Abstract
Lactating rabbit females (Oryctolagus cuniculus) emit abdominal, ventral odour cues that are involved in guiding the pups to the nipples. We tested the impact of the females’ social rank and age on the emission of this odour signal; both factors are highly collinear in wild rabbits and we did not aim to disentangle them in our study. We predicted that the abdominal odours of young, low-ranking females, which are usually more stressed and have a comparatively lower body condition, should be less attractive to pups than those of older, high-ranking females. For the experiment, we caught females from a population of wild-type European rabbits living in a large field enclosure. Pairs of adult females were placed in boxes with wire-mesh floor fixed over an arena with three rabbit pups aged 4–7 days old. First, we evaluated the effectiveness of our two-choice design by testing lactating females (LF) against non-lactating (NLF) controls (n = 17 pairs). In accordance with recent studies, the pups showed a clear preference for lactating females by means of a higher exploration time and more local searching under the ventral region of these females. In a second experiment, the pups chose between lactating 1-year-old, low-ranking females (Y/LRF) and older, high-ranking females (O/HRF) (n = 10 pairs). These latter assays suggested a comparatively lower attractiveness of Y/LRF females to pups searching for milk. Although the pups showed no significant preference in exploration behaviour, they preferably directed local searching events to the abdominal region of O/HRF females. In conclusion, our study suggests that mother–offspring chemosensory communication is modified by the mother’s age and social rank, i.e., by a complex of factors that are strongly linked in rabbit females in the wild.
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References
Akema T, Chiba A, Shinozaki R, Oshida M, Kimura F, Toyoda J (1996) Acute immobilization stress and intraventricular injection of CRF suppress naloxone-induced LH release in ovariectomized estrogen-primed rats. J Neuroendocrin 8:647–652
Alberts JR, May B (1980) Ontogeny of olfaction: development of the rats’ sensitivity to urine and amyl acetate. Physiol Behav 24:965–970
Albrecht ED, Nightingale MS, Towsley JD (1977) Stress decreases serum progesterone concentrations in pregnant baboons. Fed Proc 36:390
Blass EM, Teicher MH (1980) Suckling. Science 210:15–22
Brambell FWR (1944) The reproduction of the wild rabbit Oryctolagus cuniculus (L.). Proc Zool Soc Lond 114:1–45
Broekhuizen S, Mulder L (1983) Differences and similarities in nursing behaviour of hares and rabbits. Acta Zool Fennica 174:61–63
Bronson FH (1989) Mammalian reproductive biology. University of Chicago Press, Chicago
Chatterton RT, Hill PD, Aldag JC, Hodges KR, Belknap SM, Zinaman MJ (2000) Relation of plasma oxytocin and prolactin concentrations to milk production in mothers of preterm infants: influence of stress. J Clin Endocrin Metab 85:3661–3668
Coureaud G (2001) Olfactory regulation of sucking in newborn rabbit: Ethological and chemical characterization of a pheromonal signal. PhD Thesis, University Paris 13, France
Coureaud G, Schaal B (2000) Attraction of newborn rabbits to abdominal odors of adult conspecifics differing in sex and physiological state. Dev Psychobiol 36:271–281
Coureaud G, Schaal B (2008) Psychobiological functions of the mammary pheromone in newborn rabbits. In: Hurst JL, Beynon RJ, Roberts SC, Wyatt TD (eds) Chemical signals in vertebrates, vol 11. Springer, New York, pp 305–313
Coureaud G, Schaal B, Coudert P, Rideaud P, Fortun-Lamothe L, Hudson R, Orgeur P (2000) Immediate postnatal suckling in the rabbit: its influence on pup survival and growth. Reprod Nutr Dev 40:19–32
Coureaud G, Schaal B, Langlois D, Perrier G (2001) Orientation response of newborn rabbits to odours emitted by lactating females: relative effectiveness of surface and milk cues. Anim Behav 61:153–162
Coureaud G, Schaal B, Hudson R, Orgeur P, Coudert P (2002) Transnatal olfactory continuity in the rabbit: behavioral evidence and short-term consequence of its disruption. Dev Psychobiol 40:372–390
Coureaud G, Langlois D, Perrier G, Schaal B (2003) A single-key odorant accounts for the pheromonal effect of rabbit milk: further test of the mammary pheromone’s activity against a wide sample of volatiles from milk. Chemoecology 13:187–192
Coureaud G, Langlois D, Sicard G, Schaal B (2004) Newborn rabbit responsiveness to the mammary pheromone is concentration-dependent. Chem Senses 29:341–350
Coureaud G, Langlois D, Perrier G, Schaal B (2006) Convergent changes in the maternal emission and pup reception of the rabbit mammary pheromone. Chemoecology 16:169–174
Coureaud G, Fortun-Lamothe L, Langlois D, Schaal B (2007) The reactivity of neonatal rabbits to the mammary pheromone as a probe for viability. Animal 1:1026–1032
Coureaud G, Fortun-Lamothe L, Rödel HG, Monclús R, Schaal B (2008a) Development of the social and feeding behaviour in young rabbits. In: Xiccato G, Trocino A, Lukefahr SD (eds) Proceedings of the 9th World Rabbit Congress, Verona, Italy. FIZZ, Brescia, Italy, pp 1131–1146
Coureaud G, Rödel HG, Kurz CA, Schaal B (2008b) The responsiveness of young rabbits to the mammary pheromone: developmental course in domestic and wild pups. Chemoecology 18:53–59
González-Mariscal G, Rosenblatt JS (1996) Maternal behavior in rabbits: a historical and multidisciplinary perspective. Adv Stud Behav 25:333–360
González-Mariscal G, Chirino R, Hudson R (1994) Prolactin stimulates emission of nipple pheromone in ovariectomized New Zealand white rabbits. Biol Reprod 50:373–376
Hudson R, Distel H (1983) Nipple location by newborn rabbits: behavioural evidence for pheromonal guidance. Behaviour 85:260–275
Hudson R, Distel H (1984) Nipple-search pheromone in rabbits: dependence on season and reproductive state. J Comp Physiol A 155:13–17
Hudson R, Distel H (1990) Sensitivity of female rabbits to changes in photoperiod as measured by pheromone emission. J Comp Physiol A 167:225–230
Hudson R, Gonzáles-Mariscal G, Beyer C (1990) Chin marking behavior, sexual reception, and pheromone emission in steroid-treated, ovariectomized rabbits. Horm Behav 24:1–13
Hudson R, Bilkó Á, Altbäcker V (1996) Nursing, weaning and the development of independent feeding in the rabbit. Z Säugetierkd 61:39–48
Hudson R, Rojas C, Arteaga L, Martínez-Gómez M, Distel H (2008) Rabbit nipple-search pheromone versus rabbit mammary pheromone revisited. In: Hurst JL, Beynon RJ, Roberts SC, Wyatt TD (eds) Chemical signals in vertebrates, vol 11. Springer, New York, pp 315–324
Kam K, Park Y, Cheon M, Son GH, Kim K, Ryu K (2000) Effects of immobilization stress on estrogen-induced surges of luteinizing hormone and prolactin in ovariectomized rats. Endocrine 12:279–287
Keil W, von Stralendorff F, Hudson R (1990) A behavioral bioassay for analysis of rabbit nipple-search pheromone. Physiol Behav 47:525–529
König B (1994) Communal nursing in mammals. Verh Dtsch Zool Ges 87:115–127
Leon M, Moltz H (1971) Maternal pheromone: discrimination by pre-weanling albino rats. Physiol Behav 7:265–267
Macfarlane AJ (1975) Olfaction in the development of social preferences in human neonates. Ciba Found Symp 33:103–117
Martin P, Bateson P (1986) Measuring behaviour. Cambridge University Press, Cambridge
Montigny D, Coureaud G, Schaal B (2006) Newborn rabbit response to the mammary pheromone: from automatism to prandial control. Physiol Behav 89:742–749
Myers K, Poole WE (1961) A study of the biology of the wild rabbit, Oryctolagus cuniculus (L.), in confined populations. II. The effects of season and population increase on behaviour. CSIRO Wildl Res 6:1–41
Myers K, Bults HG, Gilbert N (1977) Stress in the rabbit. Part XI in the series: the biology of the wild rabbit in climatically different regions in Australia. Austr J Ecol 10:103–136
Mykytowycz R (1958) Social behaviour of an experimental colony of wild rabbits, Oryctolagus cuniculus (L.). I. Establishment of the colony. CSIRO Wildl Res 3:7–25
Mykytowycz R, Fullagar PJ (1973) Effects of social environment on reproduction in the rabbit, Oryctolagus cuniculus (L.). J Reprod Fert 19:503–522
Rödel HG (2000) Low temperature effects and social influences on physiological condition of subadult wild rabbits. In: Heldmaier G, Klingenspor M (eds) Life in the cold. Springer, Berlin, pp 511–518
Rödel HG (2005) Winter feeding behaviour of European rabbits in a temperate zone habitat. Mamm Biol 70:300–306
Rödel HG, Bora A, Kaiser J, Kaetzke P, Khaschei M, von Holst D (2004a) Density-dependent reproduction in the European rabbit: a consequence of individual response and age-dependent reproductive performance. Oikos 104:529–539
Rödel HG, Bora A, Kaetzke P, Khaschei M, Hutzelmeyer H, von Holst D (2004b) Over-winter survival in subadult European rabbits: weather effects, density-dependence, and the impact of individual characteristics. Oecologia 140:566–576
Rödel HG, Starkloff A, Bruchner B, von Holst D (2008a) Social environment and reproduction in female European rabbits (Oryctolagus cuniculus): benefits of the presence of litter sisters. J Comp Psychol 122:73–83
Rödel HG, Starkloff A, Bautista A, Friedrich AC, von Holst D (2008b) Infanticide and maternal offspring defence in European rabbits under natural breeding conditions. Ethology 114:22–31
Rödel HG, Starkloff A, Prager G, Seltmann MW, von Holst D (2008c) Causes and predictors of nest mortality in a European rabbit population. Mamm Biol. doi:10.1016/j.mambio.2008.04.003
Schaal B (1988) Olfaction in infants and children: developmental and functional perspectives. Chem Senses 13:145–190
Schaal B, Coureaud G, Langlois D, Giniès C, Sémon E, Perrier G (2003) Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 424:68–72
Schaal B, Coureaud G, Moncomble AS, Langlois D, Perrier G (2008) A myriad of common odour cues and (at least) one pheromone shaping the behaviour of young rabbits: a brief survey. In: Alves PC, Ferrand NM, Hackländer K (eds) Lagomorph biology. Evolution, ecology and conservation. Springer, Berlin, pp 189–209
Schley P (1979) Olfaction and suckling behavior in young rabbits. In: Proceedings of World Lagomorph Conference, Guelph, Canada, pp 291–294
Schradin C (2006) Whole day follows of the striped mouse. J Ethol 24:37–43
Schradin C, Pillay N (2004) The striped mouse (Rhabdomys pumilio) from the succulent karoo of South Africa: a territorial group living solitary forager with communal breeding and helpers at the nest. J Comp Psychol 118:37–47
Steven DA, Köstner EP (1972) Open-field responses of rats to odors from stressed and nonstressed predecessors. Behav Biol 7:519–525
Valenta JG, Rigby MK (1968) Discrimination of the odor of stressed rats. Science 161:599–601
von Holst D (1998) The concept of stress and its relevance for animal behavior. Adv Study Behav 27:1–131
von Holst D, Hutzelmeyer HD, Kaetzke P, Khaschei M, Schönheiter R (1999) Social rank, stress, fitness, and life expectancy in wild rabbits. Naturwissenschaften 86:338–393
von Holst D, Hutzelmeyer HD, Kaetzke P, Khaschei M, Rödel HG, Schrutka H (2002) Social rank, fecundity and lifetime reproductive success in wild European rabbits (Oryctolagus cuniculus). Behav Ecol Sociobiol 51:245–254
Wallage-Drees M (1989) A field study on seasonal changes in circadian activity of rabbits. Z Säugetierkd 51:26–36
Wiebold JL, Stanfield PH, Becker WC, Hiller JK (1986) The effect of restrain stress in early pregnancy mice. J Reprod Fertil 35:183–186
Wyatt TD (2003) Pheromones and animal behaviour. Communication by smell and taste. Cambridge University Press, Cambridge
Zarrow MX, Denenberg VM, Anderson CO (1965) Rabbit: frequency of suckling in the pup. Science 150:1835–1836
Acknowledgments
We are grateful to Manuela Zapka, Barbara Bruchner, Anett Starkloff and Christfried Kurz who helped with the field work. The manuscript was improved by helpful discussions with Dietrich von Holst and Carsten Schradin. We are very much obliged to Rainer Kolb for the generous delivery of vaccines for our rabbit population. All animal experiments were performed according to the current law of Germany. Permission for studies on the European rabbit population of the field enclosure was granted by the government of Middle Franconia (211-3894a).
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Rödel, H.G., Coureaud, G., Monclús, R. et al. Abdominal odours of young, low-ranking European rabbit mothers are less attractive to pups: an experiment with animals living under natural breeding conditions. J Ethol 27, 307–315 (2009). https://doi.org/10.1007/s10164-008-0120-1
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DOI: https://doi.org/10.1007/s10164-008-0120-1