Abstract
Mammals owe part of their evolutionary success to the harmonious exchanges of information, energy and immunity between females and their offspring. This functional reciprocity is vital for the survival and normal development of infants, and for the inclusive fitness of parents1,2. It is best seen in the intense exchanges taking place around the mother's offering of, and the infant's quest for, milk. All mammalian females have evolved behavioural and sensory methods of stimulating and guiding their inexperienced newborns to their mammae, whereas newborns have coevolved means to respond to them efficiently3. Among these cues, maternal odours have repeatedly been shown to be involved4,5,6, but the chemical identity and pheromonal nature of these cues have not been definitively characterized until now. Here we focus on the nature of an odour signal emitted by the female rabbit to which newborn pups respond by attraction and oral grasping, and provide a complete chemical and behavioural description of a pheromone of mammary origin in a mammalian species.
Your institute does not have access to this article
Relevant articles
Open Access articles citing this article.
-
Structural Identification, Synthesis and Biological Activity of Two Volatile Cyclic Dipeptides in a Terrestrial Vertebrate
Scientific Reports Open Access 09 March 2020
-
Nasal mucus glutathione transferase activity and impact on olfactory perception and neonatal behavior
Scientific Reports Open Access 28 February 2019
-
Repeated gestational exposure to diesel engine exhaust affects the fetal olfactory system and alters olfactory-based behavior in rabbit offspring
Particle and Fibre Toxicology Open Access 17 January 2019
Access options
Subscribe to Journal
Get full journal access for 1 year
$199.00
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Buy article
Get time limited or full article access on ReadCube.
$32.00
All prices are NET prices.




References
Clutton-Brock, T. H. The Evolution of Parental Care (Princeton Univ. Press, 1991)
Rosenblatt, J. S. & Snowdon, T. C. Parental Care, Evolution, Mechanisms and Adaptive Significance (Academic, Orlando, 1996)
Rosenblatt, J. S. Olfaction mediates developmental transition in the altricial newborn of selected species of mammals. Dev. Psychobiol. 16, 347–375 (1983)
Leon, M. & Moltz, H. Maternal pheromone: Discrimination by pre-weanling albino rats. Physiol. Behav. 7, 265–267 (1971)
Blass, E. M. & Teicher, M. H. Suckling. Science 210, 15–22 (1980)
Macfarlane, A. J. Olfaction in the development of social preferences in the human neonate. Ciba Found. Symp. 33, 103–117 (1975)
Zarrow, M. X., Denenberg, V. H. & Anderson, C. O. Rabbit: Frequency of suckling in the pup. Science 150, 1835–1836 (1965)
Coureaud, G. et al. Immediate postnatal sucking in the rabbit: Its influence on pup survival and growth. Reprod. Nutr. Dev. 40, 19–32 (2000)
Schley, P. Geruchssinn und Saugverhalten bei Jungkaninchen. Kleintier Praxis 26, 261–263 (1981)
Hudson, R. & Distel, H. Nipple location by newborn rabbits: Evidence for pheromonal guidance. Behaviour 85, 260–275 (1983)
Coureaud, G. & Schaal, B. Attraction of newborn rabbits to abdominal odors of adult conspecifics differing in sex and physiological state. Dev. Psychobiol. 36, 271–281 (2000)
Keil, W., von Stralendorff, F. & Hudson, R. A behavioral bioassay for analysis of rabbit nipple-search pheromone. Physiol. Behav. 47, 525–529 (1990)
Coureaud, G., Schaal, B., Langlois, D. & Perrier, G. Orientation response of newborn rabbits to odours of lactating females: Relative effectiveness of surface and milk cues. Anim. Behav. 61, 153–162 (2001)
Coureaud, G. Régulation Olfactive de la Prise Lactée chez le Lapereau: Caractérisation Éthologique et Chimique d'un Signal Phéromonal. Thesis, Univ. Paris 13 (2001)
Beauchamp, G. K., Doty, R. L., Moulton, D. G. & Mugford, R. A. in Olfaction, Behavior, and Mammalian Reproduction (ed. Doty, R. L.) 143–160 (Academic, New York, 1976)
Johnston, R. E. in The Neurobiology of Taste and Smell, 2nd edn (eds Finger, T. E., Silver, W. L. & Restrepo, D.) 101–127 (Wiley-Liss, New York, 2000)
Goodrich, B. S., Hesterman, E. R., Shaw, K. S. & Mykytowycz, R. Identification of some volatile compounds in the odor of fecal pellets of the rabbit, Oryctolagus cuniculus. J. Chem. Ecol. 7, 817–827 (1981)
Pedersen, P. A. & Blass, E. M. in The Development of Perception: Psychobiological Perspectives (eds Aslin, R. N., Alberts, J. R. & Petersen, M. R.) 359–381 (Academic, New York, 1981)
Galef, B. G., Mason, J. F., Preti, G. & Bean, N. J. Carbon disulfide: A semiochemical mediating socially-induced diet choice in rats. Physiol. Behav. 42, 119–124 (1988)
Coureaud, G., Schaal, B., Hudson, R., Orgeur, P. & Coudert, P. Transnatal olfactory continuity in the rabbit: Behavioral evidence and short-term consequence of its disruption. Dev. Psychobiol. 40, 372–390 (2002)
Muller-Schwarze, D. et al. in Chemical Signals in Vertebrates 4 (eds Duvall, D., Muller-Schwarze, D. & Silverstein, R. M.) 561–570 (Plenum, New York, 1986)
Morrow-Tesch, J. & McGlone, J. J. Sensory systems and nipple attachment behavior in neonatal pigs. Physiol. Behav. 47, 1–4 (1989)
Teicher, M. H. & Blass, E. M. First suckling response of the newborn albino rat: The roles of olfaction and amniotic fluid. Science 198, 635–636 (1977)
Sam, M. et al. Odorants may arouse instinctive behaviours. Nature 412, 142 (2001)
Zou, Z., Horowitz, L. F., Montmayeur, J. P., Snapper, S. & Buck, L. B. Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Nature 414, 173–179 (2001)
Johnson, B. A. & Leon, M. Odorant molecular length: One aspect of the olfactory code. J. Comp. Neurol. 426, 330–338 (2000)
Uchida, N., Takahashi, Y., Tanifuji, M. & Mori, K. Odor maps in the mammalian olfactory bulb: Domain organization and odorant structural features. Nature Neurosci. 3, 1035–1043 (2000)
Abbott, N., Etievant, P., Issanchou, S. & Langlois, D. Critical evaluation of two commonly used techniques for the treatment of data from extract dilution sniffing analysis. J. Agric. Food Chem. 41, 1698–1703 (1993)
Schley, P. Untersuchung zur kuenstlichen Aufzucht von Hauskaninchen. Thesis, Univ. Giessen (1976)
Lebas, F. Description d'une machine à traire les lapines. Ann. Zootech. 19, 223–228 (1970)
Acknowledgements
We thank J. L. Le Quéré for support and advice; P. Coudert, J. Ponceau, J. L. Vrillon and P. Mercier for giving access to their colonies; P. Orgeur, J. P. Drouet, M. Jouanno, F. Lebas, L. Fortun-Lamothe, M. Theau-Clément, G. Thébault, G. Bolet, A. Locatelli, Y. Breuzin and J. P. Francinot for contributions; D. Licois and R. Hudson for providing Lebas' and Schley's milking devices; R. L. Doty, V. H. Dennenberg, A. Holley, J. P. Montmayeur, P. Coudert, R. Hudson, P. Salin and H. Distel for discussions; and R. Langlois, E. Hertling and C. Ferdenzi for logistic support. This work was conducted in part while B.S. and G.C. were at Unité de Physiologie de la Reproduction, CNRS-Inra, Nouzilly, France. G.C. was sponsored by Région Poitou-Charente-Inra and the Fyssen Foundation.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing financial interests.
Rights and permissions
About this article
Cite this article
Schaal, B., Coureaud, G., Langlois, D. et al. Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 424, 68–72 (2003). https://doi.org/10.1038/nature01739
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature01739
Further reading
-
Sniffing out smell’s effects on human behaviour
Nature (2022)
-
Composition and compound proportions affect the response to complex chemical signals in a spiny lizard
Behavioral Ecology and Sociobiology (2021)
-
Structural Identification, Synthesis and Biological Activity of Two Volatile Cyclic Dipeptides in a Terrestrial Vertebrate
Scientific Reports (2020)
-
Structural, morphometric and immunohistochemical study of the rabbit accessory olfactory bulb
Brain Structure and Function (2020)
-
The evolution of (non)species-specific pheromones
Evolutionary Ecology (2020)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.