Hostname: page-component-848d4c4894-75dct Total loading time: 0 Render date: 2024-05-28T20:56:12.560Z Has data issue: false hasContentIssue false
  • English
  • Français

Ewe–lamb bonding behaviours at birth are affected by maternal undernutrition in pregnancy

Published online by Cambridge University Press:  09 March 2007

Cathy M. Dwyer ,
Alistair B. Lawrence ,
Stephen C. Bishop  and
Mitch Lewis
Cathy M. Dwyer*
Affiliation:
Animal Biology Division, SAC, West Mains Road, Edinburgh EH9 3JG, Scotland, UK
Alistair B. Lawrence
Affiliation:
Animal Biology Division, SAC, West Mains Road, Edinburgh EH9 3JG, Scotland, UK
Stephen C. Bishop
Affiliation:
Roslin Institute, Roslin, Midlothian EH25 9PS, Scotland, UK
Mitch Lewis
Affiliation:
Animal Biology Division, SAC, West Mains Road, Edinburgh EH9 3JG, Scotland, UK
*
*Corresponding Author: Dr C. M. Dwyer, fax +44 131 535 3121, email c.dwyer@ed.sac.ac.uk
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.

Maternal undernutrition in pregnancy results in low birth-weights and impaired postnatal survival in sheep. Largely anecdotal evidence suggests that the expression of appropriate maternal and neonate behaviours may also be disrupted by undernutrition. In the present study, we investigated the effect of a moderate (35 %) reduction in ewe nutritional intake in pregnancy on the expression of ewe–lamb bonding behaviours in primiparous Scottish Blackface ewes. Low-intake (L) ewes had significantly higher plasma progesterone than high-intake (H) ewes from mid-gestation onwards (e.g. plasma progesterone at 20 weeks (n/l): H 15·72, L 22·38, SED 1·80, P<0·001), AND A LOWER OESTRADIOL: PROGESTERONE VALUE THAN H EWES AT DELIVERY (H 0·46, L 0·35, sed 0·05, P<0·05). Lamb birth-weight was reduced in the L lambs compared with H lambs (mean body weight (kg): H 3·31, L 3·00, sed 0·14, P<0·05), but the incidence of malpresentation at delivery was greater in L lambs. L ewes spent significantly less time licking their lambs than H ewes after delivery (time grooming in 2 h after birth (%): H 56·12, L 48·17, sed 2·639, P<0·01) and were more aggressive towards the lambs. Lamb behaviours were not directly affected by maternal nutritional treatment, but lamb birth-weight had a significant effect on neonatal developmental progress. Low-birth-weight lambs were slower than heavier lambs to stand and sucked less frequently. In tests of maternal attachment to the lamb, H ewes received higher scores than L ewes at both 24 h after birth (ewes receiving high scores (%): H 41·3, L 21·4, P<0·05) and at 3 d postnatal. We conclude that even a moderate level of undernutrition impairs the attachment between ewes and lambs by affecting maternal behaviours expressed at birth. In addition, the results suggest that levels of nutrition resulting in a decrease in birth weight will affect neonatal lamb behavioural progress.

Keywords

Food restrictionPregnancyMaternal behaviourNeonate behaviour
Type
Research Article
Information
British Journal of Nutrition , Volume 89 , Issue 1 , January 2003 , pp. 123 - 136
Copyright
Copyright © The Nutrition Society 2003

References

Agriculture and Food Research Council (1993) Energy and Protein Requirements of Ruminants. Wallingford, Oxon.: CAB International.Google Scholar
Bizelis, JA, Charismiadou, MA & Rogdakis, E (2000) Metabolic changes during the perinatal period in dairy sheep in relation to level of nutrition and breed. II Early lactation. Journal of Animal Physiology and Animal Nutrition 84, 73–84.CrossRefGoogle Scholar
Broad, KD, Kendrick, KM, Sirinathsinghji, DJS & Keverne, EB (1993) Changes in oxytocin immunoreactivity and mRNA 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
Brunelli, SA, Shair, HN & Hofer, MA (1994) Hypothermic vocalisations of rat pups (Rattus norvegicus) elicit and direct maternal search behaviour. Journal of Comparative Psychology 108, 298–303.CrossRefGoogle Scholar
Budge, H, Bispham, J, Dandrea, J, Evans, E, Heasman, L, Ingleton, PM, Sullivan, C, Wilson, V, Stephenson, T & Symonds, ME (2000) Effect of maternal nutrition on brown adipose tissue and its prolactin receptor status in the fetal lamb. Pediatric Research 47, 781–786.Google Scholar
Charismiadou, MA, Bizelis, JA & Rogdakis, E (2000) Metabolic changes during the perinatal period in dairy sheep in relation to level of nutrition and breed. I Late pregnancy. Journal of Animal Physiology and Animal Nutrition 84, 61–72.Google Scholar
Clarke, L, Yakubu, DP & Symonds, ME (1997) Influence of maternal bodyweight on size, conformation and survival of newborn lambs. Reproduction, Fertility and Development 9, 509–514.Google Scholar
Cloete, SWP (1993) Observations on neonatal progress of Dormer and South African Mutton Merino lambs. South African Journal of Animal Science 23, 38–42.Google Scholar
Dauncey, MJ & Bicknell, RJ (1999) Nutrition and neurodevelopment: mechanisms of developmental dysfunction and disease in later life. Nutrition Research Reviews 12, 231–253.CrossRefGoogle ScholarPubMed
Doerr, HK, Siegel, HI & Rosenblatt, JS (1981) Effects of progesterone withdrawal and estrogen on maternal behaviour in nulliparous rats. Behavioural and Neural Biology 32, 35–44.CrossRefGoogle ScholarPubMed
Dwyer, CM, Dingwall, WS & Lawrence, AB (1999) Physiological correlates of mother–offspring behaviour in sheep: A factor analysis. Physiology and Behavior 67, 443–454.Google Scholar
Dwyer, CM & 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.CrossRefGoogle Scholar
Dwyer, CM & Lawrence, AB (2000) Maternal behaviour in domestic sheep (Ovis aries): Constancy and change with maternal experience. Behaviour 137, 1391–1413.CrossRefGoogle Scholar
Dwyer, CM, Lawrence, AB & Bishop, SC (2001) The effects of selection for lean tissue content on maternal and neonatal lamb behaviours in Scottish Blackface sheep. Animal Science 72, 555–571.CrossRefGoogle Scholar
Dwyer, CM, Lawrence, AB, Brown, HE & Simm, G (1996) The effect of ewe and lamb genotype on gestation length, lambing ease and neonatal behaviour of lambs. Reproduction, Fertility and Development 8, 1123–1129.Google Scholar
Dwyer, CM, McLean, KA, Deans, LA, Chirnside, J, Calvert, SK & Lawrence, AB (1998) Vocalisations between mother and young in the sheep: Effects of breed and maternal experience. Applied Animal Behaviour Science 58, 105–119.CrossRefGoogle Scholar
Fahrbach, SE, Morrell, JI & Pfaff, DW (1984) Oxytocin induction of short-latency maternal behaviour in nulliparous, estrogen-primed female rats. Hormones and Behavior 18, 267–286.CrossRefGoogle ScholarPubMed
Gauthier, D, Terqui, M & Mauleon, P (1983) Influence of nutrition on pre-partum plasma levels of progesterone and total oestrogens and postpartum levels of luteinising hormone and follicle-stimulating hormone in suckling cattle. Animal Production 37, 89–96.Google Scholar
Gramsbergen, A & Westerga, J (1992) Locomotor development in undernourished rats. Behavioural Brain Research 48, 57–64.CrossRefGoogle ScholarPubMed
Hall, DG, Holst, PJ & 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.CrossRefGoogle Scholar
Hinch, GN, Lynch, JJ, Nolan, JV, Leng, RA, Bindon, BM & 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.CrossRefGoogle Scholar
Kendrick, KM & 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
Keverne, EB (1988) Central mechanisms underlying the neural and neuroendocrine determinants of maternal behaviour. Psychoneuroendocrinology 13, 127–141.CrossRefGoogle ScholarPubMed
Keverne, EB & Kendrick, KM (1991) Morphine and corticotrophin-releasing factor potentiate maternal acceptance in multiparous ewes after vaginocervical stimulation. Brain Research 540, 55–62.CrossRefGoogle ScholarPubMed
Keverne, EB & 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 & Kendrick, KM (1994) Maternal behaviour in sheep and its neuroendocrine regulation. Acta Paediatrica 83, 47–56.CrossRefGoogle Scholar
Kleeman, DO, Walker, SK, Walkley, JRW, Ponzoni, RW, Smith, DH, Grimson, RJ & 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.CrossRefGoogle Scholar
Langenau, EE & Lerg, JM (1976) The effects of winter nutritional stress on maternal and neonatal behavior in penned white-tailed deer. Applied Animal Ethology 2, 207–223.CrossRefGoogle Scholar
Lévy, F, Locatelli, A, Piketty, V, Tillet, Y & Poindron, P (1995) Involvement of the main but not the accessory olfactory system in maternal behaviour of primiparous and multiparous ewes. Physiology and Behavior 57, 97–104.CrossRefGoogle Scholar
Lévy, F & Poindron, P (1987) The importance of amniotic fluids for the establishment of maternal behaviour in experienced and inexperienced ewes. Animal Behaviour 35, 1188–1192.CrossRefGoogle Scholar
McDonald, IW (1962) Ewe fertility and neonatal lamb mortality. New Zealand Veterinary Journal 10, 45–52.CrossRefGoogle Scholar
McNeilly, AS & Fraser, HM (1987) Effect of gonadotrophin-releasing hormone agonist induced suppression of LH and FSH on follicle growth and corpus luteum function in the ewe. Journal of Endocinology 115, 273–282.CrossRefGoogle ScholarPubMed
Mallard, C, Loeliger, M, Copolov, D & Rees, S (2000) Reduced number of neurons in the hippocampus and the cerebellum in the postnatal guinea-pig following intrauterine growth-restriction. Neuroscience 100, 327–333.CrossRefGoogle ScholarPubMed
Mann, GE, Lamming, GE & Fray, MD (1995) Plasma oestradiol and progesterone during early pregnancy in the cow and the effects of treatment with buserelin. Animal Reproduction Science 37, 121–131.Google Scholar
Mellor, DJ (1983) Nutritional and placental determinants of foetal growth rate in sheep and consequences for the new born lamb. British Veterinary Journal 139, 307–324.Google Scholar
Mellor, DJ, Flint, DJ, Vernon, RG & 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.CrossRefGoogle ScholarPubMed
Mellor, DJ & 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
Moore, RW, Millar, CM & Lynch, PR (1986) The effects of prenatal nutrition and type of birth and rearing of lambs on vigour, temperature and weight at birth, and weight and survival at weaning. Proceedings of the New Zealand Society of Animal Production 46, 259–262.Google Scholar
Morgane, PJ, Austin-LaFrance, R, Bronzino, J, Tonkiss, J, Diaz-Cintra, S, Cintra, L, Kemper, T & Galler, JR (1993) Prenatal malnutrition and development of the brain. Neuroscience and Biobehavioural Reviews 17, 91–128.CrossRefGoogle ScholarPubMed
Noldus, LPJJ, Trienes, RJH, Hendriksen, AHM, Jansen, H & Jansen, RG (2000) The Observer Video-Pro: New software for the collection, management, and presentation of time-structured data from videotapes and digital media files. Behavior Research Methods, Instruments, and Computers 32, 197–206.CrossRefGoogle ScholarPubMed
Nowak, R (1996) Neonatal survival: contributions from behavioural studies in sheep. Applied Animal Behaviour Science 49, 61–72.CrossRefGoogle Scholar
Nowak, R, Murphy, TM, Lindsay, DR, Alster, P, Andersson, R & Uvnäs-Moberg, K (1997) Development of a preferential relationship with the mother: importance of the sucking activity. Physiology and Behavior 62, 681–688.CrossRefGoogle ScholarPubMed
Nowak, R, Porter, RH, Lévy, F, Orgeur, P & Schaal, B (2000) Role of mother–young interactions in the survival of offspring in domestic mammals. Reviews of Reproduction 5, 153–163.Google Scholar
O'Connor, CE, Jay, NP, Nicol, AM & Beatson, PR (1985) Ewe maternal behaviour score and lamb survival. Proceedings of the New Zealand Society for Animal Production 45, 159–162.Google Scholar
O'Connor, CE, Lawrence, AB & Wood-Gush, DGM (1992) Influence of litter size and parity on maternal behaviour at parturition in Scottish Blackface sheep. Applied Animal Behaviour Science 33, 345–355.CrossRefGoogle Scholar
O'Doherty, JV & Crosby, TF (1996) The effect of diet in late pregnancy on progesterone concentration and colostrum yield in ewes. Theriogenology 46, 233–241.CrossRefGoogle ScholarPubMed
Owens, JL, Bindon, BM, Edey, TN & Piper, LR (1985) Behaviour at parturition and lamb survival of Booroola Merino sheep. Livestock Production Science 13, 359–372.CrossRefGoogle Scholar
Patterson, HD & Thompson, R (1971) Recovery of inter-block information when block sizes are unequal. Biometrika 58, 545–554.CrossRefGoogle Scholar
Pryce, CR, Abbott, DH, Hodges, JK & Martin, RD (1988) Maternal behaviour is related to prepartum urinary oestradiol levels in red-bellied tamarin monkeys. Physiology and Behaviour 44, 717–726.Google Scholar
Pryce, CR, Dobeli, M & Martin, RD (1993) Effects of sex steroids on maternal motivation in the common marmoset (Callithrix jacchus) – Development and application of an operant system with maternal reinforcement. Journal of Comparative Psychology 107, 99–115.CrossRefGoogle ScholarPubMed
Putu, IG, Poindron, P & 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
Rees, S, Mallard, C, Breen, S, Stringer, M, Cock, M & Harding, R (1998) Fetal brain injury following prolonged hypoxemia and placental insufficiency: A review. Comparative Biochemistry and Physiology 119A, 653–660.Google Scholar
Reynolds, CK & Tyrell, HF (1990) Energy metabolism in lactating and dry beef cows. Journal of Animal Science 68, Suppl. 1, 523.Google Scholar
Robinson, JJ & Aitken, RP (1985) Effects of nutrition on prenatal growth and implications for perinatal survival in lambs. In Factors Affecting the Survival of Newborn Lambs. Seminar in CEC Programme of Co-ordination of Agricultural Research, pp. 177–189 [Alexander, G, Barker, JD and Slee, J, editors]. Brussels: Commission of European Communities.Google Scholar
Robinson, JJ, McEvoy, TG & Sinclair, KD (1999) Nutritional effects on foetal growth. Animal Science 68, 315–331.CrossRefGoogle Scholar
Rosenblatt, JS (1994) Psychobiology of maternal behaviour – Contributions to the clinical understanding of maternal behaviour among humans. Acta Paediatrica 83, 3–8.Google Scholar
Rosenblatt, JS & Siegel, HI (1981) Factors governing the onset and maintenance of maternal behaviour among nonprimate mammals. In Parental Care in Mammals, pp. 13–76 [Gubernick, DJ and Klopfer, PH, editors]. New York: Plenum Press.CrossRefGoogle Scholar
Russel, AJF, Gunn, RG & Doney, JM (1968) Components of weight loss in pregnant hill ewes during winter. Animal Production 10, 43–51.CrossRefGoogle Scholar
Scales, GH, Burton, RN & Moss, RA (1986) Lamb mortality, birthweight and nutrition in late pregnancy. New Zealand Journal of Agricultural Research 29, 75–82.Google Scholar
Shillito, EE (1972) Vocalisation in sheep. Journal of Physiology 226, 45P–46P.Google Scholar
Shipka, MP & Ford, SP (1991) Relationship of circulating oestrogen and progesterone concentrations during later pregnancy and the onset phase of maternal behaviour in the ewe. Applied Animal Behaviour Science 31, 91–99.CrossRefGoogle Scholar
Thomson, AM & Thomson, W (1949) Lambing in relation to the diet of the pregnant ewe. British Journal of Nutrition 2, 290–305.CrossRefGoogle Scholar
Vincent, IC, Williams, HL & Hill, R (1985) The influence of a low-nutrient intake after mating on gestation and perinatal survival of lambs. British Veterinary Journal 141, 611–617.Google Scholar
Waterhouse, A, Roger, LC & Ash worth, SA (1992) Reducing lamb mortality in hill sheep. In Neonatal Survival and Growth. Occasional Publication of British Society of Animal Production no. 10, pp. 43–50 [Varley, MA, Williams, PEV and Lawrence, TLJ, editors]. Midlothian, UK: British Society for Animal Production.Google Scholar
Weary, DM & Fraser, D (1995) Calling by domestic piglets: reliable signals of need? Animal Behaviour 50, 1047–1055.CrossRefGoogle Scholar