Abstract
We report a range of lateralized coping strategies adopted by large social groups of cattle in response to mild challenges posed by humans of varying degrees of familiarity. At either 14 or 18 pens at a commercial feedlot, with 90 to 200 cattle in each, we conducted a series of video recorded ‘pressure tests’. ‘Frontal’ pressure tests involved walking from a position perpendicular to the concrete feed bunk of a given pen, towards the geometric centre of the line of feeding cattle. ‘Bunk-side’ pressure tests involved experimenters walking closely past a pen of feeding cattle in one direction, before returning in the opposite direction shortly afterwards. Experimenters wore white dust masks to alter their facial features in the bunk-side pressure tests. In both frontal and bunk-side pressure tests, distance from the experimenter influenced cattle’s choice of binocular viewing, cessation of feeding, standing or stepping backwards to monitor the approach and leaving the feed bunk. The frequency of these coping strategies differed in a lateralized manner. The cattle were more likely to accept the close positioning of a generally familiar, unmasked human on their left, which is traditionally referred to as the “near” side. By contrast, when responding to the approach of an unfamiliar, masked human, cattle conformed to the general vertebrate model and were more likely to remove themselves from the potential threat viewed within the left and not right visual field. We argue that the traditional terms for livestock sidedness as “near” (left) and “off” (right) sides demonstrate a knowledge of behavioural lateralization in domestic livestock that has existed for over 300 years of stock handling.
Similar content being viewed by others
References
Austin NP, Rogers LJ (2007) Asymmetry of flight and escape turning responses in horses. Laterality 12:464–474. https://doi.org/10.1080/13576500701495307
Austin NP, Rogers LJ (2012) Limb preferences and lateralization of aggression, reactivity and vigilance in feral horses, Equus caballus. Anim Behav 83:239–247. https://doi.org/10.1016/j.anbehav.2011.10.033
Austin NP, Rogers LJ (2014) Lateralization of agonistic and vigilance responses in Przewalski horses (Equus przewalskii). Appl Anim Behav Sci 151:43–50. https://doi.org/10.1016/j.applanim.2013.11.011
Bauer RH (1993) Lateralization of neural control for vocalization by the frog (Rana pipiens). Psychobiol 21:243–248. https://doi.org/10.3758/BF03327141
Bisazza A, Cantalupo C, Capocchiano M, Vallortigara G (2000) Population lateralisation and social behaviour: a study with 16 species of fish. Laterality 5:269–284. https://doi.org/10.1080/713754381
Boissy A, Erhard HW (2014) Chap. 3—How studying interactions between animal emotions, cognition, and personality can contribute to improve farm animal welfare. In: Grandin T, Deesing MJ (eds) Genetics and the behavior of domestic animals, 2nd edn. Academic Press, San Diego, pp 81–113
Boissy A, Manteuffel G, Jensen MB et al (2007) Assessment of positive emotions in animals to improve their welfare. Physiol Behav 92:375–397. https://doi.org/10.1016/j.physbeh.2007.02.003
Broom DM (2011) Advances in studies of behaviour and welfare in relation to animal production. Rev Bras Zootec 40:15–25
Cerqueira JJ, Almeida OFX, Sousa N (2008) The stressed prefrontal cortex. Left? Right! Brain Behav Immun 22:630–638. https://doi.org/10.1016/j.bbi.2008.01.005
Espmark Y, Kinderås K (2002) Behavioural lateralisation in reindeer. Rangifer 22:51–59. https://doi.org/10.7557/2.22.1.687
Farmer K, Krueger K, Byrne RW (2010) Visual laterality in the domestic horse (Equus caballus) interacting with humans. Anim Cogn 13:229–238. https://doi.org/10.1007/s10071-009-0260-x
Galin D (1974) Implications for psychiatry of left and right cerebral specialization: a neurophysiological context for unconscious processes. Arch Gen Psychiatry 31:572–583. https://doi.org/10.1001/archpsyc.1974.01760160110022
Gerendai I (1987) Laterality in the neuroendocrine system. In: Ottoson D (ed) Duality and unity of the brain. Springer US, New York, pp 17–28
Ghirlanda S, Vallortigara G (2004) The evolution of brain lateralization: a game-theoretical analysis of population structure. Proc Biol Sci 271:853–857
Ghirlanda S, Frasnelli E, Vallortigara G (2009) Intraspecific competition and coordination in the evolution of lateralization. Philos Trans R Soc Lond B Biol Sci 364:861–866. https://doi.org/10.1098/rstb.2008.0227
Gibbs ME, Andrew RJ, Ng KT (2003) Hemispheric lateralization of memory stages for discriminated avoidance learning in the chick. Behav Brain Res 139:157–165. https://doi.org/10.1016/S0166-4328(02)00245-0
Grandin T (2015) Chap. 5—How to improve livestock handling and reduce stress. In: Grandin T (ed) Improving Animal Welfare: A Practical Approach, 2nd edn. CABI, Wallingford, pp 69–95
Grandin T, Shivley C (2015) How farm animals react and perceive stressful situations such as handling, restraint, and transport. Animals 5:1233–1251. https://doi.org/10.3390/ani5040409
Grandin T, Oldfield JE, Boyd LJ (1998) Review: reducing handling stress improves both productivity and welfare. Prof Anim Sci 14:1–10. https://doi.org/10.15232/S1080-7446(15)31783-6
Hamp E (2001) A Rule of the road. Gen Linguist 41:147–158
Koboroff A, Kaplan G, Rogers LJ (2008) Hemispheric specialization in australian magpies (Gymnorhina tibicen) shown as eye preferences during response to a predator. Brain Res Bull 76:304–306. https://doi.org/10.1016/j.brainresbull.2008.02.015
Kovács L, Kézér FL, Bakony M, Hufnágel L, Tőzsér J, Jurkovich V (2015) Associations between heart rate variability parameters and housing- and individual-related variables in dairy cows using canonical correspondence analysis. PLoS One 10:e0145313. https://doi.org/10.1371/journal.pone.0145313
Leliveld LM, Langbein J, Puppe B (2013) The emergence of emotional lateralization: evidence in non-human vertebrates and implications for farm animals. Appl Anim Behav Sci 145:1–14
McGinley JJ, Friedman BH (2015) Autonomic responses to lateralized cold pressor and facial cooling tasks. Psychophysiology 52:416–424. https://doi.org/10.1111/psyp.12332
Morgante M, Vallortigara G (2009) Animal welfare: neuro-cognitive approaches. Ital J Anim Sci 8 supp1:255–264
Neveu PJ (2002) Cerebral lateralization and the immune system. Int Rev Neurobiol 52:303–323
Nottebohm F (1971) Neural lateralization of vocal control in a passerine bird. I. Song. J Exp Zool 177:229–261. https://doi.org/10.1002/jez.1401770210
OED Online (2017a) Online Oxford University Press, nearside, n. and adj. http://www.oed.com/view/Entry/255739. Accessed 24 Mar 2017
OED Online (2017b)Online Oxford University Press, offside, n. and adj. http://www.oed.com/view/Entry/238817. Accessed 24 Mar 2017
Proudfoot KL, Weary DM, von Keyserlingk MAG (2012) Linking the social environment to illness in farm animals. Appl Anim Behav Sci 138:203–215. https://doi.org/10.1016/j.applanim.2012.02.008
Rizhova LY, Kokorina EP (2005) Behavioural asymmetry is involved in regulation of autonomic processes: left side presentation of food improves reproduction and lactation in cows. Behav Brain Res 161:75–81. https://doi.org/10.1016/j.bbr.2005.01.007
Robins A, Phillips C (2010) Lateralised visual processing in domestic cattle herds responding to novel and familiar stimuli. Laterality 15:514–534. https://doi.org/10.1080/13576500903049324
Robins A, Rogers LJ (2006) Complementary and lateralized forms of processing in Bufo marinus for novel and familiar prey. Neurobiol Learn Mem 86:214–227
Robins A, Chen P, Beazley LD, Dunlop SA (2005) Lateralized predatory responses in the ornate dragon lizard (Ctenophorus ornatus). Neuroreport 16:849–852
Rogers LJ (1989) Laterality in animals. Int J Comp Psychol 3:5–25
Rogers LJ (2000) Evolution of hemispheric specialization: advantages and disadvantages. Brain Lang 73:236–253. https://doi.org/10.1006/brln.2000.2305
Rogers LJ (2002) Lateralization in vertebrates: Its early evolution, general pattern, and development. In: Slater PJB, Charles JSR, Snowdon T, Roper TJ (eds) Advances in the study of behavior. Academic Press, New York, pp 107–161
Rogers LJ (2010) Relevance of brain and behavioural lateralization to animal welfare. Appl Anim Behav Sci 127:1–11
Rogers LJ, Andrew R (2002) Comparative vertebrate lateralization. Cambridge University Press, Cambridge
Rogers LJ, Zucca P, Vallortigara G (2004) Advantages of having a lateralized brain. Proc R Soc Lond B Biol Sci 271:S420–S422. https://doi.org/10.1098/rsbl.2004.0200
Smith AV, Proops L, Grounds K, Wathan J, McComb (2016) Functionally relevant responses to human facial expressions of emotion in the domestic horse (Equus caballus). Biol Lett 12:20150907. https://doi.org/10.1098/rsbl.2015.0907
Sutherland MA, Rogers AR, Verkerk GA (2012) The effect of temperament and responsiveness towards humans on the behavior, physiology and milk production of multi-parous dairy cows in a familiar and novel milking environment. Physiol Behav 107:329–337. https://doi.org/10.1016/j.physbeh.2012.07.013
Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–589. https://doi.org/10.1017/S0140525X05000105
Voisinet BD, Grandin T, Tatum JD (1997) Feedlot cattle with calm temperaments have higher average daily gains than cattle with excitable temperaments. J Anim Sci 75:892–896
Wittling W (1997) Brain asymmetry and autonomic control of the heart. Eur Psychol 2:313–327
Wrona D (2006) Neural–immune interactions: an integrative view of the bidirectional relationship between the brain and immune systems. J Neuroimmunol 172:38–58. https://doi.org/10.1016/j.jneuroim.2005.10.017
Acknowledgements
The authors thank the managerial staff of Freestone Feedlot, Warwick, Queensland, for their support and permission to conduct the observational research reported in this study. The constructive criticism from anonymous reviewers has also been invaluable to the production of this work.
Funding
The study was funded by a Rosalind Dixon Memorial Scholarship for Farm Animal Welfare Research from the Humane Society International (HSI) and University of Queensland Centre for Animal Welfare and Ethics (CAWE).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest associated with the publication of this research.
Ethics
The observational research complied with ethical standards of the Australian Code for the Care and Use of Animals for Scientific Purposes 8th edition (2013).
Rights and permissions
About this article
Cite this article
Robins, A., Goma, A.A., Ouine, L. et al. The eyes have it: lateralized coping strategies in cattle herds responding to human approach. Anim Cogn 21, 685–702 (2018). https://doi.org/10.1007/s10071-018-1203-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-018-1203-1