Quantifying faecal cortisol metabolites in rescued orphaned koala joeys undergoing rehabilitation†
Harsh Gaurav Pahuja
A * and Edward Jitik Narayan A B
+ Author Affiliations
- Author Affiliations
A School of Agriculture and Food Sciences, Faculty of Science, The University of Queensland, St Lucia, Brisbane, Qld 4072, Australia.
B Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St Lucia, Brisbane, Qld 4072, Australia. Email: e.narayan@uq.edu.au
Australian Mammalogy 45(3) 317-323 https://doi.org/10.1071/AM22030
Submitted: 2 November 2022 Accepted: 19 April 2023 Published: 8 May 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the Australian Mammal Society.
Abstract
Mortality is prevalent in koala joeys being hand reared/rehabilitated, with little knowledge about the causes of such high rates of mortality. Wildlife hospitals/rehabilitation expose koala joeys to novel husbandry environments that create stressful stimulus for these animals. Furthermore, loss of the mother and/or being raised by a human can be threatening and/or stressful. The hypothalamic–pituitary–adrenal axis plays a vital role in mediating the stress endocrine response of vertebrate species including marsupials (by adrenocortical release of glucocorticoids such as cortisol), however, there are no studies that quantify cortisol metabolites in koala joeys. To contribute to this dearth of knowledge, the primary aim of this study was to quantify the levels of faecal cortisol metabolites (as an index of physiological stress) in koala joeys undergoing rehabilitation. A total of 39 faecal samples were collected from four koala joeys admitted at a wildlife hospital in New South Wales, Australia. The samples were processed and analysed for faecal cortisol metabolites (FCM) using a polyclonal R4866 cortisol enzyme-immunoassay which has been previously biologically validated in adult koalas. The results indicated that there was significant inter-individual variation in FCM concentrations among the joeys, however, these differences were not based on the sex of the joeys. The average FCM concentration among joeys varied from 18.34 to 44.18 ng/g. Our study provides the first record of physiological stress in male and female rescued koala joeys by indexing FCM concentrations during rehabilitation.
Keywords: cortisol, enzyme-immuno assay, faeces, glucocorticoids, joey, koala, rehabilitation, stress.
References
Barker, C. J., Gillett, A., Polkinghorne, A., and Timms, P. (2013). Investigation of the koala (Phascolarctos cinereus) hindgut microbiome via 16S pyrosequencing. Veterinary Microbiology 167, 554–564.| Investigation of the koala (Phascolarctos cinereus) hindgut microbiome via 16S pyrosequencing.Crossref | GoogleScholarGoogle Scholar |
Burton, E., and Tribe, A. (2016). The rescue and rehabilitation of koalas (Phascolarctos cinereus) in Southeast Queensland. Animals 6, 56.
| The rescue and rehabilitation of koalas (Phascolarctos cinereus) in Southeast Queensland.Crossref | GoogleScholarGoogle Scholar |
Charalambous, R., and Narayan, E. (2020). A 29-year retrospective analysis of koala rescues in New South Wales, Australia. PLoS One 15, e0239182.
| A 29-year retrospective analysis of koala rescues in New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |
Charalambous, R., Simonato, T., Peel, M., and Narayan, E. J. (2021). Physiological stress in rescued wild koalas (Phascolarctos cinereus) being held in a rehabilitation sanctuary: a pilot study. Animals 11, 2864.
| Physiological stress in rescued wild koalas (Phascolarctos cinereus) being held in a rehabilitation sanctuary: a pilot study.Crossref | GoogleScholarGoogle Scholar |
Cockrem, J. F. (2013). Individual variation in glucocorticoid stress responses in animals. General and Comparative Endocrinology 181, 45–58.
| Individual variation in glucocorticoid stress responses in animals.Crossref | GoogleScholarGoogle Scholar |
Coverdale, T. C., Herrmann, N. C., Altieri, A. H., and Bertness, M. D. (2013). Latent impacts: the role of historical human activity in coastal habitat loss. Frontiers in Ecology and the Environment 11, 69–74.
| Latent impacts: the role of historical human activity in coastal habitat loss.Crossref | GoogleScholarGoogle Scholar |
Crombie, A. C. (1947). Interspecific competition. The Journal of Animal Ecology 16, 44–73.
| Interspecific competition.Crossref | GoogleScholarGoogle Scholar |
Davies, N., Gillett, A., McAlpine, C., Seabrook, L., Baxter, G., Lunney, D., and Bradley, A. (2013a). The effect of ACTH upon faecal glucocorticoid excretion in the koala. Journal of Endocrinology 219, 1–12.
| The effect of ACTH upon faecal glucocorticoid excretion in the koala.Crossref | GoogleScholarGoogle Scholar |
Davies, N. A., Gramotnev, G., McAlpine, C., Seabrook, L., Baxter, G., Lunney, D., Rhodes, J. R., and Bradley, A. (2013b). Physiological stress in koala populations near the arid edge of their distribution. PLoS One 8, e79136.
| Physiological stress in koala populations near the arid edge of their distribution.Crossref | GoogleScholarGoogle Scholar |
DCCEEW (2022). Koala listing under national environmental law. Available at https://www.dcceew.gov.au/environment/biodiversity/threatened/species/koala#:~:text=The%20koala%20(combined%20populations%20of,have%20any%20impacts%20to%20koalas [accessed 12 August 2022].
Evans, N., Narayan, E. J., and Hero, J.-M. (2013). Effects of natural weathering conditions on faecal cortisol metabolite measurements in the greater bilby (Macrotis lagotis). Australian Journal of Zoology 61, 351–356.
| Effects of natural weathering conditions on faecal cortisol metabolite measurements in the greater bilby (Macrotis lagotis).Crossref | GoogleScholarGoogle Scholar |
Gallini, S. H., Di Girolamo, N., Hann, E., Paluch, H., and DiGeronimo, P. M. (2021). Outcomes of 4819 cases of marine animals presented to a wildlife rehabilitation center in New Jersey, USA (1976–2016). Scientific Reports 11, 2182.
| Outcomes of 4819 cases of marine animals presented to a wildlife rehabilitation center in New Jersey, USA (1976–2016).Crossref | GoogleScholarGoogle Scholar |
Garcês, A., Pires, I., Pacheco, F., Fernandes, L. S., Soeiro, V., Lóio, S., Prada, J., Cortes, R., and Queiroga, F. (2019). Natural and anthropogenic causes of mortality in wild birds in a wildlife rehabilitation centre in northern Portugal: a ten-year study. Bird Study 66, 484–493.
| Natural and anthropogenic causes of mortality in wild birds in a wildlife rehabilitation centre in northern Portugal: a ten-year study.Crossref | GoogleScholarGoogle Scholar |
Gaston, K. J., Blackburn, T. M., and Goldewijk, K. K. (2003). Habitat conversion and global avian biodiversity loss. Proceedings of the Royal Society of London. Series B: Biological Sciences 270, 1293–1300.
| Habitat conversion and global avian biodiversity loss.Crossref | GoogleScholarGoogle Scholar |
Gipp, G. (2004). ‘Handraising orphaned koalas’. pp. 1–13. (Wildcare Australia.) Available at https://www.awrc.org.au/uploads/5/8/6/6/5866843/nwcc-gipp-040726.pdf?fbclid=IwAR03XObcwQZX0VoRVYplB3gRzGfDftG1dWYfetkd7sD5FZQNA2JbC7SYW3s [accessed 13 August 2021].
Gonzalez-Astudillo, V., Allavena, R., McKinnon, A., Larkin, R., and Henning, J. (2017). Decline causes of Koalas in South East Queensland, Australia: a 17-year retrospective study of mortality and morbidity. Scientific Reports 7, 42587.
| Decline causes of Koalas in South East Queensland, Australia: a 17-year retrospective study of mortality and morbidity.Crossref | GoogleScholarGoogle Scholar |
Goudie, A. S. (2018). ‘Human Impact on the Natural Environment.’ (John Wiley & Sons, Incorporated: Newark, UK.)
Griffith, J. E., Dhand, N. K., Krockenberger, M. B., and Higgins, D. P. (2013). A retrospective study of admission trends of koalas to a rehabilitation facility over 30 years. Journal of Wildlife Diseases 49, 18–28.
| A retrospective study of admission trends of koalas to a rehabilitation facility over 30 years.Crossref | GoogleScholarGoogle Scholar |
Hautier, Y., Tilman, D., Isbell, F., Seabloom, E. W., Borer, E. T., and Reich, P. B. (2015). Anthropogenic environmental changes affect ecosystem stability via biodiversity. Science 348, 336–340.
| Anthropogenic environmental changes affect ecosystem stability via biodiversity.Crossref | GoogleScholarGoogle Scholar |
Kalman, B., and Levigne, H. (2002). ‘The Life Cycle of a Koala.’ (Crabtree Publishing Company.)
Keay, J. M., Singh, J., Gaunt, M. C., and Kaur, T. (2006). Fecal glucocorticoids and their metabolites as indicators of stress in various mammalian species: a literature review. Journal of Zoo and Wildlife Medicine 37, 234–244.
| Fecal glucocorticoids and their metabolites as indicators of stress in various mammalian species: a literature review.Crossref | GoogleScholarGoogle Scholar |
Lloyd, J. K. F. (2017). Minimising stress for patients in the veterinary hospital: why it is important and what can be done about it. Veterinary Sciences 4, 22.
| Minimising stress for patients in the veterinary hospital: why it is important and what can be done about it.Crossref | GoogleScholarGoogle Scholar |
Machado, P. M., Suciu, M. C., Costa, L. L., Tavares, D. C., and Zalmon, I. R. (2017). Tourism impacts on benthic communities of sandy beaches. Marine Ecology 38, e12440.
| Tourism impacts on benthic communities of sandy beaches.Crossref | GoogleScholarGoogle Scholar |
Mantyka-pringle, C. S., Martin, T. G., and Rhodes, J. R. (2012). Interactions between climate and habitat loss effects on biodiversity: a systematic review and meta-analysis. Global Change Biology 18, 1239–1252.
| Interactions between climate and habitat loss effects on biodiversity: a systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Molina-López, R. A., Casal, J., and Darwich, L. (2011). Causes of morbidity in wild raptor populations admitted at a wildlife rehabilitation centre in Spain from 1995-2007: a long term retrospective study. PLoS One 6, e24603.
| Causes of morbidity in wild raptor populations admitted at a wildlife rehabilitation centre in Spain from 1995-2007: a long term retrospective study.Crossref | GoogleScholarGoogle Scholar |
Morris, K. M., O’Meally, D., Zaw, T., Song, X., Gillett, A., Molloy, M. P., Polkinghorne, A., and Belov, K. (2016). Characterisation of the immune compounds in koala milk using a combined transcriptomic and proteomic approach. Scientific Reports 6, 35011.
| Characterisation of the immune compounds in koala milk using a combined transcriptomic and proteomic approach.Crossref | GoogleScholarGoogle Scholar |
Munro, C., and Stabenfeldt, G. (1985). ‘Development of a cortisol enzyme-immunoassay in plasma, Clinical Chemistry.’ (American Association for Clinical Chemistry: Washington, DC, USA.)
Narayan, E. (2019). Physiological stress levels in wild koala sub-populations facing anthropogenic induced environmental trauma and disease. Scientific Reports 9, 6031.
| Physiological stress levels in wild koala sub-populations facing anthropogenic induced environmental trauma and disease.Crossref | GoogleScholarGoogle Scholar |
Narayan, E., and Vanderneut, T. (2019). Physiological stress in rescued wild koalas are influenced by habitat demographics, environmental stressors, and clinical intervention. Frontiers in Endocrinology 10, 18.
| Physiological stress in rescued wild koalas are influenced by habitat demographics, environmental stressors, and clinical intervention.Crossref | GoogleScholarGoogle Scholar |
Narayan, E. J., and Williams, M. (2016). Understanding the dynamics of physiological impacts of environmental stressors on Australian marsupials, focus on the koala (Phascolarctos cinereus). BMC Zoology 1, 2.
| Understanding the dynamics of physiological impacts of environmental stressors on Australian marsupials, focus on the koala (Phascolarctos cinereus).Crossref | GoogleScholarGoogle Scholar |
Narayan, E. J., Webster, K., Nicolson, V., Mucci, A., and Hero, J. -M. (2013). Non-invasive evaluation of physiological stress in an iconic Australian marsupial: the Koala (Phascolarctos cinereus). General and Comparative Endocrinology 187, 39–47.
| Non-invasive evaluation of physiological stress in an iconic Australian marsupial: the Koala (Phascolarctos cinereus).Crossref | GoogleScholarGoogle Scholar |
Pahuja, H. K., and Narayan, E. J. (2023a). Comparing the agreement of a commercial cortisol kit with a biologically validated assay in evaluating faecal cortisol metabolite levels in koala joeys. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 276, 111353.
| Comparing the agreement of a commercial cortisol kit with a biologically validated assay in evaluating faecal cortisol metabolite levels in koala joeys.Crossref | GoogleScholarGoogle Scholar |
Pahuja, H. P., and Narayan, E. J. (2023b). An 8-year long retrospective analysis identifies the major causes of morbidity and mortality in rescued koala joeys. Wildlife Research , .
| An 8-year long retrospective analysis identifies the major causes of morbidity and mortality in rescued koala joeys.Crossref | GoogleScholarGoogle Scholar |
Pardini, R., Nichols, E., and Püttker T. (2017). Biodiversity response to habitat loss and fragmentation. In ‘Encyclopedia of the Anthropocene. Vol. 3’. (Eds D. A. Dellasala, M. I. Goldstein.) pp. 229–239. (Elsevier: Oxford, UK.)
Parmesan, C. (2006). Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics 37, 637–669.
| Ecological and evolutionary responses to recent climate change.Crossref | GoogleScholarGoogle Scholar |
Rytwinski, T., and Fahrig, L. (2012). Do species life history traits explain population responses to roads? A meta-analysis. Biological Conservation 147, 87–98.
| Do species life history traits explain population responses to roads? A meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Santamaria, F., Palme, R., Schlagloth, R., Klobetz-Rassam, E., and Henning, J. (2021a). Seasonal variations of faecal cortisol metabolites in koalas in south east Queensland. Animals 11, 1622.
| Seasonal variations of faecal cortisol metabolites in koalas in south east Queensland.Crossref | GoogleScholarGoogle Scholar |
Santamaria, F., Schlagloth, R., Palme, R., and Henning, J. (2021b). Over time decay of cortisol metabolites in faecal pellets of koalas in central Queensland. Animals 11, 3376.
| Over time decay of cortisol metabolites in faecal pellets of koalas in central Queensland.Crossref | GoogleScholarGoogle Scholar |
Schenk, A. (2017). Causes of morbidity and mortality of wildlife species presented to a wildlife clinic in east Tennessee, USA, 2000–2011. Journal of Veterinary Science & Animal Husbandry 5, 404.
| Causes of morbidity and mortality of wildlife species presented to a wildlife clinic in east Tennessee, USA, 2000–2011.Crossref | GoogleScholarGoogle Scholar |
Short, F. T., and Burdick, D. M. (1996). Quantifying eelgrass habitat loss in relation to housing development and nitrogen loading in Waquoit Bay, Massachusetts. Estuaries 19, 730–739.
| Quantifying eelgrass habitat loss in relation to housing development and nitrogen loading in Waquoit Bay, Massachusetts.Crossref | GoogleScholarGoogle Scholar |
Taylor-Brown, A., Booth, R., Gillett, A., Mealy, E., Ogbourne, S. M., Polkinghorne, A., and Conroy, G. C. (2019). The impact of human activities on Australian wildlife. PLoS One 14, e0206958.
| The impact of human activities on Australian wildlife.Crossref | GoogleScholarGoogle Scholar |
Valiela, I., Lloret, J., Bowyer, T., Miner, S., Remsen, D., Elmstrom, E., Cogswell, C., and Robert Thieler, E. (2018). Transient coastal landscapes: rising sea level threatens salt marshes. Science of the Total Environment 640–641, 1148–1156.
| Transient coastal landscapes: rising sea level threatens salt marshes.Crossref | GoogleScholarGoogle Scholar |
Webster, K., Narayan, E., and De Vos, N. (2017). Fecal glucocorticoid metabolite response of captive koalas (Phascolarctos cinereus) to visitor encounters. General and Comparative Endocrinology 244, 157–163.
| Fecal glucocorticoid metabolite response of captive koalas (Phascolarctos cinereus) to visitor encounters.Crossref | GoogleScholarGoogle Scholar |
Woinarski, J., and Burbidge, A. A. (2020). Phascolarctos cinereus. The IUCN Red List of Threatened Species e.T16892A166496779. Available at
| Crossref | [accessed 12 August 2021].
