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Immanuel Kant’s Sparrow An integrative approach to canary-like singing House Sparrow (Passer domesticus) DISSERTATION der Fakultät für Biologie der Ludwig-Maximilian-Universität München vorgelegt von Lucie H. Salwiczek München, Mai 2004 durchgeführt am Max-Planck-Institut für Verhaltensphysiologie in Seewiesen 1. Gutachter: Prof. Dr. Wolfgang Wickler 2. Gutachter: Prof. Dr. Gerhard Neuweiler Tag der Abgabe: 05.05.2004 Tag der mündlichen Prüfung: 22.07.2004 Teaching birds to imitate tunes was a popular and lucrative hobby in the 18th century. The Bird Fancyer’s delight was the first collection of tunes, published by the rivals J. Meares (1717) and J. Walsh (1717). From Godman 1954. The most famous house sparrow was Clare Kipps’ Clarence. He produced a remarkable song with two sections (see below): first an introduction with the usual sparrow chirping, though less harsh in tone, followed by a several times repeated four note trills. The second more melodious part „opened with an eight-note trill, followed by a high, sweet, plaintive note. Then, descending by an interval of which I am not quite sure, it rose again to a second trill of eight notes a perfect fourth higher than the first. This theme was repeated several times and sometimes ended abruptly but more often returned to the tonic.“ From Kipps 1956b. III ABSTRACT The adoption of foreign song elements occurs under natural conditions in various songbird species including the house sparrow Passer domesticus, even though it may go largely unnoticed by humans. House sparrows singing canary song have been known by hobbyists for a long time. My study is the first to analyse the imitative abilities of house sparrows in detail. I used an integrative approach considering features that are particularly important for the degree of vocal learning that can be displayed by a species. These included (1) a genetic predisposition, (2) body condition of the parents, (3) food availability during early ontogeny, (4) social factors, (5) neuronal mechanisms, (6) hormonal states, and (7) body size and morphology of the vocal tract. House sparrows provided for 3 generations with food ad libitum could afford a high parental investment already at egg laying; this resulted in significantly higher hatchling weights of male and female neonates in the third breeding season in captivity. However, I could not find indications that hatchling weight influenced nestling growth, song learning, androgen levels or body size in adulthood. Sparrows are obligate insect eaters in the first two weeks after hatching, and thus suffered from low quality food when they were reared by seed eating canary foster parents. This resulted in a significantly lower body mass gain during the day. Canary-raised sparrows can learn the canary typical tour (= repetition of one type of syllables), but their songs did not match completely with the model. Tours are significantly shorter in sparrows than in canaries. While canaries sing several tours without a break, sparrows separate tours by a short silent interval. This goes in line with an increased volume of HVc, which codes besides others for syllable identity. However, this alone does not explain, why sparrows include such silent intervals. House sparrows distinguish between sequences comprising syllables only, or both tours and single syllables: they produce significantly less different syllable types per time in a pure syllable sequence than in a sequence with syllables and tours. The nucleus hyperstriatum ventrale pars caudale (HVc), a song control nucleus that is thought to coordinate temporal patterns, proved to be significantly increased in size in sparrow males IV singing canary-like song compared to no-tour singing sparrows, independent of the rearing parent species. Sparrow-reared sparrows did not differ from canary-reared sparrows, whether singing canary tours or not, in any of the other brain measures. The sparrow male’s song control system undergoes seasonal changes. Nevertheless, it happened that a sparrow produced canary-like tours with appropriate temporal patterning in autumn, when song nuclei are significantly smaller than during the breeding season. This is a surprising result since it has been shown for other birds that song deteriorates with reduced brain area size. Indeed some syllables varied between seasons. Singing proficiency was not enhanced by artificially elevated androgen plasma levels, nor did canary-like singing males possess naturally higher testosterone plasma levels. Testosterone implantation did not increase the dehydroepiandrosterone (DHEA) plasma levels and tour- singing sparrows did not show naturally higher DHEA plasma levels. But individuals who were kept in a sound-proof chamber for 2.5 days to study IEG response showed significanlty higher DHEA plasma level independend of their origin (wild-caught or bred in captivity) than individuals caged in ordinary rooms. Canary-raised sparrows were able to learn the canary-typical tour, but their songs did not match completely with the model. Differences between model and imitation may reflect distorted production rather than copying errors, because morphology can act as an interfering factor. When taking into account the birds’ body size and beak dimensions, it became probable that the house sparrow’s vocal proficiency for singing canary-like tours may be limited by intrinsic jaw mechanics and respiratory demands. House sparrows singing canary-like songs provide a rich tool for further integrative approaches. I suggest an interpretation combining all the above features under the perspective of female choice. Instead of searching for a „key adaptation“ or single explanation for the imitative ability (song learning ability) in passerines, it might be more appropriate to focus on the multiplicity of factors involved in song production that - shaped by different selective forces - promote the highly specific song adaptations. V ZUSAMMENFASSUNG Schon seit Jahrhunderten sind Haussperlinge bei Vogelliebhabern als gelehrige Imitatoren fremder Laute und Gesänge bekannt. Am häufigsten wird von Sperlingen berichtet, die von Kanarienvögeln aufgezogen wurden und den Kanariengesang lernten. Wissenschaftlern hingegen blieb dieses Wissen bislang weitgehend verborgen. In dieser Arbeit wird erstmals der wissenschaftliche Nachweis erbracht, daß Sperlinge tatsächlich den Kanariengesang lernen und produzieren. Dazu habe ich einen integrativen Forschungsansatz verwendet, der folgende Aspekte umfaßt: (1) Einflüsse der Aufzucht durch Kanarienvögel oder Sperlinge; (2) Gesänge von Haussperlingen, aufgezogen von Kanarienvögeln oder Sperlingen; (3) Gehirnstrukturen (HVc, RA), welche dem Gesang zugrunde liegen; (4) Einflüsse von Steroidhormonen (Testosteron, DHEA) auf die Gesangsproduktion; (5) Einflüsse des Stimmapparates auf die Gesangsproduktion. (1) Haussperlinge sind in ihren ersten beiden Lebenswochen obligate Insektenfresser, Kanarienvögel aber lebenslang weitgehend Körnerfresser. Spatzenjunge in Kanariennestern erhalten folglich vergleichsweise weniger Protein in der Zeit größten Wachstums als ihre Sperlingsgeschwister im elterlichen Nest. Die unterschiedliche Ernährung wurde u.a. im Körpergewicht deutlich: Sperlingsjunge in Kanariennestern zeigten einen signifikant geringeren Gewichtszuwachs pro Tag als ihre Geschwister unter Fürsorge ihrer Eltern (Kapitel 2). (2) Männliche, von Kanarienvögeln aufgezogene Haussperlinge kopierten die für ihren Ziehvater typischen Touren (= rasche Wiederholung einer Silbe), wenn auch in modifizierter Form (Kapitel 3). Touren sind bei Sperlingen deutlich kürzer (selten länger als 1 Sekunde) als bei Kanarienmännchen (mehrere Sekunden). Sperlinge trennen aufeinanderfolgende Touren durch eine kurze Stille, während Kanarienmännchen sie ohne Pause aneinanderreihen. Dadurch muten von Spatzen gesungene Touren wie eine komplizierte Einzelsilbe an, die viele (gleiche) Elemente enthält. Weibchen verschiedener Vogelarten bevorzugen Männchen, die viele verschiedene Silben in möglichst kurzer Zeit singen. Von Kanarienvögeln aufgezogene Sperlinge produzieren sowohl Sequenzen, die nur Sperlingssilben enthalten, als auch Sequenzen, in denen sie Sperlingssilben VI und Kanarientouren kombinieren: In kombinierten Sequenzen werden signifikant mehr verschiedene Silben pro Zeiteinheit gesungen als in reinen Sperlingssequenzen. Dies gilt ausschließlich für Sperlinge, die als Nestlinge nicht nur den Kanariengesang gehört haben, sondern auch von Kanarienvögeln gefüttert wurden (Kapitel 3). (3) Der Gesangskern HVc ist nachweislich zuständig für das Erkennen von Silben sowie für das zeitliche Muster des Gesangs (Kapitel 4). Von Kanarien aufgezogene Sperlinge, die Touren singen, besitzen einen signifikant größeren HVc als Sperlinge, die ebenfalls von Kanarienvögeln aufgezogen wurden, aber keine Touren singen. Die Volumenzunahme kann zum einen auf einer stärkeren Vernetzung der Nervenzellen basieren, wie sie auch von anderen Tierarten bekannt ist. In der neueren Vogelliteratur finden sich andererseits Hinweise, daß auch Gliazellen bei Volumenzunahme eine größere Bedeutung haben als bisher gedacht. Von verschiedenen Tierarten ist bekannt, daß mehrjährige Gefangenschaftshaltung die Größe verschiedener Gehirnbereiche negativ beeinflussen kann. Bei meinen Haussperlingen konnte ich einen solchen Einfluß nicht finden (Kapitel 4). Wohl aber variierten die Volumina der Gehirnkerne in Abhängigkeit von der Jahreszeit; im Herbst und Winter waren sie signifikant kleiner als im Sommer. Trotz des verkleinerten HVc, zuständig
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