Developmental stress and birdsong: Current evidence and future directions

Journal of Ornithology

Volumn 153, Issue SUPPL. 1, 2012, Pages 105-117

  MacDougall Shackleton, Scott A ^a   Spencer, Karen A ^b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

Birdsong; Developmentally correlated traits; Glucocorticoids; HVC

Indexed keywords

DEVELOPMENTAL BIOLOGY; PASSERINE; PHENOTYPE; SONG;

AVES;

EID: 84865821617     PISSN: 21937192     EISSN: 21937206     Source Type: Journal    
DOI: 10.1007/s10336-011-0807-x     Document Type: Review

References (97)

1. Andersson M (1994) Sexual selection. Princeton University Press, Princeton.
2. Blas J, Baos R, Bortolotti GR, Marchant T, Hiraldo F (2005) A multi-tier approach to identifying environmental stress in altricial nestling birds. Funct Ecol 19: 315-322.
3. Bolhuis JJ, Gahr M (2006) Neural mechanisms of birdsong memory. Nat Rev Neurosci 7: 347-357. doi: 10. 1038/nrn1904.
4. Boogert NJ, Giraldeau L-A, Lefebvre L (2008) Song complexity correlates with learning ability in zebra finch males. Anim Behav 76: 1735-1741. doi: 10. 1016/j. anbehav. 2008. 08. 009.
5. Brenowitz EA (1991) Altered perception of species-specific song by female birds after lesions of a forebrain nucleus. Science 251: 303-305.
6. Brumm H, Zollinger SA, Slater PJB (2009) Developmental stress affects song learning, but not song complexity and vocal amplitude in zebra finches. Behav Ecol Sociobiol 63: 1387-1395.
7. Buchanan KL, Spencer KA, Goldsmith AR, Catchpole CK (2003) Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris). Proc R Soc Lond B 270: 1149-1156.
8. Buchanan KL, Leitner S, Spencer KA, Goldsmith AR, Catchpole CK (2004) Developmental stress selectively affects the song control nucleus HVC in the zebra finch. Proc R Soc Lond B 271: 2381-2386.
9. Burt JM, Lent KL, Beecher MD, Brenowitz EA (2000) Lesions of the anterior forebrain song control pathway in female canaries affect song perception in an operant task. J Neurobiol 42: 1-13.
10. Catchpole CK (1996) Song and female choice: good genes and big brains? Trends Ecol Evol 11: 358-360.
11. Catchpole CK, Slater PJB (2008) Bird song: biological themes and variations, 2nd edn. Cambridge University Press, Cambridge.
12. Chaiken M, Bohner J, Marler P (1994) Repertoire turnover and the timing of song acquisition in European starlings. Behaviour 128: 25-39.
13. Clayton NS (1990) Subspecies recognition and song learning in zebra finches. Anim Behav 40: 1009-1017.
14. Criscuolo F, Monaghan P, Nasir L, Metcalfe NB (2008) Early nutrition and phenotypic development: 'catch-up' growth leads to elevated metabolic rate in adulthood. Proc R Soc Lond B 275: 1565-1570.
15. de Kloet ER (2000) Stress in the brain. Eur J Pharmacol 405: 187-198.
16. de Kogel CH, Prijs HJ (1996) Effects of brood size manipulations on sexual attractiveness of offspring in the zebra finch. Anim Behav 51: 699-708.
17. Del Negro C, Gahr M, Leboucher G, Kreutzer M (1998) The selectivity of sexual responses to song displays: effects of partial chemical lesion of the HVC in female canaries. Behav Brain Res 96: 151-159.
18. Doutrelant C, Blondel J, Perret P, Lambrechts MM (2000) Blue tit song repertoire size, male quality and interspecific competition. J Avian Biol 31: 360-366.
19. Dreiss A, Richard M, Moyen F, White J, Møller AP, Danchin E (2006) Sex ratio and male sexual characters in a population of blue tits, Parus caeruleus. Behav Ecol 17: 13-1.
20. Dubovicky M, Skultetyova S, Jezova D (1999) Neonatal stress alters habituation of exploratory behavior in adult male but not female rats. Pharmacol Biochem Behav 64: 681-686.
21. Gil D, Naguib M, Riebel K, Rutstein A, Gahr M (2006) Early condition, song learning, and the volume of song brain nuclei in the zebra finch (Taeniopygia guttata). J Neurobiol 66: 1602-1612.
22. Gorissen L, Snoeijs T, van Duyse E, Eens M (2005) Heavy metal pollution affects dawn singing behaviour in a small passerine bird. Oecologia 145: 504-509.
23. Grafen A (1990) Biological signals as handicaps. J Theor Biol 144: 517-546.
24. Hasselquist D, Bensch S, vonSchantz T (1996) Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler. Nature 381: 229-232.
25. Hernandez AM, Pfaff JA, MacDougall-Shackleton EA, MacDougall-shackleton SA (2009) The development of geographic song preferences in female song sparrows Melospiza melodia. Ethology 115: 513-521.
26. Hiebert SM, Stoddard PK, Arcese P (1989) Repertoire size, territory acquisition and reproductive success in the song sparrow. Anim Behav 37: 266-273.
27. Holveck MJ, Riebel K (2010) Low-quality females prefer low-quality males when choosing a mate. Proc R Soc Lond B 277: 153-160. doi: 10. 1098/rspb. 2009. 1222.
28. Holveck MJ, Vieira de Castro AC, Lachlan RF, ten Cate C, Riebel K (2008) Accuracy of song syntax learning and singing consistency signal early condition in zebra finches. Behav Ecol 19: 1267-1281.
29. Kent S, Tom C, Levine S (1997) Effect of interleukin-1beta on pituitary-adrenal responses and body weight in neonatal rats: Interaction with maternal deprivation. Stress 1: 213-230.
30. Kitaysky AS, Piatt JF, Wingfield JC, Romano M (1999) The adrenocortical stress-response of black-legged kittiwake chicks in relation to dietary restrictions. J Comp Physiol B Biochem Syst Environ Physiol 169: 303-310.
31. Kroodsma DE (1978) Aspects of learning in the ontogeny of birdsong. In: Burghardt GM, Bekoff M (eds) The development of behavior: comparative and evolutionary aspects. Garland, New York, pp 215-230.
32. 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.
33. MacDonald IF, Kempster B, Zanette L, MacDougall-Shackleton SA (2006) Early nutritional stress impairs development of a song-control brain region in both male and female juvenile song sparrows (Melospiza melodia) at the onset of song learning. Proc R Soc Lond B 273: 2559-2564.
34. MacDougall-Shackleton SA (1997) Sexual selection and the evolution of song repertoires. Curr Ornith 14: 81-125.
35. MacDougall-Shackleton SA, Hulse SH, Ball GF (1998) Neural bases of song preferences in female zebra finches (Taeniopygia guttata). Neuroreport 9: 3047-3052.
36. MacDougall-Shackleton EA, Derryberry EP, Hahn TP (2002) Nonlocal male mountain white-crowned sparrows have lower paternity and higher parasite loads than males singing local dialect. Behav Ecol 13: 682-689.
37. MacDougall-Shackleton SA, Dindia L, Newman AEM, Potvin DA, Stewart KA, MacDougall-Shackleton EA (2009) Stress, song and survival in sparrows. Biol Lett 5: 746-748. doi: 10. 1098/rsbl. 2009. 0382.
38. Markman S, Leitner S, Catchpole C, Barnsley S, Müller CT, Pascoe D, Buchanan KL (2008) Pollutants increase song complexity and the volume of the brain area hvc in a songbird. PLoS ONE 3: e1674.
39. Marler P, Peters S (1987) A aensitive period for song acquisition in the song sparrow, Melospiza melodia-a case of age-limited learning. Ethology 76: 89-100.
40. Marler P, Tamura M (1964) Song "dialects" in three populations of white-crowned sparrows. Science 146: 1483-1486.
41. McEwen BS (1999) Stress and hippocampal plasticity. Annu Rev Neurosci 22: 105-122.
42. McGregor PK, Krebs JR, Perrins CM (1981) Song repertoires and lifetime reproductive success in the great tit (Parus major). Am Nat 118: 149-159.
43. Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Evol Ecol 16: 254-260.
44. Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Philos Trans R Soc Lond B 363: 1635-1645.
45. Naguib M, Nemitz A, Gil D (2006) Maternal developmental stress reduces reproductive success of female offspring in zebra finches. Proc R Soc Lond B 273: 1901-1905.
46. Naguib M, Heim C, Gil D (2008) Early developmental conditions and male attractiveness in zebra finches. Ethology 114: 255-261.
47. Newman AEM, MacDougall-Shackleton SA, An Y-S, Kriengwatana B, Soma KK (2010) Corticosterone and dehydroepiandrosterone have opposing effects on adult neuroplasticity in the avian song control system. J Comp Neurol 518: 3662-3678. doi: 10. 1002/cne. 22395.
48. Nordeen KW, Marler P, Nordeen EJ (1989) Addition of song-related neurons in swamp sparrows coincides with memorization, not production, of learned songs. J Neurobiol 20: 651-661.
49. Nottebohm F (2005) The neural basis of birdsong. PLoS Biol 3: 759-761.
50. Nottebohm F, Nottebohm ME, Crane L (1986) Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song-control nuclei. Behav Neural Biol 46: 445-471.
51. Nowicki S, Searcy WA (2005a) Adaptive priorities in brain development: theoretical comment on Pravosudov et al. (2005). Behav Neurosci 119: 1415-1418.
52. Nowicki S, Searcy WA (2005b) Song and mate choice in birds: how the development of behavior helps us understand function. Auk 122: 1-14.
53. Nowicki S, Peters S, Podos J (1998) Song learning, early nutrition and sexual selection in songbirds. Am Zool 38: 179-190.
54. Nowicki S, Hasselquist D, Bensch S, Peters S (2000) Nestling growth and song repertoire sire in great reed warblers: evidence for song learning as an indicator mechanism in mate choice. Proc R Soc Lond B 267: 2419-2424.
55. Nowicki S, Searcy WA, Peters S (2002) Brain development, song learning and mate choice in birds: a review and experimental test of the "nutritional stress hypothesis". J Comp Physiol A Sens Neural Behav Physiol 188: 1003-1014.
56. Pfaff JA, Zanette L, MacDougall-Shackleton SA, MacDougall-Shackleton EA (2007) Song repertoire size varies with HVC volume and is indicative of male quality in song sparrows (Melospiza melodia). Proc R Soc Lond B 274: 2035-2040.
57. Pravosudov VV, Kitaysky AS (2006) Effects of nutritional restrictions during post-hatching development on adrenocortical function in western scrub-jays (Aphelocoma californica). Gen Comp Endocrinol 145: 25-31.
58. Pravosudov VV, Lavenex P, Omanska A (2005) Nutritional deficits during early development affect hippocampal structure and spatial memory later in life. Behav Neurosci 119: 1368-1374.
59. Reid JM, Arcese P, Cassidy A, Hiebert SM, Smith JNM, Stoddard PK, Marr AB, Keller LF (2004) Song repertoire size predicts initial mating success in male song sparrows, Melospiza melodia. Anim Behav 68: 1055-1063.
60. Reid JM, Arcese P, Cassidy A, Hiebert SM, Smith JNM, Stoddard PK, Marr AB, Keller LF (2005a) Fitness correlates of song repertoire size in free-living song sparrows (Melospiza melodia). Am Nat 165: 299-310.
61. Reid JM, Arcese P, Cassidy A, Marr AB, Smith JNM, Keller LF (2005b) Hamilton and Zuk meet heterozygosity? Song repertoire size indicates inbreeding and immunity in song sparrows (Melospiza melodia). Proc R Soc Lond B 272: 481-487.
62. Riebel K, Naguib M, Gil D (2009) Experimental manipulation of the rearing environment influences adult female zebra finch song preferences. Anim Behav 78: 1397-1404.
63. Rowland E, Love OP, Verspoor JJ, Sheldon L, Williams TD (2007) Manipulating rearing conditions reveals developmental sensitivity in the smaller sex of a passerine bird, the European starling Sturnus vulgaris. J Avian Biol 38: 612-618.
64. Sapolsky RM (2000a) Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 57: 925-935.
65. Sapolsky RM (2000b) Stress hormones: good and bad. Neurobiol Dis 7: 540-542.
66. Searcy WA (1992) Song repertoire and mate choice in birds. Am Zool 32: 71-80.
67. Searcy WA, Andersson M (1986) Sexual selection and the evolution of song. Annu Rev Ecol Syst 17: 507-533.
68. Searcy WA, Nowicki S (2005) The evolution of animal communication. Princeton University Press, Princeton.
69. Sims CG, Holberton RL (2000) Development of the corticosterone stress response in young northern mockingbirds (Mimus polyglottos). Gen Comp Endocrinol 119: 193-201.
70. Smith GT, Brenowitz EA, Wingfield JC, Baptista LF (1995) Seasonal changes in song nuclei and song behavior in Gambel's white-crowned sparrows. J Neurobiol 28: 114-125.
71. Smith GT, Brenowitz EA, Beecher MD, Wingfield JC (1997) Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds. J Neurosci 17: 6001-6010.
72. Sockman KW, Schwabl H (2001) Plasma corticosterone in nestling American kestrels: effects of age, handling stress, yolk androgens, and body condition. Gen Comp Endocrinol 122: 205-212.
73. Soma M, Takahasi M, Ikebuchi M, Yamada H, Suzuki M, Hasegawa T, Okanoya K (2006) Early rearing conditions affect the development of body size and song in Bengalese finches. Ethology 112: 1071-1078.
74. Spencer KA, MacDougall-Shackleton SA (2011) Indicators of development as sexually selected traits: the developmental stress hypothesis in context. Behav Ecol 22: 1-9. doi: 10. 1093/beheco/arq068.
75. Spencer KA, Buchanan KL, Goldsmith AR, Catchpole CK (2003) Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Horm Behav 44: 132-139.
76. Spencer KA, Buchanan KL, Goldsmith AR, Catchpole CK (2004) Developmental stress, social rank and song complexity in the European starling (Stumus vulgaris). Proc R Soc Lond B 271: S121-S123.
77. Spencer KA, Buchanan KL, Leitner S, Goldsmith AR, Catchpole CK (2005a) Parasites affect song complexity and neural development in a songbird. Proc R Soc Lond B 272: 2037-2043.
78. Spencer KA, Wimpenny JH, Buchanan KL, Lovell PG, Goldsmith AR, Catchpole CK (2005b) Developmental stress affects the attractiveness of male song and female choice in the zebra finch (Taeniopygia guttata). Behav Ecol Sociobiol 58: 423-428.
79. Spencer KA, Harris S, Baker PJ, Cuthill IC (2007) Song development in birds: the role of early experience and its potential effect on rehabilitation success. Anim Welf 16: 1-13.
80. Spencer KA, Evans NP, Monaghan P (2009) Postnatal stress in birds: a novel model of glucocorticoid programming of the hypothalamic-pituitary-adrenal axis. Endocrinology 150: 1931-1934. doi: 10. 1210/en. 2008-1471.
81. Stewart KA, MacDougall-Shackleton EA (2008) Local song elements indicate local genotypes and predict physiological condition in song sparrows Melospiza melodia. Biol Lett 4: 240-242.
82. Sullivan KA (1989) Predation and starvation: age-specific mortality in juvenile juncos (Junco phaenotus). J Anim Ecol 58: 275-286.
83. Suzuki K, Matsunaga E, Kobayashi T, Okanoya K (2011) Expression patterns of mineralocorticoid and glucocorticoid receptors in Bengalese finch (Lonchura striata var. domestica) brain suggest a relationship between stress hormones and song-system development. Neuroscience (in press). doi: 10. 1016/j. neuroscience. 2011. 07. 073.
84. Tinbergen N (1963) On aims and methods in ethology. Z Tierpsychol 20: 410-433.
85. Tramontin AD, Brenowitz EA (2000) Seasonal plasticity in the adult brain. Trends Neurosci 23: 251-258.
86. Tschirren B, Rutstein AN, Postma E, Mariette M, Griffith SC (2009) Short- and long-term consequences of early developmental conditions: a case study on wild and domesticated zebra finches. J Evol Biol 22: 387-395.
87. Wada H, Hahn TP, Breuner CW (2007) Development of stress reactivity in white-crowned sparrow nestlings: total corticosterone response increases with age, while free corticosterone response remains low. Gen Comp Endocrinol 150: 405-413.
88. Ward IL, Ward OB, Winn RJ, Bielawski D (1994) Male and female sexual behavior potential of male rats prenatally exposed to the influence of alcohol, stress, or both factors. Behav Neurosci 108: 1188-1195.
89. Weinstock M (2008) The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev 32: 1073-1086.
90. Williams CT, Kitaysky AS, Kettle AB, Buck CL (2008) Corticosterone levels of tufted puffins vary with breeding stage, body condition index, and reproductive performance. Gen Comp Endocrinol 158: 29-35. doi: 10. 1016/j. ygcen. 2008. 04. 018.
91. Wingfield JC (2005) The concept of allostasis: coping with a capricious environment. J Mammal 86: 248-254.
92. Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone-behavior interactions: The "emergency life history stage". Am Zool 38: 191-206.
93. Woodgate JL, Bennett ATD, Leitner S, Catchpole CK, Buchanan KL (2010) Developmental stress and female choice behaviour in the zebra finch. Anim Behav 79: 1381-1390. doi: 10. 1016/j. anbehav. 2010. 03. 018.
94. Woodgate JL, Leitner S, Catchpole CK, Berg ML, Bennett ATD, Buchanan KL (2011) Developmental stressors that impair song learning in males do not appear to affect female preferences for song complexity in the zebra finch. Behav Ecol 22: 566-573.
95. Zahavi A (1975) Mate selection-selection for a handicap. J Theor Biol 53: 205-214.
96. Zanette L, MacDougall-Shakleton E, Clinchy M, Smith JNM (2005) Brown-headed cowbirds skew host offspring sex ratios. Ecology 86: 815-820.
97. Zann R, Cash E (2008) Developmental stress impairs song complexity but not learning accuracy in non-domesticated zebra finches (Taeniopygia guttata). Behav Ecol Sociobiol 62: 391-400.