, Volume 173, Issue 3, pp 731–743 | Cite as

Can synchronizing feather-based measures of corticosterone and stable isotopes help us better understand habitat–physiology relationships?

  • Graham D. FairhurstEmail author
  • Matthias Vögeli
  • David Serrano
  • Antonio Delgado
  • José L. Tella
  • Gary R. Bortolotti
Physiological Ecology - Original Research


Physiological mechanisms link the environment with population dynamics, and glucocorticoid hormones are of particular interest because they respond adaptively to environmental change and can influence vertebrate reproduction and fitness. We tested a novel approach of synchronizing feather-based measures of corticosterone (the primary avian glucocorticoid; CORTf) and ratios of stable isotopes (SIs) of C (δ13C) and N (δ15N) to provide information about environmental conditions and an integrated physiological response to those conditions over the same period of feather synthesis. Using a fragmented metapopulation of Dupont’s larks Chersophilus duponti, an endangered steppe songbird, we analyzed interrelationships among CORTf, δ13C, δ15N, and the physical environment, including measures of habitat loss and fragmentation. CORTf was not related to any habitat variable measured directly. However, we detected a significant spatial structure to CORTf values and food availability, with greater similarity in both at smaller spatial scales. Using SIs as proxies for the local environment, we found CORTf was negatively related to δ13C. Values of CORTf, δ13C, and the relationship between the two were likely driven by variation in agricultural land use surrounding lark habitat patches. Our feather-based approach revealed that individual physiology was sensitive to environmental conditions (e.g., an interaction of food availability and variation in habitat) at a local scale, but not patch or landscape scales. Combining CORTf and SIs may be a promising tool because it can provide individual-based information about habitat, physiology, and their relationship during the same time period.


Biomarker Physiological conservation Dupont’s lark Fragmentation Stress hormone 



We thank all collaborators during fieldwork, especially M. Méndez, P. Laiolo, M. A. Carrero and I. Afán. We thank T. Marchant for generously allowing us to use her lab and I. Luque and V. Fachal for their assistance with the corticosterone analyses. We are particularly grateful to P. Ostrom, K. Hobson, A. Bond, and two anonymous reviewers for helping improve the manuscript. G. D. F. was supported by a Dr. Ruby Larson Student Research Fund in Biology, a Malcolm A. Ramsay Memorial Award, a Nature Saskatchewan Graduate Student Award, and a Candace Savage and Keith Bell Fellowship in Grassland Ecology Studies. M. V. was supported by a pre- and postdoctoral fellowship (I3P-CSIC and MICINN). Funds were provided by Junta de Andalucía Excellence Project P07RNM 02918 (M. V., D. S., J. L. T.), the Natural Science and Engineering Research Council of Canada (G. R. B.), and the University of Saskatchewan (G. D. F., G. R. B.).

Supplementary material

442_2013_2678_MOESM1_ESM.doc (197 kb)
Supplementary Appendices (DOC 197 kb)


  1. Alguacil MD, Roldan A, Salinas-Garcia JR, Querejeta JI (2011) No tillage affects the phosphorus status, isotopic composition and crop yield of Phaseolus vulgaris in a rain-fed farming system. J Sci Food Agric 91:268–272CrossRefGoogle Scholar
  2. Andrén H (1994) Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos 71:355–366CrossRefGoogle Scholar
  3. Aragüés A (1992) Estudio de la alondra de Dupont en la región Aragonesa (Study of the Dupont’s lark in the region of Aragón). Ph.D. University of Zaragoza, ZaragozaGoogle Scholar
  4. Astheimer LB, Buttemer WA, Wingfield JC (1992) Interactions of corticosterone with feeding, activity and metabolism in passerine birds. Ornis Scand 23:355–365CrossRefGoogle Scholar
  5. Bennett PM, Hobson KA (2009) Trophic structure of a boreal forest arthropod community revealed by stable isotope (δ13C, δ15N) analyses. Entomol Sci 12:17–24CrossRefGoogle Scholar
  6. Benton TG, Bryant DM, Cole L, Crick HQP (2002) Linking agricultural practice to insect and bird populations: a historical study over three decades. J Appl Ecol 39:673–687CrossRefGoogle Scholar
  7. Blas J, Bortolotti GR, Tella JL, Baos R, Marchant TA (2007) Stress response during development predicts fitness in a wild, long lived vertebrate. Proc Natl Acad Sci USA 104:8880–8884PubMedCrossRefGoogle Scholar
  8. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135PubMedCrossRefGoogle Scholar
  9. Bond AL, Lavers JL (2011) Trace element concentrations in feathers of flesh-footed shearwaters (Puffinus carneipes) from across their breeding range. Arch Environ Contam Toxicol 61:318–326PubMedCrossRefGoogle Scholar
  10. Bortolotti GR (2010) Flaws and pitfalls in the chemical analysis of feathers: bad news-good news for avian chemoecology and toxicology. Ecol Appl 20:1766–1774PubMedCrossRefGoogle Scholar
  11. Bortolotti GR, Dawson RD, Murza GL (2002) Stress during feather development predicts fitness potential. J Anim Ecol 71:333–342CrossRefGoogle Scholar
  12. Bortolotti GR, Marchant TA, Blas J, German T (2008) Corticosterone in feathers is a long-term, integrated measure of avian stress physiology. Funct Ecol 22:494–500CrossRefGoogle Scholar
  13. Bortolotti GR, Marchant T, Blas J, Cabezas S (2009) Tracking stress: localisation, deposition and stability of corticosterone in feathers. J Exp Biol 212:1477–1482PubMedCrossRefGoogle Scholar
  14. Braun-Blanquet J, de Bolós O (1957) Les groupement végétaux du bassin moyen de l’Ebre et leur dynamisme. Anal Estac Exp Aula Dei 5:1–266Google Scholar
  15. Briones MJI, Bol R, Sleep D, Allen D, Sampedro L (2001) Spatio-temporal variation of stable isotope ratios in earthworms under grassland and maize cropping systems. Soil Biol Biochem 33:1673–1682CrossRefGoogle Scholar
  16. Burger J, Gochfeld M (2000) Metal levels in feathers of 12 species of seabirds from Midway Atoll in the northern Pacific Ocean. Sci Total Environ 257:37–52PubMedCrossRefGoogle Scholar
  17. Burnham KP, Anderson DR (2002) Model selection and multiple inference: a practical information-theoretic approach, 2nd edn. Springer, HeidelbergGoogle Scholar
  18. Busch DS, Hayward LS (2009) Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables. Biol Conserv 142:2844–2853CrossRefGoogle Scholar
  19. Carrete M, Serrano D, Illera JC, López G, Vögeli M, Delgado A, Tella JA (2009) Goats, birds, and emergent diseases: apparent and hidden effects of exotic species in an island environment. Ecol Appl 19:840–853PubMedCrossRefGoogle Scholar
  20. Carrete M, Bortolotti GR, Sánchez-Zapata JA, Delgado A, Cortés-Avizanda A, Grande JM, Donázar JA (2013) Stressful conditions experienced by endangered by endangered Egyptian vultures on African wintering areas. Anim Conserv. doi: 10.1111/acv.12001
  21. Choi WJ, Chang SX, Allen HL, Kelting DL, Ro HM (2005) Irrigation and fertilization effects on foliar and soil carbon and nitrogen isotope ratios in a loblolly pine stand. For Ecol Manage 213:90–101CrossRefGoogle Scholar
  22. Clarke GM (1995) Relationships between developmental stability and fitness: application for conservation biology. Conserv Biol 9:18–24CrossRefGoogle Scholar
  23. Cramp S (ed) (1988) Handbook of the birds of Europe, the Middle East and North Africa. Oxford University Press, OxfordGoogle Scholar
  24. Diggs NE, Marra PP, Cooper RJ (2011) Resource limitation drives patterns of habitat occupancy during the nonbreeding season for an omnivorous songbird. Condor 113:646–654CrossRefGoogle Scholar
  25. ESRI (2004) ArcGIS 9. ESRI, RedlandsGoogle Scholar
  26. Evans MR, Roberts ML, Buchanan KL, Goldsmith AR (2006) Heritability of corticosterone response and changes in life history traits during selection in the zebra finch. J Evol Biol 19:343–352PubMedCrossRefGoogle Scholar
  27. Fairhurst GD, Frey MD, Reichert JF, Szelest I, Kelly DM, Bortolotti GR (2011) Does environmental enrichment reduce stress? An integrated measure of corticosterone from feathers provides a novel perspective. PLoS ONE 6:e17663PubMedCrossRefGoogle Scholar
  28. Fairhurst GD, Navarro J, González-Solís J, Marchant TA, Bortolotti GR (2012) Feather corticosterone of a nestling seabird reveals consequences of sex-specific parental investment. Proc R Soc B Biol Sci 279:177–184CrossRefGoogle Scholar
  29. Fokidis HB, Orchinik M, Deviche P (2011) Context-specific territorial behavior in urban birds: no evidence for involvement of testosterone or corticosterone. Horm Behav 59:133–143PubMedCrossRefGoogle Scholar
  30. Frampton GK, van den Brink PJ, Gould PJL (2000) Effects of spring drought and irrigation on farmland arthropods in southern Britain. J Appl Ecol 37:865–883CrossRefGoogle Scholar
  31. Gobierno de Navarra (GDN) (2011) Meteorología y climatología de Navarra. Accessed April 2011
  32. Grubb TC (2006) Ptilochronology: feather time and the biology of birds. Oxford University Press, OxfordGoogle Scholar
  33. Hanski I, Kuussaari M, Nieminen M (1994) Metapopulation structure and migration in the butterfly Melitaea cinxia. Ecology 75:747–762CrossRefGoogle Scholar
  34. Harms NJ, Fairhurst GD, Bortolotti GR, Smits JEG (2010) Variation in immune function, body condition, and feather corticosterone in nestling tree swallows (Tachycineta bicolor) on reclaimed wetlands in the Athabasca oil sands, Alberta, Canada. Environ Pollut 158:841–848PubMedCrossRefGoogle Scholar
  35. Hebert CE, Wassenaar LI (2001) Stable nitrogen isotopes in waterfowl feathers reflect agricultural land use in western Canada. Environ Sci Technol 35:3482–3487PubMedCrossRefGoogle Scholar
  36. Herranz J, Yanes M, Suárez F (1993) First record on the diet of Dupont’s lark Chersophilus duponti nestlings in the Iberian Peninsula. Ardeola 40:77–79Google Scholar
  37. Hobson KA (1999) Stable-carbon and nitrogen isotope ratios of songbird feathers grown in two terrestrial biomes: implications for evaluating trophic relationships and breeding origins. Condor 101:799–805CrossRefGoogle Scholar
  38. Hobson KA, Bairlein F (2003) Isotopic fractionation and turnover in captive garden warblers (Sylvia borin): implications for delineating dietary and migratory associations in wild passerines. Can J Zool Rev Can Zool 81:1630–1635CrossRefGoogle Scholar
  39. Hobson KA, Wassenaar LI (eds) (2008) Tracking animal migration with stable isotopes. Academic Press, New YorkGoogle Scholar
  40. Homyack JA (2010) Evaluating habitat quality of vertebrates using conservation physiology tools. Wildl Res 37:332–342CrossRefGoogle Scholar
  41. Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150:447–461CrossRefGoogle Scholar
  42. Instituto Aragonés de Estadistica (IAE) (2011) Clima. Accessed April 2011
  43. Jovani R, Diaz-Real J (2012) Fault bars timing and duration: the power of studying feather fault bars and growth bands together. J Avian Biol 43:97–101CrossRefGoogle Scholar
  44. Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool Rev Can Zool 78:1–27CrossRefGoogle Scholar
  45. Kilgas P, Mand R, Magi M, Tilgar V (2006) Hematological parameters in brood-rearing great tits in relation to habitat, multiple breeding and sex. Comp Biochem Physiol Mol Integr Physiol 144:224–231CrossRefGoogle Scholar
  46. Kitaysky AS, Kitaiskaia EV, Wingfield JC, Piatt JF (2001) Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks. J Comp Physiol B Biochem Syst Environ Physiol 171:701–709CrossRefGoogle Scholar
  47. Kitaysky AS, Romano MD, Piatt JF, Wingfield JC, Kikuchi M (2005) The adrenocortical response of tufted puffin chicks to nutritional deficits. Horm Behav 47:606–619PubMedCrossRefGoogle Scholar
  48. Kitaysky AS, Kitaiskaia EV, Piatt JF, Wingfield JC (2006) A mechanistic link between chick diet and decline in seabirds? Proc R Soc B Biol Sci 273:445–450CrossRefGoogle Scholar
  49. Laiolo P (2008) Characterizing the spatial structure of songbird cultures. Ecol Appl 18:1774–1780PubMedCrossRefGoogle Scholar
  50. Laiolo P, Tella JL (2006) Landscape bioacoustics allow detection of the effects of habitat patchiness on population structure. Ecology 87:1203–1214PubMedCrossRefGoogle Scholar
  51. Laiolo P, Tella JL (2008) Social determinants of songbird vocal activity and implications for the persistence of small populations. Anim Conserv 11:433–441CrossRefGoogle Scholar
  52. Laiolo P, Vögeli M, Serrano D, Tella JL (2008) Song diversity predicts the viability of fragmented bird populations. PLoS ONE 3:e1822PubMedCrossRefGoogle Scholar
  53. Lattin CR, Reed JM, DesRochers DW, Romero LM (2011) Elevated corticosterone in feathers correlates with corticosterone-induced decreased feather quality: a validation study. J Avian Biol 42:247–252CrossRefGoogle Scholar
  54. Lens L, Eggermont H (2008) Fluctuating asymmetry as a putative marker of human-induced stress in avian conservation. Bird Conserv Int 18:S125–S143CrossRefGoogle Scholar
  55. 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 116:284–292CrossRefGoogle Scholar
  56. Marra PP, Hobson KA, Holmes RT (1998) Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science 282:1884–1886PubMedCrossRefGoogle Scholar
  57. Mazerolle DF, Hobson KA (2002) Physiological ramifications of habitat selection in territorial male ovenbirds: consequences of landscape fragmentation. Oecologia 130:356–363CrossRefGoogle Scholar
  58. Méndez M, Tella JL, Godoy JA (2011) Restricted gene flow and genetic drift in recently fragmented populations of an endangered steppe bird. Biol Conserv 144:2615–2622CrossRefGoogle Scholar
  59. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  60. Newton I (1998) Population limitation in birds. Academic Press, LondonGoogle Scholar
  61. Oliver I, Beattie AJ (1993) A possible method for the rapid assessment of biodiversity. Conserv Biol 7:572–578CrossRefGoogle Scholar
  62. Ostrom PH, Colunga-Garcia M, Gage SH (1997) Establishing pathways of energy flow for insect predators using stable isotope ratios: field and laboratory evidence. Oecologia 109:108–113CrossRefGoogle Scholar
  63. Ouyang JQ, Sharp PJ, Dawson A, Quetting M, Hau M (2011) Hormone levels predict individual differences in reproductive success in a passerine bird. Proc R Soc B Biol Sci 278:2537–2545CrossRefGoogle Scholar
  64. Peñuelas J, Filella I, Terradas J (1999) Variability of plant nitrogen and water use in a 100-m transect of a subdesertic depression of the Ebro valley (Spain) characterized by leaf δ13C and δ15N. Acta Oecol 20:119–123CrossRefGoogle Scholar
  65. Podlesak DW, McWilliams SR (2006) Metabolic routing of dietary nutrients in birds: effects of diet quality and macronutrient composition revealed using stable isotopes. Physiol Biochem Zool 79:534–549PubMedCrossRefGoogle Scholar
  66. Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316CrossRefGoogle Scholar
  67. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  68. Rangel TF, Diniz JAF, Bini LM (2010) SAM: a comprehensive application for spatial analysis in macroecology. Ecography 33:46–50CrossRefGoogle Scholar
  69. Raouf SA, Smith LC, Brown MB, Wingfield JC, Brown CR (2006) Glucocorticoid hormone levels increase with group size and parasite load in cliff swallows. Anim Behav 71:39–48CrossRefGoogle Scholar
  70. Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462–468CrossRefGoogle Scholar
  71. Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255PubMedCrossRefGoogle Scholar
  72. Romero LM, Wikelski M (2001) Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events. Proc Natl Acad Sci USA 98:7366–7370PubMedCrossRefGoogle Scholar
  73. Romero LM, Reed JM, Wingfield JC (2000) Effects of weather on corticosterone responses in wild free-living passerine birds. Gen Comp Endocrinol 118:113–122PubMedCrossRefGoogle Scholar
  74. Sahin K, Sahin N, Onderci M, Gursu F, Cikim G (2002) Optimal dietary concentration of chromium for alleviating the effect of heat stress on growth, carcass qualities, and some serum metabolites of broiler chickens. Biol Trace Elem Res 89:53–64PubMedCrossRefGoogle Scholar
  75. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89PubMedCrossRefGoogle Scholar
  76. Saunders DA, Hobbs RJ, Margules CR (1991) Biological consequences of ecosystem fragmentation: a review. Conserv Biol 5:18–32CrossRefGoogle Scholar
  77. Scheuerlein A, Van’t Hof TJ, Gwinner E (2001) Predators as stressors? Physiological and reproductive consequences of predation risk in tropical stonechats (Saxicola torquata axillaris). Proc R Soc Lond Ser B Biol Sci 268:1575–1582CrossRefGoogle Scholar
  78. Seoane J, Justribo JH, Garcia F, Retamar J, Rabadan C, Atienza JC (2006) Habitat-suitability modelling to assess the effects of land-use changes on Dupont’s lark Chersophilus duponti: a case study in the Layna Important Bird Area. Biol Conserv 128:241–252CrossRefGoogle Scholar
  79. Shannon CE, Weaver W (1949) A mathematical model of communication. University of Illinois Press, UrbanaGoogle Scholar
  80. SIGPAC (2011) Sistema de información geográfica de parcelas agrícolas (SIGPAC)
  81. Sokal RR, Oden NL (1978) Spatial autocorrelation in biology. 1. Methodology. Biol J Linn Soc 10:199–228CrossRefGoogle Scholar
  82. Suorsa P et al (2003) Forest management is associated with physiological stress in an old-growth forest passerine. Proc R Soc Lond Ser B Biol Sci 270:963–969CrossRefGoogle Scholar
  83. Svensson L (1992) Identification guide to European passerines. British Trust for Ornithology, StockholmGoogle Scholar
  84. Vaida F, Blanchard S (2005) Conditional Akaike information for mixed-effects models. Biometrika 92:351–370CrossRefGoogle Scholar
  85. Vickery JA et al (2001) The management of lowland neutral grasslands in Britain: effects of agricultural practices on birds and their food resources. J Appl Ecol 38:647–664CrossRefGoogle Scholar
  86. Vögeli M, Serrano D, Tella JL, Méndez M, Godoy JA (2007) Sex determination Duponts lark Chersophilus duponti using molecular sexing and discriminant functions. Ardeola 54:69–79Google Scholar
  87. Vögeli M, Laiolo P, Serrano D, Tella JL (2008) Who are we sampling? Apparent survival differs between methods in a secretive species. Oikos 117:1816–1823CrossRefGoogle Scholar
  88. Vögeli M, Serrano D, Pacios F, Tella JL (2010) The relative importance of patch habitat quality and landscape attributes on a declining steppe-bird metapopulation. Biol Conserv 143:1057–1067CrossRefGoogle Scholar
  89. Vögeli M, Lemus JA, Serrano D, Blanco G, Tella JL (2011) An island paradigm at mainland: population fragmentation impairs the community of avian pathogens. Proc R Soc B Biol Sci 278:2668–2676CrossRefGoogle Scholar
  90. Weitner A, Dupouey JL, Lefèvre Y, Bréda N, Badeau V, Ferhi A, Duquesnay A, Thimonier A (2007) Roles of soil chemistry and water availability in site-related δ13C variations in French beech forests. Tree Physiol 27:1043–1051PubMedCrossRefGoogle Scholar
  91. Wenninger EJ, Inouye RS (2008) Insect community response to plant diversity and productivity in a sagebrush-steppe ecosystem. J Arid Environ 72:24–33CrossRefGoogle Scholar
  92. Wikelski M, Cooke SJ (2006) Conservation physiology. Trends Ecol Evol 21:38–46PubMedCrossRefGoogle Scholar
  93. Wiley AE, Ostrom PH, Stricker CA, James HF, Gandhi H (2010) Isotopic characterization of flight feathers in two pelagic seabirds: sampling strategies for ecological studies. Condor 112:337–346CrossRefGoogle Scholar
  94. Wingfield JC, Moore MC, Farner DS (1983) Endocrine responses to inclement weather in naturally breeding populations of white-crowned sparrows (Zonotrichia leucophrys pugetensis). Auk 100:56–62Google Scholar
  95. Wingfield JC, Vleck CM, Moore MC (1992) Seasonal changes of the adrenocortical response to stress in birds of the Sonoran desert. J Exp Zool 264:419–428PubMedCrossRefGoogle Scholar
  96. Wright GC, Rao RCN, Farquhar GD (1994) Water-use efficiency and carbon isotope discrimination in peanut under water deficit conditions. Crop Sci 34:92–97CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Graham D. Fairhurst
    • 1
    Email author
  • Matthias Vögeli
    • 1
    • 2
  • David Serrano
    • 2
  • Antonio Delgado
    • 3
  • José L. Tella
    • 2
  • Gary R. Bortolotti
    • 1
  1. 1.Department of BiologyUniversity of SaskatchewanSaskatoonCanada
  2. 2.Estación Biológica de Doñana (EBD-CSIC)SevillaSpain
  3. 3.Instituto Andaluz de Ciencias de la Tierra IACT (CSIC-UGR)ArmillaSpain

Personalised recommendations