and Veterinary Sciences Research Group, SRUC, West Mains Road, Edinburgh EH9 3JG, UK
*
* Contact for correspondence and requests for reprints: [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The pre-natal period is of critical importance in defining how individuals respond to their environment throughout life. Stress experienced by pregnant females has detrimental effects on offspring behaviour, health and productivity. The sheep (Ovis aries) has been used as a model to inform human studies; however, in a farming context, the consequences for the lamb of stress experienced by the ewe have received less attention. The stressors that pregnant ewes are most frequently exposed to include sub-optimal nutrition and acute and chronic stressors related to husbandry and the environment. This review focuses upon the young sheep, from around 100 days old until adulthood and uses material identified from a systematic survey of the literature relating to production-relevant maternal stressors and lamb outcomes. Overall, the results demonstrated that stressors imposed upon the ewe altered progeny behavioural and physiological responses. However, detailed analysis of the literature shows several deficiencies in the field, as a whole, which greatly limit the ability to draw conclusions as to how welfare may be affected by pre-natal challenges in commercial sheep. These deficiencies included a lack of consistency in response due to the variety of both stressors imposed and responses measured. Key gaps in knowledge include the impact of ewe disease during pregnancy on outcomes for their progeny and more generally how different commercially relevant stressors interact. Furthermore, there is a need to develop a systematic series of behavioural and physiological measures that can be integrated to provide a holistic and practically applicable picture of offspring welfare.

Keywords

animal welfaregestationpractical applicationoffspring responsesheepstress
Type
Research Article
Information
Animal Welfare , Volume 26 , Issue 4 , November 2017 , pp. 403 - 415
Copyright
© 2017 Universities Federation for Animal Welfare

References

Arnott, G, Roberts, D, Rooke, JA, Turner, SP, Lawrence, AB and Rutherford, KMD 2012 Board invited review: The importance of the gestation period for welfare of calves: maternal stres-sors and difficult births. Journal of Animal Science 90: 5021–5034. https://doi.org/10.2527/jas.2012-5463CrossRefGoogle ScholarPubMed
Averós, X, Marchewka, J, de Heredia, IB, Zanella, AJ, Ruiz, R and Estevez, I 2015 Space allowance during gestation and early maternal separation: effects on the fear response and social motivation of lambs. Applied Animal Behaviour Science 163: 98–109. https://doi.org/10.1016/j.applanim.2014.11.015CrossRefGoogle Scholar
Barker, DJP, Osmond, C, Golding, J, Kuh, D and Wadsworth, MEJ 1989 Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular dis-ease. British Medical Journal 298: 564–567. https://doi.org/10.1136/bmj.298.6673.564CrossRefGoogle Scholar
Bloomfield, FH, Oliver, MH, Giannoulias, CD, Gluckman, PD, Harding, JE and Challis, JRG 2003 Brief undernutrition in late-gestation sheep programs the hypothalamic-pituitary-adrenal axis in adult offspring. Endocrinology 144: 2933–2940. https://doi.org/10.1210/en.2003-0189CrossRefGoogle ScholarPubMed
Burt, BE, Hess, BW, Nathanielsz, PW and Ford, SP 2007 Flock differences in the impact of maternal dietary restriction on offspring growth and glucose tolerance in female offspring. Society for Reproduction and Fertility Supplement 64: 411–424. https://doi.org/10.5661/RDR-VI-411Google ScholarPubMed
Campbell, MLH, Mellor, DJ and Sandøe, P 2014 How should the welfare of fetal and neurologically immature postnatal animals be protected? Animal Welfare 23: 369–379. https://doi.org/10.7120/09627286.23.4.369CrossRefGoogle ScholarPubMed
Chadio, SE, Kotsampasi, B, Papadomichelakis, G, Deligeorgis, S, Kalogiannis, D, Menegatos, I and Zervas, G 2007 Impact of maternal undernutrition on the hypothalamic-pitu-itaryadrenal axis responsiveness in sheep at different ages postna-tal. Journal of Endocrinology 192: 495–503. https://doi.org/10.1677/JOE-06-0172Google Scholar
Corner, R, Kenyon, P, Stafford, K, West, D, Morris, S and Blair, H 2005 Does the ewe nutrition during pregnancy affect the behaviour of ewe lambs at 1 and 2 years of age? Proceedings of the New Zealand Society of Animal Production 65: 29–32Google Scholar
Coulon, M, Hild, S, Schroeer, A, Janczak, A and Zanella, A 2011 Gentle vs aversive handling of pregnant ewes: II. Physiology and behavior of the lambs. Physiology and Behavior 103: 575–584. https://doi.org/10.1016/j.physbeh.2011.04.010CrossRefGoogle ScholarPubMed
Coulon, M, Nowak, R, Andanson, S, Petit, B, Levy, F and Boissy, A 2015 Effects of prenatal stress and emotional reactivity of the mother on emotional and cognitive abilities in lambs. Developmental Psychobiology 57: 626–636. https://doi.org/10.1002/dev.21320CrossRefGoogle ScholarPubMed
Coulon, MF, Levy, C, Ravel, R, Nowak, S and Boissy, A 2014 Mild effects of gestational stress and social reactivity on the onset of mother-young interactions and bonding in sheep. Stress, The International Journal on the Biology of Stress 17: 460–470Google ScholarPubMed
Dixon, LM, Sparks, NHC and Rutherford, KMD 2016 Early experiences matter: a review of the effects of prenatal environ-ment on offspring characteristics in poultry. Poultry Science 95:489–499. https://doi.org/10.3382/ps/pev343CrossRefGoogle Scholar
Donovan, E, Hernandez, C, Matthews, L, Oliver, M, Jaquiery, A, Bloomfield, F and Harding, J 2013 Periconceptional undernutrition in sheep leads to decreased loco-motor activity in a natural environment. Journal of Developmental Origins of Health and Disease 4: 296–299. https://doi.org/10.1017/S2040174413000214CrossRefGoogle Scholar
Dwyer, CM and Smith, LA 2008 Parity effects on maternal behaviour are not related to circulating oestradiol concentrations in two breeds of sheep. Physiology and Behavior 93: 148–154. https://doi.org/10.1016/j.physbeh.2007.08.007CrossRefGoogle Scholar
English Beef and Lamb Executive (EBLEX) 2014 EBLEX 2014 The breeding structure of the British sheep industry 2012. Agriculture and Horticulture Development board (AHDB): Kenilworth, Warwickshire, UKGoogle Scholar
Erhard, HW, Boissy, A, Rae, MT and Rhind, SM 2004 Effects of prenatal undernutrition on emotional reactivity and cognitive flexibility in adult sheep. Behavioural Brain Research 151: 25–35. https://doi.org/10.1016/j.bbr.2003.08.003CrossRefGoogle ScholarPubMed
Erhard, HW and Rhind, SM 2004 Prenatal and postnatal expo-sure to environmental pollutants in sewage sludge alters emotion-al reactivity and exploratory behaviour in sheep. Science of the Total Environment 332: 101–108. https://doi.org/10.1016/j.sci-totenv.2004.04.012CrossRefGoogle Scholar
European Food Safety Authority (EFSA) Panel on Animal Health and Welfare (AHAW) 2012 Guidance on risk assessment for animal welfare. EFSA Journal 10: 2513. https://doi.org/10.2903/j.efsa.2012.2513Google Scholar
European Food Safety Authority (ESFA) Panel on Animal Health and Welfare (AHAW) 2014 Scientific opin-ion on the welfare risk related to the farming of sheep for wool, meat and milk production. EFSA Journal 12: 3933. https://doi.org/10.2903/j.efsa.2014.3933Google Scholar
Fisher, RE, Karrow, NA, Quinton, M, Finegan, EJ, Miller, SP, Atkinson, JL and Boermans, HJ 2010 Endotoxin exposure during late pregnancy alters ovine offspring febrile and hypothalamic-pituitary-adrenal axis responsiveness later in life. Stress, the International Journal on the Biology of Stress 13: 335–343CrossRefGoogle ScholarPubMed
Ford, S and Long, N 2012 Evidence for similar changes in off-spring phenotype following either maternal undernutrition or overnutrition: potential impact on fetal epigenetic mechanisms. Reproduction Fertility and Development 24: 105–111. https://doi.org/10.1071/RD11911CrossRefGoogle Scholar
Forkman, B, Boissy, A, Meunier-Salauen, MC, Canali, E and Jones, RB 2007 A critical review of fear tests used on cattle, pigs, sheep, poultry and horses Physiology and Behavior 92: 340–374. https://doi.org/10.1016/j.physbeh.2007.03.016CrossRefGoogle ScholarPubMed
Gardner, DS, Van Bon, BWM, Dandrea, J, Goddard, PJ, May, SF, Wilson, V, Stephenson, T and Symonds, ME 2006 Effect of periconceptional undernutrition and gender on hypothal-amic-pituitary-adrenal axis function in young adult sheep. Journal of Endocrinology 190: 203–212. https://doi.org/10.1677/joe.1.06751Google ScholarPubMed
Gluckman, PD and Hanson, MA 2004 Developmental origins of disease paradigm: A mechanistic and evolutionary perspective. Pediatric Research 56: 311–317. https://doi.org/10.1203/01.PDR.0000135998.08025.FBCrossRefGoogle ScholarPubMed
Groothuis, TGG and Taborsky, B 2015 Introducing biological realism into the study of developmental plasticity in behaviour. Frontiers in Zoology 12(S1): S6. https://doi.org/10.1186/1742-9994-12-S1-S6CrossRefGoogle Scholar
Gutleb, AC, Lilienthal, H, Erhard, HW, Zimmer, KE, Skaare, JU and Ropstad, E 2011 Effects of pre- and postnatal polychlori-nated biphenyl exposure on emotional reactivity observed in lambs before weaning. Ecotoxicology and Environmental Safety 74: 1396–1401. https://doi.org/10.1016/j.ecoenv.2011.03.004CrossRefGoogle ScholarPubMed
Hernandez, CE, Harding, JE, Oliver, MH, Bloomfield, FH, Held, SDE and Matthews, LR 2009 Effects of litter size, sex and periconceptional ewe nutrition on side preference and cognitive flexibility in the offspring. Behavioural Brain Research 204: 82–87. https://doi.org/10.1016/j.bbr.2009.05.019Google ScholarPubMed
Hernandez, CE, Matthews, LR, Oliver, MH, Bloomfield, FH and Harding, JE 2010 Effects of sex, litter size and periconceptional ewe nutrition on offspring behavioural and physiological response to isolation. Physiology and Behavior 101: 588–594. https://doi.org/10.1016/j.physbeh.2010.08.020CrossRefGoogle ScholarPubMed
Ioannidis, JPA 2005 Meta-analysis in public health: potentials and problems. European Journal of Public Health 15: 60–61Google Scholar
King, S, Dancause, K, Turcotte-Tremblay, A-M, Veru, F and Laplante, DP 2012 Using natural disasters to study the effects of prenatal maternal stress on child health and development. Birth Defects Research (Part C) 96: 273–288. https://doi.org/10.1002/bdrc.21026CrossRefGoogle Scholar
Long, NM, Ford, SP and Nathanielsz, PW 2013 Multigenerational effects of fetal dexamethasone exposure on the hypothalamic-pituitary-adrenal axis of first- and second-generation female offspring. American Journal of Obstetrics and Gynecology (online) 208: 217.e1-8. https://doi.org/10.1016/j.ajog.2012.12.014Google ScholarPubMed
Long, NM, Nathanielsz, PW and Ford, SP 2012 The impact of maternal overnutrition and obesity on hypothalamic-pituitary-adre-nal axis response of offspring to stress. Domestic Animal Endocrinology 42: 195–202. https://doi.org/10.1016/j.domaniend.2011.12.002CrossRefGoogle ScholarPubMed
Long, NM, Nijland, MJ, Nathanielsz, PW and Ford, SP 2010 The effect of early to mid-gestational nutrient restriction on female offspring fertility and hypothalamic-pituitary-adrenal axis response to stress. Journal of Animal Science 88: 2029–2037. https://doi.org/10.2527/jas.2009-2568CrossRefGoogle ScholarPubMed
Lumey, LH, Stein, AD and Susser, E 2011 Prenatal famine and adult health. Annual Review of Public Health 32: 237–262. https://doi.org/10.1146/annurev-publhealth-031210-101230CrossRefGoogle ScholarPubMed
Luther, JS, Redmer, DA, Reynolds, LP and Wallace, JM 2005 Nutritional paradigms of ovine fetal growth restriction: implications for human pregnancy. Human Fertility 8: 179–187. https://doi.org/10.1080/14647270500320121CrossRefGoogle ScholarPubMed
Munoz, C, Carson, AF, McCoy, MA, Dawson, LER, O’Connell, NE and Gordon, AW 2009 Effect of plane of nutrition of 1-and 2-year-old ewes in early and mid-pregnancy on ewe reproduction and offspring performance up to weaning. Animal 3:657–669. https://doi.org/10.1017/S1751731109003917CrossRefGoogle ScholarPubMed
Oliver, MH, Bloomfield, FH, Jaquiery, AL, Todd, SE, Thorstensen, EB and Harding, JE 2012 Periconceptional undernutrition suppresses cortisol response to arginine vaso-pressin and corticotropin-releasing hormone challenge in adult sheep offspring. Journal of Developmental Origins of Health and Disease 3: 52–58. https://doi.org/10.1017/S2040174411000626CrossRefGoogle Scholar
Otten, W, Kanitz, E and Tuchscherer, M 2015 The impact of pre-natal stress on offspring development in pigs. Journal of Agricultural Science 153: 907–919. https://doi.org/10.1017/S0021859614001361Google Scholar
Robinson, JJ, McEvoy, TG and Rooke, JA 2002 Nutrition for conception and pregnancy. In: Freer, M and Dove, H (eds) Sheep Nutrition pp 189–211. CABI Publishing: Wallingford, UK. https://doi.org/10.1079/9780851995953.0189CrossRefGoogle Scholar
Rooke, JA, Arnott, G, Dwyer, CM and Rutherford, KMD 2015 The importance of the gestation period for welfare of lambs: maternal stressors and lamb vigour and well-being. Journal of Agricultural Science 153: 497–519. https://doi.org/10.1017/S002185961400077XCrossRefGoogle Scholar
Rooke, JA, Houdijk, JGM, McIlvaney, K, Ashworth, CJ and Dwyer, CM 2010 Differential effects of maternal undernutrition between days 1 and 90 of pregnancy on ewe and lamb perform-ance and lamb parasitism in hill or lowland breeds. Journal of Animal Science 88: 3833–3842. https://doi.org/10.2527/jas.2010-2991CrossRefGoogle ScholarPubMed
Roussel, S, Hemsworth, PH, Boissy, A and Duvaux-Ponter, C 2004 Effects of repeated stress during pregnancy in ewes on the behavioural and physiological responses to stressful events and birth weight of their offspring. Applied Animal Behaviour Science 85: 259–276. https://doi.org/10.1016/j.applanim.2003.11.006CrossRefGoogle Scholar
Roussel-Huchette, S, Hemsworth, PH, Boissy, A and Duvaux-Ponter, C 2008 Repeated transport and isolation during pregnancy in ewes: Differential effects on emotional reactivity and weight of their offspring. Applied Animal Behaviour Science 109:275–291. https://doi.org/10.1016/j.applanim.2007.02.005CrossRefGoogle Scholar
Rutherford, KMD, Donald, RD, Arnott, G, Rooke, JA, Dixon, L, Mettam, J, Turnbull, J and Lawrence, AB 2012 Farm animal wel-fare: assessing risks attributable to the prenatal environment. Animal Welfare 21: 419–429. https://doi.org/10.7120/09627286.21.3.419CrossRefGoogle Scholar
Sargeant, JM, Rajic, A, Read, S and Ohlsson, A 2006 The process of systematic review and its application in agri-food pub-lic-health. Preventive Veterinary Medicine 75: 141–151. https://doi.org/10.1016/j.prevetmed.2006.03.002CrossRefGoogle Scholar
Simitzis, PE, Charismiadou, MA, Kotsampasi, B, Papadomichelakis, G, Christopoulou, EP, Papavlasopoulou, EK and Deligeorgis, SG 2009 Influence of maternal undernutrition on the behaviour of juvenile lambs. Applied Animal Behaviour Science 116: 191–197. https://doi.org/10.1016/j.applanim.2008.09.007CrossRefGoogle Scholar
Sinclair, KD, Rutherford, KMD, Wallace, JM, Brameld, JM, Stöger, R, Alberio, R, Sweetman, S, Gardner, DS, Perry, V, Adam, C, Ashworth, C, Robinson, J and Dwyer, CM 2016 Epigenetics and developmental programming of welfare and pro-duction traits in farm animals. Reproduction, Fertility and Development 28: 1443–1478. https://doi.org/10.1071/RD16102CrossRefGoogle Scholar
Sloboda, DM, Moss, TJ, Gurrin, LC, Newnham, JP and Challis, JRG 2002 The effect of prenatal betamethasone adminis-tration on postnatal ovine hypothalamic-pituitary-adrenal function. Journal of Endocrinology 172: 71–81. https://doi.org/10.1677/joe.0.1720071CrossRefGoogle Scholar
Sloboda, DM, Moss, TJM, Li, SF, Doherty, D, Nitsos, I, Challis, JRG and Newnham, JP 2007 Prenatal betamethasone exposure results in pituitary-adrenal hyporesponsiveness in adult sheep. American Journal of Physiology: Endocrinology and Metabolism 292: E61–E70. https://doi.org/10.1152/ajpendo.00270.2006Google ScholarPubMed
Smulders, FJM and Algers, B 2009 Welfare of Production Animals: Assessment and Management of Risks. Wageningen Academic Publishers: Wageningen, The Netherlands. https://doi.org/10.3920/978-90-8686-690-8CrossRefGoogle Scholar
Wallace, JM, Milne, JS, Green, LR and Aitken, RP 2011 Postnatal hypothalamic-pituitary-adrenal function in sheep is influ-enced by age and sex, but not by prenatal growth restriction. Reproduction Fertility and Development 23: 275–284. https://doi.org/10.1071/RD10103Google Scholar