Mother-young vocal communication and acoustic recognition promote preferential nursing in sheep

Journal of Experimental Biology

Volumn 211, Issue 22, 2008, Pages 3554-3562

  Sèbe, Frédéric ^a,b   Aubin, Thierry ^b   Boué, Amélie ^a   Poindron, Pascal ^a  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^b CNRS   (France)

Author keywords

Bleats; Ewe; Lamb; Maternal behaviour; Mother young interactions; Motivation; Playback; Selectivity; Suckling

Indexed keywords

ANIMAL; ANIMAL COMMUNICATION; ARTICLE; FEMALE; MATERNAL BEHAVIOR; NEWBORN; PHYSIOLOGY; PSYCHOLOGICAL ASPECT; PUERPERIUM; RECOGNITION; SHEEP; SUCKING; VOCALIZATION;

ANIMAL COMMUNICATION; ANIMALS; ANIMALS, NEWBORN; FEMALE; MATERNAL BEHAVIOR; POSTPARTUM PERIOD; RECOGNITION (PSYCHOLOGY); SHEEP; SUCKING BEHAVIOR; VOCALIZATION, ANIMAL;

MAMMALIA; OVIS ARIES;

EID: 55949123591     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.016055     Document Type: Article

References (70)

1. Alegria, J. and Noirot, E. (1978). Neonate orientation behavior towards human voice. Int. J. Behav. Dev. 1, 291-312.
2. Alexander, G. (1978). Odour, and the recognition of lambs by Merino ewes. Appl. Anim. Ethol. 4, 153-158.
3. Alexander, G. and Shillito, E. E. (1977a). The importance of odour, appearance and voice in maternal recognition of the young in Merino sheep (Ovis aries). Appl. Anim. Ethol. 3, 127-135.
4. Alexander, G. and Shillito, E. E. (1977b). Importance of visual clues from various body regions in maternal recognition of the young in Merino sheep (Ovis aries). Appl. Anim. Ethol. 3, 137-143.
5. Alexander, G. and Shillito-Walser, E. E. (1978). Visual discrimination between ewes by lambs. Appl. Anim. Ethol. 4, 81-85.
6. Balcombe, J. P. (1990). Vocal recognition of pups by mother Mexican free-tailed bats, Tadarida brasiliensis mexicana. Anim. Behav. 39, 960-966.
7. Balcombe, J. P. and McCracken, G. F. (1992). Vocal recognition in Mexican free-tailed bats: do pups recognize mothers? Anim. Behav. 43, 79-87.
8. Bandura, A. (1977). Social Learning Theory. New York: Prentice Hall.
9. Bouissou, M. F. (1968). Effet de l'ablation des bulbes olfactifs sur la reconnaissance du jeune par sa mère chez les ovins. Rev. Comp. Anim. 2, 77-83.
10. Charrier, I., Mathevon, N. and Jouventin, P. (2001). Mother's voice recognition by seal pups. Nature 412, 873.
11. Charrier, I., Mathevon, N. and Jouventin, P. (2002a). How does a fur seal mother recognize the voice of her pup? An experimental study of Arctocephalus tropicalis. J. Exp. Biol. 205, 603-612.
12. Charrier, I., Mathevon, N., Hassnaoui, M., Carraro, L. and Jouventin, P. (2002b). The subantarctic fur seal pup switches its begging behaviour during maternal absence. Can. J. Zool. 80, 1250-1255.
13. Clutton-Brock, T. H. (1991). The Evolution of Parental Care. Princeton, NJ: Princeton University Press.
14. Dwyer, C. M., McLean, K. A., Chirnside, J., Calvert, S. K. and Lawrence, A. B. (1997). The role of maternal vocalizations in parturient sheep. In Proceedings of the 31st International Congress of the ISAE (ed. P. H. Hemsworth, M. Spinka and L. Kostal), pp. 66. Prague: International Society for Applied Ethology.
15. Dwyer, C. M., McLean, K. A., Deans, L. A., Chirnside, J., Calvert, S. K. and Lawrence, A. B. (1998). Vocalisations between mother and young in sheep: effects of breed and maternal experience. Appl. Anim. Behav. Sci. 58, 105-119.
16. Engh, A. L., Hoffmeier, R. R., Cheney, D. L. and Seyfarth, R. M. (2006). Who, me? Can baboons infer the target of vocalizations? Anim. Behav. 71, 381-387.
17. Espmark, Y. (1971). Individual recognition by voice in reindeer mother-young relationship: field observations and playback experiments. Behaviour 40, 295-301.
18. Ewbank, R. (1964). Observations on the suckling habits of twin lambs. Anim. Behav. 12, 34-37.
19. Fletcher, I. C. (1971). Relationships between frequency of suckling, lamb growth and post-partum oestrous behaviour in ewes. Anim. Behav. 19, 108-111.
20. Goldman, J. A., Phillips, D. P. and Fentress, J. C. (1995). An acoustic basis for maternal recognition in timber wolves (Canis lupus)? J. Acoust. Soc. Am. 3, 1970-1973.
21. González-Mariscal, G. and Poindron, P. (2002). Parental care in mammals: immediate internal and sensory factors of control. In Hormones, Brain and Behavior. Vol. 1 (ed. D. W. Pfaff, A. P. Arnold, A. M. Etgen, S. E. Fahrfbach and R. T. Rubin), pp. 215-298. New York: Academic Press.
22. Gordon, K. and Siegmann, M. (1991). Suckling behavior of ewes in early lactation. Physiol. Behav. 50, 1079-1081.
23. Graves, H. B., Wilson, L. L. and Hess, C. E. (1977). Some observations on activities of a small group of confined ewes with single, twin, or triplet lambs. Appl. Anim. Ethol. 3, 83-88.
24. Hall, W. G., Hudson, R. and Brake, S. C. (1988). Terminology for use in investigations of nursing and suckling. Dev. Psychobiol. 21, 89-91.
25. Hersher, L., Richmond, J. B. and Morre, A. U. (1963). Maternal behavior in sheep and goats. In Maternal Behavior in Mammals (ed. H. L. Rheingold), pp. 203-232. New York: John Wiley.
26. Hess, C. E., Graves, H. B. and Wilson, L. L. (1974). Individual preweaning suckling behavior of single, twin and triplet lambs. J. Anim. Sci. 38, 1313-1318.
27. Hinch, G. N. (1989). The sucking behaviour of triplet, twin and single lambs at pasture. Appl. Anim. Behav. Sci. 22, 39-48.
28. Hinch, G. N., Lécrivain, E., Lynch, J. J. and Elwin, R. L. (1987). Changes in maternal-young associations with increasing age of lambs. Appl. Anim. Behav. Sci. 17, 305-318.
29. Keller, M., Meurisse, M., Poindron, P., Nowak, R., Ferreira, G., Shayit, M. and Levy, F. (2003). Maternal experience influences the establishment of visual/auditory, but not olfactory recognition of the newborn lamb by ewes at parturition. Dev. Psychobiol. 43, 167-176.
30. Kendrick, K. M., Da Costa, A. P. C., Broad, K. D., Ohkura, S., Guevara, R., Levy, F. and Keverne, E. B. (1997). Neural control of maternal behaviour and olfactory recognition of offspring. Brain Res. Bull. 44, 383-395.
31. Lévy, F. and Fleming, A. S. (2006). The neurobiology of maternal behavior in mammals. In The Development of Social Engagement: Neurobiological Perspectives (ed. P. J. Marshall and N. A. Fox), pp. 197-246. Oxford: Oxford University Press.
32. Lévy, F., Kendrick, K., Keverne, E. B., Porter, R. H. and Romeyer, A. (1996). Physiological, sensory and experiential factors of parental care in sheep. Adv. Study Behav. Horm. Behav. 25, 385-473.
33. Lévy, F., Keller, M. and Poindron, P. (2004). Olfactory regulation of maternal behavior in mammals. Horm. Behav. 46, 284-302.
34. Ligout, S., Sèbe, F. and Porter, R. H. (2004). Vocal discrimination of kin and non-kin agemates among lambs. Behaviour 141, 355-369.
35. Lindsay, D. R. and Fletcher, I. C. (1968). Sensory involvement in the recognition of lambs by their dams. Anim. Behav. 16, 415-417.
36. Lynch, J. J., Hinch, G. N. and Adams, D. B. (1992). The behaviour of sheep: biological principles and implications for production: CSIRO Publications and CAB International.
37. McGregor, P. K. (1992). Playback and Studies of Animal Communication. New York: Plenum Press.
38. McGregor, P. K. (2005a). Animal Communication Networks. Cambridge: Cambridge University Press.
39. McGregor, P. K. (2005b). Part II: The effect of particular contexts. In Animal Communication Networks, pp. 129-240. Cambridge: Cambridge University Press.
40. Montigny, D., Coureaud, G. and Schaal, B. (2006). Rabbit pup response to the mammary pheromone: from automatism to prandial control. Physiol. Behav. 89, 742-749.
41. Noirot, E. and Alegria, J. (1983). Neonate orientation towards human voice differs with type of feeding. Behav. Processes 8, 65-71.
42. Noldus, L. P., Trienes, R. J., Hendriksen, A. H., Jansen, H. and Jansen, R. G. (2000). The Observer Video-Pro: new software for the collection, management, and presentation of time-structured data from videotapes and digital media files. Behav. Res. Methods Instrum. Comput. 32, 197-206.
43. Nowak, R. (1990). Lamb's bleats: important for the establishment of the mother-young bond? Behaviour 115, 14-29.
44. Nowak, R. (1991). Senses involved in the discrimination of Merino ewes at close contact and from a distance by their newborn lambs. Anim. Behav. 42, 357-366.
45. Nowak, R. (2006). Suckling, milk, and the development of preferences toward maternal cues by neonates: from early learning to filial attachment? Adv. Study Behav. 36.
46. Nowak, R. and Lindsay, D. R. (1992). Discrimination of Merino ewes by their newborn lambs: important for survival? Appl. Anim. Behav. Sci. 34, 61-74.
47. Nowak, R. and Poindron, P. (2006). From birth to colostrum: early steps leading to lamb survival. Reprod. Nutr. Dev. 46, 431-446.
48. Nowak, R., Murphy, T. M., Lindsay, D. R., Alster, P., Andersson, R. and Uvnas-Moberg, K. (1997). Development of a preferential relationship with the mother by the newborn lamb: importance of the sucking activity. Physiol. Behav. 62, 681-688.
49. Poindron, P. (1976). Mother-young relationships in intact or anosmic ewes at the time of suckling. Biol. Behav. 2, 161-177.
50. Poindron, P. and Carrick, M. J. (1976). Hearing recognition of the lamb by its mother. Anim. Behav. 24, 600-602.
51. Poindron, P., Le Neindre, P., Raksanyi, I., Trillat, G. and Orgeur, P. (1980). Importance of the characteristics of the young in the manifestation and establishment of maternal behaviour in sheep. Reprod. Nutr. Dev. 20, 817-826.
52. Poindron, P., Levy, F. and Keller, M. (2007). Maternal responsiveness and maternal selectivity in domestic sheep and goats: the two facets of maternal attachment. Dev. Psychobiol. 49, 54-70.
53. Ruiz-Miranda, C. R., Szymanski, M. D. and Ingals, J. W. (1993). Physical characteristics of the vocalizations of domestic goat does Capra hircus in response to their offspring cries. Bioacoustics 5, 99-116.
54. Schirar, A., Cognie, Y., Louault, F., Poulin, N., Levasseur, M. C. and Martinet, J. (1989). Resumption of oestrous behaviour and cyclic ovarian activity in suckling and non-suckling ewes. J. Reprod. Fertil. 87, 789-794.
55. Searby, A. and Jouventin, P. (2003). Mother-lamb acoustic recognition in sheep: a frequency coding. Proc. R. Soc. Lond., B, Biol. Sci. 270, 1765-1771.
56. Sèbe, F., Nowak, R., Poindron, P. and Aubin, T. (2007). Establishment of vocal communication and discrimination between ewes and their lamb in the first two days after parturition. Dev. Psychobiol. 49, 375-386.
57. Shillito, E. E. (1975). A comparison of the role of vision and hearing in lambs finding their own dams. Appl. Anim. Ethol. 1, 369-377.
58. Shillito-Walser, E. E., Hague, P. and Walters, E. (1981). Vocal recognition of recorded lamb's voices by ewes of three breeds of sheep. Behaviour 78, 260-272.
59. Shillito-Walser, E. E., Walters, D. and Ellison, J. (1984). Observation of ewes and lambs in the field. Behaviour 91, 190-203.
60. Siegel, S. and Castellan, J. N. J. (1988). Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill.
61. Snowdon, C. T. and Hausberger, M. (1997). Social Influences on Vocal Development. Cambridge: Cambridge University Press.
62. Terrazas, A., Ferreira, G., Levy, F., Nowak, R., Serafin, N., Orgeur, P., Soto, R. and Poindron, P. (1999). Do ewes recognize their lambs within the first day postpartum without the help of olfactory cues? Behav. Processes 47, 19-29.
63. Terrazas, A., Nowak, R., Serafin, N., Ferreira, A., Lévy, F. and 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. Dev. Psychobiol. 40, 408-418.
64. Terrazas, A., Serafin, N., Hernandez, H., Nowak, R. and 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. Dev. Psychobiol. 43, 311-320.
65. Torriani, M. V. G., Vannoni, E. and McElligott, A. G. (2006). Mother-young recognition in an ungulate hider species: a unidirectional process. Am. Nat. 168, 412-420.
66. Treacher, T. T. (1983). Nutrient requirements for lactation in the ewe. In Sheep Production (ed. W. Haresign), pp. 133-153. London: Butterworths.
67. Val-Laillet, D., Simon, M. and Nowak, R. (2004). A full belly and colostrum: two major determinants of filial love. Dev. Psychobiol. 45, 163-173.
68. Vankova, D. and Malek, J. (1997). Characteristics of the vocalizations of Red Deer Cervus elaphus hinds and calves. Bioacoustics 7, 281-289.
69. Vince, M. A. (1993). Newborn lambs and their dams: the interaction that leads to sucking. Adv. Study Behav. 22, 239-268.
70. Walser, E. S. (1978). Some aspects of maternal behaviour in mammals. Med. Biol. 56, 262-271.