Abstract
There is growing recognition that ecological research must expand its focus beyond inference based on pattern-process relationships to the direct measurement of ecological and physiological processes. Physiological assessment is important because vertebrates cope with unpredictable and noxious stimuli by initiating a stress response. However, an over-activation of the acute stress response by numerous novel and potentially stressful anthropogenic pressures, including those associated with urban edges, has the potential to generate chronic stress and a greater susceptibility to disease, reduce fecundity and survivorship. An individual’s physiological response to edge habitats with varying degrees of contrast to the adjacent disturbed urban matrix (e.g. major vs. minor roads), may provide insight into their survival likelihood in fragmented urban landscapes. Although demographic changes in wildlife resulting from urbanization have been documented, only recently have physiological consequences been examined. We addressed this problem using a case study of the squirrel glider (Petaurus norfolcensis) in the fragmented urban landscape of southeast Queensland, Australia. Hair samples were used to enable a comparison of hair cortisol levels in individual squirrel gliders, providing an indication of potential stress. We applied a linear mixed-effect modeling approach clustered by patch to quantify the influence of site-level habitat factors and relative abundance comparative to edge contrast on hair cortisol levels. We found that edge type had a strong positive effect on hair cortisol levels; but this depended on the availability of abundant nest hollows at a site. We conclude that individual hair cortisol concentration, providing an index of stress, was lowest in interior habitats and highest in edge habitats adjacent to major roads. Furthermore, gliders occupying low edge contrast habitats adjacent to residential areas and minor roads, and containing abundant tree nest hollows, had low-moderate hair cortisol levels. This highlights the potential importance of these habitats for the conservation of arboreal mammals such as the squirrel glider in urban landscapes.
Similar content being viewed by others
References
Ahlering MA, Millspaugh JJ, Woods RJ, Western D, Eggert LS (2011) Elevated levels of stress hormones in crop-raiding male elephants. Anim Conserv 14:124–130
Akaike H (1983) Information measures and model selection, vol 44. International Statistical Institute, Madrid, pp 277–291
Arlettaz R, Patthey P, Baltic M, Leu T, Schaub M, Palme R, Jenni-Eiermann S (2007) Spreading free-riding snow sports represent a novel serious threat for wildlife. Proc R Soc B 274:1219–1224
Australian Bureau of Statistics (2012) 3218.0—Regional population growth, Australia, 2010–11. Australian Bureau of Statistics. http://www.abs.gov.au/ausstats/abs@.nsf/Products/3218.0~2010-11~Main+Features~Queensland?OpenDocument. Accessed 11 May 2012
Baker PJ, Harris S (2007) Urban mammals: what does the future hold? An analysis of the factors affecting patterns of use of residential gardens in Great Britain. Mamm Rev 37:297–315
Ball TM, Goldingay RL (2008) Can wooden poles be used to reconnect habitat for a gliding mammal? Landsc Urban Plan 87:140–146
Ball T, Adams E, Goldingay RL (2010) Diet of the squirrel glider in a fragmented landscape near Mackay, central Queensland. Aust J Zool 57:295–304
Bell SL (2005) The squirrel glider: Petaurus norfolcensis. Ecophysiology, reproduction and social behaviour of island populations. Honours Thesis 2005, The University of Queensland, Brisbane
Beyer GL, Goldingay RL, Sharpe DJ (2008) The characteristics of squirrel glider (Petaurus norfolcensis) den trees in subtropical Australia. Aust J Zool 56:13–21
Booth GD, Niccolucc, MJ, Schuster EG (1994) Identifying proxy sets in multiple linear regression: an aid to better coefficient interpretation. Research paper INT-470, United States Department of Agriculture, Forest Service, Ogden
Bradley AJ, Stoddart DM (1992) Seasonal changes in plasma androgens, glucocorticoids and glucocorticoid-binding proteins in the marsupial sugar glider Petaurus breviceps. J Endocrinol 132:21–31
Bradley AJ, Stoddart DM (1993) The dorsal paracloacal gland and its relationship with seasonal changes in cutaneous gland morphology and plasma androgen in the marsupial sugar glider (Petaurus breviceps; Marsupialia: Petauridae). J Zool (Lond) 229:331–346
Bradley AJ, Stoddart DM (1997) Plasma androgen, social position, and response to GnRH in the marsupial sugar glider Petaurus breviceps (Marsupialia: Petauridae). J Zool (Lond) 241:579–587
Brearley GK (2004) Physiological, morphological, behavioural and demographic changes during the life history of island populations of the squirrel glider (Petaurus norfolcensis). Honours Thesis 2004, The University of Queensland, Brisbane
Brearley G, Bradley A, Bell S, McAlpine C (2010) Influence of contrasting urban edges on the abundance of arboreal mammals: a study of squirrel gliders (Petaurus norfolcensis) in southeast Queensland, Australia. Biol Conserv 143:60–71
Brearley G, Bradley A, Bell S, McAlpine C (2011a) Change in habitat resources and structure near urban edges and its influence on the squirrel glider (Petaurus norfolcensis) in southeast Queensland, Australia. Austral Ecol 36(4):425–432
Brearley G, McAlpine C, Bell S, Bradley A (2011b) Squirrel glider (Petaurus norfolcensis) home-ranges near urban edges in eastern Australia. J Zool (Lond) 285(4):256–265
Burger J, Bowman R, Woolfenden GE, Gochfeld M (2004) Metal and metalloid concentrations in the eggs of threatened Florida scrubjays in suburban habitat from south-central Florida. Sci Total Environ 328:185–193
Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a Practical Information-Theoretic Approach, 2nd edn. Springer, New York
Busch SD, Hayward LS (2009) Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables. Biol Conserv 142:2844–2853
Chen J, Franklin JF, Spies TA (1992) Vegetation responses to edge environments in old-growth Douglas-Fir forests. Ecol Appl 2:387–396
Coffin AW (2007) From road kill to road ecology: a review of the ecological effects of roads. J Transp Geogr 15:396–406
Creel S, Fox JE, Hardy A, Sands J, Garrott B, Peterson RO (2002) Snowmobile activity and glucocorticoid stress responses in wolves and elk. Conserv Biol 16:809–814
Crino OL, Van Oorschot BK, Johnson EE, Malisch JL, Breuner CW (2011) Proximity to a high traffic road: glucocorticoid and life history consequences for nestling white-crowned sparrows. Gen Comp Endocrinol 173:323–332
Davenport MD, Tiefenbacher S, Lutz CK, Novak MA, Meyer JS (2006) Analysis of endogenous cortisol levels in the hair of rhesus macaques. Gen Comp Endocrinol 147:255–261
Dobson M, Goldingay RL, Sharpe DJ (2005) Feeding behaviour of the squirrel glider in remnant habitat in Brisbane. Aust Mammal 27:27–35
Dowding CV, Harris S, Poulton S, Baker PJ (2010) Nocturnal ranging behavior of urban hedgehogs, Erinaceua europaeus, in relation to risk and rewards. Anim Behav 80:13–21
Eby P, Law B (2008) Ranking the feeding habitat of Grey-headed flying foxes for conservation management. Department of Environment and Climate Change (NSW), Sydney
Ellenberg U, Setiawan AN, Cree A, Houston DM, Seddon PJ (2007) Elevated hormonal stress response and reduced reproductive output in Yellow-eyed penguins exposed to unregulated tourism. Gen Comp Endocrinol 152:54–63
Fernandez-Juricic E (2002) Can human disturbance promote nestedness? A case study with breeding birds in urban habitat fragments. Oecologia 131:269–278
Fowler GS (1999) Behavioral and hormonal responses of Magellanic Penguins (Spheniscus magellanicus) to tourism and nest site visitation. Biol Conserv 90:143–149
French SS, Fokidis BH, Moore MC (2008) Variation in stress and innate immunity in the tree lizard (Urosaurus ornatus) across an urban-rural gradient. J Comp Physiol B 178:997–1005
Fuentes-Montemayor E, Cuaron AD, Vazquez-Dominguez E, Benitez-Malvido J, Valenzuela-Galvan D, Andresen E (2009) Living on the edge: roads and edge effects on small mammals populations. J Anim Ecol 78:857–865
Gibbons P, Lindenmayer D (2002) Tree hollows and wildlife conservation in Australia. CSIRO Publishing, Collingwood
Goldingay RL, Sharpe DJ (2004) How do we conserve the squirrel glider in Brisbane’s urban matrix? In: Lunney D (ed) Conservation of Australia’s forest fauna, 2nd edn. Royal Zoological Society of New South Wales, Mosman, pp 663–677
Goldingay RL, Taylor BD (2009) Gliding performance and its relevance to gap crossing by the squirrel glider (Petaurus norfolcensis). Aust J Zool 57:99–104
Goldingay RL, Sharpe DJ, Beyer GL, Dobson M (2006) Using ecological studies to understand the conservation needs of the squirrel glider in Brisbane’s urban-forest remnants. Aust Mammal 28:173–186
Goosem M (2000) Effects of tropical rainforest roads on small mammals: edge changes in community composition. Wildl Res 27:151–163
Higham JP, Vitale AB, Rivera AM, Ayala JE, Maestripieri D (2010) Measuring salivary analytes from free-ranging monkeys. Physiol Behav 101:601–607
Hoeting JA, Madigan D, Raftery AE, Volinsky CT (1999) Bayesian model averaging: a tutorial (with discussion). Stat Sci 14:382–417
Hopkins WA, Mendonca MT, Congdon JD (1997) Increased circulating levels of testosterone and corticosterone in southern toads, Bufo terrestris, exposed to coal combustion waste. Gen Comp Endocrinol 108:237–246
Hurvich CM, Tsai C-L (1989) Regression and time series model selection in small samples. Biometrika 76:297–307
Johnstone CP, Lill A, Reina RD (2011) Response of the agile antechinus to habitat edge, configuration and condition in fragmented forest. PLoS ONE 6(11):1–15
Johnstone CP, Lill A, Reina RD (2012) Does habitat fragmentation cause stress in the agile antechinus? A haematological approach. J Comp Physiol B 182:139–155
Koren L, Mokady O, Karaskov T, Klein J, Koren G, Geffen E (2002) A novel method using hair for determining hormonal levels in wildlife. Anim Behav 63:403–406
Lane J (2006) Can non-invasive glucocorticoid measures be used as reliable indicators of stress in animals. Anim Welf 15:331–342
Law B, Mackowski C, Schoer L, Tweedie T (2000) Flowering phenology of myrtaceous trees and their climatic, environmental and disturbance variables in northern New South Wales. Austral Ecol 25(2):160–178
Mallick J, Stoddart DM, Jones I, Bradley AJ (1994) Behavioural and endocrinological correlates of social status in the male sugar glider (Petaurus breviceps Marsupialia: Petauridae). Physiol Behav 55:1131–1134
Marra PP, Holberton RL (1998) Corticosterone levels as indicators of habitat quality: effects of habitat segregation in a migratory bird during the non-breeding season. Oecologia 116:284–292
Martin JGA, Reale D (2006) Animal temperament and human disturbance: implications for the responses of wildlife to tourism. Behav Process 77:66–72
Martínez-Mota R, Valdespino C, Sánchez-Ramos MA, Serio-Silva JC (2007) Effects of forest fragmentation on the physiological stress response of black howler monkeys. Anim Conserv 10:374–379
McAlpine CA, Rhodes JR, Callaghan JG, Bowen ME, Lunney D, Mitchell DL, Pullar DV, Possingham HP (2006) The importance of forest area and configuration relative to local habitat factors for conserving forest mammals: a case study of koalas in Queensland, Australia. Biol Conserv 132:153–165
McCall SC, McCarthy MA, van der Ree R, Harper MJ, Cesarini S, Soanes K (2010) Evidence that a highway reduced the apparent survival rates of squirrel gliders, Ecol Soc 15(3):Article 27
McDonald RA, Gelehrter TD (1981) Glucocorticoid regulation of amino-acid transport in anucleate rat hepatmoa (HTC) cells. J Cell Biol 88:536–542
McLean MA, Angilletta MJ, Williams KS (2005) If you can’t stand the heat, stay out of the city: thermal reaction norms of chitinolytic fungi in an urban heat island. J Therm Biol 30:384–391
Millis AL (2000) Reproduction and sociality in the marsupial squirrel glider (Petaurus norfolcensis) in south east Queensland; with notes on the sugar glider (Petaurus breviceps). PhD Thesis, University of Queensland, Brisbane
Millspaugh JJ, Woods RJ, Hunt KE, Raedeke KJ, Brundige GC, Washburn BE, Wasser SK (2001) Fecal glucocorticoid assays and the physiological stress response in elk. Wildl Soc Bull 29:899–907
Mooney HA, Hobbs RJ (eds) (2000) Invasive species in a changing world. Island Press, Washington, DC
Mullner A, Linsenmair KE, Wikelski M (2004) Exposure to ecotourism reduces survival and affects stress response in hoatzin chicks (Opisthocomus hoazin). Biol Conserv 118:549–558
Oddie CJ, Blaine EH, Bradshaw SD, Coghlan JP, Denton DA, Nelson JF, Scoggins BA (1976) Blood Corticosteroids in Australian marsupial and placental mammals and one monotreme. J Endocrinol 69:341–348
Partecke J, Schwabl I, Gwinner E (2006) Stress and the city: urbanization and its effects on the stress physiology in European Blackbirds. Ecology 87:1945–1952
Queensland Museum (1995) Wildlife of greater Brisbane. Queensland Museum, Brisbane
Quin DG (1995) Population ecology of the squirrel glider (Petaurus norfolcensis) and the sugar glider (Petaurus breviceps) (Marsupialia: Petauridae) at Limeburners Creek, on the central north coast of New South Wales. Wildl Res 22:471–505
Romero ML (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255
Romero ML, Wikelski M (2002) Exposure to tourism reduces stress-induced corticosterone levels in Galapagos marine iguanas. Biol Conserv 108:371–374
Rowston C, Catterall CP, Hurst C (2002) Habitat preferences of squirrel gliders, Petaurus norfolcensis, in the fragmented landscape of south-east Queensland. For Ecol Manag 164:197–209
Rytwinski T, Fahrig L (2007) Effect of road density on abundance of white-footed mice. Landscape Ecol 22:1501–1512
Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89
Sharpe DJ, Goldingay RL (1998) Feeding behaviour of the squirrel glider at Bungawalbin Nature Reserve, north-eastern New South Wales. Wildl Res 25:243–254
Sharpe DJ, Goldingay RL (2007) Home range of the Australian squirrel glider, Petaurus norfolcensis (Diprotodontia). J Mammal 88:1515–1522
Sharpe DJ, Goldingay RL (2010) Population ecology of the nectar-feeding squirrel glider (Petaurus norfolcensis) in remnant forest in subtropical Australia. Wildl Res 37:77–88
Sheriff MJ, Krebs CJ, Boonstra R (2010) Assessing stress in animal populations: do fecal and plasma glucocorticoids tell the same story? Gen Comp Endocrinol 166(3):614–619
Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R (2011) Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166(4):869–887
Stoddart MD, Bradley AJ (1991) Measurement of short term changes in heart rate and in plasma concentrations of cortisol and catecholamine in a small marsupial. J Chem Ecol 17:1333–1341
Stoddart MD, Bradley AJ, Mallick J (1994) Plasma testosterone concentration, body weight, social dominance and scent marking in male marsupial sugar gliders (Petaurus breviceps; Marsupialia: Petauridae). J Zool (Lond) 232:595–601
Suckling GC (1984) Population ecology of the sugar glider, Petaurus breviceps, in a system of fragmented habitats. Aust Wildl Res 11:49–75
Suorsa P, Huhta E, Nikula A, Nikinmaa M, Jantti A, Helle H, Hakkarainen H (2003) Forest management is associated with physiological stress in an old growth forest passerine. Proc R Soc B 270:963–969
van der Ree R (2002) The population ecology of the squirrel glider (Petaurus norfolcensis) within a network of remnant linear habitats. Wildl Res 29:329–340
van der Ree R (2006) Road upgrade in Victoria a filter to the movement of the endangered squirrel glider (Petaurus norfolcensis): results of a pilot study. Ecol Manag Restor 7(3):226–228
van der Ree R, Cesarini S, Sunnucks P, Moore JL, Taylor A (2010) Large gaps in canopy reduce road crossing by a gliding mammal. Ecol Soc 15(4):Article 35
Van Meter PE, French JA, Dloniak SM, Watts HE, Kolowski JM, Holekamp KE (2009) Fecal glucocorticoids reflect socio-ecological and anthropogenic stressors in the lives of wild spotted hyenas. Horm Behav 55:329–337
Walker B, Boersma P, Wingfield J (2005) Physiological and behavioural differences in Magellanic Penguin chicks in undisturbed and tourist-visited locations of a colony. Conserv Biol 19:1571–1577
Walker B, Boersma P, Wingfield J (2006) Habituation of adult Magellanic Penguins to human visitation as expressed through behaviour and corticosterone secretion. Conserv Biol 20:146–154
Wasser SK, Bevis K, King G, Hanson E (1997) Noninvasive physiological measures of disturbance in the Northern Spotted Owl. Conserv Biol 11:1019–1022
Yang HL, Lan J, Meng YJ, Wan XJ, Han DW (1998) A preliminary study of steroid hormones in human hair. J Steroid Biochem Mol Biol 67:447–450
Acknowledgments
We gratefully acknowledge the generous support of the Winifred Violet Scott Estate, the Queensland Environmental Protection Agency and the Logan City Council for funding this study. We would particularly like to thank Peggy Eby and Brad Law for their assistance with data collaboration, along with Jim Napier, Michael Anderson and the Logan City Council staff for their constant support with field surveys. Many thanks also to the numerous volunteers who helped with the field surveys.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Brearley, G., McAlpine, C., Bell, S. et al. Influence of urban edges on stress in an arboreal mammal: a case study of squirrel gliders in southeast Queensland, Australia. Landscape Ecol 27, 1407–1419 (2012). https://doi.org/10.1007/s10980-012-9790-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10980-012-9790-8