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The Onset of Maternal Behavior in Sheep and Goats: Endocrine, Sensory, Neural, and Experiential Mechanisms

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Patterns of Parental Behavior

Part of the book series: Advances in Neurobiology ((NEUROBIOL,volume 27))

Abstract

In sheep and goats, the onset of maternal behavior at parturition is characterized by a first phase called maternal responsiveness during which the mother is attracted to any newborn. In a second phase, called maternal selectivity, the mother establishes a selective bond with her young so that she only accepts it at suckling. After a description of the behavioral expression of both phases, this chapter reviews the physiological, sensory, and neural mechanisms involved. These two behavioral processes are synchronized with parturition by the vaginocervical stimulation induced by the expulsion of the newborn. Olfactory cues provided by the neonate are involved in maternal responsiveness and selectivity. Oxytocin supported by estrogens is the key factor for maternal responsiveness. The neural network involved in maternal responsiveness is mainly hypothalamic and is different from the circuitry involved in selectivity, which mainly concerns olfactory processing regions. Visual and auditory cues are necessary for offspring recognition at a distance. This multisensory recognition suggests that mothers form a mental image of their young. Maternal experience renders mothers more responsive to maternally relevant physiology and to young-related sensory inputs.

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References

  • Ahmadzadeh L, Hosseinkhani A, Taghizadeh A, Ghasemi-Panahi B, Hamidian G. Effect of late gestational feed restriction and glucogenic precursor on behaviour and performance of Ghezel ewes and their offspring. Appl Anim Behav Sci. 2020;231:105030.

    Article  Google Scholar 

  • Ainsworth MD, Bell SM. Attachment, exploration, and separation: illustrated by the behavior of one-year-olds in a strange situation. Child Dev. 1970;41(1):49–67.

    Article  CAS  PubMed  Google Scholar 

  • Alexander G. Odour, and the recognition of lambs by Merino ewes. Appl Anim Ethol. 1978;4:153–8.

    Article  Google Scholar 

  • Alexander G. What makes a good mother?: components and comparative aspects of maternal behaviour in ungulates. Proc Aust Soc Anim Prod. 1988;17:25–41.

    Google Scholar 

  • Alexander G, Shillito EE. Importance of visual clues from various body regions in maternal recognition of the young in Merino sheep (Ovis aries). Appl Anim Ethol. 1977;3:137–143.

    Google Scholar 

  • Alexander G, Shillito EE. Recognition of washed lambs by merino ewes. Appl Anim Ethol. 1981;7:77–86.

    Article  Google Scholar 

  • Alexander G, Stevens D. Odour cues to maternal recognition of lambs: an investigation of some possible sources. Appl Anim Ethol. 1982;9(2):165–75.

    Article  Google Scholar 

  • Alexander G, Stevens D, Bradley LR. Washing lambs and confinement as aids to fostering. Appl Anim Ethol. 1983a;10:251–61.

    Article  Google Scholar 

  • Alexander G, Stevens D, Kilgour R, de Langen H, Mottershead BE, Lynch JJ. Separation of ewes from twin lambs: incidence in several sheep breeds. Appl Anim Ethol. 1983b;10:301–17.

    Article  Google Scholar 

  • Alexander G, Stevens D, Bradley LR. Maternal behaviour in ewes following caesarian section. Appl Anim Ethol. 1988;19:273–7.

    Google Scholar 

  • Alexander G, Stevens D, Bradley LR. Distribution of field birth-sites of lambing ewes. Aust J Exp Agric. 1990a;30:759–67.

    Article  Google Scholar 

  • Alexander G, Stevens D, Bradley LR, Barwick SA. Maternal-behavior in Border Leicester, Glen Vale (Border Leicester derived) and Merino sheep. Aust J Exp Agric. 1990b;30(1):27–38.

    Article  Google Scholar 

  • Alexander G, Stevens D, Baker P, Bradley LR. The timing of birth in grazing Merino sheep. Aust J Exp Agric. 1993;33(5):557–60.

    Article  Google Scholar 

  • Allan CJ, Holst PJ, Hinch GN. Behaviour of parturient Australian bush goats. I. Doe behaviour and kid vigour. Appl Anim Behav Sci. 1991;32:55–64.

    Article  Google Scholar 

  • Arnold GW, Dudzinski ML. Maternal behaviour. In: Arnold GW, Dudzinski ML, editors. Ethology of free-ranging domestic animals. Amsterdam: Elsevier Scientific Publishing Company; 1978. p. 137–65.

    Google Scholar 

  • Arnold GW, Morgan PD. Behaviour of the ewe and lamb at lambing and its relationship to lamb mortality. Appl Anim Ethol. 1975;2(1):25–46.

    Article  Google Scholar 

  • Arnould C, Piketty V, Lévy F. Behavior of ewes at parturition toward amniotic fluids from sheep, cows and goats. Appl Anim Behav Sci. 1991;32(2-3):191–6.

    Article  Google Scholar 

  • Baldwin BA, Shillito EE. The effects of ablation of the olfactory bulbs on parturition and maternal behaviour in Soay sheep. Anim Behav. 1974;22(1):220–3.

    Article  CAS  PubMed  Google Scholar 

  • Bannerman DM, Lemaire M, Yee BK, Iversen SD, Oswald CJ, Good MA, et al. Selective cytotoxic lesions of the retrohippocampal region produce a mild deficit in social recognition memory. Exp Brain Res. 2002;142(3):395–401.

    Article  CAS  PubMed  Google Scholar 

  • Basiouni GF, Gonyou HW. Use of birth fluids and cervical stimulation in lamb fostering. J Anim Sci. 1988;66(4):872–9.

    Article  CAS  PubMed  Google Scholar 

  • Belnoue L, Malvaut S, Ladeveze E, Abrous DN, Koehl M. Plasticity in the olfactory bulb of the maternal mouse is prevented by gestational stress. Sci Rep. 2016;6:37615.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bickell SL, Nowak R, Poindron P, Ferguson D, Blache D. Maternal behaviour at parturition in outdoor conditions differs only moderately between single-bearing ewes selected for their calm or nervous temperament. Anim Prod Sci. 2010;50(7):675–82.

    Article  Google Scholar 

  • Bordi A, De Rosa G, Napolitano F, Litterio M, Marino V, Rubino R. Postpartum development of the mother-young relationship in goats. Appl Anim Behav Sci. 1994;42:145–52.

    Article  Google Scholar 

  • Bouissou MF. Effet de l’ablation des bulbes olfactifs sur la reconnaissance du jeune par sa mère chez les Ovins. Revue de Comportement Animal. 1968;2:77–83.

    Google Scholar 

  • Bridges RS. Neuroendocrine regulation of maternal behavior. Front Neuroendocrinol. 2015;36:178–96.

    Article  CAS  PubMed  Google Scholar 

  • Briefer E, McElligott AG. Mutual mother–offspring vocal recognition in an ungulate hider species (Capra hircus). Anim Cogn. 2011;14(4):585–98.

    Article  PubMed  Google Scholar 

  • Broad KD, Kendrick KM, Sirinathsinghji DJ, Keverne EB. Changes in oxytocin immunoreactivity and mRNA expression in the sheep brain during pregnancy, parturition and lactation and in response to oestrogen and progesterone. J Neuroendocrinol. 1993;5(4):435–44.

    Article  CAS  PubMed  Google Scholar 

  • Broad KD, Lévy F, Evans G, Kimura T, Keverne EB, Kendrick KM. Previous maternal experience potentiates the effect of parturition on oxytocin receptor mRNA expression in the paraventricular nucleus. Eur J Neurosci. 1999a;11(10):3725–37.

    Article  CAS  PubMed  Google Scholar 

  • Broad KD, Da Costa AP, Keverne EB, Kendrick KM, editors. The role of the pyriform cortex in olfactory memory. Society for Neuroscience Abstract; 1999b.

    Google Scholar 

  • Broad KD, Hinton MR, Keverne EB, Kendrick KM. Involvement of the medial prefrontal cortex in mediating behavioural responses to odour cues rather than olfactory recognition memory. Neuroscience. 2002;114(3):715–29.

    Article  CAS  PubMed  Google Scholar 

  • Brouette-Lahlou I, Amouroux R, Chastrett I, Cosnier J, Stoffelsma J, Vernet-Maury E. Dodecyl propionate, the attractant from rat pups preputial gland, characterization and identification. J Chem Ecol. 1991;17:1343–54.

    Article  CAS  PubMed  Google Scholar 

  • Brouette-Lahlou I, Godinot F, Vernet-Maury E. The mother rat’s vomeronasal organ is involved in detection of dodecyl propionate, the pup’s preputial gland pheromone. Physiol Behav. 1999;66(3):427–36.

    Article  CAS  PubMed  Google Scholar 

  • Brown DJ, Fogarty NM, Iker CL, Ferguson DM, Blache D, Gaunt GM. Genetic evaluation of maternal behaviour and temperament in Australian sheep. Anim Prod Sci. 2016;56(4):767–74.

    Article  Google Scholar 

  • Brus M, Meurisse M, Franceschini I, Keller M, Lévy F. Evidence for cell proliferation in the sheep brain and its down-regulation by parturition and interactions with the young. Horm Behav. 2010;58(5):737–46.

    Article  CAS  PubMed  Google Scholar 

  • Brus M, Meurisse M, Keller M, Lévy F. Interactions with the young down-regulate adult olfactory neurogenesis and enhance the maturation of olfactory neuroblasts in sheep mothers. Front Behav Neurosci. 2014;8.

    Google Scholar 

  • Burger BV, Viviers MZ, Le Roux NJ, Morris J, Bekker JPI, Le Roux M. Olfactory cue mediated neonatal recognition in sheep, Ovis aries. J Chem Ecol. 2011;37(10):1150–63.

    Article  CAS  PubMed  Google Scholar 

  • Butz M, Teuchert-Noodt G, Grafen K, van Ooyen A. Inverse relationship between adult hippocampal cell proliferation and synaptic rewiring in the dentate gyrus. Hippocampus. 2008;18(9):879–98.

    Article  PubMed  Google Scholar 

  • Caba M, Poindron P, Krehbiel D, Lévy F, Romeyer A, Vénier G. Naltrexone delays the onset of maternal behavior in primiparous parturient ewes. Pharmacol Biochem Behav. 1995;52(4):743–8.

    Article  CAS  PubMed  Google Scholar 

  • Challis JRG, Linzell JL. The concentration of total unconjugated oestrogens in the plasma of pregnant goats. Reprod Fertil Dev. 1971;26:401–4.

    Article  CAS  Google Scholar 

  • Chamley WA, Buckmaster J, Cereni ME, Cumming IA, Goding JR, Obst JM, et al. Changes in the levels of progesterone, corticosteroids, estrone, oestradiol-17ß, luteinizing hormone and prolactin in the peripheral plasma of the ewe during late pregnancy and at parturition. Biol Reprod. 1973;9:30–5.

    Article  CAS  PubMed  Google Scholar 

  • Cloete SWP, Scholtz AJ, Ten Hoope JM, Lombard PJA, Franken MC. Ease of birth relation to pelvic dimensions, litter weight and conformation of sheep. Small Rumin Res. 1998;31(1):51–60.

    Article  Google Scholar 

  • Cloete SWP, Scholtz AJ, Taljaard R. Lambing behaviour of Merino ewes from lines subjected to divergent selection for multiple rearing ability from the same base population. S Afr J Anim Sci. 2002;32(1):57–65.

    Article  Google Scholar 

  • Cohen L, Rothschild G, Mizrahi A. Multisensory integration of natural odors and sounds in the auditory cortex. Neuron. 2011;72(2):357–69.

    Article  CAS  PubMed  Google Scholar 

  • Collias NE. The analysis of socialization in sheep and goats. Ecology. 1956;37(2):228–39.

    Article  Google Scholar 

  • Corner RA, Kenyon PR, Stafford KJ, West DM, Morris ST, Oliver MH. The effects of pasture availability for twin- and triplet-bearing ewes in mid and late pregnancy on ewe and lamb behaviour 12 to 24 h after birth. Animal. 2010;4(1):108–15.

    Article  CAS  PubMed  Google Scholar 

  • Corona R, Meurisse M, Cornilleau F, Moussu C, Keller M, Lévy F. Exposure to young preferentially activates adult-born neurons in the main olfactory bulb of sheep mothers. Brain Struct Funct. 2017;222(3):1219–29.

    Article  CAS  PubMed  Google Scholar 

  • Corona R, Meurisse M, Cornilleau F, Moussu C, Keller M, Lévy F. Disruption of adult olfactory neurogenesis induces deficits in maternal behavior in sheep. Behav Brain Res. 2018;347:124–31.

    Article  CAS  PubMed  Google Scholar 

  • Coulon M, Lévy F, Ravel C, Nowak R, Boissy A. Mild effects of gestational stress and social reactivity on the onset of mother-young interactions and bonding in sheep. Stress. 2014;17(6):460–70.

    Article  PubMed  Google Scholar 

  • Currie WB, Gorewit RC, Michel FJ. Endocrine changes, with special reference on estradiol 17-beta, prolactin and oxytocin before and during labour and delivery in goats. J Reprod Fertil. 1988;82:299–308.

    Article  CAS  PubMed  Google Scholar 

  • Da Costa AP, Guevara-Guzman RG, Ohkura S, Goode JA, Kendrick KM. The role of oxytocin release in the paraventricular nucleus in the control of maternal behaviour in the sheep. J Neuroendocrinol. 1996;8(3):163–77.

    Article  PubMed  Google Scholar 

  • Da Costa AP, Broad KD, Kendrick KM. Olfactory memory and maternal behaviour-induced changes in c-fos and zif/268 mRNA expression in the sheep brain. Brain Res Mol Brain Res. 1997;46(1-2):63–76.

    Article  PubMed  Google Scholar 

  • Das N, Tomer OS. Time pattern on parturition sequences in Beetal goats and crosses: comparison between primiparous and multiparous does. Small Rumin Res. 1997;26(1-2):157–61.

    Article  Google Scholar 

  • Davis SL, Reichert LE, Niswender LE. Serum levels of prolactin as measured by radioimmunoassay. Biol Reprod. 1971;4:145–7.

    Article  CAS  PubMed  Google Scholar 

  • Dwyer CM. Individual variation in the expression of maternal behaviour: a review of the neuroendocrine mechanisms in the sheep. J Neuroendocrinol. 2008a;20(4):526–34.

    Article  CAS  PubMed  Google Scholar 

  • Dwyer CM. Genetic and physiological determinants of maternal behavior and lamb survival: implications for low-input sheep management1,2. J Anim Sci. 2008b;86(suppl_14):E246–E58.

    Article  Google Scholar 

  • Dwyer CM, Lawrence AB. Variability in the expression of maternal behaviour in primiparous sheep: effects of genotype and litter size. Appl Anim Behav Sci. 1998;58(3-4):311–30.

    Article  Google Scholar 

  • Dwyer CM, Lawrence AB. Does the behaviour of the neonate influence the expression of maternal behaviour in sheep? Behaviour. 1999a;136:367–89.

    Article  Google Scholar 

  • Dwyer CM, Lawrence AB. Ewe-ewe and ewe-lamb behaviour in a hill and a lowland breed of sheep: a study using embryo transfer. Appl Anim Behav Sci. 1999b;61(4):319–34.

    Article  Google Scholar 

  • Dwyer CM, Lawrence AB. Effects of maternal genotype and behaviour on the behavioural development of their offspring in sheep. Behaviour. 2000a;137(12):1629–54.

    Article  Google Scholar 

  • Dwyer CM, Lawrence AB. Maternal behaviour in domestic sheep (Ovis aries): constancy and change with maternal experience. Behaviour. 2000b;137(10):1391–413.

    Article  Google Scholar 

  • Dwyer CM, Lawrence AB, Brown HE, Simm G. Effect of ewe and lamb genotype on gestation length, lambing ease and neonatal behaviour of lambs. Reprod Fertil Dev. 1996;8(8):1123–9.

    Article  CAS  PubMed  Google Scholar 

  • Dwyer CM, McLean KA, Deans LA, Chirnside J, Calvert SK, Lawrence AB. Vocalisations between mother and young in sheep: effects of breed and maternal experience. Appl Anim Behav Sci. 1998;58(1-2):105–19.

    Article  Google Scholar 

  • Dwyer CM, Lawrence AB, Bishop SC. The effects of selection for lean tissue content on maternal and neonatal lamb behaviours in Scottish Blackface sheep. Anim Sci. 2001;72:555–71.

    Article  Google Scholar 

  • Dwyer CM, Lawrence AB, Bishop SC, Lewis M. Ewe–lamb bonding behaviours at birth are affected by maternal undernutrition in pregnancy. Br J Nutr. 2003;89(1):123–36.

    Article  CAS  PubMed  Google Scholar 

  • Echeverri AC, Gonyou HW, Ghent AW. Preparturient behavior of confined ewes: time budgets, frequencies, spatial distribution and sequential analysis. Appl Anim Behav Sci. 1992;34(4):329–44.

    Article  Google Scholar 

  • Ekiz B, Kocak O, Ozcan M, Yilmaz A. Effects of parity and litter size on maternal behaviour in Kivircik ewes. Acta Agriculturae Scandinavica Section A-Animal Science. 2007;57(2):81–8.

    Article  Google Scholar 

  • Everett-Hincks JM, Cullen NG. Genetic parameters for ewe rearing performance1. J Anim Sci. 2009;87(9):2753–8.

    Article  CAS  PubMed  Google Scholar 

  • Everett-Hincks JM, Blair HT, Stafford KJ, Lopez-Villalobos N, Kenyon PR, Morris ST. The effect of pasture allowance fed to twin- and triplet-bearing ewes in late pregnancy on ewe and lamb behaviour and performance to weaning. Livest Prod Sci. 2005;97(2–3):253–66.

    Article  Google Scholar 

  • Fahmy MH, Robert S, Castonguay F. Ewe and lamb behaviour at parturition in prolific and non-prolific sheep. Can J Anim Sci. 1997;77(1):9–15.

    Article  Google Scholar 

  • Farrell WJ, Alberts JR. Maternal responsiveness to infant rat ultrasonic vocalizations during the maternal behavior cycle and following steroid and experiential induction regimens. J Comp Psychol. 2002;116:286–96.

    Article  PubMed  Google Scholar 

  • Ferreira G, Gervais R, Durkin TP, Lévy F. Postacquisition scopolamine treatments reveal the time course for the formation of lamb odor recognition memory in parturient ewes. Behav Neurosci. 1999;113(1):136–42.

    Article  CAS  PubMed  Google Scholar 

  • Ferreira G, Terrazas A, Poindron P, Nowak R, Orgeur P, Lévy F. Learning of olfactory cues is not necessary for early lamb recognition by the mother. Physiol Behav. 2000;69(4–5):405–12.

    Article  CAS  PubMed  Google Scholar 

  • Ferreira G, Meurisse M, Gervais R, Ravel N, Lévy F. Extensive immunolesions of basal forebrain cholinergic system impair offspring recognition in sheep. Neuroscience. 2001;106(1):103–15.

    Article  CAS  PubMed  Google Scholar 

  • Ferreira G, Keller M, Saint-Dizier H, Perrin G, Levy F. Transfer between views of conspecific faces at different ages or in different orientations by sheep. Behav Process. 2004;67(3):491–499. https://doi.org/10.1016/j.beproc.2004.08.005

  • Fleming AS, Li M. Psychobiology of maternal behavior and its early determinants in nonhuman mammals. In: Bornstein MH, editor. Handbook of parenting. 2nd ed. Mahwah: Lawrence Erlbaum Associates; 2002. p. 61–97.

    Google Scholar 

  • Gheusi G, Lledo PM. Control of early events in olfactory processing by adult neurogenesis. Chem Senses. 2007;32(4):397–409.

    Article  PubMed  Google Scholar 

  • Gonyou HW, Stookey JM. Use of lambing cubicles and the behavior of ewes at parturition. J Anim Sci. 1983;56(4):787–91.

    Article  CAS  PubMed  Google Scholar 

  • Gonyou HW, Stookey JM. Behavior of parturient ewes in group-lambing pens with and without cubicles. Appl Anim Behav Sci. 1984;14(2):163–71.

    Article  Google Scholar 

  • Gonzalez EGY, Cuellar A, Hernandez H, Nandayapa E, Alvarez L, Tortora J, et al. Maternal experience in Romanov sheep impairs mother-lamb recognition during the first 24 hours postpartum. J Vet Behav Clin Appl Res. 2015;10(1):66–72.

    Article  Google Scholar 

  • Gonzalez-Mariscal G, Poindron P. Parental care in mammals: immediate internal and sensory factors of control. Hormones, brain and behavior. I. Elsevier Science; 2002. p. 215–98.

    Google Scholar 

  • Gonzalez-Stagnaro C, Madrid-Bury N. Parturition in native goats. Revista Cientifica-Facultad De Ciencias Veterinarias. 2004;14(2):124–32.

    Google Scholar 

  • Gubernick DJ. Mechanisms of maternal “labelling” in goats. Anim Behav. 1981;29:305–6.

    Article  Google Scholar 

  • Gubernick DJ, Corbeau Jones K, Klopfer PH. Maternal imprinting in goats? Anim Behav. 1979;27:314–5.

    Article  Google Scholar 

  • Hazard D, Mace T, Kempeneers A, Delval E, Foulquie D, Bouix J, et al. Genetic parameters estimates for ewes’ behavioural reactivity towards their litter after lambing. J Anim Breed Genet. 2020;137(4):374–83.

    Article  PubMed  Google Scholar 

  • Hernandez H, Serafin N, Terrazas A, Marnet P, Kann G, Delgadillo J, et al. Maternal olfaction differentially modulates oxytocin and prolactin release during suckling in goats. Horm Behav. 2002;42(2):232–44.

    Article  CAS  PubMed  Google Scholar 

  • Herscher L, Richmond JB, Moore AU. Maternal behavior in sheep and goats. In: Rheingold HL, editor. Maternal behavior in mammals. New York: Wiley; 1963. p. 203–32.

    Google Scholar 

  • Hydbring E, Madej A, MacDonald E, Drugge B, Berglund B, Olsson K. Hormonal changes during parturition in heifers and goats are related to the phases and severity of labour. J Endocrinol. 1999;160:75–85.

    Article  CAS  PubMed  Google Scholar 

  • Kasikci D. Maternal behaviors of Saanen × Hair Goat crosses at partum and early postpartum doe-kid relationships. Appl Ecol Environ Res. 2018;16(6):7791–8.

    Article  Google Scholar 

  • Keil NM, Imfeld-Mueller S, Aschwanden J, Wechsler B. Are head cues necessary for goats (Capra hircus) in recognising group members? Anim Cogn. 2012;15(5):913–21.

    Article  PubMed  Google Scholar 

  • Keller M, Meurisse M, Poindron P, Nowak R, Ferreira G, Shayit M, et al. Maternal experience influences the establishment of visual/auditory, but not olfactory recognition of the newborn lamb by ewes at parturition. Dev Psychobiol. 2003;43(3):167–76.

    Article  PubMed  Google Scholar 

  • Keller M, Meurisse M, Lévy F. Mapping the neural substrates involved in maternal responsiveness and lamb olfactory memory in parturient ewes using Fos imaging. Behav Neurosci. 2004a;118(6):1274–84.

    Article  PubMed  Google Scholar 

  • Keller M, Perrin G, Meurisse M, Ferreira G, Lévy F. Cortical and medial amygdala are both involved in the formation of olfactory offspring memory in sheep. Eur J Neurosci. 2004b;20(12):3433–41.

    Article  PubMed  Google Scholar 

  • Keller M, Meurisse M, Lévy F. Mapping of brain networks involved in consolidation of lamb recognition memory. Neuroscience. 2005;133(2):359–69.

    Article  CAS  PubMed  Google Scholar 

  • Kendrick KM. Neurobiological correlates of visual and olfactory recognition in sheep. Behav Process. 1994;33:89–112.

    Article  CAS  Google Scholar 

  • Kendrick KM. Oxytocin, motherhood and bonding. Exp Physiol. 2000;85:111–24.

    Article  Google Scholar 

  • Kendrick KM, Keverne EB. Importance of progesterone and estrogen priming for the induction of maternal behavior by vaginocervical stimulation in sheep: effects of maternal experience. Physiol Behav. 1991;49(4):745–50.

    Article  CAS  PubMed  Google Scholar 

  • Kendrick KM, Keverne EB. Control of synthesis and release of oxytocin in the sheep brain. Ann N Y Acad Sci. 1992;652:102–21.

    Article  CAS  PubMed  Google Scholar 

  • Kendrick KM, Keverne EB, Baldwin BA, Sharman DF. Cerebrospinal fluid levels of acetylcholinesterase, monoamines and oxytocin during labour, parturition, vaginocervical stimulation, lamb separation and suckling in sheep. Neuroendocrinology. 1986;44:149–56.

    Article  CAS  PubMed  Google Scholar 

  • Kendrick KM, Keverne EB, Baldwin BA. Intracerebroventricular oxytocin stimulates maternal behaviour in the sheep. Neuroendocrinology. 1987;46:56–61.

    Article  CAS  PubMed  Google Scholar 

  • Kendrick KM, Keverne EB, Chapman C, Baldwin BA. Intracranial dialysis measurement of oxytocin, monoamine and uric acid release from the olfactory bulb and substantia nigra of sheep during parturition, suckling, separation from lambs and eating. Brain Res. 1988a;439(1-2):1–10.

    Article  CAS  PubMed  Google Scholar 

  • Kendrick KM, Keverne EB, Shapman C, Baldwin BA. Microdialysis measurement of oxytocin, aspartate, gama-aminobutyric acid and glutamate release from the olfactory bulb of the sheep during vaginocervical stimulation. Brain Res. 1988b;442:171–4.

    Article  CAS  PubMed  Google Scholar 

  • Kendrick KM, Keverne EB, Hinton MR, Goode JA. Cerebrospinal fluid and plasma concentrations of oxytocin and vasopressin during parturition and vaginocervical stimulation in the sheep. Brain Res Bull. 1991a;26(5):803–7.

    Article  CAS  PubMed  Google Scholar 

  • Kendrick KM, Lévy F, Keverne EB. Importance of vaginocervical stimulation for the formation of maternal bonding in primiparous and multiparous parturient ewes. Physiol Behav. 1991b;50(3):595–600.

    Article  CAS  PubMed  Google Scholar 

  • Kendrick KM, Keverne EB, Hinton MR, Goode JA. Oxytocin, amino acid and monoamine release in the region of the medial preoptic area and bed nucleus of the stria terminalis of the sheep during parturition and suckling. Brain Res. 1992a;569(2):199–209.

    Article  CAS  PubMed  Google Scholar 

  • Kendrick KM, da Costa AP, Hinton MR, Keverne EB. A simple method for fostering lambs using anoestrus ewes with artificially induced lactation and maternal behaviour. Appl Anim Behav Sci. 1992b;34:345–57.

    Article  Google Scholar 

  • Kendrick KM, Lévy F, Keverne EB. Changes in the sensory processing of olfactory signals induced by birth in sheep. Science. 1992c;256(5058):833–6.

    Article  CAS  PubMed  Google Scholar 

  • Kendrick KM, Atkins K, Hinton MR, Heavens P, Keverne B. Are faces special for sheep? Evidence from facial and object discrimination learning tests showing effects of inversion and social familiarity. Behav Process. 1996;38:19–35.

    Google Scholar 

  • Kendrick KM, Da Costa APC, Broad KD, Ohkura S, Guevara R, Lévy F, et al. Neural control of maternal behaviour and olfactory recognition of offspring. Brain Res Bull. 1997a;44(4):383–95.

    Article  CAS  PubMed  Google Scholar 

  • Kendrick KM, Guevara-Guzman R, Zorrilla J, Hinton MR, Broad KD, Mimmack M, et al. Formation of olfactory memories mediated by nitric oxide. Nature. 1997b;388(6643):670–4.

    Article  CAS  PubMed  Google Scholar 

  • Kendrick KM, Leigh A, Peirce J. Behavioural and neural correlates of mental imagery in sheep using face recognition paradigms. Anim Welf. 2001;10:S89–S101.

    Google Scholar 

  • Keverne EB, Kendrick KM. Morphine and corticotrophin-releasing factor potentiate maternal acceptance in multiparous ewes after vaginocervical stimulation. Brain Res. 1991;540(1-2):55–62.

    Article  CAS  PubMed  Google Scholar 

  • Keverne EB, Lévy F, Poindron P, Lindsay DR. Vaginal stimulation: an important determinant of maternal bonding in sheep. Science. 1983;219(4580):81–3.

    Article  CAS  PubMed  Google Scholar 

  • Keverne EB, Lévy F, Guevara-Guzman R, Kendrick KM. Influence of birth and maternal experience on olfactory bulb neurotransmitter release. Neuroscience. 1993;56(3):557–65.

    Article  CAS  PubMed  Google Scholar 

  • Kilgour RJ, Szantar-Coddington MR. Arena behaviour of ewes selected for superior mothering ability differs from that of unselected ewes. Anim Reprod Sci. 1995;37(2):133–41.

    Article  Google Scholar 

  • Klopfer PH, Gamble J. Maternal imprinting in goats: the role of chemical senses. Zeitschrift Fur Tierpsychologie. 1966;23(5):588–92.

    Article  CAS  PubMed  Google Scholar 

  • Klopfer PH, Adams DK, Klopfer MS. Maternal imprinting in goats. Proc Natl Acad Sci U S A. 1964;52:911–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knox D. The role of basal forebrain cholinergic neurons in fear and extinction memory. Neurobiol Learn Mem. 2016;133:39–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kopel H, Schechtman E, Groysman M, Mizrahi A. Enhanced synaptic integration of adult-born neurons in the olfactory bulb of lactating mothers. J Neurosci. 2012;32(22):7519–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krehbiel D, Poindron P, Lévy F, Prud’Homme MJ. Peridural anesthesia disturbs maternal behavior in primiparous and multiparous parturient ewes. Physiol Behav. 1987;40(4):463–72.

    Article  CAS  PubMed  Google Scholar 

  • Lambe NR, Conington J, Bishop SC, Waterhouse A, Simm G. A genetic analysis of maternal behaviour score in Scottish Blackface sheep. Anim Sci. 2001;72(2):415–25.

    Article  Google Scholar 

  • Langbein J, Scheibe KM, Eichhorn K. Investigations on periparturient behaviour in free-ranging mouflon sheep (Ovis orientalis musimon). J Zool. 1998;244:553–61.

    Article  Google Scholar 

  • Lazarini F, Lledo PM. Is adult neurogenesis essential for olfaction? Trends Neurosci. 2011;34(1):20–30.

    Article  CAS  PubMed  Google Scholar 

  • Le Neindre P, Poindron P, Delouis C. Hormonal induction of maternal behavior in non-pregnant ewes. Physiol Behav. 1979;22(4):731–4.

    Article  PubMed  Google Scholar 

  • Lepousez G, Nissant A, Lledo PM. Adult neurogenesis and the future of the rejuvenating brain circuits. Neuron. 2015;86(2):387–401.

    Article  CAS  PubMed  Google Scholar 

  • Lévy F, Keller M. Olfactory mediation of maternal behavior in selected mammalian species. Behav Brain Res. 2009;200(2):336–45.

    Article  PubMed  Google Scholar 

  • Lévy F, Poindron P. Influence of amniotic fluids in the manifestation of maternal-behavior in parturient ewe. Biol Behav. 1984;9(3):271–8.

    Google Scholar 

  • Levy F, Poindron P. The importance of amniotic fluids for the establishment of maternal-behavior in experienced and inexperienced ewes. Anim Behav. 1987;35:1188–92.

    Article  Google Scholar 

  • Lévy F, Poindron P. The importance of amniotic fluids for the establishment of maternal behavior in experienced and non-experienced ewes. Anim Behav. 1987;35:1188–92.

    Article  Google Scholar 

  • Lévy F, Poindron P, Le Neindre P. Attraction and repulsion by amniotic fluids and their olfactory control in the ewe around parturition. Physiol Behav. 1983;31:687–92.

    Article  PubMed  Google Scholar 

  • Lévy F, Keverne EB, Piketty V, Poindron P. Physiological determinism of olfactory attraction for amniotic fluids in sheep. In: MacDonald DW, Müller-Schwarze D, Natynczuck SE, editors. Chemical signals in vertebrates, vol. 5. Oxford: Oxford University Press; 1990a. p. 162–5.

    Google Scholar 

  • Lévy F, Gervais R, Kindermann U, Orgeur P, Piketty V. Importance of beta-noradrenergic receptors in the olfactory bulb of sheep for recognition of lambs. Behav Neurosci. 1990b;104:464–9.

    Article  PubMed  Google Scholar 

  • Lévy F, Gervais R, Kindermann U, Litterio M, Poindron P, Porter R. Effects of early post-partum separation on maintenance of maternal responsiveness and selectivity in parturient ewes. Appl Anim Behav Sci. 1991;31(1-2):101–10.

    Article  Google Scholar 

  • Lévy F, Kendrick KM, Keverne EB, Piketty V, Poindron P. Intracerebral oxytocin is important for the onset of maternal behavior in inexperienced ewes delivered under peridural anesthesia. Behav Neurosci. 1992;106(2):427–32.

    Article  PubMed  Google Scholar 

  • Lévy F, Guevara-Guzman R, Hinton MR, Kendrick KM, Keverne EB. Effects of parturition and maternal experience on noradrenaline and acetylcholine release in the olfactory bulb of sheep. Behav Neurosci. 1993;107:662–8.

    Article  PubMed  Google Scholar 

  • Lévy F, Locatelli A, Piketty V, Tillet Y, Poindron P. Involvement of the main but not the accessory olfactory system in maternal-behavior of primiparous and multiparous ewes. Physiol Behav. 1995a;57(1):97–104.

    Article  PubMed  Google Scholar 

  • Lévy F, Kendrick KM, Goode JA, Guevara-Guzman R, Keverne EB. Oxytocin and vasopressin release in the olfactory bulb of parturient ewes: changes with maternal experience and effects on acetylcholine, γ-aminobutyric acid, glutamate and noradrenaline release. Brain Res. 1995b;669(2):197–206.

    Article  PubMed  Google Scholar 

  • Lévy F, Richard P, Meurisse M, Ravel N. Scopolamine impairs the ability of parturient ewes to learn to recognise their lambs. Psychopharmacology. 1997;129(1):85–90.

    Article  PubMed  Google Scholar 

  • Lévy F, Meurisse M, Ferreira G, Thibault J, Tillet Y. Afferents to the rostral olfactory bulb in sheep with special emphasis on the cholinergic, noradrenergic and serotonergic connections. J Chem Neuroanat. 1999;16(4):245–63.

    Article  PubMed  Google Scholar 

  • Lévy F, Keller A, Poindron P. Olfactory regulation of maternal behavior in mammals. Horm Behav. 2004;46(3):284–302.

    Article  PubMed  Google Scholar 

  • Lévy F, Keller M, Cornilleau F, Moussu C, Ferreira G. Vaginocervical stimulation of ewes induces the rapid formation of a new bond with an alien young without interfering with a previous bond. Dev Psychobiol. 2010;52(6):537–44.

    Article  PubMed  Google Scholar 

  • Lickliter RE. Mother-infant spatial relationships in domestic goats. Appl Anim Behav Sci. 1984a;13:93–100.

    Article  Google Scholar 

  • Lickliter RE. Hiding behaviour in domestic goat kids. Appl Anim Behav Sci. 1984b;12:245–51.

    Article  Google Scholar 

  • Lickliter RE. Behavior associated with parturition in the domestic goat. Appl Anim Behav Sci. 1985;13(4):335–45.

    Article  Google Scholar 

  • Lledo PM, Alonso M, Grubb MS. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci. 2006;7(3):179–93.

    Article  CAS  PubMed  Google Scholar 

  • Luna-Orozco JR, Meza-Herrera CA, Contreras-Villarreal V, Hernandez-Macias N, Angel-Garcia O, Carrillo E, et al. Effects of supplementation during late gestation on goat performance and behavior under rangeland conditions. J Anim Sci. 2015;93(8):4153–60.

    Article  CAS  PubMed  Google Scholar 

  • Lv S-J, Yang Y, Li F-K. Parity and litter size effects on maternal behavior of Small Tail Han sheep in China. Anim Sci J. 2016;87(3):361–9.

    Article  PubMed  Google Scholar 

  • Malfatti A, Lucamoni A, Debenedetlt A. Behavior associated with parturition in goats. Appl Anim Behav Sci. 1991;30(1-2):191.

    Article  Google Scholar 

  • Martinez M, Otal J, Ramirez A, Hevia ML, Quiles A. Variability in the behavior of kids born of primiparous goats during the first hour after parturition: effect of the type of parturition, sex, duration of birth, and maternal behavior. J Anim Sci. 2009;87(5):1772–7.

    Article  CAS  PubMed  Google Scholar 

  • Meurisse M, Gonzalez A, Delsol G, Caba D, Lévy F, Poindron P. Estradiol receptor-alpha expression in hypothalamic and limbic regions of ewes is influenced by physiological state and maternal experience. Horm Behav. 2005;48(1):34–43.

    Article  CAS  PubMed  Google Scholar 

  • Meurisse M, Chaillou E, Levy F. Afferent and efferent connections of the cortical and medial nuclei of the amygdala in sheep. J Chem Neuroanat. 2009;37(2):87–97.

    Article  CAS  PubMed  Google Scholar 

  • Meyer S, Nurnberg G, Puppe B, Langbein J. The cognitive capabilities of farm animals: categorisation learning in dwarf goats (Capra hircus). Anim Cogn. 2012;15(4):567–76.

    Article  PubMed  Google Scholar 

  • Moreno MM, Bath K, Kuczewski N, Sacquet J, Didier A, Mandairon N. Action of the noradrenergic system on adult-born cells is required for olfactory learning in mice. J Neurosci. 2012;32(11):3748–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morgan PD, Boundy CAP, Arnold GW, Lindsay DR. The roles played by the senses of the ewe in the location and recognition of lambs. Appl Anim Ethol. 1975;1:139–50.

    Article  Google Scholar 

  • Mota-Rojas D, Orihuela A, Strappini A, Villanueva-Garcia D, Napolitano F, Mora-Medina P, et al. Consumption of maternal placenta in humans and nonhuman mammals: beneficial and adverse effects. Animals. 2020;10(12):16.

    Article  Google Scholar 

  • Mouly AM, Gervais R. Polysynaptic potentiation at different levels of rat olfactory pathways following learning. Learn Mem. 2002;9(2):66–75.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mouly AM, Fort A, Ben-Boutayab N, Gervais R. Olfactory learning induces differential long-lasting changes in rat central olfactory pathways. Neuroscience. 2001;102(1):11–21.

    Article  CAS  PubMed  Google Scholar 

  • Nowak R. Neonatal survival: contributions from behavioural studies in sheep. Appl Anim Behav Sci. 1996;49(1):61–72.

    Article  Google Scholar 

  • Nowak R, Keller M, Val-Laillet D, Lévy F. Perinatal visceral events and brain mechanisms involved in the development of mother-young bonding in sheep. Horm Behav. 2007;52(1):92–8.

    Article  CAS  PubMed  Google Scholar 

  • Nowak R, Keller M, Lévy F. Mother–young relationships in sheep: a model for a multidisciplinary approach of the study of attachment in mammals. J Neuroendocrinol. 2011;23(11):1042–53.

    Article  CAS  PubMed  Google Scholar 

  • Numan M, Insel TR. In: Ball GF, Balthazart J, Nelson RJ, editors. The neurobiology of parental behavior. Springer; 2003. p. 417.

    Google Scholar 

  • Numan M, Numan MJ. A lesion and neuroanatomical tract-tracing analysis of the role of the bed nucleus of the stria terminalis in retrieval behavior and other aspects of maternal responsiveness in rats. Dev Psychobiol. 1996;29(1):23–51.

    Article  CAS  PubMed  Google Scholar 

  • O’Brien PH. Feral goat parturition and lying-out sites: spatial, physical and meteorological characteristics. Appl Anim Behav Sci. 1983;10:325–39.

    Google Scholar 

  • O’Brien PH. Leavers and stayers: maternal post-partum strategies in feral goats. Appl Anim Behav Sci. 1984;12:233–43.

    Article  Google Scholar 

  • O’Connor CE, Lawrence AB, Wood-Gush DGM. Influence of litter size and parity on maternal behaviour at parturition on Scottish Blackface sheep. Appl Anim Behav Sci. 1992;33:345–55.

    Article  Google Scholar 

  • Olazabal DE, Pereira M, Agrati D, Ferreira A, Fleming AS, Gonzalez-Mariscal G, et al. Flexibility and adaptation of the neural substrate that supports maternal behavior in mammals. Neurosci Biobehav Rev. 2013;37(8):1875–92.

    Article  PubMed  Google Scholar 

  • Onoda N, Imamura K, Obata E, Iino M. Response selectivity of neocortical neurons to specific odors in the rabbit. J Neurophysiol. 1984;52(4):638–52.

    Article  CAS  PubMed  Google Scholar 

  • Otal J, Lévy F, Cornilleau F, Moussu C, Keller M, Poindron P. Preventing physical interactions between parturient ewes and their neonate differentially impairs the development of maternal responsiveness and selectivity depending on maternal experience. Appl Anim Behav Sci. 2009;120(3-4):140–9.

    Article  Google Scholar 

  • Otal J, Martinez M, Quiles A, Hevia ML, Ramirez A. Effect of litter size and sex on the birth weight of newborn kids and in the behaviour of primiparous goats before, during and after the parturition. Can J Anim Sci. 2010;90(4):483–90.

    Article  Google Scholar 

  • Peirce JW, Leigh AE, Kendrick KM. Configurational coding, familiarity and the right hemisphere advantage for face recognition in sheep. Neuropsychol. 2000;38(4):475–483.

    Google Scholar 

  • Perrin G, Meurisse M, Lévy F. Inactivation of the medial preoptic area or the bed nucleus of the stria tenninalis differentially disrupts maternal behavior in sheep. Horm Behav. 2007;52(4):461–73.

    Article  CAS  PubMed  Google Scholar 

  • Petrulis A, Eichenbaum H. The perirhinal-entorhinal cortex, but not the hippocampus, is critical for expression of individual recognition in the context of the Coolidge effect. Neuroscience. 2003;122(3):599–607.

    Article  CAS  PubMed  Google Scholar 

  • Pissonnier D, Thiéry JC, Fabre-Nys C, Poindron P, Keverne EB. The importance of olfactory bulb noradrenalin for maternal recognition in sheep. Physiol Behav. 1985;35(3):361–3.

    Article  CAS  PubMed  Google Scholar 

  • Plush KJ, Hebart ML, Brien FD, Hynd PI. The genetics of temperament in Merino sheep and relationships with lamb survival. Appl Anim Behav Sci. 2011;134(3-4):130–5.

    Article  Google Scholar 

  • Poindron P. Mother-young relationships in intact or anosmic ewes at the time of suckling. Biol Behav. 1976;2:161–77.

    Google Scholar 

  • Poindron P, Le Neindre P. Endocrine and sensory regulation of maternal behavior in the ewe. In: Rosenblatt JS, Hinde RA, Beer C, editors. Advances in the study of behavior. 11. New York: Academic; 1980. p. 75–119.

    Google Scholar 

  • Poindron P, Martin GB, Hooley RD. Effects of lambing induction on the sensitive period for the establishment of maternal behaviour in sheep. Physiol Behav. 1979;23(6):1081–7.

    Article  CAS  PubMed  Google Scholar 

  • Poindron P, Le Neindre P, Raksanyi I, Trillat G, Orgeur P. Importance of the characteristics of the young in the manifestation and establishment of maternal behaviour in sheep. Reprod Nutr Dev. 1980;20(3B):817–26.

    Article  CAS  PubMed  Google Scholar 

  • Poindron P, Leneindre P, Lévy F, Keverne EB. The physiological mechanisms of the acceptance of the newborn among sheep. Biol Behav. 1984a;9(1):65–88.

    Google Scholar 

  • Poindron P, Raksanyi I, Orgeur P, Le Neindre P. Comparaison du comportement maternel en bergerie à la parturition chez des brebis primipares ou multipares de race Romanov, Préalpes de Sud et Ile-de-France. Génétique, Sélection, Evolution. 1984b;16(4):503–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poindron P, Lévy F, Krehbiel D. Genital, olfactory, and endocrine interactions in the development of maternal behaviour in the parturient ewe. Psychoneuroendocrinology. 1988;13(1-2):99–125.

    Article  CAS  PubMed  Google Scholar 

  • Poindron P, Caba M, Gomora Arrati P, Krehbiel D, Beyer C. Responses of maternal and non-maternal ewes to social and mother-young separation. Behav Process. 1994;31(1):97–110.

    Article  CAS  Google Scholar 

  • Poindron P, Soto R, Romeyer A. Decrease of response to social separation in preparturient ewes. Behav Process. 1997;40(1):45–51.

    Article  CAS  Google Scholar 

  • Poindron P, Gilling G, Hernandez H, Serafin N, Terrazas A. Early recognition of newborn goat kids by their mother: I. Nonolfactory discrimination. Dev Psychobiol. 2003;43(2):82–9.

    Article  PubMed  Google Scholar 

  • Poindron P, Terrazas A, de Oca MD, Serafin N, Hernandez H. Sensory and physiological determinants of maternal behavior in the goat (Capra hircus). Horm Behav. 2007a;52(1):99–105.

    Article  PubMed  Google Scholar 

  • Poindron P, Lévy F, Keller M. Maternal responsiveness and maternal selectivity in domestic sheep and goats: the two facets of maternal attachment. Dev Psychobiol. 2007b;49(1):54–70.

    Article  CAS  PubMed  Google Scholar 

  • Poindron P, Otal J, Ferreira G, Keller M, Guesdon V, Nowak R, et al. Amniotic fluid is important for the maintenance of maternal responsiveness and the establishment of maternal selectivity in sheep. Animal. 2010;4(12):2057–64.

    Article  CAS  PubMed  Google Scholar 

  • Porter RH, Doane HM. Studies of maternal behavior in spiny mice (Acomis cahirinus). Zeitschrift Fur Tierpsychologie. 1978;47:225–35.

    Google Scholar 

  • Porter RH, Lévy F, Poindron P, Litterio M, Schaal B, Beyer C. Individual olfactory signatures as major determinants of early maternal discrimination in sheep. Dev Psychobiol. 1991;24(3):151–8.

    Article  CAS  PubMed  Google Scholar 

  • Porter RH, Romeyer A, Lévy F, Krehbiel D, Nowak R. Investigations of the nature of lambs individual odor signatures. Behav Process. 1994;31(2-3):301–8.

    Article  CAS  Google Scholar 

  • Pritchard CE, Williams AP, Davies P, Jones D, Smith AR. Spatial behaviour of sheep during the neonatal period: preliminary study on the influence of shelter. Animal. 2021;15(7):100252.

    Article  CAS  PubMed  Google Scholar 

  • Putu IG, Poindron P, Lindsay DR. A high level of nutrition during late pregnancy improves subsequent maternal behaviour of merino ewes. Proc Aust Soc Anim Prod. 1988;17:294–7.

    Google Scholar 

  • Putu IG, Poindron P, Oldham CM, Gray SJ, Ballard M. Lamb desertion in primiparous and multiparous Merino ewes induced to lamb with dexamethasone. Proc Aust Soc Anim Prod. 1986;16:315–318.

    Google Scholar 

  • Ramírez A, Quiles A, Hevia M, Sotillo F. Behavior of the Murciano-Granadina goat in the hour before parturition. Appl Anim Behav Sci. 1995;44:29–35.

    Article  Google Scholar 

  • Ramirez A, Quiles A, Hevia M, Sotillo F. Observations on the birth of goats. Can J Anim Sci. 1995;75(1):165–7.

    Article  Google Scholar 

  • Ramírez A, Quiles A, Hevia ML, Sotillo F, Ramírez MC. Effects of immediate and early postpartum separation on maintenance of maternal responsiveness in parturient multiparous goats. Appl Anim Behav Sci. 1996;48:215–24.

    Article  Google Scholar 

  • Ramírez-Vera S, Terrazas A, Delgadillo JA, Flores JA, Serafín N, Vielma J, et al. Inclusion of maize in the grazing diet of goats during the last 12 days of gestation reinforces the expression of maternal behaviour and selectivity during the sensitive period. Livest Sci. 2012;148(1):52–9.

    Article  Google Scholar 

  • Regueiro M, López-Mazz C, Jorge-Smeding E, Baldi F, Banchero G. Duration of phase II of labour negatively affects maternal behaviour and lamb viability in wool-type primiparous ewes under extensive rearing. Appl Anim Behav Sci. 2021;234:105207.

    Article  Google Scholar 

  • Restrepo D, Lin W, Salcedo E, Yamazaki K, Beauchamp G. Odor types and MHC peptides: complementary chemosignals of MHC haplotype? Trends Neurosci. 2006;29(11):604–9.

    Article  CAS  PubMed  Google Scholar 

  • Romeyer A, Porter RH, Lévy F, Nowak R, Orgeur P, Poindron P. Maternal labelling is not necessary for the establishment of discrimination between kids by recently parturient goats. Anim Behav. 1993a;46(4):705–12.

    Article  Google Scholar 

  • Romeyer A, Porter RH, Poindron P, Orgeur P, Chesné P, Poulain N. Recognition of dizygotic and monozygotic twin lambs by ewes. Behaviour. 1993b;127:119–39.

    Article  Google Scholar 

  • Romeyer A, Poindron P, Orgeur P. Olfaction mediates the establishment of selective bonding in goats. Physiol Behav. 1994a;56(4):693–700.

    Article  CAS  PubMed  Google Scholar 

  • Romeyer A, Poindron P, Porter RH, Lévy F, Orgeur P. Establishment of maternal bonding and its mediation by vaginocervical stimulation in goats. Physiol Behav. 1994b;55(2):395–400.

    Article  CAS  PubMed  Google Scholar 

  • Rosenblatt JS. Psychobiology of maternal behavior: contribution to the clinical understanding of maternal behavior among humans. Acta Paediatr Suppl. 1994;397:3–8.

    Article  CAS  PubMed  Google Scholar 

  • Rosenblatt JS, Lehrman DS. Maternal behavior in the laboratory rat. In: Rheingold HL, editor. Maternal behavior in mammals. New York: Wiley; 1963. p. 8–57.

    Google Scholar 

  • Rosenblatt JS, Siegel HI. Factors governing the onset and maintenance of maternal behavior among nonprimate mammals. In: Gubernick DJ, Klopfer PH, editors. Parental care in mammals. New York: Plenum Press; 1981. p. 13–76.

    Chapter  Google Scholar 

  • Ruiz-Miranda CR. Use of pelage pigmentation in the recognition of mothers in a group by 2- to 4-month-old domestic goat kids. Appl Anim Behav Sci. 1993;36(4):317–26.

    Article  Google Scholar 

  • Sambraus HH, Wittmann M. Observations of the birth and suckling behavior of goats. Tierarztliche Praxis. 1989;17(4):359–65.

    CAS  PubMed  Google Scholar 

  • Schneirla TC, Rosenblatt JS, Tobach E. Maternal behavior in the cat. In: Rheingold HL, editor. Maternal behavior in mammals. New York: Wiley; 1963. p. 122–68.

    Google Scholar 

  • Sèbe F, Nowak R, Poindron P, Aubin T. Establishment of vocal communication and discrimination between ewes and their lamb in the first two days after parturition. Dev Psychobiol. 2007;49(4):375–86.

    Article  PubMed  Google Scholar 

  • Sebe F, Aubin T, Boue A, Poindron P. Mother-young vocal communication and acoustic recognition promote preferential nursing in sheep. J Exp Biol. 2008;211(Pt 22):3554–62.

    Article  PubMed  Google Scholar 

  • Sèbe F, Duboscq J, Aubin T, Ligout S, Poindron P. Early vocal recognition of mother by lambs: contribution of low- and high-frequency vocalizations. Anim Behav. 2010;79(5):1055–66.

    Article  Google Scholar 

  • Sèbe F, Poindron P, Ligout S, Sèbe O, Aubin T. Amplitude modulation is a major marker of individual signature in lamb bleats. Bioacoustics. 2018;27(4):359–75.

    Article  Google Scholar 

  • Shillito EE. Vocalization in sheep. J Physiol London. 1972;226(2):P45.

    Google Scholar 

  • Shillito EE, Alexander G. Mutual recognition amongst ewes and lambs of four breeds of sheep. Appl Anim Ethol. 1975;1:151–65.

    Article  Google Scholar 

  • Shipka MP, Ford SP. Relationship of circulating estrogen and progesterone concentrations during late pregnancy and the onset phase of maternal behavior in the ewe. Appl Anim Behav Sci. 1991;31:91–9.

    Article  Google Scholar 

  • Simitzis P, Galani K, Vasiliou P, Koutsouli P, Bizelis I. Effect of breed and litter size on the display of maternal perinatal and offspring postnatal behavior in dairy sheep. J Vet Behav. 2016;13:10–8.

    Article  Google Scholar 

  • Soto R, Terrazas A, Poindron P, González-Mariscal G. Regulation of maternal behavior, social isolation responses, and postpartum estrus by steroid hormones and vaginocervical stimulation in sheep. Horm Behav. 2021;136:105061.

    Article  CAS  PubMed  Google Scholar 

  • Stevens D, Alexander G, Lynch JJ. Do Merino ewes seek isolation or shelter at lambing? Appl Anim Ethol. 1981;7:149–55.

    Article  Google Scholar 

  • Strott CA, Sundel H, Stahlman MT. Maternal and fetal plasma progesterone, cortisol, testosterone and 17beta-estradiol in preparturient sheep: response to fetal ACTH infusion. Endocrinology. 1974;95(5):1327–39.

    Article  CAS  PubMed  Google Scholar 

  • Terrazas A, Ferreira G, Lévy F, Nowak R, Serafin N, Orgeur P, et al. Do ewes recognize their lambs within the first day postpartum without the help of olfactory cues? Behav Process. 1999;47(1):19–29.

    Article  CAS  Google Scholar 

  • Terrazas A, Serafin N, Hernandez H, Nowak R, Poindron P. Vocal recognition of 2-day-old goat kids by their mother: evidence of individual acoustic signatures in neonates. 2003.

    Google Scholar 

  • Terrazas A, Robledo V, Serafín N, Soto R, Hernández H, Poindron P. Differential effects of undernutrition during pregnancy on the behaviour of does and their kids at parturition and on the establishment of mutual recognition. Animal. 2009;3(2):294–306.

    Article  CAS  PubMed  Google Scholar 

  • Uriarte N, Agrati D, Banchero G, González A, Zuluaga MJ, Cawen E, et al. Different chemical fractions of fetal fluids account for their attractiveness at parturition and their repulsiveness during late-gestation in the ewe. Physiol Behav. 2012;107(1):45–9.

    Article  CAS  PubMed  Google Scholar 

  • Vince MA, Lynch JJ, Mottershead B, Green G, Elwin R. Sensory factors involved in immediately postnatal ewe/lamb bonding. Behaviour. 1985;94:60–84.

    Article  Google Scholar 

  • Viviers MZ, Bekker JP, Burger BV, le Roux NJ, Morris J, le Roux M. Characterization of amniotic fluid of Dohne Merino ewes (Ovis aries) and its possible role in neonatal recognition. Z Naturforsch C J Biosci. 2015;70(5-6):115–28.

    Article  CAS  PubMed  Google Scholar 

  • Whateley J, Kilgour R, Dalton DC. Behaviour of hill country sheep breeds during farming routines. Proc N Z Soc Anim Prod. 1974:28–36.

    Google Scholar 

  • Wierucka K, Pitcher BJ, Harcourt R, Charrier I. Multimodal mother-offspring recognition: the relative importance of sensory cues in a colonial mammal. Anim Behav. 2018;146:135–42.

    Article  Google Scholar 

  • Yamin M, Payne G, Blackshaw JK. The time of birth and the choice of birth sites by Booroola Merino ewes and Angora goats. Appl Anim Behav Sci. 1995;45(1-2):89–96.

    Article  Google Scholar 

  • Yu GZ, Kaba H, Okutani F, Takahashi S, Higuchi T, Seto K. The action of oxytocin originating in the hypothalamic paraventricular nucleus on mitral and granule cells in the rat main olfactory bulb. Neuroscience. 1996;72(4):1073–82.

    Article  CAS  PubMed  Google Scholar 

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    Frédéric Lévy

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    Gabriela González-Mariscal

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Lévy, F. (2022). The Onset of Maternal Behavior in Sheep and Goats: Endocrine, Sensory, Neural, and Experiential Mechanisms. In: González-Mariscal, G. (eds) Patterns of Parental Behavior. Advances in Neurobiology, vol 27. Springer, Cham. https://doi.org/10.1007/978-3-030-97762-7_3

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