The effect of acute stress and long-term corticosteroid administration on plasma metabolites in an urban and desert songbird

Physiological and Biochemical Zoology

Volumn 86, Issue 1, 2013, Pages 47-60

  Davies, Scott ^a   Rodriguez, Natalie S ^b   Sweazea, Karen L ^b   Deviche, Pierre ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTEROID; FATTY ACID; GLYCOGEN; URIC ACID;

BODY MASS; DESERT; DEVELOPMENTAL BIOLOGY; ENVIRONMENTAL STRESS; GLUCOSE; LIFE HISTORY; METABOLISM; METABOLITE; MOBILIZATION; PHYSIOLOGICAL RESPONSE; PLASMA; SONGBIRD; STEROID; URBAN AREA;

ANIMAL; ARTICLE; BLOOD; DESERT CLIMATE; ENVIRONMENT; GLUCOSE BLOOD LEVEL; LIVER; MALE; METABOLISM; PECTORALIS MAJOR MUSCLE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RANDOMIZATION; SONGBIRD; UNITED STATES;

ADRENAL CORTEX HORMONES; ANIMALS; ARIZONA; BLOOD GLUCOSE; DESERT CLIMATE; ENVIRONMENT; FATTY ACIDS, NONESTERIFIED; GLYCOGEN; LIVER; MALE; PECTORALIS MUSCLES; RANDOM ALLOCATION; SONGBIRDS; STRESS, PHYSIOLOGICAL; URIC ACID;

ARIZONA; PHOENIX; UNITED STATES;

ANIMALIA; AVES; MELOZONE; PASSERI; PIPILO;

EID: 84872290385     PISSN: 15222152     EISSN: None     Source Type: Journal    
DOI: 10.1086/667990     Document Type: Article

References (101)

1. Adams N.J., M.J. Farnworth, J. Rickett, K.A. Parker, and J.F. Cockrem. 2011. Behavioural and corticosterone responses to capture and confinement of wild blackbirds (Turdus merula). Appl Anim Behav Sci 134:255.
2. Alonso-Alvarez C., A. Velando, M. Ferrer, and J.A.R. Veira. 2002. Changes in plasma biochemistry and body mass during incubation in the yellow-legged gull. Waterbirds 25:253-258.
3. Angelier F., C. Clément-Chastel, G. Gabrielsen, and O. Chastel. 2007. Corticosterone and time-activity budget: an experiment with black-legged kittiwakes. Horm Behav 52:482-491.
4. Astheimer L.B., W.A. Buttemer, and J.C. Wingfield. 1995. Seasonal and acute changes in adrenocortical responsiveness in an arctic-breeding bird. Horm Behav 29:442-457.
5. Awerman J.L. and L.M. Romero. 2010. Chronic psychological stress alters body weight and blood chemistry in European starlings (Sturnus vulgaris). Comp Biochem Physiol A 156: 136-142.
6. Bears H., J.N.M. Smith, and J.C. Wingfield. 2003. Adrenocortical sensitivity to stress in dark-eyed juncos (Junco hyemalis oregonus) breeding in low and high elevation habitat. Ecoscience 54:127-133.
7. Benítez-López A., R. Alkemade, and P.A. Verweij. 2010. The impacts of roads and other infrastructure on mammal and bird populations: a meta-analysis. Biol Conserv 143:1307-1316.
8. Bintz G.L. and C.E. Strand. 1983. Nitrogen catabolism during starvation and starvation with water deprivation in Richardson's ground squirrels. J Comp Physiol B 149:565-572.
9. Bjorklund M., I. Ruiz, and J.C. Senar. 2010. Genetic differentiation in the urban habitat: the great tits (Parus major) of the parks of Barcelona city. Biol J Linn Soc 99:9-19.
10. Bonier F., P.R. Martin, I.T. Moore, and J.C. Wingfield. 2009. Do baseline glucocorticoids predict fitness? Trends Ecol Evol 24:634-642.
11. Bonier F., P.R. Martin, K.S. Sheldon, J.P. Jensen, S.L. Foltz, and J.C. Wingfield. 2007. Sex-specific consequences of life in the city. Behav Ecol 18:121-129.
12. Braun E.J. and K.L. Sweazea. 2008. Glucose regulation in birds. Comp Biochem Physiol B 151:1-9.
13. Burgess S.C., T.T. He, Z. Yan, J. Lindner, A.D. Sherry, C.R. Malloy, J.D. Browning, and M.A. Magnuson. 2007. Cytosolic phosphoenolpyruvate carboxykinase does not solely control the rate of hepatic gluconeogenesis in the intact mouse liver. Cell Metab 5:313-320.
14. Busch D.S., W.D. Robinson, T.R. Robinson, and J.C. Wingfield. 2011. Influence of proximity to a geographical range limit on the physiology of a tropical bird. J Anim Ecol 80:649.
15. Busch D.S., T.S. Sperry, E. Peterson, C.T. Do, J.C. Wingfield, and E.H. Boyd. 2008. Impacts of frequent, acute pulses of corticosterone on condition and behavior of Gambel's whitecrowned sparrow (Zonotrichia leucophrys gambelii). Gen Comp Endocrinol 158:224-233.
16. Buyantuyev A. and J. Wu. 2009. Urbanization alters spatiotemporal patterns of ecosystem primary production: a case study of the Phoenix metropolitan region, USA. J Arid Environ 73:512-520.
17. Chakravarty K., H. Cassuto, L. Reshef, and R.W. Hanson. 2005. Factors that control the tissue-specific transcription of the gene for phosphoenolpyruvate carboxykinase-C. Crit Rev Biochem Mol Biol 40:129-154.
18. Cohen A.A., M. Hau, and M. Wikelski. 2008. Stress, metabolism, and antioxidants in two wild passerine bird species. Physiol Biochem Zool 81:463-472.
19. Cohen A.A., K. Klasing, and R. Ricklefs. 2007. Measuring cir-culating antioxidants in wild birds. Comp Biochem Physiol B 147:110-121.
20. Conover W.J. and R.L. Iman. 1981. Rank transformations as a bridge between parametric and nonparametric statistics. Am Stat 35:124-129.
21. Cook W.M. and S.H. Faeth. 2006. Irrigation and land use drive ground arthropod community patterns in an urban desert. Environ Entomol 35:1532-1540.
22. Corbel H., S. Geiger, and R. Groscolas. 2010. Preparing to fledge: the adrenocortical and metabolic responses to stress in king penguin chicks. Funct Ecol 24:82-92.
23. Cyr N.E., K. Earle, C. Tam, and L.M. Romero. 2007. The effect of chronic psychological stress on corticosterone, plasma metabolites, and immune responsiveness in European starlings. Gen Comp Endocrinol 154:59-66.
24. Cyr N.E. and L.M. Romero. 2007. Chronic stress in free-living European starlings reduces corticosterone concentrations and reproductive success. Gen Comp Endocrinol 151:82-89.
25. das Neves J., L.P.N. Hackl, C.G. Freitas, M.A. Paschoalini, and J. Marino-Neto. 2000. Central injections of noradrenaline and adrenaline differentially affect plasma free fatty acid and glucose in conscious pigeons (Columba livia). J Comp Physiol B 170:379-386.
26. Davison T.F., J. Rea, and J.G. Rowell. 1983. Effects of dietary corticosterone on the growth and metabolism of immature Gallus domesticus. Gen Comp Endocrinol 50:463-468.
27. Delaney K.S., S.P.D. Riley, and R.N. Fisher. 2010. A rapid, strong, and convergent genetic response to urban habitat fragmentation in four divergent and widespread vertebrates. PLoS ONE 5:e12767.
28. DeNardo D.F. and P. Licht. 1993. Effects of corticosterone on social behavior of male lizards. Horm Behav 27:184-199.
29. DesRochers D.W., J.M. Reed, J. Awerman, J.A. Kluge, J. Wilkinson, L.I. van Griethuijsen, J. Aman, and L.M. Romero. 2009. Exogenous and endogenous corticosterone alter feather quality. Comp Biochem Physiol A 152:46-52.
30. Faeth S.H., P.S. Warren, E. Shochat, and W.A. Marussich. 2005. Trophic dynamics in urban communities. BioScience 55:399-407.
31. Falsone K., S. Jenni-Eiermann, and L. Jenni. 2009. Corticosterone in migrating songbirds during endurance flight. Horm Behav 56:548-556.
32. Fokidis H.B. 2011. Homeowners associations: friend or foe to native desert avifauna? conservation concerns and opportunities for research. J Arid Environ 75:394-396.
33. Fokidis H.B., L. Hurley, C. Rogowski, K. Sweazea, and P. Deviche. 2011. Effects of captivity and body condition on plasma corticosterone, locomotor behavior, and plasma metabolites in curve-billed thrashers. Physiol Biochem Zool 84:595-606.
34. Fokidis H.B., M. Orchinik, and P. Deviche. 2009. Corticosterone and corticosteroid binding globulin in birds: relation to urbanization in a desert city. Gen Comp Endocrinol 160: 259-270.
35. Freeman B.M. 1969. Effect of noradrenaline on the plasma free fatty acid and glucose levels in Gallus domesticus. Comp Biochem Physiol 30:993-996.
36. Goldstein R., D. Wasserman, O. McGuinness, D. Lacy, A. Cherrington, and N. Abumrad. 1993. Effects of chronic elevation in plasma cortisol on hepatic carbohydrate metabolism. Am J Physiol 264:E119.
37. Goutte A., F. Angelier, J. Welcker, B. Moe, C. Clément-Chastel, G. Gabrielsen, C. Bech, and O. Chastel. 2010. Long-term survival effect of corticosterone manipulation in black-legged kittiwakes. Gen Comp Endocrinol 167:246-251.
38. Gray J.M., D. Yarian, and M. Ramenofsky. 1990. Corticosterone, foraging behavior, and metabolism in dark-eyed juncos, Junco hyemalis. Gen Comp Endocrinol 79:375-384.
39. Grégoire F., C. Genart, N. Hauser, and C. Remacle. 1991. Glucocorticoids induce a drastic inhibition of proliferation and stimulate differentiation of adult rat fat cell precursors. Exp Cell Res 196:270-278.
40. Grimm N.B., S.H. Faeth, N.E. Golubiewski, C.L. Redman, J. Wu, X. Bai, and J.M. Briggs. 2008. Global change and the ecology of cities. Science 319:756-760.
41. Guglielmo C.G., D.J. Cerasale, and C. Eldermire. 2005. A field validation of plasma metabolite profiling to assess refueling performance of migratory birds. Physiol Biochem Zool 78: 116-125.
42. Hanson R.W. and A.J. Garber. 1972. Phosphoenolpyruvate carboxykinase. I. Its role in gluconeogenesis. Am J Clin Nutr 25:1010-1021.
43. Heil L., E. Fernández-Juricic, D. Renison, A.M. Cingolani, and D.T. Blumstein. 2007. Avian responses to tourism in the biogeographically isolated high Córdoba Mountains, Argentina. Biodivers Conserv 16:1009-1026.
44. Helms C.W. and W.H. Drury. 1960. Winter and migratory weight and fat field studies on some North American buntings. Bird Band 31:1-40.
45. Hofer C., F.J. Gallagher, and C. Holzapfel. 2010. Metal accumulation and performance of nestlings of passerine bird species at an urban brownfield site. Environ Pollut 158:1207-1213.
46. Hollmén T., J.C. Franson, M. Hario, S. Sankari, M. Kilpi, and K. Lindström. 2001. Use of serum biochemistry to evaluate nutritional status and health of incubating common eiders (Somateria mollissima) in Finland. Physiol Biochem Zool 74: 333-342.
47. Holmes W.N. and J.G. Phillips. 1976. The adrenal cortex of birds. Pp. 293-420 in I. Chester-Jones and I. Henderson, eds. General, comparative and clinical endocrinology of the adrenal cortex. Academic Press, New York.
48. Imhoff M.L., L. Bounoua, R. DeFries, W.T. Lawrence, D. Stutzer, C.J. Tucker, and T. Ricketts. 2004. The consequences of urban land transformation on net primary productivity in the United States. Remote Sens Environ 89:434-443.
49. Jenni L. and S. Jenni-Eiermann. 1998. Fuel supply and metabolic constraints in migrating birds. J Avian Biol 29:521-528.
50. Jenni L., S. Jenni-Eiermann, F. Spina, and H. Schwabl. 2000. Regulation of protein breakdown and adrenocortical response to stress in birds during migratory flight. Am J Physiol 278:R1182-R1189.
51. Jenni-Eiermann S., L. Jenni, A. Kvist, A. Lindstrom, T. Piersma, and G.H. Visser. 2002. Fuel use and metabolic response to endurance exercise: a wind tunnel study of a long-distance migrant shorebird. J Exp Biol 205:2453-2460.
52. Kitaysky A.S., E.V. Kitaiskaia, J.F. Piatt, and J.C. Wingfield. 2003. Benefits and costs of increased levels of corticosterone in seabird chicks. Horm Behav 43:140-149.
53. Kitaysky A.S., J.C. Wingfield, and J.F. Piatt. 2001. Corticosterone facilitates begging and affects resource allocation in the black-legged kittiwake. Behav Ecol 12:619-625.
54. Klaassen M. 1996. Metabolic constraints on long-distance migration in birds. J Exp Biol 199:57-64.
55. Klasing K.C. 1998. Comparative avian nutrition. Cab International, New York.
56. Landys M.M., T. Piersma, C.G. Guglielmo, J. Jukema, M. Ramenofsky, and J.C. Wingfield. 2005. Metabolic profile of long-distance migratory flight and stopover in a shorebird. Proc R Soc B 272:295-302.
57. Landys M.M., M. Ramenofsky, C.G. Guglielmo, and J.C. Wingfield. 2004. The low-affinity glucocorticoid receptor regulates feeding and lipid breakdown in the migratory Gambel's white-crowned sparrow Zonotrichia leucophrys gambelii. J Exp Biol 207:143-154.
58. Landys M.M., M. Ramenofsky, and J.C. Wingfield. 2006. Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen Comp Endocrinol 148:132-149.
59. Leung K. and A. Munck. 1975. Peripheral actions of glucocorticoids. Annu Rev Physiol 37:245-272.
60. Lin H., E. Decuypere, and J. Buyse. 2004a. Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus). 1. Chronic exposure. Comp Biochem Physiol B 139:737-744.
61. Lin H., E. Decuypere, and J. Buyse. 2004b. Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus). 2. Short-term effect. Comp Biochem Physiol B 139:745-751.
62. Lo S., J. Russell, and A. Taylor. 1970. Determination of glycogen in small tissue samples. J Appl Physiol 28:234-236.
63. Malchoff D.M., B.L. Maloff, J.N. Livingston, and D.H. Lockwood. 1982. Influence of dexamethasone on insulin action: inhibition of basal and insulin-stimulated hexose transport is dependent on length of exposure in vitro. Endocrinology 110:2081-2087.
64. Martin L.B., J. Gilliam, P. Han, K. Lee, and M. Wikelski. 2005. Corticosterone suppresses cutaneous immune function in temperate but not tropical house sparrows, Passer domesticus. Gen Comp Endocrinol 140:126-135.
65. McKinney M.L. 2002. Urbanization, biodiversity, and conservation. BioScience 52:883-890.
66. Milesi C., C.D. Elvidge, R.R. Nemani, and S.W. Running. 2003. Assessing the impact of urban land development on net primary productivity in the southeastern United States. Remote Sens Environ 86:401-410.
67. Nakwa A., N. Sitasuwan, A. Jatisatein, P. Chantaramongko, W. Pupichit, and P. Srisak. 2008. The effects of tourists on bird diversity in tourist area compared to restricted area of seasonal evergreen forest at Tung Salang Luang National Park, Phetchabun Province, Thailand. Int J Zool Res 4:96-105.
68. Nemeth E. and H. Brumm. 2010. Birds and anthropogenic noise: are urban songs adaptive? Am Nat 176:465-475.
69. O'Brien R.M., P.C. Lucas, C.D. Forest, M.A. Magnuson, and D.K. Granner. 1990. Identification of a sequence in the PEPCK gene that mediates a negative effect of insulin on transcription. Science 249:533-537.
70. Okumura J.I. and I. Tasaki. 1969. Effect of fasting, refeeding and dietary protein level on uric acid and ammonia content of blood, liver and kidney in chickens. J Nutr 97:316-320.
71. Partecke J., I. Schwabl, and E. Gwinner. 2006. Stress and the city: urbanization and its effects on the stress physiology in European blackbirds. Ecology 87:1945-1952.
72. Pyle P. 1997. Identification guide to North American birds. Pt. 1. Columbidae to Ploceidae. Slate Creek, Bolinas, CA.
73. Remage-Healey L. and L.M. Romero. 2000. Daily and seasonal variation in response to stress in captive starlings (Sturnus vulgaris): glucose. Gen Comp Endocrinol 119:60-68.
74. Remage-Healey L. and L.M. Romero. 2001. Corticosterone and insulin interact to regulate glucose and triglyceride levels during stress in a bird. Am J Physiol 281:994-1003.
75. Rich E.L. and L.M. Romero. 2005. Exposure to chronic stress downregulates corticosterone responses to acute stressors. Am J Physiol 288:1628-1636.
76. Robin J.P., Y. Cherel, H. Girard, A. Géloen, and Y. Maho. 1987. Uric acid and urea in relation to protein catabolism in longterm fasting geese. J Comp Physiol 157:491-499.
77. Robin J.P., M. Frain, C. Sardet, R. Groscolas, and Y. Le Maho. 1988. Protein and lipid utilization during long-term fasting in emperor penguins. Am J Physiol 254:61-68.
78. Rodríguez P., F.S. Tortosa, and R. Villafuerte. 2005. The effects of fasting and refeeding on biochemical parameters in the red-legged partridge (Alectoris rufa). Comp Biochem Physiol A 140:157-164.
79. Rognstad R. 1979. Rate-limiting steps in metabolic pathways. J Biol Chem 254:1875-1878.
80. Romero L.M., D. Strochlic, and J.C. Wingfield. 2005. Corticosterone inhibits feather growth: potential mechanism explaining seasonal down regulation of corticosterone during molt. Comp Biochem Physiol A 142:65-73.
81. Romero L.M. and M. Wikelski. 2001. Corticosterone levels predict survival probabilities of Galápagos marine iguanas during El Niño events. Proc Natl Acad Sci USA 98:7366-7370.
82. Rosenberg K.V., R.D. Ohmart, W.C. Hunter, and B.W. Anderson. 1991. Birds of the lower Colorado River valley. University of Arizona Press, Tucson.
83. Rothe H.J., W. Biesel, and W. Nachtigall. 1987. Pigeon flight in a wind tunnel. I. Gas exchange and power requirements. J Comp Physiol B 157:99-109.
84. Rudman D. and M. DiGirolamo. 1971. Effect of adrenal cortical steroids on lipid metabolism. Harper & Row, New York.
85. Salvante K.G. and T.D. Williams. 2003. Effects of corticosterone on the proportion of breeding females, reproductive output and yolk precursor levels. Gen Comp Endocrinol 130:205-214.
86. Sapolsky R.M., L.M. Romero, and A.U. Munck. 2000. How do glucocorticoids influence stress responses? integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55-89.
87. Schoech S.J., R. Bowman, E.S. Bridge, and R.K. Boughton. 2007. Baseline and acute levels of corticosterone in Florida scrubjays (Aphelocoma coerulescens): effects of food supplementation, suburban habitat, and year. Gen Comp Endocrinol 154:150-160.
88. Schoech S.J., R. Bowman, and S.J. Reynolds. 2004. Corticosterone, nutrition, and timing of reproduction in Florida scrubjays. Horm Behav 46:121.
89. Schwabl H. 1995. Individual variation of the acute adrenocortical response to stress in the white-throated sparrow. Zoology 99:113-120.
90. Schwilch R., L. Jenni, and S. Jenni-Eiermann. 1996. Metabolic responses of homing pigeons to flight and subsequent recovery. J Comp Physiol B 166:77-87.
91. Small T.W., P.J. Sharp, and P. Deviche. 2007. Environmental regulation of the reproductive system in a flexibly breeding Sonoran Desert bird, the rufous-winged sparrow, Aimophila carpalis. Horm Behav 51:483-495.
92. t-methylhistidine. Biochem J 178:139-146.
93. Tweit R.C. and D.M. Finch. 1994. Abert's towhee (Melozone aberti). In A. Poole, ed. The birds of North America. Cornell Lab of Ornithology, Ithaca, NY.
94. Van Heezik Y., A. Smyth, A. Adams, and J. Gordon. 2010. Do domestic cats impose an unsustainable harvest on urban bird populations? Biol Conserv 143:121-130.
95. Watford M. 1989. Hormonal and nutritional regulation of phosphoenolpyruvate carboxykinase mRNA levels in chicken kidney. J Nutr 119:319-322.
96. Watford M., Y. Hod, Y.B. Chiao, M.F. Utter, and R.W. Hanson. 1981. The unique role of the kidney in gluconeogenesis in the chicken: the significance of a cytosolic form of phosphoenolpyruvate carboxykinase. J Biol Chem 256:10023-10027.
97. Wingfield J.C., D.L. Maney, C.W. Breuner, J.D. Jacobs, S. Lynn, M. Ramenofsky, and R.D. Richardson. 1998. Ecological bases of hormone-behavior interactions: the "emergency life history stage. " Am Zool 38:191-206.
98. Wingfield J.C. and B. Silverin. 1986. Effects of corticosterone on territorial behavior of free-living male song sparrows Melospiza melodia. Horm Behav 20:405-417.
99. Yamada F., S. Inoue, T. Saitoh, K. Tanaka, S. Satoh, and Y. Takamura. 1993. Glucoregulatory hormones in the immobilization stress-induced increase of plasma glucose in fasted and fed rats. Endocrinology 132:2199.
100. Zhang S., F. Lei, S. Liu, D. Li, C. Chen, and P. Wang. 2011. Variation in baseline corticosterone levels of tree sparrow (Passer montanus) populations along an urban gradient in Beijing, China. J Ornithol 152:1-6.
101. Zhao J., H. Lin, H. Jiao, and Z. Song. 2009. Corticosterone suppresses insulin-and NO-stimulated muscle glucose uptake in broiler chickens (Gallus gallus domesticus). Comp Biochem Physiol C 149:448-454.