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Behavioural and Hormonal Indicators of Enduring Environmental Stress in Dogs

Published online by Cambridge University Press:  11 January 2023

B Beerda ,
M B H Schilder ,
J A R A M van Hooff ,
H W de Vries  and
J A Mol
B Beerda
Affiliation:
Department of Clinical Sciences of Companion Animals, Utrecht University, The Netherlands Department of Ethology and Socio-Ecology, Utrecht University, Padualaan 14, PO Box 14, 3508 TB, Utrecht, The Netherlands
M B H Schilder*
Affiliation:
Department of Ethology and Socio-Ecology, Utrecht University, Padualaan 14, PO Box 14, 3508 TB, Utrecht, The Netherlands
J A R A M van Hooff
Affiliation:
Department of Ethology and Socio-Ecology, Utrecht University, Padualaan 14, PO Box 14, 3508 TB, Utrecht, The Netherlands
H W de Vries
Affiliation:
Department of Clinical Sciences of Companion Animals, Utrecht University, The Netherlands
J A Mol
Affiliation:
Department of Clinical Sciences of Companion Animals, Utrecht University, The Netherlands
*
† Contact for correspondence and requests for reprints
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Abstract

Four groups of dogs, which had been subjected to housing conditions of varying quality for years, were assumed to experience different levels of stress. The groups were compared for behavioural and hormonal parameters in order to identify measures that indicate chronic stress in the dog and which may help to identify poor welfare in this species. As a standard for comparison, one of the four groups was composed of privately owned dogs; we assumed that chronic stress levels were relatively low in this group (GI). The three remaining groups of dogs (GII, Gill and GIV) were kept under conditions of low to relatively high austerity, and had basal urinary ratios of Cortisol to creatinine, adrenaline to creatinine and, to a lesser extent, noradrenaline to creatinine, that varied from low to high, respectively. Significant differences (P < 0.05) were found in Cortisol to creatinine ratios when comparing GI to GII, GUI and GIV and when GII was compared to GIV. Statistical analyses indicated that the mean adrenaline to creatinine ratio in GI differed from that in the remaining groups and that the ratio in GII differed from that in GUI. Noradrenaline to creatinine ratios differed significantly only between GI and GUI. Dopamine to creatinine ratios and noradrenaline to adrenaline ratios did not differ significantly between groups. When dogs were not disturbed, those that were kept under the most austere conditions typically had high levels of locomotor activity, nosing, urinating and paw lifting. After mild disturbance by a slamming door or in the presence of a researcher these animals reacted actively, with increased locomotor activity, circling and nosing, and they showed high levels of behaviours that have previously been associated with acute stress: body shaking, yawning, ambivalent postures and displacement behaviours. Chronic stress in dogs may be identified by increased paw lifting when animals are not disturbed and by ample behavioural expressions of arousal when they are mildly stimulated. Since some behaviours may occur in contexts not related to stress, behavioural data are easily misinterpreted with regard to chronic stress. Interpretation will only be meaningful when physiological measures such as urinary adrenaline to creatinine ratios and, especially, urinary Cortisol to creatinine ratios are also determined.

Keywords

animal welfarebehaviourchronic stressdogurinary catecholaminesurinary Cortisol
Type
Research Article
Information
Animal Welfare , Volume 9 , Issue 1 , February 2000 , pp. 49 - 62
Copyright
© 2000 Universities Federation for Animal Welfare

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References

Anderson, D E and Brady, J V 1972 Differential preparatory cardiovascular responses to aversive and appetitive behavioral conditioning. Conditional Reflex 7: 82–96CrossRefGoogle ScholarPubMed
Assia, E, Epstein, Y, Magazanik, A, Shapiro, Y and Sohar, E 1989 Plasma-cortisol levels in experimental heatstroke in dogs. International Journal of Biometeorology 33: 85–88CrossRefGoogle ScholarPubMed
Beerda, B, Schilder, M B H, Janssen, N S C R M and Mol, J A 1996 The use of saliva Cortisol, urinary Cortisol and catecholamine measurements for a noninvasive assessment of stress responses in dogs. Hormones and Behavior 30: 272–279Google ScholarPubMed
Beerda, B, Schilder, MBH, van Hooff, J A R A M, de Vries, H W and Mol, J A 1998 Behavioural, saliva Cortisol and heart rate responses to different types of stimuli in dogs. Applied Animal Behaviour Science 58: 365–381CrossRefGoogle Scholar
Beerda, B, Schilder, M B H, van Hooff, J A R A M, de Vries, H W and Mol, J A 1999a Chronic stress in dogs subjected to social and spatial restriction. I. Behavioral responses. Physiology and Behavior 66: 233–242CrossRefGoogle ScholarPubMed
Beerda, B, Schilder, MBH, van Hooff, J A R A M, de Vries, H W and Mol, J A 1999b Chronic stress in dogs subjected to social and spatial restriction. II. Hormonal and immunological responses. Physiology and Behavior 66: 243–254CrossRefGoogle ScholarPubMed
Bueno, L, Gue, M, Fargeas, M J, Alvinerie, M, Junien, J L and Fioramonti, J 1989 Vagally mediated inhibition of acoustic stress-induced Cortisol release by orally administered κ-opioid substances in dogs. Endocrinology 124: 1788–1793CrossRefGoogle ScholarPubMed
Clark, J D, Rager, D R, Crowell-Davis, S and Evans, D L 1997 Housing and exercise of dogs: effects on behavior, immune function, and Cortisol concentration. Laboratory Animal Science 47: 500–510Google ScholarPubMed
Clower, B R, Andy, O J, Montalvo, M and Peeler, D 1979 The hippocampus and stress induced 17-OHCS elevations. Pavlovian Journal of Biological Science 14: 86–91CrossRefGoogle ScholarPubMed
Corson, SA 1971 Pavlovian and operant conditioning techniques in the study of psychosocial and biological relationships. Society, Stress and Disease 1: 7–21Google Scholar
Craig, J V, Craig, J A and Vargas, J 1986 Corticosteroids and other indicators of hens’ well-being in four laying-house environments. Poultry Science 65: 856–863CrossRefGoogle ScholarPubMed
Dess, N K, Linwick, D, Patterson, J and Overmier, J B 1983 Immediate and proactive effects of controllability and predictability on plasma Cortisol responses to shocks in dogs. Behavioral Neuroscience 97: 1005–1016CrossRefGoogle ScholarPubMed
Engeland, W C, Miller, P and Gann, D S 1990 Pituitary-adrenal adrenomedullary responses to noise in awake dogs. American Journal of Physiology 258: R672–R677Google ScholarPubMed
Gaebelein, C J, Galosy, R A, Botticelli, L, Howard, J L and Obrist, P A 1977 Blood pressure and cardiac changes during signalled and unsignalled avoidance in dogs. Physiology & Behavior 19: 69–74CrossRefGoogle ScholarPubMed
Galosy, R A, Clarke, L K and Mitchell, J H 1979 Cardiac changes during behavioral stress in dogs. American Journal of Physiology 236: H750–H758Google ScholarPubMed
Gamallo, A, Villanua, A, Trancho, G and Fraile, A 1986 Stress adaptation and adrenal activity in isolated and crowded rats. Physiology & Behavior 36: 217–221CrossRefGoogle ScholarPubMed
Gue, M, Alvinerie, M, Junien, J L and Bueno, L 1989 Stimulation of κ opiate receptors in intestinal wall affects stress-induced increase of plasma Cortisol in dogs. Brain Research 502: 143–148CrossRefGoogle ScholarPubMed
Herbert, T B and Cohen, S 1993 Stress and immunity in humans: a meta-analytic review. Psychosomatic Medicine 55: 364–379CrossRefGoogle ScholarPubMed
Hetts, S, Clark, J D, Calpin, J P, Arnold, C E and Mateo, J M 1992 Influence of housing conditions on beagle behaviour. Applied Animal Behaviour Science 34: 137–155Google Scholar
Hilton, B A 1989 The relationship of uncertainty, control, commitment, and threat of recurrence to coping strategies used by women diagnosed with breast cancer. Journal of Behavioral Medicine 12: 39–54Google ScholarPubMed
Hubrecht, R C, Serpell, J A and Poole, T B 1992 Correlates of pen size and housing conditions on the behaviour of kennelled dogs. Applied Animal Behaviour Science 34: 365–383CrossRefGoogle Scholar
Hughes, H C and Campbell, S A 1990 Effect of primary enclosure size and human contact. In: Mench J A and Krulisch E (eds) Canine Research Environment, Proceedings of a Conference, 22 June 1989, Bethesda pp 66-73. Scientists Center for Animal Welfare: Bethesda, MD, USAGoogle Scholar
Jones, C A, Refsal, K R, Lippert, A C, Nachreiner, R F and Schwacha, M M 1990 Changes in adrenal Cortisol secretion as reflected in the urinary cortisol/creatinine ratio in dogs. Domestic Animal Endocrinology 7: 559572CrossRefGoogle ScholarPubMed
Jørgensen, L S, Christiansen, P, Raundahl, U, Østgaard, S, Christensen, N J, Fenger, M and Flachs, H 1990 Autonomic response to an experimental psychological stressor in healthy subjects: measurement of sympathetic, parasympathetic, and pituitary-adrenal parameters: test-retest reliability. Scandinavian Journal of Clinical and Laboratory Investigation 50: 823–829Google Scholar
Kathol, R G, Jaeckle, R S, Lopez, J F and Meller, W H 1989 Pathophysiology of HPA axis abnormalities in patients with major depression: an update. American Journal of Psychiatry 146: 311–317Google ScholarPubMed
Lown, B, Verrier, R and Corbalan, R 1973 Psychologic stress and threshold for repetitive ventricular response. Science 182: 834–836CrossRefGoogle ScholarPubMed
Mekhedova, A Ya and Ghadirian, A M 1979 The influence of experimental neurosis on the conditional reflexes and the content of blood catecholamines and acetylcholine in dogs. Pavlovian Journal of Biological Science 14: 79–85CrossRefGoogle ScholarPubMed
Mertens, P A and Unshelm, J 1996 Effects of group and individual housing on the behavior of kennelled dogs in animal shelters. Anthrozoös IX: 40–51CrossRefGoogle Scholar
Morrison, D F 1976 Multivariate Statistical Methods 2nd edition. McGraw-Hill-Kogakusha Ltd: Tokyo, JapanGoogle Scholar
Pagani, M, Rimoldi, O, Pizzinelli, P, Furian, R, Crivellare, W, Liberati, D, Cerutti, S and Malliani, A 1991 Assessment of the neural control of the circulation during psychological stress. Journal of the Autonomic Nervous System 35: 33–42CrossRefGoogle ScholarPubMed
Palazzolo, D L and Quadri, S K 1987 Plasma thyroxine and Cortisol under basal conditions and during cold stress in the aging dog. Proceedings of the Society for Experimental Biology and Medicine 185: 305–311CrossRefGoogle ScholarPubMed
Parrilla, P, Ramirez, P, Muelas, M S, Perez, J M, Fuente, T, Ruiz, J M and Ponce, J L 1990 Changes in small intestinal motility in acute physical stress - an experimental study. Hepato-gastroenterology 37: 140–146Google ScholarPubMed
Rijnberk, A, van Wees, A and Mol, J A 1988 Assessment of two tests for the diagnosis of canine hyperadrenocorticism. Veterinary Record 122: 178–180CrossRefGoogle ScholarPubMed
Roger, G K, Anton, R, Noyes, R and Gehris, T 1989 Direct comparison of urinary free Cortisol excretion in patients with depression and panic disorder. Biological Psychiatry 25: 873–878Google Scholar
Rushen, J 1985 Stereotypies, aggression and feeding schedules of tethered sows. Applied Animal Behaviour Science 14: 137–147CrossRefGoogle Scholar
Sassenrath, E N 1970 Increased adrenal responsiveness related to social stress in rhesus monkeys. Hormones and Behavior 1: 283–298CrossRefGoogle Scholar
Schwizgebel, D 1982 Zusammenhänge zwischen dem Verhalten des Tierlehrers und dem Verhalten des deutschen Schäferhundes im Hinblick auf tiergerechte Ausbildung. Aktuelle Arbeiten zur Artgemäßen Tierhaltung 138–148Google Scholar
Silver, R L and Wortman, C B 1980 Coping with undesirable life events. In: Garber, J and Seligman, M E P (eds) Human Helplessness pp 279–375. Academic Press: New York, USAGoogle Scholar
Solomon, R L and Wynne, L C 1953 Traumatic avoidance learning: acquisition in normal dogs. Psychological Monographs: General and Applied 67(4): 1–19CrossRefGoogle Scholar
Stafleu, F R, Rivas, E, Rivas, T, Vorstenbosch, J, Heeger, F R and Beynen, A C 1992 The use of analogous reasoning for assessing discomfort in laboratory animals. Animal Welfare 1: 77–84Google Scholar
Stoline, MR 1981 The status of multiple comparisons: simultaneous estimation of all pairwise comparisons in one-way ANOVA designs. The American Statistician 35: 134–141Google Scholar
Tuber, D S, Hennessy, M B, Sanders, S and Miller, J A 1996 Behavioral and glucocorticoid responses of adult domestic dogs (Canis familiaris) to companionship and social separation. Journal of Comparative Psychology 110: 103–108CrossRefGoogle ScholarPubMed
van Vonderen, I K, Kooistra, H S and Rijnberk, A 1997 Intra- and interindividual variation in urine osmolality and urine specific gravity in healthy pet dogs of various ages. Journal of Veterinary Internal Medicine 11: 30–35CrossRefGoogle ScholarPubMed
von Hoist, D 1986 Vegetative and somatic components of tree shrews’ behaviour. Journal of the Autonomic Nervous System (suppl.): 657–670Google Scholar