Vet Med - Czech, 2016, 61(11):595-611 | DOI: 10.17221/255/2014-VETMED
Sensory factors involved in mother-young bonding in sheep: a reviewReview
- 1 Metropolitan Autonomous University, Mexico City, Mexico
- 2 Faculty of Agriculture and Livestock Sciences, Autonomous University of the State of Morelos, Cuernavaca, Mexico
- 3 Neurobiology Service, National Rehabilitation Institute, Mexico City, Mexico
- 4 Animal Welfare Department, University of the Mexican Valley, Mexico City, Mexico
- 5 Department of Livestock Sciences, National Autonomous University of Mexico, Cuautitlan Izcalli, Mexico
The aim of this review is to discuss sensory recognition (olfaction, vision, vocalisation, hearing and direct contact) in relation to the ewe-lamb bond, and the relevance of this information for animal management, considering that sensory recognition between ewes and their offspring is a key element of lamb welfare. In some parental care strategies, parents promote recognition of their own young in order to ensure their survival by providing them - and only them - with food, while the young simultaneously learn features of the environment. In the specific case of sheep, mother-young bonding is established during the sensitive period of the first 4 h after birth. The ewe prints a distinctive signal on her lambs that marks her as the legitimate mother, while stimulating the offspring's learning processes through olfactory, visual and acoustic cues. However, the sensory basis for proximal recognition of lambs changes over time as they learn to recognise the signals emitted by the mother. After 4 h - or less - the ewe becomes maternally selective; this means that she accepts only her own lambs at the udder, while actively rejecting alien newborns. Likewise, newborn lambs develop a preference for their mothers in less than one day. This preference is regulated by the difference between the acceptance behaviour manifested by the lamb's own mother and the aggressive rejecting behaviour shown by alien ewes. This early discriminative ability allows the lamb to avoid the aggressive actions of alien dams and maintain close contact with its own lactating mother. At around one week of age, lambs learn to develop the sensory cues that allow them to recognize their mother. These include olfactory, visual, acoustic and tactile information. Mutual ewe-lamb recognition at an early age also ensures that newborns will be fed and cared for by their own mother, which satisfies some of the requirements for their survival and welfare. For all these reasons, any disruption of ewe-lamb bonding during parturition is detrimental to lamb welfare and survival.
Keywords: ewe-lamb bond; welfare; recognition; olfactory; vocalisation; vision
Published: November 30, 2016 Show citation
ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
References
- Alexander G (1978): Odour, and the recognition of lambs by Merino ewes. Applied Animal Ethology 4, 153-158.
Go to original source...
- Alexander G (1988): What makes a good mother? Components and comparative aspects of maternal behaviour in ungulates. Proceedings of Australian Society of Animal Production 17, 25-41.
- Alexander RD, Borgia G (1978): Group selection, altruism, and the levels of organization of life. Annual Review of Ecology and Systematics 9, 449-474.
Go to original source...
- Alexander G, Shillito-Walser EE (1978): Visual discrimination between ewes by lambs. Applied Animal Ethology 4, 81-85.
Go to original source...
- Alexander G, Stevens D, Kilgour R, De Langen H, Mottershead BE, Lynch JJ (1983): Separation of ewes from twin lambs: incidence in several sheep breeds. Applied Animal Ethology 10, 301-317.
Go to original source...
- Arch-Tirado E, Collado-Corona MA (2002): Analysis of vocalizations in newborn guinea pigs with normal hearing and deafness caused by periods of solitude. Cirugia y Cirujanos 70, 442-448.
- Arch-Tirado E, Verduzco-Mendoza A, Taboada-Picazo V, Mota-Rojas D, Alonso-Spilsbury M, Alfaro-Rodriguez A (2009): Analysis of normal and denerved laryngeal vocalization in guinea pigs (Cavia porcellus). Journal of Voice 23, 34-39.
Go to original source...
Go to PubMed...
- Archunan G, Rajanarayanan S, Karthikeyan K (2014): 16 Cattle pheromones. In: Caretta C (ed.): Neurobiology of Chemical Communication. 1st edn. CRC Press, New York. 461-479.
- Arnold GW, Boundy CAP, Morgan PD, Bartle G (1975): The roles of sight and hearing in the lamb in the location and discrimination between ewes. Applied Animal Ethology 1, 167-176.
Go to original source...
- Arteaga-Castaneda ML, Martinez-Gomez M, GuevaraGuzman R, Hudson R (2007): Chemical communication in domestic mammals. Veterinaria Mexico 38, 105-123.
- Beny Y, Kimchi T (2014): Innate and learned aspects of pheromone-mediated social behaviours. Animal Behaviour 97, 301-311.
Go to original source...
- Bergamasco L, Macchi E, Facello C, Badino P, Odore R, Pagliasso S, Bellino C, Osella MC, Re G (2005): Effects of brief maternal separation in kids on neurohormonal and electroencephalographic parameters. Applied Animal Behaviour Science 93, 39-52.
Go to original source...
- Bielsky IF, Young, LJ (2004): Oxytocin, vasopressin, and social recognition in mammals. Peptides 25, 1565-1574.
Go to original source...
Go to PubMed...
- Boivin X, Nowak R, Garcia AT (2001): The presence of the dam affects the efficiency of gentling and feeding on the early establishment of the stockperson-lamb relationship. Applied Animal Behaviour Science 72, 89-103.
Go to original source...
Go to PubMed...
- Booth KK, Katz LS (2000): Role of the vomeronasal organ in neonatal offspring recognition in sheep. Biology of Reproduction 63, 953-958.
Go to original source...
Go to PubMed...
- Brennan PA, Kendrick KM (2006): Mammalian social odours: attraction and individual recognition. Philosophical Transactions of the Royal Society, B-Biological Sciences 361, 2061-2078.
Go to original source...
Go to PubMed...
- Bridges RS (2015): Neuroendocrine regulation of maternal behavior. Frontiers in Neuroendocrinology 36, 178-196
Go to original source...
Go to PubMed...
- Broad KD, Mimmack ML, Kendrick KM (2000): Is right hemisphere specialization for face discrimination specific to humans? European Journal of Neuroscience 12, 731-741.
Go to original source...
Go to PubMed...
- Broad KD, Curley JP, Keverne EB (2006): Mother-infant bonding and the evolution of mammalian social relationships. Philosophical Transactions of the Royal Society, B-Biological Sciences 361, 2199-2214.
Go to original source...
Go to PubMed...
- Burger BV, Viviers MZ, Le Roux NJ, Morris J, Bekker JPI, Le Roux M (2011): Olfactory cue mediated neonatal recognition in sheep, Ovis aries. Journal of Chemical Ecology 37, 1150-1163.
Go to original source...
Go to PubMed...
- Carter CS, Williams JR, Witt DM, Insel TR (1992): Oxytocin and social bonding. Annals of the New York Academy of Sciences 652, 204-211.
Go to original source...
Go to PubMed...
- Charra R, Datiche F, Casthano A, Gigot V, Schaal B, Coureaud G (2012): Brain processing of the mammary pheromone in newborn rabbits. Behavioral and Brain Research 226, 179-188.
Go to original source...
Go to PubMed...
- Charrier I, Mathevon N, Jouventin P (2001): Mother's voice recognition by seal pups - Newborns need to learn their mother's call before she can take off on a fishing trip. Nature 412, 873.
Go to original source...
Go to PubMed...
- Charrier I, Mathevon N, Jouventin P (2003): Vocal signature recognition of mothers by fur seal pups. Animal Behaviour 65, 543-550.
Go to original source...
- Coulon M, Nowak R, Andanson S, Ravel C, Marnet PG, Boissy A, Boivin X (2013): Human-lamb bonding: Oxytocin, cortisol and behavioural responses of lambs to human contacts and social separation. Psychoneuroendocrinology 38, 499-508.
Go to original source...
Go to PubMed...
- Darwish RA, 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.
Go to original source...
Go to PubMed...
- Dwyer CM (2008): 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.
Go to original source...
Go to PubMed...
- Dwyer CM, Bornett HL (2004): Chronic stress in sheep: assessment tools and their use in different management conditions. Animal Welfare 13, 293-304.
Go to original source...
- Dwyer CM, McLean KA, Deans LA, Chirnside J, Calvert SK, Lawrence AB (1998): Vocalisations between mother and young in sheep: effects of breed and maternal experience. Applied Animal Behaviour Science 58, 105-119.
Go to original source...
- Dwyer CM, Lawrence AB, Bishop SC, Lewis M (2003): Ewelamb bonding behaviours at birth are affected by maternal undernutrition in pregnancy. British Journal of Nutrition 89, 123-136.
Go to original source...
Go to PubMed...
- Fay RR, Popper AN (2000): Evolution of hearing in vertebrates: the inner ears and processing. Hearing Research 149, 1-10.
Go to original source...
Go to PubMed...
- Ferreira G, Gervais R, Durkin TP, Levy F (1999): Postacquisition scopolamine treatments reveal the time course for the formation of lamb odor recognition memory in parturient ewes. Behavioral Neuroscience 113, 136-142.
Go to original source...
- Ferreira G, Terrazas A, Poindron P, Nowak R, Orgeur P, Levy F (2000): Learning of olfactory cues is not necessary for early lamb recognition by the mother. Physiology and Behavior 69, 405-412.
Go to original source...
Go to PubMed...
- Ferreira-Pereira SM (2011): Influence of bioacoustics in the development of science in Portugal. Interface of bioacoustics and monitoring of biodiversity. [MSc Thesis.] Technical University of Lisbon, Portugal.
- Fichtel C, Manzer M (2010): 2. Vocal communication in social groups. In: Peter K (ed.): Animal Behaviour: Evolution and Mechanisms. 1st edn. Springer-Verlag, Berlin. 29-54.
Go to original source...
- Gelez H, Archer E, Chesneau D, Campan R, Fabre-Nys C (2004): Importance of learning in the response of ewes to male odor. Chemical Senses 29, 555-563.
Go to original source...
Go to PubMed...
- Goncalves L, Dafre AL, Carobrez SG, Gasparotto OC (2008): A temporal analysis of the relationships between social stress, humoral immune response and glutathionerelated antioxidant defenses. Behavioural Brain Research 192, 226-231.
Go to original source...
Go to PubMed...
- Gonzalez-Mariscal G, Poindron P (2002): Parental care in mammals: immediate internal and sensory factors of control. In: Pfaff DW, Arnold AP, Etgen AM, Fahrfbach SE, Rubin RT (eds): Hormones, Brain and Behavior. 1st edn. Academic Press, San Diego. 215-298.
Go to original source...
- Hernandez H, Serafin N, Terrazas AM, Marnet PG, Kann G, Delgadillo JA, Poindron P (2002): Maternal olfaction differentially modulates oxytocin and prolactin release during suckling in goats. Hormones and Behavior 42, 232-244.
Go to original source...
Go to PubMed...
- Hernandez H, Terrazas A, Poindron P, Ramirez-Vera S, Flores JA, Delgadillo JA, Vielma J, Duarte G, Fernandez IG, Fitz-Rodriguez G, Retana-Marquez S, Munoz-Gutierrez M, Serafin N (2012): Sensorial and physiological control of maternal behavior in small ruminants: sheep and goats. Tropical and Subtropical Agroecosystems 15, S91-S102.
- Hewson C (2003): What is animal welfare? Common definitions and their practical consequences. Canadian Veterinary Journal 44, 496-499.
- Hild S, Clark CCA, Dwyer CM, Murrell JC, Mendl M, Zanella AJ (2011): Ewes are more attentive to their offspring experiencing pain but not stress. Applied Animal Behaviour Science 132, 114-120.
Go to original source...
- Hutson GD (2007): 10. Behavioural principles of sheep handling. In: Grandin T (ed.): Livestock Handling and Transport. 3rd edn. CAB International, Boston. 155-174.
Go to original source...
- Keller M, Levy F (2012): The main but not the accessory olfactory system is involved in the processing of socially relevant chemosignals in ungulates. Frontiers in Neuroanatomy 39, 1-8.
Go to original source...
Go to PubMed...
- Keller M, Meurisse M, Poindron P, Nowak R, Ferreira G, Shayit M, Levy F (2003): Maternal experience influences the establishment of visual/auditory, but not olfactory recognition of the newborn lamb by ewes at parturition. Developmental Psychobiology 43, 167-176.
Go to original source...
Go to PubMed...
- Keller M, Meurisse M, Levy F (2004a): Mapping the neural substrates involved in maternal responsiveness and lamb olfactory memory in parturient ewes using Fos imaging. Behavioral Neuroscience 118, 1274-1284.
Go to original source...
Go to PubMed...
- Keller M, Perrin G, Meurisse M, Ferreira G, Levy F (2004b): Cortical and medial amygdala are both involved in the formation of olfactory offspring memory in sheep. European Journal of Neuroscience 20, 3433-3441.
Go to original source...
Go to PubMed...
- Keller M, Meurisse M, Levy F (2005): Mapping of brain networks involved in consolidation of lamb recognition memory. Neuroscience 133, 359-369.
Go to original source...
Go to PubMed...
- Kendrick KM, Keverne EB (1991): Importance of progesterone and estrogen priming for the induction of maternalbehavior by vaginocervical stimulation in sheep - effects of maternal experience. Physiology and Behavior 49, 745-750.
Go to original source...
Go to PubMed...
- Kendrick KM, Levy F, Keverne EB (1992): Changes in the sensory processing of olfactory signals induced by birth in sheep. Science 256, 833-836.
Go to original source...
Go to PubMed...
- Kendrick KM, Atkins K, Hinton MR, Broad KD, Fabre-Nys C, Keverne B (1995): Facial and vocal discrimination in sheep. Animal Behaviour 49, 1665-1676.
Go to original source...
- Kendrick KM, Atkins K, Hinton MR, Heavens P, Keverne B (1996): Are faces special for sheep? Evidence from facial and object discrimination learning tests showing effects of inversion and social familiarity. Behavioural Processes 38, 19-35.
Go to original source...
Go to PubMed...
- Keverne EB, Kendrick KM (1992): Oxytocin facilitation of maternal-behavior in sheep. Annals of the New York Academy of Sciences 652, 83-101.
Go to original source...
Go to PubMed...
- Komaromy AM (2010): Day blind sheep and the importance of large animal disease models. The Veterinary Journal 185, 241-242.
Go to original source...
Go to PubMed...
- Lambert KG (2012): The parental brain: Transformations and adaptations. Physiology and Behavior 107, 792-800.
Go to original source...
Go to PubMed...
- Levy 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.
Go to original source...
- Levy F, Poindron P, 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.
Go to original source...
Go to PubMed...
- Levy F, Locatelli A, Piketty V, Tillet Y, Poindron P (1995): Involvement of the main but not the accessory olfactory system in maternal behavior of primiparous and multiparous ewes. Physiology and Behavior 57, 97-104.
Go to original source...
Go to PubMed...
- Levy F, Keller M, Poindron P (2004): Olfactory regulation of maternal behavior in mammals. Hormones and Behavior 46, 284-302.
Go to original source...
Go to PubMed...
- Liberles SD (2014): Mammalian pheromones. Annual Review of Physiology 76, 151-175.
Go to original source...
Go to PubMed...
- Logan DW, Brunet LJ, Webb WR, Cutforth T, Ngai J, Stowers L (2012): Learned recognition of maternal signature odors mediates the first suckling episode in mice. Current Biology 22, 1998-2007.
Go to original source...
Go to PubMed...
- Long CV (2007): Vocalisations of the degu Octodon degus, a social caviomorph rodent. Bioacoustics - The International Journal of Animal Sound and its Recording 16, 223-244.
Go to original source...
- Maldonado A, Orihuela A, Aguirre V, Vazquez R, FloresPerez I (2015): Changes in mother-offspring relationships with the increasing age of the lamb in hair sheep (Ovis aries). Journal of Veterinary Behavior 10, 166-170.
Go to original source...
- Manteuffel G, Puppe B, Schon PC (2004): Vocalization of farm animals as a measure of welfare. Applied Animal Behaviour Science 88, 163-182.
Go to original source...
- Martinez MG, Gonzalez RS, Massot PP, Ramirez LA, Mendez JD, Diaz FR, Garcia AM (2011): Maternal behaviour around birth and mother-young recognition in Pelibuey sheep. Veterinaria Mexico 42, 27-46.
- Marx G, Horn T, Thielebein J, Knubel B, von Borell E (2003): Analysis of pain-related vocalization in young pigs. Journal of Sound and Vibration 266, 687-698.
Go to original source...
- Mateo JM (2006): The nature and representation of individual recognition odours in Belding's ground squirrels. Animal Behaviour 71, 141-154.
Go to original source...
- McComb K, Reby D (2005): Vocal communication networks in large terrestrial mammals. In: McGregor P (ed.): Animal Communication Networks. Cambridge University Press, Cambridge. 372-389.
Go to original source...
- Meurisse M, Gonzalez A, Delsol G, Caba M, Levy F, Poindron P (2005): Estradiol receptor-α expression in hypothalamic and limbic regions of ewes is influenced by physiological state and maternal experience. Hormones and Behavior 48, 34-43.
Go to original source...
Go to PubMed...
- Mora-Medina P (2016): Animal welfare in lambs: motheryoung separation. [PhD Thesis.] Metropolitan Autonomous University, Mexico City, Mexico.
- Mora-Medina P, Mota-Rojas D, Arch-Tirado E, Orozco H (2015): Animal welfare in lambs: ewe-lamb separation. Large Animal Review 21, 39-44.
- Moura DJ, Silva WT, Naas IA, Tolon YA, Lima KAO, Vale MM (2008): Real time computer stress monitoring of piglets using vocalization analysis. Computers and Electronics in Agriculture 64, 11-18.
Go to original source...
- Mukasa-Mugerwa E, Lahlou-Kassi A, Anindo D, Rege JEO, Tembely S, Tibbo M, Baker RL (2000): Between and within breed variation in lamb survival and the risk factors associated with major causes of mortality in indigenous Horro and Menz sheep in Ethiopia. Small Ruminant Research 37, 1-12.
Go to original source...
Go to PubMed...
- Nowak R (1990): Lamb's bleats: important for the establishment of the mother-young bond? Behaviour 115, 14-29.
Go to original source...
- Nowak R (1991): Senses involved in the discrimination of Merino ewes at close contact and from a distance by their newborn lambs. Animal Behaviour 42, 357-366.
Go to original source...
- Nowak R (2006). Suckling, milk, and the development of preferences toward maternal cues by neonates: from early learning to filial attachment? Advanced Study Behavior 36, 1-58.
Go to original source...
- Nowak R, Boivin X (2015): Filial attachment in sheep: Similarities and differences between ewe-lamb and humanlamb relationships. Applied Animal Behaviour Science 164, 12-28.
Go to original source...
- Nowak R, Poindron P (2006): From birth to colostrum: early steps leading to lamb survival. Reproduction Nutrition Development 46, 431-446.
Go to original source...
Go to PubMed...
- Nowak R, Poindron P, Le Neindre P, Putu IG (1987): Ability of 12-hour-old merino and crossbred lambs to recognise their mothers. Applied Animal Behaviour Science 17, 263-271.
Go to original source...
- Nowak R, Porter RH, Levy 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.
Go to original source...
Go to PubMed...
- Nowak R, Keller M, Val-Laillet D, Levy F (2007): Perinatal visceral events and brain mechanisms involved in the development of mother-young bonding in sheep. Hormones and Behavior 52, 92-98.
Go to original source...
Go to PubMed...
- Numan M, Insel TR (eds) (2003): The Neurobiology of Parental Behavior: Hormones, Brain, and Behavior. 1st edn. Springer-Verlag, New York. 428 pp.
- Numan M, Fleming A, Levy F (2006): Maternal behavior. In: Neill JD (ed.): Knobil and Neill's Physiology of Reproduction. Academic Press, San Diego. 1921-1994.
Go to original source...
- Pedersen CA (1997): Oxytocin control of maternal behavior - Regulation by sex steroids and offspring stimuli. Integrative Neurobiology of Affiliation 807, 126-145.
Go to original source...
Go to PubMed...
- Pfister JA, Davidson TW, Panter KE, Cheney CD, Molyneux RJ (2006): Maternal ingestion of locoweed III. Effects on lamb behaviour at birth. Small Ruminant Research 65, 70-78.
Go to original source...
- Piggins D, Phillips CJC (1996): The eye of the domesticated sheep with implications for vision. Animal Science 62, 301-308.
Go to original source...
- Poindron P (1976): Effects of odor removal, without damaging the olfactory bulbs and the selectivity of maternal behavior of the ewe (in French). Comptes Rendus Hebdomadaires des Seances de l'Academie des Sciences, Serie D 282, 489-491.
- Poindron P (2005): Mechanisms of activation of maternal behaviour in mammals. Reproduction Nutrition Development 45, 341-351.
Go to original source...
Go to PubMed...
- Poindron P, Le Neindre P, Raksanyi I, Trillat G, Orgeur P (1980): Importance of the characteristics of the young in the manifestation and establishment of maternal behaviour in sheep. Reproduction Nutrition Development 20, 817-826.
Go to original source...
Go to PubMed...
- Poindron P, Le Neindre P, Levy F, Keverne EB (1984): The physiological-mechanisms of the acceptance of the newborn among sheep. Biology of Behaviour 9, 65-88.
- Poindron P, Caba M, Gomora Arrati P, Krehbiel D, Beyer C (1994): Responses of maternal and non-maternal ewes to social and mother-young separation. Behavioural Processes 31, 97-110.
Go to original source...
Go to PubMed...
- Poindron P, Gilling G, Hernandez H, Serafin N, Terrazas A (2003): Early recognition of newborn goat kids by their mother: I. Nonolfactory discrimination. Developmental Psychobiology 43, 82-89.
Go to original source...
Go to PubMed...
- Poindron P, Levy F, Keller M (2007): Maternal responsiveness and maternal selectivity in domestic sheep and goats: the two facets of maternal attachment. Developmental Psychobiology 49, 54-70.
Go to original source...
Go to PubMed...
- Poindron P, Otal J, Ferreira G, Keller M, Guesdon V, Nowak R, Levy F (2010): Amniotic fluid is important for the maintenance of maternal responsiveness and the establishment of maternal selectivity in sheep. Animal 4, 2057-2064.
Go to original source...
Go to PubMed...
- Porter RH, Levy F, Poindron P, Litterio M, Schaal B, Beyer C (1991): Individual olfactory signatures as major determinants of early maternal discrimination in sheep. Developmental Psychobiology 24, 151-158.
Go to original source...
Go to PubMed...
- Ramirez M, Soto R, Poindron P, Alvarez L, Valencia JJ, Gonzalez F, Terrazas A (2011): Maternal behaviour around birth and mother-young recognition in Pelibuey sheep. Veterinaria Mexico 42, 27-46.
- Rosenblatt JS (1983): Olfaction mediated developmental transition in the altricial newborn of selected species of mammals. Developmental Psychobiology 16, 347-375.
Go to original source...
Go to PubMed...
- Rovira-Castro CE (1973): Phylogenetic evolution of vision life. Revista Medica de Costa Rica 445, 477-499.
- Schaal B, Coureaud G, Langlois D, Ginies C, Semon E, Perrier G (2003): Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 424, 68-72.
Go to original source...
Go to PubMed...
- Schrader L, Todt D (1998): Vocal quality is correlated with levels of stress hormones in domestic pigs. Ethology 104, 859-876.
Go to original source...
- Searby A, Jouventin P (2003): Mother-lamb acoustic recognition in sheep: a frequency coding. Proceedings of the Royal Society B-Biological Sciences 270, 1765-1771.
Go to original source...
Go to PubMed...
- Sebe F, Nowak R, Poindron P, Aubin T (2007): Establishment of vocal communication and discrimination between ewes and their lamb in the first two days after parturition. Developmental Psychobiology 49, 375-386.
Go to original source...
Go to PubMed...
- Sebe F, Aubin T, Boue A, Poindron P (2008): Mother-young vocal communication and acoustic recognition promote preferential nursing in sheep. Journal of Experimental Biology 211, 3554-3562.
Go to original source...
Go to PubMed...
- Sebe F, Duboscq J, Aubin T, Ligout S, Poindron P (2010): Early vocal recognition of mother by lambs: contribution of low- and high-frequency vocalizations. Animal Behaviour 5, 1055-1066.
Go to original source...
- Shillito EE (1975): A comparison of the role of vision and hearing in lambs finding their own dams. Applied Animal Ethology 1, 369-377.
Go to original source...
- Shinozaki A, Hosaka Y, Imagawa T, Uehara M (2010): Topography of ganglion cells and photoreceptors in the sheep retina. Journal of Comparative Neurology 518, 2305-2315.
Go to original source...
Go to PubMed...
- Sugnaseelan S, Prescott NB, Broom D, Wathes CM, Phillips CJC (2013): Visual discrimination learning and spatial acuity in sheep. Applied Animal Behaviour Science 147, 104-111.
Go to original source...
- Terrazas A, Ferreira G, Levy F, Nowak R, Serafin N, Orgeur P, Soto R, Poindron P (1999): Do ewes recognize their lambs within the first day postpartum without the help of olfactory cues? Behavioural Processes 47, 19-29.
Go to original source...
Go to PubMed...
- Terrazas A, Nowak R, Serafin N, Ferreira G, Levy F, Poindron P (2002): Twenty-four-hour-old lambs rely more on maternal behavior than on the learning of individual characteristics to discriminate between their own and an alien mother. Developmental Psychobiology 40, 408-418.
Go to original source...
Go to PubMed...
- Terrazas A, Serafin N, Hernandez H, Nowak R, Poindron P (2003): Early recognition of newborn goat kids by their mother: II. Auditory recognition and evidence of an individual acoustic signature in the neonate. Developmental Psychobiology 43, 311-320.
Go to original source...
Go to PubMed...
- Thorhallsdottir AG, Provenza FD, Balph DF (1990): Ability of lambs to learn about novel foods while observing or participating with social models. Applied Animal Behaviour Science 25, 25-33.
Go to original source...
- Tibbetts EA, Dale J (2007): Individual recognition: it is good to be different. Trends in Ecology and Evolution 22, 529-537.
Go to original source...
Go to PubMed...
- Tomizawa K, Iga N, Lu YF, Moriwaki A, Matsushita M, Li ST, Miyamoto O, Itano T, Matsui H (2003): Oxytocin improves long-lasting spatial memory during motherhood through MAP kinase cascade. Nature Neuroscience 6, 384-390.
Go to original source...
Go to PubMed...
- Val-Laillet D, Nowak R (2006): Socio-spatial criteria are important for the establishment of maternal preference in lambs. Applied Animal Behaviour Science 96, 269-280.
Go to original source...
- Vazquez R, Orihuela A, Flores-Perez FI, Aguirre V (2015): Reducing early maternal licking of male lambs (Ovis aries) does not impair their sexual behavior in adulthood. Journal of Veterinary Behavior 10, 78-82.
Go to original source...
- Vince MA (1993): Newborn lambs and their dams: the interaction that leads to sucking. Advances in the Study of Behavior 22, 239-268.
Go to original source...
- von Borstel UK, Moors E, Schichowski C, Gauly M (2011): Breed differences in maternal behaviour in relation to lamb (Ovis orientalis aries) productivity. Livestock Science 137, 42-48.
Go to original source...
- Winslow JT, Insel TR (2004): Neuroendocrine basis of social recognition. Current Opinion in Neurobiology 14, 248-253.
Go to original source...
Go to PubMed...
This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.