Abstract
Vocal plasticity may allow birds to reduce masking effects of noise pollution arising from urbanization. Mountain chickadees (Poecile gambeli) use both songs and calls during the dawn chorus, which vary in masking susceptibility. Thus, increasing song or call frequency, or switching between vocalization types are all potential mechanisms to reduce masking during fluctuating noise conditions. Further, prior experience with noise pollution may be a necessary precursor to allow birds to alter signals in response to sudden noisy conditions. To determine how mountain chickadee songs, calls, and chorus composition are affected by noise, we recorded 55 males across gradients of local ambient noise and habitat urbanization in three cities in British Columbia, Canada. Of these individuals, 31 were also exposed to 5-min experimental noise treatments. Habitat urbanization was quantified through a continuous index reflecting properties of urbanized areas. Only song frequency increased with local ambient noise, and this effect varied regionally. In response to experimental noise exposure, males increased the frequency of their calls (but not of their songs), and varied their use of songs vs. calls. Interestingly, this response was dependent on local ambient noise levels: males in noisy areas shifted to using relatively more songs, whereas males in quiet areas shifted to using relatively more calls. These findings may suggest that although mountain chickadees are capable of adjusting their vocalizations, choosing a response which can lead to masking release may require prior exposure to high levels of ambient noise.
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References
Bagwell C, Sykes R, Giard P (2013) SoX. Version 14.4.0. http://sox.sourceforge.net
Baker MC, Becker AM (2002) Mobbing calls of black-capped chickadees: effects of urgency on call production. Wilson Bull 114:510–516
Bates D, Maechler M, Bolker B, Walker S (2016) lme4: Linear mixed-effects models using Eigen and S4. http://CRAN.R-project.org/package=lme4
Bermúdez-Cuamatzin E, Ríos-Chelén AA, Gil D, Garcia CM (2009) Strategies of song adaptation to urban noise in the house finch: syllable pitch plasticity or differential syllable use? Behaviour 146:1269–1286
Bermúdez-Cuamatzin E, Ríos-Chelén AA, Gil D, Garcia CM (2011) Experimental evidence for real-time song frequency shift in response to urban noise in a passerine bird. Biol Lett 7:36–38
Branch CL, Pravosudov VV (2015) Mountain chickadees from different elevations sing different songs: acoustic adaptation, temporal drift or signal of local adaptation? R Soc Open Sci 2:150019. doi:10.1098/rsos.150019
Browne WJ, Subramanian SV, Jones K, Goldstein H (2005) Variance partitioning in multilevel logistic models that exhibit overdispersion. J R Stat Soc Ser A Stat Soc 168:599–613. doi:10.1111/j.1467-985X.2004.00365.x
Brumm H (2004) The impact of environmental noise on song amplitude in a territorial bird. J Anim Ecol 73:434–440
Brumm H, Zollinger SA (2011) The evolution of the Lombard effect: 100 years of psychoacoustic research. Behaviour 148:1173–1198. doi:10.1163/000579511X605759
Clergeau P, Croci S, Jokimäki J et al (2006) Avifauna homogenisation by urbanisation: analysis at different European latitudes. Biol Conserv 127:336–344
des Aunay GH, Slabbekoorn H, Nagle L et al (2014) Urban noise undermines female sexual preferences for low-frequency songs in domestic canaries. Anim Behav 87:67–75
Dowling JL, Luther DA, Marra PP (2012) Comparative effects of urban development and anthropogenic noise on bird songs. Behav Ecol 23:201–209. doi:10.1093/beheco/arr176
Francis CD, Ortega CP, Cruz A (2011) Different behavioural responses to anthropogenic noise by two closely related passerine birds. Biol Lett 7:850–852. doi:10.1098/rsbl.2011.0359
Fuller RA, Warren PH, Gaston KJ (2007) Daytime noise predicts nocturnal singing in urban robins. Biol Lett 3:368–370
Gaddis PK (1985) Structure and variability in the vocal repertoire of the mountain chickadee. Wilson Bull 97:30–46
Google Inc (2012) Google Earth http://google.com/earth/
Grace MK, Anderson RC (2014) No frequency shift in the “D” notes of Carolina chickadee calls in response to traffic noise. Behav Ecol Sociobiol 69:1–11. doi:10.1007/s00265-014-1838-0
Grava A, Otter KA, Grava T et al (2013) Character displacement in dawn chorusing behaviour of sympatric mountain and black-capped chickadees. Anim Behav 86:177–187
Halfwerk W, Slabbekoorn H (2009) A behavioural mechanism explaining noise-dependent frequency use in urban birdsong. Anim Behav 78:1301–1307
Halfwerk W, Bot S, Buikx J et al (2011) Low-frequency songs lose their potency in noisy urban conditions. Proc Natl Acad Sci 108:14549–14554. doi:10.1073/pnas.1109091108
Ho R (2006) Handbook of univariate and multivariate data analysis and interpretation with SPSS. Chapman and Hall/CRC, Boca Raton
Hu Y, Cardoso GC (2010) Which birds adjust the frequency of vocalizations in urban noise? Anim Behav 79:863–867
Hughes M, Nowicki S, Lohr B (1998) Call learning in black-capped chickadees (Parus atricapillus): the role of experience in the development of “Chick-A-Dee” calls. Ethology 104:232–249. doi:10.1111/j.1439-0310.1998.tb00065.x
Kahle D, Wickham H (2013) Ggmap: spatial visualization with ggplot2. R J 5:144–161
Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: Tests in Linear Mixed Effects Models. http://CRAN.R-project.org/package=lmerTest
LaZerte SE, Otter KA, Slabbekoorn H (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. doi:10.1080/09524622.2015.1060531
LaZerte SE, Slabbekoorn H, Otter KA (2016) Learning to cope: vocal adjustment to urban noise is correlated with prior experience in black-capped chickadees. Proc R Soc B Biol Sci 283:20161058
Legendre P, Legendre L (1998) Numerical ecology, 2nd edn. Elsevier, Amsterdam
Lohr B (2008) Pitch-related cues in the songs of sympatric mountain and black-capped chickadees. Behav Process 77:156–165. doi:10.1016/j.beproc.2007.11.003
Luther D, Magnotti J (2014) Can animals detect differences in vocalizations adjusted for anthropogenic noise? Anim Behav 92:111–116. doi:10.1016/j.anbehav.2014.03.033
Mammen DL, Nowicki S (1981) Individual differences and within-flock convergence in chickadee calls. Behav Ecol Sociobiol 9:179–186. doi:10.1007/BF00302935
McCallum DA, Grundel R, Dahlsten DL (1999) Mountain chickadee (Poecile gambeli). In: Poole A (ed) The birds of North America online. Cornell Laboratory of Ornithology, Ithaca
McClure CJW, Ware HE, Carlisle J et al (2013) An experimental investigation into the effects of traffic noise on distributions of birds: avoiding the phantom road. Proc R Soc B Biol Sci 280:20132290. doi:10.1098/rspb.2013.2290
McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260
Mennill DJ, Otter KA (2007) Status signalling and communication networks in chickadees: complex communication with a simple song. In: Otter KA (ed) Ecology and behavior of chickadees and titmice. Oxford University Press, Oxford, pp 215–235
Mostrum AM, Curry RL, Lohr B (2002) Carolina chickadee (Poecile carolinensis). In: Rodewald PG (ed) The birds of North America online. Cornell Laboratory of Ornithology, Ithaca
Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605. doi:10.1111/j.1469-185X.2007.00027.x
Nowicki S (1989) Vocal plasticity in captive black-capped chickadees: the acoustic basis and rate of call convergence. Anim Behav 37:64–73
Otter KA, Chruszcz B, Ratcliffe L (1997) Honest advertisement and song output during the dawn chorus of black-capped chickadees. Behav Ecol 8:167–173
Patricelli GL, Blickley JL (2006) Avian communication in urban noise: causes and consequences of vocal adjustment. Auk 123:639–649
Potvin DA, Parris KM, Mulder RA (2011) Geographically pervasive effects of urban noise on frequency and syllable rate of songs and calls in silvereyes (Zosterops lateralis). Proc R Soc B Biol Sci 278:2464–2469. doi:10.1098/rspb.2010.2296
Potvin DA, Mulder RA, Parris KM (2014) Silvereyes decrease acoustic frequency but increase efficacy of alarm calls in urban noise. Anim Behav 98:27–33. doi:10.1016/j.anbehav.2014.09.026
Quinn GGP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Read J, Jones G, Radford AN (2014) Fitness costs as well as benefits are important when considering responses to anthropogenic noise. Behav Ecol 25:4–7. doi:10.1093/beheco/art102
Rı́os-Chelén AA, Salaberria C, Barbosa I et al (2012) The learning advantage: bird species that learn their song show a tighter adjustment of song to noisy environments than those that do not learn. J Evol Biol 25:2171–2180. doi:10.1111/j.1420-9101.2012.02597.x
Ripmeester EAP, Kok JS, van Rijssel JC, Slabbekoorn H (2010) Habitat-related birdsong divergence: a multi-level study on the influence of territory density and ambient noise in European blackbirds. Behav Ecol Sociobiol 64:409–418
Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113. doi:10.1111/j.2041-210X.2010.00012.x
Slabbekoorn H (2013) Songs of the city: noise-dependent spectral plasticity in the acoustic phenotype of urban birds. Anim Behav 85:1089–1099
Slabbekoorn H, Bouton N (2008) Soundscape orientation: a new field in need of sound investigation. Anim Behav 76:e5–e8
Slabbekoorn H, den Boer-Visser A (2006) Cities change the songs of birds. Curr Biol 16:2326–2331
Slabbekoorn H, Peet M (2003) Birds sing at a higher pitch in urban noise. Nature 424:267
Slabbekoorn H, Ripmeester EAP (2008) Birdsong and anthropogenic noise: implications and applications for conservation. Mol Ecol 17:72–83
Sol D, Lapiedra O, Gonzalez-Lagos C (2013) Behavioural adjustments for a life in the city. Anim Behav 85:1101–1112. doi:10.1016/j.anbehav.2013.01.023
Specht R (2012) Avisoft-SASLab pro. Avisoft Bioacoustics
Sueur J, Aubin T, Simonis C (2008) Seewave: a free modular tool for sound analysis and synthesis. Bioacoustics 18:213–226
Templeton CN, Greene E, Davis K (2005) Allometry of alarm calls: black-capped chickadees encode information about predator size. Science 308:1934–1937. doi:10.1126/science.1108841
The GIMP Team (2013) GIMP. http://www.gimp.org
Verzijden MN, Ripmeester EAP, Ohms VR et al (2010) Immediate spectral flexibility in singing chiffchaffs during experimental exposure to highway noise. J Exp Biol 213:2575–2581
Warren PS, Katti M, Ermann M, Brazel A (2006) Urban bioacoustics: It’s not just noise. Anim Behav 71:491–502
Wendorf CA (2004) Primer on multiple regression coding: common forms and the additional case of repeated contrasts. Underst Stat 3:47–57
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York
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. doi:10.1016/j.anbehav.2012.04.026
Acknowledgements
The assistance of technicians Samantha Krause and Kristen Marini was greatly appreciated. We wish to thank BC Parks, City of Williams Lake, City of Kelowna, City of Kamloops, Regional District of the Central Okanagan, Thompson Rivers University, and University of British Columbia Okanagan for permitting us to conduct our studies in their parks and on their grounds. Financial support was provided by The James L. Baillie Memorial Fund of Bird Studies Canada to SE LaZerte; by the Natural Sciences and Engineering Research Council of Canada (NSERC) through a personal PGS doctoral scholarship to SE LaZerte and through a Discovery grant to KA Otter; and by the University of Northern British Columbia through Graduate Entrance Research Awards and a Research Project Award to SE LaZerte.
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This work was approved by the University of Northern British Columbia Animal Care and Use Committee (protocol No. 2011–05).
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LaZerte, S.E., Otter, K.A. & Slabbekoorn, H. Mountain chickadees adjust songs, calls and chorus composition with increasing ambient and experimental anthropogenic noise. Urban Ecosyst 20, 989–1000 (2017). https://doi.org/10.1007/s11252-017-0652-7
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DOI: https://doi.org/10.1007/s11252-017-0652-7