Skip to main content Accessibility help

Understanding oral stereotypies in calves: alternative strategies, hypothalamic–pituitary–adrenal axis (re)activity and gene by environment interactions

  • L. E Webb (a1), C. G van Reenen (a1) (a2), B Engel (a3), H Berends (a4), W. J. J Gerrits (a5) and E. A. M Bokkers (a1)...


Stereotypies are used as indicators of poor animal welfare and it is, therefore, important to understand underlying factors mediating their development. In calves, two oral stereotypies, that is, tongue playing and object manipulation, result mostly from insufficient structure in the diet. Three hypotheses were studied: (1) oral stereotypies in calves are one of two alternative strategies, the alternative being hypo-activity; (2) stereotyping and non-stereotyping calves differ in terms of cortisol secretion; (3) oral stereotypy development in calves rests on a gene by environment interaction. Eight-week-old bull calves (n=48) were assigned to one of four solid feed allowances (0, 9, 18 or 27 g dry matter/kg metabolic weight per day) with the following composition: 50% concentrate, 25% maize silage and 25% straw on dry matter basis. The calves received milk replacer in buckets, the provision of which was adjusted to achieve equal growth rates. At 14 to 18 weeks of age, calves were exposed to a challenge, that is, tethering inside cages. Oral stereotypies and inactivity were recorded in the home pens in the 4 weeks before the challenge using instantaneous scan sampling. Salivary cortisol levels were measured at −120, +40, +80, +120 min and +48 h relative to the challenge. Individual differences in behaviour were recorded in the first 30 min after challenge implementation using focal animal sampling and continuous recording, and these elements were entered into a principal component (PC) analysis to extract PCs. Regression analyses were performed to find relationships between stereotypies and inactivity, stereotypies and cortisol, and stereotypies and PCs (individual differences, genes) and solid feed (environment). Relationships between PCs and cortisol were also investigated to help with the interpretation of PCs. Hypotheses 1 and 2 were rejected. Hypothesis 3, however, was supported: calves with a zero solid feed allowance, that is, in the most barren environment, showed links between stereotypies and two of the PCs. Calves that displayed high levels of idle and rapid locomotion and low levels of oral contact with the cage during the challenge also displayed high levels of object manipulation in the home pens. Calves that displayed low levels of stepping and turning attempts during the challenge also displayed high levels of tongue playing in the home pens. This study corroborates the gene by environment interaction on the development of oral stereotypies in calves.


Corresponding author



Hide All
Andersen, IL, Boe, KE, Foerevik, G, Janczak, AM and Bakken, M 2000. Behavioural evaluation of methods for assessing fear responses in weaned pigs. Applied Animal Behaviour Science 69, 227240.
Berends, H, van den Borne, JJGC, Alferink, SJJ, van Reenen, CG, Bokkers, EAM and Gerrits, WJJ 2012. Low-protein solid feed improves the utilization of milk replacer for protein gain in veal calves. Journal of Dairy Science 95, 66546664.
Bergeron, R, Badnell-Waters, AJ, Lambton, S and Mason, G 2006. Stereotypic oral behaviour in captive ungulates: foraging, diet and gastrointestinal function. In Stereotypic animal behaviour. Fundamentals and applications to welfare (ed. G Mason and J Rushen), pp. 1957. CAB International, Wallingford, UK.
Cabib, S 2006. The neurobiology of stereotypy II: the role of stress. In Stereotypic animal behaviour. Fundamentals and applications to welfare (ed. G Mason and J Rushen), pp. 227255. CAB International, Wallingford, UK.
Cronin, GM 1985. The development and significance of abnormal stereotyped behaviours in tethered sows. Agricultural University of Wageningen, Wageningen, The Netherlands.
Freymond, SB, Bardou, D, Briefer, EF, Bruckmaier, R, Fouche, N, Fleury, J, Maigrot, AL, Ramseyer, A, Zuberbuhler, K and Bachmann, I 2015. The physiological consequences of crib-biting in horses in response to an ACTH challenge test. Physiology & Behavior 151, 121128.
Friend, TH, Dellmeier, GR and Gbur, EE 1985. Comparison of four methods of calf confinement. 1. Physiology. Journal of Animal Science 60, 10951101.
Fureix, C, Walker, M, Harper, L, Reynolds, K, Saldivia-Woo, A and Mason, G 2016. Stereotypic behaviour in standard non-enriched cages is an alternative to depression-like responses in C57BL/6 mice. Behavioural Brain Research 305, 186190.
Gabriels, RL, Agnew, JA, Pan, ZX, Holt, KD, Reynolds, A and Laudenslager, ML 2013. Elevated repetitive behaviors are associated with lower diurnal salivary cortisol levels in autism spectrum disorder. Biological Psychology 93, 262268.
Gottlieb, DH, Capitanio, JP and McCowan, B 2013. Risk factors for stereotypic behavior and self-biting in rhesus macaques (Macaca mulatta): animal’s history, current environment, and personality. American Journal of Primatology 75, 9951008.
Ijichi, CL, Collins, LM and Elwood, RW 2013. Evidence for the role of personality in stereotypy predisposition. Animal Behaviour 85, 11451151.
Jensen, KH, Pedersen, LJ, Nielsen, EK, Heller, KE, Ladewig, J and Jorgensen, E 1996. Intermittent stress in pigs: effects on behavior, pituitary-adrenocortical axis, growth, and gastric ulceration. Physiology & Behavior 59, 741748.
Kenward, MG and Roger, JH 1997. Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53, 983997.
Mason, GJ 1991. Stereotypies and suffering. Behavioural Processes 25, 103115.
Mason, GJ and Latham, NR 2004. Can’t stop, won’t stop: is stereotypy a reliable animal welfare indicator? Animal Welfare 13, S57S69.
McBride, SD and Cuddeford, D 2001. The putative welfare-reducing effects of preventing equine stereotypic behaviour. Animal Welfare 10, 173189.
Meagher, RK, Campbell, DL, Dallaire, JA, Díez-León, M, Palme, R and Mason, GJ 2013. Sleeping tight or hiding in fright? The welfare implications of different subtypes of inactivity in mink. Applied Animal Behaviour Science 144, 138146.
Miller, GE, Chen, E and Zhou, ES 2007. If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychological Bulletin 133, 2545.
Morisse, JP, Cotte, JP, Huonnic, D and Martrenchar, A 1999. Influence of dry feed supplements on different parameters of welfare in veal calves. Animal Welfare 8, 4352.
Mormède, P, Andanson, S, Auperin, B, Beerda, B, Guemene, D, Malmkvist, J, Manteca, X, Manteuffel, G, Prunet, P, van Reenen, CG, Richard, S and Veissier, I 2007. Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiology & Behavior 92, 317339.
Nagy, K, Bodo, G, Bardos, G, Banszky, N and Kabai, P 2010. Differences in temperament traits between crib-biting and control horses. Applied Animal Behaviour Science 122, 4147.
Negrâo, JA, Porcinato, MA, De Passillé, AM and Rushen, J 2004. Cortisol in saliva and plasma of cattle after ACTH administration and milking. Journal of Dairy Science 87, 17131718.
Redbo, I 1998. Relations between oral stereotypies, open-field behavior, and pituitary-adrenal system in growing dairy cattle. Physiology & Behavior 64, 273278.
Reimert, I, Bolhuis, JE, Kemp, B and Rodenburg, TB 2013. Indicators of positive and negative emotions and emotional contagion in pigs. Physiology & Behavior 109, 4250.
Schouten, WGP and Wiepkema, PR 1991. Coping styles of tethered sows. Behavioural Processes 25, 125132.
Ursin, H and Eriksen, HR 2004. The cognitive activation theory of stress. Psychoneuroendocrinology 29, 567592.
van Reenen, CG, Engel, B and Ruis-Heutinck, LFM 2004. Behavioural reactivity of heifer calves in potentially alarming test situations: a multivariate and correlational analysis. Applied Animal Behaviour Science 85, 1130.
Webb, LE, Bokkers, EAM, Engel, B, Berends, H, Gerrits, WJJ and van Reenen, CG 2012. Behaviour and welfare of veal calves fed different amounts of solid feed supplemented to a milk replacer ration adjusted for similar growth. Applied Animal Behaviour Science 136, 108116.
Webb, LE, van Reenen, CG, Berends, H, Engel, B, de Boer, IJM, Gerrits, WJJ and Bokkers, EAM 2015. The role of solid feed amount and composition and of milk replacer supply in veal calf welfare. Journal of Dairy Science 98, 54675481.
Wiepkema, PR 1987. Developmental aspects of motivated behavior in domestic animals. Journal of Animal Science 65, 12201227.
Würbel, H, Bergeron, R and Cabib, S 2006. The coping hypothesis of stereotypic behaviour. In Stereotypic animal behaviour. Fundamentals and applications to welfare (ed. G Mason and J Rushen), pp. 1415. CAB International, Wallingford, UK.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 1751-7311
  • EISSN: 1751-732X
  • URL: /core/journals/animal
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed