Abstract
There is growing concern that anthropogenic noise has various deleterious effects on wildlife in urban environments. In humans, it has been suggested that anthropogenic noise exposure during childhood can have long-term effects on cognitive processes in adulthood. Here we tested if urban noise impacts avian cognitive performance by testing adult zebra finches (Taeniopygia guttata) on several cognition tasks in the presence or absence of urban noise playback. We also tested if urban noise impacts growth and cognitive development by testing adult zebra finches on cognition tasks after exposing them to urban noise, pink noise, or no noise during their first 90 days of life. We found that urban noise exposure marginally reduced cognitive performance during tests of a novel motor skill but did not reduce performance during tests of color association learning or spatial memory tasks. We found that urban noise exposure during development marginally affected cognitive performance in adulthood on a color association task. While urban noise exposure during development did not affect adult body size, treated males and females developed less bright bill coloration and redder bills, respectively, than untreated birds. Our results suggest that urban noise exposure may affect morphological traits, such as bill color, that influence social interactions and mate choice. Future studies should examine how noise exposure affects other cognitive behaviors, such as social behavior, and how social behavior in turn might exacerbate or mitigate negative effects of noise.
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Data Availability
The datasets generated during and/or analysed during the current study are available in the Figshare repository, https://doi.org/10.6084/m9.figshare.21706580.v2.
References
Afarinesh MR, Akhtardanesh B, Haghpanah T, Golshan F, Meftahi GM, Ghanbarpour N, Fakhri A, Sheikhshoaei S, Sheibani V (2018) Urban traffic noise pollution disturbs spatial learning and memory and increases anxiety-like behavior in adult male rats. J Physiol Pharmacol 220:146–154
Anderson RC, Searcy WA, Peters S, Hughes M, DuBois AL, Nowicki S (2017) Song learning and cognitive ability are not consistently related in a songbird. Anim Cogn 20:309–320. https://doi.org/10.1007/s10071-016-1053-7
Andersson M (1994) Sexual selection. Princeton University Press, Princeton (NJ)
Ardia DR, Broughton DR, Gleicher MJ (2010) Short-term exposure to testosterone propionate leads to rapid bill color and dominance changes in zebra finches. Horm Behav 58(3):526–532. https://doi.org/10.1016/j.yhbeh.2010.04.004
Ashton BJ, Ridley AR, Edwards EK, Thornton A (2018) Cognitive performance is linked to group size and affects fitness in Australian magpies. Nature 554:364–367. https://doi.org/10.1038/nature25503
Barber JR, Burdett CL, Reed SE, Warner KA, Formichella C, Crooks KR, Theobald DM, Fristrup KM (2011) Anthropogenic noise exposure in protected natural areas: estimating the scale of ecological consequences. Landsc Ecol 26(9):1281–1295. https://doi.org/10.1007/s10980-011-9646-7
Babisch W, Beule B, Schust M, Kersten N, Ising H (2005) Traffic noise and risk of myocardial infarction. Epidemiology 16(1):33–40. https://doi.org/10.1097/01.ede.0000147104.84424.24
Bauer GB, Mobley JR, Herman LM (1993) Responses of wintering humpback whales to vessel traffic. J Acoust Soc Am 94(5). https://doi.org/10.1121/1.407708
Bee MA, Swanson EM (2007) Auditory masking of anuran advertisement calls by road traffic noise. Anim Behav 74(6):1765–1776. https://doi.org/10.1016/j.anbehav.2007.03.019
Boogert NJ, Anderson RC, Peters S, Searcy WA, Nowicki S (2011) Song repertoire size in male song sparrows correlates with detour reaching, but not with other cognitive measures. Anim Behav 81(6):1735–1741. https://doi.org/10.1016/j.anbehav.2011.03.004
Boruszewska K, Witkowski A, Jaszczak K (2007) Selected growth and development traits of the zebra finch (Poephila guttata) nestlings in amateur breeding. Anim Sci Pap Rep 25(2):97–110
Bruintjes R, Radford AN (2013) Context-dependent impacts of anthropogenic noise on individual and social behaviour in a cooperatively breeding fish. Anim Behav 85(6):1343–1349. https://doi.org/10.1016/j.anbehav.2013.03.025
Chan AAY-H, Giraldo-Perez P, Smith S, Blumstein DT (2010) Anthropogenic noise affects risk assessment and attention: the distracted prey hypothesis. Biol Lett 6:458–461. https://doi.org/10.1098/rsbl.2009.1081
Chen J, Zou Y, Sun Y-H, ten Cate C (2019) Problem-solving males become more attractive to female budgerigars. Science 363(6423):166–167. https://doi.org/10.1126/science.aau8181
Connelly F, Hall ML, Johnsson RD, Elliot-Kerr S, Dow BR, Lesku JA, Mulder RA (2022) Urban noise does not affect cognitive performance in wild Australian magpies. Anim Behav 188:35–44. https://doi.org/10.1016/j.anbehav.2022.03.021
Coon JJ, Nelson SB, West AC, Bradley IA, Miller JR (2018) An observation of parental infanticide in Dickcissels (Spiza americana): video evidence and potential mechanisms. Wilson J Ornithol 130(1):341–345. https://doi.org/10.1676/1559-4491-130.1.341
Cyr NE, Romero LM (2007) Chronic stress in free-living European Starlings reduces corticosterone concentrations and reproductive success. Gen Comp Endocrinol 151(1):82–89. https://doi.org/10.1016/j.ygcen.2006.12.003
Davies S, Haddad N, Ouyang JQ (2017) Stressful city sounds: glucocorticoid responses to experimental traffic noise are environmentally dependent. Biol Lett 13(10):20170276. https://doi.org/10.1098/rsbl.2017.0276
Dorado-Correa AM, Zollinger SA, Heidinger B, Brumm H (2018) Timing matters: traffic noise accelerates telomere loss rate differently across developmental stages. Front Zoo 15:29. https://doi.org/10.1186/s12983-018-0275-8
DuBois AL, Nowicki S, Peters S, Rivera-Caceres KD, Searcy WA (2018) Song is not a reliable signal of general cognitive ability in a songbird. Anim Behav 137:205–213. https://doi.org/10.1016/j.anbehav.2018.01.020
Flores R, Penna M, Wingfield JC, Cuevas E, Vásquez RA, Quirici V (2019) Effects of traffic noise exposure on corticosterone, glutathione and tonic immobility in chicks of a precocial bird. Conserv Physiol 7(1):coz061. https://doi.org/10.1093/conphys/coz061
Gilby AJ, Mainwaring MC, Rollin LA, Griffith SC (2011) Parental care in wild and captive zebra finches: measuring food delivery to quantify parental effort. Anim Behav 81(1):289–295. https://doi.org/10.1016/j.anbehav.2010.10.020
Grabarczyk EE, Gill SA (2019) Anthropogenic noise masking diminishes house wren (Troglodytes aedon) song transmission in urban natural areas. Bioacoustics 20(5):518–532. https://doi.org/10.1080/09524622.2019.1621209
Grunst AS, Grunst ML, Pinxten R, Eens M (2019) Personality and plasticity in neophobia levels vary with anthropogenic disturbance but not toxic metal exposure in urban great tits: Urban disturbance, metal pollution and neophobia. Sci Total Environ 656:997–1009. https://doi.org/10.1016/j.scitotenv.2018.11.383
Halfwerk W, Holleman LJM, Lessells CM, Slabbekoorn H (2010) Negative impact of traffic noise on avian reproductive success. J Appl Ecol 48:210–219. https://doi.org/10.1111/j.1365-2664.2010.01914.x
Hall JM, Mitchell TS, Thawley CJ, Stroud JT, Warner DA (2020) Adaptive seasonal shift towards investment in fewer, larger offspring: evidence from field and laboratory studies. J Anim Ecol 89(5):1242–1253. https://doi.org/10.1111/1365-2656.13182
Johnson K, Rosetta D, Burley DN (1993) Preferences of female American goldfinches (Carduelis tristis) for natural and artificial male traits. Behav Ecol 4(2):138–143. https://doi.org/10.1093/beheco/4.2.138
Katsis A, Buchanan K, Kleindorfer S, Mariette M (2021) Long-term effects of prenatal sound experience on songbird behavior and their relation to song learning. Behav Ecol Sociobio 75. https://doi.org/10.1007/s00265-020-02939-5
Khan N, Peters RA, Robert K (2016) Compensating for a stressful start: maternal corticosterone, offspring survival, and size at fledging in the zebra finch Taeniopygia guttata. Emu 116(3):262–272. https://doi.org/10.1071/MU15095
Kleindorfer S, Hoi H, Evans C, Mahr K, Robertson J, Hauber ME, Colombelli-Négrel D (2014) The cost of teaching embryos in superb fairy-wrens. Behav Ecol 25(5):1131–1135. https://doi.org/10.1093/beheco/aru097
Lenth RV (2022) emmeans: estimated marginal means, aka least-squares means. R package version 1.7.3. https://CRAN.R-project.org/package=emmeans. Accessed 3 Aug 2022
Leonard ML, Horn AG (2008) Does ambient noise affect growth and begging call structure in nestling birds? Behav Ecol 19(3):502–507. https://doi.org/10.1093/beheco/arm161
Lercher P, Evans GW, Meis M (2003) Ambient noise and cognitive processes among primary schoolchildren. Environ Behav 35(6):725–735. https://doi.org/10.1177/0013916503256260
Love OP, Williams TD (2008) The adaptive value of stress-induced phenotypes: effects of maternally derived corticosterone on sex-biased investment, cost of reproduction, and maternal fitness. Am Nat 172(4):E135–E149. https://doi.org/10.1086/590959
MacLean EL, Hare BA, Nunn CL et al (2014) The evolution of self control. Proc Natl Acad Sci USA 11(20):E2140–E2148. https://doi.org/10.1073/pnas.1323533111
Maia R, Gruson H, Endler JA, White TE (2019) Pavo 2: new tools for the spectral and spatial analysis of colour in R. Methods Ecol Evol 10(7):1097–1107. https://doi.org/10.1111/2041-210X.13174
Mariette MM, Buchanan KL (2016) Prenatal acoustic communication programs offspring for high posthatching temperatures in a songbird. Science 353(6301):812–814. https://doi.org/10.1126/science.aaf7049
Matsui T, Stansfeld S, Haines M, Head J (2004) Children's cognition and aircraft noise exposure at home-the West London Schools Study. Noise Health 7(25):49–57
McGraw K, Lee K, Lewin A (2011) The effect of capture-and-handling stress on carotenoid-based beak coloration in zebra finches. J Comp Physiol 197(6):683–691. https://doi.org/10.1007/s00359-011-0631-z
Meillère A, Brischoux F, Ribout C, Angelier F (2015) Traffic noise exposure affects telomere length in nestling house sparrows. Biol Lett 11:20150559. https://doi.org/10.1098/rsbl.2015.0559
Merrill L, Naylor MF, Dalimonte M, McLaughlin S, Stewart TE, Grindstaff JL (2017) Early-life immune activation increases song complexity and alters phenotypic associations between sexual ornaments. Funct Ecol 31(12):2263–2273. https://doi.org/10.1111/1365-2435.12916
Miley WM, Blustein J, Kennedy K (1982) Prenatal stimulation and postnatal testosterone affects infanticide in female rats. Physiol Behav 28(4):627–629. https://doi.org/10.1016/0031-9384(82)90042-7
Morris-Drake A, Kern JM, Radford AN (2016) Cross-modal impacts of anthropogenic noise on information use. Curr Biol 26: R911–R912. https://doi.org/10.1016/j.cub.2016.08.064
Müllner A, Linsenmair KE, Wikelski M (2004) Exposure to ecotourism reduces survival and affects stress response in Hoatzin chicks (Opisthocomus hoazin). Biol Conserv 118(4):549–558. https://doi.org/10.1016/j.biocon.2003.10.003
Murphy TG, Rosenthal MF, Montgomerie R, Tarvin KA (2009) Female American goldfinches use carotenoid-based bill coloration to signal status. Behav Ecol 20(6):1348–1355. https://doi.org/10.1093/beheco/arp140
Osbrink A, Meatte MA, Tran A, Herranen KK, Meek L, Murakami-Smith M, Ito J, Bhadra S, Nunnenkamp S, Templeton CN (2021) Traffic noise inhibits cognitive performance in a songbird. Proc R Soc B 288:20202851. https://doi.org/10.1098/rspb.2020.2851
Pandit MM, Eapen J, Pineda-Sabillon G, Caulfield ME, Moreno A, Wilhelm J, Ruyle JE, Bridge ES, Proppe DS (2021) Anthropogenic noise alters parental behavior and nestling developmental patterns, but not fledging condition. Behav Ecol 32(4):747–755. https://doi.org/10.1093/beheco/arab015
Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York. https://doi.org/10.1007/b98882
Potvin DA, MacDougall-Shackleton SA (2015) Traffic noise affects embryo mortality and nestling growth rates in captive zebra finches. J Exp Zool A Ecol Integr Physiol 323(10):722–730. https://doi.org/10.1002/jez.1965
Raap T, Pinxten R, Casasole G, Dehnhard G, Eens M (2017) Ambient anthropogenic noise but not light is associated with the ecophysiology of free-living songbird nestlings. Sci Rep 7:2754. https://doi.org/10.1038/s41598-017-02940-5
Rosenthal MF, Murphy TG, Darling N, Tarvin KA (2012) Ornamental bill color rapidly signals changing condition. J Avian Biol 43(6):553–564. https://doi.org/10.1111/j.1600-048X.2012.05774.x
Salmón P, Nilsson JF, Nord A, Bensch S, Isaksson C (2016) Urban environment shortens telomere length in nestling great tits, Parus Major. Biol Lett 12:20160155 https://doi.org/10.1098/rsbl.2016.0155
Simons MJP, Verhulst S (2011) Zebra finch females prefer males with redder bills independent of song rate—a meta-analysis. Behav Ecol 22(4):755–762. https://doi.org/10.1093/beheco/arr043
Simpson SD, Purser J, Radford AN (2014) Anthropogenic noise compromises antipredator behaviour in European eels. Glob Chang Biol 21(2):586–593. https://doi.org/10.1111/gcb.12685
Simpson SD, Radford AN, Nedelec SL, Ferrari MCO, Chivers DP, McCormick MI, Meekan MG (2016) Anthropogenic noise increases fish mortality by predation. Nat Commun 7:10544. https://doi.org/10.1038/ncomms10544
Slevin MC, Houtz JC, Bradshaw DJ, Anderson RC (2020) Evidence supporting the microbiota–gut–brain axis in a songbird. Biol Lett 16(11):20200430. https://doi.org/10.1098/rsbl.2020.0430
Soha JA, Peters S, Anderson RC, Searcy WA, Nowicki S (2019) Performance on tests of cognitive ability is not repeatable across years in a songbird. Anim Behav 158:281–288. https://doi.org/10.1016/j.anbehav.2019.09.020
Stansfeld SA, Berglund B, Clark C, Lopez-Barrio I, Fischer P, Öhrström E, Haines MM, Head J, Hygge S, van Kamp I, Berry BF (2005) Aircraft and road traffic noise and children’s cognition and health: a cross-national study. Lancet 365(9475):1942–1949. https://doi.org/10.1016/S0140-6736(05)66660-3
Stansfeld S, Clark C (2015) Health effects of noise exposure in children. Curr Envir Health Rpt 2:171–178. https://doi.org/10.1007/s40572-015-0044-1
Swaddle JP, Page LC (2007) High levels of environmental noise erode pair preferences in zebra finches: implications for noise pollution. Anim Behav 74(3):363–368. https://doi.org/10.1016/j.anbehav.2007.01.004
Szendro P, Vincze G, Szasz A (2001) Pink noise behaviour of the bio-systems. Eur Biophys J 30:227–231. https://doi.org/10.1007/s002490100143
Van den Berg CP, Troscianko J, Endler JA, Marshall NJ, Cheney KL (2020) Quantitative colour pattern analysis (QCPA): a comprehensive framework for the analysis of colour patterns in nature. Methods Ecol Evol 11(2):316–332. https://doi.org/10.1111/2041-210X.13328
Voellmy IK, Purser J, Flynn D, Kennedy P, Simpson SD, Radforda AN (2014) Acoustic noise reduces foraging success in two sympatric fish species via different mechanisms. Anim Behav 89:191–198. https://doi.org/10.1016/j.anbehav.2013.12.029
Wright AJ, Aguilar de Soto N, Baldwin A, Bateson M, Beale C, Clark WC, Deak T, Edwards E, Fernandez A, Godinho AI, Hatch L, Kakuschke AK, Lusseau D, Martineau D, Romero LM, Weilgart LS, Wintle B, Notarbartolo di Sciara G, Martín A (2007) Anthropogenic noise as a stressor in animals: a multidisciplinary perspective. J Comp Psychol 20:250–273
Zollinger SA, Dorado-Correa A, Goymann W, Forstmeier W, Knief U, Bastidas-Urrutia AM, Brumm H (2019) Traffic noise exposure depresses plasma corticosterone and delays offspring growth in breeding zebra finches. Conserv Physiol 7:coz056. https://doi.org/10.1093/conphys/coz056
Schroeder J, Nakagawa S, Cleasby IR, Burke T (2012) Passerine Birds Breeding under Chronic Noise Experience Reduced Fitness. PLoS ONE 7(7):e39200. https://doi.org/10.1371/journal.pone.0039200
Boogert NJ, Giraldeau LA, Lefebvre L (2008) Song complexity correlates with learning ability in zebra finch males. Anim Behav 76(5):1735–1741 S0003347208003679. https://doi.org/10.1016/j.anbehav.2008.08.009
Acknowledgements
We wish to thank Mylene Mariette and two anonymous reviewers for their helpful comments, which strengthened our manuscript. We thank Isabella Dixon, Carson Ennis, Elisset Proveda, Leena Al-Hraki, and Kristen Palmer for their assistance with running cognition trials.
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The Florida Atlantic University Office of Undergraduate Research and Inquiry, FAU College of Science, and the FAU Department of Biological Sciences provided funding and logistical support.
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Daria, C., Slevin, M.C. & Anderson, R.C. Effects of anthropogenic noise on cognition, bill color, and growth in the zebra finch (Taeniopygia guttata). acta ethol (2022). https://doi.org/10.1007/s10211-022-00406-0
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DOI: https://doi.org/10.1007/s10211-022-00406-0
Keywords
- Urban noise
- Zebra finch
- Cognition
- Bill ornamentation