The stress response is attenuated during inclement weather in parental, but not in pre-parental, Lapland longspurs (Calcarius lapponicus) breeding in the Low Arctic

Hormones and Behavior

Volumn 83, Issue , 2016, Pages 68-74

  Krause, Jesse S ^a   Pérez, Jonathan H ^a   Chmura, Helen E ^a   Meddle, Simone L ^b   Hunt, Kathleen E ^c   Gough, Laura ^d   Boelman, Natalie ^d,e   Wingfield, John C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c NEW ENGLAND AQUARIUM   (United States)

^d TOWSON UNIVERSITY   (United States)

^e Department of Earth and Environmental Sciences   (United States)

Author keywords

Corticosterone; HPA axis; Life history trade offs; Parental care; Snowstorms; Stress

Indexed keywords

CORTICOSTERONE;

ACUTE STRESS; ARCTIC; ARTICLE; BIRD; BODY CONSTITUTION; CALCARIUS LAPPONICUS; CONTROLLED STUDY; ENVIRONMENTAL STRESS; FEMALE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION STRESS; LIPID STORAGE; MALE; NONHUMAN; PARENTAL BEHAVIOR; PRIORITY JOURNAL; REPRODUCTIVE EFFORT; SEX DIFFERENCE; SNOWSTORM; WEATHER; ANIMAL; ANIMAL BEHAVIOR; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; NESTING; PASSERIFORMES; PHYSIOLOGICAL STRESS; PHYSIOLOGY; REPRODUCTION; SEASON;

ANIMALS; ARCTIC REGIONS; BEHAVIOR, ANIMAL; CORTICOSTERONE; FEMALE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; NESTING BEHAVIOR; PASSERIFORMES; PITUITARY-ADRENAL SYSTEM; REPRODUCTION; SEASONS; STRESS, PHYSIOLOGICAL; WEATHER;

EID: 84971470108     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2016.05.018     Document Type: Article

References (74)

1. Angelier F., Chastel O. Stress, prolactin and parental investment in birds: a review. Gen. Comp. Endocrinol. 2009, 163:142-148.
2. Angelier F., Wingfield J.C. Importance of the glucocorticoid stress response in a changing world: theory, hypotheses and perspectives. Gen. Comp. Endocrinol. 2013, 190:118-128.
3. Angelier F., Wingfield J.C., Parenteau C., Pellé M., Chastel O. Does short-term fasting lead to stressed-out parents? A study of incubation commitment and the hormonal stress responses and recoveries in snow petrels. Horm. Behav. 2015, 67:28-37.
4. Astheimer L.B., Buttemer W.A., Wingfield J.C. Interactions of corticosterone with feeding, activity and metabolism in passerine birds. Ornis Scand. 1992, 23:355-365.
5. Astheimer L.B., Buttemer W.A., Wingfield J.C. Seasonal and acute changes in adrenocortical responsiveness in an arctic-breeding bird. Horm. Behav. 1995, 29:442-457.
6. Bailey R.E. The incubation patch of passerine birds. The Condor 1952, 54:121-136.
7. Bókony V., Lendvai ÁZ., Liker A., Angelier F., Wingfield J.C., Chastel O. Stress response and the value of reproduction: are birds prudent parents?. Am. Nat. 2009, 173:589-598.
8. Bonier F., Moore I., Martin P., Robertson R. The relationship between fitness and baseline glucocorticoids in a passerine bird. Gen. Comp. Endocrinol. 2009, 163.
9. Boonstra R. Coping with changing northern environments: the role of the stress axis in birds and mammals. Integr. Comp. Biol. 2004, 44:95-108.
10. Boyle W.A., Norris D.R., Guglielmo C.G. Storms drive altitudinal migration in a tropical bird. Proceedings of the Royal Society of London B: Biological Sciences 2010.
11. Breuner C.W., Hahn T.P. Integrating stress physiology, environmental change, and behavior in free-living sparrows. Horm. Behav. 2003, 43:115-123.
12. Breuner C.W., Orchinik M. Seasonal regulation of membrane and intracellular corticosteroid receptors in the house sparrow brain. J. Neuroendocrinol. 2001, 13:412-420.
13. Cockrem J.F. Corticosterone responses and personality in birds: individual variation and the ability to cope with environmental changes due to climate change. Gen. Comp. Endocrinol. 2013, 190:156-163.
14. Cockrem J.F., Silverin B. Variation within and between birds in corticosterone responses of great tits (Parus major). Gen. Comp. Endocrinol. 2002, 125:197-206.
15. Cohen J. A power primer. Psychol. Bull. 1992, 112:155.
16. Custer T.W., Pitelka F.A. Demographic features of a Lapland longspur population near Barrow, Alaska. Auk 1977, 94:505-525.
17. Custer T.W., Pitelka F.A. Seasonal trends in summer diet of the Lapland longspur near Barrow, Alaska. Condor 1978, 80:295-301.
18. de Bruijn R., Romero L.M. Behavioral and physiological responses of wild-caught European starlings (Sturnus vulgaris) to a minor, rapid change in ambient temperature. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2011, 160:260-266.
19. de Bruijn R., Romero L.M. Artificial rain and cold wind act as stressors to captive molting and non-molting European starlings (Sturnus vulgaris). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2013, 164:512-519.
20. Dickens M., Romero L.M., Cyr N.E., Dunn I.C., Meddle S.L. Chronic stress alters glucocorticoid receptor and mineralocorticoid receptor mRNA expression in the European starling (Sturnus vulgaris) brain. J. Neuroendocrinol. 2009, 21:832-840.
21. Environmental Data Center Meteorological monitoring program at Toolik, Alaska 2014, Toolik Field Station, Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, AK 99775, (Retrieved March 13, 2013). http://toolik.alaska.edu/edc/abiotic_monitoring/data_query.php.
22. Harding A.A., Welcker J., Steen H., Hamer K., Kitaysky A., Fort J., Talbot S., Cornick L., Karnovsky N., Gabrielsen G., Grémillet D. Adverse foraging conditions may impact body mass and survival of a high Arctic seabird. Oecologia 2011, 167:49-59.
23. Harris H.J., Kotelevtsev Y., Mullins J.J., Seckl J.R., Holmes M.C. Intracellular regeneration of glucocorticoids by 11β-hydroxysteroid dehydrogenase (11β-HSD)-1 plays a key role in regulation of the hypothalamic-pituitary-adrenal Axis: analysis of 11β-HSD-1-deficient mice. Endocrinology 2001, 142:114-120.
24. Holberton R.L., Wingfield J.C. Modulating the corticosterone stress response: a mechanism for balancing individual risk and reproductive success in arctic-breeding sparrows?. Auk 2003, 120:1140-1150.
25. Hunt K.E., Wingfield J.C. Effect of estradiol implants on reproductive behavior of female Lapland longspurs (Calcarius lapponicus). Gen. Comp. Endocrinol. 2004, 137:248-262.
26. Jacobs J.D., Wingfield J.C. Endocrine control of life-cycle stages: a constraint on response to the environment?. Condor 2000, 102:35-51.
27. Jasper M.S., Engeland W.C. Splanchnic neural activity modulates ultradian and circadian rhythms in adrenocortical secretion in awake rats. Neuroendocrinology 1994, 59:97-109.
28. Kaiser A. A new multi-category classification of subcutaneous fat deposits of songbirds (Una Nueva Clasificación, con Multi-categorías, para los Depósitos de Grasa en Aves Canoras). J. Field Ornithol 1993, 64:246-255.
29. Kitaysky A.S., Kitaiskaia E.V., Wingfield J.C., Piatt J.F. Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks. J. Comp. Physiol. B. 2001, 171:701-709.
30. Kitaysky A., Wingfield J., Piatt J. Dynamics of food availability, body condition and physiological stress response in breeding black-legged kittiwakes. Funct. Ecol. 1999, 13:577-584.
31. Krause J.S., Chmura H.E., Pérez J.H., Quach L.N., Asmus A., Word K.R., McGuigan M.A., Sweet S.K., Meddle S.L., Gough L., Boelman N., Wingfield J. Breeding on the leading edge of a northward range expansion: differences in morphology and the stress response in the arctic Gambel's white-crowned sparrow. Oecologia 2015, 1-12.
32. Krause J.S., McGuigan M.A., Bishop V.R., Wingfield J.C., Meddle S.L. Decreases in mineralocorticoid but not glucocorticoid receptor mRNA expression during the short Arctic breeding season in free-living Gambel's white-crowned sparrow (Zonotrichia leucophrys gambelii). J. Neuroendocrinol. 2015, 27:66-75.
33. Krause J.S., Meddle S.L., Wingfield J.C. The effects of acute restraint stress on plasma levels of prolactin and corticosterone across life-history stages in a short-lived bird: Gambel's white-crowned sparrow (Zonotrichia leucophrys gambelii). Physiol. Biochem. Zool. 2015, 88:589-598.
34. Lattin C.R., Romero L.M. Seasonal variation in glucocorticoid and mineralocorticoid receptors in metabolic tissues of the house sparrow (Passer domesticus). Gen. Comp. Endocrinol. 2015, 214:95-102.
35. Lattin C.R., Breuner C.W., Romero L.M. Does corticosterone regulate the onset of breeding in free-living birds?: the CORT-flexibility hypothesis and six potential mechanisms for priming corticosteroid function. Horm. Behav. 2016, 78:107-120.
36. Lattin C.R., Waldron-Francis K., Richardson J.W., de Bruijn R., Bauer C.M., Breuner C.W., Michael Romero L. Pharmacological characterization of intracellular glucocorticoid receptors in nine tissues from house sparrow (Passer domesticus). Gen. Comp. Endocrinol. 2012, 179:214-220.
37. Lendvai Á.Z., Giraudeau M., Chastel O. Reproduction and modulation of the stress response: an experimental test in the house sparrow. Proc. R. Soc. B Biol. Sci. 2007, 274:391-397.
38. Lendvai Á.Z., Ouyang J.Q., Schoenle L.A., Fasanello V., Haussmann M.F., Bonier F., Moore I.T. Experimental food restriction reveals individual differences in corticosterone reaction norms with no oxidative costs. PLoS One 2014, 9.
39. Liebl A.L., Martin L.B. Stress hormone receptors change as range expansion progresses in house sparrows. Biol. Lett. 2013, 9.
40. Lynn S.E., Breuner C.W., Wingfield J.C. Short-term fasting affects locomotor activity, corticosterone, and corticosterone binding globulin in a migratory songbird. Horm. Behav. 2003, 43:150-157.
41. Lynn S.E., Stamplis T.B., Barrington W.T., Weida N., Hudak C.A. Food, stress, and reproduction: short-term fasting alters endocrine physiology and reproductive behavior in the zebra finch. Horm. Behav. 2010, 58:214-222.
42. Lyon B.E., Montgomerie R.D. Ecological correlates of incubation feeding: a comparative study of high arctic finches. Ecology 1987, 68:713-722.
43. Meddle S.L., Owen-Ashley N.T., Richardson M.I., Wingfield J.C. Modulation of the hypothalamic-pituitary-adrenal axis of an Arctic-breeding polygynandrous songbird, the Smith's longspur, Calcarius pictus. Proceedings of the Royal Society of London. Series B: Biological Sciences 2003, 270:1849-1856.
44. Ouyang J.Q., Hau M., Bonier F. Within seasons and among years: when are corticosterone levels repeatable?. Horm. Behav. 2011, 60:559-564.
45. Ouyang J.Q., Muturi M., Quetting M., Hau M. Small increases in corticosterone before the breeding season increase parental investment but not fitness in a wild passerine bird. Horm. Behav. 2013, 63.
46. Ouyang J.Q., Quetting M., Hau M. Corticosterone and brood abandonment in a passerine bird. Anim. Behav. 2012, 84:261-268.
47. Raouf S.A., Smith L.C., Brown M.B., Wingfield J.C., Brown C.R. Glucocorticoid hormone levels increase with group size and parasite load in cliff swallows. Anim. Behav. 2006, 71:39-48.
48. Reneerkens J., Morrison G., Ramenofsky M., Piersma T., Wingfield J.C. Baseline and stress-induced levels of corticosterone during different life cycle substages in a shorebird on the high arctic breeding grounds. Physiol. Biochem. Zool. 2002, 75:200-208.
49. Ricklefs R.E., Wikelski M. The physiology/life-history nexus. Trends in ecology &. Evolution 2002, 17:462-468.
50. Rogers C.M., Ramenofsky M., Ketterson E.D., Nolan V., Wingfield J.C. Plasma corticosterone, adrenal mass, winter weather, and season in nonbreeding populations of dark-eyed juncos (Junco hyemalis hyemalis). Auk 1993, 110:279-285.
51. Romero M.L. Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen. Comp. Endocrinol. 2002, 128:1-24.
52. Romero L.M., Reed J.M. Collecting baseline corticosterone samples in the field: is under 3 min good enough?. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2005, 140:73-79.
53. Romero L.M., Reed J.M., Wingfield J.C. Effects of weather on corticosterone responses in wild free-living passerine birds. Gen. Comp. Endocrinol. 2000, 118:113-122.
54. Romero L.M., Soma K.K., Wingfield J.C. Hypothalamic-Pituitary-Adrenal Axis Changes Allow Seasonal Modulation of Corticosterone in a Bird 1998.
55. Sapolsky R.M., Romero L.M., Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 2000, 21:55-89.
56. Silverin B. Corticosterone-binding proteins and behavioral effects of high plasma levels of corticosterone during the breeding period in the pied flycatcher. Gen Comp Endocrinol 1986, 64.
57. Smith G.T., Wingfield J.C., Veit R.R. Adrenocortical response to stress in the common diving petrel, Pelecanoides urinatrix. Physiol. Zool. 1994, 67:526-537.
58. Spée M., Beaulieu M., Dervaux A., Chastel O., Le Maho Y., Raclot T. Should I stay or should I go? Hormonal control of nest abandonment in a long-lived bird, the Adélie penguin. Horm. Behav. 2010, 58:762-768.
59. Spée M., Marchal L., Lazin D., Maho Y., Chastel O., Beaulieu M., Raclot T. Exogenous corticosterone and nest abandonment: a study in a long-lived bird, the Adélie penguin. Horm Behav 2011, 60.
60. Thierry A.-M., Massemin S., Handrich Y., Raclot T. Elevated corticosterone levels and severe weather conditions decrease parental investment of incubating Adélie penguins. Horm. Behav. 2013, 63:475-483.
61. Ulrich-Lai Y.M., Arnhold M.M., Engeland W.C. Adrenal Splanchnic Innervation Contributes to the Diurnal Rhythm of Plasma Corticosterone in Rats by Modulating Adrenal Sensitivity to ACTH 2006.
62. Vitousek M.N., Jenkins B.R., Safran R.J. Stress and success: individual differences in the glucocorticoid stress response predict behavior and reproductive success under high predation risk. Horm. Behav. 2014, 66:812-819.
63. Walker B.G., Meddle S.L., Romero L.M., Landys M.M., Reneerkens J., Wingfield J.C. Breeding on the extreme edge: modulation of the adrenocortical response to acute stress in two high arctic passerines. J. Exp. Zool. A Ecol. Genet. Physiol. 2015, 323:266-275.
64. Wingfield J.C. Influences of weather on reproductive function in female song sparrows, Melospiza melodia. J. Zool. 1985, 205:545-558.
65. Wingfield J.C. Comparative endocrinology, environment and global change. Gen. Comp. Endocrinol. 2008, 157:207-216.
66. Wingfield J.C., Kitaysky A.S. Endocrine responses to unpredictable environmental events: stress or anti-stress hormones?. Integr. Comp. Biol. 2002, 42:600-609.
67. Wingfield J.C., Sapolsky R.M. Reproduction and resistance to stress: when and how. J. Neuroendocrinol. 2003, 15:711-724.
68. Wingfield J.C., Deviche P., Sharbaugh S., Astheimer L.B., Holberton R., Suydam R., Hunt K. Seasonal changes of the adrenocortical responses to stress in redpolls, Acanthis flammea, in Alaska. J. Exp. Zool. 1994, 270:372-380.
69. Wingfield J.C., Maney D.L., Bruener C.W., Jacobs J.D., Lynn S., Ramenofsky M., Richardson R.D. Ecological bases of hormone-behavior interactions: the "emergency life history stage". Am. Zool. 1998, 38:191-206.
70. Wingfield J.C., Moore M.C., Farner D.S. Endocrine responses to inclement weather in naturally breeding populations of white-crowned sparrows (Zonotrichia leucophrys pugetensis). The Auk 1983, 56-62.
71. Wingfield J.C., O'Reilly K.M., Astheimer L.B. Modulation of the adrenocortical responses to acute stress in Arctic birds: a possible ecological basis. Am. Zool. 1995, 35:285-294.
72. Wingfield J.C., Owen-Ashley N., Benowitz-Fredericks Z.M., Lynn S., Hahn T., Wada H., Breuner C., Meddle S., Romero L.M. Arctic spring: the arrival biology of migrant birds. Acta Zool. Sin. 2004, 50:948-960.
73. Wingfield J.C., Suydam R., Hunt K. The adrenocortical responses to stress in snow buntings (Plectrophenax nivalis) and Lapland longspurs (Calcarius lapponicus) at barrow, Alaska. Comp. Biochem. Physiol. C: Pharmacol. Toxicol. Endocrinol. 1994, 108:299-306.
74. Wingfield J.C., Vleck C.M., Moore M.C. Seasonal changes of the adrenocortical response to stress in birds of the Sonoran desert. J. Exp. Zool. 1992, 264:419-428.