Abstract
As urbanization expands globally, the communication systems of an increasing number of species are affected. Because bird song is a long-distance signal used to attract mates and defend territories, the evolution of bird song is often shaped by habitat structure and background noise. These potential drivers of song evolution are more often studied in natural areas than in urbanized areas, leaving open the question of how anthropogenic changes to the landscape are affecting the evolution of bird song. One songbird that persists in both urbanized and rural areas in North America is the White-crowned Sparrow (Zonotrichia leucophrys). Our previous work demonstrates that increased background noise in cities and in natural habitats affects acoustic adaptation in this species. However, we lack information about how sound transmits in urban and rural habitats. Because cities tend to have different physical properties than rural areas, it is pertinent to understand the influence of urban habitat structure on song evolutionary processes. Here, we test the acoustic adaptation theory and hypothesize that differences in the sound transmission properties of urban and rural habitats affect song divergence between urban and rural populations. We conducted sound transmission trials of tones from 1 to 8 kHz on 59 White-crowned Sparrow territories in three urban and three rural locations around San Francisco and Point Reyes, California, at varying heights and rates of note production. We also recorded and analyzed songs of males from each location to see if differences in signal–noise ratio, attenuation, reverberation, and distortion predicted song divergence. We found that urban locations have higher attenuation and reverberation than rural locations and urban songs tend to have short whistles, faster trills, and narrower bandwidth. These findings partially support acoustic adaptation theory, though faster trills in the city may instead be driven by cultural drift or sexual selection. Overall, our results add to a rapidly growing area of research and allow us to better understand the complexity of influences on song divergence.
Zusammenfassung
Erhöhte Dämpfung und Nachhall sind mit niedrigeren Maximalfrequenzen und einer engen Bandbreite von Vogelliedern in Städten verbunden
Da die Urbanisierung weltweit zunimmt, sind die Kommunikationssysteme einer zunehmenden Anzahl von Arten betroffen. Da Vogelgesang ein Fernsignal ist, das verwendet wird, um Partner anzuziehen und Gebiete zu verteidigen, wird die Entwicklung des Vogelgesangs häufig durch die Struktur des Lebensraums und Hintergrundgeräusche geprägt. Diese potenziellen Treiber der Liedentwicklung werden häufiger in natürlichen Gebieten als in städtischen Gebieten untersucht, wobei die Frage offen bleibt, wie sich anthropogene Veränderungen der Landschaft auf die Entwicklung des Vogelgesangs auswirken. Ein Singvogel, der sowohl in städtischen als auch in ländlichen Gebieten Nordamerikas vorkommt, ist der Weißkronenspatz (Zonotrichia leucophrys). Unsere früheren Arbeiten zeigen, dass vermehrte Hintergrundgeräusche in Städten und in natürlichen Lebensräumen die akustische Anpassung dieser Art beeinflussen. Es fehlen jedoch Informationen darüber, wie Schall in städtischen und ländlichen Lebensräumen übertragen wird. Da Städte tendenziell andere physikalische Eigenschaften haben als ländliche Gebiete, ist es wichtig, den Einfluss der städtischen Lebensraumstruktur auf die Entwicklungsprozesse von Liedern zu verstehen. Hier testen wir die Theorie der akustischen Anpassung und stellen die Hypothese auf, dass Unterschiede in den Schallübertragungseigenschaften von städtischen und ländlichen Lebensräumen die Lieddivergenz zwischen städtischen und ländlichen Bevölkerungsgruppen beeinflussen. Wir haben Schallübertragungsversuche mit Tönen von 1 bis 8 kHz in 59 White-Crowned Sparrow-Gebieten in drei städtischen und drei ländlichen Gebieten um San Francisco und Point Reyes, Kalifornien, in unterschiedlichen Höhen und Raten der Notenproduktion durchgeführt. Wir haben auch Songs von Männern von jedem Ort aufgenommen und analysiert, um festzustellen, ob Unterschiede im Signal-Rausch-Verhältnis, der Dämpfung, dem Nachhall und der Verzerrung die Song-Divergenz vorhersagen. Wir haben festgestellt, dass städtische Standorte eine höhere Dämpfung und einen höheren Nachhall aufweisen als ländliche Standorte und städtische Songs tendenziell kurze Pfeifen, schnellere Triller und eine geringere Bandbreite aufweisen. Diese Ergebnisse stützen teilweise die akustische Anpassungstheorie, obwohl schnellere Triller in der Stadt stattdessen durch kulturelle Drift oder sexuelle Selektion angetrieben werden können. Insgesamt tragen unsere Ergebnisse zu einem schnell wachsenden Forschungsbereich bei und ermöglichen es uns, die Komplexität der Einflüsse auf die Songdivergenz besser zu verstehen.
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References
Andersson MB (1994) Sexual selection. Princeton University Press, Princeton
Baker MC, Thompson DB, Sherman GL et al (1982) Allozyme frequencies in a linear series of song dialect populations. Evolution (N Y) 36:1020–1029. https://doi.org/10.2307/2408079
Baptista LF (1975) Song dialects and demes in sedentary populations of the white-crowned sparrow (Zonotrichia leucophrys nuttalli). Univ Calif Publ Zool 105:20
Beeman K (1998) Digital signal analysis, editing, and synthesis. In: Hopp SL, Owren MJ, Evans CS (eds) Animal acoustic communication: sound analysis and research methods. Springer, Berlin
Billings AC (2018) The low-frequency acoustic structure of mobbing calls differs across habitat types in three passerine families. Anim Behav 138:e74–e74. https://doi.org/10.1016/j.anbehav.2018.02.001
Blanchard BD (1936) Continuity of behavior in the Nuttall white-crowned sparrow. Condor 38:145–150
Blanchard BD (1941) The white-crowned sparrows (Zonotrichia leucophrys) of the Pacific seaboard: environment and annual cycle. University of California Press, Oakland, California, USA
Boncoraglio G, Saino N (2007) Habitat structure and the evolution of bird song: a meta-analysis of the evidence for the acoustic adaptation hypothesis. Funct Ecol 21:134–142. https://doi.org/10.1111/j.1365-2435.2006.01207.x
Boughman JW (2002) How sensory drive can promote speciation. Trends Ecol Evol 17:571–577
Chilton G, Baker MC, Barrentine CD, Cunningham MA (1995) White-crowned sparrow (Zonotrichia leucophrys). In: Poole A, Gill FB (eds) The birds of North America, vol 183. Academy of Natural Sciences. Philadelphia, Pennsylvania, USA, pp 1–28
Derryberry EP (2007) Evolution of bird song affects signal efficacy: an experimental test using historical and current signals. Evolution (N Y) 61:1938–1945. https://doi.org/10.1111/j.1558-5646.2007.00154.x
Derryberry EP (2009) Ecology shapes birdsong evolution: variation in morphology and habitat explains variation in white-crowned sparrow song. Am Nat 174:24–33. https://doi.org/10.1086/599298
Derryberry EP, Danner RM, Danner JE et al (2016) Patterns of song across natural and anthropogenic soundscapes suggest that white-crowned sparrows minimize acoustic masking and maximize signal content. PLoS One 11:e0154456. https://doi.org/10.1371/journal.pone.0154456
DeSante D, Baptista L(1989) Factors affecting the termination of breeding in Nuttall's White-crowned Sparrows. Wilson Bull 101(1):120–124
Dowling JL, Luther DA, Marra PP (2011) Comparative effects of urban development and anthropogenic noise on bird songs. Behav Ecol 23:201–209. https://doi.org/10.1093/beheco/arr176
Endler J (1992) Signals, signal conditions, and the direction of evolution. Am Nat139:125–153
Gall MD, Ronald KL, Bestrom ES, Lucas JR (2012) Effects of habitat and urbanization on the active space of brown-headed cowbird song. J Acoust Soc Am 132:4053–4062. https://doi.org/10.1121/1.4764512
Homer CG, Dewitz JA, Yang L, Jin S, Danielson P, Xian G et al (2011) Completion of the 2006 national land cover database for the conterminous United States. Photogramm Eng Remote Sens 77:858–566
Homer CH, Fry JA, Barnes CA (2012). The national land cover database. U.S. Geological Survey Fact Sheet 2012-3020, p 4. https://doi.org/10.3133/fs20123020
Katti M, Warren PS (2004) Tits, noise and urban bioacoustics. Trends Ecol Evol 19:109–110. https://doi.org/10.1016/j.tree.2003.12.006
Kight CR, Hinders MK, Swaddle JP (2013) Chapter 5: acoustic space is affected by anthropogenic habitat features: implications for avian vocal communication. Ornithol Monogr 74:47–62. https://doi.org/10.1525/om.2012.74.1.47.3
Kight CR, Saha MS, Swaddle JP (2012) Anthropogenic noise is associated with reductions in the productivity of breeding Eastern Bluebirds (Sialia sialis). Ecol Appl 22:1989–1996. https://doi.org/10.1890/12-0133.1
Lazerte SE, Otter KA, Slabbekoorn H et al (2015) Relative effects of ambient noise and habitat openness on signal transfer for chickadee vocalizations in rural and urban green-spaces. Bioacoustics 24:233–252. https://doi.org/10.1080/09524622.2015.1060531
LaZerte SE, Slabbekoorn H, Otter KA et al (2016) Learning to cope: vocal adjustment to urban noise is correlated with prior experience in black-capped chickadees. Proc R Soc B 283:e27052–e27052. https://doi.org/10.1098/rspb.2016.1058
Lee C, MacDonald J (2013) Golden gate national recreation area: acoustical monitoring 2007/2008. Fort Collins, CO
Lee C, MacDonald J (2011) Baseline ambient sound levels in Point Reyes National Seashore. Los Angeles
Luther D, Baptista L (2010) Urban noise and the cultural evolution of bird songs. Proc R Soc B 277:469–473. https://doi.org/10.1098/rspb.2009.1571
Luther DA, Phillips J, Derryberry EP (2016) Not so sexy in the city: urban birds adjust songs to noise but compromise vocal performance. Behav Ecol 27:332–340. https://doi.org/10.1093/beheco/arv162
Luther DA, Phillips J, Derryberry EP (2015) Not so sexy in the city: urban birds adjust songs to noise but compromise vocal performance. Behav Ecol. https://doi.org/10.1093/beheco/arv162
Marler P, Tamura M (1962) Song “Dialects” in three populations of white-crowned sparrows. Condor 64:368–377
Mewaldt RL, King JR (1977) The annual cycle of white-crowned sparrows (Zonotrichia leucophrys nuttalli) in coastal California. The Condor 79:445–455
Mockford EJ, Marshall RC, Dabelsteen T (2011) Degradation of rural and urban great tit song: testing transmission efficiency. PLoS One 6:e28242. https://doi.org/10.1371/journal.pone.0028242
Morton ES (1975) Ecological sources of selection on avian sounds. Am Nat 109:17–34
Moseley DL, Derryberry GE, Phillips JN et al (2018) Acoustic adaptation to city noise through vocal learning by a songbird. Proc R Soc B 285:20181356
Nelson DA, Soha JA (2004) Perception of geographical variation in song by male Puget Sound white-crowned sparrows, Zonotrichia leucophrys pugetensis. Anim Behav 68:395–405. https://doi.org/10.1016/j.anbehav.2003.08.027
Nemeth E, Dabelsteen T, Pedersen SB, Winkler H (2006) Rainforests as concert halls for birds: are reverberations improving sound transmission of long song elements? J Acoust Soc Am 119:620. https://doi.org/10.1121/1.2139072
Peters S, Derryberry EP, Nowicki S (2012) Songbirds learn songs least degraded by environmental transmission. Biol Lett 8:736–739. https://doi.org/10.1098/rsbl.2012.0446
Phillips JN, Berlow M, Derryberry EP (2018) The effects of landscape urbanization on the gut microbiome: an exploration into the gut of urban and rural white-crowned sparrows. Front Ecol Evol 6:148. https://doi.org/10.3389/fevo.2018.00148
Phillips JN, Derryberry EP (2017a) Equivalent effects of bandwidth and trill rate: support for a performance constraint as a competitive signal. Anim Behav 132:209–215. https://doi.org/10.1016/j.anbehav.2017.08.012
Phillips JN, Derryberry EP (2017b) Vocal performance is a salient signal for male–male competition in White-crowned Sparrows. Auk 134:564–574. https://doi.org/10.1642/AUK-17-2.1
Phillips JN, Derryberry EP (2018) Urban sparrows respond to a sexually selected trait with increased aggression in noise. Sci Rep 8:7505. https://doi.org/10.1038/s41598-018-25834-6
Price MA, Attenborough K, Heap NW (1988) Sound attenuation through trees: measurements and models. J Acoust Soc Am 84:1836–1844. https://doi.org/10.1121/1.397150
R Development Core Team R (2015) R: a language and environment for statistical computing
Richards DG, Wiley RH (1980) Reverberations and amplitude fluctuations in the propagation of sound in a forest: implications for animal comunication. Am Nat 115:381–399
Slabbekoorn H (2013) Songs of the city: noise-dependent spectral plasticity in the acoustic phenotype of urban birds. Anim Behav 85:1089–1099. https://doi.org/10.1016/j.anbehav.2013.01.021
Slabbekoorn H, den Boer-Visser A (2006) Cities change the songs of birds. Curr Biol 16:2326–2331. https://doi.org/10.1016/j.cub.2006.10.008
Slabbekoorn H, Ellers J, Smith (2002) Birdsong and sound transmission: the benefits of reverberations. Condor 104:564–573
Slabbekoorn H, Yeh P, Hunt K (2007) Sound transmission and song divergence: a comparison of urban and forest acoustics. Condor 109:67–78
Soha JA, Marler P (2001) Cues for early discrimination of conspecific song in the white-crowned sparrow (Zonotrichia leucophrys). Ethology 107:813–826. https://doi.org/10.1046/j.1439-0310.2001.00713.x
Swaddle JP, Francis CD, Barber JR et al (2015) A framework to assess evolutionary responses to anthropogenic light and sound. Trends Ecol Evol 30:550–560. https://doi.org/10.1016/j.tree.2015.06.009
Tobias JA, Aben J, Brumfield RT et al (2010) Song divergence by sensory drive in Amazonian birds. Evolution (N Y) 64:2820–2839
Warren PS, Katti M, Ermann M, Brazel A (2006) Urban bioacoustics: it’s not just noise. Anim Behav 71:491–502. https://doi.org/10.1016/j.anbehav.2005.07.014
Wiley RH (2006) Signal detection and animal communication. Adv Study Behav 36:217–247. https://doi.org/10.1016/S0065-3454(06)36005-6
Wiley RH, Richards DG (1982) Adaptations for acoustic communication in birds: sound transmission and signal detection. In: Kroodsma DE, Miller EH, Ouellet H (eds) Acoustic communication in birds. Academic Press, New York
Wiley RH, Richards DG (1978) Physical constraints on acoustic communication in the atmosphere: implications for the evolution of animal vocalizations. Behav Ecol Sociobiol 3:69–94
Zollinger SA, Podos J, Nemeth E et al (2012) On the relationship between, and measurement of, amplitude and frequency in birdsong. Anim Behav 84:e1–e9. https://doi.org/10.1016/j.anbehav.2012.04.026
Acknowledgements
Several students helped JNP and CR analyze the song data, including S. McCombs, K. Wadsworth, and M. Schmidt. Funding provided by National Science Foundation Integrative Organismal Systems (award number 1354756 and 1354763).
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All studies adhered to ethical guidelines approved by Tulane Institutional Animal Care and Use Committee and the National Park Service Institutional Animal Care and Use Committee. Permits were provided by U.S. Fish and Wildlife Service (MB679782-1), the Bird Banding Laboratory (23900), and the California National Resources Agency (SC-6799), Golden Gate National Recreation Area (SCI-0007), San Francisco Parks and Recreation (041415), and by Point Reyes National Seashore (SCI-0016).
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This article is a contribution to the Topical Collection 27th International Ornithological Congress, Vancouver, Canada, 19–26 August 2018.
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Phillips, J.N., Rochefort, C., Lipshutz, S. et al. Increased attenuation and reverberation are associated with lower maximum frequencies and narrow bandwidth of bird songs in cities. J Ornithol 161, 593–608 (2020). https://doi.org/10.1007/s10336-020-01751-2
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DOI: https://doi.org/10.1007/s10336-020-01751-2