Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH FRONT

Hormones, stress and the welfare of animals

A. J. Tilbrook A B C and C. R. Ralph A
+ Author Affiliations
- Author Affiliations

A Animal Welfare Science Centre, Division of Livestock and Farming Systems, South Australian Research and Development Institute, University of Adelaide, Roseworthy, SA 5371, Australia.

B Present address: Centre for Animal Science, Queensland Alliance for Agriculture and Food Innovation, Level 3, Queensland Bioscience Precinct, Building 80, University of Queensland, 306 Carmody Road, St Lucia, Qld 4072, Australia.

C Corresponding author. Email: a.tilbrook@uq.edu.au

Animal Production Science 58(3) 408-415 https://doi.org/10.1071/AN16808
Submitted: 12 December 2016  Accepted: 1 June 2017   Published: 28 July 2017

Abstract

There are numerous endocrine (hormonal) responses during stress and these are often complex. This complexity makes the study of endocrine stress responses challenging and the challenges are intensified when attempts are made to use measures of hormones to assess the welfare of animals because so many endocrine systems are activated during stress and because there are countless stimuli that trigger these systems. Most research has concentrated on only a small number of these endocrine systems, particularly the hypothalamo–pituitary adrenal axis and the sympathoadrenal system, and there is a need to broaden the scope of endocrine systems that are studied. Furthermore, systematic approaches are required to establish when the actions of hormones associated with stress responses result in physiological and/or behavioural consequences that will have negative or positive effects on the welfare of animals.


References

Barnett JL, Cronin GM, Winfield CG (1981) The effects of individual and group penning of pigs on total and free plasma corticosteroids and the maximum corticosteroid binding capacity. General and Comparative Endocrinology 44, 219–225.
The effects of individual and group penning of pigs on total and free plasma corticosteroids and the maximum corticosteroid binding capacity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXksVSis78%3D&md5=90075de17bd1ea2e588f0eba489ccb26CAS |

Barnett JL, Hemsworth PH, Cronin GM, Newman EA, Mccallum TH, Chilton D (1992) Effects of pen size, partial stalls and method of feeding on welfare-related behavioral and physiological-responses of group-housed pigs. Applied Animal Behaviour Science 34, 207–220.
Effects of pen size, partial stalls and method of feeding on welfare-related behavioral and physiological-responses of group-housed pigs.Crossref | GoogleScholarGoogle Scholar |

Beausoleil NJ, Mellor DJ (2015a) Advantages and limitations of the five domains model for assessing welfare impacts associated with vertebrate pest control. New Zealand Veterinary Journal 63, 37–43.
Advantages and limitations of the five domains model for assessing welfare impacts associated with vertebrate pest control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVKrt7bM&md5=5395e9f2d54b9054f339966f84c25671CAS |

Beausoleil NJ, Mellor DJ (2015b) Introducing breathlessness as a significant animal welfare issue. New Zealand Veterinary Journal 63, 44–51.
Introducing breathlessness as a significant animal welfare issue.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cbgsV2jsA%3D%3D&md5=81b7bd61acc4a7063b07b81bb9b72609CAS |

Brambell FWR, Barbour DS, Barnett MB, Ewer TK, Hobson A, Pitchforth H, Smith WR, Thorpe WH, Winship FJW (1965) Report of the Technical Committee to enquire into the welfare of animals kept under intensive husbandry systems. Her Majesty’s Stationary Office, London.

Burnard C, Ralph C, Hynd P, Edwards JH, Tilbrook AJ (2017) Hair cortisol and its potential value as a physiological measure of stress response in human and non-human animals. Animal Production Science 57, 401–414.
Hair cortisol and its potential value as a physiological measure of stress response in human and non-human animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhvFynuro%3D&md5=d45a54255ba53dbcf2b0e646de8c85f4CAS |

Cannon W (1929) ‘Bodily changes in pain, hunger, fear, and rage.’ (Appleton: New York)

Cannon W (1932) ‘The wisdom of the body.’ (Norton: New York)

Cawadias AP (1940) The history of endocrinology. Proceedings of the Royal Society of Medicine 34, 25–30.

Clarke IJ, Hemsworth PH, Barnett JL, Tilbrook AJ (1992) Stress and reproduction in farm-animals. Stress and Reproduction 86, 239–252.

Dawkins MS (2008) The science of animal suffering. Ethology 114, 937–945.
The science of animal suffering.Crossref | GoogleScholarGoogle Scholar |

Dawkins MS (2017) Animal welfare and efficient farming: is conflict inevitable? Animal Production Science 57, 201–208.

Fraser D, Duncan IJH, Edwards SA, Grandin T, Gregory NG, Guyonnet V, Hemsworth PH, Huertas SM, Huzzey JM, Mellor DJ, Mench JA, Spinka M, Whay HR (2013) General principles for the welfare of animals in production systems: the underlying science and its application. Veterinary Journal (London, England) 198, 19–27.
General principles for the welfare of animals in production systems: the underlying science and its application.Crossref | GoogleScholarGoogle Scholar |

Green TC, Mellor DJ (2011) Extending ideas about animal welfare assessment to include ‘quality of life’ and related concepts. New Zealand Veterinary Journal 59, 263–271.
Extending ideas about animal welfare assessment to include ‘quality of life’ and related concepts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbltlOltQ%3D%3D&md5=653a3a9ced69f8e9a1e3fa476d9d8d15CAS |

Gross CG (1998) Claude Bernard and the constancy of the internal environment. The Neuroscentist 4, 380–385.
Claude Bernard and the constancy of the internal environment.Crossref | GoogleScholarGoogle Scholar |

Hemsworth PH, Mellor DJ, Cronin GM, Tilbrook AJ (2015) Scientific assessment of animal welfare. New Zealand Veterinary Journal 63, 24–30.
Scientific assessment of animal welfare.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2M7lt1Cntg%3D%3D&md5=0109e2f0d79eff7df2ecaac616283d9bCAS |

Johnson EO, Kamilaris TC, Chrousos GP, Gold PW (1992) Mechanisms of stress: a dynamic overview of hormonal and behavioral homeostasis. Neuroscience and Biobehavioral Reviews 16, 115–130.
Mechanisms of stress: a dynamic overview of hormonal and behavioral homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XltVCgsLs%3D&md5=764267db7c6e58819f2ea7e8fead680aCAS |

Korte SM, Olivier B, Koolhaas JM (2007) A new animal welfare concept based on allostasis. Physiology & Behavior 92, 422–428.
A new animal welfare concept based on allostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtF2htr%2FN&md5=dda600a0785068676f341cf344802ccbCAS |

Lane J (2006) Can non-invasive glucocorticoid measures be used as reliable indicators of stress in animals? Animal Welfare (South Mimms, England) 15, 331–342.

McEwen B, Lasley EN (2003) Allostatic load: when protection gives way to damage. Advances in Mind-Body Medicine 19, 28–33.

McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Hormones and Behavior 43, 2–15.
The concept of allostasis in biology and biomedicine.Crossref | GoogleScholarGoogle Scholar |

McEwen BS, Wingfield JC (2010) What is in a name? Integrating homeostasis, allostasis and stress. Hormones and Behavior 57, 105–111.
What is in a name? Integrating homeostasis, allostasis and stress.Crossref | GoogleScholarGoogle Scholar |

Mellor DJ (2012) Animal emotions, behaviour and the promotion of positive welfare states. New Zealand Veterinary Journal 60, 1–8.
Animal emotions, behaviour and the promotion of positive welfare states.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38%2Fot1Wgug%3D%3D&md5=eda4271f5e82e5a3d2cc88b23dbd3cc5CAS |

Mellor DJ (2015) Positive animal welfare states and reference standards for welfare assessment. New Zealand Veterinary Journal 63, 17–23.
Positive animal welfare states and reference standards for welfare assessment.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cjntFOgsA%3D%3D&md5=a04b5b2523df5b1ffa9bb707717a3d05CAS |

Mellor DJ (2016) Updating animal welfare thinking: moving beyond the ‘five freedoms’ towards ‘a life worth living’. Animals (Basel) 6, 21
Updating animal welfare thinking: moving beyond the ‘five freedoms’ towards ‘a life worth living’.Crossref | GoogleScholarGoogle Scholar |

Mellor DJ, Reid CWS (1994) Concepts of animal well-being and predicting the impact of procedures on experimental animals. In ‘Improving the well-being of animals in the research environment’. pp. 3–18. (The Australian and New Zealand Council for the Care of Animals in Research and Teaching: Adelaide)

Melmed S, Polonsky KS, Larsen PR, Kronenberg HM (2016) ‘Williams textbook of endocrinology.’ (Elsevier: Philadelphia, PA)

Moberg GP (1987) Influence of the adrenal axis upon the gonads. Oxford Reviews of Reproductive Biology 9, 456–496.

Moberg GP (1996) Suffering from stress: an approach for evaluating the welfare of an animal. Acta Agriculturae Scandinavica, Section A – Animal Science 46–49.

Moberg GP (1999) When does stress become distress? Lab Animal 28, 22–26.

Möstl E, Rettenbacher S, Palme R (2005) Measurement of corticosterone metabolites in birds’ droppings: an analytical approach. Annals of the New York Academy of Sciences 1046, 17–34.
Measurement of corticosterone metabolites in birds’ droppings: an analytical approach.Crossref | GoogleScholarGoogle Scholar |

Papargiris MM, Rivalland ET, Clarke IJ, Smith JT, Pereira A, Tilbrook AJ (2011) Evidence that RF-amide related peptide-3 is not a mediator of the inhibitory effects of psychosocial stress on gonadotrophin secretion in ovariectomised ewes. Journal of Neuroendocrinology 23, 208–215.
Evidence that RF-amide related peptide-3 is not a mediator of the inhibitory effects of psychosocial stress on gonadotrophin secretion in ovariectomised ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjtVahsrk%3D&md5=2974d39aeca5f05e547a275ffd94332aCAS |

Ralph CR, Tilbrook AJ (2016) INVITED REVIEW: the usefulness of measuring glucocorticoids for assessing animal welfare. Journal of Animal Science 94, 457–470.
INVITED REVIEW: the usefulness of measuring glucocorticoids for assessing animal welfare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtVymu73J&md5=8df20a3f1cc021418809f78b784a365eCAS |

Ralph CR, Hemsworth PH, Leury BJ, Tilbrook AJ (2015) Relationship between plasma and tissue corticosterone in laying hens (Gallus gallus domesticus): implications for stress physiology and animal welfare. Domestic Animal Endocrinology 50, 72–82.
Relationship between plasma and tissue corticosterone in laying hens (Gallus gallus domesticus): implications for stress physiology and animal welfare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhslKjtrrM&md5=7319ed5dafeb38afcb765d05cd3b39fdCAS |

Ralph CR, Lehman MN, Goodman RL, Tilbrook AJ (2016) Impact of psychosocial stress on gonadotrophins and sexual behaviour in females: role for cortisol? Reproduction (Cambridge, England) 152, R1–R14.
Impact of psychosocial stress on gonadotrophins and sexual behaviour in females: role for cortisol?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhslaqtbnF&md5=acaab41fda615d6831da9af1d26f03f3CAS |

Romero LM, Dickens MJ, Cyr NE (2009) The reactive scope model: a new model integrating homeostasis, allostasis, and stress. Hormones and Behavior 55, 375–389.
The reactive scope model: a new model integrating homeostasis, allostasis, and stress.Crossref | GoogleScholarGoogle Scholar |

Sapolsky RM (2000) Stress hormones: good and bad. Neurobiology of Disease 7, 540–542.
Stress hormones: good and bad.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsVGnu7o%3D&md5=6ec50cf678fbcf515b1399bdea684c39CAS |

Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21, 55–89.

Sawchenko PE, Li HY, Ericsson A (2000) Ciruits and mechanisms governing hypothalamic responses to stress: a tale of two paradigms. Progress in Brain Research 122, 61–78.
Ciruits and mechanisms governing hypothalamic responses to stress: a tale of two paradigms.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3gtFaqsg%3D%3D&md5=abe5777846603866cfeff73eee9f8b58CAS |

Selye H (1946) The general adaptation syndrome and the diseases of adaptation. The Journal of Clinical Endocrinology and Metabolism 6, 117–230.
The general adaptation syndrome and the diseases of adaptation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaH28XhvFGmug%3D%3D&md5=42aa89294827238b7f3b51195cb762b6CAS |

Selye H (1955a) ‘Critical period’ for inhibition of inflammation by a primarily neurogenic stress-situation. Psychosomatic Medicine 17, 124–127.
‘Critical period’ for inhibition of inflammation by a primarily neurogenic stress-situation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG2M%2FntlGqsQ%3D%3D&md5=7f976c0be2fbf6e870cfebb44ee14641CAS |

Selye H (1955b) Stress and disease. Laryngoscope 65, 500–514.
Stress and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2MXntVentw%3D%3D&md5=2cb67d76ab6b9388d6f03f97d39acf01CAS |

Selye H (1955c) Stress and disease. Geriatrics 10, 253–261.

Selye H (1955d) Stress, hormones and inflammation. American Journal of Proctology 6, 226–227.

Selye H (1956a) Stress and psychiatry. The American Journal of Psychiatry 113, 423–427.
Stress and psychiatry.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG2s%2FgvVOjsA%3D%3D&md5=1a8a6a833e72033e78304b9f7638cd63CAS |

Selye H (1956b) ‘The stress of life.’ (McGraw-Hill: New York)

Selye H (1956c) The stress-concept as it presents itself in 1956. Antibiotics and Chemotherapy 3, 1–17.
The stress-concept as it presents itself in 1956.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG2s%2FivVaqtA%3D%3D&md5=0de2dae8b9e47eeaa08adad484a91f12CAS |

Stackpole CA, Clarke IJ, Breen KM, Turner AI, Karsch FJ, Tilbrook AJ (2006) Sex difference in the suppressive effect of cortisol on pulsatile secretion of luteinizing hormone in sheep. Endocrinology 147, 5921–5931.
Sex difference in the suppressive effect of cortisol on pulsatile secretion of luteinizing hormone in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1yqtr3L&md5=c80f307acfc0020d683c5c91f9b9c578CAS |

Starling EH (1905) The Croonian lectures. 1. On the chemical correlation of the functions of the body. Lancet 166, 339–341.
The Croonian lectures. 1. On the chemical correlation of the functions of the body.Crossref | GoogleScholarGoogle Scholar |

Tilbrook AJ (2007) Neuropeptides, stress-related. In ‘Encyclopedia of stress. Vol. 2’. (Ed. G Fink) pp. 903–908. (Academic Press: Oxford, UK)

Tilbrook AJ, Clarke IJ (2006) Neuroendocrine mechanisms of innate states of attenuated responsiveness of the hypothalamo–pituitary adrenal axis to stress. Frontiers in Neuroendocrinology 27, 285–307.
Neuroendocrine mechanisms of innate states of attenuated responsiveness of the hypothalamo–pituitary adrenal axis to stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVyisLfO&md5=9499f345125db9594ede6dd9aee91cb7CAS |

Tilbrook AJ, Canny BJ, Serapiglia MD, Ambrose TJ, Clarke IJ (1999a) Suppression of the secretion of luteinizing hormone due to isolation/restraint stress in gonadectomised rams and ewes is influenced by sex steroids. The Journal of Endocrinology 160, 469–481.
Suppression of the secretion of luteinizing hormone due to isolation/restraint stress in gonadectomised rams and ewes is influenced by sex steroids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktVeqtr0%3D&md5=447eed523708020297a6d9f0174ee2e9CAS |

Tilbrook AJ, Canny BJ, Stewart BJ, Serapiglia MD, Clarke IJ (1999b) Central administration of corticotrophin releasing hormone but not arginine vasopressin stimulates the secretion of luteinizing hormone in rams in the presence and absence of testosterone. The Journal of Endocrinology 162, 301–311.
Central administration of corticotrophin releasing hormone but not arginine vasopressin stimulates the secretion of luteinizing hormone in rams in the presence and absence of testosterone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlt1OltrY%3D&md5=c107453e501df66aea7d2369b06744e3CAS |

Trans Hoff HE, Guillemin R, Guillemin L (1974) Bernard, C. In ‘Lectures on the phemonena common to animals and plants’. (Springfield, IL)

Turner AI, Tilbrook AJ (2006) Stress, cortisol and reproduction in female pigs. Society of Reproduction and Fertility Supplement 62, 191–203.

Turner AI, Keating C, Tilbrook AJ (2012) Sex differences and the role of sex steroids in sympatho–adrenal mudullary system and hypothalamo–pituitary responses to stress. In ‘Sex steroids’. (Ed. SM Kahn) pp. 115–136. (Tech Publishing: Rijeka, Croatia)

Wagenmaker ER, Breen KM, Oakley AE, Tilbrook AJ, Karsch FJ (2010) The estrous cycle of the ewe is resistant to disruption by repeated, acute psychosocial stress. Biology of Reproduction 82, 1206–1215.
The estrous cycle of the ewe is resistant to disruption by repeated, acute psychosocial stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVCgtLo%3D&md5=3df75f54766f234cd937518b4f3d47d4CAS |