Quantification of salivary cortisol from captive dingoes (Canis dingo) in relation to age, sex, and breeding season: implications for captive management
Bradley Smith A D , Matthew Flavel B and Bradley Simpson C
+ Author Affiliations
- Author Affiliations
A Appleton Institute, Central Queensland University, 44 Greenhill Road, Wayville, SA 5034, Australia.
B School of Life Science, Department of Agriculture, La Trobe University, Melbourne, Vic. 3086, Australia.
C Flinders Centre for Innovation in Cancer, Flinders University, GPO Box 2100, Adelaide, SA 5001, Australia and School of Pharmacy and Medical Sciences, University of South Australia, GPO Box 2471, Adelaide, SA 5001, Australia.
D Corresponding author. Email: b.p.smith@cqu.edu.au
Australian Mammalogy 38(1) 21-28 https://doi.org/10.1071/AM15017
Submitted: 31 May 2015 Accepted: 17 August 2015 Published: 25 September 2015
Abstract
Captive-breeding programs can play a key role in the conservation of threatened species such as the Australian dingo (Canis dingo). It is important to determine whether holding and rearing practices impose stressors that impact negatively on program outcomes and the health and wellbeing of the captive population. Despite evidence that chronic stress has significant welfare implications, our understanding of ‘stress’ in either wild or captive dingoes remains limited. In a first attempt to rectify this, we report salivary cortisol concentrations in juvenile and adult dingoes held in a captive colony. Dingo puppies (n = 8, M = 0.484 ± 0.09 μg dL–1) were found to have higher concentrations than adults (n = 12, M = 0.106 ± 0.031 μg dL–1) (P < 0.0001). Concentrations in adult females (n = 6, M = 0.113 ± 0.030 μg dL–1) and males (n = 6, M = 0.099 ± 0.033 μg dL–1) did not significantly differ (P = 0.4740). Our preliminary findings also suggest that during the annual breeding season, males (but not females) have elevated levels of corticosteroids. Establishing a reference range for cortisol concentrations is vital for researchers and wildlife carers attempting to measure stressors in both captive and wild dingo populations. This study provides useful insight into the influence of time of day, development, and seasonality on cortisol concentrations. Suggestions for future research and implications of routine cortisol evaluation to aid better management practices are also discussed.
Additional keywords: captivity, dingo, endocrinology, physiology, salivary cortisol, seasonality, stress, welfare.
References
Asa, C. (2010). The importance of reproductive management and monitoring in canid husbandry and endangered-species recovery. International Zoo Yearbook 44, 102–108.| The importance of reproductive management and monitoring in canid husbandry and endangered-species recovery.Crossref | GoogleScholarGoogle Scholar |
Beerda, B., Schilder, M., Janssen, N., and Mol, J. (1996). The use of saliva cortisol, urinary cortisol, and catecholamine measurements for a noninvasive assessment of stress responses in dogs. Hormones and Behavior 30, 272–279.
| The use of saliva cortisol, urinary cortisol, and catecholamine measurements for a noninvasive assessment of stress responses in dogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmvFOhtb8%3D&md5=ca732c479ea7ae309f0a653334b899bdCAS | 8918684PubMed |
Beerda, B., Schilder, M. B. H., van Hooff, J. A., 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, 365–381.
| Behavioural, saliva cortisol and heart rate responses to different types of stimuli in dogs.Crossref | GoogleScholarGoogle Scholar |
Beerda, B., Schilder, M. B. H., Bernardina, W., van Hoof, J. A. R. A. M., de Vries, H. W., and Mol, J. A. (1999). Chronic stress in dogs subjected to social and spatial restriction. II. Hormonal and immunological responses. Physiology & Behavior 66, 243–254.
| Chronic stress in dogs subjected to social and spatial restriction. II. Hormonal and immunological responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjtFGmt7o%3D&md5=22a625f91e24a91ee98ceb00664c8ca5CAS |
Bennett, A., and Hayssen, V. (2010). Measuring cortisol in hair and saliva from dogs: coat color and pigment differences. Domestic Animal Endocrinology 39, 171–180.
| Measuring cortisol in hair and saliva from dogs: coat color and pigment differences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFWqtb7O&md5=b7a0e1b81725d4495cb26ba847e10b71CAS | 20705413PubMed |
Bradshaw, S. (2007). Environmental endocrinology. General and Comparative Endocrinology 152, 125–141.
| Environmental endocrinology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvV2iu74%3D&md5=6c1c7a230737ddbc9854659742956843CAS |
Breuner, C., Delahanty, B., and Boonstra, R. (2013). Evaluating stress in natural populations of vertebrates: total CORT is not good enough. Functional Ecology 27, 24–36.
| Evaluating stress in natural populations of vertebrates: total CORT is not good enough.Crossref | GoogleScholarGoogle Scholar |
Corbett, L. K. (1988). Social dynamics of a captive dingo pack: population regulation by dominant female infanticide. Ethology 78, 177–198.
| Social dynamics of a captive dingo pack: population regulation by dominant female infanticide.Crossref | GoogleScholarGoogle Scholar |
Corbett, L. K. (2004). Australia and Oceania (Australasian): dingo (Canis lupus dingo). In ‘Canids: Foxes, Wolves, Jackals and Dogs – 2004 Status Survey and Conservation Action Plan’. (Eds C. Sillero-Zubiri, M. Hoffmann and D. W. Macdonald.) pp. 223–230. (IUCN/SSC Canid Specialist Group: Gland/Cambridge.)
Creel, S., Fox, J., Hardy, A., Sands, J., Garrott, B., and Peterson, R. (2002). Snowmobile activity and glucocorticoid stress responses in wolves and elk. Conservation Biology 16, 809–814.
| Snowmobile activity and glucocorticoid stress responses in wolves and elk.Crossref | GoogleScholarGoogle Scholar |
Derix, R., van Hooff, J., de Vries, H., and Wensing, J. (1993). Male and female mating competition in wolves: female suppression vs. male intervention. Behaviour 127, 141–174.
| Male and female mating competition in wolves: female suppression vs. male intervention.Crossref | GoogleScholarGoogle Scholar |
Dreschel, N., and Granger, D. (2009). Methods of collection for salivary cortisol measurement in dogs. Hormones and Behavior 55, 163–168.
| Methods of collection for salivary cortisol measurement in dogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjvF2isg%3D%3D&md5=38d8bcf52172ea7c5a88a6702f560370CAS | 18948108PubMed |
Dreschel, N., Cobb, M., Iskandarani, K., and Chinchilli, V. (2014). A meta-analysis of saliva cortisol measurement in domestic canines. Journal of Veterinary Behavior 9, e11–e12.
| A meta-analysis of saliva cortisol measurement in domestic canines.Crossref | GoogleScholarGoogle Scholar |
Eggermann, J., Theuerkauf, J., Pirga, B., Milanowski, A., and Gula, R. (2013). Stress-hormone levels of wolves in relation to breeding season, pack size, human activity, and prey density. Annales Zoologici Fennici 50, 170–175.
| Stress-hormone levels of wolves in relation to breeding season, pack size, human activity, and prey density.Crossref | GoogleScholarGoogle Scholar |
Gunnar, M., and Donzella, B. (2002). Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology 27, 199–220.
| Social regulation of the cortisol levels in early human development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXpt1ahtbo%3D&md5=b34cf820f3af4d6e00f9cf96804c14afCAS | 11750779PubMed |
Hennessy, M. (2013). Using hypothalamic–pituitary–adrenal measures for assessing and reducing the stress of dogs in shelters: a review. Applied Animal Behaviour Science 149, 1–12.
| Using hypothalamic–pituitary–adrenal measures for assessing and reducing the stress of dogs in shelters: a review.Crossref | GoogleScholarGoogle Scholar |
Jackson, S. (2006). Dingoes. In ‘Australian Mammals: Biology and Captive Management’. (Ed. S. Jackson.) pp. 381–407. (CSIRO Publishing: Melbourne.)
Jensen, P. (2007). Mechanisms and function in dog behaviour. In ‘The Behavioural Biology of Dogs’. (Ed. P. Jensen.) pp. 61–75. (CAB International: Oxfordshire, UK.)
Klinghammer, E., and Goodmann, P. A. (1987). Socialization and management of wolves in captivity. In ‘Man and Wolf; Advances, Issues and Problems in Captive Wolf Research’. (Ed. H. Frank.) pp. 31–59. (Dr W. Junk Publishers: Dordrecht.)
Kobelt, A., Hemsworth, P., Barnett, J., and Butler, K. (2003). Sources of sampling variation in saliva cortisol in dogs. Research in Veterinary Science 75, 157–161.
| Sources of sampling variation in saliva cortisol in dogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVSntLY%3D&md5=529d7beeaea9b2127a5abdf1e5743714CAS | 12893165PubMed |
Kolevská, J., Brunclík, V., and Svoboda, M. (2003). Circadian rhythm of cortisol secretion in dogs of different daily activities. A meta-analysis of salivary cortisol measurement in domestic canines. Acta Veterinaria Brno 72, 599–605.
| Circadian rhythm of cortisol secretion in dogs of different daily activities. A meta-analysis of salivary cortisol measurement in domestic canines.Crossref | GoogleScholarGoogle Scholar |
Koyama, T., Omata, Y., and Saito, A. (2003). Change in salivary cortisol concentrations during a 24-hour period in dogs. Hormone and Metabolic Research. Hormon- und Stoffwechselforschung. Hormones et Metabolisme 35, 355–357.
| Change in salivary cortisol concentrations during a 24-hour period in dogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnt12qur4%3D&md5=e9b445ce73927cdebf7e64ebf6fd0c12CAS | 12920657PubMed |
Lord, K., Feinstein, M., Smith, B., and Coppinger, R. (2013). Variation in reproductive traits of members of the genus Canis with special attention to the domestic dog (Canis familiaris). Behavioural Processes 92, 131–142.
| Variation in reproductive traits of members of the genus Canis with special attention to the domestic dog (Canis familiaris).Crossref | GoogleScholarGoogle Scholar | 23124015PubMed |
Mallonee, J., and Joslin, P. (2004). Traumatic stress disorder observed in an adult wild captive wolf (Canis lupus). Journal of Applied Animal Welfare Science 7, 107–126.
| Traumatic stress disorder observed in an adult wild captive wolf (Canis lupus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlslent7g%3D&md5=4105bc0c36bea84e7ce647c8e5fc5af1CAS | 15234887PubMed |
Marks, C. (2010). Haematological and biochemical responses of red foxes (Vulpes vulpes) to different capture methods and shooting. Animal Welfare (South Mimms, England) 19, 223–234.
| 1:CAS:528:DC%2BC3cXhtVClurjP&md5=a09e1508dccfdbfdb7faedbae40ce8b2CAS |
McEwen, B. (1998). Stress, adaptation, and disease: allostasis and allostatic load. Annals of the New York Academy of Sciences 840, 33–44.
| Stress, adaptation, and disease: allostasis and allostatic load.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3pt1ykuw%3D%3D&md5=04c055b8e1642437a50820953a034ba9CAS | 9629234PubMed |
McEwen, B., and Sapolsky, R. (1995). Stress and cognitive function. Current Opinion in Neurobiology 5, 205–216.
| Stress and cognitive function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlsVGitL4%3D&md5=694a6beca9161dc63ecd9dfe21ecf40fCAS | 7620309PubMed |
McEwen, B., and Wingfield, J. (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 | 12614627PubMed |
McLeod, P., Moger, W., Ryon, J., Gadbois, S., and Fentress, J. (1996). The relation between urinary cortisol levels and social behaviour in captive timber wolves. Canadian Journal of Zoology 74, 209–216.
| The relation between urinary cortisol levels and social behaviour in captive timber wolves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XisFOqu7o%3D&md5=e66b3c4a145f4a6db9d9e89ed8fb2074CAS |
Mech, L. D., and Boitani, L. (2003). ‘Wolves: Behavior, Ecology, and Conservation.’ (University of Chicago Press: Chicago.)
Morgan, K., and Tromborg, C. (2007). Sources of stress in captivity. Applied Animal Behaviour Science 102, 262–302.
| Sources of stress in captivity.Crossref | GoogleScholarGoogle Scholar |
Oddie, C., Blaine, E., Bradshaw, S., Coghlan, J., Denton, D., Nelson, J., and Scoggins, B. (1976). Blood corticosteroids in Australian marsupial and placental mammals and one monotreme. The Journal of Endocrinology 69, 341–348.
| Blood corticosteroids in Australian marsupial and placental mammals and one monotreme.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVCis74%3D&md5=326630c61830f417ae12d70c6767f5daCAS | 181514PubMed |
Pifarré, M., Valdex, R., Gonázles-Rebeles, C., Vázquez, C., Romano, M., and Galindo, F. (2012). The effect of zoo visitors on the behaviour and faecal cortisol of the Mexican wolf (Canis lupus baileyi). Applied Animal Behaviour Science 136, 57–62.
| The effect of zoo visitors on the behaviour and faecal cortisol of the Mexican wolf (Canis lupus baileyi).Crossref | GoogleScholarGoogle Scholar |
Romero, L. (2012). Using the reactive scope model to understand why stress physiology predicts survival during starvation in Galapagos marine iguanas. General and Comparative Endocrinology 176, 296–299.
| Using the reactive scope model to understand why stress physiology predicts survival during starvation in Galapagos marine iguanas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvFyisL8%3D&md5=d7ffa616aaac2d2e57a5b82f21109e32CAS | 22101208PubMed |
Romero, L., Dickens, M., and Cyr, N. (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 | 19470371PubMed |
Ruis, M., Te Brake, J., Engel, B., Ekkel, E., Buist, W., Blokhuis, H., and Koolhaas, J. (1997). The circadian rhythm of salivary cortisol in growing pigs: effects of age, gender and stress. Physiology & Behavior 62, 623–630.
| The circadian rhythm of salivary cortisol in growing pigs: effects of age, gender and stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlsVGgtb4%3D&md5=9a124b68c4bb94c02d5c6dd176b0ffe7CAS |
Sandri, M., Colussi, A., Perrotta, M., and Stefanon, B. (2015). Salivary cortisol concentration in healthy dogs is affected by size, sex, and housing context. Journal of Veterinary Behavior , .
| Salivary cortisol concentration in healthy dogs is affected by size, sex, and housing context.Crossref | GoogleScholarGoogle Scholar |
Sheriff, M., Dantzer, B., Delehanty, B., Palme, R., and Boonstra, R. (2011). Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166, 869–887.
| Measuring stress in wildlife: techniques for quantifying glucocorticoids.Crossref | GoogleScholarGoogle Scholar | 21344254PubMed |
Shivik, J., Palmer, G., Gese, E., and Osthaus, B. (2009). Captive coyotes compared to their counterparts in the wild: does environmental enrichment help? Journal of Applied Animal Welfare Science 12, 223–235.
| Captive coyotes compared to their counterparts in the wild: does environmental enrichment help?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptFehsr0%3D&md5=43736e5bac3cc9e43706b4067f654c75CAS | 20183476PubMed |
Smith, B. (2015). Biology and behaviour of the dingo. In ‘The Dingo Debate: Origins, Behaviour and Conservation’. (Ed. B. Smith.) pp. 25–53. (CSIRO Publishing: Melbourne.)
Smith, B., and Litchfield, C. (2010). Dingoes (Canis dingo) can use human social cues to locate hidden food. Animal Cognition 13, 367–376.
| Dingoes (Canis dingo) can use human social cues to locate hidden food.Crossref | GoogleScholarGoogle Scholar | 19779743PubMed |
Smith, B., and Watson, L. (2015). The role of private sanctuaries in dingo conservation and the management of dingoes in captivity. In ‘The Dingo Debate: Origins, Behaviour and Conservation’. (Ed. B. Smith.) pp. 277–299. (CSIRO Publishing: Melbourne.)
Sterling, P., and Eyer, J. (1988). Allostasis: a new paradigm to explain arousal pathology. In ‘Handbook of Life Stress, Cognition and Health’. (Eds K. Fisher and J. Reason.) pp. 629–649. (Wiley: New York.)
van Kesteren, F., Sillero-Zubiri, C., Millar, R., Argaw, K., Macdonald, D., and Paris, M. (2012). Sex, stress and social status: patterns in fecal testosterone and glucocorticoid metabolites in male Ethiopian wolves. General and Comparative Endocrinology 179, 30–37.
| Sex, stress and social status: patterns in fecal testosterone and glucocorticoid metabolites in male Ethiopian wolves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlGqtL7P&md5=e8f71580c98ee0e9a46315a8ca31a066CAS | 22841807PubMed |
Vincent, L. C., and Michell, A. R. (1992). Comparison of cortisol concentrations in saliva and plasma of dogs. Research in Veterinary Science 53, 342–345.
| Comparison of cortisol concentrations in saliva and plasma of dogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhtFKqtL8%3D&md5=60292f4e26b9c73d926cede8eb15c0e2CAS |
Wilton, A. (2001). DNA methods of assessing dingo purity. In ‘A Symposium on the Dingo’. (Eds C. Dickman and D. Lunney.) pp. 49–56. (Royal Zoological Society of New South Wales: Sydney.)
Wingfield, J., and Sapolsky, R. (2003). Reproduction and resistance to stress: when and how. Journal of Neuroendocrinology 15, 711–724.
| Reproduction and resistance to stress: when and how.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVOqtLw%3D&md5=a1704c74d78dacad2965b78155048af6CAS | 12834431PubMed |
Zimen, E. (1976). On the regulation of pack size in wolves. Zeitschrift für Tierpsychologie 40, 300–341.
| On the regulation of pack size in wolves.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE287otVGqtg%3D%3D&md5=7ddccec8fe0dfe6ecd39e63016b818d6CAS |
