, Volume 179, Issue 1, pp 89–101 | Cite as

Agricultural land use and human presence around breeding sites increase stress-hormone levels and decrease body mass in barn owl nestlings

  • Bettina AlmasiEmail author
  • Paul Béziers
  • Alexandre Roulin
  • Lukas Jenni
Population ecology - Original research


Human activities can have a suite of positive and negative effects on animals and thus can affect various life history parameters. Human presence and agricultural practice can be perceived as stressors to which animals react with the secretion of glucocorticoids. The acute short-term secretion of glucocorticoids is considered beneficial and helps an animal to redirect energy and behaviour to cope with a critical situation. However, a long-term increase of glucocorticoids can impair e.g. growth and immune functions. We investigated how nestling barn owls (Tyto alba) are affected by the surrounding landscape and by human activities around their nest sites. We studied these effects on two response levels: (a) the physiological level of the hypothalamus–pituitary–adrenal axis, represented by baseline concentrations of corticosterone and the concentration attained by a standardized stressor; (b) fitness parameters: growth of the nestlings and breeding performance. Nestlings growing up in intensively cultivated areas showed increased baseline corticosterone levels late in the season and had an increased corticosterone release after a stressful event, while their body mass was decreased. Nestlings experiencing frequent anthropogenic disturbance had elevated baseline corticosterone levels, an increased corticosterone stress response and a lower body mass. Finally, breeding performance was better in structurally more diverse landscapes. In conclusion, anthropogenic disturbance affects offspring quality rather than quantity, whereas agricultural practices affect both life history traits.


Anthropogenic disturbance Breeding success Corticosterone Disturbance Fitness 



We warmly thank all the field assistants who helped during the long field days and nights from 2004 to 2010. We thank C. Frey and C. Sonnay for collecting and preparing the data on habitat characteristics, and F. Korner-Nievergelt and G. Pasinelli for discussing model selection and averaging. S. Jenni-Eiermann, Z. Tablado, Y. Bötsch and Hannu Pöysä and two anonymous reviewers gave valuables comments on an earlier draft. The Swiss National Science Foundation supported the study financially (no. 31003A-127057 to L. J., no. 31003A-120517 to A. R.).

Supplementary material

442_2015_3318_MOESM1_ESM.pdf (150 kb)
Supplementary material 1 (PDF 150 kb)


  1. Almasi B, Jenni L, Jenni-Eiermann S, Roulin A (2010) Regulation of stress response is heritable and functionally linked to melanin-based coloration. J Evol Biol 23:987–996CrossRefPubMedGoogle Scholar
  2. Anderson DR, Burnham KP, Thompson WL (2000) Null hypothesis testing: problems, prevalence, and an alternative. J Wildl Manage 64:912–923CrossRefGoogle Scholar
  3. Angelier F, Wingfield JC, Weimerskirch H, Chastel O (2010) Hormonal correlates of individual quality in a long-lived bird: a test of the ‘corticosterone-fitness hypothesis’. Biol Lett 6:846–849PubMedCentralCrossRefPubMedGoogle Scholar
  4. Arlettaz R, Krähenbühl M, Almasi B, Roulin A, Schaub M (2010) Wildflower areas within revitalized agricultural matrices boost small mammal populations but not breeding barn owls. J Ornithol 151:553–564CrossRefGoogle Scholar
  5. Aschwanden J, Birrer S, Jenni L (2005) Are ecological compensation areas attractive hunting sites for common kestrels (Falco tinnunculus) and long-eared owls (Asio otus)? J Ornithol 146:279–286CrossRefGoogle Scholar
  6. Aschwanden J, Holzgang O, Jenni L (2007) Importance of ecological compensation areas for small mammals in intensively farmed areas. Wildl Biol 13:150–158CrossRefGoogle Scholar
  7. Bates D, Maechler M, Bolker B (2012) lme4: linear mixed-effects models using S4 classes. R package version 0.999999-0.
  8. Bauer CM, Skaff NK, Bernard AB, Trevino JM, Ho JM, Romero LM, Ebensperger LA, Hayes LD (2013) Habitat type influences endocrine stress response in the degu (Octodon degus). Gen Comp Endocrinol 186:136–144CrossRefPubMedGoogle Scholar
  9. Bechard MJ (1982) Effect of vegetative cover on foraging site selection by Swainsons hawk. Condor 84:153–159CrossRefGoogle Scholar
  10. Bernaards C, Jennrich R (2012) GPArotation: GPA factor rotation. R package version 2012.3-1.
  11. Bonier F, Martin PR, Sheldon KS, Jensen JP, Foltz SL, Wingfield JC (2007) Sex-specific consequences of life in the city. Behav Ecol 18:121–129CrossRefGoogle Scholar
  12. Bonier F, Martin PR, Moore IT, Wingfield JC (2009a) Do baseline glucocorticoids predict fitness? Trends Ecol Evol 24:634–642CrossRefPubMedGoogle Scholar
  13. Bonier F, Moore IT, Martin PR, Robertson RJ (2009b) The relationship between fitness and baseline glucocorticoids in a passerine bird. Gen Comp Endocrinol 163:208–213CrossRefPubMedGoogle Scholar
  14. Breuner CW, Patterson SH, Hahn TP (2008) In search of relationships between the acute adrenocortical response and fitness. Gen Comp Endocrinol 157:288–295CrossRefPubMedGoogle Scholar
  15. Bundesamt für Landwirtschaft (BLW) (2014) Agrarbericht 2014Google Scholar
  16. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, BerlinGoogle Scholar
  17. Chavez-Zichinelli CA, MacGregor-Fors I, Quesada J, Rohana PT, Romano MC, Valdez R, Schondube JE (2013) How stressed are birds in an urbanizing landscape? Relationships between the physiology of birds and three levels of habitat alteration. Condor 115:84–92CrossRefGoogle Scholar
  18. Cockrem JF, Silverin B (2002) Variation within and between birds in corticosterone responses of great tits (Parus major). Gen Comp Endocrinol 125:197–206CrossRefPubMedGoogle Scholar
  19. Cyr NE, Romero L (2007) Chronic stress in free-living European starlings reduces corticosterone concentrations and reproductive success. Gen Comp Endocrinol 151:82–89CrossRefPubMedGoogle Scholar
  20. Cyr NE, Romero LM (2009) Identifying hormonal habituation in field studies of stress. Gen Comp Endocrinol 161:295–303CrossRefPubMedGoogle Scholar
  21. Cyr NE, Earle K, Tam C, Romero L (2007) The effect of chronic psychological stress on corticosterone, plasma metabolites, and immune responsiveness in European starlings. Gen Comp Endocrinol 154:59–66CrossRefPubMedGoogle Scholar
  22. Dickens MJ, Romero LM (2013) A consensus endocrine profile for chronically stressed wild animals does not exist. Gen Comp Endocrinol 191:177–189CrossRefPubMedGoogle Scholar
  23. Donald PF, Green RE, Heath MF (2001) Agricultural intensification and the collapse of Europe’s farmland bird populations. Proc R Soc Lond Ser B Biol Scie 268:25–29CrossRefGoogle Scholar
  24. Fowler GS (1999) Behavioral and hormonal responses of Magellanic penguins (Spheniscus magellanicus) to tourism and nest site visitation. Biol Conserv 90:143–149CrossRefGoogle Scholar
  25. Frey C, Sonnay C, Dreiss AN, Roulin A (2011) Habitat, breeding performance, diet and individual age in Swiss barn owls (Tyto alba). J Ornithol 152:279–290CrossRefGoogle Scholar
  26. Hollander FA, Van Dyck H, Martin GS, Titeux N (2011) Maladaptive habitat selection of a migratory passerine bird in a human-modified landscape. Plos One 6:e25703PubMedCentralCrossRefPubMedGoogle Scholar
  27. Hull KL, Cockrem JF, Bridges JP, Candy EJ, Davidson CM (2007) Effects of corticosterone treatment on growth, development, and the corticosterone response to handling in young Japanese quail. Comp Biochem Physiol A Mol Integr Physiol 148:531–543CrossRefPubMedGoogle Scholar
  28. Johnston RF (2001) Synanthropic birds of North America. In: Marzluff JM, Bowman R, Donnelly RE (eds) Avian ecology and conservation in an urbanizing world. Kluwer, Boston, pp 49–67CrossRefGoogle Scholar
  29. Kitaysky AS, Piatt JF, Wingfield JC (2007) Stress hormones link food availability and population processes in seabirds. Mar Ecol Progr Ser 352:245–258CrossRefGoogle Scholar
  30. Kitaysky AS, Piatt JF, Hatch SA, Kitaiskaia EV, Benowitz-Fredericks ZM, Shultz MT, Wingfield JC (2010) Food availability and population processes: severity of nutritional stress during reproduction predicts survival of long-lived seabirds. Funct Ecol 24:625–637CrossRefGoogle Scholar
  31. Konstantinov VM (1996) Anthropogenic transformations of bird communities in the forest zone of the Russian plain. Acta Ornithol (Warsaw) 31:53–58Google Scholar
  32. Lynn SE, Prince LE, Phillips MM (2010) A single exposure to an acute stressor has lasting consequences for the hypothalamo-pituitary-adrenal response to stress in free-living birds. Gen Comp Endocrinol 165:337–344CrossRefPubMedGoogle Scholar
  33. Madliger CL, Love OP (2014) The need for a predictive, context-dependent approach to the application of stress hormones in conservation. Conserv Biol 28:283–287CrossRefPubMedGoogle Scholar
  34. Marzluff JM (2001) Worldwide urbanization and its effects on birds. In: Marzluff JM, Bowman R, Donnelly RE (eds) Avian ecology and conservation in an urbanizing world. Kluwer, Boston, pp 19–49CrossRefGoogle Scholar
  35. Mebs T, Scherzinger W (2000) Die Eulen Europas. Biologie, Kennzeichen, Bestände. Franckh-Kosmos, StuttgartGoogle Scholar
  36. Müller C, Jenni-Eiermann S, Blondel J, Perret P, Caro SP, Lambrechts M, Jenni L (2006) Effect of human presence and handling on circulating corticosterone levels in breeding blue tits (Parus caeruleus). Gen Comp Endocrinol 148:163–171CrossRefPubMedGoogle Scholar
  37. Müller C, Jenni-Eiermann S, Jenni L (2009) Effects of a short period of elevated circulating corticosterone on postnatal growth in free-living Eurasian kestrels Falco tinnunculus. J Exp Biol 212:1405–1412CrossRefPubMedGoogle Scholar
  38. Müllner A, Linsenmair KE, Wikelski M (2004) Exposure to ecotourism reduces survival and affects stress response in hoatzin chicks (Opisthocomus hoazin). Biol Conserv 118:549–558CrossRefGoogle Scholar
  39. Munro CJ, Lasley BL (1988) Non-radiometric methods for immunoassay of steroid hormones. In: Albertson BD, Haseltine FP (eds) Non-radiometric assays: technology and application in polypeptide and steroid hormone detection. Liss, New York, pp 289–329Google Scholar
  40. Munro CJ, Stabenfeldt G (1984) Development of a microtitre plate enzyme immunoassay for the determination of progesterone. J Endocrinol 101:41–49CrossRefPubMedGoogle Scholar
  41. Partecke J, Schwabl I, Gwinner E (2006) Stress and the city: urbanization and its effects on the stress physiology in European blackbirds. Ecology 87:1945–1952CrossRefPubMedGoogle Scholar
  42. Perrins CM, McCleery RH (2001) The effect of fledging mass on the lives of great tits Parus major. Ardea 89:135–142Google Scholar
  43. R Development Core Team (2012) R: A language and environment for statistical computing. R Development Core Team, R Foundation for Statistical Computing, ViennaGoogle Scholar
  44. Revelle W (2012) Psych: procedures for psychological, psychometric, and personality research. R package version 1.2.8.
  45. Rich EL, Romero LM (2005) Exposure to chronic stress downregulates corticosterone responses to acute stressors. Am J Physiol 288:1628–1636Google Scholar
  46. Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255CrossRefPubMedGoogle Scholar
  47. Romero LM, Reed JM (2005) Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp Biochem Physiol 140:73–79CrossRefGoogle Scholar
  48. Romero LM, Wikelski M (2002) Exposure to tourism reduces stress-induced corticosterone levels in Galapagos marine iguanas. Biol Conserv 108:371–374CrossRefGoogle Scholar
  49. Romero LM, Wikelski M (2010) Stress physiology as a predictor of survival in Galapagos marine iguanas. Proc R Soc B Biol Scie 277:3157–3162CrossRefGoogle Scholar
  50. Roulin A (2002) Short- and long-term fitness correlates of rearing conditions in barn owls Tyto alba. Ardea 90:259–267Google Scholar
  51. Roulin A (2004a) Covariation between plumage colour polymorphism and diet in the barn owl Tyto alba. Ibis 146:509–517CrossRefGoogle Scholar
  52. Roulin A (2004b) The function of food stores in bird nests: observations and experiments in the barn owl Tyto alba. Ardea 92:69–78Google Scholar
  53. Roulin A, Almasi B, Jenni L (2010) Temporal variation in glucocorticoid levels during the resting phase is associated in opposite way with maternal and paternal melanic coloration. J Evol Biol 23:2046–2053CrossRefPubMedGoogle Scholar
  54. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrinol Rev 21:55–89Google Scholar
  55. Schoech SJ, Mumme RL, Wingfield JC (1997) Corticosterone, reproductive status, and body mass in a cooperative breeder, the Florida scrub-jay (Aphelocoma coerulescens). Physiol Zool 70:68–73PubMedGoogle Scholar
  56. Strasser EH, Heath JA (2013) Reproductive failure of a human-tolerant species, the American kestrel, is associated with stress and human disturbance. J Appl Ecol 50:912–919CrossRefGoogle Scholar
  57. Taylor IR (1993) Age and sex determination of barn owls Tyto alba alba. Ringing Migr 14:94–102CrossRefGoogle Scholar
  58. Thiel D, Jenni-Eiermann S, Braunisch V, Palme R, Jenni L (2008) Ski tourism affects habitat use and evokes a physiological stress response in capercaillie Tetrao urogallus: a new methodological approach. J Appl Ecol 45:845–853CrossRefGoogle Scholar
  59. Walker BG, Boersma PD, Wingfield JC (2005) Physiological and behavioral differences in Magellanic penguin chicks in undisturbed and tourist-visited locations of a colony. Conserv Biol 19:1571–1577CrossRefGoogle Scholar
  60. Wikelski M, Cooke SJ (2006) Conservation physiology. Trends Ecol Evol 21:38–46CrossRefPubMedGoogle Scholar
  61. Wingfield JC, Deviche P, Sharbaugh S, Astheimer LB, Holberton R, Suydam R, Hunt K (1994) Seasonal-changes of the adrenocortical responses to rtress in redpolls, Acanthis flammea, in Alaska. J Exp Zool 270:372–380CrossRefGoogle Scholar
  62. Wingfield JC, Maney DL, Breuner C, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone-behavior interactions: the “emergency life history stage”. Am Zool 38:191–206Google Scholar
  63. Zhang SP, Lei FM, Liu SL, Li DM, Chen C, Wang PZ (2011) Variation in baseline corticosterone levels of tree sparrow (Passer montanus) populations along an urban gradient in Beijing, China. J Ornithol 152:801–806CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Bettina Almasi
    • 1
    Email author
  • Paul Béziers
    • 2
  • Alexandre Roulin
    • 2
  • Lukas Jenni
    • 1
  1. 1.Swiss Ornithological InstituteSempachSwitzerland
  2. 2.Department of Ecology and Evolution, Biophore BuildingUniversity of LausanneLausanneSwitzerland

Personalised recommendations