Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-23T08:43:08.039Z Has data issue: false hasContentIssue false

Monitoring stress hormone metabolites as a useful, non-invasive tool for welfare assessment in farm animals

Published online by Cambridge University Press:  01 January 2023

R Palme*
Affiliation:
Department of Biomedical Sciences/Biochemistry, University of Veterinary Medicine, Veterinärplatz 1, 1210 Vienna, Austria

Abstract

A multitude of endocrine mechanisms are involved in coping with challenges. Glucocorticoids, secreted by the adrenal glands, are in the front line of the battle to overcome stressful situations. They are usually measured in plasma samples as parameters of adrenal activity and thus of disturbance. Unfortunately, collecting blood samples itself can disturb an animal. Thus, non-invasive methods for the determination of glucocorticoids or their metabolites have become increasingly popular. The pros and cons of various non-invasive sample materials (saliva, excreta, milk, hair/feathers and eggs) for glucocorticoid determination are given. Above all, faecal samples offer the advantage that they can be collected easily. In faecal samples, circulating hormone levels are integrated over a certain period of time and represent the cumulative secretion of hormones. Thus, the levels are less affected by short fluctuations or the pulse-like nature of hormone secretion. However, using this technique to assess an animal's adrenocortical activity is not especially simple. Whether frequent sampling is necessary or single samples will suffice depends upon the study's aim (whether one is examining the impact of acute or chronic stressors). Background knowledge of the metabolism and excretion of cortisol/corticosterone metabolites is required and a careful validation for each species and sex investigated is obligatory. The present review also addresses analytical issues regarding sample storage, extraction procedures and immunoassays and includes a comprehensive list of published studies (up to 2011) describing the use of such methods in farmed animals. Applied properly, non-invasive techniques to monitor glucocorticoid metabolites in faecal samples of various species are a useful tool for welfare assessment, especially as they are easily applied at farm or group level.

Type
Research Article
Copyright
© 2012 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

Akre, AK, Bakken, M, Hovland, AL, Palme, R and Mason, G 2011 Clustered environmental enrichments induce more aggression and stereotypic behavior than do dispersed enrichments in female mice. Applied Animal Behaviour Science 131: 145152. http://dx.doi.org/10.1016/j.applanim.2011.01.010CrossRefGoogle Scholar
Alvarez-Rodriguez, J, Palacio, J and Sanz, A 2010 Effects of nursing frequency and parity on the productive, metabolic and reproductive parameters of beef cows. Livestock Science 129: 111121. http://dx.doi.org/10.1016/j.livsci.2010.01.013CrossRefGoogle Scholar
Belo, CJ, Schlegel, S, Moll, J, Möstl, E and Bruckmaier, RM 2009 Milk ejection disorders in Swiss dairy cows: a field study. Journal of Dairy Research 76: 222228. http://dx.doi.org/10.1017/S002202990900394XCrossRefGoogle ScholarPubMed
Berghold, P, Möstl, E and Aurich, C 2007 Effects of reproductive status and management on cortisol secretion and fertility of oestrous horse mares. Animal Reproduction Science 102: 276285. http://dx.doi.org/10.1016/j.anireprosci.2006.11.009CrossRefGoogle ScholarPubMed
Broom, DM 2001 Coping, stress and welfare. In: Broom, DM (ed) Coping with Challenge: Welfare in Animals Including Humans pp 112. Dahlem University Press: Berlin, GermanyGoogle Scholar
Broom, DM and Johnson, KG 1993 Stress and Animal Welfare. Chapman & Hall: London, UK10.1007/978-94-024-0980-2CrossRefGoogle Scholar
Buijs, S, Keeling, L, Rettenbacher, S, Van Poucke, E and Tuyttens, FAM 2009 Stocking density effects on broiler welfare: identifying sensitive ranges for different indicators. Poultry Science 88: 15361543. http://dx.doi.org/10.3382/ps.2009-00007CrossRefGoogle ScholarPubMed
Buijs, S, Keeling, LJ, Rettenbacher, S and Tuyttens, FAM 2011 Glucocorticoid metabolites in rabbit faeces — influence of environmental enrichment and cage size. Physiology & Behavior 104: 469473. http://dx.doi.org/10.1016/j.physbeh.2011.05.008CrossRefGoogle ScholarPubMed
Christofoletti, MD, Pereira, RJG and Duarte, JMB 2010 Influence of husbandry systems on physiological stress reactions of captive brown brocket (Mazama gouazoubira) and marsh deer (Blastocerus dichotomus): noninvasive analysis of fecal cortisol metabolites. European Journal of Wildlife Research 56: 561568. http://dx.doi.org/10.1007/s10344-009-0350-8CrossRefGoogle Scholar
Cook, CJ, Mellor, DJ, Harris, PJ, Ingram, JR and Matthews, LR 2000 Hands-on and hands-off measurement of stress. In: Moberg, GP and Mench, JA (eds) The Biology of Animal Stress pp 123146. CABI Publishing: Oxon/New York, UK/USAGoogle Scholar
Dantzer, B, McAdam, AG, Palme, R, Humphries, MM, Boutin, S and Boonstra, R 2011 How does diet affect fecal steroid hormone metabolite concentrations? An experimental examination in red squirrels. General and Comparative Endocrinology 174: 124131. http://dx.doi.org/10.1016/j.ygcen.2011.08.010CrossRefGoogle ScholarPubMed
Downing, JA and Bryden, WL 2008 Determination of corticosterone concentrations in egg albumen: a non-invasive indicator of stress in laying hens. Physiology & Behavior 95: 381387. http://dx.doi.org/10.1016/j.physbeh.2008.07.001CrossRefGoogle ScholarPubMed
El-Bahr, SM, Kahlbacher, H, Rausch, WD and Palme, RG 2005 Excretion of catecholamines (adrenaline and noradrenaline) in domestic livestock. Wiener Tierärztliche Monatsschrift 92: 207213Google Scholar
Faleiro, AG, Gonzalez, LA, Blanch, M, Cavini, S, Castells, L, de la Torre, JLR, Manteca, X, Calsamiglia, S and Ferret, A 2011 Performance, ruminal changes, behaviour and welfare of growing heifers fed a concentrate diet with or without barley straw. Animal 5: 294303. http://dx.doi.org/10.1017/S1751731110001904CrossRefGoogle ScholarPubMed
Fisher, AD, Stewart, M, Verkerk, GA, Morrow, CJ and Matthews, LR 2003 The effects of surface type on lying behaviour and stress responses of dairy cows during periodic weather-induced removal from pasture. Applied Animal Behaviour Science 81: 111. http://dx.doi.org/10.1016/S0168-1591(02)00240-XCrossRefGoogle Scholar
Flauger, B, Krüger, K, Gerhards, H and Möstl, E 2010 Simplified method to measure glucocorticoid metabolites in faeces of horses. Veterinary Research Communications 34: 185195CrossRefGoogle ScholarPubMed
González, LA, Ferret, A, Manteca, X, Ruíz-de-la-Torre, JL, Calsamiglia, S, Devant, M and Bach, A 2008a Effect of the number of concentrate feeding places per pen on performance, behavior, and welfare indicators of Friesian calves during the first month after arrival at the feedlot. Journal of Animal Science 86: 41943110.2527/jas.2007-0362CrossRefGoogle ScholarPubMed
González, LA, Ferret, A, Manteca, X, Ruíz-de-la-Torre, JL, Calsamiglia, S, Devant, M and Bach, A 2008b Performance, behavior, and welfare of Friesian heifers housed in pens with two, four, and eight individuals per concentrate feeding place. Journal of Animal Science 86: 14461458. http://dx.doi.org/10.2527/jas.2007-0675CrossRefGoogle ScholarPubMed
González, LA, Correa, LB, Ferret, A, Manteca, X, Ruíz-de-la-Torre, JL and Calsamiglia, S 2009 Intake, water consumption, ruminal fermentation, and stress response of beef heifers fed after different lengths of delays in the daily feed delivery time. Journal of Animal Science 87: 27092718. http://dx.doi.org/10.2527/jas.2008-1709CrossRefGoogle ScholarPubMed
Gorgasser, I, Tichy, A and Palme, R 2007 Faecal cortisol metabolites in Quarter horses during initial training under field conditions. Wiener Tierärztliche Monatsschrift 94: 226230Google Scholar
Hansen, SW, Malmkvist, J, Palme, R and Damgaard, BM 2007 Do double cages and access to occupational materials improve the welfare of farmed mink? Animal Welfare 16: 6376CrossRefGoogle Scholar
Hay, M and Mormède, P 1998 Urinary excretion of catecholamines, cortisol and their metabolites in Meishan and Large White sows: validation as a non-invasive and integrative assessment of adrenocortical and symphatoadrenal axis activity. Veterinary Research 29: 119128Google Scholar
Hoffmann, G, Bockisch, FJ and Kreimeier, P 2009 Influence of the husbandry system on the movement activity and stress exposure of horses in discharge husbandry systems. Landbauforschung Völkenrode 59: 105111Google Scholar
Hopster, H, Bruckmaier, RM, Van der Werf, JTN, Korte, SM, Macuhova, J, Korte-Bouws, G and van Reenen, CG 2002 Stress responses during milking; Comparing conventional and automatic milking in primiparous dairy cows. Journal of Dairy Science 85: 32063216. http://dx.doi.org/10.3168/jds.S0022-0302(02)74409-3CrossRefGoogle ScholarPubMed
Huzzey, JM, Nydam, DV, Grant, RJ and Overton, TR 2011 Associations of prepartum plasma cortisol, haptoglobin, fecal cortisol metabolites, and non-esterified fatty acids with postpartum health status in Holstein dairy cows. Journal of Dairy Science 94: 58785889. http://dx.doi.org/10.3168/jds.2010-3391CrossRefGoogle Scholar
Jakubowska, I, Rettenbacher, S and van den Hoven, R 2010 Faecal cortisol metabolite excretion and stress in Standardbred Trotters under field conditions and during treadmill training. Wiener Tierärztliche Monatsschrift 97: 3136Google Scholar
Janczak, AM, Torjesen, P, Palme, R and Bakken, M 2007 Effects of stress in hens on the behaviour of their offspring. Applied Animal Behaviour Science 107: 6677. http://dx.doi.org/10.1016/j.applanim.2006.09.016CrossRefGoogle Scholar
Keckeis, K, Lepschy, M, Schöpper, H, Moser, L, Troxler, J and Palme, R 2012 Hair cortisol: a parameter of chronic stress? Insights from a radiometabolism study in guinea pigs. Journal of Comparative Physiology B, in press. http://dx.doi.org/10.1007/s00360-012-0674-7CrossRefGoogle Scholar
Kjaer, JB, Glawatz, H, Scholz, B, Rettenbacher, S and Tauson, R 2011 Reducing stress during welfare inspection. Validation of a non-intrusive version of the LayWel plumage scoring system for laying hens. British Poultry Science 52: 149154. http://dx.doi.org/10.1080/00071668.2011.554799CrossRefGoogle ScholarPubMed
Kleinsasser, C, Graml, , Klobetz-Rassam, E, Barth, K, Waiblinger, S and Palmer, R 2010 Physiological validation of a non-invasive method for measuring adrenocortical activity in goats. Weiner Tierärztliche Monatsschrift 97: 259262Google Scholar
Kolbe, T, Palme, R, Touma, C and Rülicke, T 2012 Repeated use of foster mothers for embryo transfer in the mouse. Biology of Reproduction 86: 16CrossRefGoogle Scholar
Konjević, D, Janicki, Z, Slavica, A, Severin, K, Krapinec, K, Božić, F and Palme, R 2011 Non-invasive monitoring of adrenocortical activity in free-ranging fallow deer (Dama dama L.). European Journal of Wildlife Research 57: 7781CrossRefGoogle Scholar
Lepschy, M, Touma, C, Hruby, R and Palme, R 2007 Noninvasive measurement of adrenocortical activity in male and female rats. Laboratory Animals 41: 372387CrossRefGoogle ScholarPubMed
Lepschy, M, Rettenbacher, S, Touma, C and Palme, RG 2008 Excretion of catecholamines in rats, mice and chickens. Journal of Comparative Physiology B 178: 62963610.1007/s00360-008-0254-zCrossRefGoogle Scholar
Lexen, E, El-Bahr, SM, Sommerfeld-Stur, I, Palme, R and Möstl, E 2008 Monitoring the adrenocortical response to disturbances in sheep by measuring glucocorticoid metabolites in the faeces. Wiener Tierärztliche Monatsschrift 95: 6471Google Scholar
Lexer, D, Hagen, K, Palme, R, Troxler, J and Waiblinger, S 2009 Time budgets and adrenocortical activity of cows milked in a robot or a milking parlour: inter-relationships and influence of social rank. Animal Welfare 18: 7380CrossRefGoogle Scholar
Malmkvist, J and Palme, R 2008 Periparturient nest building: Implications for parturition, kit survival, maternal stress and behaviour in farmed mink (Mustela vison). Applied Animal Behaviour Science 114: 270283. http://dx.doi.org/10.1016/j.applan-im.2008.01.018CrossRefGoogle Scholar
Malmkvist, J, Jeppesen, LL and Palme, R 2011 Stress and stereotypic behaviour in mink (Mustela vison): a focus on adrenocortical activity. Stress 14: 312323CrossRefGoogle ScholarPubMed
Merl, S, Scherzer, S, Palme, R and Möstl, E 2000 Pain causes increased concentrations of glucocorticoid metabolites in horse feces. Journal of Equine Veterinary Science 20: 586590. http://dx.doi.org/10.1016/S0737-0806(00)70267-XCrossRefGoogle Scholar
Moberg, GP 2000 Biological response to stress: implications for animal welfare. In: Moberg, GP and Mench, JA (eds) The Biology of Animal Stress pp 121. CABI Publishing: Oxon/New York, UK/USAGoogle Scholar
Monclús, R, Rödel, HG, Palme, R, von Holst, D and De Miguel, J 2006 Non-invasive measurement of the physiological stress response of wild rabbits to the odour of a predator. Chemoecology 16: 2529. http://dx.doi.org/10.1007/s00049-005-0324-6CrossRefGoogle Scholar
Montanholi, YR, Swanson, KC, Palme, R, Schenkel, FS, McBride, BW, Lu, D and Miller, SP 2010 Assessing feed efficiency in beef steers through feeding behavior, infrared thermography and glucocorticoids. Animal 4: 692701. http://dx.doi.org/10.1017/S1751731109991522CrossRefGoogle ScholarPubMed
Mormède, P, Andanson, S, Aupérin, B, Beerda, B, Gueméné, 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. http://dx.doi.org/10.1016/j.physbeh.2006.12.003CrossRefGoogle ScholarPubMed
Morrow, CJ, Kolver, ES, Verkerk, GA and Matthews, LR 2002 Fecal glucocorticoid metabolites as a measure of adrenal activity in dairy cattle. General and Comparative Endocrinology 126: 229241. http://dx.doi.org/10.1006/gcen.2002.7797CrossRefGoogle ScholarPubMed
Möstl, E and Palme, R 2002 Hormones as indicators of stress. Domestic Animal Endocrinology 23: 6774. http://dx.doi.org/10.1016/S0739-7240(02)00146-7CrossRefGoogle ScholarPubMed
Möstl, E, Messmann, S, Bagu, E, Robia, C and Palme, R 1999 Measurement of glucocorticoid metabolite concentrations in faeces of domestic livestock. Journal of Veterinary Medicine A 46: 621632. http://dx.doi.org/10.1046/j.1439-0442.1999.00256.xGoogle ScholarPubMed
Möstl, E, Maggs, JL, Schrötter, G, Besenfelder, U and Palme, R 2002 Measurement of cortisol metabolites in faeces of ruminants. Veterinary Research Communications 26: 127139. http://dx.doi.org/10.1023/A:1014095618125CrossRefGoogle ScholarPubMed
Möstl, E, Rettenbacher, S and Palme, R 2005 Measurement of corticosterone metabolites in birds’ droppings: an analytical approach. Annals of the New York Academy of Sciences 1046: 1734. http://dx.doi.org/10.1196/annals.1343.004CrossRefGoogle ScholarPubMed
Mülleder, C, Palme, R, Menke, C and Waiblinger, S 2003 Individual differences in behaviour and in adrenocortical activity in beef-suckler cows. Applied Animal Behaviour Science 84: 167183. http://dx.doi.org/10.1016/j.applanim.2003.08.007CrossRefGoogle Scholar
Nordmann, E, Keil, NM, Schmied-Wagner, C, Graml, C, Langbein, J, Aschwanden, J, von Hof, J, Maschat, K, Palme, R and Waiblinger, S 2011 Feed barrier design affects behaviour and physiology in goats. Applied Animal Behaviour Science 133: 4053. http://dx.doi.org/10.1016/j.applanim.2011.04.016CrossRefGoogle Scholar
Palme, R 2005 Measuring fecal steroids: guidelines for practical application. Annals of the New York Academy of Sciences 1046: 7580. http://dx.doi.org/10.1196/annals.1343.007CrossRefGoogle ScholarPubMed
Palme, R and Möstl, E 1997 Measurement of cortisol metabolites in faeces of sheep as a parameter of cortisol concentration in blood. International Journal of Mammalian Biology 62(S2): 192197Google Scholar
Palme, R, Fischer, P, Schildorfer, H and Ismail, MN 1996 Excretion of infused 14C-steroid hormones via faeces and urine in domestic livestock. Animal Reproduction Science 43: 4363. http://dx.doi.org/10.1016/0378-4320(95)01458-6CrossRefGoogle Scholar
Palme, R, Robia, C, Messmann, S, Hofer, J and Möstl, E 1999 Measurement of faecal cortisol metabolites in ruminants: a noninvasive parameter of adrenocortical function. Wiener Tierärztliche Monatsschrift 86: 237241Google Scholar
Palme, R, Robia, C, Baumgartner, W and Möstl, E 2000 Transport stress in cattle as reflected by an increase in faecal cortisol metabolites. Veterinary Record 146: 108109. http://dx.doi.org/10.1136/vr.146.4.108CrossRefGoogle Scholar
Palme, R, Rettenbacher, S, Touma, C, El-Bahr, SM and Möstl, E 2005 Stress hormones in mammals and birds: comparative aspects regarding metabolism, excretion and noninvasive measurement in fecal samples. Annals of the New York Academy of Sciences 1040: 162171. http://dx.doi.org/10.1196/annals.1327.021CrossRefGoogle ScholarPubMed
Palme, R, Wetscher, F and Winckler, C 2003 Measuring faecal cortisol metabolites: a non-invasive tool to assess animal welfare in cattle? Proceedings of the IVth Central European Buiatric Congress in Lovran pp 145150. 23-27 April 2003, Lovran, CroatiaGoogle Scholar
Pesenhofer, G, Palme, R, Pesenhofer, RM and Kofler, J 2006 Comparison of two methods of fixation during functional claw trimming, walk-in crush versus tilt table, in dairy cows using faecal cortisol metabolite concentrations and daily milk yield as parameters. Wiener Tierärztliche Monatsschrift 93: 288294Google Scholar
Rettenbacher, S and Palme, R 2009 Biological validation of a non-invasive method for the stress assessment in chickens. Berliner Münchner Tierärztliche Wochenschrift 122: 812Google ScholarPubMed
Rettenbacher, S, Möstl, E, Hackl, R, Ghareeb, K and Palme, R 2004 Measurement of corticosterone metabolites in chicken droppings. British Poultry Science 45: 704711. http://dx.doi.org/10.1080/00071660400006156CrossRefGoogle ScholarPubMed
Rettenbacher, S, Möstl, E, Hackl, R and Palme, R 2005 Corticosterone in chicken eggs. Annals of the New York Academy of Sciences 1046: 193203. http://dx.doi.org/10.1196/annals.1343.016CrossRefGoogle ScholarPubMed
Rettenbacher, S, Möstl, E and Groothuis, TGG 2009 Gestagens and glucocorticoids in chicken eggs. General and Comparative Endocrinology 164: 125129. http://dx.doi.org/10.1016/j.ygcen.2009.05.019CrossRefGoogle ScholarPubMed
Rouha-Mülleder, C, Palme, R and Waiblinger, S 2010 Assessment of animal welfare in 80 dairy cow herds in cubicle housing: animal health and other animal-related parameters. Wiener Tierärztliche Monatsschrift 97: 231241Google Scholar
Rushen, J 2000 Some issues in the interpretation of behavioural responses to stress. In: Moberg, GP and Mench, JA (eds) The Biology of Animal Stress pp 2342. CABI Publishing: Oxon/New York, UK/USAGoogle Scholar
Rushen, J, Butterworth, A and Swanson, JC 2011 Animal behavior and well-being symposium: farm animal welfare assurance: science and application. Journal of Animal Science 89: 12191228. http://dx.doi.org/10.2527/jas.2010-3589CrossRefGoogle ScholarPubMed
Schmidt, A, Biau, S, Möstl, E, Becker-Birck, M, Marillon, B, Aurich, J, Faure, J-M and Aurich, C 2010a Changes in cortisol release and heart rate variabilty in sport horses during long-distance road transport. Domestic Animal Endocrinology 38: 179189. http://dx.doi.org/10.1016/j.domaniend.2009/10.002CrossRefGoogle Scholar
Schmidt, A, Hödl, S, Möstl, E, Aurich, J, Müller, J and Aurich, C 2010b Cortisol release, heart rate, and heart rate variability in transport-naive horses during repeated road transport. Domestic Animal Endocrinology 39: 205213. http://dx.doi.org/10.1016/j.domaniend.2010.06.002CrossRefGoogle ScholarPubMed
Schmidt, A, Möstl, E, Wehnert, C, Aurich, J, Müller, J and Aurich, C 2010c Cortisol release and heart rate variabilty in horses during road transport of one, 3.5 and 8 hours duration. Hormones & Behavior 57: 209215. http://dx.doi.org/10.1016/j.yhbeh.2009.11.003CrossRefGoogle Scholar
Sheriff, MJ, Dantzer, B, Delehanty, B, Palme, R and Boonstra, R 2011 Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166: 869887. http://dx.doi.org/10.1007/s00442-011-1943-yCrossRefGoogle ScholarPubMed
Skobowiat, C, Dowdy, JC, Sayre, RM, Tuckey, RC and Slominski, A. 2011 Cutaneous hypothalamic-pituitary-adrenal axis homolog: regulation by ultraviolet radiation. American Journal of Physiology Endocrinology and Metabolism 301: E484E493CrossRefGoogle ScholarPubMed
Svendsen, PM, Hansen, BK, Malmkvist, J, Hansen, SW, Palme, R and Jeppesen, LJ 2007 Selection against stereotypic behaviour may have contradictory consequences for the welfare in farm mink (Mustela vison). Applied Animal Behaviour Science 107: 110119. http://dx.doi.org/10.1016/j.applanim.2006.09.014CrossRefGoogle Scholar
Taves, MD, Gomez-Sanchez, CE and Soma, KK 2011 Extra-adrenal glucocorticoids and mineralocorticoids: evidence for local synthesis, regulation, and function. American Journal of Physiology Endocrinology and Metabolism 301: E11E24. http://dx.doi.org/10.1152/ajpendo.00100.2011CrossRefGoogle ScholarPubMed
Touma, C and Palme, R 2005 Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Annals of the New York Academy of Sciences 1046: 5474. http://dx.doi.org/10.1196/annals.1343.006CrossRefGoogle ScholarPubMed
Touma, C, Sachser, N, Möstl, E and Palme, R 2003 Effect of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. General and Comparative Endocrinology 130: 267278CrossRefGoogle ScholarPubMed
Touma, C, Palme, R and Sachser, N 2004 Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones. Hormones & Behavior 45: 1022. http://dx.doi.org/10.1016/j.yhbeh.2003.07.002CrossRefGoogle ScholarPubMed
Tucker, CB, Dalley, DE, Burke, JLK and Clark, DA 2007a Milking cows once daily influences behavior and udder firmness at peak and mid lactation. Journal of Dairy Science 90: 16921703. http://dx.doi.org/10.3168/jds.2006-577CrossRefGoogle ScholarPubMed
Tucker, CB, Rogers, AR, Verkerk, GA, Kendall, PE, Webster, JR and Matthews, LR 2007b Effects of shelter and body condition on the behaviour and physiology of dairy cattle in winter. Applied Animal Behaviour Science 105: 113. http://dx.doi.org/10.1016/j.applanim.2006.06.009CrossRefGoogle Scholar
von Borell, E, Langbein, J, Després, G, Hansen, S, Leterrier, C, Marchant-Forde, J, Marchant-Forde, R, Minero, M, Mohr, E, Prunier, A, Valance, D and Veissier, I 2007 Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals: a review. Physiology & Behavior 92: 293316CrossRefGoogle ScholarPubMed
Webster, JR, Stewart, M, Rogers, AR and Verkerk, GA 2008 Assessment of welfare from physiological and behavioural responses of New Zealand dairy cows exposed to cold and wet conditions. Animal Welfare 17: 1926CrossRefGoogle Scholar
Weiss, D, Helmreich, S, Möstl, E, Dzidic, A and Bruckmaier, RM 2004 Coping capacity of dairy cows during the change from conventional to automatic milking. Journal of Animal Science 82: 563570CrossRefGoogle ScholarPubMed
Weiss, D, Möstl, E and Bruckmaier, RM 2005 Physiological and behavioural effects of changeover from conventional to automatic milking in dairy cows with and without previous experience. Veterinary Medicine Czech 50: 253261CrossRefGoogle Scholar