Hostname: page-component-76fb5796d-wq484 Total loading time: 0 Render date: 2024-04-25T14:50:42.770Z Has data issue: false hasContentIssue false

Can't stop, won't stop: is stereotypy a reliable animal welfare indicator?

Published online by Cambridge University Press:  11 January 2023

GJ Mason*
Affiliation:
Department of Zoology, Oxford University, South Parks Road, Oxford OXI 3PS, UK
NR Latham
Affiliation:
Department of Zoology, Oxford University, South Parks Road, Oxford OXI 3PS, UK
*
* Contact for correspondence and requests for reprints: Georgia.Mason@zoo.ox.ac.uk

Abstract

We estimate that stereotypies are currently displayed by over 85 million farm, laboratory and zoo animals worldwide. This paper investigates their reliability as welfare indicators, by surveying studies relating stereotypy to other welfare measures and by analysing the mechanisms underlying this behaviour. Where data exist, most (approximately 68%) situations that cause/increase stereotypies also decrease welfare. Stereotypy-eliciting situations are thus likely to be poor for welfare, although exceptions exist. Within such an environment, however, most (approximately 60%) accounts link individual stereotypy performance with improved welfare (cf approximately 20% linking it with reduced welfare). Thus, in a sub-optimal environment, non-stereotyping or low-stereotyping individuals could well have the poorest welfare, although again exceptions exist. Examining the mechanisms underlying stereotypy performance, we discuss four processes that could account for these complex links between stereotypy and welfare. Beneficial consequences from performing the specific source-behaviour of the stereotypy (‘do-it-yourself enrichment’), or arising from repetition per se (‘mantra effects’), may ameliorate welfare in poor environments. In addition, stereotypies that have become centrally controlled (habit-like), or that arise from autistic-like changes in the control of all behaviour (perseveration), are likely to be unreliable indicators of current state because they can be elicited by, or persist in, circumstances that improve welfare. To refine the role of stereotypy in welfare assessment, we suggest the collection of specific additional data to reveal when any of these four processes is acting. Until such research increases our understanding, stereotypies should always be taken seriously as a warning sign of potential suffering, but never used as the sole index of welfare; non-stereotyping or low-stereotyping individuals should not be overlooked or assumed to be faring well; simple measures of frequency should not be used to compare stereotypies that differ in age, form, or the biological or experiential characteristics of the performing animal; enrichments that do not immediately reduce stereotypies should not be assumed failures with respect to welfare; and finally, stereotypies should not be reduced by means other than tackling their underlying motivations.

Type
Research Article
Copyright
© 2004 Universities Federation for Animal Welfare

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ames, A 1994 The Welfare and Management of Bears in Zoological Gardens. UFAW Animal Welfare Research Report No. 7. Universities Federation for Animal Welfare: Wheathampstead, Herts, UKGoogle Scholar
Appleby, M 1999 What Should We Do About Animal Welfare? Blackwell Science: Oxford, UKGoogle Scholar
Archer, J 1979 Behavioural aspects of fear. In: Sluckin, W (ed) Fear in Animals and Man pp 5685. Van Nostrand Reinhold: New York, USAGoogle Scholar
Bashaw, M, Tarou, L, Maki, T and Maple, T 2001 A survey assessment of variables related to stereotypy in captive giraffe and okapi. Applied Animal Behaviour Science 73: 235247CrossRefGoogle ScholarPubMed
Beauchamp, A and Gluck, J 1988 Associative processes in differentially reared monkeys (Macaca mulatta): sensory preconditioning. Developmental Psychobiology 21: 355364CrossRefGoogle ScholarPubMed
Benus, R, den Daas, S, Koolhaas, J and van Oortmerssen, G 1990 Routine formation and flexibility in social and non-social behaviour of aggressive and non-aggressive mice. Behaviour 112: 176193Google Scholar
Benus, R, Koolhaas, J and van Oortmerssen, G 1987 Individual differences in behavioural reaction to a changing environment in mice and rats. Behaviour 100: 105122Google Scholar
Bernardi, L, Sleight, P, Bandinelli, G, Cencetti, S, Fattorini, L, Wdowczyc-Szulc, J and Lagi, A 2001 Effect of rosary prayer and yoga mantras on autonomic cardiovascular rhythms: comparative study. British Medical Journal 323: 14461449CrossRefGoogle ScholarPubMed
Bildsøe, M, Heller, K and Jeppesen, L 1991 Effects of immobility stress and food restriction on stereotypies in low and high stereotyping female ranch mink. Behavioural Processes 25: 179189CrossRefGoogle ScholarPubMed
Broom, D 1983 Stereotypies as animal welfare indicators. In: Schmidt, D (ed) Indicators Relevant to Farm Animal Welfare pp 8187. Martinus Nijhoff: The Hague, The NetherlandsCrossRefGoogle Scholar
Broom, D 1986 Responsiveness of stall-housed sows. Applied Animal Behaviour Science 15: 186CrossRefGoogle Scholar
Broom, D 1991 Animal welfare: concepts and measurement. Journal of Animal Science 69: 41674175CrossRefGoogle ScholarPubMed
Broom, D and Johnson, K 1993 Stress and Animal Welfare. Chapman and Hall: London, UKCrossRefGoogle Scholar
Broom, D and Potter, M 1984 Factors affecting the occurrence of stereotypies in stall-housed dry sows. In: Unshelm, J, van Putten, G and Zeeb, K (eds) Proceedings of the International Congress on Applied Ethology of Farm Animals pp 229231. KTBL: Darmstadt, GermanyGoogle Scholar
Brouckaert, K, Steenhaut, M, Martens, A, Vlaminck, L, Pille, F, Arnaerts, L and Gasthuys, F 2002 Resultaten na operatieve behandeling van luchtzuigen bij het paard: een retrospectieve studie (1990-2000). Vlaams Diergeneeskundig Tijdschrift 71: 249255. [Title translation: Wind-sucking in the horse, results of surgical treatment: a retrospective study (1990-2000)]Google Scholar
Bumin, G, Uyanik, M, Kayihan, H, Duger, T and Topcu, M 2002 The effect of hand splints on stereotypic behavior in Rett's syndrome. Turkish Journal of Pediatrics 44: 2529Google ScholarPubMed
Canali, E, Ferrante, V, Mattiello, S, Gottardo, F and Verga, M 2001 Are oral stereotypies and abomasal lesions correlated in veal calves? In: Garner, J P, Mench, J A and Heekin, S P (eds) Proceedings of the 35th Congress of the International Society for Applied Ethology p 103 (Abstract). Center for Animal Welfare at UC Davis: California, USAGoogle Scholar
Clubb, R E 2001 The roles of foraging niche, rearing condition and current husbandry on the development of stereotypies in carnivores. PhD thesis, University of Oxford, UK.Google Scholar
Clubb, R and Mason, G 2002 A Review of the Welfare of Elephants in European Zoos. Royal Society for the Prevention of Cruelty to Animals: Horsham, UK. Available at: http://www.rspca.org.uk/servlet/ContentServer?pagename=RSPCACampaigns/Elephants/FactsAndReports&articleid=1024473728261Google Scholar
Cooper, J J, McDonald, L and Mills, D S 2000 The effects of increasing visual horizons on stereotypic weaving: implications for the social housing of stabled horses. Applied Animal Behaviour Science 69: 6783CrossRefGoogle ScholarPubMed
Cooper, J, Ödberg, F and Nicol, C 1996 Limitations of the effectiveness of environmental improvement in reducing stereotypic behaviour in bank voles (Clethrionomys glareolus). Applied Animal Behaviour Science 48: 237248CrossRefGoogle Scholar
Cosyns, P and Ödberg, F 2000 Obsessive compulsive disorders: clinical hallmarks and animal models. Neuroscience Research Communications 26: 3013123.0.CO;2-4>CrossRefGoogle Scholar
Country Supplies 2003 Cribbing and Weaving Aids. Available at: http://www.countrysupplies.com/dept.asp?dept%SFid=388.Google Scholar
Dana 2001 Dana's View from the Inside. Available at: http://www.danasview.net.Google Scholar
Dantzer, R 1986 Behavioural, physiological and functional aspects of stereotyped behaviour: a review and reinterpretation. Journal of Animal Science 62: 17761786CrossRefGoogle ScholarPubMed
Dawkins, M S 1990 From an animal's point of view: motivation, fitness and animal welfare. Behavioral and Brain Sciences 13: 161CrossRefGoogle Scholar
de Jonge, G, Carlstead, K and Wiepkema, P 1986 The Welfare of Ranch Mink. (Translated from Dutch). The Centre for Poultry Research and Extension (COVP) Issue No. 8. The Spelderholt Institute: Beekbergen, The NetherlandsGoogle Scholar
Delacalle, J, Burba, D J, Tetens, J and Moore, R M 2002 YAG laser-assisted modified Forsell's procedure for treatment of cribbing (crib-biting) in horses. Veterinary Surgery 31: 111116Google Scholar
De Passille, A M B, Christopherson, R and Rushen, J 1993 Non-nutritive sucking by the calf and postprandial secretion of insulin, CCK and gastrin. Physiology and Behavior 54: 10691073CrossRefGoogle Scholar
Di Giovanni, M and Valente, M 2001 Trial and error — attempting to change the lives of socially and environmentally deprived primates. In: Hare, V J, Worley, K E and Myers, K (eds) Proceedings of the 4th International Conference on Environmental Enrichment. The Shape of Enrichment: San Diego, USAGoogle Scholar
Dollinger, P, Baumgartner, R, Pagan, O and Wechsler, B 1996 Husbandry and pathology of Polar bears (Thalarctos maritimus) in Swiss zoos. Proceedings of the European Association of Zoo and Wildlife Veterinarians (EAZWV) First Scientific Meeting, May 16-18, Rostock, Germany. Available at: http://www.bvet.admin.ch/artenschutz/d/berichte_publikat/vortraege/polar_bears/rostock96.html.Google Scholar
Eaton, G G, Kelley, S T, Axthelm, M K, lliffsizemore, S A and Shiigi, S M 1994 Psychological well-being in paired adult female rhesus (Macaca mulatta). American Journal of Primatology 33: 8999CrossRefGoogle ScholarPubMed
EC 1996 Report of the Scientific Veterinary Committee Animal Welfare Section on the Welfare of Laying Hens. Commission of the European Communities: Brussels, BelgiumGoogle Scholar
EC 1997 The Welfare of Intensively Kept Pigs — Report of the Scientific Committee on Animal Health and Animal Welfare. Commission of the European Communities: Brussels, BelgiumGoogle Scholar
EC 1999 Commission of the European Communities Second Report on the Number of Animals used for Experimental and Other Scientific Purposes. Commission of the European Communities: Brussels, BelgiumGoogle Scholar
EC 2000 The Welfare of Chickens Kept for Meat Production (Broilers) — Report of the Scientific Committee on Animal Health and Animal Welfare. Commission of the European Communities: Brussels, BelgiumGoogle Scholar
EC 2001 The Welfare of Animals Kept for Fur Production — Report of the Scientific Committee on Animal Health and Animal Welfare. Commission of the European Communities: Brussels, BelgiumGoogle Scholar
Fentress, J 1973 Specific and non-specific factors in the causation of behavior. In: Bateson, P and Hinde, R (eds) Perspectives in Ethology pp 155218. Cambridge University Press: Cambridge, UKCrossRefGoogle Scholar
Fentress, J 1976 Dynamic boundaries of patterned behaviour: interaction and self organisation. In: Bateson, P and Hinde, R (eds) Perspectives in Ethology pp 135169. Plenum Press: New York, USAGoogle Scholar
Fox, M 1984 Farm Animals: Husbandry, Behavior and Veterinary Practice. University Park Press: Baltimore, USAGoogle Scholar
Francis, D, Zaharia, M, Shanks, N and Anisman, H 1995 Stress-induced disturbances in Morris water maze performance — interstrain variability. Physiology and Behavior 58: 5765CrossRefGoogle ScholarPubMed
Frith, C and Done, D J 1983 Stereotyped responding by schizophrenic patients on a two-choice guessing task. Psychological Medicine 13: 779786CrossRefGoogle ScholarPubMed
Frith, C D and Done, D J 1990 Stereotyped behaviour in madness and in health. In: Cooper, S J and Dourish, C T (eds) Neurobiology of Stereotyped Behaviour pp 232259. Clarendon Press: Oxford, UKGoogle Scholar
Frith, U 1970 Studies in pattern detection in normal and autistic children: 11. Reproduction and production of colour sequences. Journal of Experimental Child Psychology 10: 120135CrossRefGoogle Scholar
Frith, U 1972 Cognitive mechanisms in autism: experiments with colour and tone sequence production. Journal of Autism and Childhood Schizophrenia 2: 160173CrossRefGoogle ScholarPubMed
Garner, J P 1999 The Etiology of Stereotypy. PhD Thesis, Oxford University, UK.Google Scholar
Garner, J and Mason, G 2002 Evidence for a relationship between cage stereotypies and behavioural disinhibition in laboratory rodents. Behavioural Brain Research 136: 8392CrossRefGoogle ScholarPubMed
Garner, J P, Mason, G J and Smith, R 2003 Stereotypic route-tracing in experimentally-caged songbirds correlates with general behavioural disinhibition. Animal Behaviour 66: 711727CrossRefGoogle Scholar
Gillberg, C 2003 On Autism. Available at: http://www.atlasindia.com/autismusa/autism.html.Google Scholar
Gluck, J and Sackett, G 1976 Extinction deficits in socially isolated rhesus monkeys (Macaca mulatta). Developmental Psychobiology 12: 173174Google Scholar
Grandin, T and Scariano, M 1986 Emergence: Labelled Autistic. Arena Press: Novato, California, USAGoogle Scholar
Guess, D and Carr, E 1991 Emergence and maintenance of stereotypy and self-injury. American Journal on Mental Retardation 96: 299319Google ScholarPubMed
Handley, G 2001 Asperger's Syndrome From the Horse's Mouth. Available at: http://www.webspawner.com/users/asperger.Google Scholar
Haskell, M J, Mendl, M T, Lawrence, A B and Austin, E 2000 The effect of delayed feeding on the post-feeding behaviour of sows. Behavioural Processes 49: 8597CrossRefGoogle ScholarPubMed
Hicks, A L, Martin, K A, Ditor, D S, Latimer, A E, Craven, C, Bugaresti, J and McCartney, N 2003 Long-term exercise training in persons with spinal cord injury: effects on strength, arm ergometry performance and psychological well-being. Spinal Cord 41: 3443CrossRefGoogle ScholarPubMed
Hudson, A 1969 Perseveration. Brain 91: 571582CrossRefGoogle Scholar
Ironmonger, J 1992 The Good Zoo Guide. Harper and Collins: London, UKGoogle Scholar
Irven, P 1993 The decline of bears in British zoos. International Zoo News 40: 2528Google Scholar
Janowiak, J J and Hackman, R 1994 Meditation and college students’ self-actualization and rated stress. Psychological Reports 75: 10071010CrossRefGoogle ScholarPubMed
Jeppesen, L L and Falkenberg, H 1990 Effects of play balls on pelt-biting, behaviour and levels of stress in ranch mink. Scientifur 14: 179186Google Scholar
Kalen 2000 Dispelling Some Myths About Autism. Available at: http://www.nas.org.uk/peoplew/personal/kalen.html.Google Scholar
Kennes, D and Ödberg, F O 1987 Developmental study of the effect of haloperidol and naloxone on captivity-induced stereotypies. Applied Animal Behaviour Science 17: 379 (Abstract)CrossRefGoogle Scholar
Kohnke, J 2000 Aerophagia or Oral Windsucking’ in Horses. Available at: http://www.petalia.com.au/Templates/StoryTemplate_Process.cfm?Story_No=1305&specie=6.Google Scholar
Korhonen, H, Niemela, P and Jauhianinen, L 2001 Effect of space and floor material on the behaviour of farmed blue foxes. Canadian Journal of Animal Science 81: 189197CrossRefGoogle Scholar
Laidlow, R 2001 The State of the Ark: a Review of Conditions at the Granby Zoo, 2001. Available at: http://www.wspa.ca/reports/granbyzoo.html.Google Scholar
Lawrence, A B and Terlouw, E M C 1993 A review of behavioral factors involved in the development and continued performance of stereotypic behaviors in pigs. Journal of Animal Science 71: 28152825CrossRefGoogle ScholarPubMed
Lawrence, A and Rushen, J 1993 Stereotypic Animal Behaviour — Fundamentals and Applications to Welfare. CAB International: Wallingford, UKGoogle Scholar
Lee, M S, Bac, B H, Ryu, H, Sohn, J H, Kim, S Y and Chung, H T 1997 Changes in alpha wave and state anxiety during ChunDoSunBupQi-training in trainees with open eyes. American Journal of Chinese Medicine 25: 289299CrossRefGoogle ScholarPubMed
Loftin, A 2003 Survey of Autism. Available at: http://www.space-host.us/-aliki/autism/index.html.Google Scholar
Lopatto, D, Ogier, S, Wickelgren, E, Gibbens, C, Smith, A, Sullivan, L and Muns, M 1998 Cautiousness, stereotypy and variability in older and younger adults. Psychological Record 48: 571589CrossRefGoogle Scholar
Lourie, R S 1949 The role of rhythmic patterns in childhood. American Journal of Psychiatry 105: 653660CrossRefGoogle ScholarPubMed
Luria, A 1965 Two kinds of motor perseveration in massive injury of the frontal lobes. Brain 88: 110CrossRefGoogle ScholarPubMed
Martiniuk, R 1976 Information Processing in Motor Skills. Holt, Rinehart and Winston: New York, USAGoogle Scholar
Mason, G 1991a Stereotypies: a critical review. Animal Behaviour 41: 10151037CrossRefGoogle Scholar
Mason, G 1991b Stereotypies and suffering. Behavioural Processes 25: 103115CrossRefGoogle ScholarPubMed
Mason, G 1992 Individual variation in the stereotypies of caged mink. PhD thesis, University of Cambridge, UK.Google Scholar
Mason, G J 1993 Age and context affect the stereotypies of caged mink. Behaviour 127: 191229CrossRefGoogle Scholar
Mason, G and Mendl, M 1993 Why is there no simple way of measuring animal welfare? Animal Welfare 2: 301320Google Scholar
Mason, G and Turner, M 1993 Mechanisms involved in the development and control of stereotypies. In: Bateson, P (ed) Perspectives in Ethology 10 pp 5385. Plenum Press: New York, USAGoogle Scholar
McBride, S and Cuddeford, D 2001 The putative welfare-reducing effects of preventing equine stereotypic behaviour. Animal Welfare 10: 173189Google Scholar
McGreevy, P and Nicol, C 1998 Physiological and behavioral consequences associated with short-term prevention of crib-biting in horses. Physiology and Behavior 65: 1523CrossRefGoogle ScholarPubMed
Meehan, C L, Mench, J A and Garner, J P 2001 Environmental enrichment prevents the development of abnormal behaviors and modifies fear responses in young Orange-winged Amazon parrots. In: Garner, J P, Mench, J A and Heekin, S P (eds) Proceedings of the 35th International Congress of the International Society for Applied Ethology p 42 (Abstract). The Center for Animal Welfare at UC Davis: California, USAGoogle Scholar
Melman, S 1995 Use of Prozac in Animals for Selected Dermatological and Behavioral Conditions. Available at: http://www.dermapet.com/articles/art-06.html.Google Scholar
Meyer-Holzapfel, M 1968 Abnormal behaviour in zoo animals. In: Fox (ed) Abnormal Behaviour in Animals pp 476503. WB Saunders: Philadelphia, USAGoogle Scholar
Mills, A, Duncan, I, Slee, G and Clarke, J 1985b Heart rate and laying behaviour in two strains of domestic chicken. Physiology and Behavior 35: 145147CrossRefGoogle ScholarPubMed
Mills, A, Wood-Gush, D and Hughes, B 1985a Genetic analysis of strain differences in pre-laying behaviour in battery cages. British Poultry Science 26: 187197CrossRefGoogle ScholarPubMed
Milner, B 1963 Effects of different brain lesions on card sorting. Archives of Neurology 9: 90100CrossRefGoogle Scholar
Minero, M, Canali, E, Ferrant, M, Verga, M and Ödberg, F O 1999 Heart rate and behavioural responses of crib-biting horses to two acute stressors. Veterinary Record 145: 430433CrossRefGoogle ScholarPubMed
Murphy, M, Nevill, A, Neville, C, Biddle, S and Hardman, A 2002 Accumulating brisk walking for fitness, cardiovascular risk, and psychological health. Medicine and Science in Sports and Exercise 34: 14681474CrossRefGoogle ScholarPubMed
NAS (National Autistic Society) 2002 Living with Autism — Basic Guidelines for Parents and Carers Dealing with Children with Autistic Spectrum Disorder (ASD). Available at: http://www.nas.org.uk/family/parents/dealing.html.Google Scholar
Neral 2002 Stereotypy. Available at: http://users.telenet.be/neral/.Google Scholar
Nevison, C, Hurst, J and Barnard, C 1999a Why do male ICR (CD-I) mice perform bar-related (stereotypic) behaviour? Behavioural Processes 47: 95111CrossRefGoogle Scholar
Nevison, C, Hurst, J and Barnard, C 1999b Strain-specific effects of cage enrichment in male laboratory mice (Mus musculus). Animal Welfare 8: 361379Google Scholar
Nicol, C 2000 Equine stereotypies. In: Houpt, K (ed) Recent Advances in Companion Animal Behavior Problems. International Veterinary Information Service: Ithaca, New York, USA. Available at: http://www.ivis.org/advances/Behavior_Houpt/nicol/chapter_frm.asp?LA=IGoogle Scholar
Nicol, C J, Davidson, H P D, Harris, P A, Waters, A J and Wilson, A D 2002 Study of crib-biting and gastric inflammation and ulceration in young horses. Veterinary Record 151: 658660CrossRefGoogle ScholarPubMed
Novak, M A and Harlow, H F 1975 Social recovery of monkeys isolated for the first year of life: I. Rehabilitation and therapy. Developmental Psychology 11(4): 453465CrossRefGoogle Scholar
Ödberg, F 1978 Introduction to abnormal behaviours: stereotypies. Proceedings of the Ist World Congress on Ethology Applied to Zootechnics pp 475480. Industrias Graficas: Madrid, SpainGoogle Scholar
Pell, S M and McGreevy, P D 1999 A study of cortisol and beta-endorphin levels in stereotypic and normal Thoroughbreds. Applied Animal Behaviour Science 64: 8190CrossRefGoogle Scholar
Poulsen, E, Honeyman, V, Valentine, P and Teskey, G 1995 The successful treatment of a chronic stereotype in one polar bear using enrichment programming, enclosure redesign, and medical therapy. In: Holst, B (ed) Proceedings of the 2nd International Conference on Environmental Enrichment pp 209217. Copenhagen Zoo: Frederiksberg, DenmarkGoogle Scholar
Redbo, I 1992 The influence of restraint on the occurrence of oral stereotypies in dairy cows. Applied Animal Behaviour Science 35: 115123CrossRefGoogle Scholar
Redbo, I 1993 Stereotypies and cortisol secretion in heifers subjected to tethering. Applied Animal Behaviour Science 38: 213225CrossRefGoogle Scholar
Redbo, I 1998 Relations between oral stereotypies, open field behaviour and pituitary-adrenal system in growing dairy cattle. Physiology and Behavior 64: 273278CrossRefGoogle ScholarPubMed
Robbins, T, Mittleman, G, O'Brien, J and Winn, P 1990 The neurobiological significance of stereotypy induced by stimulant drugs. In: Cooper, S and Dourish, C (eds) The Neurobiology of Stereotyped Behaviour pp 2563. Clarendon Press: Oxford, UKGoogle Scholar
Rushen, J 1991 Problems associated with the interpretation of physiological data in the assessment of animal-welfare. Applied Animal Behaviour Science 28(4): 381386CrossRefGoogle Scholar
Sacks, O 1986 The Man who Mistook his Wife for a Hat. Picador: London, UKGoogle Scholar
Sakakibara, A 1996 The effects of repeated exposure of music on pleasure — redundancy of rhythm pattern and prototypicality of harmony. Japanese Journal of Educational Psychology 44: 92101Google Scholar
Sanchez, M, Ladd, C and Plotsky, P 2001 Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Development and Psychopathology 13: 419449CrossRefGoogle ScholarPubMed
Sandson, J and Albert, M 1984 Varieties of perseveration. Neuropsychologia 22: 715732CrossRefGoogle ScholarPubMed
Sandson, J and Albert, M 1987 Perseveration in behavioural neurology. Neurology 37: 17361741CrossRefGoogle Scholar
Sato, S, Kubo, T and Abe, M 1992 Factors influencing tongue-rolling and the relationship between tongue-rolling and production traits in fattening cattle. Journal of Animal Science 70 (Suppl I): 157 (Abstract)Google Scholar
Schofield, W and Mulville, J 1998 Assessment of the modified Forsell's procedure for the treatment of oral stereotypies in 10 horses. Veterinary Record 142: 572575CrossRefGoogle Scholar
Seo, T, Sato, S, Kosaka, K, Sakamoto, N and Tokumoto, K 1998 Tongue-playing and heart rate in calves. Applied Animal Behaviour Science 58: 179182CrossRefGoogle Scholar
Shepherdson, D J, Mellen, J D and Hutchins, M 1999 Second Nature — Environmental Enrichment for Captive Animals, Second Edition. Smithsonian Institute Press: Washington, USAGoogle Scholar
Sherwin, C 1998 Voluntary wheel running: a review and novel interpretation. Animal Behaviour 56: 1127CrossRefGoogle Scholar
Sroufe, L and Cooper, R 1988 Child Development — Its Nature and Course. Alfred A Knopf: New York, USAGoogle Scholar
Stevenson, M 1983 The captive environment: its effect on exploratory and related behavioural responses in wild animals. In: Archer, J and Birke, L (eds) Exploration in Animals and Humans p 176-197. Van Nostrand Reinhold: London, UKGoogle Scholar
Thelen, E 1981 Rhythmical behavior in infancy: an ethological perspective. Developmental Psychology 17: 237257CrossRefGoogle Scholar
Toates, F 2000 Multiple factors controlling behaviour: implications for stress and welfare. In: Moberg, G and Mench, J (eds) The Biology of Animal Stress pp 199226. CAB International: Wallingford, UKGoogle Scholar
Toates, F 2001 Biological Psychology. Pearson Education Limited: Harlow, UKGoogle Scholar
Turner, M 1997 Towards an executive dysfunction account of repetitive behaviour in autism. In: Russell, J (ed) Autism as an Executive Disorder pp 57100. Oxford University Press: New York, USAGoogle Scholar
Turner, M 1999a Generating novel ideas: fluency performance in high-functioning and learning disabled individuals with autism. Journal of Child Psychology and Psychiatry 40: 189201CrossRefGoogle ScholarPubMed
Turner, M 1999b Annotation: repetitive behaviour in autism: a review of psychological research. Journal of Child Psychology and Psychiatry 40: 839849CrossRefGoogle ScholarPubMed
Van Reenen, C G, Strappini, A C, van der Werf, J T N, Schouten, W G P and Veissier, I 2001 Physiological correlates of abnormal oral behaviours in veal calves. In: Garner, J P, Mench, J A and Heekin, S P (eds) Proceedings of the 35th Congress of the International Society for Applied Ethology p 101 (Abstract). Center for Animal Welfare at UC Davis: California, USAGoogle Scholar
Vestergaard, K S, Skadhauge, E and Lawson, L G 1997 The stress of not being able to perform dustbathing in laying hens. Physiology and Behavior 62: 413419CrossRefGoogle Scholar
Vickery, S S and Mason, G J 2003 Behavioural persistence in captive bears: implication for reintroduction. Ursus 14: 3543Google Scholar
Vinke, C M, Eenkhoorn, N C, Netto, W J, Fermont, P C J and Spruijt, B M 2002 Stereotypic behaviour and tail biting in farmed mink (Mustela vison) in a new housing system. Animal Welfare 11: 231245Google Scholar
Waters, A J 2002 Factors influencing the development of stereotypic and redirected behaviour in young horses. PhD thesis, University of Bristol, UK.Google Scholar
Watkins, E and Brown, R 2002 Rumination and executive function in depression: an experimental study. Journal of Neurology, Neurosurgery and Psychiatry 72: 400402CrossRefGoogle ScholarPubMed
Wiedenmayer, C 1997 Causation of the ontogenic development of stereotypic digging in gerbils. Animal Behaviour 53: 461470CrossRefGoogle Scholar
Wielebnowski, N C, Fletchall, N, Carlstead, K, Busso, J M and Brown, J L 2002 Noninvasive assessment of adrenal activity associated with husbandry and behavioral factors in the North American clouded leopard population. Zoo Biology 21: 7798CrossRefGoogle Scholar
Wiepkema, P, Broom, D, Duncan, I and van Putten, G 1983 Abnormal Behaviours in Farm Animals — Report of the Commission of the European Communities. Commission of the European Communities: Brussels, Belgium.Google Scholar
Wiepkema, P, van Hellemond, K, Roessingh, P and Romberg, H 1987 Behaviour and abomasal damage in individual veal calves. Applied Animal Behaviour Science 18: 257268CrossRefGoogle Scholar
Wolf, D B and Abell, N 2003 Examining the benefits of meditation techniques on psychosocial functioning. Research on Social Work Practice 13: 2742CrossRefGoogle Scholar
Würbel, H, Stauffacher, M and von Holst, D 1996 Stereotypies in laboratory mice — quantitative and qualitative description of the ontogeny of wire-gnawing and jumping in Zur:ICR and Zur:ICR nu. Ethology 102: 371385CrossRefGoogle Scholar
Young, R 2003 Environmental Enrichment. Blackwell Science: Oxford, UKGoogle Scholar