Proceedings of the Royal Society B: Biological Sciences
You have accessResearch articles

Avian maternal response to chick distress

    The extent to which an animal is affected by the pain or distress of a conspecific will depend on its capacity for empathy. Empathy most probably evolved to facilitate parental care, so the current study assessed whether birds responded to an aversive stimulus directed at their chicks. Domestic hens were exposed to two replicates of the following conditions in a counterbalanced order: control (C; hen and chicks undisturbed), air puff to chicks (APC; air puff directed at chicks at 30 s intervals), air puff to hen (APH; air puff directed at hen at 30 s intervals) and control with noise (CN; noise of air puff at 30 s intervals). During each test, the hens' behaviour and physiology were measured throughout a 10 min pre-treatment and a 10 min treatment period. Hens responded to APH and APC treatments with increased alertness, decreased preening behaviour and a reduction in eye temperature. No such changes occurred during any control period. Increased heart rate and maternal vocalization occurred exclusively during the APC treatment, even though chicks produced few distress vocalizations. The pronounced and specific reaction observed indicates that adult female birds possess at least one of the essential underpinning attributes of empathy.

    References

    • 1
      Preston S. D.& de Waal F. B. M.. 2002Empathy: its ultimate and proximate bases. Behav. Brain Sci. 25, 1–2.doi:10.1017/S0140525X02000018 (doi:10.1017/S0140525X02000018). Crossref, PubMedGoogle Scholar
    • 2
      de Waal F. B. M.. 2003On the possibility of animal empathy. Feelings and emotions: the Amsterdam symposium (eds , Manstead A. S. R., Frijda N. H.& Fisch A.), ch. 22, pp. 377–399. Cambridge, UK: Cambridge University Press. Google Scholar
    • 3
      de Waal F. B. M.. 2008Putting the altruism back into altruism: the evolution of empathy. Annu. Rev. Psychol. 59, 279–300.doi:10.1146/annurev.psych.59.103006.093625 (doi:10.1146/annurev.psych.59.103006.093625). Crossref, PubMedGoogle Scholar
    • 4
      Singer T.. 2006The neuronal basis and ontogeny of empathy and mind reading: review of literature and implications for future research. Neurosci. Biobehav. Rev. 30, 855–863.doi:10.1016/j.neubiorev.2006.06.011 (doi:10.1016/j.neubiorev.2006.06.011). Crossref, PubMedGoogle Scholar
    • 5
      Wascher C. A. F., Isabella Scheiber I. B. R.& Kotrschal K.. 2008Heart rate modulation in bystanding geese watching social and non-social events. Proc. R. Soc. B 275, 1653–1659.doi:10.1098/rspb.2008.0146 (doi:10.1098/rspb.2008.0146). LinkGoogle Scholar
    • 6
      Fraser O. N.& Bugnyar T.. 2010Do ravens show consolation? Responses to distressed others. PLoS ONE 5, e10605.doi:10.1371/journal.pone.0010605 (doi:10.1371/journal.pone.0010605). Crossref, PubMedGoogle Scholar
    • 7
      Jeon D., Kim S., Chetana M., Jo D., Ruley H. E., Lin S. Y., Rabah D., Kinet J. P.& Shin H. S.. 2010Observational fear learning involves affective pain system and Ca(v)1.2 Ca2+ channels in ACC. Nat. Neurosci. 13, 482–488.doi:10.1038/nn.2504 (doi:10.1038/nn.2504). Crossref, PubMedGoogle Scholar
    • 8
      Walker C.-D., Kudreikis K., Sherrard A.& Johnston C. C.. 2003Repeated neonatal pain influences maternal behavior, but not stress responsiveness in rat offspring. Brain Res. Dev. Brain Res. 140, 253–261.doi:10.1016/S0165-3806(02)00611-9 (doi:10.1016/S0165-3806(02)00611-9). Crossref, PubMedGoogle Scholar
    • 9
      Wilkins L. J., Pope S., Leeb C., Glen E., Phillips A., Zimmerman P., Nicol C.& Brown S. N.. 2005Fracture rate in laying-strain hens at the end of the rearing period and the end of the laying period. Anim. Sci. Pap. Rep. 23, 189–194. Google Scholar
    • 10
      Knowles T. G., Kestin S. C., Haslam S. M., Brown S. N., Green L. E., Butterworth A., Pope S. J., Pfeiffer D.& Nicol C. J.. 2008Leg disorders in broiler chickens: prevalence, risk factors and prevention. PLoS ONE 6, e1545. (doi:10.1371/journal.pone.0001545). Google Scholar
    • 11
      Wauters A. M.& Richard-Yris M. A.. 2003Maternal food calling in domestic hens: influence of feeding context. C. R. Biol. 326, 677–686.doi:10.1016/s1631-0691(03)00128-8 (doi:10.1016/s1631-0691(03)00128-8). Crossref, PubMedGoogle Scholar
    • 12
      Roden C.& Wechsler B.. 1998A comparison of the behaviour of domestic chicks reared with or without a hen in enriched pens. Appl. Anim. Behav. Sci. 55, 317–326.doi:10.1016/S0168-1591(97)00073-7 (doi:10.1016/S0168-1591(97)00073-7). CrossrefGoogle Scholar
    • 13
      Shimmura T., Kamimura E., Azuma T., Kansaku N., Uetake K.& Tanaka T.. 2010Effect of broody hens on behaviour of chicks. Appl. Anim. Behav. Sci. 126, 125–133.doi:10.1016/j.applanim.2010.06.011 (doi:10.1016/j.applanim.2010.06.011). CrossrefGoogle Scholar
    • 14
      Nicol C. J.& Pope S. J.. 1996The maternal feeding display of domestic hens is sensitive to perceived chick error. Anim. Behav. 52, 767–774.doi:10.1006/anbe.1996.0221 (doi:10.1006/anbe.1996.0221). CrossrefGoogle Scholar
    • 15
      Lowe J. C., Abeyesinghe S. M., Demmers T. G. M., Wathes C. M.& McKeegan D. E. F.. 2007A novel telemetric logging system for recording physiological signals in unrestrained animals. Comput. Electron. Agric. 57, 74–79.doi:10.1016/j.compag.2007.02.003 (doi:10.1016/j.compag.2007.02.003). CrossrefGoogle Scholar
    • 16
      Nicol C. J., Caplen G., Edgar J.& Browne W. J.. 2009Associations between welfare indicators and environmental choice in laying hens. Anim. Behav. 78, 413–424.doi:10.1016/j.anbehav.2009.05.016 (doi:10.1016/j.anbehav.2009.05.016). CrossrefGoogle Scholar
    • 17
      Collias N.& Joos M.. 1953The spectrographic analysis of sound signals of the domestic fowl. Behaviour 5, 175–188.doi:10.1163/156853953X00104 (doi:10.1163/156853953X00104). CrossrefGoogle Scholar
    • 18
      Schaefer A. L., Stewart M., Webster J. R., Cook N. J., Colyn J. J., Lepage P., Church J. S.& Haley D. B.. 2006Objective measurement of pain and fear in cattle using infrared thermography. In Proc. of the Int. Society of Applied Ethology, North American Regional Meeting, Vancouver, Canada. Wageningen, The Netherlands: Wageningen Academic Publishers. Google Scholar
    • 19
      Cabanac M.& Aizawa S.. 2000Fever and tachycardia in a bird (Gallus domesticus) after simple handling. Physiol. Behav. 69, 541–545.doi:10.1016/S0031-9384(00)00227-4 (doi:10.1016/S0031-9384(00)00227-4). Crossref, PubMedGoogle Scholar
    • 20
      Reefmann N., Wechsler B.& Gygax L.. 2009Behavioural and physiological assessment of positive and negative emotion in sheep. Anim. Behav. 78, 651–659.doi:10.1016/j.anbehav.2009.06.015 (doi:10.1016/j.anbehav.2009.06.015). CrossrefGoogle Scholar
    • 21
      Campler M., Jongren M.& Jensen P.. 2009Fearfulness in red junglefowl and domesticated white leghorn chickens. Behav. Process. 81, 39–43.doi:10.1016/j.beproc.2008.12.018 (doi:10.1016/j.beproc.2008.12.018). Crossref, PubMedGoogle Scholar
    • 22
      Fortomaris P., Arsenos G., Tserveni-Gousi A.& Yannakopoulos A.. 2007Performance and behaviour of broiler chickens as affected by the housing system. Arch. Geflugelkd 71, 97–104. Google Scholar
    • 23
      Pohle K.& Cheng H. W.. 2009Furnished cage system and hen well-being: comparative effects of furnished cages and battery cages on behavioral exhibitions in White Leghorn chickens. Poult. Sci. 88, 1559–1564.doi:10.3382/ps.2009-00045 (doi:10.3382/ps.2009-00045). Crossref, PubMedGoogle Scholar
    • 24
      Bouwknecht J. A., Olivier B.& Paylor R. E.. 2007The stress-induced hyperthermia paradigm as a physiological animal model for anxiety: a review of pharmacological and genetic studies in the mouse. Neurosci. Biobehav. Rev. 31, 41–59.doi:10.1016/j.neubiorev.2006.02.002 (doi:10.1016/j.neubiorev.2006.02.002). Crossref, PubMedGoogle Scholar
    • 25
      Bakken M., Moe R. O., Smith A. J.& Selle G. M. E.. 1999Effects of environmental stressors on deep body temperature and activity levels in silver fox vixens (Vulpes vulpes). Appl. Anim. Behav. Sci. 64, 141–151.doi:10.1016/S0168-1591(99)00022-2 (doi:10.1016/S0168-1591(99)00022-2). CrossrefGoogle Scholar
    • 26
      Busnardo C., Tavares R. F., Resstel L. B. M., Elias L. L. K.& Correa F. M. A.. 2010Paraventricular nucleus modulates autonomic and neuroendocrine responses to acute restraint stress in rats. Auton. Neurosci. 158, 51–57.doi:10.1016/j.autneu.2010.06.003 (doi:10.1016/j.autneu.2010.06.003). Crossref, PubMedGoogle Scholar
    • 27
      Lowe T. E., Cook C. J., Ingram J. R.& Harris P. J.. 2005Changes in ear-pinna temperature as a useful measure of stress in sheep (Ovis aries). Anim. Welf. 14, 35–42. Google Scholar
    • 28
      Field S. E., Rickard N. S., Toukhsati S. R.& Gibbs M. E.. 2007Maternal hen calls modulate memory formation in the day-old chick: the role of noradretialine. Neurobiol. Learn Mem. 88, 321–330.doi:10.1016/j.nim.2007.04.001 (doi:10.1016/j.nim.2007.04.001). Crossref, PubMedGoogle Scholar
    • 29
      Collias N. E.. 1987The vocal repertoire of the red junglefowl—a spectrographic classification and the code of communication. Condor 89, 510–524.doi:10.2307/1368641 (doi:10.2307/1368641). CrossrefGoogle Scholar
    • 30
      Rolls E. T.. 2005Emotion explained. Oxford, UK: Oxford University Press. (doi:10.1093/acprof:oso/9780198570035.001.0001). CrossrefGoogle Scholar
    • 31
      Mendl M., Burman O. H. P.& Paul E. S.. 2010An integrative and functional framework for the study of animal emotion and mood. Proc. R. Soc. B 277, 2895–2904.doi:10.1098/rspb.2010.0303 (doi:10.1098/rspb.2010.0303). LinkGoogle Scholar
    • 32
      Berridge K. C.& Winkielman P.. 2003What is an unconscious emotion? (The case for unconscious ‘liking’). Cogn. Emotion 17, 181–211.doi:10.1080/02699930244000273 (doi:10.1080/02699930244000273). Crossref, PubMedGoogle Scholar