Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-27T03:17:50.846Z Has data issue: false hasContentIssue false
  • English
  • Français

Maternal behaviour and lamb survival: from neuroendocrinology to practical application*

Published online by Cambridge University Press:  08 October 2013

C. M. Dwyer
C. M. Dwyer*
Affiliation:
Animal Behaviour and Welfare, Animal and Veterinary Science Research Group, SRUC, West Mains Road, Edinburgh EH9 3JG, Scotland
*
†E-mail: [email protected]
Get access

Abstract

Parental care promotes offspring survival and, for livestock species, this care is provided solely by the mother. Maternal behaviour in the sheep has been exceptionally well-studied compared with other species and many of the underpinning biological processes leading to the expression of maternal care are known. In this review the current state of play with regard to the biology of maternal care will be reviewed, and its application to provide practical solutions to reduce lamb mortality considered. For maternal care to be elicited at birth the ewe requires elevated circulating oestradiol in late gestation, which stimulates the expression of oxytocin receptors in both peripheral and central areas (particularly the hypothalamic and limbic areas of the brain). At birth stretching of the vaginocervical canal elicits a spinal reflex which triggers the release of oxytocin primarily from neurones within the paraventricular nucleus of the hypothalamus. Oxytocin release causes an increase in the neurotransmitters noradrenaline, acetylcholine, glutamate and γ-aminobutyric acid (GABA) in the olfactory bulb, and other brain regions important for maternal behaviour. Finally, sensory cues provided by the lamb, in particular the amniotic fluids surrounding it, lead to the expression of maternal behaviours (licking, low-pitched bleats, acceptance of the lamb at the udder and suckling). This allows the expression of the two facets of maternal behaviour in the ewe: nurturance of the young and maternal selectivity, whereby a specific olfactory memory for the ewes own lamb is formed and the expression of maternal care is restricted to this lamb. Variation in the expression of maternal care has been demonstrated in primiparous ewes compared with multiparous, in different sheep genotypes, with undernutrition, stress in pregnancy, following a difficult delivery, and may occur with variation in ewe temperament. An understanding of the importance of the timing of various events in late pregnancy and during parturition, as well as the factors that can disrupt these events, can help to design management activities to minimise risks to the successful onset of maternal behaviour. Management practices that work with the biology of the ewe will be the most successful in ensuring that maternal care is expressed, so improving the welfare of the ewe and lamb, and the profitability of the farm.

Keywords

maternal behaviouroestradioloxytocinneonatal survivalsheep
Type
Full Paper
Information
animal , Volume 8 , Issue 1 , January 2014 , pp. 102 - 112
Copyright
Copyright © The Animal Consortium 2013 

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.)

Footnotes

*

This paper is based on a presentation to the joint Annual Conference of the British Society of Animal Science, Animal Science Forum, and the Association for Veterinary Teaching and Research Work, held in Nottingham, UK from 24 to 25 April 2012.

References

Alexander, G 1988. What makes a good mother? Components and comparative aspects of maternal behaviour in ungulates. Proceedings of the Australian Society for Animal Production 17, 25–41.Google Scholar
Alexander, G and Bradley, L 1985. Fostering in sheep. 4. Use of restraint. Applied Animal Behaviour Science 14, 355–364.CrossRefGoogle Scholar
Alexander, G, Stevens, D and Bradley, L 1985. Fostering in sheep. 1. Facilitation by use of textile lamb coats. Applied Animal Behaviour Science 14, 315–334.CrossRefGoogle Scholar
Alexander, G, Stevens, D and Bradley, L 1987. Fostering in sheep – fostering lambs onto ewes whose lambs have died soon after birth. Australian Journal of Experimental Agriculture 27, 765–769.CrossRefGoogle Scholar
Alexander, G, Stevens, D and Bradley, L 1989. Fostering in sheep – an exploratory comparison of several approaches. Australian Journal of Experimental Agriculture 29, 509–512.Google Scholar
Alexander, G, Stevens, D and Bradley, L 1990. Distribution of field birth-sites of lambing ewes. Australian Journal of Experimental Agriculture 30, 759–767.CrossRefGoogle Scholar
Alexander, G, Stevens, D, Kilgour, R, de Langen, H, Mottershead, BE and Lynch, JJ 1983. Separation of ewes from twin lambs: incidence in several sheep breeds. Applied Animal Ethology 10, 301–317.CrossRefGoogle Scholar
Arnold, GW and Morgan, PD 1975. Behaviour of the ewe and lamb at lambing and its relationship to lamb mortality. Applied Animal Ethology 2, 25–46.CrossRefGoogle Scholar
Arnould, C, Piketty, V and Lévy, F 1991. Behavior of ewes at parturition towards amniotic fluids of sheep, cows and goats. Applied Animal Behaviour Science 32, 191–196.CrossRefGoogle Scholar
Atkins, KD 1980. The comparative productivity of five breeds of ewe: 1. Lamb growth and survival. Australian Journal of Experimental Agriculture and Animal Husbandry 20, 272–279.CrossRefGoogle Scholar
Avital, E and Jablonka, E 1994. Social learning and evolution of behaviour. Animal Behaviour 48, 1195–1199.CrossRefGoogle Scholar
Basiouni, GF and Gonyou, HW 1988. Use of birth fluids and cervical stimulation in lamb fostering. Journal of Animal Science 66, 872–879.CrossRefGoogle ScholarPubMed
Bates, JE, Wachs, TD and Vandenbos, GR 1995. Trends in research on temperament. Psychiatric Services 46, 661–663.Google ScholarPubMed
Beausoleil, NJ, Blache, D, Stafford, KJ, Mellor, DJ and Noble, ADL 2008. Exploring the basis of divergent selection for ‘temperament’ in domestic sheep. Applied Animal Behaviour Science 109, 261–274.CrossRefGoogle Scholar
Beausoleil, NJ, Blache, D, Stafford, KJ, Mellor, DJ and Noble, ADL 2012. Selection for temperament in sheep: domain-general and context-specific traits. Applied Animal Behaviour Science 139, 74–85.CrossRefGoogle Scholar
Bickell, SL, Nowak, R, Poindron, P, Ferguson, D and Blache, D 2010. Maternal behaviour at parturition in outdoor conditions differs only moderately between single-bearing ewes selected for their calm or nervous temperament. Animal Production Science 50, 675–682.Google Scholar
Bickell, S, Poindron, P, Nowak, R, Ferguson, D, Blackberry, M and Blache, D 2011. Maternal behaviour and peripartum levels of oestradiol and progesterone show little difference in Merino ewes selected for calm or nervous temperament under indoor housing conditions. Animal 4, 608–614.CrossRefGoogle Scholar
Bickell, SL, Nowak, R, Poindron, P, Sébé, F, Chadwick, A, Ferguson, D and Blache, D 2009. Temperament does not affect the overall establishment of mutual preference between the mother and her young in sheep measured in a choice test. Developmental Psychobiology 51, 429–438.Google Scholar
Binns, SH, Cox, IJ, Rizvi, S and Green, LE 2002. Risk factors for lamb mortality on UK sheep farms. Preventive Veterinary Medicine 52, 287–303.CrossRefGoogle ScholarPubMed
Blache, D and Ferguson, D 2005. Increasing sheep meat production efficiency and animal welfare by selection for temperament – Part A. Final Report to Meat and Livestock Australia on Project SHGEN.025.Google Scholar
Broad, KD, Kendrick, KM, Sirinathsinghji, DJS and Keverne, EB 1993. Changes in oxytocin immunoreactivity and messenger RNA expression in the sheep brain during pregnancy, parturition and lactation and in response to oestrogen and progesterone. Journal of Neuroendocrinology 5, 435–444.Google Scholar
Broad, KD, Lévy, F, Evans, G, Kimura, T, Keverne, EB and Kendrick, KM 1999. Previous maternal experience potentiates the effect of parturition on oxytocin receptor mRNA expression in the paraventricular nucleus. European Journal of Neuroscience 11, 3725–3737.CrossRefGoogle ScholarPubMed
Brus, M, Meurisse, M, Franceschini, I, Keller, M and Lévy, F 2010. Evidence for cell proliferation in the sheep brain and its down-regulation by parturition and interactions with the young. Horomones and Behavior 58, 737–746.Google Scholar
Champagne, F and Meaney, MJ 2001. Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Progress in Brain Research 133, 287–302.CrossRefGoogle ScholarPubMed
Champagne, FA and Meaney, MJ 2006. Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biological Psychiatry 59, 1227–1235.Google Scholar
Cloete, JJE, Cloete, SWP and Hoffman, LC 2010. Behaviour of Merino ewes divergently selected for multiple rearing ability in response to human beings. Proceedings of the 9th World Congress on Genetics applied to Livestock Production. Retrieved July 2013 from http://www.kongressband.de/wcgalp2010/assets/pdf/0703.pdf Google Scholar
Cloete, SWP and Scholtz, AJ 1998. Lamb survival in relation to lambing and neonatal behaviour in medium wool Merinos lines divergently selected for multiple rearing ability. Australian Journal of Experimental Agriculture 38, 801–811.Google Scholar
Cloete, SWP, Scholtz, AJ, Gilmour, AR and Olivier, JJ 2002. Genetic and environmental effects on lambing and neonatal behaviour of Dormer and SA Mutton Merino lambs. Livestock Production Science 78, 183–193.CrossRefGoogle Scholar
Cloete, SWP, van Wyk, JB, Scholtz, AJ and Gilmour, AR 2003. Genetic and environmental parameters for lambing behaviour in Merino lines divergently selected for ewe multiple rearing ability. Proceedings of the New Zealand Society for Animal Production 63, 169–172.Google Scholar
Da Costa, APC, Guevara-Guzman, RG, Ohkura, S, Goode, JA and Kendrick, KM 1996. The role of oxytocin release in the paraventricular nucleus in the control of maternal behaviour in the sheep. Journal of Neuroendocrinology 8, 163–177.CrossRefGoogle ScholarPubMed
Darwish, RA and Ashmawy, TAM 2011. The impact of lambing stress on post-parturient behaviour of sheep with consequences on neonatal homeothermy and survival. Theriogenology 76, 999–1005.Google Scholar
Darwish, RA, Abou-Ismail, UA and El-Kholya, SZ 2010. Differences in post-parturient behaviour, lamb performance and survival rate between purebred Egyptian Rahmani and its crossbred Finnish ewes. Small Ruminant Research 89, 57–61.CrossRefGoogle Scholar
Dodd, CL, Pitchford, WS, Edwards, JEH and Hazel, SJ 2012. Measures of behavioural reactivity and their relationships with production traits in sheep: a review. Applied Animal Behaviour Science 140, 1–15.Google Scholar
Dwyer, CM 2003. Behavioural development in the neonatal lamb: effect of maternal and birth-related factors. Theriogenology 59, 1027–1050.Google Scholar
Dwyer, CM 2008a. Individual variation in the expression of maternal behaviour: a review of the neuroendocrine mechanisms in the sheep (Ovis aries). Journal of Neuroendocrinology 20, 526–535.Google Scholar
Dwyer, CM 2008b. Genetic and physiological effects on maternal behavior and lamb survival. Journal of Animal Science 86, E246–E258.Google Scholar
Dwyer, CM and Lawrence, AB 1997. Induction of maternal behaviour in non-pregnant, hormone-primed ewes. Animal Science 65, 403–408.CrossRefGoogle Scholar
Dwyer, CM and Lawrence, AB 1998. Variability in the in expression of maternal behaviour in primiparous sheep: effects of genotype and litter size. Applied Animal Behaviour Science 58, 311–330.Google Scholar
Dwyer, CM and Lawrence, AB 2000. Maternal behaviour in domestic sheep (Ovis aries): constancy and change with maternal experience. Behaviour 137, 1391–1413.CrossRefGoogle Scholar
Dwyer, CM and Lawrence, AB 2005a. A review of the behavioural and physiological adaptations of extensively managed breeds of sheep that favour lamb survival. Applied Animal Behaviour Science 92, 235–260.Google Scholar
Dwyer, CM and Lawrence, AB 2005b. Frequency and cost of human intervention at lambing: an interbreed comparison. The Veterinary Record 157, 101–104.Google Scholar
Dwyer, CM and Morgan, CA 2006. Maintenance of body temperature in the neonatal lamb: effects of breed, birth weight and litter size. Journal of Animal Science 84, 1093–1101.Google 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.CrossRefGoogle Scholar
Dwyer, CM and Bünger, L 2012. Factors affecting dystocia and offspring vigour in different sheep genotypes. Preventive Veterinary Medicine 103, 257–264.CrossRefGoogle ScholarPubMed
Dwyer, CM, Dingwall, WA and Lawrence, AB 1999. Physiological correlates of maternal-offspring behaviour in sheep: a factor analysis. Physiology and Behavior 67, 443–454.Google Scholar
Dwyer, CM, Gilbert, CL and Lawrence, AB 2004. Pre-partum plasma estradiol and post-partum cortisol, but not oxytocin, are associated with individual differences in the expression of maternal behavior in sheep. Hormones and Behavior 46, 529–543.Google Scholar
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, 123–136.CrossRefGoogle ScholarPubMed
Dwyer, CM, McLean, KA, Deans, LA, Chirnside, J, Calvert, SK and Lawrence, AB 1998. Vocalisations between mother and young in the sheep: effects of breed and maternal experience. Applied Animal Behaviour Science 58, 105–119.Google Scholar
Fisher, MW 2003. New Zealand narratives of the benefits of reduced human intervention during lambing in extensive farming systems. Journal of Agricultural and Environmental Ethics 16, 77–90.CrossRefGoogle Scholar
Fuchs, AR, Ayromlooi, J and Rasmussen, AB 1987. Oxytocin response to conditioned and nonconditioned stimuli in lactating ewes. Biology of Reproduction 37, 301–305.CrossRefGoogle ScholarPubMed
Gonyou, HW and Stookey, JM 1983. Use of lambing cubicles and the behaviour of ewes at parturition. Journal of Animal Science 56, 787–791.Google Scholar
Gonyou, HW and Stookey, JM 1985. Behavior of parturient ewes in group-lambing pens with and without cubicles. Applied Animal Behaviour Science 14, 163–171.Google Scholar
Goursaud, AP and Nowak, R 1999. Colostrum mediates the development of mother preference by newborn lambs. Physiology and Behavior 67, 49–56.Google Scholar
Hall, DG, Holst, PJ and Shutt, DA 1992. The effect of nutritional supplements in late pregnancy on ewe colostrum production, plasma progesterone and IGF-1 concentrations. Australian Journal of Agricultural Research 43, 325–337.Google Scholar
Hawken, PAR, Luckins, N, Tilbrook, A, Fiol, C, Martin, GB and Blache, D 2013. Genetic selection for temperament affects behaviour and the secretion of adrenal and reproductive hormones in sheep subjected to stress. Stress 16, 130–142.Google Scholar
Hild, S, Coulon, M, Schroeer, A, Andersen, IL and Zanella, AJ 2011. Gentle vs. aversive handling of pregnant ewes: I. Maternal cortisol and behaviour. Physiology and Behavior 104, 384–391.CrossRefGoogle Scholar
Hinch, GN, Lynch, JJ, Nolan, JV, Leng, RA, Bindon, BM and Piper, LR 1996. Supplementation of high fecundity Border Leicester×Merino ewes with a high protein feed: its effect on lamb survival. Australian Journal of Experimental Agriculture 36, 129–136.Google Scholar
Hough, D, Swart, P and Cloete, S 2013. Exploration of the hypothalamic-pituitary-adrenal axis to improve animal welfare by means of genetic selection: lessons from the South African Merino. Animals 3, 442–474.Google Scholar
Hydbring, E, Madej, A, MacDonald, E, Drugge-Boholm, C, Berglund, B and Olsson, K 1999. Hormonal changes during parturition in heifers and goats are related to the phases and severity of labour. Journal of Endocrinology 160, 75–85.Google 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, 68–80.Google Scholar
Keller, M, Meurisse, M, Poindron, P, Nowak, R, Shayit, M, Ferreira, G and Lévy, F 2003. Maternal experience influences the establishment of visual/auditory, but not of olfactory recognition of the newborn lamb by ewes at parturition. Developmental Psychobiology 43, 167–176.CrossRefGoogle Scholar
Kendrick, KM 2000. Oxytocin, motherhood and bonding. Experimental Physiology 85, 111S–124S.CrossRefGoogle ScholarPubMed
Kendrick, KM and Keverne, EB 1991. Importance of progesterone and estrogen priming for the induction of maternal behavior by vaginocervical stimulation in sheep: effects of maternal experience. Physiology and Behavior 49, 745–750.Google Scholar
Kendrick, KM, Lévy, F and Keverne, EB 1992a. Changes in the sensory processing of olfactory signals induced by birth in sheep. Science 256, 833–836.Google Scholar
Kendrick, KM, da Costa, AP, Hinton, MR and Keverne, EB 1992b. A simple method for fostering lambs using anestrous ewes with artificially induced lactation and maternal behaviour. Applied Animal Behaviour Science 34, 345–357.Google Scholar
Kendrick, KM, da Costa, APC, Broad, KD, Ohkura, S, Guevara, R, Lévy, F and Keverne, EB 1997. Neural control of maternal behaviour and olfactory recognition of the young. Brain Research Bulletin 44, 383–395.Google Scholar
Keverne, EB and Kendrick, KM 1992. Oxytocin facilitation of maternal behaviour in sheep. Annals of the New York Academy of Sciences 652, 83–101.Google Scholar
Keverne, EB, Lévy, F, Guevara-Guzman, R and Kendrick, KM 1993. Influence of birth and maternal experience on olfactory bulb neurotransmitter release. Neuroscience 56, 557–565.Google Scholar
Kikusui, T, Isaka, Y and Mori, Y 2005. Early weaning deprives mouse pups of maternal care and decreases their maternal behavior in adulthood. Behavioural Brain Research 162, 200–206.Google Scholar
Kilgour, RJ and Szantar-Coddington, MR 1995. Arena behavior of ewes selected for superior mothering ability differs from that of unselected ewes. Animal Reproduction Science 37, 133–141.Google Scholar
Kleeman, DO, Walker, SK, Walkley, JRW, Ponzoni, RW, Smith, DH, Grimson, RJ and Seamark, RF 1993. Effect of nutrition during pregnancy on birth weight and lamb survival in FecB Booroola×South Australian Merino ewes. Animal Reproduction Science 31, 213–224.Google Scholar
Krehbiel, D, Poindron, P, Lévy, F and Prud’homme, MJ 1987. Peridural anesthesia disturbs maternal behaviour in primiparous and multiparous parturient ewes. Physiology and Behavior 40, 463–472.Google Scholar
Le Neindre, P, Murphy, PM, Boissy, A, Purvis, IW, Lindsay, D, Orgeur, P, Bouix, J and Bibé, B 1998. Genetics of maternal ability in cattle and sheep. Proceedings of the 6th World Congress of the Genetics of Livestock Production 27, 23–30.Google Scholar
Lent, PC 1974. Mother-infant relationships in ungulates. In The behaviour of ungulates and its relationship to management, IUCN Publication No. 24 (ed. V Geist and F Walther), pp. 14–55. International Union for the Conservation of Nature, Morges, Switzerland.Google Scholar
Lévy, F and Poindron, P 1987. The importance of amniotic fluids for the establishment of maternal behaviour in experienced and inexperienced ewes. Animal Behaviour 35, 1188–1192.Google Scholar
Lévy, F, Poindon, P and Le Neindre, P 1983. Attraction and repulsion by amniotic fluids and their olfactory control in the ewe around parturition. Physiology and Behavior 31, 687–692.Google Scholar
Lévy, F, Gheusi, G and Keller, M 2011. Plasticity of the parental brain: a case for neurogenesis. Journal of Neuroendocrinology 23, 984–993.Google Scholar
Lévy, F, Kendrick, KM, Keverne, EB, Piketty, V and Poindron, P 1992. Intracerebral oxytocin is important for the onset of maternal behavior in inexperienced ewes delivered under peridural anesthesia. Behaviour Neuroscience 106, 427–432.Google Scholar
Lévy, F, Guevara-Guzman, R, Hinton, MR, Kendrick, KM and Keverne, EB 1993. Effects of parturition and maternal experience on noradrenaline and acetylcholine release in the olfactory bulb of sheep. Behavioural Neuroscience 107, 662–668.Google Scholar
Lévy, F, Kendrick, KM, Goode, JA, Guevara-Guzman, R and Keverne, EB 1995. Oxytocin and vasopression release in the olfactory bulb of parturient ewes – changes with maternal experience and effects on acetylcholine, gamma-aminobutyric acid, glutamate and noradrenaline release. Brain Research 669, 197–206.Google Scholar
Lévy, F, Gervais, R, Kinderman, U, Litterio, M, Poindron, P and Porter, R 1991. Effects of early postpartum separation on maternal selectivity and responsiveness in parturient ewes. Applied Animal Behaviour Science 31, 101–110.Google Scholar
Lindsay, DR, Nowak, R, Putu, IG and McNeill, D 1990. 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 (ed. CM Oldham, GB Martin and IW Purvis), pp. 191–205. University of Western Australia, Perth, Australia.Google Scholar
Matheson, SM, Bünger, L and Dwyer, CM 2012. Genetic parameters for fitness and neonatal behavior traits in sheep. Behavior Genetics 42, 899–911.Google Scholar
Matheson, SM, Rooke, JA, McIlvaney, KM, Ison, S, Jack, M, Bunger, L, Ashworth, CJ and Dwyer, CM 2011. Development and validation of ‘on-farm’ behavioural scoring systems to assess birth assistance and lamb vigour. Animal 5, 776–783.CrossRefGoogle ScholarPubMed
Mellor, DJ and Murray, L 1985. Effects of maternal nutrition on udder development during late pregnancy and on colostrum production in Scottish Blackface ewes with twin lambs. Research in Veterinary Science 39, 230–234.Google Scholar
Mellor, DJ, Dingwall, RA and King, TJ 1993. Successful fostering of orphan lambs by non-pregnant ewes induced to lactate using exogenous hormone treatment. New Zealand Veterinary Journal 41, 200–204.CrossRefGoogle ScholarPubMed
Mellor, DJ, Flint, DJ, Vernon, RG and Forsyth, IA 1987. Relationships between plasma hormone concentrations, udder development and the production of early mammary secretions in twin-bearing ewes on different planes of nutrition. Quarterly Journal of Experimental Physiology and Cognate Medical Sciences 72, 345–356.Google Scholar
Meurisse, M, Gonzalez, A, Delsol, G, Caba, D, Lévy, F and Poindron, P 2005. Estradiol receptor-alpha expression in hypothalamic and limbic regions of ewes is influenced by physiological state and maternal experience. Hormones and Behavior 48, 34–43.Google Scholar
Murphy, PM, Purvis, IW, Lindsay, DR, LeNeindre, P, Orgeur, P and Poindron, P 1994. Measures of temperament are highly repeatable in Merino sheep and some are related to maternal behaviour. Proceedings of the Australian Society for Animal Production 20, 247–248.Google Scholar
Nelson, EE and Panksepp, J 1998. Brain substrates of infant-mother attachment: contributions of opioids, oxytocin, and norepinephrine. Neuroscience and Biobehavioural Reviews 22, 437–452.Google Scholar
O’Doherty, JV and Crosby, TF 1996. The effect of diet in late pregnancy on progesterone concentration and colostrum yield in ewes. Theriogenology 46, 233–241.Google Scholar
Otal, J, Lévy, F, Cornilleau, F, Moussu, C, Keller, M and Poindron, P 2009. Preventing physical interactions between parturient ewes and their neonate differentially impairs the development of maternal responsiveness and selectivity depending on maternal experience. Applied Animal Behaviour Science 120, 140–149.Google Scholar
Packer, C, Lewis, S and Pusey, A 1992. A comparative analysis of non-offspring nursing. Animal Behaviour 43, 265–281.Google Scholar
Patin, V, Lordi, B, Vincent, A, Thoumas, JL, Vaudry, H and Caston, J 2002. Effects of prenatal stress on maternal behavior in the rat. Developmental Brain Research 139, 1–8.Google Scholar
Pedersen, CA and Boccia, ML 2002. Oxytocin links mothering received, mothering bestowed and adult stress responses. Stress 5, 259–267.Google Scholar
Pena, CJ and Champagne, FA 2013. Implications of temporal variation in maternal care for the prediction of neurobiological and behavioral outcomes in offspring. Behavioral Neuroscience 127, 33–46.Google Scholar
Perrin, G, Meurisse, M and Lévy, F 2007. Inactivation of the medial preoptic area or the bed nucleus of the stria tenninalis differentially disrupts maternal behavior in sheep. Hormones and Behavior 52, 461–473.Google Scholar
Pickup, HE and Dwyer, CM 2011. Breed differences in the expression of maternal care at parturition persist throughout the lactation period in sheep. Applied Animal Behaviour Science 132, 33–41.Google Scholar
Plush, KJ, Hebart, ML, Brien, FD and Hynd, PI 2011. The genetics of temperament in Merino sheep and relationships with lamb survival. Applied Animal Behaviour Science 134, 130–136.Google Scholar
Poindron, P, Lévy, F and Keller, M 2007. Maternal responsiveness and maternal selectivity in sheep and goats: the two facets of maternal attachment. Developmental Psychobiology 49, 54–70.Google Scholar
Poindron, P, Le Neindre, P, Lévy, F and Keverne, EB 1984. The physiological mechanisms of the acceptance of the newborn among sheep. Biology of Behaviour 9, 65–88.Google Scholar
Poindron, P, Otal, J, Ferreira, G, Keller, M, Guesdon, V, Nowak, R and Lévy, F 2010. Amniotic fluid is important for the maintenance of maternal responsiveness and the establishment of maternal selectivity in sheep. Animal 4, 2057–2064.Google Scholar
Price, EO, Dally, MR and Hernandez, L 2003. A note on the use of odor manipulation to facilitate the adoption of alien lambs by ewes bearing twins. Applied Animal Behaviour Science 81, 127–131.Google Scholar
Putu, IG, Poindron, P and Lindsay, DR 1988. A high level of nutrition during late pregnancy improves subsequent maternal behaviour in Merino ewes. Proceedings of the Australian Society of Animal Production 17, 294–297.Google Scholar
Rooke, JA, Houdijk, JGM, McIlvaney, KM, Ashworth, CJ and Dwyer, CM 2010. Differential effects of maternal nutrient restriction between days one and ninety of pregnancy on ewe and lamb performance and lamb parasitism of ewes in hill and lowland breeds. Journal of Animal Science 88, 3833–3842.Google Scholar
Rosenblatt, JS 2003. Outline of the evolution of behavioral and nonbehavioral patterns of parental care among the vertebrates: critical characteristics of mammalian and avian parental behaviour. Scandinavian Journal of Psychology 44, 265–271.Google Scholar
Roussel, S, Hemsworth, PH, Leruste, H, White, C, Duvaux-Ponter, C, Nowak, R and Boissy, A 2006. Repeated transport and isolation during pregnancy in ewes: effects on the reactivity to humans and to their offspring after lambing. Applied Animal Behaviour Science 97, 172–189.CrossRefGoogle Scholar
Russell, AF and Lummaa, V 2009. Maternal effects in cooperative breeders: from hymenopterans to humans. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 1143–1167.CrossRefGoogle ScholarPubMed
Shillito-Walser, E 1980. Maternal recognition and breed identity in lambs living in a mixed flock of Jacob, Clun Forest and Dalesbred sheep. Applied Animal Ethology 6, 221–231.Google Scholar
Shoji, H and Kato, K 2009. Maternal care affects the development of maternal behavior in inbred mice. Developmental Psychobiology 51, 345–357.Google Scholar
Smith, JW, Seckl, JR, Evans, AT, Costall, B and Smythe, JW 2004. Gestational stress induces post-partum depression-like behaviour and alters maternal care in rats. Psychoneuroendocrinology 29, 227–244.CrossRefGoogle ScholarPubMed
Szyf, M, Weaver, ICG, Champagne, FA, Diorio, J and Meaney, MJ 2005. Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Frontiers in Neuroendocrinology 26, 139–162.CrossRefGoogle ScholarPubMed
Szyf, M, Weaver, ICG, Cervoni, N, D'Alessio, AC, Champagne, FA and Meaney, MJ 2003. Transgenerational epigenomic imprinting by maternal behavior through DNA methylation and its reversal by histone deacetylase inhibitors. American Journal of Medical Genetics 122B, 13.Google Scholar
Thomson, AM and Thomson, W 1949. Lambing in relation to the diet of the pregnant ewe. British Journal of Nutrition 2, 290–305.Google Scholar
von Borstel, UK, Moors, E, Schichowski, C and Gauly, M 2011. Breed differences in maternal behaviour in relation to lamb (Ovis orientalis aries) productivity. Livestock Science 137, 42–48.Google Scholar
Ward, SJ, Liste, G and Tinarwo, A 2011. Attitudes of UK sheep farmers towards fostering methods: A national survey. Small Ruminant Research 99, 87–92.Google Scholar
Weaver, ICG, Cervoni, N, Champagne, FA, D'Alessio, AC, Sharma, S, Seckl, JR, Dymov, S, Szyf, M and Meaney, MJ 2004. Epigenetic programming by maternal behaviour. Nature Neuroscience 7, 847–854.Google Scholar
Young, LJ, Wang, ZX, Donaldson, R and Rissman, EF 1998. Estrogen receptor alpha is essential for the induction of oxytocin receptor by estrogen. Neuroreport 9, 933–936.Google Scholar