Do baseline glucocorticoids simultaneously represent fitness and environmental quality in a declining aerial insectivore?

Oikos

Volumn 125, Issue 12, 2016, Pages 1824-1837

  Madliger, Christine L ^a   Love, Oliver P ^a,b  

^a UNIVERSITY OF WINDSOR   (Canada)

^b UNIVERSITY OF WINDSOR   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AERIAL SURVEY; BODY CONDITION; CLUTCH SIZE; ENVIRONMENTAL INDICATOR; FITNESS; HABITAT QUALITY; HABITAT TYPE; HORMONE; INSECTIVORE; NESTING BEHAVIOR; PASSERINE; POPULATION DECLINE; REPRODUCTIVE SUCCESS; RIPARIAN ZONE;

TACHYCINETA; TACHYCINETA BICOLOR;

EID: 84973487333     PISSN: 00301299     EISSN: 16000706     Source Type: Journal    
DOI: 10.1111/oik.03354     Document Type: Article

References (129)

1. Allen, L. C. et al. 2010. Variation in physiological stress between bridge- and cave-roosting Brazilian free-tailed bats. – Conserv. Biol. 25: 374–381.
2. Angelier, F. and Wingfield, J. C. 2013. Importance of the glucocorticoid stress response in a changing world: theory, hypotheses and perspectives. – Gen. Comp. Endocrinol. 190: 118–128.
3. Angelier, F. et al. 2006. Effect of age, breeding experience and senescence on corticosterone and prolactin levels in a long-lived seabird: the wandering albatross. – Gen. Comp. Endocrinol. 149: 1–9.
4. Angelier, F. et al. 2010. Hormonal correlates of individual quality in a long-lived bird: a test of the “corticosterone-fitness hypothesis.” – Biol. Lett. 6: 846–849.
5. Ardia, D. R. and Clotfelter, E. D. 2007. Individual quality and age affect responses to an energetic constraint in a cavity-nesting bird. – Behav. Ecol. 18: 259–266.
6. Arlettaz, R. et al. 2014. Disturbance of wildlife by outdoor winter recreation: allostatic stress response and altered activity–energy budgets. – Ecol. Appl. 25: 1197–1212.
7. Baker, M. R. et al. 2013. Review of factors influencing stress hormones in fish and wildlife. – J. Nat. Conserv. 21: 309–318.
8. Bauer, C. M. et al. 2013. Habitat type influences endocrine stress response in the degu (Octodon degus). – Gen. Comp. Endocrinol. 186: 136–144.
9. Belanger, C. B. et al. 2016. Seasonal variation in baseline and maximum whole-body glucocorticoid concentrations in a small-bodied stream fish independent of habitat quality. – Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 192: 1–6.
10. Bell, G. P. 1990. Birds and mammals on an insect diet: a primer on diet composition analysis in relation to ecological energetics. – Stud. Avian Biol. 13: 416–426.
11. Benjamini, Y. and Hochberg, Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. – J. R. Stat. Soc. B Meth. 57: 289–300.
12. Blevins, Z. W. et al. 2013. Land use drives the physiological properties of a stream fish. – Ecol. Indic. 24: 224–235.
13. Bókony, V. et al. 2009. Stress response and the value of reproduction: are birds prudent parents? – Am. Nat. 173: 589–598.
14. Bonier, F. 2012. Hormones in the city: endocrine ecology of urban birds. – Horm. Behav. 61: 763–772.
15. Bonier, F. et al. 2006. Sex-specific consequences of life in the city. – Behav. Ecol. 18: 121–129.
16. Bonier, F. et al. 2009. Do baseline glucocorticoids predict fitness? – Trends Ecol. Evol. 24: 634–642.
17. Bonier, F. et al. 2011. The stress of parenthood? Increased glucocorticoids in birds with experimentally enlarged broods. – Biol. Lett. 7: 944–946.
18. Boonstra, R. 2013. Reality as the leading cause of stress: rethinking the impact of chronic stress in nature. – Funct. Ecol. 27: 11–23.
19. Boyle, W. A. et al. 2012. Rapid loss of fat but not lean mass prior to chick provisioning supports the flight efficiency hypothesis in tree swallows. – Funct. Ecol. 26: 895–903.
20. Breuner, C. W. et al. 1999. Diel rhythms of basal and stress-induced corticosterone in a wild, seasonal vertebrate, Gambel's white-crowned sparrow. – J. Exp. Zool. 284: 334–342.
21. Breuner, C. W. et al. 2008. In search of relationships between the acute adrenocortical response and fitness. – Gen. Comp. Endocrinol. 157: 288–295.
22. Bryant, D. M. and Bryant, V. M. T. 1988. Assimilation efficiency and growth of nestling insectivores. – Ibis 130: 268–274.
23. Busch, D. S. and Hayward, L. S. 2009. Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables. – Biol. Conserv. 142: 2844–2853.
24. Carey, C. 2005. How physiological methods and concepts can be useful in conservation biology. – Integr. Comp. Biol. 45: 4–11.
25. Cash, W. B. and Holberton, R. L. 2005. Endocrine and behavioral response to a decline in habitat quality: effects of pond drying on the slider turtle, Trachemys scripta. – J. Exp. Zool. A Comp. Exp. Biol. 303A: 872–879.
26. Chaurand, T. and Weimerskirch, H. 1994. Incubation routine, body mass regulation and egg neglect in the blue petrel Halobaena caerulea. – Ibis 136: 285–290.
27. Clemmons, J. and Buchholz, R. 2002. Behavioral approaches to conservation in the wild. – Cambridge Univ. Press.
28. Cockrem, J. F. 2005. Conservation and behavioral neuroendocrinology. – Horm. Behav. 48: 492–501.
29. Cooke, S. J. 2014. Conservation physiology today and tomorrow. – Conserv. Physiol. 2: doi: 10.1093/conphys/cot033.
30. Crespi, E. J. et al. 2013. Life history and the ecology of stress: how do glucocorticoid hormones influence life-history variation in animals? – Funct. Ecol. 27: 93–106.
31. D'Alba, L. et al. 2011. State dependent effects of elevated hormone: nest site quality, corticosterone levels and reproductive performance in the common eider. – Gen. Comp. Endocrinol. 172: 218–224.
32. Dantzer, B. et al. 2014. Measures of physiological stress: a transparent or opaque window into the status, management and conservation of species? – Conserv. Physiol. 2: doi: 10.1093/conphys/cou023.
33. de Steven, D. 1978. The influence of age on the breeding biology of the tree swallow Iridoprocne bicolor. – Ibis 120: 516–523.
34. Drent, R. and Daan, S. 1980. The prudent parent: energetic adjustments in avian breeding. – Ardea 68: 225–252.
35. Dunn, E. H. 1979. Age of effective momeothermy in nestling tree swallows according to brood size. – Wilson Bull. 91: 455–457.
36. Dunn, P. O. and Whittingham, L. A. 2005. Radio-tracking of female tree swallows prior to egg-laying. – J. Field Ornithol. 76: 259–263.
37. Escribano-Avila, G. et al. 2013. Testing cort-fitness and cort-adaptation hypotheses in a habitat suitability gradient for roe deer. – Acta Oecol. 53: 38–48.
38. Fontaine, J. J. and Martin, T. E. 2006. Parent birds assess nest predation risk and adjust their reproductive strategies. – Ecol. Lett. 9: 428–434.
39. Freed, L. A. 1981. Loss of mass in breeding wrens: stress or adaptation? – Ecology 62: 1179–1186.
40. French, S. S. et al. 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.
41. Ghilain, A. and Bélisle, M. 2008. Breeding success of tree swallows along a gradient of agricultural intensification. – Ecol. Appl. 18: 1140–1154.
42. Glickman, M. E. et al. 2014. False discovery rate control is a recommended alternative to Bonferroni-type adjustments in health studies. – J. Clin. Epidemiol. 67: 850–857.
43. Gobush, K. S. et al. 2008. Long-term impacts of poaching on relatedness, stress physiology and reproductive output of adult female African elephants. – Conserv. Biol. 22: 1590–1599.
44. Goymann, W. 2012. On the use of non-invasive hormone research in uncontrolled, natural environments: the problem with sex, diet, metabolic rate and the individual. – Meth. Ecol. Evol. 3: 757–765.
45. Hämäläinen, A. et al. 2015. The stress of growing old: sex- and season-specific effects of age on allostatic load in wild grey mouse lemurs. – Oecologia 178: 1063–1075.
46. Harding, A. M. A. et al. 2009. Impacts of experimentally increased foraging effort on the family: offspring sex matters. – Anim. Behav. 78: 321–328.
47. Hayward, L. S. et al. 2011. Impacts of acute and long-term vehicle exposure on physiology and reproductive success of the northern spotted owl. – Ecosphere 2: 1–20.
48. Heintz, M. R. et al. 2011. Validation of a cortisol enzyme immunoassay and characterization of salivary cortisol circadian rhythm in chimpanzees (Pan troglodytes). – Am. J. Primatol. 73: 903–908.
49. Homan, R. N. et al. 2003. Corticosterone concentrations in free-living spotted salamanders (Ambystoma maculatum). – Gen. Comp. Endocrinol. 130: 165–171.
50. Hopkins, W. A. and DuRant, S. E. 2011. Innate immunity and stress physiology of eastern hellbenders (Cryptobranchus alleganiensis) from two stream reaches with differing habitat quality. – Gen. Comp. Endocrinol. 174: 107–115.
51. Huber, S. et al. 2003. Effects of season, sex, and sample collection on concentrations of fecal cortisol metabolites in red deer (Cervus elaphus). – Gen. Comp. Endocrinol. 130: 48–54.
52. Husak, J. F. and Moore, I. T. 2008. Stress hormones and mate choice. – Trends Ecol. Evol. 23: 532–534.
53. Hussell, D. J. 1983. Age and plumage color in female tree swallows. – J. Field Ornithol. 54: 312–318.
54. Hussell, D. J. and Quinney, T. E. 1987. Food abundance and clutch size of tree swallows Tachycineta bicolor. – Ibis 129: 243–258.
55. Jenni-Eiermann, S. et al. 2008. Glucocorticoid response to food availability in breeding barn swallows (Hirundo rustica). – Gen. Comp. Endocrinol. 155: 558–565.
56. Kaiser, K. et al. 2015. Effects of anthropogenic noise on endocrine and reproductive function in White's treefrog, Litoria caerulea. – Conserv. Physiol. 3: doi: 10.1093/confys/cou061.
57. Kern, M. et al. 2005. Blood metabolite and corticosterone levels in breeding adult pied flycatchers. – Condor 107: 665–677.
58. Klaassen, M. et al. 1994. Influence of growth rate retardation on time budgets and energetics of Arctic tern Sterna paradisaea and common tern S. hirundo chicks. – Ibis 136: 197–204.
59. Korte, S. M. et al. 2005. The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the tradeoffs in health and disease. – Neurosci. Biobehav. Rev. 29: 3–38.
60. Kriska, G. et al. 1998. Why do mayflies lay their eggs en masse on dry asphalt roads? Water-imitating polarized light reflected from asphalt attracts Ephemeroptera. – J. Exp. Biol. 201: 2273–2286.
61. Lanctot, R. B. et al. 2003. Are corticosterone levels a good indicator of food availability and reproductive performance in a kittiwake colony? – Horm. Behav. 43: 489–502.
62. Landys, M. M. et al. 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.
63. Leffelaar, D. and Robertson, R. J. 1986. Equality of feeding roles and the maintenance of monogamy in tree swallows. – Behav. Ecol. Sociobiol. 18: 199–206.
64. Lendvai, Á. Z. et al. 2015. Analysis of the optimal duration of behavioral observations based on an automated continuous monitoring system in tree swallows (Tachycineta bicolor): is one hour good enough? – PLoS ONE 10 (11): eo141194.
65. Leshyk, R. et al. 2012. Logging affects fledgling sex ratios and baseline corticosterone in a forest songbird. – PLoS ONE 7 (3): e33124.
66. Love, O. P. and Williams, T. 2008. Plasticity in the adrenocortical response of a free-living vertebrate: the role of pre- and post-natal developmental stress. – Horm. Behav. 54: 496–505.
67. Love, O. P. et al. 2004. Mediation of a corticosterone-induced reproductive conflict. – Horm. Behav. 46: 59–65.
68. Madliger, C. L. and Love, O. P. 2014. The need for a predictive, context-dependent approach to the application of stress hormones in conservation. – Conserv. Biol. 28: 283–287.
69. Madliger, C. L. and Love, O. P. 2015. The power of physiology in changing landscapes: considerations for the continued integration of conservation and physiology. – Integr. Comp. Biol. 55: 545–553.
70. Madliger, C. L. and Love, O. P. 2016. Data from: Do baseline glucocorticoids simultaneously represent fitness and environmental quality in a declining aerial insectivore? – Dryad Digital Repository, < http://dx.doi.org/10.5061/dryad.qg630 >.
71. Madliger, C. L. et al. 2015. Assessing baseline stress physiology as an integrator of environmental quality in a wild avian population: implications for use as a conservation biomarker. – Biol. Conserv. 192: 409–417.
72. McCarty, J. P. 2001. Variation in growth of nestling tree swallows across multiple temporal and spatial scales. – Auk 118: 176–190.
73. McCarty, J. P. and Winkler, D. W. 1999. Foraging ecology and diet selectivity of tree swallows feeding nestlings. – Condor 101: 246–254.
74. McEwen, B. S. and Wingfield, J. C. 2010. What is in a name? Integrating homeostasis, allostasis and stress. – Horm. Behav. 57: 105–111.
75. Millspaugh, J. J. and Washburn, B. E. 2004. Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation. – Gen. Comp. Endocrinol. 138: 189–199.
76. Moore, I. T. and Jessop, T. S. 2003. Stress, reproduction, and adrenocortical modulation in amphibians and reptiles. – Horm. Behav. 43: 39–47.
77. Moore, I. T. et al. 2000. Relationships between annual cycles of testosterone, corticosterone and body condition in male red-spotted garter snakes, Thamnophis sirtalis concinnus. – Physiol. Biochem. Zool. 73: 307–312.
78. Morbey, Y. E. and Ydenberg, R. C. 2000. Seasonal decline in nestling growth: support for the parental-quality hypothesis in Cassin's auklets. – Auk 117: 1065–1068.
79. Nebel, S. et al. 2010. Declines of aerial insectivores in North America follow a geographic gradient. – Avian Conserv. Ecol. 5: 1.
80. Neto, J. M. and Gosler, A. G. 2009. Variation in body condition of breeding Savi's warblers Locustella luscinioides: the reproductive stress and flight adaptation hypothesis revisited. – J. Ornithol. 151: 201–210.
81. Newcomb Homan, R. et al. 2003. Impacts of varying habitat quality on the physiological stress of spotted salamanders (Ambystoma maculatum). – Anim. Conserv. 6: 11–18.
82. Nilsson, J.-Å. 2002. Metabolic consequences of hard work. – Proc. R. Soc. B 269: 1735–1739.
83. Norberg, R. A. 1981. Temporary weight decrease in breeding birds may result in more fledged young. – Am. Nat. 118: 838–850.
84. Ouyang, J. Q. et al. 2011. Within seasons and among years: when are corticosterone levels repeatable? – Horm. Behav. 60: 559–564.
85. Patterson, S. H. et al. 2011. Glucocorticoids, individual quality and reproductive investment in a passerine bird. – Anim. Behav. 81: 1239–1247.
86. Pavitt, A. T. et al. 2015. Cortisol but not testosterone is repeatable and varies with reproductive effort in wild red deer stags. – Gen. Comp. Endocrinol. 222: 62–68.
87. Perrins, C. M. and Moss, D. 1975. Reproductive rates in the great tit. – J. Anim. Ecol. 44: 695–706.
88. Quinney, T. E. and Ankney, C. D. 1985. Prey size selection by tree swallows. – Auk 102: 245–250.
89. Quinney, T. E. et al. 1986. Sources of variation in growth of tree swallows. – Auk: 389–400.
90. Razeng, E. and Watson, D. M. 2015. Nutritional composition of the preferred prey of insectivorous birds: popularity reflects quality. – J. Avian Biol. 46: 89–96.
91. Rector, M. E. et al. 2012. Corticosterone levels of Atlantic puffins vary with breeding stage and sex but are not elevated in poor foraging years. – Gen. Comp. Endocrinol. 178: 408–416.
92. Reeder, D. M. and Kramer, K. M. 2005. Stress in free-ranging mammals: integrating physiology, ecology and natural history. – J. Mammal. 86: 225–235.
93. Rehnus, M. et al. 2014. Mountain hares Lepus timidus and tourism: stress events and reactions. – J. Appl. Ecol. 51: 6–12.
94. Ricklefs, R. E. and Wikelski, M. 2002. The physiology/life-history nexus. – Trends Ecol. Evol. 17: 462–468.
95. Riechert, J. et al. 2012. Why do experienced birds reproduce better? Possible endocrine mechanisms in a long-lived seabird, the common tern. – Gen. Comp. Endocrinol. 178: 391–399.
96. Riechert, J. et al. 2014. Predicting reproductive success from hormone concentrations in the common tern (Sterna hirundo) while considering food abundance. – Oecologia 176: 715–727.
97. Robertson, R. J. et al. 1992. Tree swallow (Tachycineta bicolor). – In: Poole, A. et al. (eds), Birds of North America. Vol. 11. Acad. Nat. Sci., Washington, DC: Am. Ornithol. Union N. Am, pp. 1–28.
98. Romero, L. M. 2002. Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. – Gen. Comp. Endocrinol. 128: 1–24.
99. Romero, L. M. and Wikelski, M. 2001. Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events. – Proc. Natl Acad. Sci. USA 98: 7366–7370.
100. Romero, L. M. and Reed, J. M. 2005. Collecting baseline corticosterone samples in the field: is under 3 min good enough? – Comp. Biochem. Physiol. Part. A. Mol. Integr. Physiol. 140: 73–79.
101. Romero, L. M. et al. 2000. Effects of weather on corticosterone responses in wild free-living passerine birds. – Gen. Comp. Endocrinol. 118: 113–122.
102. Romero, L. M. et al. 2009. The reactive scope model – a new model integrating homeostasis, allostasis and stress. – Horm. Behav. 55: 375–389.
103. Satterthwaite, W. H. et al. 2012. Linking climate variability, productivity and stress to demography in a long-lived seabird. – Mar. Ecol. Prog. Ser. 454: 221–235.
104. Sheriff, M. J. et al. 2009. The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. – J. Anim. Ecol. 78: 1249–1258.
105. Sih, A. et al. 2011. Evolution and behavioural responses to human-induced rapid environmental change. – Evol. Appl. 4: 367–387.
106. Silverin, B. 1982. Endocrine correlates of brood size in adult pied flycatchers, Ficedula hypoleuca. – Gen. Comp. Endocrinol. 47: 18–23.
107. Spée, M. et al. 2010. Should I stay or should I go? Hormonal control of nest abandonment in a long-lived bird, the Adélie penguin. – Horm. Behav. 58: 762–768.
108. Steffen, W. et al. 2004. Global change and the Earth system: a planet under pressure. – Springer.
109. Strasser, E. H. and Heath, J. A. 2013. Reproductive failure of a human-tolerant species, the American kestrel, is associated with stress and human disturbance. – J. Appl. Ecol. 50: 912–919.
110. Stutchbury, B. J. and Robertson, R. J. 1988. Within-season and age-related patterns of reproductive performance in female tree swallows (Tachycineta bicolor). – Can. J. Zool. 66: 827–834.
111. Stutchbury, B. J. and Rohwer, S. 1990. Molt patterns in the tree swallow (Tachycineta bicolor). – Can. J. Zool. 68: 1468–1472.
112. Suorsa, P. et al. 2003. Forest management is associated with physiological stress in an old-growth forest passerine. – Proc. R. Soc. B 270: 963–969.
113. Tarlow, E. M. and Blumstein, D. T. 2007. Evaluating methods to quantify anthropogenic stressors on wild animals. – Appl. Anim. Behav. Sci. 102: 429–451.
114. Tarlow, E. M. et al. 2003. Diel changes in plasma melatonin and corticosterone concentrations in tropical Nazca boobies (Sula granti) in relation to moon phase and age. – Gen. Comp. Endocrinol. 133: 297–304.
115. Touma, C. and Palme, R. 2005. Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. – Ann. N. Y. Acad. Sci. 1046: 54–74.
116. Touma, C. et al. 2003. Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. – Gen. Comp. Endocrinol. 130: 267–278.
117. Velando, A. and Alonso-Alvarez, C. 2003. Differential body condition regulation by males and females in response to experimental manipulations of brood size and parental effort in the blue-footed booby. – J. Anim. Ecol. 72: 846–856.
118. Walker, B. G. et al. 2005. Field endocrinology and conservation biology. – Integr. Comp. Biol. 45: 12–18.
119. Wasser, S. K. et al. 1997. Noninvasive physiological measures of disturbance in the northern spotted owl. – Conserv. Biol. 11: 1019–1022.
120. Wheelwright, N. T. et al. 1991. The costs of reproduction in tree swallows (Tachycineta bicolor). – Can. J. Zool. 69: 2540–2547.
121. Wikelski, M. and Cooke, S. J. 2006. Conservation physiology. – Trends Ecol. Evol. 21: 38–46.
122. Williams, J. B. 1988. Field metabolism of tree swallows during the breeding season. – Auk 105: 706–714.
123. Williams, C. T. et al. 2008. Corticosterone levels of tufted puffins vary with breeding stage, body condition index, and reproductive performance. – Gen. Comp. Endocrinol. 158: 29–35.
124. Willmer, P. et al. 2009. Environmental physiology of animals. – Blackwell.
125. Wingfield, J. C. and Kitaysky, A. S. 2002. Endocrine responses to unpredictable environmental events: stress or anti-stress hormones? – Integr. Comp. Biol. 42: 600–609.
126. Wingfield, J. C. et al. 1997. Environmental stress, field endocrinology and conservation biology. – In: Clemmons, J. and Buchholz, R. (eds), Behavioral approaches to conservation in the wild. Cambridge Univ. Press.
127. Winkler, D. W. and Allen, P. E. 1995. Effects of handicapping on female condition and reproduction in tree swallows (Tachycineta bicolor). – Auk 112: 737–747.
128. Winkler, D. W. and Allen, P. E. 1996. The seasonal decline in tree swallow clutch size: physiological constraint or strategic adjustment? – Ecology 77: 922–932.
129. Winkler, D. W. et al. 2004. Breeding dispersal and philopatry in the tree swallow. – Condor 106: 768–776.