Embryonic exposure of chicken chicks (Gallus gallus domesticus) leads to heightened sensitivities towards the exposed scent

in Behaviour
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In chickens, food consumption can be altered by exposing the chicks to scents as embryos. We exposed eggs to an orange-scented food additive in the final days of incubation. Following hatching, we tested these exposed chicks’ ability to detect this scent at a variety of concentrations. We found that orange-exposed chicks responded to an orange-scented solution at lower concentrations than control chicks. This sensitization may allow chicks to be more effective at locating acceptable food items but requires further testing to determine its significance. Orange-exposed and control chicks were also tested with the scent of raspberry. Orange-exposed chicks responded to the raspberry presentation significantly more than the control chicks did, suggesting that the embryonic exposure to orange may have influenced how the chicks responded towards another fruity smell. This result suggests that chicks may be learning general characteristics of exposed scents while in the egg, though this needs further research.



Aigueperse, N., Calandreau, L. & Bertin, A. (2013). Maternal diet influences offspring feeding behavior and fearfulness in the precocial chicken. — PLoS ONE 8: e77583.

Amo, L., Jansen, J.J., van Dam, N.M., Dicke, M. & Visser, M.E. (2013). Birds exploit herbivore-induced plant volatiles to locate herbivorous prey. — Ecol. Lett. 16: 1348-1355.

Ayer-Le Lievre, C., Lapointe, F. & Leibovici, M. (1995). Avian olfactory neurogenesis. — Biol. Cell. 84: 25-34.

Bang, B.G. (1971). Functional anatomy of the olfactory system in 23 orders of birds. — Acta Anat. 79(Suppl. 1): 1-76.

Bang, B.G. & Cobb, S. (1968). The size of the olfactory bulb in 108 species of birds. — Auk 85: 55-61.

Bertin, A., Calandreau, L., Arnould, C. & Levy, F. (2012). The developmental stage of chicken embryos modulates the impact of in ovo olfactory stimulation on food preferences. — Chem. Senses. 37: 253-261.

Bertin, A., Calandreau, L., Arnould, C., Nowak, R., Levy, F., Noirot, V., Bouvarel, I. & Leterrier, C. (2010). In ovo olfactory experience influences post-hatch feeding behaviour in young chickens: prehatch olfaction and feeding. — Ethology 116: 1027-1037.

Board, R.G. (1982). Properties of avian egg shells and their adaptive value. — Biol. Rev. 57: 1-28.

Bonadonna, F., Caro, S., Jouventin, P. & Nevitt, G.A. (2006). Evidence that blue petrel, Halobaena caerulea, fledglings can detect and orient to dimethyl sulfide. — J. Exp. Biol. 209: 2165-2169.

Caspers, B.A., Hagelin, J., Bock, S. & Krause, E.T. (2015). An easy method to test odour recognition in songbird hatchlings. — Ethology 121: 882-887.

Caspers, B.A., Hagelin, J.C., Paul, M., Bock, S., Willeke, S. & Krause, E.T. (2017). Zebra Finch chicks recognise parental scent, and retain chemosensory knowledge of their genetic mother, even after egg cross-fostering. — Sci. Rep. 7: 12859.

Coureaud, G., Hamdani, Y., Schaal, B. & Thomas-Danguin, T. (2009). Elemental and configural processing of odour mixtures in the newborn rabbit. — J. Exp. Biol. 212: 2525-2531.

Coureaud, G., Thomas-Danguin, T., Le Berre, E. & Schaal, B. (2008). Perception of odor blending mixtures in the newborn rabbit. — Physiol. Behav. 95: 194-199.

Culik, B. (2001). Finding food in the open ocean: foraging strategies in Humboldt penguins. — Zoology 104: 327-338.

Cunningham, G.B. & Bonadonna, F. (2015). King penguins can detect two odours associated with conspecifics. — J. Exp. Biol. 218: 3374-3376.

Cunningham, G.B., Strauss, V. & Ryan, P.G. (2008). African penguins (Spheniscus demersus) can detect dimethyl sulphide, a prey-related odour. — J. Exp. Biol. 211: 3123-3127.

Cunningham, G.B., Van Buskirk, R.W., Bonadonna, F., Weimerskirch, H. & Nevitt, G.A. (2003). A comparison of the olfactory abilities of three species of procellariiform chicks. — J. Exp. Biol. 206: 1615-1620.

Drapkin, P.T. & Silverman, J. (1999). Development of the chick olfactory nerve. — Dev. Dyn. 214: 349-360.

Fluck, E., Hogg, S., Mabbut, P.S. & File, S.E. (1996). Behavioural and neurochemical responses of male and female chicks to cat odour. — Pharmacol. Biochem. Behav. 54: 85-91.

Gomez, G. & Celii, A. (2008). The peripheral olfactory system of the domestic chicken: physiology and development. — Brain Res. Bull. 76: 208-216.

Graves, G.R. (1992). Greater yellow-headed vulture (Cathartes melambrotus) locates food by olfaction. — J. Raptor Res. 26: 38-39.

Grubb, T.C. (1972). Smell and foraging in shearwaters and petrels. — Nature. 237: 404-405.

Hagelin, J.C. (2007). Odors and chemical signaling. — In: Reproductive behavior and phylogeny of aves, Vol. 6B (Jamieson, B.G.M., ed.). Science Publishers, Enfield, NH, p. 76-119.

Hagelin, J.C., Simonet, J.C. & Lyson, T.R. (2013). Embryonic domestic chickens can detect compounds in an avian chemosignal before breathing air. — In: Chemical signals in vertebrates 12 (East, M.L. & Dehnhard, M., eds). Springer, New York, NY, p. 363-377.

Hutchison, L.V. & Wenzel, B.M. (1980). Olfactory guidance in foraging by procellariformes. — Condor 82: 314-319.

Jones, R.B. (1987). Food neophobia and olfaction in domestic chicks. — Bird Behav. 7: 78-81.

Jones, R.B. & Carmichael, N.L. (1999). Domestic chicks are attracted to a familiar odorant in a novel test situation: a brief report. — Appl. Anim. Behav. Sci. 61: 351-356.

Jones, R.B., Facchin, L. & McCorquodale, C. (2002). Social dispersal by domestic chicks in a novel environment: reassuring properties of a familiar odourant. — Anim. Behav. 63: 659-666.

Jones, R.B. & Gentle, M.J. (1985). Olfaction and behavioral modification in domestic chicks (Gallus domesticus). — Physiol. Behav. 34: 917-924.

Jones, R.B. & Roper, T.J. (1997). Olfaction in the domestic fowl: a critical review. — Physiol. Behav. 62: 1009-1018.

Krause, E.T., Schrader, L. & Caspers, B.A. (2016). Olfaction in chicken (Gallus gallus): a neglected mode of social communication?FEVO 4: 94.

Lalloue, F.L., Ayer Le-Lievre, C. & Sicard, G. (2003). Analysis of the functional maturation of olfactory neurons in chicks before and after birth. — Chem. Senses. 28: 729-737.

Liu, A., Savya, S. & Urban, N.N. (2016). Early odorant exposure increases the number of mitral and tufted cells associated with a single glomerulus. — J. Neurosci. 36: 11646-11653.

McKeegan, D.E.F., Demmers, T.G., Wathes, C., Jones, R.B. & Gentle, M.J. (2002). Stimulus-response functions of single avian olfactory bulb neurones. — Brain Res. 953: 101-111.

McKeegan, D.E.F. & Lippens, N. (2003). Adaptation responses of single avian olfactory bulb neurones. — Neurosci. Lett. 344: 83-86.

Mennerat, A. (2008). Blue tits (Cyanistes caeruleus) respond to an experimental change in the aromatic plant odour composition of their nest. — Behav. Processes. 79: 189-191.

O’Neill, G., Musto, C. & Gomez, G. (2016). Chronic odorant exposure upregulates acquisition of functional properties in cultured embryonic chick olfactory sensory neurons: odors modulate olfactory neuron differentiation. — J. Neurosci. Res. 95: 1216-1224.

Owre, O.T. & Northington, P.O. (1961). Indication of the sense of smell in the Turkey vulture, Cathartes aura (Linnaeus), from feeding tests. — Am. Midl. Nat. 66: 200-205.

Porter, R.H., Hepper, P.G., Bouchot, C. & Picard, M. (1999). A simple method for testing odor detection and discrimination in chicks. — Physiol. Behav. 67: 459-462.

Porter, R.H., Picard, M., Arnould, C. & Tallet, C. (2002). Chemosensory deficits are associated with reduced weight gain in newly hatched chicks. — Anim. Res. 51: 337-345.

Sneddon, H., Hadden, R. & Hepper, P.G. (1998). Chemosensory learning in the chicken embryo. — Physiol. Behav. 64: 133-139.

Todrank, J., Heth, G. & Restrepo, D. (2010). Effects of in utero odorant exposure on neuroanatomical development of the olfactory bulb and odour preferences. — Proc. Roy. Soc. Lond. B: Biol. Sci. 278: 1949-1955.

Turro, I., Porter, R.H. & Picard, M. (1994). Olfactory cues mediate food selection by young chicks. — Physiol. Behav. 55: 761-767.

Voznessenskaya, V.V., Parfyonova, V.M. & Wysocki, C.J. (1994). Induced olfactory sensitivity in rodents: a general phenomenon. — Adv. Biosci. 93: 399-406.

Yee, K.K. & Wysocki, C.J. (2001). Odorant exposure increases olfactory sensitivity: olfactory epithelium is implicated. — Physiol. Behav. 72: 705-711.


  • The number of orange-exposed and control chicks responding to each presentation.

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  • Responses of orange-exposed birds (black bars) and control birds (grey bars) to different concentrations of McCormick imitation orange extract, or water. Panel a shows that orange-exposed birds had significantly greater responses to 100, 50 and 25% orange extract, as compared to their response to water (p<0.05; Wilcoxon signed-rank test). Panel b shows that control chicks had significantly greater responses to 100% and 50% orange extract as compared to their response to water (p<0.05). See Results for details.

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  • Multiple regression model testing whether the order of the presentation of the odour, the presentation (orange dilution series or water), or the interaction between order and the presentation affect the response given by the chicks.

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  • Responses of (a) orange-exposed birds (black bars) and (b) control birds (grey bars) to McCormick imitation raspberry or almond extract, or water. Compared to the response to water, the response to raspberry was higher for orange-exposed chicks (p<0.05, Mann–Whitney U-test), but not for control chicks. Both groups responded similarly to the almond presentation as compared to water. See Results for details.

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  • Data collected from Gas Chromatograph for (a) orange and (b) raspberry extract. Data were collected on a Thermo Scientific Trace 1300 Series Gas Chromatograph-ISQ Single Quadrupole Mass Spectrometer using a 30 m × 0.25 mm i.d. Capillary column with a 0.25 mm coating of 5%phenyl/95% methyl silicone (Crossbond™, Restek catalog No. 12223) with a carrier flow of 1.5 ml He/min and collected as EI mass spectra. The temperature program was 40°C for 1 min, ramped at 20°C/min to 250°C and then held at 250°C for 1 min. Samples were injected neat as 1 μl samples with a split ratio of 33.

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