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Long-term effects of prenatal sound experience on songbird behavior and their relation to song learning

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Abstract

Across multiple taxa, prenatal exposure to rhythmic sound can promote neural development and alter postnatal behavior. In recent studies using zebra finches, stimulating embryos with parental “heat calls” affected their begging behavior as nestlings and song learning as adults. This song learning effect is potentially mediated by broader changes to offspring behavior that affect how they interact with potential song tutors; however, the long-term behavioral effects of prenatal sound are still poorly understood. In this study, therefore, we used captive wild-derived zebra finches to experimentally test (1) whether prenatal sound experience affected long-term behavioral traits and (2) whether these traits were correlated with song learning outcomes. Offspring that had experienced heat calls (treatment) or contact calls (control) in the egg were raised after hatching in a colony environment. We then used four assays to quantify different aspects of their adult behavior, including food neophobia, detour reaching, and exploration in a novel environment. Treatment offspring were less food neophobic (quicker to eat a novel food item), adding to increasing evidence that prenatal sound can affect long-term behavior. However, levels of food neophobia did not, in turn, predict song learning. Differences in offspring song learning may instead be explained by exploration behavior, as fast-exploring males produced more syllables from non-paternal tutors. While our findings do not support the hypothesis that behavior mediates the effects of prenatal sound on song learning, they nevertheless bring us closer to understanding the behavioral mechanisms through which prenatal sound might affect postnatal outcomes.

Significance statement

Sounds experienced inside the egg can influence an individual’s behavior after hatching. In the zebra finch, exposing embryos to a parental “heat call” altered their song learning later in life, but the mechanism driving this effect is unknown. In this study, we tested whether prenatal playback of heat calls affected a suite of adult behavioral traits and whether any of these traits were associated with song learning. Exposure to heat calls produced adult zebra finches that were less neophobic towards a novel food item, but this trait was not itself correlated with song learning. Overall, these findings highlight the importance of the prenatal sound environment for shaping future offspring behavior, which may in turn have unappreciated fitness consequences.

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All datasets generated or analyzed during this study are included in this published article and its supplementary information files.

References

  • Aleksandrov LI, Dmitrieva LP (1992) Development of auditory sensitivity of altricial birds: absolute thresholds of the generation of evoked potentials. Neurosci Behav Physiol 22:132–137

    Article  CAS  PubMed  Google Scholar 

  • Anderson DK, Rhees RW, Fleming DE (1985) Effects of prenatal stress on differentiation of the sexually dimorphic nucleus of the preoptic area (SDN-POA) of the rat brain. Brain Res 332:113–118

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Bech C, Midtgård U (1981) Brain temperature and the rete mirabile ophthalmicum in the Zebra finch (Poephila guttata). J Comp Physiol B 145:89–93

    Article  Google Scholar 

  • Bennett PM, Harvey PH (1985) Brain size, development and metabolism in birds and mammals. J Zool 207:491–509

    Article  Google Scholar 

  • Böhner J (1983) Song learning in the zebra finch (Taeniopygia guttata): selectivity in the choice of a tutor and accuracy of song copies. Anim Behav 31:231–237

    Article  Google Scholar 

  • Bókony V, Kulcsár A, Tóth Z, Liker A (2012) Personality traits and behavioral syndromes in differently urbanized populations of house sparrows (Passer domesticus). PLoS ONE 7:e36639

  • 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 81:1209–1216

    Article  Google Scholar 

  • Boogert NJ, Farine DR, Spencer KA (2014) Developmental stress predicts social network position. Biol Lett 10:20140561

    Article  PubMed  PubMed Central  Google Scholar 

  • Boogert NJ, Giraldeau L-A, Lefebvre L (2008) Song complexity correlates with learning ability in zebra finch males. Anim Behav 76:1735–1741

    Article  Google Scholar 

  • Boogert NJ, Lachlan RF, Spencer KA, Templeton CN, Farine DR (2018) Stress hormones, social associations and song learning in zebra finches. Philos Trans R Soc B 373:20170290

    Article  Google Scholar 

  • Boogert NJ, Reader SM, Laland KN (2006) The relation between social rank, neophobia and individual learning in starlings. Anim Behav 72:1229–1239

    Article  Google Scholar 

  • Both C, Dingemanse NJ, Drent PJ, Tinbergen JM (2005) Pairs of extreme avian personalities have highest reproductive success. J Anim Ecol 74:667–674

    Article  Google Scholar 

  • Boucaud ICA, Mariette MM, Villain AS, Vignal C (2016) Vocal negotiation over parental care? Acoustic communication at the nest predicts partners’ incubation share. Biol J Linn Soc 117:322–336

    Article  Google Scholar 

  • Cauchoix M, Chow PKY, van Horik JO, Atance CM, Barbeau EJ, Barragan-Jason G, Bize P, Boussard A, Buechel SD, Cabirol A, Cauchard L, Claidière N, Dalesman S, Devaud JM, Didic M, Doligez B, Fagot J, Fichtel C, Henke-von der Malsburg J, Hermer E, Huber L, Huebner F, Kappeler PM, Klein S, Langbein J, Langley EJG, Lea SEG, Lihoreau M, Lovlie H, Matzel LD, Nakagawa S, Nawroth C, Oesterwind S, Sauce B, Smith EA, Sorato E, Tebbich S, Wallis LJ, Whiteside MA, Wilkinson A, Chaine AS, Morand-Ferron J (2018) The repeatability of cognitive performance: a meta-analysis. Philos Trans R Soc B 373:20170281

    Article  Google Scholar 

  • Chaudhury S, Nag TC, Wadhwa S (2006) Prenatal acoustic stimulation influences neuronal size and the expression of calcium-binding proteins (calbindin D-28K and parvalbumin) in chick hippocampus. J Chem Neuroanat 32:117–126

    Article  CAS  PubMed  Google Scholar 

  • Clayton NS (1987) Song tutor choice in zebra finches. Anim Behav 35:714–721

    Article  Google Scholar 

  • Cohen MM, Jing D, Yang RR, Tottenham N, Lee FS, Casey BJ (2013) Early-life stress has persistent effects on amygdala function and development in mice and humans. P Nat Acad Sci USA 110:18274–18278

    Article  CAS  Google Scholar 

  • Coleman K, Wilson DS (1998) Shyness and boldness in pumpkinseed sunfish: individual differences are context-specific. Anim Behav 56:927–936

    Article  CAS  PubMed  Google Scholar 

  • Coleman SL, Mellgren RL (1994) Neophobia when feeding alone or in flocks in zebra finches, Taeniopygia guttata. Anim Behav 48:903–907

    Article  Google Scholar 

  • Colombelli-Négrel D, Hauber ME, Kleindorfer S (2014) Prenatal learning in an Australian songbird: habituation and individual discrimination in superb fairy-wren embryos. Proc R Soc B 281:20141154

  • Colombelli-Négrel D, Hauber ME, Robertson J, Sulloway FJ, Hoi H, Griggio M, Kleindorfer S (2012) Embryonic learning of vocal passwords in superb fairy-wrens reveals intruder cuckoo nestlings. Curr Biol 22:2155–2160

    Article  PubMed  Google Scholar 

  • Colombelli-Négrel D, Kleindorfer S (2017) Prenatal environment affects embryonic response to song. Biol Lett 13:20170302

    Article  PubMed  PubMed Central  Google Scholar 

  • Coomes CM, Danner RM, Derryberry EP (2019) Elevated temperatures reduce discrimination between conspecific and heterospecific sexual signals. Anim Behav 147:9–15

    Article  Google Scholar 

  • David M, Auclair Y, Cézilly F (2012) Assessing short-and long-term repeatability and stability of personality in captive zebra finches using longitudinal data. Ethology 118:932–942

    Article  Google Scholar 

  • Dingemanse NJ, Both C, Drent PJ, Tinbergen JM (2004) Fitness consequences of avian personalities in a fluctuating environment. Proc R Soc B 271:847–852

  • DuBois AL, Nowicki S, Peters S, Rivera-Cáceres KD, Searcy WA (2018) Song is not a reliable signal of general cognitive ability in a songbird. Anim Behav 137:205–213

    Article  Google Scholar 

  • Farrell TM, Morgan A, MacDougall-Shackleton SA (2016) Developmental stress impairs performance on an association task in male and female songbirds, but impairs auditory learning in females only. Anim Cogn 19:1–14

    Article  PubMed  Google Scholar 

  • Farrell TM, Weaver K, An Y-S, MacDougall-Shackleton SA (2012) Song bout length is indicative of spatial learning in European starlings. Behav Ecol 23:101–111

    Article  Google Scholar 

  • Gomes ACR, Guerra S, Silva PA, Marques CI, Trigo S, Boogert NJ, Cardoso GC (2020) Proactive common waxbills make fewer mistakes in a cognitive assay, the detour-reaching task. Behav Ecol Sociobiol 74:31

    Article  Google Scholar 

  • Greenberg R, Mettke-Hofmann C (2001) Ecological aspects of neophobia and neophilia in birds. In: Nolan V Jr, Thompson CF (eds) Current ornithology. Kluwer Academic/Plenum Publishers, New York, pp 119–178

    Google Scholar 

  • Guillette LM, Hahn AH, Hoeschele M, Przyslupski A-M, Sturdy CB (2015) Individual differences in learning speed, performance accuracy and exploratory behaviour in black-capped chickadees. Anim Cogn 18:165–178

    Article  PubMed  Google Scholar 

  • Hall ML, van Asten T, Katsis AC, Dingemanse NJ, Magrath MJL, Mulder RA (2015) Animal personality and pace-of-life syndromes: do fast-exploring fairy-wrens die young? Front Ecol Evol 3:28

    Article  Google Scholar 

  • Hauser MD (1999) Perseveration, inhibition and the prefrontal cortex: a new look. Curr Opin Neurobiol 9:214–222

    Article  CAS  PubMed  Google Scholar 

  • Herborn KA, Macleod R, Miles WTS, Schofield ANB, Alexander L, Arnold KE (2010) Personality in captivity reflects personality in the wild. Anim Behav 79:835–843

    Article  Google Scholar 

  • Jacqmin-Gadda H, Sibillot S, Proust C, Molina J-M, Thiébaut R (2007) Robustness of the linear mixed model to misspecified error distribution. Comput Stat Data Anal 51:5142–5154

    Article  Google Scholar 

  • Jones AE, Slater PJB (1996) The role of aggression in song tutor choice in the zebra finch: cause or effect? Behaviour 133:103–115

    Article  Google Scholar 

  • Katsis AC, Davies MH, Buchanan KL, Kleindorfer S, Hauber ME, Mariette MM (2018) Prenatal exposure to incubation calls affects song learning in the zebra finch. Sci Rep 8:15232

    Article  PubMed  PubMed Central  Google Scholar 

  • Katz M, Lachlan RF (2003) Social learning of food types in zebra finches (Taeniopygia guttata) is directed by demonstrator sex and feeding activity. Anim Cogn 6:11–16

    Article  CAS  PubMed  Google Scholar 

  • Keagy J, Savard J-F, Borgia G (2011) Complex relationship between multiple measures of cognitive ability and male mating success in satin bowerbirds, Ptilonorhynchus violaceus. Anim Behav 81:1063–1070

    Article  Google Scholar 

  • Kelly DJ, Marples NM (2004) The effects of novel odour and colour cues on food acceptance by the zebra finch, Taeniopygia guttata. Anim Behav 68:1049–1054

    Article  Google Scholar 

  • Kim H, Lee M-H, Chang H-K, Lee TH, Lee HH, Shin MC, Shin MS, Won R, Shin HS, Kim CJ (2006) Influence of prenatal noise and music on the spatial memory and neurogenesis in the hippocampus of developing rats. Brain Dev 28:109–114

    Article  PubMed  Google Scholar 

  • Krause ET, Naguib M (2011) Compensatory growth affects exploratory behaviour in zebra finches, Taeniopygia guttata. Anim Behav 81:1295–1300

    Article  Google Scholar 

  • MacKinlay RD, Shaw RC (2019) Male New Zealand robin (Petroica longipes) song repertoire size does not correlate with cognitive performance in the wild. Intelligence 74:25–33

    Article  Google Scholar 

  • Mainwaring MC, Beal JL, Hartley IR (2011) Zebra finches are bolder in an asocial, rather than social, context. Behav Process 87:171–175

    Article  Google Scholar 

  • Mann N, Slater P (1995) Song tutor choice by zebra finches in aviaries. Anim Behav 49:811–820

    Article  Google Scholar 

  • Mariette MM, Buchanan KL (2016) Prenatal acoustic communication programs offspring for high ambient temperatures in a songbird. Science 353:812–814

    Article  CAS  PubMed  Google Scholar 

  • Mariette MM, Buchanan KL (2019) Calling in the heat: the zebra finch incubation call depends on heat AND reproductive stage—a comment on McDiarmid et al. 2018. Behav Ecol 30:1–3

    Article  Google Scholar 

  • Mariette MM, Griffith SC (2013) Does coloniality improve foraging efficiency and nestling provisioning? A field experiment in the wild Zebra finch. Ecology 94:325–335

    Article  PubMed  Google Scholar 

  • Mariette MM, Griffith SC (2015) The adaptive significance of provisioning and foraging coordination between breeding partners. Am Nat 185:270–280

    Article  PubMed  Google Scholar 

  • Mariette MM, Pessato A, Buttemer WA, McKechnie AE, Udino E, Collins RN, Meillère A, Bennett ATD, Buchanan KL (2018) Parent-embryo acoustic communication: a specialised heat vocalisation allowing embryonic eavesdropping. Sci Rep 8:17721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marples NM, Quinlan M, Thomas RJ, Kelly DJ (2007) Deactivation of dietary wariness through experience of novel food. Behav Ecol 18:803–810

    Article  Google Scholar 

  • McCowan LS, Mariette MM, Griffith SC (2015) The size and composition of social groups in the wild zebra finch. Emu 115:191–198

    Article  Google Scholar 

  • Murton RK (1971) The significance of a specific search image in the feeding behaviour of the wood-pigeon. Behaviour 40:10–40

    Article  Google Scholar 

  • Mutzel A, Dingemanse NJ, Araya-Ajoy YG, Kempenaers B (2013) Parental provisioning behaviour plays a key role in linking personality with reproductive success. Proc R Soc B 280:20131019

  • Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956

    PubMed  Google Scholar 

  • Nowicki S, Searcy WA, Peters S (2002) Brain development, song learning and mate choice in birds: a review and experimental test of the “nutritional stress hypothesis”. J Comp Physiol A 188:1003–1014

    Article  CAS  Google Scholar 

  • Partanen E, Kujala T, Näätänen R, Liitola A, Sambeth A, Huotilainen M (2013) Learning-induced neural plasticity of speech processing before birth. P Nat Acad Sci USA 110:15145–15150

  • Patrick SC, Weimerskirch H (2014) Personality, foraging and fitness consequences in a long lived seabird. PLoS ONE 9:e87269

  • Pessato A, McKechnie AE, Buchanan KL, Mariette MM (2020) Vocal panting: a novel thermoregulatory mechanism for enhancing heat tolerance in a desert-adapted bird. Sci Rep 10:18914

    Article  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.org

  • Roper A, Zann R (2006) The onset of song learning and song tutor selection in fledgling zebra finches. Ethology 112:458–470

    Article  Google Scholar 

  • Rowe C, Healy SD (2014) Measuring variation in cognition. Behav Ecol 25:1287–1292

    Article  Google Scholar 

  • Santos CD, Cramer JF, Pârâu LG, Miranda AC, Wikelski M, Dechmann DKN (2015) Personality and morphological traits affect pigeon survival from raptor attacks. Sci Rep 5:15490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanyal T, Kumar V, Nag TC, Jain S, Sreenivas V, Wadhwa S (2013a) Prenatal loud music and noise: differential impact on physiological arousal, hippocampal synaptogenesis and spatial behavior in one day-old chicks. PLoS ONE 8:e67347

  • Sanyal T, Palanisamy P, Nag TC, Roy TS, Wadhwa S (2013b) Effect of prenatal loud music and noise on total number of neurons and glia, neuronal nuclear area and volume of chick brainstem auditory nuclei, field L and hippocampus: a stereological investigation. Int J Dev Neurosci 31:234–244

    Article  PubMed  Google Scholar 

  • Schuett W, Dall SRX (2009) Sex differences, social context and personality in zebra finches, Taeniopygia guttata. Anim Behav 77:1041–1050

    Article  Google Scholar 

  • Searcy WA, Nowicki S (2019) Birdsong learning, avian cognition and the evolution of language. Anim Behav 151:217–227

    Article  Google Scholar 

  • Sewall KB, Soha JA, Peters S, Nowicki S (2013) Potential trade-off between vocal ornamentation and spatial ability in a songbird. Biol Lett 9:20130344

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Spencer K, Buchanan K, Goldsmith A, Catchpole C (2003) Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Horm Behav 44:132–139

    Article  CAS  PubMed  Google Scholar 

  • Starck JM, Ricklefs RE (1998) Patterns of development: the altricial-precocial spectrum. In: Starck JM, Ricklefs RE (eds) Avian growth and development: evolution within the altricial-precocial spectrum. Oxford University Press, New York, pp 3–30

    Google Scholar 

  • Stoffel MA, Nakagawa S, Schielzeth H (2017) rptR: repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol Evol 8:1639–1644

    Article  Google Scholar 

  • Tebbich S, Stankewitz S, Teschke I (2012) The relationship between foraging, learning abilities and neophobia in two species of Darwin’s finches. Ethology 118:135–146

    Article  Google Scholar 

  • Templeton CN, Laland KN, Boogert NJ (2014) Does song complexity correlate with problem-solving performance in flocks of zebra finches? Anim Behav 92:63–71

    Article  Google Scholar 

  • Titulaer M, van Oers K, Naguib M (2012) Personality affects learning performance in difficult tasks in a sex-dependent way. Anim Behav 83:723–730

  • van Horik JO, Langley EJG, Whiteside MA, Madden JR (2017) Differential participation in cognitive tests is driven by personality, sex, body condition and experience. Behav Process 134:22–30

    Article  Google Scholar 

  • van Horik JO, Madden JR (2016) A problem with problem solving: motivational traits, but not cognition, predict success on novel operant foraging tasks. Anim Behav 114:189–198

    Article  PubMed  PubMed Central  Google Scholar 

  • Verbeek MEM, Drent PJ, Wiepkema PR (1994) Consistent individual differences in early exploratory behaviour of male great tits. Anim Behav 48:1113–1121

    Article  Google Scholar 

  • Webb AR, Heller HT, Benson CB, Lahav A (2015) Mother’s voice and heartbeat sounds elicit auditory plasticity in the human brain before full gestation. P Nat Acad Sci USA 112:3152–3157

    Article  CAS  Google Scholar 

  • Williams H (1990) Models for song learning in the zebra finch: fathers or others? Anim Behav 39:745–757

    Article  Google Scholar 

  • Xu J, Yu L, Cai R, Zhang J, Sun X (2009) Early auditory enrichment with music enhances auditory discrimination learning and alters NR2B protein expression in rat auditory cortex. Behav Brain Res 196:49–54

    Article  PubMed  Google Scholar 

  • Zann R (1996) The zebra finch: a synthesis of field and laboratory studies. Oxford University Press, New York

    Google Scholar 

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Acknowledgments

We thank Mzuri Davies for her work collecting and analyzing zebra finch song and Rodney Collins, Bruce Newell, and Deakin University animal care staff for husbandry and logistical support. Multiple anonymous reviewers provided insightful feedback that greatly improved this manuscript.

Funding

This work was supported by the Holsworth Wildlife Research Endowment (Equity Trustees Charitable Foundation & Ecological Society of Australia to ACK) and the Australian Research Council (grant numbers FT140100131 to KLB; DE170100824 to MMM; DP180101207 to KLB and MMM).

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Correspondence to Andrew C. Katsis.

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All housing and experimental procedures were approved by the Animal Ethics Committee of Deakin University (G29-2013) and conformed with Australian legal requirements. All applicable international, national, and/or institutional guidelines for the use of animals were followed.

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Katsis, A.C., Buchanan, K.L., Kleindorfer, S. et al. Long-term effects of prenatal sound experience on songbird behavior and their relation to song learning. Behav Ecol Sociobiol 75, 18 (2021). https://doi.org/10.1007/s00265-020-02939-5

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