Physiological and behavioral responses of migrants to environmental cues

Journal of Ornithology

Volumn 153, Issue SUPPL. 1, 2012, Pages 181-191

  Ramenofsky, Marilyn ^a   Cornelius, Jamie M ^b   Helm, Barbara ^b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^c UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Environmental conditions; Facultative migrants; Hypothalamic pituitary axis; Obligate migrants; Predictable cues; Unpredictable cues

Indexed keywords

BEHAVIORAL RESPONSE; BIRD; ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL CUE; MIGRATORY BEHAVIOR; PHYSIOLOGICAL RESPONSE;

EID: 84865815981     PISSN: 21937192     EISSN: 21937206     Source Type: Journal    
DOI: 10.1007/s10336-012-0817-3     Document Type: Review

References (113)

1. Adriaensen F, Dhondt AA (1990) Population dynamics and partial migration of the European robin (Erithacus rubecula) in different habitats. J Anim Ecol 59: 1077-1090.
2. Astheimer LB, Buttemer WA, Wingfield JC (1992) Interactions of corticosterone with feeding, activity and metabolism in passerine birds. Orn Scand 23: 355-365.
3. Baker JR (1938) The evolution of breeding season. In: DeBeer GB (ed) Evolution: essays on aspects of evolutionary biology. Oxford University Press, Oxford, pp 161-177.
4. Battley PF (2006) Consistent annual schedules in a migratory shorebird. Biol Lett 2(4): 517-520. doi: 10. 1098/rsbl. 2006. 0535.
5. Berthold P (1977) Über eine mögliche endogene Steuerung der Zugdisposition beim Fichtenkreuzschnabel, Loxia curvirostra. J Ornithol 118: 203-204.
6. Bluhm CK, Schwabl H, Schwabl I, Perera A, Follett BK, Goldsmith AR, Gwinner E (1991) Variation in hypothalamic gonadotrophin-releasing hormone content plasma and pituitary LH, and in vitro testosterone release in a long-distance migratory bird, the garden warbler (Sylvia borin), under constant photoperiods. J Endocrinol 128: 339-345.
7. Boswell T (2005) Regulation of energy balance in birds by the neuroendocrine hypothalamus. J Poult Sci 42: 161-181.
8. Boswell T, Hall MR, Goldsmith AR (1993) Annual cycles of migratory fattening, reproduction and moult in European quail (Coturnix coturnix). J Zool Lond 231: 627-644.
9. Boswell T, Hall MR, Goldsmith AR (1995a) Testosterone is secreted extragonadally by European quail maintained on short days. Physiol Zool 68: 967-984.
10. Boswell T, Richardson RD, Seeley RJ, Ramenofsky M, Wingfield JC, Friedman MI, Woods SC (1995b) Regulation of food intake by metabolic fuels in white-crowned sparrows. Am J Physiol 269: R1462-R1468.
11. Both C (2010) Flexibility of timing of avian migration to climate change masked by environmental constraints en route. Curr Biol 20: 243-248.
12. Breuner CW, Hahn TP (2003) Integrating stress physiology, environmental change, and behaviour in free-living sparrows. Horm Behav 43: 115-123. doi: 10. 1016/s0018-506x(02)00020-x.
13. Chan K (2005) Partial migration in the silvereye (Zosteropidae: Aves): pattern, synthesis, and theories. Ethol Ecol Evol 17: 349-363.
14. Claes SJ (2004) Corticotropin-releasing hormones (CRH) in psychiatry: from stress to psychopathology. Ann Med 36: 50-61.
15. Conklin JR, Battley PF, Potter MA, Fox JW (2010) Breeding latitude drives individual schedules in a trans-hemispheric migrant bird. Nat Commun 1(6): 67. doi: 10. 1038/ncomms1072.
16. Coppack T, Pulido F (2004) Photoperiodic response and the adaptability of avian life cycles to environmental change. Adv Ecol Res 35: 131-150. doi: 10. 1016/S0065-2504(04)35007-5.
17. Cornelius J (2009) Annual schedules, environmental cues and stress physiology in an irruptive, nomadic songbird, the red crossbill (Loxia curvirostra). PhD thesis, University of California, Davis.
18. Cornelius JM, Breuner CW, Hahn TP (2010) Under a neighbour's influence: public information affects stress hormones and behaviour of a songbird. Proc R Soc Lond B 277: 2399-2404.
19. Dallimer MJ, Jones P (2002) Migration orientation behaviour of the red-billed quelea Quelea quelea. J Avian Biol 33: 89-94.
20. Dawson A, Hinsley S, Ferns P, Bonser R, Eccleston L (2000) Rate of moult affects feather quality: a mechanism linking current reproductive effort to future survival. Proc R Soc Lond B 267: 2093-2098.
21. Dawson A, King VM, Bentley GE, Ball GR (2001) Photoperiodic control of seasonality in birds. J Biol Rhythm 16: 365-380.
22. Denbow DM, Duke GE, Chaplin SB (1988) Food intake, gastric secretion, and motility as affected by avian pancreatic polypeptide administered centrally in chickens. Peptides 9: 449-454.
23. Deviche P (1992) Testosterone and opioids interact to regulate feeding in a male migratory songbird. Horm Behav 26: 394-405.
24. Deviche P, Sharp PJ (2001) Reproductive endocrinology of a free-living, opportunistically breeding passerine (white-winged crossbill, Loxia leucoptera). Gen Comp Endocrinol 123: 268-279.
25. Dingle H (2008) Bird migration in the southern hemisphere: a review comparing continents. Emu 108: 341-359.
26. Duriez O, Bauer S, Destin A, Madsen J, Nolet BA, Stillman RA, Klaassen M (2009) What decision rules might pink-footed geese use to depart on migration? An individual-based model. Behav Ecol 20: 560-569.
27. Falsone K, Jenni-Eiermann S, Jenni L (2009) Corticosterone in migrating songbirds during endurance flight. Horm Behav 56: 548-556.
28. Farner DS (1955) The annual stimulus for migration: experimental and physiologic aspects. In: Wolfson A (ed) Recent studies in avian biology. University of Illinois, Urbana, pp 198-237.
29. Farner DS, Donham RS, Moore MC, Lewis RA (1980) The temporal relationship between the cycle of testicular development and molt in the White-crowned sparrow, Zonotrichialeucophrys gambelii. Auk 97: 63-75.
30. Fusani L, Cardinale M, Schwabl I, Goymann W (2011) Food availability but not melatonin affects nocturnal restlessness in a wild migrating passerine. Horm Behav 59: 187-192.
31. Gauthreaux SA Jr. (1991) The flight behaviour of migrating birds in changing wind fields: radar and visual analyses. Am Zool 31: 187-204.
32. Gwinner E (1988) Photorefractoriness in equatorial migrants. Proc Int Ornithol Congr 19: 626-633.
33. Gwinner E (1996) Circadian and circannual programs in avian migration. J Exp Biol 199: 39-48.
34. Hahn TP (1998) Reproductive seasonality in an opportunistic breeder, the red Crossbill, Loxia curvirostra. Ecology 79: 2365-2375.
35. Hahn TP, MacDougall-Shackleton SA (2008) Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response system of birds. Philos Trans R Soc Lond B 363: 267-286.
36. Hahn TP, Boswell T, Wingfield JC, Ball GF (1997) Temporal flexibility in avian reproduction. Patterns and mechanisms. In: Nolan V, Ketterson ED, Thompson CF (eds) Current ornithology. Plenum, New York, pp 39-80.
37. Hahn TP, Sockman KW, Breuner CW, Morton ML (2004) Facultative altitudinal movements by mountain white-crowned sparrows (Zonotrichia leucophrys oriantha) in the Sierra Nevada. Auk 121: 1269-1281.
38. Hahn TP, Cornelius JM, Sewall KB, Kelsey TR, Hau M, Perfito N (2008) Environmental regulation of annual schedules in opportunistically-breeding songbirds: adaptive specialization or variations on a theme of white-crowned sprarow? Gen Comp Endocrinol 157: 217-226.
39. Hahn TP, Watts HE, Cornelius JM, Brazeal KR, MacDougall-Shackleton SA (2009) Evolution of environmental cue response mechanisms: adaptive variation in photorefractoriness. Gen Comp Endocrinol 163: 193-200. doi: S0016-6480(09)00163-4[pii].
40. Hamner WM, Stocking J (1970) Why don't bobolinks breed in Brazil? Ecology 51: 743-751.
41. Hau M, Wikelski M, Gwinner H, Gwinner E (2004) Timing of reproduction in a Darwins' finch: temporal opportunism under spatial constraints. Oikos 106: 489-500.
42. Helm B (2006) Zugunruhe of migratory and non-migratory birds in a circannual context. J Avian Biol 37: 533-540.
43. Helm B, Gwinner E (2005) Carry-over effects of day length during spring migration. J Ornithol 146: 348-354. doi: 10. 1007/s10336-005-0009-5.
44. Helm B, Gwinner E (2006) Migratory restlessness in an equatorial nonmigratory bird. PLoS Biol 4: 611-614.
45. Helm B, Piersma T, van der Jeugd H (2006) Sociable schedules: interplay between avian seasonal and social behaviour. Anim Behav 72: 1215.
46. Helm B, Schwabl I, Gwinner E (2009) Circannual basis of geographically distinct bird schedules. J Exp Biol 212: 1259-1269.
47. Helms CW (1963) The annual cycle and Zugunruhe in birds. Proc Int Ornithol Congr 13: 925-939.
48. Jenni L, Kéry M (2003) Timing of autumn bird migration under climate change: advances in long-distance migrants, delays in short-distance migrants. Proc R Soc Lond B 270: 1467-1471.
49. Jenni L, Schaub M (2003) Behavioural and physiological reaction to environmental variation in bird migration: a review. In: Berthold PEGES (ed) Bird migration. Springer, Berlin, pp 155-171.
50. Jenni L, Winkler R (1994) Moult and ageing of European passerines. Academic, London.
51. King JR, Farner DS (1963) The relationship of fat deposition to Zugunruhe and migration. Condor 65: 200-223.
52. Knudsen E, Lindén A, Both C, Jonzén N, Pulido F, Saino N, Sutherland WJ, Bach LA, Coppack T, Ergon T, Gienapp P, Gill JA, Gordo O, Hedenström A, Lehikoinen E, Marra PP, Møller AP, Nilsson ALK, Péron G, Ranta E, Rubolini D, Sparks TH, Spina F, Studds CE, Sæther SA, Tryjanowski P, Stenseth NC (2011) Challenging claims in the study of migratory birds and climate change. Biol Rev 86: 928-946. doi: 10. 1111/j. 1469-185X. 2011. 00179. x.
53. Kuenzel WJ, McMurtry J (1988) Neuropeptide Y: brain localization and central effects on plasma insulin levels in chicks. Physiol Behav 44: 669-678.
54. Kullberg C, Lind J, Fransson T, Jakobsson S, Vallin A (2003) Magnetic cues and time of season affect fuel deposition in migratory thrush nightingales (Luscinia luscinia). Proc R Soc Lond B 270: 373-378.
55. Landys-Ciannelli MM, Landys-Ciannelli MM, Ramenofsky M, Piersma T, Jukema J, Wingfield JC, Castricum Ringing Group (2002) Baseline and stress-induced plasma corticosterone during long-distance migration in the bar-tailed godwit, Limosa lapponica. Physiol Biochem Zool 75: 101-110.
56. Lohmus M, Sandberg R, Holberton RL, Moore FR (2003) Corticosterone levels in relation to migratory readiness in red-eyed vireos (Vireo olivaceus). Behav Ecol Sociobiol 54: 233-239.
57. Lynn SE, Breuner CW, Wingfield JC (2003) Short-term fasting affects locomotor activity, corticosterone, and corticosterone binding globulin in a migratory songbird. Horm Behav 43: 150-157.
58. Marsh RL (1984) Adaptations of the gray catbird Dumetella carolinensis to long-distance migration: flight muscle hypertrophy associated with elevated body mass. Physiol Zool 57: 105-117.
59. McFarlan JT, Bonen A, Guglielmo CG (2009) Seasonal upregulation of fatty acid transporters in flight muscles of migratory white-throated sparrows (Zonotrichia albicollis). J Exp Biol 212: 2934-2940.
60. Moore MC, Donham R, Farner DS (1982) Physiological preparation for autumnal migration in white-crowned sparrows. Condor 84: 410-419.
61. Morton ML (1992) Effects of sex and birth date on premigration biology, migration schedules, return rates and natal dispersal in the mountain white-crowned sparrows. Condor 94: 117-133.
62. Morton ML (2002) The mountain white-crowned sparrow: migration and reproduction at high altitude. Stud Avian Biol 24: 236.
63. Morton ML, Mewaldt LR (1962) Some effects of castration on a migratory sparrow (Zonotrichia atricapilla). Physiol Zool 35: 237-247.
64. Newton I (2008) The migration ecology of birds. Academic, Oxford.
65. Newton I (2011) Obligate and facultative migration in birds: ecological aspects. J Ornithol. doi: 10. 1007/s10336-011-0765-3.
66. Nicholls TJ, Goldsmith AR, Dawson A (1988) Photorefractoriness in birds and comparison with mammals. Physiol Rev 68: 133-176.
67. Noskov G, Rymkevich T, Iovchenko N (1999) Intraspecific variation of molt: adaptive significance and ways of realisation. Proceedings of the 22nd international ornithological congress, vol 22. BirdLife South Africa, Johannesburg, pp 544-563.
68. Palacín C, Alonso JC, Alonso JA, Magaña M, Martín CA (2011) Cultural transmission and flexibility of partial migration patterns in a long-lived bird, the great bustard Otis tarda. J Avian Biol 42: 301-308. doi: 10. 1111/j. 1600-048X. 2011. 05395. x.
69. Perfito N, Zann RA, Bentley GE, Hau M (2007) Opportunism at work: hatibtat predictability affects reproductive readiness in free-living zebra finches. Funct Ecol 21: 291-301.
70. Perrins CM (1970) The timing of birds' breeding seasons. Ibis 112: 242-255.
71. Piersma T, van Gils JA (2011) The flexible phenotype: a body-centred integration of ecology, physiology and behaviour. Oxford University Press, Oxford.
72. Piersma T, Everaarts JM, Jukema J (1996) Build-up of red blood cells in refuelling bar-tailed godwits in relation to individual migratory quality. Condor 98: 363-370.
73. Piersma T, Reneerkens J, Ramenofsky M (2000) Baseline corticosterone peaks in shorebirds with maximal energy stores for migration: a general preparatory mechanism for rapid behavioural and metabolic transitions? Gen Comp Endocrinol 120: 118-126.
74. Piersma T, Brugge M, Spaans B, Battley PF (2008) Endogenous circannual rhythmicity in body mass, molt, and plumage of great knots (Calidris tenuirostris). Auk 125: 140-148. doi: 10. 1525/auk. 2008. 125. 1. 140.
75. Pravosudov VV, Kitaysky AS, Wingfield JC, Clayton NS (2001) Long-term unpredictable foraging conditions and physiological stress response in mountain chickadees (Poecile gambeli). Gen Comp Endocrinol 123: 324-331.
76. Price E, Staples JF, Milligan CL, Guglielmo CG (2011) Carnitine palmitoyl transferase activity and whole muscle oxidation rates vary with fatty acid substrate in avian flight muscles. J Comp Physiol B 181: 565-573.
77. Ramenofsky M (2011) Hormones in migration and reproductive cycles of birds. In: Norris D, Lopez KH (eds) Hormones and reproduction in vertebrates. Academic, San Diego, pp 205-236.
78. Ramenofsky M, Wingfield JC (2006) Behavioural and physiological conflicts in migrants: the transition between migration and breeding. J Ornithol 147: 135-145.
79. Ramenofsky M, Wingfield JC (2007) Regulation of migration. Bioscience 57: 135-143.
80. Ramenofsky M, Moffat J, Bentley GE (2008) Corticosterone and migratory behaviour of captive white-crowned sparrows. International proceedings of ICA-CPB, pressures of life: molecules to migration, pp. 575-582.
81. Reneerkens J, Morrison RI, Ramenofsky M, Piersma T, Wingfield JC (2002a) Baseline and stress-induced levels of corticosterone after a long migratory flight, preparation for breeding and during incubation of a high arctic breeding shorebird (red knot, Calidris canutus). Physiol Biochem Zool 75: 200-208.
82. Reneerkens J, Ramenofsky M, Piersma T (2002b) An experimental test of the relationship between temporal variability of feeding opportunities and baseline levels of corticosterone in a shorebird. J Exp Zool 293: 81-88.
83. Richardson WJ (1990) Timing of bird migration in relation to weather. In: Gwinner E (ed) Bird migration, physiology and ecophysiology. Springer, Berlin, pp 78-101.
84. Richardson RD, Boswell T, Raffety BD, Seeley RJ, Wingfield JC, Woods SC (1995) NPY increases food intake in white-crowned sparrows: effect in short and long photoperiods. Am J Physiol Regul Integr Comp Physiol 268: 1418-1422.
85. Romero LM, Dickens MJ, Cyr NE (2009) The reactive scope model-a new model integrating homeostais, allostasis and stress. Gen Comp Endocrinol 55: 375-389.
86. Rowan W (1926) On photoperiodism, reproductive periodicity and the annual migrations of birds and certain fishes. Proc Boston Soc Nat Hist 38: 147-189.
87. Schwabl H, Farner DS (1989) Dependency on testosterone of photoperiodically-induced vernal fat deposition in female white-crowned sparrows. Condor 91: 108-112.
88. Silverin B (1997) The stress response and autumn dispersal behaviour in willow tits. Anim Behav 53: 451-459.
89. Smith JW, Benkman CW, Coffey K (1999) The use and misuse of public information by foraging red crossbills. Behav Ecol 10: 54-62.
90. Stetson M, Erickson JE (1972) Hormonal control of photoperiodically induced fat deposition in white-crowned sparrows. Gen Comp Endocrinol 19: 355-362. doi: 10. 1016/0016-6480(72)90118-9.
91. Studds CE, Marra PP (2011) Rainfall-induced changes in food availability modify the spring departure programme of a migratory bird. Proc R Soc Lond B 278: 3437-3443. doi: 10. 1098/rspb. 2011. 0332.
92. Terrill SB (1987) Social dominance and migratory restlessness in the dark-eyed junco (Junco hyemalis). Behav Ecol Sociobiol 21: 1-11.
93. Terrill SB (1990) Ecophysiological aspects of movements by migrants in the wintering quarters. In: Gwinner E (ed) Bird migration. Physiology and ecophysiology. Springer, Berlin, pp 130-143.
94. Terrill SB, Ohmart RD (1984) Facultative extension of fall migration by yellow-rumped warblers (Dendroica coronata). Auk 101: 427-438.
95. Tewary PD, Kumar V (1981) Effects of castration on photoperiodically induced weight gain, in a migratory finch: black-headed bunting (Emberiza melanocephala) (Aves). Indian J Exp Biol 19: 469-471.
96. Thapliyal JP, Lal P, Pati AK, Gupta BBP (1983) Thyroid and gonad in the oxidative metabolism, erythyropoiesis, and light response of migratory red-headed bunting, Emberiza bruniceps. Gen Comp Endocrinol 51: 444-453.
97. Tonra CM, Marra PP, Holberton RL (2011) Early elevation of testosterone advances migratory preparation in a songbird. J Expertl Biol 214: 2761-2767.
98. Végvári Z, Barta Z, Mustakallio P, Szkékely T (2011) Consistent avoidance of human disturbance over large geographical distances by a migratory bird. Biol Lett 7: 814-817. doi: 10. 1098/rsbl. 2011. 0295 (online early).
99. Visser ME, Caro SP, van Oers K, Schaper SV, Helm B (2010) Phenology, seasonal timing and circannual rhythms: towards a unified framework. Philos Trans R Soc Lond B 365: 3113-3127.
100. Voigt C, Goymann W, Leitner S (2007) Green matters! Growing vegetation stimulates breeding under short-day conditions in wild canaries (Serinus canaria). J Biol Rhythm 22: 554-557.
101. Weise CM (1967) Castration and spring migration in the white-throated sparrow. Condor 69: 49-68. doi: 10. 2307/1366372.
102. Wingfield JC (2003) Avian migration: regulation of facultative-type movements. In: Berthold P, Gwinner E, Sonnenschein E (eds) Avian migration. Springer, Berlin, pp 113-126.
103. Wingfield JC (2008a) Organization of vertebrate annual cycles; implications for control mechanisms. Philos Trans R Soc Lond B 363: 425-441.
104. Wingfield JC (2008b) Comparative endocrinology, environment and global change. Gen Comp Endocrinol 157: 207-216.
105. Wingfield JC, Farner DS (1978) The annual cycle of plasma irLH and steroid hormones in feral populations of the white-crowned sparrow, Zzonotrichia leucophrys gambelii. Biol Reprod 19: 1046-1056.
106. Wingfield JC, Farner DS (1979) Some endocrine correlates of renesting after loss of clutch or brood in the white-crowned sparrow, Zonotrichia leucophrys gambelii. Gen Comp Endocrinol 38: 322-331. doi: 10. 1016/0016-6480(79)90066-2.
107. Wingfield JC, Ramenofsky M (1999) Hormones and behavioural ecology of stress. In: Balm PHE (ed) Stress phyisology of animals. Sheffield University Press, Sheffield, pp 1-51.
108. Wingfield JC, Ramenofsky M (2011) Hormone-behavior interrelationships of birds in response to weather. In: Brockmann HJ, Roper TJ, Naguib M, Mitani JC, Simmons LW (eds) Advances in the study of behavior, vol 43. Academic, Burlington, pp 93-188.
109. Wingfield JC, Romero LM (2001). Adrenocortical responses to stress and their modulation in free-living vertebrates. In: McEwen BS (ed) Handbook of physiology, section 7, the endocrine system, vol 4: coping with the environment: neural and endocrine mechanisms. Oxford University Press, Oxford, p. 211+236.
110. Wingfield JC, Schwabl H, Mattocks PW Jr. (1990) Endocrine mechanisms of migration. In: Gwinner E (ed) Bird migration: physiology and ecophysiology. Springer, Berlin, pp 232-256.
111. Wingfield JC, Hahn TP, Wada M, Ashteimer LB, Schoech S (1996) Interrelationship of day lenth and temperature on the control of gonadal development, body mass, and fat score in white-crowned sparrows, Zonotrichia leucophrys gambelii. Gen Comp Endocrinol 101: 242-255.
112. Wingfield JC, Hahn TP, Maney DL, Schoech SJ, Wada M, Morton ML (2003) Effects of temperature on photoperiodically induced reproductive development, circulating plasma luteinizing hormone and thyroid hormones, body mass, fat deposition and molt in mountain white-crowned sparrows, Zonotrichia leucophrys oriantha. Gen Comp Endocrinol 131: 143-158.
113. Yokoyama K (1976) Hypothalamic and hormonal control of photoperiodically induced vernal functions in the white-crowned sparrow Zonotrichia leucophrys gambelii. I. The effects of hypothalamic lesions and exogenous hormones. Cell Tissue Res 174: 391-416.