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Farm animal welfare: assessing risks attributable to the prenatal environment

Published online by Cambridge University Press:  01 January 2023

KMD Rutherford*
Affiliation:
Animal Behaviour and Welfare, Animal and Veterinary Sciences Research Group, SAC, West Mains Rd, Edinburgh EH9 3JG, UK
RD Donald
Affiliation:
Animal Behaviour and Welfare, Animal and Veterinary Sciences Research Group, SAC, West Mains Rd, Edinburgh EH9 3JG, UK
G Arnott
Affiliation:
Animal Behaviour and Welfare, Animal and Veterinary Sciences Research Group, SAC, West Mains Rd, Edinburgh EH9 3JG, UK
JA Rooke
Affiliation:
Animal Behaviour and Welfare, Animal and Veterinary Sciences Research Group, SAC, West Mains Rd, Edinburgh EH9 3JG, UK
L Dixon
Affiliation:
Animal Behaviour and Welfare, Animal and Veterinary Sciences Research Group, SAC, West Mains Rd, Edinburgh EH9 3JG, UK
JJM Mehers
Affiliation:
Institute of Aquaculture, University of Stirling, Stirlingshire FK9 4LA, UK
J Turnbull
Affiliation:
Institute of Aquaculture, University of Stirling, Stirlingshire FK9 4LA, UK
AB Lawrence
Affiliation:
Animal Behaviour and Welfare, Animal and Veterinary Sciences Research Group, SAC, West Mains Rd, Edinburgh EH9 3JG, UK
*
* Contact for correspondence and requests for reprints: kenny.rutherford@sac.ac.uk

Abstract

An ever-expanding scientific literature highlights the impact of the prenatal environment on many areas of biology. Across all major farmed species, experimental studies have clearly shown that prenatal experiences can have a substantial impact on outcomes relevant to later health, welfare and productivity. In particular, stress or sub-optimal nutrition experienced by the mother during pregnancy has been shown to have wide-ranging and important effects on how her offspring cope with their social, physical and infectious environment. Variation in the conditions for development provided by the reproductive tract or egg, for instance by altered nutritional supply or hormonal exposure, may therefore explain a large degree of variation in many welfare- and productivity-relevant traits. The scientific literature suggests a number of management practices for pre-birth/hatch individuals that could compromise their later welfare. Such studies may have relevance for the welfare of animals under human care, depending on the extent to which real life conditions involve exposure to these practices. Overall, the findings highlight the importance of extending the focus on animal welfare to include the prenatal period, an aspect which until recently has been largely neglected.

Type
Research Article
Copyright
© 2012 Universities Federation for Animal Welfare

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References

Adams, R, Garry, FB, Holland, MD and Odde, KG 1995 Clinicopathologic measurement in newborn beef calves experiencing mild to moderate degrees of dystocia. Agri-practice 16: 511Google Scholar
Ashworth, CJ, Hogg, CO, Hoeks, CWF, Donald, RD, Duncan, WC, Lawrence, AB and Rutherford, KMD 2011 Pre-natal social stress and post-natal pain affect the developing pig reproductive axis. Reproduction 142: 907914. http://dx.doi.org/10.1530/REP-11-0280CrossRefGoogle ScholarPubMed
Ashworth, CJ, Toma, LM and Hunter, MG 2009 Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability. Philosophical Transactions of the Royal Society B364: 33513361. http://dx.doi.org/10.1098/rstb.2009.0184CrossRefGoogle Scholar
Barker, DJP, Osmond, C, Golding, J, Kuh, D and Wadsworth, MEJ 1989a Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. British Medical Journal 298: 564567. http://dx.doi.org/10.1136/bmj.298.6673.564CrossRefGoogle ScholarPubMed
Barker, DJP, Osmond, C, Winter, PD, Margetts, B and Simmonds, SJ 1989b Weight in infancy and death from ischaemic heart disease. The Lancet 334: 577580. http://dx.doi.org/10.1016/S0140-6736(89)90710-1CrossRefGoogle Scholar
Bateson, P 2007 Developmental plasticity and evolutionary biology. Journal of Nutrition 137: 10601062CrossRefGoogle ScholarPubMed
Bateson, P, Barker, D, Clutton-Brock, T, Deb, D, D’Udine, B, Foley, RA, Gluckman, P, Godfrey, K, Kirkwood, T, Lahr MM. McNamara, J, Metcalfe, NB, Monaghan, P, Spencer, HG and Sultan, SE 2004 Developmental plasticity and human health. Nature 430: 419421. http://dx.doi.org/10.1038/nature02725CrossRefGoogle ScholarPubMed
Beattie, VE, Walker, N and Sneddon, IA 1996 Influence of maternal experience on pig behaviour. Applied Animal Behaviour Science 46: 159166. http://dx.doi.org/10.1016/0168-1591(95)00646-XCrossRefGoogle Scholar
Bellows, RA and Lammoglia, MA 2000 Effects of severity of dystocia on cold tolerance and serum concentrations of glucose and cortisol in neonatal beef calves. Theriogenology 53: 803813. http://dx.doi.org/10.1016/S0093-691X(99)00275-7CrossRefGoogle ScholarPubMed
Blair, HT, Jenkinson, CMC, Peterson, SW, Kenyon, PR, van der Linden, DS, Davenport, LC, MacKenzie, DDS, Morris, ST and Firth, EC 2010 Dam and granddam feeding during pregnancy in sheep affects milk supply in offspring and reproductive performance in grand-offspring. Journal of Animal Science 88: E40E50. http://dx.doi.org/10.2527/jas.2009-2523CrossRefGoogle ScholarPubMed
Bonduriansky, R and Day, T 2009 Nongenetic inheritance and its evolutionary implications. Annual Review of Ecology, Evolution and Systematics 40: 103125. http://dx.doi.org/10.1146/annurev.ecol-sys.39.110707.173441CrossRefGoogle Scholar
Braastad, BO 1998 Effects of prenatal stress on behaviour of offspring of laboratory and farmed mammals. Applied Animal Behaviour Science 61: 159180. http://dx.doi.org/10.1016/S0168-1591(98)00188-9CrossRefGoogle Scholar
Brown, AS, Susser, ES, Lin, SP, Neugebauer, R and Gorman, JM 1995 Increased risk of affective disorders in males after second trimester prenatal exposure to the Dutch hunger winter of 1944-45. British Journal of Psychiatry 166: 601606. http://dx.doi.org/10.1192/bjp.166.5.601CrossRefGoogle Scholar
Brunton, PJ and Russell, JA 2008 The expectant brain: adapting for motherhood. Nature Reviews Neuroscience 9: 1125. http://dx.doi.org/10.1038/nrn2280CrossRefGoogle ScholarPubMed
Brunton, PJ and Russell, JA 2011 Neuroendocrine control of maternal stress responses and fetal programming by stress in pregnancy. Progress in Neuro-Psychopharmacology & Biological Psychiatry 35: 11781191. http://dx.doi.org/10.1016/j.pnpbp.2010.12.023CrossRefGoogle ScholarPubMed
Burke, JM, Miller, JE and Brauer, DK 2005 The effectiveness of copper oxide wire particles as an anthelmintic in pregnant ewes and safety to offspring. Veterinary Parasitology 131: 291297. http://dx.doi.org/10.1016/j.vetpar.2005.05.009CrossRefGoogle ScholarPubMed
Campbell, PM, Pottinger, TG and Sumpter, JP 1994 Preliminary evidence that chronic confinement stress reduces the quality of gametes produced by brown and rainbow trout. Aquaculture 120: 151169. http://dx.doi.org/10.1016/0044-8486(94)90230-5CrossRefGoogle Scholar
Chadio, SE, Kotsampasi, B, Papadomichelakis, G, Deligeorgis, S, Kalogiannis, D, Menegatos, I and Zervas, G 2007 Impact of maternal undernutrition on the hypothalamic-pituitary-adrenal axis responsiveness in sheep at different ages postnatal. Journal of Endocrinology 192: 495503. http://dx.doi.org/10.1677/JOE-06-0172CrossRefGoogle ScholarPubMed
Chadwick, MA, Vercoe, PE, Williams, IH and Revell, DK 2009 Programming sheep production on saltbush: adaptations of offspring from ewes that consumed high amounts of salt during pregnancy and early lactation. Animal Production Science 49: 311317. http://dx.doi.org/10.1071/EA08234CrossRefGoogle Scholar
Charil, A, Laplante, DP, Vaillancourt, C and King, S 2010 Prenatal stress and brain development. Brain Research Reviews 65: 5679. http://dx.doi.org/10.1016/j.brainresrev.2010.06.002CrossRefGoogle ScholarPubMed
Collier, RJ, Doelger, SG, Head, HH, Thatcher, WW and Wilcox, CJ 1982 Effects of heat stress during pregnancy on maternal hormone concentrations, calf birth weight and postpartum milk yield of Holstein cows. Journal of Animal Science 54: 30931910.2527/jas1982.542309xCrossRefGoogle ScholarPubMed
Corner, RA, Kenyon, PR, Stafford, JK, West, DM and Oliver, MH 2006 The effect of mid-pregnancy shearing or yarding stress on ewe post-natal behaviour and the birth weight and post-natal behaviour of their lambs. Livestock Science 102: 121129. http://dx.doi.org/10.1016/j.livprodsci.2005.12.001CrossRefGoogle Scholar
Coulon, M, Hild, S, Schroeer, A, Janczak, AM and Zanella, AJ 2011 Gentle vs aversive handling of pregnant ewes: II Physiology and behavior of the lambs. Physiology & Behavior 103: 575584. http://dx.doi.org/10.1016/j.physbeh.2011.04.010CrossRefGoogle ScholarPubMed
Daniel, JA, Carroll, JA, Keisler, DH and Kojima, CJ 2008 Evaluation of immune system function in neonatal pigs born vaginally or by Caesarean section. Domestic Animal Endocrinology 35: 818710.1016/j.domaniend.2008.02.002CrossRefGoogle ScholarPubMed
Daniel, JA, Keisler, DH, Sterle, JA, Matteri, RL and Carroll, JA 1999 Birth by Caesarian section alters postnatal function of the hypothalamic-pituitary-adrenal axis in young pigs. Journal of Animal Science 77: 742749CrossRefGoogle ScholarPubMed
D’Eath, RB, Conington, J, Lawrence, AB, Olsson, IAS and Sandøe, P 2010 Breeding for behavioural change in farm animals: practical, economic and ethical considerations. Animal Welfare 19: 1727CrossRefGoogle Scholar
Diaz, R, Brown, RW and Seckl, JR 1998 Distinct ontogeny of glucocorticoid and mineralocorticoid receptor and 11 beta-hydroxysteroid dehydrogenase types I and II mRNAs in the fetal rat brain suggest a complex control of glucocorticoid actions. Journal of Neuroscience 18: 2570258010.1523/JNEUROSCI.18-07-02570.1998CrossRefGoogle ScholarPubMed
Dufty, AM, Clobert, J and Moller, AP 2002 Hormones, developmental plasticity and adaptation. Trends in Ecology and Evolution 17: 190196CrossRefGoogle Scholar
Dwyer, CM 2003 Behavioural development in the neonatal lamb: effect of maternal and birth-related factors. Theriogenology 59: 1027105010.1016/S0093-691X(02)01137-8CrossRefGoogle ScholarPubMed
Dwyer, CM, Lawrence, AB, Bishop, SC and Lewis, M 2003 Ewe-lamb bonding behaviours at birth are affected by maternal undernutrition in pregnancy. British Journal of Nutrition 89: 123136CrossRefGoogle ScholarPubMed
Eisenberg, DTA 2011 An evolutionary review of human telomere biology: the thrifty telomere hypothesis and notes on potential adaptive paternal effects. American Journal of Human Biology 23: 149167CrossRefGoogle ScholarPubMed
Emack, J and Matthews, SG 2011 Effects of chronic maternal stress on hypothalamo-pituitary-adrenal (HPA) function and behavior: No reversal by environmental enrichment. Hormones and Behavior 60: 58959810.1016/j.yhbeh.2011.08.008CrossRefGoogle ScholarPubMed
Eriksson, JG, Kajantie, E, Osmond, C, Thornburg, K and Barker, DJP 2010 Boys live dangerously in the womb. American Journal of Human Biology 22: 330335CrossRefGoogle ScholarPubMed
Field, T, Diego, M and Hernandez-Reif, M 2006 Prenatal depression effects on the fetus and newborn: a review. Infant Behavior & Development 29: 44545510.1016/j.infbeh.2006.03.003CrossRefGoogle ScholarPubMed
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 13: 33534310.3109/10253891003663762CrossRefGoogle ScholarPubMed
Foxcroft, GR, Dixon, WT, Novak, S, Putman, CT, Town, SC and Vinsky, MDA 2006 The biological basis for prenatal programming of postnatal performance in pigs. Journal of Animal Science 84: E105E11210.2527/2006.8413_supplE105xCrossRefGoogle ScholarPubMed
Fthenakis, GC, Karagiannidis, A, Alexopoulos, C, Brozos, C and Papadopoulos, E 2001 Effects of sarcoptic mange on the reproductive performance of ewes and transmission of Sarcoptes scabiei to newborn lambs. Veterinary Parasitology 95: 6371. http://dx.doi.org/10.1016/S0304-4017(00)00417-9CrossRefGoogle ScholarPubMed
Gluckman, PD, Hanson, MA and Spencer, HG 2005 Predictive adaptive responses and human evolution. Trends in Ecology and Evolution 20: 527533. http://dx.doi.org/10.1016/j.tree.2005.08.001CrossRefGoogle ScholarPubMed
Guibert, F, Richard-Yris, M-A, Lumineau, S, Kotrschal, K, Möstl, E and Houdelier, C 2011 Yolk testosterone levels and offspring phenotype correlate with parental age in a precocial bird. Physiology & Behavior 105: 242250. http://dx.doi.org/10.1016/j.physbeh.2011.08.009CrossRefGoogle Scholar
Hales, CN and Barker, DJP 2001 The thrifty phenotype hypothesis. British Medical Bulletin 60: 520. http://dx.doi.org/10.1093/bmb/60.1.5CrossRefGoogle ScholarPubMed
Hickson, RE, Lopez-Villalobos, N, Kenyon, PR and Morris, ST 2008 Duration of parturition and frequency of abdominal contractions in primiparous, 2-year-old Angus heifers and the relevance of body dimensions of calves to dystocia. Australian Journal of Experimental Agriculture 48: 935939. http://dx.doi.org/10.1071/EA08002CrossRefGoogle Scholar
Jablonka, E and Lamb, MJ 2005 Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral, and Symbolic Variation in the History of Life. MIT Press: Cambridge, MA, USAGoogle Scholar
Janczak, AM, Torjesen, P, Palme, R and Bakken, M 2007 Effects of stress in hens on the behaviour of their offspring. Applied Animal Behaviour Science 107: 6677. http://dx.doi.org/10.1016/j.applanim.2006.09.016CrossRefGoogle Scholar
Jarvis, S, Moinard, C, Robson, SK, Baxter, E, Ormandy, E, Douglas, AJ, Seckl, JR, Russell, JA and Lawrence, AB 2006 Programming the offspring of the pig by prenatal social stress: neuroendocrine activity and behaviour. Hormones and Behavior 49: 6880. http://dx.doi.org/10.1016/j.yhbeh.2005.05.004CrossRefGoogle ScholarPubMed
Kapoor, A, Kostaki, A, Janus, C and Matthews, SG 2009 The effects of prenatal stress on learning in adult offspring is dependent on the timing of the stressor. Behavioural Brain Research 197: 144149. http://dx.doi.org/10.1016/j.bbr.2008.08.018CrossRefGoogle ScholarPubMed
Khashan, AS, McNamee, R, Henriksen, TB, Pedersen, MG, Kenny, LC, Abel, KM and Mortensen, PB 2011 Risk of affective disorders following prenatal exposure to severe life events: a Danish population-based cohort study. Journal of Psychiatric Research 45: 879885. http://dx.doi.org/10.1016/j.jpsy-chires.2010.12.005CrossRefGoogle ScholarPubMed
Lankin, V 1997 Factors of diversity of domestic behaviour in sheep. Genetics Selection Evolution 29: 7392. http://dx.doi.org/10.1186/1297-9686-29-1-73CrossRefGoogle Scholar
Laplante, DP, Brunet, A, Schmitz, N, Ciampi, A and King, S 2008 Project ice storm: prenatal maternal stress affects cognitive and linguistic functioning in 5 1/2-year old children. Journal of the American Academy of Child & Adolescent Psychiatry 47: 10631072. http://dx.doi.org/10.1097/CHI.0b013e31817eec80CrossRefGoogle ScholarPubMed
Lay, DC 2000 Consequences of stress during development. In: Moberg, GP and Mench, JA (eds) The Biology of Animal stress: Basic Principles and Implications for Animal Welfare pp 249267. CAB International: Wallingford, UK. http://dx.doi.org/10.1079/9780851993591.0249CrossRefGoogle Scholar
Lay, DC, Kattesh, HG, Cunnick, JE, Daniels, MJ, McMunn, KA, Toscano, MJ and Roberts, MP 2008 Prenatal stress effects on pig development and response to weaning. Journal of Animal Science 86: 13161324. http://dx.doi.org/10.2527/jas.2007-0812CrossRefGoogle ScholarPubMed
Lindqvist, C, Janczak, AM, Nätt, D, Baranowska, I, Lindqvist, N, Wichman, A, Lundeberg, J, Lindberg, J, Torjesen, PA and Jensen, P 2007 Transmission of Stress-Induced Learning Impairment and Associated Brain Gene Expression from Parents to Offspring in Chickens. PLoS ONE 2: e364. http://dx.doi.org/10.1371/journal.pone.0000364CrossRefGoogle Scholar
Lombard, JE, Garry, FB, Tomlinson, SM and Garber, LP 2007 Impacts of dystocia on health and survival of dairy calves. Journal of Dairy Science 90: 17511760. http://dx.doi.org/10.3168/jds.2006-295CrossRefGoogle ScholarPubMed
Lumey, LH, Stein, AD, Kahn, HS, van der Pal-de Bruin, KM, Blauw, GJ, Zybert, PA, Susser, ES 2007 Cohort Profile: The Dutch Hunger Winter Families study. International Journal of Epidemiology 36: 11961204. http://dx.doi.org/10.1093/ije/dym126CrossRefGoogle ScholarPubMed
Maruoka, T, Kodomari, I, Yamauchi, R, Wada, E and Wada, K 2009 Maternal enrichment affects prenatal hippocampal proliferation and open-field behaviours in female offspring mice. Neuroscience Letters 454: 2832. http://dx.doi.org/10.1016/j.neulet.2009.02.052CrossRefGoogle ScholarPubMed
Mellor, DJ and Diesch, TJ 2006 Onset of sentience: the potential for suffering in fetal and newborn farm animals. Applied Animal Behaviour Science 100: 4857. http://dx.doi.org/10.1016/j.applanim.2006.04.012CrossRefGoogle Scholar
Meyer, U, Yee, BK and Feldon, J 2007 The neurodevelopmental impact of prenatal infections at different times of pregnancy: the earlier the worse. Neuroscientist 13: 241256. http://dx.doi.org/10.1177/1073858406296401CrossRefGoogle ScholarPubMed
Monaghan, P 2008 Early growth conditions, phenotypic development and environmental change. Philosophical Transactions of the Royal Society B363: 1635164510.1098/rstb.2007.0011CrossRefGoogle Scholar
Mousseau, TA and Fox, CW 1998 Maternal effects as adaptations. Oxford University Press: Oxford, UKGoogle Scholar
Niekamp, SR, Sutherland, MA, Dahl, GE and Salak-Johnson, JL 2006 Photoperiod influences the immune status of multiparous pregnant sows and their piglets. Journal of Animal Science 84: 20722082. http://dx.doi.org/10.2527/jas.2005-597CrossRefGoogle ScholarPubMed
Oostindjer, M, Bolhuis, JE, van den Brand, H, Roura, E and Kemp, B 2010 Prenatal flavor exposure affects growth, health and behaviour of newly weaned piglets. Physiology & Behavior 99: 579586. http://dx.doi.org/10.1016/j.physbeh.2010.01.031CrossRefGoogle ScholarPubMed
Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjöström M, Golding J and ALSPAC Study Team 2006 Sex-specific male-line transgenerational responses in humans. European Journal of Human Genetics 14: 159166CrossRefGoogle Scholar
Poore, KR and Fowden, AL 2003 The effect of birth weight on hypothalamo-pituitary-adrenal axis function in juvenile and adult pigs. Journal of Physiology 547: 107116. http://dx.doi.org/10.1113/jphysiol.2002.024349CrossRefGoogle ScholarPubMed
Provenza, FD 2008 What does it mean to be locally adapted and who cares anyway? Journal of Animal Science 86: E271E284. http://dx.doi.org/10.2527/jas.2007-0468CrossRefGoogle ScholarPubMed
Ringgenberg, N, Bergeron, R, Meunier-Salaün, M-C and Devillers, N 2012 Impact of social stress during gestation and environmental enrichment during lactation on the maternal behavior of sows. Applied Animal Behaviour Science 136: 12613510.1016/j.applanim.2011.12.012CrossRefGoogle Scholar
Roehe, R 1999 Genetic determination of individual birth weight and its association with sow productivity using Bayesian analyses. Journal of Animal Science 77: 33034310.2527/1999.772330xCrossRefGoogle ScholarPubMed
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 performance and lamb parasitism in hill or lowland breeds. Journal of Animal Science 88: 38333842. http://dx.doi.org/10.2527/jas.2010-2991CrossRefGoogle ScholarPubMed
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: 275291. http://dx.doi.org/10.1016/j.applanim.2007.02.005CrossRefGoogle Scholar
Rutherford, KMD, Robson, SK, Donald, RD, Jarvis, S, Sandercock, DA, Nolan, AM and Lawrence, AB 2009 Prenatal stress amplifies the immediate behavioural responses to acute pain in piglets. Biology Letters 5: 452454. http://dx.doi.org/10.1098/rsbl.2009.0175CrossRefGoogle ScholarPubMed
Ryan, BC and Vandenbergh, JG 2002 Intrauterine position effects. Neuroscience and Biobehavioral Reviews 26: 665678. http://dx.doi.org/10.1016/S0149-7634(02)00038-6CrossRefGoogle ScholarPubMed
Sargison, ND, Scott, PR, Penny, CD and Pirie, RS 1995 Effect of an outbreak of sheep scab (Psoroptes ovis infestation) during mid-pregnancy on ewe body condition and lamb birthweight. Veterinary Record 136: 287289. http://dx.doi.org/10.1136/vr.136.12.287CrossRefGoogle ScholarPubMed
Sferruzzi-Perri, AN, Vaughan, OR, Coan, PM, Suciu, MC, Darbyshire, R, Constancia, M, Burton, GJ and Fowden, AL 2011 Placental-specific Igf2 deficiency alters developmental adaptations to undernutrition in mice. Endocrinology 152: 32023212CrossRefGoogle ScholarPubMed
Shine, R and Downes, SJ 1999 Can pregnant lizards adjust their offspring phenotypes to environmental conditions? Oecologia 119: 18. http://dx.doi.org/10.1007/s004420050754CrossRefGoogle ScholarPubMed
Sorrells, AD, Eicher, SD, Scott, KA, Harris, MJ, Pajor, EA, Lay, DC Jr and Richert, BT 2006 Postnatal behavioral and physiological responses of piglets from gilts housed individually or in groups during gestation. Journal of Animal Science 84: 75776610.2527/2006.843757xCrossRefGoogle ScholarPubMed
Storm, JJ and Lima, SL 2010 Mothers forewarn offspring about predators: a transgenerational maternal effect on behavior. American Naturalist 175: 382390. http://dx.doi.org/10.1086/650443CrossRefGoogle ScholarPubMed
Störmer, C 2011 Sex differences in the consequences of early-life exposure to epidemiological stress - a life-history approach. American Journal of Human Biology 23: 201208CrossRefGoogle Scholar
Stott, GH and Reinhard, EJ 1978 Adrenal function and passive immunity in the dystocial calf. Journal of Dairy Science 61:14571461. http://dx.doi.org/10.3168/jds.S0022-0302(78)83749-7CrossRefGoogle ScholarPubMed
Tobi, EW, Lumey, LH, Talens, RP, Kremer, D, Putter, H, Stein, AD, Slagboom, PE and Heijmans, BT 2009 DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Human Molecular Genetics 18: 40464053. http://dx.doi.org/10.1093/hmg/ddp353CrossRefGoogle ScholarPubMed
Veras, MM, Damaceno-Rodrigues, NR, Silva, RMG, Scoriza, JN, Saldiva, PH, Caldini, EG and Dolhnikoff, M 2009 Chronic exposure to fine particulate matter emitted by traffic affects reproductive and fetal outcomes in mice. Environmental Research 109: 536543. http://dx.doi.org/10.1016/j.envres.2009.03.006CrossRefGoogle ScholarPubMed
Vermorel, M, Vernet, J, Dardillat, C, Saido, , Damigne, C and Davicco, M-J 1989 Energy metabolism and thermoregulation in the newborn calf; effect of calving conditions. Canadian Journal of Animal Science 69: 113122CrossRefGoogle Scholar
Waldner, CL and Rosengren, LB 2009 Factors associated with serum immunoglobulin levels in beef calves from Alberta and Saskatchewan and association between passive transfer and health outcomes. Canadian Veterinary Journal 50: 275281Google ScholarPubMed
Wassink, GJ, King, EM, Grogono-Thomas, R, Brown, JC, Moore, LJ and Green, LE 2010 A within farm clinical trial to compare two treatment (parenteral antibacterials and hoof trimming) for sheep lame with footrot. Preventive Veterinary Medicine 96: 93103. http://dx.doi.org/10.1016/j.prevetmed.2010.05.006CrossRefGoogle ScholarPubMed
Weinstock, M 2007 Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochemical Research 32: 17301740. http://dx.doi.org/10.1007/s11064-007-9339-4CrossRefGoogle ScholarPubMed
Welberg, LAM, Seckl, JR and Holmes, MC 2000 Inhibition of 11 beta-hydroxysteroid dehydrogenase, the foeto-placental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxiety-like behaviour in the offspring. European Journal of Neuroscience 12: 10471054. http://dx.doi.org/10.1046/j.1460-9568.2000.00958.xCrossRefGoogle ScholarPubMed
Welberg, LAM, Thrivikraman, KV and Plotsky, PM 2005 Chronic maternal stress inhibits the capacity to up-regulate placental 11β-hydroxysteroid dehydrogenase type 2 activity. Journal of Endocrinology 186: R7R12. http://dx.doi.org/10.1677/joe.1.06374CrossRefGoogle ScholarPubMed
White, PJ, Ward, MP, Toribio, J-ALML and Windsor, PA 2010 The association between congenital chondrodystrophy of unknown origin (CCUO) in beef cattle and drought in south-eastern Australia. Preventive Veterinary Medicine 94: 178184. http://dx.doi.org/10.1016/j.prevetmed.2010.02.002CrossRefGoogle ScholarPubMed
Wilcox, AJ 2001 On the importance - and the unimportance - of birthweight. International Journal of Epidemiology 30: 12331241. http://dx.doi.org/10.1093/ije/30.6.1233CrossRefGoogle ScholarPubMed
Wolf, JB and Wade, MJ 2009 What are maternal effects (and what are they not)? Philosophical Transactions of the Royal Society B364: 11071115CrossRefGoogle Scholar
Yahav, S, Collin, A, Shinder, D and Picard, M 2004 Thermal manipulations during broiler chick embryogenesis: effects of timing and temperature. Poultry Science 83: 19591963CrossRefGoogle ScholarPubMed
Yehuda, R, Engel, SM, Brand, SR, Seckl, J, Marcus, SM and Berkowitz, GS 2005 Transgenerational effects of posttraumatic stress disorder in babies of mothers exposed to the world trade center attacks during pregnancy. Journal of Clinical Endocrinology and Metabolism 90: 41154118. http://dx.doi.org/10.1210/jc.2005-0550CrossRefGoogle Scholar