Employing individual measures of baseline glucocorticoids as population-level conservation biomarkers: Considering within-individual variation in a breeding passerine

Conservation Physiology

Volumn 4, Issue 1, 2016, Pages

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

^a UNIVERSITY OF WINDSOR   (Canada)

^b UNIVERSITY OF WINDSOR   (Canada)

Author keywords

Biomarker; Consistency; Corticosterone; Individual variation; Repeatability; Tree swallow

Indexed keywords

EID: 85017247922     PISSN: None     EISSN: 20511434     Source Type: Journal    
DOI: 10.1093/conphys/cow048     Document Type: Article

References (98)

1. Abdi H (2004) Factor rotations in factor analyses. In M Lewisbeck, A Bryman, T Futing Liao, eds, Encyclopedia for Research Methods for the Social Sciences. Sage Publications, Inc., Thousand Oaks, CA, USA, pp 792–795.
2. 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: 846–849.
3. Ardia DR, Clotfelter ED (2007) Individual quality and age affect responses to an energetic constraint in a cavity-nesting bird. Behav Ecol 18: 259–266.
4. Arlettaz R, Nussle S, Baltic M, Vogel P, Palme R, Jenni-Eiermann S, Patthey P, Genoud M (2015) Disturbance of wildlife by outdoor winter recreation: allostatic stress response and altered activity-energy budgets. Ecol Appl 25: 1197–1212.
5. Ashley EP, Robinson JT (1996) Road mortality of amphibians, reptiles and other wildlife on the Long Point Causeway, Lake Erie, Ontario. Can Field Nat 110: 403–412.
6. Ayres KL, Booth RK, Hempelmann JA, Koski KL, Emmons CK, Baird RW, Balcomb-Bartok K, Hanson MB, Ford MJ, Wasser SK (2012) Distinguishing the impacts of inadequate prey and vessel traffic on an endangered killer whale (Orcinus orca) population. PLoS One 7, e36842.
7. Baker MR, Gobush KS, Vynne CH (2013) Review of factors influencing stress hormones in fish and wildlife. J Nat Conserv 21: 309–318.
8. Bell AM (2007) Future directions in behavioural syndromes research. Proc Biol Sci 274: 755–761.
9. Biro PA, Stamps JA (2015) Using repeatability to study physiological and behavioural traits: ignore time-related change at your peril. Anim Behav 105: 223–230.
10. Bonier F, Martin PR, Moore IT, Wingfield JC (2009a) Do baseline glucocorticoids predict fitness? Trends Ecol Evol 24: 634–642.
11. Bonier F, Moore IT, Martin PR, Robertson RJ (2009b) The relationship between fitness and baseline glucocorticoids in a passerine bird. Gen Comp Endocrinol 163: 208–213.
12. Bonier F, Moore IT, Robertson RJ (2011) The stress of parenthood? Increased glucocorticoids in birds with experimentally enlarged broods. Biol Lett 7: 944–946.
13. Bradshaw C, Brook B (2010) The conservation biologist’s toolbox – principles for the design and analysis of conservation studies. In NS Sodhi, P Ehrlich, eds, Conservation Biology for All. Oxford University Press, New York, NY, USA, pp 313–336.
14. Brommer JE, Merilä J, Sheldon BC, Gustafsson L (2005) Natural selection and genetic variation for reproductive reaction norms in a wild bird population. Evolution 59: 1362–1371.
15. 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: 2844–2853.
16. Carey C (2005) How physiological methods and concepts can be useful in conservation biology. Integr Comp Biol 45: 4–11.
17. Cockrem JF (2013) Individual variation in glucocorticoid stress responses in animals. Gen Comp Endocrinol 181: 45–58.
18. Cook KV, O’Connor CM, Gilmour KM, Cooke SJ (2011) The glucocorticoid stress response is repeatable between years in a wild teleost fish. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 197: 1189–1196.
19. Cooke SJ, Sack L, Franklin CE, Farrell AP, Beardall J, Wikelski M, Chown SL (2013) What is conservation physiology? Perspectives on an increasingly integrated and essential science. Conserv Physiol 1: cot001; doi:10.1093/conphys/cot001.
20. D’Agostino RB, Russell HK (2005) Scree test. In P Armitage, T Colton, eds, Encyclopedia of Biostatistics. John Wiley & Sons, Ltd, New York, NY, USA.
21. Dantzer B, Fletcher QE, Boonstra R, Sheriff MJ (2014) Measures of physiological stress: a transparent or opaque window into the status, management and conservation of species? Conserv Physiol 2: cou023; doi:10.1093/conphys/cou023.
22. Dickens MJ, Romero LM (2013) A consensus endocrine profile for chronically stressed wild animals does not exist. Gen Comp Endocrinol 191: 177–189.
23. Dijak WD, Thompson FR III (2000) Landscape and edge effects on the distribution of mammalian predators in Missouri. J Wildl Manag 64: 209–216.
24. Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82: 39–54.
25. Dingemanse NJ, Edelaar P, Kempenaers B (2010) Why is there variation in baseline glucocorticoid levels? Trends Ecol Evol 25: 261–262.
26. Durner GM, Gates JE (1993) Spatial ecology of black rat snakes on Remington Farms, Maryland. J Wildl Manag 57: 812–826.
27. Ellenberg U, Mattern T, Seddon PJ, Jorquera GL (2006) Physiological and reproductive consequences of human disturbance in Humboldt penguins: the need for species-specific visitor management. Biol Conserv 133: 95–106.
28. Ellenberg U, Setiawan AN, Cree A, Houston DM, Seddon PJ (2007) Elevated hormonal stress response and reduced reproductive output in Yellow-eyed penguins exposed to unregulated tourism. Gen Comp Endocrinol 152: 54–63.
29. Escribano-Avila G, Pettorelli N, Virgós E, Lara-Romero C, Lozano J, Barja I, Cuadra FS, Puerta M (2013) Testing Cort-Fitness and Cort-Adaptation hypotheses in a habitat suitability gradient for roe deer. Acta Oecologica 53: 38–48.
30. Fefferman NH, Romero LM (2013) Can physiological stress alter population persistence? A model with conservation implications. Cons Physiol 1: cot012; doi:10.1093/conphys/cot012.
31. Finch DM (1990) Effects of predation and competitor interference on nesting success of House Wrens and Tree Swallows. Condor 92: 674.
32. Garcia Pereira RJ, Barbanti Duarte JM, Negrão JA (2006) Effects of environmental conditions, human activity, reproduction, antler cycle and grouping on fecal glucocorticoids of free-ranging Pampas deer stags (Ozotoceros bezoarticus bezoarticus). Horm Behav 49: 114–122.
33. Ghalambor CK, Mckay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21: 394–407.
34. Ghilain A, Bélisle M (2008) Breeding success of tree swallows along a gradient of agricultural intensification. Ecol Appl 18: 1140–1154.
35. Hothorn T, Zeileis A, Farebrother RW, Cummins C, Millo G, Mitchell D (2015) lmtest: Testing Linear Regression Models. R package version 0.9–34.
36. James FC, McCulloch CE (1990) Multivariate analysis in ecology and systematics: Panacea or Box? Annu Rev Ecol Syst 21: 129–166.
37. Joly K, Wasser SK, Booth R (2015) Non-invasive assessment of the interrelationships of diet, pregnancy rate, group composition, and physiological and nutritional stress of barren-ground caribou in late winter. PLoS One 10: e0127586.
38. Killen SS, Adriaenssens B, Marras S, Claireaux G, Cooke SJ (2016) Context dependency of trait and its relevance for management and conservation of fish populations. Conserv Physiol 4: cow007; doi:10.1093/conphys/cow007.
39. Kluen E, Brommer JE (2013) Context-specific repeatability of personality traits in a wild bird: a reaction-norm perspective. Behav Ecol 24: 650–658.
40. Kociolek AV, Clevenger AP, St Clair CC, Proppe DS (2011) Effects of road networks on bird populations. Conserv Biol 25: 241–249.
41. Landys MM, Ramenofsky M, Wingfield JC (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.
42. Leimeister S (2010) IT Outsourcing Governance: Client Types and Their Management Strategies. Gabler Verlag, Wiesbaden, Germany.
43. Lennox R, Cooke SJ (2014) State of the interface between conservation and physiology: a bibliometric analysis. Conserv Physiol 2: cou003; doi:10.1093/conphys/cou003.
44. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104: 116–121.
45. Lindström KM, Hawley DM, Davis AK, Wikelski M (2005) Stress responses and disease in three wintering house finch (Carpodacus mexicanus) populations along a latitudinal gradient. Gen Comp Endocrinol 143: 231–239.
46. Love OP, Williams TD (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.
47. Love OP, Breuner CW, Vézina F, Williams TD (2004) Mediation of a corticosterone-induced reproductive conflict. Horm Behav 46: 59–65.
48. Love OP, Madliger CL, Bourgeon S, Semeniuk CAD, Williams TD (2014) Evidence for baseline glucocorticoids as mediators of reproductive investment in a wild bird. Gen Comp Endocrinol 199: 65–69.
49. Lynch M, Walsh B (1998) Genetics and Analysis of Quantitative Traits. Sinauer Associates, Sunderland, MA.
50. McCarty JP (1995) Effects of short-term changes in environmental conditions on the foraging ecology and reproductive success of tree swallows, Tachycineta bicolor. PhD Dissertation. Cornell University, Ithaca, NY, USA.
51. McCarty JP, Winkler DW (1999) Foraging ecology and diet selectivity of tree swallows feeding nestlings. Condor 101: 246–254.
52. McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43: 2–15.
53. Madliger CL, Love OP (2014) The need for a predictive, context-dependent approach to the application of stress hormones in conservation. Conserv Biol 28: 283–287.
54. Madliger CL, Love OP (2015) The power of physiology in changing landscapes: considerations for the continued integration of conservation and physiology. Integr Comp Biol 55: 545–553.
55. Madliger CL, Cooke SJ, Crespi EJ, Funka JL, Hultines KR, Hunt KE, Rohr JR, Sinclair BJ, Suski CD, Willis CKR et al. (2016) Success stories and emerging themes in conservation physiology. Conserv Physiol. 4: doi:10.1093/conphys/cov057.
56. Madliger CL, Love OP (2016) Do baseline glucocorticoids simultaneously represent fitness and environmental quality in a declining aerial insectivore? Oikos. doi:10.1111/oik.03354.
57. Madliger CL, Semeniuk CA, Harris CM, Love OP (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.
58. 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: 284–292.
59. Martin JGA, Nussey DH, Wilson AJ, Réale D (2011) Measuring individual differences in reaction norms in field and experimental studies: a power analysis of random regression models. Methods Ecol Evol 2: 362–374.
60. Martin LB, Liebl AL (2014) Physiological flexibility in an avian range expansion. Gen Comp Endocrinol 206: 227–234.
61. Montiglio PO, Garant D, Thomas D, Réale D (2010) Individual variation in temporal activity patterns in open-field tests. Anim Behav 80: 905–912.
62. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85: 935–956.
63. Narayan EJ, Hero JM (2013) Repeatability of baseline corticosterone and acute stress responses to capture, and patterns of reproductive hormones in vitellogenic and non‐vitellogenic female Fijian ground frog (Platymantis vitiana). J Exp Zool A Ecol Gen Physiol 319: 471–481.
64. Narayan EJ, Cockrem JF, Hero JM (2013) Are baseline and short-term corticosterone stress responses in free-living amphibians repeatable? Comp Biochem Physiol A Mol Integr Physiol 164: 21–28.
65. Nathiya G, Punitha SC, Punithavalli M (2010) An analytical study on behavior of clusters using K means, EM and K* means algorithm. Int J Comput Sci Inf Secur 7: 185–190.
66. Nebel S, Mills A, McCracken JD, Taylor PD (2010) Declines of aerial insectivores in North America follow a geographic gradient. Avian Conserv Ecol 5. doi:10.5751/ACE-00391-050201.
67. Nussey DH, Wilson AJ, Brommer JE (2007) The evolutionary ecology of individual phenotypic plasticity in wild populations. J Evol Biol 20: 831–844.
68. Ouyang JQ, Hau M, Bonier F (2011a) Within seasons and among years: when are corticosterone levels repeatable? Horm Behav 60: 559–564.
69. Ouyang JQ, Sharp PJ, Dawson A, Quetting M, Hau M (2011b) Hormone levels predict individual differences in reproductive success in a passerine bird. Proc Biol Sci 278: 2537–2545.
70. Ouyang JQ, Sharp P, Quetting M, Hau M (2013) Endocrine phenotype, reproductive success and survival in the great tit, Parus major. J Evol Biol 26: 1988–1998.
71. Parren SG (1991) Evaluation of nest-box sites selected by Eastern Bluebirds, Tree Swallows, and House Wrens. Wildl Soc Bull 19: 270–277.
72. Patterson SH, Winkler DW, Breuner CW (2011) Glucocorticoids, individual quality and reproductive investment in a passerine bird. Anim Behav 81: 1239–1247.
73. Pavitt AT, Walling CA, Möstl E, Pemberton JM, Kruuk LEB (2015) Cortisol but not testosterone is repeatable and varies with reproductive effort in wild red deer stags. Gen Comp Endocrinol 222: 62–68.
74. Piersma T, Drent J (2003) Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18: 228–233.
75. Pinheiro J, Bates D (2000) Mixed-Effects Models in S and S-PLUS. Springer-Verlag, New York, NY, USA.
76. R Development Core Team. (2015) R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
77. Reijnen R, Foppen R (2006) Impact of road traffic on breeding bird populations. In PJ Davenport, JL Davenport, eds, The Ecology of Transportation: Managing Mobility for the Environment. Springer, Dordrecht, The Netherlands, pp 255–274.
78. Rendell WB, Robertson RJ (1990) Influence of forest edge on nest-site selection by tree swallows. Wilson Bull 102: 634–644.
79. Rensel MA, Schoech SJ (2011) Repeatability of baseline and stress-induced corticosterone levels across early life stages in the Florida scrub-jay (Aphelocoma coerulescens). Horm Behav 59: 497–502.
80. Robertson RJ, Stutchbury BJ, Cohen RR (1992) The Birds of North America Online – Tree Swallow (Tachycineta bicolor). http://bna.birds.cornell.edu/bna/species/011/articles/introduction.
81. Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128: 1–24.
82. Romero LM, Reed JM (2005) Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp Biochem Physiol A Mol Integr Physiol 140: 73–79.
83. 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.
84. Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R (2011) Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166: 869–887.
85. Sparkman AM, Bronikowski AM, Williams S, Parsai S, Manhart W, Palacios MG (2014) Physiological indices of stress in wild and captive garter snakes: correlations, repeatability, and ecological variation. Comp Biochem Physiol A Mol Integr Physiol 174: 11–17.
86. Stevenson RD, Tuberty SR, Wingfield JC (2005) Ecophysiology and conservation: the contribution of endocrinology and immunology–introduction to the symposium. Integr Comp Biol 45: 1–3.
87. Stutchbury BJ, Rohwer S (1990) Molt patterns in the tree swallow (Tachycineta bicolor). Can J Zool 68: 1468–1472.
88. Taff CC, Vitousek MN (2016) Endocrine flexibility: optimizing phenotypes in a dynamic world? Trends Ecol Evol 31: 476–488.
89. Walker BG, Boersma PD, Wingfield JC (2005) Field endocrinology and conservation biology. Integr Comp Biol 45: 12–18.
90. Wasser SK, Keim JL, Taper ML, Lele SR (2011) The influences of wolf predation, habitat loss, and human activity on caribou and moose in the Alberta oil sands. Front Ecol Environ 9: 546–551.
91. Weatherhead PJ, Charland MB (1985) Habitat selection in an Ontario population of the snake, Elaphe obsoleta. J Herpetol 19: 12–19.
92. Wikelski M, Cooke SJ (2006) Conservation physiology. Trends Ecol Evol 21: 38–46.
93. Williams TD (2008) Individual variation in endocrine systems: moving beyond the ‘tyranny of the Golden Mean’. Philos Trans R Soc B Biol Sci 363: 1687–1698.
94. Wingfield JC (2005) The concept of allostasis: coping with a capricious environment. J Mammal 86: 248–254.
95. Wingfield JC, Kitaysky AS (2002) Endocrine responses to unpredictable environmental events: stress or anti-stress hormones? Integr Comp Biol 42: 600–609.
96. Wingfield JC, Hunt KE, Breuner CW, Dunlap K, Fowler GS, Freed L, Lepson J (1997) Environmental stress, field endocrinology and conservation biology. In J Clemmons, R Buchholz, eds, Behavioral Approaches to Conservation in the Wild. Cambridge University Press, Cambridge, UK.
97. Winkler DW, Allen PE (1995) Effects of handicapping on female condition and reproduction in tree swallows (Tachycineta bicolor). Auk 112: 737–747.
98. Winkler DW, Wrege PH, Allen PE, Kast TL, Senesac P, Wasson MF, Llambías PE, Ferretti V, Sullivan PJ (2004) Breeding dispersal and philopatry in the tree swallow. Condor 106: 768–776.