Some Ethological Implications for Neuroethology: The Ontogeny of Birdsong

  • Peter Marler
Part of the NATO Advanced Science Institutes Series book series (NSSA, volume 56)


For the past 20 years or so it has been the prevailing dogma in behavioral science, if not in neurobiology, that behaviorists solved the nature-nurture problem once and for all. Since genes interact with their environment at every turn in biological development, and every trait is the outcome of such interaction, it has been thought foolish to try to parse out the contributions of nature and nurture to the emergence of behavior. Any such attempt was viewed as not merely impractical but logically impossible. This “interactionist” view became widespread in ethology in the late 1950’s, in the wake of Lehrman’s critique of Lorenz’s theory of instinctive behavior (Lehrman, 1953). As a consequence research on innate contributions to behavioral development was virtually halted. Many students of behavior chose to ignore what I view as the central and most challenging problem in studying behavioral ontogeny, namely the nature and mode of expression of genetic instructions for adaptive responsiveness of the individual to varying environments.


Zebra Finch Auditory Feedback Syllable Type Vocal Learning Song Learning 
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  1. Arnold, A.P. 1975, The effects of castration on song development in zebra finches (Poephila guttata). J. Exp. Zool., 191:261–278.PubMedCrossRefGoogle Scholar
  2. Arnold, A.P., 1975, The effects of castration and androgen replacement on song, courtship, and aggression in zebra finches (Poephila guttata). J. Exp. Zool., 191:309–326.PubMedCrossRefGoogle Scholar
  3. Arnold, A.P., 1980, Sexual differences in the brain. Amer. Sci., 68:165–173.PubMedGoogle Scholar
  4. Arnold, A.P., 1980, Quantitative analysis of sex differences in hormone accumulation in the zebra finch brain: Methodological and theoretical issues. J. Comp. Neurol., 189:421–436.PubMedCrossRefGoogle Scholar
  5. Arnold, A.P., and Saltiel, A., 1979, Sexual difference in pattern of hormone accumulation in the brain of a songbird. Science, 205:702–705.PubMedCrossRefGoogle Scholar
  6. Baptista, L.F., 1975, Song dialects and demes in sedentary populations of the white-crowned sparrow (Zonotrichia leucophrys nuttalli). Univ. California Publ. Zool., 105:1–52.Google Scholar
  7. Baptista, L.F., and King, J.R., 1980, Geographical variation in song and song dialects of montane white-crowned sparrows. Condor, 82:267–284.CrossRefGoogle Scholar
  8. Bentley, D., and Konishi, M., 1978, Neural control of behavior. Ann. Rev. Neurosci., 1:35–59.PubMedCrossRefGoogle Scholar
  9. Bonke, D., Scheich, H., and Langner, G., 1979, Responsiveness of units in the auditory neostriatum of the guinea fowl (Numida meleagris) to species-specific calls and synthetic stimuli I: Tonotopy and functional zones of Field L. J. Comp. Physiol., 132:243–255.CrossRefGoogle Scholar
  10. Bornstein, M.H., and Kessen, W., 1979, “Physiological Development from Infancy”, John Wiley, New York.Google Scholar
  11. Bottjer, S.W., and Arnold, A.P., 1981, Identification of afferent neurons in the hypoglossal nerve of the zebra finch. Soc. Neurosci. Abstr., 7:270.Google Scholar
  12. Canady, R., Kroodsma, D., and Nottebohm, F., 1981, Significant differences in volume of song control nuclei are associated with variance in song repertoire in a free ranging songbird. Soc. Neurosci. Abstr., 7:845.Google Scholar
  13. Carterette, E.C., and Friedman, M.P., eds., 1976, “Handbook of Perception” Vol.VII: Language and Speech, Academic Press, New York.Google Scholar
  14. DeVoogd, T., and Nottebohm, F., 1981, Gonadal hormones induce dentritic growth in the adult avian brain. Science, 214:202–204.PubMedCrossRefGoogle Scholar
  15. DeVoogd, T., and Nottebohm, F., 1982, Sex differences in dendritic morphology of a song control nucleus in the canary: A quantitative golgi study. J. Comp. Neurol., (in press).Google Scholar
  16. Dittus, W.P.J., and Lemon, R.E., 1970, Auditory feedback in the singing of cardinals. Ibis, 112:544–548.CrossRefGoogle Scholar
  17. Dooling, R.J., and Searcy, M.H., 1980, Early perceptual selectivity in the swamp sparrow. Dev. Psychobiol., 13:499–506.PubMedCrossRefGoogle Scholar
  18. Eimas, P.D., and Miller, J.L., 1981, “Perspectives on the Study of Speech”, Lawrence Erlbaum, Hillsdale.Google Scholar
  19. Gibson, E.J., 1969, “Principles of Perceptual Learning and Development”, Appleton-Century-Crofts, New York.Google Scholar
  20. Green, S., and Marler, P., 1979, The analysis of animal communication, in “Handbook of Behavioral Neurobiology” Vol.3: Social Behavior and Communication, P. Marler and J.G. Vanden Bergh, eds., Plenum Press, New York.Google Scholar
  21. Greenewalt, C.H., 1968, “Bird Song: Acoustics and Physiology”, Smithsonian Institution, Washington, D.C.Google Scholar
  22. Gurney, M.E., and Konishi, M., 1980, Hormone-induced sexual differentiation of brain and behavior in zebra finches. Science, 208:1380–1383.PubMedCrossRefGoogle Scholar
  23. Güttinger, H.R. 1979, The integration of learnt and genetically programmed behaviour: A study of hierarchical organization in songs of canaries, greenfinches and their hybrids. Z. Tierpsychol., 49:285–303.CrossRefGoogle Scholar
  24. Güttinger, H.R., 1981, Self-differentiation of song organization rules by deaf canaries. Z. Tierpsychol., 56:323–340.CrossRefGoogle Scholar
  25. Güttinger, H.R., Wolffgramm, J., and Thimm, F., 1978, The relationship between species-specific song programs and individual learning in songbirds: A study of individual variation in songs of canaries, greenfinches, and hybrids between the two species. Behaviour, 65:241–262.CrossRefGoogle Scholar
  26. Hamburger, V., 1963, Some aspects of the embryology of behavior. Q. Rev. Biol., 38:342–365.PubMedCrossRefGoogle Scholar
  27. Hamilton, W.D., 1964, The genetical evolution of social behavior I and II. J. Theor. Biol. 7:1–52.PubMedCrossRefGoogle Scholar
  28. Heinemann, D., 1981, Song dialects, migration, and population structure of Puget Sound white-crowned sparrows. Auk, 98:512–521.Google Scholar
  29. Herman, R.M., Grillner, S., Stein, P.S., and Stuart, D.G., 1976, “Neural Control of Locomotion”, Plenum, New York.Google Scholar
  30. Hersh, G.L., 1966, “Bird Voices and Resonant Tuning in Helium-Air Mixtures”, Ph.D. Thesis, University of California, Berkely.Google Scholar
  31. Katz, L.I., and Gurney, M.E., 1981, Auditory responses in the zebra finch’s motor system for song. Brain Res., 211:192–197.CrossRefGoogle Scholar
  32. Kelley, D., and Nottebohm, F., 1979, Projections of a telencephalic auditory nucleus — Field L — in the canary. J. Comp. Neurol., 183:455–469.PubMedCrossRefGoogle Scholar
  33. Konishi, M., 1965, The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Z. Tierpsychol., 22:770–783.PubMedGoogle Scholar
  34. Konishi, M., 1971, Ethology and neurobiology. Amer. Sci., 59:56–63.PubMedGoogle Scholar
  35. Konishi, M., 1978, Ethological aspects of auditory pattern recognition in “Handbook of Sensory Physiology” Vol.VIII: Perception, R. Held, H.W. Leibowitz and H.-L. Teuber, eds., Springer-Verlag, Berlin.Google Scholar
  36. Konishi, M., and Nottebohm, F., 1969, Experimental studies in the ontogeny of avian vocalization, in “Bird Vocalization”, R.A. Hinde, ed., Cambridge University Press, London and New York.Google Scholar
  37. Kroodsma, D., 1981, Winter wren singing behavior: A pinnacle of song complexitiy. Condor, 82:357–365.CrossRefGoogle Scholar
  38. Kroodsma, D., and Pickert, R., 1980, Environmentally dependent sensitive periods for avian vocal learning. Nature, 288:477–478.CrossRefGoogle Scholar
  39. Kuhl, P.K., 1976, Speech perception in early infancy: The acquisition of speech-sound categories, in “Hearing and Davis”, S.K. Hirsh, D.E. Eldredge, I.J. Hirsh and S.R. Silverman, eds., Washington University Press, St. Louis.Google Scholar
  40. Lashley, K.S., 1951, The problem of serial order in behavior, in “Cerebral Mechanisms in Behavior”, L.A. Jeffries, ed., Wiley, New York.Google Scholar
  41. Lehrman, D.S., 1953, A critique of Konrad Lorenz’s theory of instinctive behavior. Q. Rev. Biol., 28:337–363.PubMedCrossRefGoogle Scholar
  42. Lemon, R.E., 1973, Nervous control of the syrinx in white-throated sparrows (Zonotrichia albicollis). J. Zool. (Lond.), 171:131–140.CrossRefGoogle Scholar
  43. Lemon, R.E., 1975, How birds develop song dialects. Condor, 77:385–406.CrossRefGoogle Scholar
  44. Lenneberg, E.H., 1967, “Biological Foundations of Language”, Wiley, New York.Google Scholar
  45. Leppelsack, H.J., and Vogt, M., 1976, Responses of auditory neurons in the forebrain of a songbird to stimulation with species-specific sounds. J. Comp. Physiol., 107:263–274.CrossRefGoogle Scholar
  46. Liberman, A.M., Cooper, F.S., Shankweiler, D.P., and Studdert-Kennedey, M., 1967, Perception of the speech-code. Psychol. Rev., 74:431–461.PubMedCrossRefGoogle Scholar
  47. Lieberman, P., 1977, “Speech Physiology and Acoustic Phonetics: An Introduction”, Macmillan Publishing Co., Inc., New York.Google Scholar
  48. Lorenz, K., 1950, The comparative method in studying innate behaviour patterns. Symp. Soc. Exp. Biol., 4:221–268.Google Scholar
  49. McCasland, J., and Konishi, M., 1981, Interaction between auditory and motor activities in an avian song control nucleus. Proc. Natl. Acad. Sci. USA, 78:7815–7819.PubMedCrossRefGoogle Scholar
  50. MacNeilage, P., 1970, Motor control of serial ordering of speech. Psychol. Rev., 77:182–192.PubMedCrossRefGoogle Scholar
  51. Marler, P., 1970, A comparative approach to vocal learning: Song development in white-crowned sparrows. J. Comp. Physiol. Psychol., 71(2):1–25.CrossRefGoogle Scholar
  52. Marler, P., 1976, Sensory templates is species-specific behavior, in “Simpler Networks and Behavior”, J. Fentress, ed., Sinauer, Assoc, Sunderland, Mass.Google Scholar
  53. Marler, P., 1977, Development and learning of recognition systems, in “Recognition of Complex Acoustic Signals”, T.H. Bullock, ed., Dahlem Konferenzen, Berlin.Google Scholar
  54. Marler, P., 1981, Birdsong: The acquisition of a learned motor skill. TINS, 4:88–94.Google Scholar
  55. Marler, P., and Peters, S., 1977, Selective vocal learning in a sparrow. Science, 198:519–521.PubMedCrossRefGoogle Scholar
  56. Marler, P., and Peters, S., 1980, Birdsong and speech: Evidence for special processing, in “Perspectives on the Study of Speech”, R. Eimas and J. Miller, eds., Lawrence Erlbaum Associates, Hillsdale.Google Scholar
  57. Marler, P., and Peters, S., 1981, Sparrows learn adult song and more from memory. Science, 213:780–782.PubMedCrossRefGoogle Scholar
  58. Marler, P., and Peters, S., 1982a, Long-term storage of learned birdsongs prior to production. Anim. Behav., (in press).Google Scholar
  59. Marler, P., and Peters, S., 1982b, Structural changes in song ontogeny in the swamp sparrow, Melospiza georgiana. Auk, (in press).Google Scholar
  60. Marler, P., and Peters, S., 1982c, Subsong and plastic song: Their role in the vocal learning process, in “Ecology and Evolution of Acoustic Communication in Birds”, D. Kroodsma and T. Miller, eds., Academic Press, New York (in press).Google Scholar
  61. Marler, P., and Peters, S., 1982d, Developmental overproduction and selective attrition: New processes in the epigenesis of birdsong. Dev. Psychobiol., (in press).Google Scholar
  62. Marler, P., and Sherman, V., 1982, Structure in sparrow songs without auditory feedback: An emendation of the auditory template hypothesis, (in prep.).Google Scholar
  63. Marler, P., and Sherman, V., 1982, A comparison of innate songs in two Melospiza sparrows, M. georgiana and M.melodia, (in prep.).Google Scholar
  64. Marler, P., and Tamura, M., 1962, Song dialects in three populations of white-crowned sparrows. Condor, 64:368–377.CrossRefGoogle Scholar
  65. Marler, P., and Waser, M.S., 1977, The role of auditory feedback in canary song development. J. Comp. Physiol. Psychol., 91:8–16.PubMedCrossRefGoogle Scholar
  66. Marler, P., Mundinger, P., Waser, M.S., and Lutjen, A., 1972, Effects of acoustical stimulation and deprivation on song development in the red-winged blackbird (Agelaius phoeniceus). Anim. Behav., 20:586–606.PubMedCrossRefGoogle Scholar
  67. Marler, P., Dooling, R., and Zoloth, S., 1980, Comparative perspectives on ethology and behavioral development, in “The Comparative Method in Psychology”, M. Bornstein, ed., Erlbaum, Hillsdale, N.J.Google Scholar
  68. Nottebohm, F., 1968, Auditory experience and song development in the chaffinch, Fringilla coelebs. Ibis, 110:549–568.CrossRefGoogle Scholar
  69. Nottebohm, F., 1969, The “critical period” for song learning. Ibis, 111:386–387.CrossRefGoogle Scholar
  70. Nottebohm, F., 1971, Neural lateralization of vocal control in a passerine bird I: Song. J. Exp. Zool., 177:229–262.PubMedCrossRefGoogle Scholar
  71. Nottebohm, F., 1972, Neural lateralization of vocal control in a passerine bird II: Subsong, calls and a theory of vocal learning. J. Exp. Zool., 179:35–49.CrossRefGoogle Scholar
  72. Nottebohm, F., 1972, The origins of vocal learning. Amer. Natur., 106:116–140.CrossRefGoogle Scholar
  73. Nottebohm, F., 1975, Vocal behavior in birds, in “Avian Biology” Vol.V, D. Farner, ed., Academic Press, New York.Google Scholar
  74. Nottebohm, F., 1977, Asymmetries in neural control of vocalization in the canary, in “Lateralization in the Nervous System”, S. Harnad, R.W. Doty, L. Goldstein, J. Jaynes and G. Krauthamer, eds., Academic Press, New York.Google Scholar
  75. Nottebohm, F., 1980, Brain pathways for vocal learning in birds: A review of the first 10 years. Progr. Psychobiol. Physiol. Psychol., 9:85–124.Google Scholar
  76. Nottebohm, F., 1981, A brain for all seasons: Cyclical anatomical changes in song control nuclei of the canary brain. Science, 214:1368–1370.PubMedCrossRefGoogle Scholar
  77. Nottebohm, F., 1981, Laterality, seasons and space govern the learning of a motor skill. TINS, 4:104–106.Google Scholar
  78. Nottebohm, F., and Arnold, A.P., 1976, Sexual dimorphism in vocal control areas of the songbird brain. Science, 194:211–213.PubMedCrossRefGoogle Scholar
  79. Nottebohm, F., and Nottebohm, M., 1976, Left hypoglossal dominance in the control of canary and white-crowned sparrow song. J. Comp. Physiol., 108:171–192.CrossRefGoogle Scholar
  80. Nottebohm, F., and Nottebohm, M.E., 1978, Relationship between song repertoire and age in the canary, Serinus canari us. Z. Tierpsychol., 46:298–305.CrossRefGoogle Scholar
  81. Nottebohm, F., Stokes, T.M., and Leonard, C.M., 1976, Central control of song in the canary, Serinus canari us. J. Comp. Neurol., 165:457–486.PubMedCrossRefGoogle Scholar
  82. Nottebohm, F., Manning, E., and Nottebohm, M., 1979, Reversal of hypoglossal dominance in canaries following unilateral syringeal denervation. J. Comp. Physiol., 134:227–240.CrossRefGoogle Scholar
  83. Nottebohm, F., Kasparian, S., and Pandazis, C., 1981, Brain space for a learned task. Brain Res., 213:99–109.PubMedCrossRefGoogle Scholar
  84. Ojemann, G., and Mateer, C., 1979, Human language cortex: Localization of memory, syntax, and sequential motor phoneme identification systems. Science, 205:1401–1403.PubMedCrossRefGoogle Scholar
  85. Payne, R.B., 1981, Population structure and social behavior: Models for testing the ecological significance of song dialects in birds, in “Natural Selection and Social Behavior: Recent Research and Theory”, R.D. Alexander and D.W. Tinkle, eds., Chiron Press, New York.Google Scholar
  86. Poulsen, H., 1959, Song learning in the domestic canary. Z. Tierpsychol., 16:173–178.CrossRefGoogle Scholar
  87. Price, P.H., 1979, Developmental determinants of structure in zebra finch song. J. Comp. Physiol. Psychol., 93:260–277.CrossRefGoogle Scholar
  88. Rosch, E., and Lloyd, B.B., eds., 1978, “Cognition and Categorization”, Lawrence Erlbaum Associates, Hillsdale, N.J.Google Scholar
  89. Scheich, H., Langner, G., and Bonke, D., 1979, Responsiveness of units in the auditory neostriatum of the guinea fowl (Numida meleagris) to species-specific calls and synthetic stimuli II: Discrimination of Iambus-like calls. J. Comp. Physiol., 132:257–276.CrossRefGoogle Scholar
  90. Sinnott, J.M., 1980, Species-specific coding in bird song. J. Acoust. Soc. Am., 68:494–497.CrossRefGoogle Scholar
  91. Stelmack, G., and Requin, J., eds., 1980, “Tutorials in Motor Behavior”, Elsevier North Holland, Amsterdam.Google Scholar
  92. Stokes, T.C., Leonard, C.M., and Nottebohm, F., 1974, A stereotaxic atlas of the telencephalon, diencephalon, and mesencephalon of the canary Serinus canarius. J. Comp. Neurol., 156:337–374.PubMedCrossRefGoogle Scholar
  93. Studdert-Kennedey, M., Liberman, A.M., Harris, K.S., and Cooper, F.S., 1970, Motor theory of speech perception: A reply to Lane’s critical review. Psychol. Rev., 77:234–249.CrossRefGoogle Scholar
  94. Talbott, R.E., and Humphrey, D.R., 1979, “Posture and Movements”, Raven Press, New York.Google Scholar
  95. Tinbergen, N., 1951, “The Study of Instinct”, Oxford University Press, London.Google Scholar
  96. Weiss, P., 1950, Experimental analysis of coordination by disarrangement of central-peripheral relations. Symp. Soc. Exp. Biol., 4:92–111.Google Scholar
  97. Wilson, E.O., 1975, “Sociobiology”, Belknap Press, Harvard University Press, Cambridge.Google Scholar
  98. Wingfield, J.C., and Farner, D.S., 1980, Control of seasonal reproduction in temperate zone birds. Prog. Reprod. Biol., 5:62–101.Google Scholar
  99. Zoloth, S.R., and Green, S., 1979, Monkey vocalizations and human speech: Parallels in perception? Brain Behav. Evol., 16:430–442.PubMedCrossRefGoogle Scholar
  100. Zoloth, S.R., Petersen, M.R., Beecher, M.D., Green, S., Marler, P., Moody, D.B., and Stebbins, W., 1979, Species-specific perceptual processing of vocal sounds by monkeys. Science, 204:870–873.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1983

Authors and Affiliations

  • Peter Marler
    • 1
  1. 1.Field Research CenterThe Rockefeller UniversityMillbrookUSA

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