Does habitat fragmentation cause stress in the agile antechinus? A haematological approach

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 182, Issue 1, 2012, Pages 139-155

  Johnstone, Christopher P ^a   Lill, Alan ^a   Reina, Richard D ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Antechinus agilis; Neutrophil lymphocyte ratio; Physiological stress; Repeatability; Small mammal

Indexed keywords

HEMOGLOBIN;

ANIMAL; ARTICLE; AUSTRALIA; BLOOD; ECOSYSTEM; EOSINOPHIL; ERYTHROCYTE; HEMATOCRIT; HYPOPHYSIS ADRENAL SYSTEM; LEUKOCYTE COUNT; LYMPHOCYTE COUNT; MARSUPIAL; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; TREE;

ANIMALS; ECOSYSTEM; EOSINOPHILS; ERYTHROCYTES; HEMATOCRIT; HEMOGLOBINS; LEUKOCYTE COUNT; LYMPHOCYTE COUNT; MARSUPIALIA; PITUITARY-ADRENAL SYSTEM; SOUTH AUSTRALIA; STRESS, PHYSIOLOGICAL; TREES;

ANTECHINUS; ANTECHINUS AGILIS; MAMMALIA; VERTEBRATA;

EID: 80455178297     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-011-0598-7     Document Type: Article

References (102)

1. Austad SN (1996) The uses of intraspecific variation in aging research. Exp Gerontol 31: 453-463.
2. Australian Bureau of Meteorology 2009. Climate statistics for Australian sites. In: (http://www. bom. gov. au/).
3. Baker ML, Gemmell RT (1999) Physiological changes in the brushtail possum (Trichosurus vulpecula) following relocation from Armidale to Brisbane, Australia. J Exp Zool 284: 42-49.
4. Baker ML, Gemmell E, Gemmell RT (1998) Physiological changes in brushtail possums, Trichosurus vulpecula, transferred from the wild to captivity. J Exp Zool 280: 203-212.
5. Banks PB, Dickman CR (2000) Effects of winter food supplementation on reproduction, body mass, and numbers of small mammals in montane Australia. Can J Zool 78: 1775-1783.
6. Banks SC, Finlayson GR, Lawson SJ, Lindenmayer DB, Paetkau D, Ward SJ, Taylor AC (2005) The effects of habitat fragmentation due to forestry plantation establishment on the demography and genetic variation of a marsupial carnivore, Antechinus agilis. Biol Conserv 122: 581-597.
7. Barker IK, Beveridge I, Bradley AJ, Lee AK (1978) Observations on spontaneous stress-related mortality among males of the Dasyurid marsupial Antechinus stuartii Macleay. Aust J Zool 26: 435-447.
8. Barnett JL (1973) A stress response in Antechinus stuartii (Macleay). Aust J Zool 21: 501-513.
9. Barnett JL, How RA, Humphreys WF (1979) Blood parameters in natural populations of Trichosurus species (Marsupialia: Phalangeridae). II. Influence of habitat and population strategies of T. caninus and T. vulpecula. Aust J Zool 27: 927-938.
10. Bearhop G, Orr F (1999) Mean corpuscular volume (MCV) as a measure of condition in birds. Ecol Lett 2: 352-356.
11. Beldomenico PM, Telfer S, Gebert S, Lukomski L, Bennett M, Begon M (2008a) The dynamics of health in wild field vole populations: a haematological perspective. J Anim Ecol 77: 984-997.
12. Beldomenico PM, Telfer S, Gebert S, Lukomski L, Bennett M, Begon M (2008b) Poor condition and infection: a vicious circle in natural populations. Proc Royal Soc Lond Series B Biol Sci (Lond) 275: 1753-1759.
13. Bennett AF (1990) Habitat corridors and the conservation of small mammals in a fragmented forest environment. Landscape Ecol 4: 109-122.
14. Bennett A, Hayssen V (2010) Measuring cortisol in hair and saliva from dogs: coat color and pigment differences. Domest Anim Endocrinol 39: 171-180.
15. Bignold LP (1995) The eosinophil leukocyte: controversies of recruitment and function. Cell Mol Life Sci 51: 317-327.
16. Bradley AJ (2003) Stress, hormones and mortality in small carnivorous marsupials. In: Jones M, Dickman CR, Archer M (eds) Predators with pouches: the biology of carnivorous marsupials. CSIRO Publishing, Collingwood, pp 250-263.
17. Braithwaite RW, Lee AK (1979) A mammalian example of semelparity. Am Nat 113: 151-155.
18. Campbell TW (1995) Avian hematology and cytology. Iowa State University Press, Ames.
19. Catling PC, Burt RJ, Forrester RI (1998) Models of the distribution and abundance of ground-dwelling mammals in the eucalypt forests of south-eastern New South Wales. Wildl Res 25: 449-466.
20. Chapman CA, Wasserman MD, Gillespie TR, Speirs ML, Lawes MJ, Saj TL, Ziegler TE (2006) Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments? Am J Phys Anthropol 131: 525-534.
21. Cheal PD, Lee AK, Barnett JL (1976) Changes in the haematology of Antechinus stuartii (Marsupialia), and their association with male mortality. Aust J Zool 24: 299-311.
22. Claridge AW, Tennant P, Chick R, Barry SC (2008) Factors influencing the occurrence of small ground-dwelling mammals in southeastern mainland Australia. J Mammal 89: 916-923.
23. Clark P, Adlard RD (2004) Haematology of Australian mammals. Csiro.
24. Cockburn A, Lazenby-Cohen KA (1992) Use of nest trees by Antechinus stuartii, a semelparous lekking marsupial. J Zool (Lond) 226: 657-680.
25. Colombelli-Négrel D, Kleindorfer S (2008) In superb fairy wrens (Malurus cyaneus), nuptial males have more blood parasites and higher haemoglobin concentration than eclipsed males. Aust J Zool 56: 117-121.
26. Crawley MJ (2007) The R book. Wiley, Chichister.
27. Davies JB, Oates AM, Trumbull-Ward AV (2002) Ecological vegetation class mapping at 1: 25, 000 in Gippsland: final report. Victorian Department of Natural Resources and Environment, Melbourne.
28. Davis GS, Anderson KE, Carroll AS (2000) The effects of long-term caging and molt of single comb white leghorn hens on heterophil to lymphocyte ratios, corticosterone and thyroid hormones. Poult Sci 79: 514-518.
29. Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22: 760-772.
30. Delehanty B, Boonstra R (2009) Impact of live trapping on stress profiles of Richardson's ground squirrel (Spermophilus richardsonii). Gen Comp Endocrinol 160: 176-182.
31. Dhabhar F, McEwen B (1997) Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking. Brain Behav Immun 11: 286-306.
32. Dhabhar FS, Miller AH, Stein M, McEwen BS, Spencer RL (1994) Diurnal and acute stress-induced changes in distribution of peripheral blood leukocyte subpopulations. Brain Behav Immun 8: 66-79.
33. Dhabhar FS, Miller AH, McEwen BS, Spencer RL (1995) Effects of stress on immune cell distribution: dynamics and hormonal mechanisms. J Immunol 154: 5511-5527.
34. Dhabhar FS, Miller AH, McEwen BS, Spencer RL (1996) Stress-induced changes in blood leukocyte distribution. Role of adrenal steroid hormones. J Immunol 157: 1638-1644.
35. Dickman CR, Parnaby HE, Crowther MS, King DH (1998) Antechinus agilis (Marsupialia: Dasyuridae), a new species from the A. stuartii complex in south-eastern Australia. Aust J Zool 46: 1-26.
36. Dorshkind K (1990) Regulation of hemopoiesis by bone marrow stromal cells and their products. Annu Rev Immunol 111: 37.
37. Dunstan CE, Fox BJ (1996) The effects of fragmentation and disturbance of rainforest on ground-dwelling small mammals on the Robertson Plateau, New South Wales, Australia. J Biogeogr 23: 187-201.
38. Engqvist L (2005) The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70: 967-971.
39. Epel ES, Blackburn EH, Lin J, Dhabhar FS, Adler NE, Morrow JD, Cawthon RM (2004) Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci USA 101: 17312-17315.
40. Ewers RM, Didham RK (2005) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81: 117-142.
41. Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16: 265-280.
42. Fisher JW, Crook JJ (1962) Influence of several hormones on erythropoiesis and oxygen consumption in the hypophysectomized rat. Blood 19: 557-565.
43. Fletcher QE, Boonstra R (2006) Impact of live trapping on the stress response of the meadow vole (Microtus pennsylvanicus). J Zool 270: 473-478.
44. Good T, Khan MZ, Lynch JW (2003) Biochemical and physiological validation of a corticosteroid radioimmunoassay for plasma and fecal samples in oldfield mice (Peromyscus polionotus). Physiol Behav 80: 405-411.
45. Hainsworth FR, Stricker EM, Epstein AN (1968) Water metabolism of rats in the heat: dehydration and drinking. Am J Physiol 214: 983-989.
46. Holland GJ, Bennett AF (2007) Occurrence of small mammals in a fragmented landscape: the role of vegetation heterogeneity. Wildl Res 34: 387-397.
47. Holland GJ, Bennett AF (2009) Differing responses to landscape change: implications for small mammal assemblages in forest fragments. Biodivers Conserv 18: 2997-3016.
48. Homan RN, Regosin JV, Rodrigues DM, Reed JM, Windmiller BS, Romero LM (2003) Impacts of varying habitat quality on the physiological stress of spotted salamanders (Ambystoma maculatum). Anim Conserv 6: 11-18.
49. Homyack JA (2010) Evaluating habitat quality of vertebrates using conservation physiology tools. Wildl Res 37: 332-342.
50. Janin A, Lena JP, Joly P (2011) Beyond occurrence: Body condition and stress hormone as integrative indicators of habitat availability and fragmentation in the common toad. Biol Conserv. doi: 10. 1016/j. biocon. 2010. 12. 009.
51. Johnstone CP, Reina RD, Lill A (2010) Impact of anthropogenic habitat fragmentation on population health in a small, carnivorous marsupial. J Mammal 91: 1332-1341.
52. Johnstone CP, Lill A, Reina RD (2011) Response of the agile antechinus to habitat edge, configuration and condition in fragmented forest. PLoS One. Accepted pending revision.
53. Keay JM, Singh J, Gaunt MC, Kaur T (2006) Fecal glucocorticoids and their metabolites as indicators of stress in various mammalian species: a literature review. J Zoo Wildl Med 37: 234-244.
54. Kelly LT, Bennett AF (2008) Habitat requirements of the yellow-footed antechinus (Antechinus flavipes) in box-ironbark forest, Victoria, Australia. Wildl Res 35: 128-133.
55. King JM, Bradshaw SD (2010) Stress in an Island kangaroo? The Barrow Island euro, Macropus robustus isabellinus. Gen Comp Endocrinol 167: 60-67.
56. Kitaysky AS, Kitaiskaia EV, Piatt JF, Wingfield JC (2006) A mechanistic link between chick diet and decline in seabirds? Proc Royal Soc B Biol Sci 273: 445.
57. Knight EH, Fox BJ (2000) Does habitat structure mediate the effects of forest fragmentation and human-induced disturbance on the abundance of Antechinus stuartii? Aust J Zool 48: 577-595.
58. Lazenby-Cohen KA, Cockburn A (1991) Social and foraging components of the home range in Antechinus stuartii (Dasyuridae: Marsupialia). Aust J Ecol 16: 301-307.
59. Le Maho Y, Karmann H, Briot D, Handrich Y, Robin JP, Mioskowski E, Cherel Y, Farni J (1992) Stress in birds due to routine handling and a technique to avoid it. Am J Physiol Regul Intergrative Comp Physiol (Am J Physiol Regul Integr Comp Physiol) 263: 775-781.
60. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104: 116-121.
61. Lewis SM, Bain BJ, Bates I, Dacie JV (2006) Dacie and Lewis practical haematology. Churchill Livingstone, London.
62. Liu J, Mori A (1999) Stress, aging, and brain oxidative damage. Neurochem Res 24: 1479-1497.
63. Lucas JR, Freeberg TM, Egbert J, Schwabl H (2006) Fecal corticosterone, body mass, and caching rates of Carolina chickadees (Poecile carolinensis) from disturbed and undisturbed sites. Horm Behav 49: 634-643.
64. Lynn SE, Porter AJ (2008) Trapping initiates stress response in breeding and non-breeding house sparrows Passer domesticus: implications for using unmonitored traps in field studies. J Avian Biol 39: 87-94.
65. Mac Nally R, Bennett AF (1997) Species-specific predictions of the impact of habitat fragmentation: local extinction of birds in the box-ironbark forests of central Victoria, Australia. Biol Conserv 82: 147-155.
66. Mac Nally R, Horrocks G (2002) Habitat change and restoration: responses of a forest-floor mammal species to manipulations of fallen timber in floodplain forests. Animal Biodivers Conserv 25: 41-52.
67. Mac Nally R, Bennett AF, Horrocks G (2000) Forecasting the impacts of habitat fragmentation. Evaluation of species-specific predictions of the impact of habitat fragmentation on birds in the box-ironbark forests of central Victoria, Australia. Biol Conserv 95: 7-29.
68. Martin RW, Handasyde KA, Skerratt LF (1998) Current distribution of sarcoptic mange in wombats. Aust Vet J 76: 411-414.
69. 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.
70. Masello JF, Choconi RG, Helmer M, Kremberg T, Lubjuhn T, Quillfeldt P (2009) Do leucocytes reflect condition in nestling burrowing parrots Cyanoliseus patagonus in the wild? Comp Biochem Physiol Part A 152: 176-181.
71. May SA, Norton TW (1996) Influence of fragmentation and disturbance on the potential impact of feral predators on native fauna in Australian forest ecosystems. Wildl Res (Wildl Res) 23: 387-400.
72. Mazerolle DF, Hobson KA (2002) Physiological ramifications of habitat selection in territorial male ovenbirds: consequences of landscape fragmentation. Oecologia 130: 356-363.
73. McEwen BS, Sapolsky RM (1995) Stress and cognitive function. Curr Opin Neurobiol 5: 205-216.
74. Menkhorst P, Knight F (2004) A field guide to the mammals of Australia. Oxford University Press, Melbourne.
75. Möstl E, Palme R (2002) Hormones as indicators of stress. Domest Anim Endocrinol 23: 67-74.
76. Nadolski J, Skwarska J, Kaliński A, Bańbura M, Śniegula R, Bańbura J (2006) Blood parameters as consistent predictors of nestling performance in great tits (Parus major) in the wild. Comp Biochem Physiol Part A 143: 50-54.
77. Naylor R, Richardson SJ, McAllan BM (2008) Boom and bust: a review of the physiology of the marsupial genus Antechinus. J Comp Physiol (B) 178: 545-562.
78. Neiger R, Hadley J, Pfeiffer DU (2002) Differentiation of dogs with regenerative and non-regenerative anaemia on the basis of their red cell distribution width and mean corpuscular volume. Vet Rec 150: 431.
79. Noyce KV, Garshelis DL (1994) Body size and blood characteristics as indicators of condition and reproductive performance in black bears. Bears Biol Manag 9: 481-496.
80. O'Brien EL, Morrison BL, Johnson LS (2001) Assessing the effects of haematophagous ectoparasites on the health of nestling birds: haematocrit vs haemoglobin levels in House Wrens parasitized by blow fly larvae. J Avian Biol 32: 73-76.
81. Oishi Y, Sodeyama S, Kondo K (1999) Oxidative stress and haematological changes in immobilized rats. Acta Physiol Scand 165: 65-69.
82. Romero LM, Romero RC (2002) Corticosterone responses in wild birds: the importance of rapid initial sampling. Condor 104: 129-135.
83. Rothenberg ME (1998) Eosinophilia. N Engl J Med 338: 1592-1600.
84. Salvante KG (2006) Techniques for studying integrated immune function in birds. Auk 123: 575-586.
85. Santos J, Benjamin M, Yang PC, Prior T, Perdue MH (2000) Chronic stress impairs rat growth and jejunal epithelial barrier function: role of mast cells. Am J Physiol Gastrointest Liver Physiol 278: 847-854.
86. 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.
87. Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86: 155-163.
88. Siegel HS (1980) Physiological stress in birds. Bioscience 30: 529-534.
89. Stevenson RD, Woods WA Jr (2006) Condition indices for conservation: new uses for evolving tools. Integr Comp Biol 46: 1169.
90. Stirrat SC (2003) Body condition and blood chemistry of agile wallabies (Macropus agilis) in the wet-dry tropics. Wildl Res 30: 59-67.
91. Stokes VL, Pech RP, Banks PB, Arthur AD (2004) Foraging behaviour and habitat use by Antechinus flavipes and Sminthopsis murina (Marsupialia: Dasyuridae) in response to predation risk in eucalypt woodland. Biol Conserv 117: 331-342.
92. Sumner J, Dickman CR (1998) Distribution and identity of species in the Antechinus stuartii--A. flavipes group (Marsupialia: Dasyuridae) in south-eastern Australia. Aust J Zool 46: 27-41.
93. Suorsa P, Helle H, Koivunen V, Huhta E, Nikula A, Hakkarainen H (2004) Effects of forest patch size on physiological stress and immunocompetence in an area-sensitive passerine, the Eurasian treecreeper (Certhia familiaris): an experiment. Proc Royal Soc Lond Series B Biol Sci (Lond) 271: 435-440.
94. Teague CR, Dhabhar FS, Barton RH, Beckwith-Hall B, Powell J, Cobain M, Singer B, McEwen BS, Lindon JC, Nicholson JK (2007) Metabonomic studies on the physiological effects of acute and chronic psychological stress in Sprague-Dawley rats. J Proteome Res 6: 2080-2093.
95. Tsigos C, Chrousos GP (2002) Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J Psychosom Res 53: 865-871.
96. Tyler RD, Cowell RL (1996) Classification and diagnosis of anaemia. Comp Haematol Int 6: 1-16.
97. Wasser SK, Bevis K, King G, Hanson E (1997) Noninvasive physiological measures of disturbance in the northern spotted owl. Conserv Biol 11: 1019-1022.
98. Wasser SK, Hunt KE, Brown JL, Cooper K, Crockett CM, Bechert U, Millspaugh JJ, Larson S, Monfort SL (2000) A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen Comp Endocrinol 120: 260-275.
99. Weber D, Millar J, Neff B (2007) Male reproductive success and female preference in bushy-tailed woodrats (Neotoma cinerea): do females prefer males in good physical condition? Can J Zool 85: 169-176.
100. Wikel SK (1996) Host immunity to ticks. Annu Rev Entomol 41: 1-22.
101. Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how. J Neuroendocrinol 15: 711-724.
102. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer Science + Business Media, New York.