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Bird vocalization

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A male Blackbird (Turdus merula) singing. Bogense havn, Funen, Denmark. Blackbird song recorded at Lille, France (help·info)

Bird vocalization includes both bird calls and bird songs. In non-technical use, bird songs are the bird sounds that are melodious to the human ear. In ornithology, bird 'songs' are often distinguished from shorter sounds, which may be termed 'calls'.

Definition

The distinction between songs and calls is somewhat arbitrary. Songs are longer and more complex and are associated with courtship and mating, while calls tend to serve such functions as alarms or keeping members of a flock in contact.[1] Other authorities such as Howell and Webb (1995) make the distinction based on function, so that short vocalisations such as those of pigeons and even non-vocal sounds such as the drumming of woodpeckers and the "winnowing" of snipes' wings in display flight are considered songs.[2] Still others require song to have syllabic diversity and temporal regularity akin to the repetitive and transformative patterns which define music.

Bird song is best developed in the order Passeriformes. Most song is emitted by male rather than female birds. Song is usually delivered from prominent perches although some species may sing when flying. Some groups are nearly voiceless, producing sounds only mechanically, such as the storks, which clatter their bills. In some manakins (Pipridae), the males have evolved several mechanisms for mechanical sound production, including mechanisms for stridulation not unlike those in the insects.[3]

The production of sounds by mechanical means as opposed to the use of the syrinx has been termed variously instrumental music by Charles Darwin, mechanical sounds[4] and more recently sonation.[5] The term sonate has been defined as the act of producing non-vocal sounds that are intentionally modulated communicative signals, produced using non-syringeal structures such as the bill, wings, tail, feet and body feathers.[5]

Anatomy

The avian vocal organ is called the syrinx; it is a bony structure at the bottom of the trachea (unlike the larynx at the top of the mammalian trachea). The syrinx and sometimes a surrounding air sac resonate to vibrations that are made by membranes past which the bird forces air. The bird controls the pitch by changing the tension on the membranes and controls both pitch and volume by changing the force of exhalation. It can control the two sides of the trachea independently, which is how some species can produce two notes at once.

Function

Scientists hypothesize that bird song has evolved through sexual selection, and experiments suggest that the quality of bird song may be a good indicator of fitness.[6] Experiments also suggest that parasites and diseases may directly affect song characteristics such as song rate, which thereby act as reliable indicators of health.[7][8] The song repertoire also appears to indicate fitness in some species.[9] The ability of male birds to hold and advertise territories using song also demonstrates their fitness.

Communication through bird calls can be between individuals of the same species or even across species. The mobbing calls of birds used to recruit individuals in an area where an owl or other predator may be present. These calls are characterized by wide frequency spectra, sharp onset and termination, and repetitiveness. These characteristics are common across species and are believed to be helpful to other potential mobbers by being easy to locate. The alarm calls of many species, on the other hand, are characteristically high-pitched and difficult to locate.[10]

Individual birds may be sensitive enough to identify each other through their calls. Many birds that nest in colonies can locate their chicks using their calls.[11] Calls are sometimes distinctive enough for individual identification even by human researchers in ecological studies.[12]

Many birds engage in duet calls. In some cases the duets are so perfectly timed as to appear almost as one call. This kind of calling is termed antiphonal duetting.[13] Such duetting is noted in a wide range of families including quails,[14] bushshrikes,[15] babblers such as the scimitar babblers, some owls[16] and parrots.[17] The function of such orchestrated calling is unclear.

Some birds are excellent mimics. In some tropical species it has been hypothesized that mimics such as the drongos may have a role in the formation of mixed-species foraging flocks.[18]

Some cave-dwelling species, including Oilbird[19] and Swiftlets (Collocalia and Aerodramus spp.),[20] use audible sound (with the majority of sonic location occurring between 2 and 5 kHz [21]) to echolocate in the darkness of caves.

The bird hearing range goes from below 50 Hz (infrasound) to above 20 kHz (ultrasound) with maximum sensitivity between 1 and 5 kHz.[22] The range of frequencies at which birds call in an environment varies with the quality of habitat and the ambient sounds. It has been suggested that narrow bandwidths, low frequencies, low-frequency modulations, and long elements and inter-element intervals should be found in habitats with complex vegetation structures (which would absorb and muffle sounds) while high frequencies, broad bandwidth, high-frequency modulations (trills), and short elements and inter-elements may be expected in habitats with herbaceous cover.[23][24] It has been hypothesized that the available frequency range is partitioned and birds call so that overlap between different species in frequency and time is reduced. This idea has been termed the "acoustic niche".[25] In urban areas with a lot of low-frequency noise, it has been noted that birds sing louder[26] as well as at a higher pitch.[27]

Language

The language of the birds has long been a topic for anecdote and speculation. That calls have meanings that are interpreted by their listeners has been well demonstrated. Domestic chicken have distinctive alarm calls for aerial and ground predators, and they respond to these alarm calls appropriately.[28][29] However a language has, in addition to words, structures and rules. Studies to demonstrate the existence of language have been difficult due to the range of possible interpretations. Research on parrots by Irene Pepperberg is claimed to demonstrate the innate ability for grammatical structures, including the existence of concepts such as nouns, adjectives and verbs.[30] Studies on starling vocalizations have also suggested that they may have recursive structures.[31]

Neurophysiology

The main brain areas involved in bird song are:

  • Anterior forebrain pathway (vocal learning) = LMAN, lateral part of the magnocellular nucleus of anterior neostriatum (homologue to mammalian basal ganglia); Area X, basal ganglia; DLM, medial nucleus of dorsolateral thalamus.
  • Song production pathway = HVC, higher vocal center; RA, robust nucleus of archistriatum; xXII, tracheosyringeal part of the hypoglossal nucleus.[32]

Both pathways show sexual dimorphism, with the male producing song most of the time.[33] It has been noted that injecting testosterone in non-singing female birds can induce growth of the HVC and thus production of song.

Birdsong production is generally thought to start at the nucleus uvaeformis of the thalamus with signals emanating along a pathway that terminates at the syrinx. The pathway from the thalamus leads to the interfacial nucleus of the nidopallium to the HVC, and then to RA, the dorso-lateral division of the medial thalamus and to the tracheosyringeal nerve.

The gene FOXP2, defects of which affect both speech and comprehension of language in humans, becomes more active in the striatal region of songbirds during the time of song learning.[34]

Recent research in birdsong learning has focused on the Ventral Tegmental Area (VTA), which sends a dopamine input to the para-olfactory lobe and Area X, LMAN and the ventrolateral medulla. Other researchers have explored the possibility that the high vocal center is responsible for syllable production, while the robust nucleus of the arcopallium, the primary song output nucleus, may be responsible for syllable sequencing and production of notes within a syllable.

Learning

The songs of different species of birds vary, and are more or less characteristic of the species. In modern-day biology, bird song is typically analysed using acoustic spectroscopy. Species vary greatly in the complexity of their songs and in the number of distinct kinds of song they sing (up to 3000 in the Brown Thrasher); in some species, individuals vary in the same way. In a few species such as starlings and mockingbirds, songs imbed arbitrary elements learned in the individual's lifetime, a form of mimicry (though maybe better called "appropriation" [Ehrlich et al.], as the bird does not pass for another species). As early as 1773 it was established that birds learnt calls and cross-fostering experiments were able to force a Linnet Acanthis cannabina to learn the song of a skylark Alauda arvensis.[35] In many species it appears that although the basic song is the same for all members of the species, young birds learn some details of their songs from their fathers, and this variations build up over generations to form dialects.[36]

Birds learn songs early in life with sub-vocalizations that develop into renditions of adult songs. Zebra Finches, the most popular species for birdsong research, develop a version of a familiar adult's song after 20 or more days from hatch. By around 35 days, the chick will have learned the adult song. The early song is "plastic" or variable and it takes the young bird two or three months to perfect the "crystallized" song (which is less variable) of sexually mature birds.[37]

File:Bird song development timeline.png

Timeline for song learning in different species. Diagram adapted from Brainard & Doupe, 2002[38].

Research indicates birds' acquisition of song is a form of motor learning that involves regions of the basal ganglia. Models of bird-song motor learning are sometimes used as models for how humans learn speech.[39] In some species such as zebra finches, learning of song is limited to the first year; they are termed 'age-limited' or 'close-ended' learners. Other species such as the canaries can develop new songs even as sexually mature adults; these are termed 'open-ended' learners.[40][41]

Researchers have hypothesized that learned songs allow the development of more complex songs through cultural interaction, thus allowing intraspecies dialects that help birds stay with their own kind within a species, and it allows birds to adapt their songs to different acoustic environments.[42]

Auditory feedback in bird song learning

Early experiments by Thorpe in 1954 showed the importance of a bird being able to hear a tutor's song. When birds are raised in isolation, away from the influence of conspecific males, they still sing. While the song they produce resembles the song of a wild bird, it lacks the complexity and sounds distinctly different[43]. The importance of the bird being able to hear himself sing in the sensorimotor period was later discovered by Konishi. Birds deafened before the song crystallization period went on to produce very different songs from the wild type.[44] These findings lead scientists to believe there could be a specific part of the brain dedicated to this specific type of learning.

File:Birdbrain.svg

Song learning pathway in birds (Based on Nottebohm, 2005)

The main focus in the search for the neuronal aspect of bird song learning was guided by the song template hypothesis. This hypothesis is the idea that when a bird is young he memorizes the song of his tutor. Later, during the development phase as an adult, he matches his own trial vocalizations using auditory feedback to an acoustic template in the brain. Based on this information, he adjusts his song if needed. To find this “song template,” experimenters lesioned certain parts of the brain and observed the effects.

  • Lesioning the song production pathway (RA, xXII or HVc) in the brain creates serious effects on song production in all birds.[45]
  • Lesions parts of the anterior forebrain pathway, or vocal learning pathway, DLM and area X, result in deficits in learning in all birds.[46]
  • Lesioning LMAN, located in the anterior forebrain pathway in young birds disrupts song production.[47]
  • Lesioning LMAN on an adult bird shows no effect.[48]
  • Lesioning LMAN on an adult canary (an "open-ended learner" species, which can learn songs later in life) shows a progressive deterioration of song.[49]

These results show that the area known as LMAN is the only brain area in the pathway that shows some plasticity and further studies have shown that this area of the brain responds best to the bird’s own song.[50][51][52]This neuroplasticity is vital for a bird being able to learn a song. The ability to make small adjustments based on auditory feedback is needed for the complexity of these beautiful songs. Just like any musician, birds need to practice and be able to evaluate what their song sounds like and what it's supposed to sound like in order to get it right.

To complete the picture on bird song learning, experimenters needed to discover the true plasticity of the brain. While deafening and creating auditory isolation were good techniques for discovering basic characteristics about the brain, a reversible procedure was needed to investigate further. The solution was found in disruption of the auditory feedback, or what a bird hears. A computer is able to capture the song of a singing bird and play back portions of its song, or selectively play back a certain syllable while the bird is signing. The computer is basically playing the age old trick of repeating whatever the bird sings, the "stop copying me" game. This creates such a disruption that an adult bird will start to decrystallize its song, which includes a loss of spectral and temporal rigidity characteristic of adult song. It reverts back to the song it started singing with, before any learning took place. Furthermore, when the feedback was stopped, the birds slowly recovered their original song, something that was unheard of. These results show that there is a fair amount of plasticity retained in the brain, even for close-ended learners[53]. This new found plasticity in adult birds and the results on the plasticity of LMAN (shown above) combine into a model for bird song learning (diagram coming soon).[54]

Identification and systematics

Song of the White-throated Sparrow

The specificity of bird calls has been used extensively for species identification. The calls of birds have been described using words or nonsense syllables. These are subject to imagination and vary greatly; a well-known example is the White-throated Sparrow's song, given in Canada as O sweet Canada Canada Canada and in New England as Old Sam Peabody Peabody Peabody (also Where are you Frederick Frederick Frederick?). In addition to nonsense words, grammatically correct phrases have been constructed as likenesses of the vocalizations of birds. For example, the Barred Owl produces a motif which some bird guides describe as Who cooks for you? Who cooks for you all? with the emphasis placed on you.[55]

Little brown dove

Sonogram of the call of a Laughing Dove. Recorded in south India (help·info)

The use of spectrographs to visualize bird song was first introduced by W. H. Thorpe.[56][57] These visual representations are also called sonograms or sonagrams. Some recent field guides for birds use sonograms to document the calls and songs of birds.[58] The sonogram is objective, unlike descriptive phrases, but proper interpretation requires experience. Sonograms can also be roughly converted back into sound.[59][60]

Bird song is an integral part of bird courtship and is a pre-zygotic isolation mechanism involved in the process of speciation. Many allopatric sub-species show differences in calls. These differences are sometimes minute, often detectable only in the sonograms. Song differences in addition to other taxonomic attributes have been used in the identification of new species.[61] The use of calls has led to proposals for splitting of species complexes such as those of the Mirafra Bushlarks.[62]

Prominent workers in the field

See also

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Cited reference

  1. ↑ Ehrlich, Paul R., David S. Dobkin, and Darryl Wheye. "Bird Voices" and "Vocal Development" from Birds of Stanford essays
  2. ↑ Howell, Steve N. G., and Sophie Webb (1995). A Guide to the Birds of Mexico and Northern Central America, Oxford University Press. ISBN 0-19-854012-4.
  3. ↑ Bostwick, Kimberly S. and Richard O. Prum (2005) Courting Bird Sings with Stridulating Wing Feathers. Science. 309(5735):736 DOI: 10.1126/science.1111701 [1]
  4. ↑ Manson-Barr, P. and Pye, J. D. (1985). Mechanical sounds. In A Dictionary of Birds (ed. B. Campbell and E. Lack), pp. 342-344. Staffordshire: Poyser.
  5. ↑ 5.0 5.1 Bostwick, Kimberly S. and Richard O. Prum 2003. High-speed video analysis of wing-snapping in two manakin clades (Pipridae: Aves). The Journal of Experimental Biology 206:3693-3706 [2]
  6. ↑ Read, A. W. and D. M. Weary 1990. Sexual selection and the evolution of bird song: A test of the Hamilton-Zuk hypothesis. Behavioral Ecology and Sociobiology. 26(1):47-56 [3]
  7. ↑ Garamszegi, L. Z., A. P. Møller, János Török, Gábor Michl, Péter Péczely and Murielle Richard. 2004. Immune challenge mediates vocal communication in a passerine bird: an experiment. Behavioral Ecology. 15(1): 148-157
  8. ↑ Redpath, S. M., Bridget M Appleby, Steve J Petty (2000) Do male hoots betray parasite loads in Tawny Owls? Journal of Avian Biology 31 (4), 457–462. [4]
  9. ↑ Reid, J. M., Peter Arcese, Alice L. E. V. Cassidy, Sara M. Hiebert, James N. M. Smith, Philip K. Stoddard, Amy B. Marr, and Lukas F. Keller (2005) Fitness Correlates of Song Repertoire Size in Free-Living Song Sparrows (Melospiza melodia) The American Naturalist, 165:299–310 [5]
  10. ↑ Marler, P. 1955. Characteristics of some animal calls. Nature 176:6-8.
  11. ↑ Lengagne, T., J. Lauga and T. Aubin. 2001. Intra-syllabic acoustic signatures used by the King Penguin in parent-chick recognition: an experimental approach. The Journal of Experimental Biology 204:663–672 [6]
  12. ↑ Wayne Delport, Alan C Kemp, J. Willem H Ferguson (2002) Vocal identification of individual African Wood Owls Strix woodfordii: a technique to monitor long-term adult turnover and residency Ibis 144 (1), 30–39.
  13. ↑ Thorpe, W. H. 1963. Antiphonal singing in birds as evidence for avian auditory reaction time. Nature, 197: 774-776.
  14. ↑ Stokes, A., W. and H. W. Williams. 1968. Antiphonal calling in quail. Auk, 85
  15. ↑ Harris, Tony; Franklin, Kim. Shrikes and Bush-Shrikes, 257–260, Princeton University Press. ISBN 0-691-07036-9.
  16. ↑ Osmaston, B. B. 1941. "Duetting" in birds. Ibis, 5: 310-311.
  17. ↑ Power, D. M. 1966. Antiphonal duetting and evidence for auditory reaction time in the Orange-chinned Parakeet. Auk, 83: 314-319.
  18. ↑ Goodale, E. and Kotagama, S. W. (2005) Testing the roles of species in mixed-species bird flocks of a Sri Lankan rain forest. Journal of Tropical Ecology 21: 669-676
  19. ↑ Suthers RA and Hector DH. 1985. The physiology of vocalization by the echolocating Oilbird, Steatornis caripensis. J Comp Physiol A156: 243-266
  20. ↑ Suthers RA and Hector DH. 1982. Mechanism for the production of echolocating clicks by the Grey Swiftlet, Collocalia spodiopygia. J Comp Physiol A148: 457-470.
  21. ↑ Coles RB, Konishi M and Pettigrew JD. 1987. Hearing and echolocation in the Australian Grey Swiftlet, Collocalia spodiopygia. J. Exp. Biol. 129:365-371
  22. ↑ Dooling, R.J. (1982) Auditory perception in birds. Acoustic Communication in Birds, Vol. 1 (eds D.E. Kroodsma & E.H. Miller), pp. 95–130. Academic Press, New York.
  23. ↑ Boncoraglio, G. and Nicola Saino (2007) Habitat structure and the evolution of bird song: a meta-analysis of the evidence for the acoustic adaptation hypothesis. Functional Ecology. 21:,134–142 [7]
  24. ↑ Morton, E.S. (1975) Ecological sources of selection on avian sounds. American Naturalist 109, 17–34.
  25. ↑ Krause, Bernard L. 1993. The Niche Hypothesis. The Soundscape Newsletter 06 [8]
  26. ↑ Henrik Brumm (2004) The impact of environmental noise on song amplitude in a territorial bird. Journal of Animal Ecology 73 (3), 434–440.
  27. ↑ Slabbekoorn, H. and Peet, M. 2003. Birds sing at a higher pitch in urban noise. Nature 424, 267.
  28. ↑ Collias, N. E. 1987. The vocal repertoire of the Red Junglefowl: A spectrographic classification and the code of communication. The Condor 89:510-524
  29. ↑ Evans, C. S., Macedonia, J. M., and Marler, P. (1993). Effects of apparent size and speed on the response of chickens, Gallus gallus, to computer-generated simulations of aerial predators. Animal Behaviour 46: 1-11
  30. ↑ Pepperberg, I.M. (2000). The Alex Studies: Cognitive and Communicative Abilities of Grey Parrots. Harvard.
  31. ↑ Marcus, Gary F. (2006-04-27). Language: Startling starlings. Nature 440 (7088): 1117-1118.
  32. ↑ Brainard, M. S. and Doupe, A. J. (2000). Auditory feedback in learning and maintenance of vocal behavior. Nature Rev. Neurosci. 1, 31-40.
  33. ↑ Bottjer, S. W. Halsema, E. A. and Arnold A. P. (1984). Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224, 901-903.
  34. ↑ Scharff C, Haesler S. 2005. An evolutionary perspective on FoxP2: strictly for the birds? Curr Opin Neurobiol. 15(6):694-703. [9]
  35. ↑ Barrington, D. 1773. Experiments and observations on the singing of birds. Philosophical Transactions of the Royal Society of London, 63, 249–291.
  36. ↑ Marler, P., & M. Tamura. 1962. Song dialects in three populations of the white-crowned sparrow. Condor 64:368–377.
  37. ↑ Nottebohm, F. (2005) The Neural Basis of Birdsong. PLoS Biol 3(5):163 [10]
  38. ↑ Brainard, M. S. and Doupe, A. J. (2002). What songbirds teach us about learning. Nature 417,351-358.
  39. ↑ Teramitsu I, Kudo LC, London SE, Geschwind DH, White SA. 2004. Parallel FoxP1 and FoxP2 expression in songbird and human brain predicts functional interaction. J. Neurosci. 24(13):3152-63. Full text
  40. ↑ Nottebohm, F. (2004) The road we travelled: discovery, choreography, and significance of brain replaceable neurons. Ann. N. Y. Acad. Sci. 1016:628–658
  41. ↑ Brenowitz, Eliot A. and Michael D. Beecher 2005. Song learning in birds: diversity and plasticity, opportunities and challenges. Trends in Neurosciences. 28(3):127-132 [11]
  42. ↑ Slater, P. J. B. 1989 Bird song learning: causes and consequences. Ethol. Ecol. Evol. 1: 19–46
  43. ↑ Thorpe, W. (1954). The process of song-learning in the chaffinch as studied by means of the sound spectograph. Nature 173, 465-469.
  44. ↑ Konishi, M. (1965). The role of auditory feedback on the control of vocalization in the white-crowned sparrow. Zeitschrift fur Tierpsychologie. 22. 770-783.
  45. ↑ Nottebohm, F.,Stokes, T. M. and Leonard, C. M. (1976). Central control of song in the canary, Serinus canaries. J. Comp. Neurol. 165, 457-486.
  46. ↑ Bottjer, S. W. Halsema, E. A. and Arnold A. P. (1984). Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224, 901-903.
  47. ↑ Bottjer, S. W. Halsema, E. A. and Arnold A. P. (1984). Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224, 901-903.
  48. ↑ Bottjer, S. W. Halsema, E. A. and Arnold A. P. (1984). Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224, 901-903.
  49. ↑ Bottjer, S. W. Halsema, E. A. and Arnold A. P. (1984). Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224, 901-903.
  50. ↑ Doupe, A. J. (1997). Song –and order – selective neurons in the songbird anterior forebrain and their emergence during vocal development. J Neurosci. 17, 1147-1167.
  51. ↑ Brainard, M. S. and Doupe, A. J. (2002). What songbirds teach us about learning. Nature 417,351-358.
  52. ↑ Brainard, M. S. and Doupe, A. J. (2000). Auditory feedback in learning and maintenance of vocal behavior. Nature Rev. Neurosci. 1, 31-40.
  53. ↑ Leonardo, A., Konishi, M. (1999). Decrystallization of adult birdsong by perturbation of auditory feedback. Letters to nature 399, 466-470.
  54. ↑ Brainard, M. S. and Doupe, A. J. (2000). Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 404, 762-766.
  55. ↑ Sibley, David (2000). The Sibley Guide to Birds, Knopf. ISBN 0-679-45122-6.
  56. ↑ Thorpe, W. H. 1958. The learning of song patterns by birds, with especial reference to the song of the chaffinch Fringilla coelebs. Ibis, 100, 535–570.
  57. ↑ Slater, P. J. B. (2003) Fifty years of bird song research: a case study in animal behaviour. Animal Behaviour 65:633–639 doi:10.1006/anbe.2003.2051
  58. ↑ Robbins, Chandler S., Bertel Bruun, Herbert S. Zim, Arthur Singer (2001). Birds of North America : A Guide To Field Identification, Golden Guides from St. Martin's Press. ISBN 1-58238-090-2.
  59. ↑ Meijer, P.B.L. 1992 An Experimental System for Auditory Image Representations. IEEE Transactions on Biomedical Engineering. 39(2):112-121 full text
  60. ↑ US Patent. 20030216649. Audible output sonogram analyzer. [12]
  61. ↑ Alström, P. & Ranft, R. 2003. The use of sounds in avian systematics, and the importance of bird sound archives. Bulletin of the British Ornithologists’ Club Supplement 123A: 114–135.
  62. ↑ Alström, P. (1998) Taxonomy of the Mirafra assamica complex. Forktail 13: 97-107 PDF

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