Behavioral Ecology and Sociobiology

, Volume 63, Issue 3, pp 363–370 | Cite as

Early ontogenetic effects on song quality in the Bengalese finch (Lonchura striata var. domestica): laying order, sibling competition, and song syntax

  • Masayo SomaEmail author
  • Mariko Hiraiwa-Hasegawa
  • Kazuo Okanoya
Original Paper


Birdsong differs from other sexual traits in that the acquisition process involves learning. Especially in close-ended learning species like the Bengalese finch, conditions experienced during the critical song-learning period can have a profound influence on song quality. Therefore, to understand song evolution from a life-history perspective, we investigated early ontogenetic effects on song quality. In particular, we focused on maternal effects and sibling competition. In asynchronously hatching bird species, the age hierarchy among nestlings affects physical development due to competition for food; mothers may influence this competition by adjusting their investment in each egg according to its sequence in the laying order. To independently assess these effects, chicks of the Bengalese finch were cross-fostered so that the age hierarchies formed in fostered broods were independent of the laying order. Our results indicate that song quality partially reflects early ontogenetic conditions, whereas song duration and note-type repertoire were independent of either laying order or age hierarchy. The syntactical complexity of note order declined over the laying sequence. This finding suggests that the song learning ability is influenced by within-clutch variation in maternal investment toward eggs. Considering that song syntactical complexity is subject to female preference in the Bengalese finch, it is likely that maternal resource allocation strategies play a role in song evolution.


Bengalese finch Development Maternal effect Song complexity Song learning 



We thank the members of the Biolinguistics team for help in maintaining the birds, and two anonymous reviewers for the comment of the manuscript. This study was supported financially by JSPS Research Fellowships for Young Scientists (DC2-17-10949 and PD-19-7732).


  1. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  2. Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296–302PubMedCrossRefGoogle Scholar
  3. Brenowitz EA, Beecher MD (2005) Song learning in birds: diversity and plasticity, opportunities and challenges. Trends Neurosci 28:127–132PubMedCrossRefGoogle Scholar
  4. 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 B 271:2381–2386PubMedCrossRefGoogle Scholar
  5. Catchpole CK, Slater PJB (2008) Bird song: biological themes and variations, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  6. Charif RA, Clark CW, Firstrup KM (2004) Raven 1.2 user’s manual. Cornell Laboratory of Ornithology, New YorkGoogle Scholar
  7. Clark MM, Galef BG (1995) Prenatal influences on reproductive life-history strategies. Trends Ecol Evol 10:151–153CrossRefGoogle Scholar
  8. Eising CM, Eikenaar C, Schwabl H, Groothuis TG (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc B 268:839–846PubMedCrossRefGoogle Scholar
  9. Eising CM, Müller W, Groothuis TG (2006) Avian mothers create different phenotypes by hormone deposition in their eggs. Biol Lett 2:20–22PubMedCrossRefGoogle Scholar
  10. Forstmeier W, Coltman DW, Birkhead TR (2004) Maternal effects influence the sexual behavior of sons and daughters in the zebra finch. Evolution 58:2574–2583PubMedGoogle Scholar
  11. Garamszegi LZ, Biard C, Eens M, Møller AP, Saino N (2007) Interspecific variation in egg testosterone levels: implications for the evolution of bird song. J Evol Biol 20:950–964PubMedCrossRefGoogle Scholar
  12. Gentner TQ, Hulse SH (2000) Female European starling preference and choice for variation in conspecific male song. Anim Behav 59:443–458PubMedCrossRefGoogle Scholar
  13. Gil D (2003) Golden eggs: maternal manipulation of offspring phenotype by egg androgen in birds. Ardeola 50:281–294Google Scholar
  14. Gil D, Gahr M (2002) The honesty of bird song: multiple constraints for multiple traits. Trends Ecol Evol 17:133–141CrossRefGoogle Scholar
  15. Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128PubMedCrossRefGoogle Scholar
  16. Gil D, Leboucher G, Lacroix A, Cue R, Kreutzer M (2004) Female canaries produce eggs with greater amounts of testosterone when exposed to preferred male song. Horm Behav 45:64–70PubMedCrossRefGoogle Scholar
  17. 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 66:1602–1612PubMedCrossRefGoogle Scholar
  18. Gilbert L, Rutstein AN, Hazon N, Graves JA (2005) Sex-biased investment in yolk androgens depends on female quality and laying order in zebra finches (Taeniopygia guttata). Naturwissenschaften 92:178–181PubMedCrossRefGoogle Scholar
  19. Godsave SF, Lohmann R, Vloet RP, Gahr M (2002) Androgen receptors in the embryonic zebra finch hindbrain suggest a function for maternal androgens in perihatching survival. J Comp Neurol 453:57–70PubMedCrossRefGoogle Scholar
  20. Groothuis TG, Schwabl H (2002) Determinants of within- and among-clutch variation in levels of maternal hormones in Black-Headed Gull eggs. Funct Ecol 16:281–289CrossRefGoogle Scholar
  21. Groothuis TG, Müller W, von Engelhardt N, Carere C, Eising C (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Behav Rev 29:329–52Google Scholar
  22. Honda E, Okanoya K (1999) Acoustical and syntactical comparisons between songs of the white-backed munia (Lonchura striata) and its domesticated strain, the Bengalese finch (Lonchura striata var. domestica). Zool Sci 16:319–326CrossRefGoogle Scholar
  23. Kimball RT, Ligon JD (1999) Evolution of avian plumage dichromatism from a proximate perspective. Am Nat 154:182–193CrossRefGoogle Scholar
  24. Krebs EA (1999) Last but not least: nestling growth and survival in asynchronously hatching crimson rosellas. J Anim Ecol 68:266–281CrossRefGoogle Scholar
  25. Leitner S, Marshall RC, Leisler B, Catchpole CK (2006) Male song quality, egg size and offspring sex in captive canaries (Serinus canaria). Ethology 112:554–563CrossRefGoogle Scholar
  26. Lemon RE, Dobson CW, Clifton PG (1993) Songs of American Redstarts Setophaga ruticilla: sequencing rules and their relationships to repertoire size. Ethology 93:198–210CrossRefGoogle Scholar
  27. Lipar JL, Ketterson ED (2000) Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc R Soc B 267:2005–2010PubMedCrossRefGoogle Scholar
  28. 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 B 273:2559–2564PubMedCrossRefGoogle Scholar
  29. Magrath MJL, Brouwer L, Komdeur J (2003) Egg size and laying order in relation to offspring sex in the extreme sexually size dimorphic brown songlark, Cinclorhamphus cruralis. Behav Ecol Sociobiol 54:240–248CrossRefGoogle Scholar
  30. Marler P (1990) Song learning: the interface between behaviour and neuroethology. Phil Trans R Soc Lond B 329:109–114CrossRefGoogle Scholar
  31. Masello JF, Quillfeldt P (2004) Are haematological parameters related to body condition, ornamentation and breeding success in wild burrowing parrots Cyanoliseus patagonus ? J Avian Biol 35:445–454CrossRefGoogle Scholar
  32. Morisaka T, Katahira K, Okaoya K (2008) Variability in preference for conspecific songs with syntactical complexity in female Bengalese Finches: towards an understanding of song evolution. Ornithol Sci 7:75–84CrossRefGoogle Scholar
  33. Nakamura KZ, Okanoya K (2004) Neural correlates of song complexity in Bengalese finch high vocal center. Neuroreport 15:1359–1363PubMedCrossRefGoogle Scholar
  34. Nowicki S, Searcy WA (2004) Song function and the evolution of female preferences—why birds sing, why brains matter. Ann NY Acad Sci 1016:704–723PubMedCrossRefGoogle Scholar
  35. Nowicki S, Searcy WA (2005) Song and mate choice in birds: how the development of behavior helps us understand function. Auk 122:1–14CrossRefGoogle Scholar
  36. Nowicki S, Peters S, Podos J (1998) Song learning, early nutrition and sexual selection in songbirds. Am Zool 38:179–190Google Scholar
  37. 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 188:1003–1014CrossRefGoogle Scholar
  38. Okanoya K (2004a) Song syntax in Bengalese finches: proximate and ultimate analyses. Adv Stud Behav 34:297–346CrossRefGoogle Scholar
  39. Okanoya K (2004b) The Bengalese finch—a window on the behavioral neurobiology of birdsong syntax. Ann NY Acad Sci 1016:724–735PubMedCrossRefGoogle Scholar
  40. Owens IPF, Short RV (1995) Hormonal basis of sexual dimorphism in birds: implications for new theories of sexual selection. Trends Ecol Evol 10:44–47CrossRefGoogle Scholar
  41. Pilz KM, Smith HG, Sandell MI, Schwabl H (2003) Interfemale variation in egg yolk androgen allocation in the European starling: do high-quality females invest more? Anim Behav 65:841–850CrossRefGoogle Scholar
  42. Podos J, Huber SK, Taft B (2004) Bird song: the interface of evolution and mechanism. Annu Rev Ecol Evol Syst 35:55–87CrossRefGoogle Scholar
  43. Qvarnström A, Price TD (2001) Maternal effects, paternal effects and sexual selection. Trends Ecol Evol 16:95–100PubMedCrossRefGoogle Scholar
  44. R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  45. Reed WL, Vleck CM (2001) Functional significance of variation in egg-yolk androgens in the American coot. Oecologia 128:164–171CrossRefGoogle Scholar
  46. Rubolini D, Romano M, Martinelli R, Leoni B, Saino N (2006) Effects of prenatal yolk androgens on armaments and ornaments of the ring-necked pheasant. Behav Ecol Sociobiol 59:549–560CrossRefGoogle Scholar
  47. Rutkowska J, Cichoń M (2002) Maternal investment during egg laying and offspring sex: an experimental study of zebra finches. Anim Behav 64:817–822CrossRefGoogle Scholar
  48. Rutkowska J, Wilk T, Cichoń M (2007) Androgen-dependent maternal effects on offspring fitness in zebra finches. Behav Ecol Sociobiol 61:1211–1217CrossRefGoogle Scholar
  49. Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, Stradi R (2002) Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proc R Soc B 269:1729–1733PubMedCrossRefGoogle Scholar
  50. Schlinger BA (1998) Sexual differentiation of avian brain and behavior: current views on gonadal hormone-dependent and independent mechanisms. Annu Rev Physiol 60:407–429PubMedCrossRefGoogle Scholar
  51. Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90:11446–11450PubMedCrossRefGoogle Scholar
  52. Schwabl H (1996) Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol A 114:271–276CrossRefGoogle Scholar
  53. Schwabl H, Mock DW, Gieg JA (1997) A hormonal mechanism for parental favouritism. Nature 386:231CrossRefGoogle Scholar
  54. Soma M, Takahasi M, Ikebuchi M, Yamada H, Suzuki M, Hasegawa T, Okanoya K (2006a) Early rearing conditions affect the development of body size and song in Bengalese finches. Ethology 112:1017–1078CrossRefGoogle Scholar
  55. Soma M, Takahasi M, Hasegwa T, Okanoya K (2006b) Trade-offs and correlations among multiple song features in the Bengalese Finch. Ornithol Sci 5:77–84CrossRefGoogle Scholar
  56. Soma M, Saito DS, Hasegawa T, Okanoya K (2007) Sex-specific maternal effect on egg mass, laying order, and sibling competition in the Bengalese finch (Lonchura striata var. domestica). Behav Ecol Sociobiol 61:1695–1705CrossRefGoogle Scholar
  57. 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 44:132–139PubMedCrossRefGoogle Scholar
  58. 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 B 271:S121–S123PubMedCrossRefGoogle Scholar
  59. Spencer KA, Buchanan KL, Leitner S, Goldsmith AR, Catchpole CK (2005) Parasites affect song complexity and neural development in a songbird. Proc R Soc B 272:2037–2043PubMedCrossRefGoogle Scholar
  60. Strasser R, Schwabl H (2004) Yolk testosterone organizes behavior and male plumage coloration in house sparrows (Passer domesticus). Behav Ecol Sociobiol 56:491–497CrossRefGoogle Scholar
  61. von Engelhardt N, Carere C, Dijkstra C, Groothuis TG (2006) Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches. Proc R Soc B 273:65–70CrossRefGoogle Scholar
  62. Zann R, Cash E (2007) Developmental stress impairs song complexity but not learning accuracy in non-domesticated zebra finches (Taeniopygia guttata). Behav Ecol Sociobiol 62:391–400CrossRefGoogle Scholar
  63. Zann R, Runciman D (2003) Primary sex ratios in zebra finches: no evidence for adaptive manipulation in wild and semi-domesticated populations. Behav Ecol Sociobiol 54:294–302CrossRefGoogle Scholar
  64. Zeng SJ, Szekely T, Zhang XW, Lu K, Liu L, Zuo MX (2007) Comparative analyses of song complexity and song-control nuclei in fourteen oscine species. Zool Sci 24:1–9PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Masayo Soma
    • 1
    • 2
    Email author
  • Mariko Hiraiwa-Hasegawa
    • 1
  • Kazuo Okanoya
    • 2
  1. 1.Hayama Center for Advanced StudiesThe Graduate University for Advanced StudiesKanagawaJapan240-0193
  2. 2.Biolinguistics LaboratoryBrain Science Institute, RIKENSaitamaJapan351-0198

Personalised recommendations