Skip to main content

Advertisement

Log in

Developmental stress impairs performance on an association task in male and female songbirds, but impairs auditory learning in females only

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

In songbirds, early-life environments critically shape song development. Many studies have demonstrated that developmental stress impairs song learning and the development of song-control regions of the brain in males. However, song has evolved through signaller–receiver networks and the effect stress has on the ability to receive auditory signals is equally important, especially for females who use song as an indicator of mate quality. Female song preferences have been the metric used to evaluate how developmental stress affects auditory learning, but preferences are shaped by many non-cognitive factors and preclude the evaluation of auditory learning abilities in males. To determine whether developmental stress specifically affects auditory learning in both sexes, we subjected juvenile European starlings, Sturnus vulgaris, to either an ad libitum or an unpredictable food supply treatment from 35 to 115 days of age. In adulthood, we assessed learning of both auditory and visual discrimination tasks. Females reared in the experimental group were slower than females in the control group to acquire a relative frequency auditory task, and slower than their male counterparts to acquire an absolute frequency auditory task. There was no difference in auditory performance between treatment groups for males. However, on the colour association task, birds from the experimental group committed more errors per trial than control birds. There was no correlation in performance across the cognitive tasks. Developmental stress did not affect all cognitive processes equally across the sexes. Our results suggest that the male auditory system may be more robust to developmental stress than that of females.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Amy M, van Oers K, Naguib M (2012) Worms under cover: relationships between performance in learning tasks and personality in great tits (Parus major). Anim Cogn 15:763–770. doi:10.1007/s10071-012-0500-3

    Article  PubMed  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. doi:10.1016/j.anbehav.2008.08.009

    Article  Google Scholar 

  • Boogert NJ, Anderson RC, Peters S et al (2011) Song repertoire size in male song sparrows correlates with detour reaching, but not with other cognitive measures. Anim Behav 81:1209–1216. doi:10.1016/j.anbehav.2011.03.004

    Article  Google Scholar 

  • Brenowitz EA, Beecher MD (2005) Song learning in birds: diversity and plasticity, opportunities and challenges. Trends Neurosci 28:127–132. doi:10.1016/j.tins.2005.01.004

    Article  PubMed  CAS  Google Scholar 

  • Buchanan KL, Spencer K, Goldsmith AR, Catchpole CK (2003) Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris). Proc Biol Sci 270:1149–1156. doi:10.1098/rspb.2003.2330

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Buchanan KL, Grindstaff JL, Pravosudov VV (2013) Condition dependence, developmental plasticity, and cognition: implications for ecology and evolution. Trends Ecol Evol 28:290–296. doi:10.1016/j.tree.2013.02.004

    Article  PubMed  PubMed Central  Google Scholar 

  • Catchpole CK (1996) Song and female choice: good genes and big brains? Trends Ecol Evol 11:358–360. doi:10.1016/0169-5347(96)30042-6

    Article  PubMed  CAS  Google Scholar 

  • Catchpole CK, Slater PJB (2008) Bird song: biological themes and variations, 2nd edn. Cambridge University Press, New York

    Book  Google Scholar 

  • Chaiken M, Böhner J (2007) Song learning after isolation in the open-ended learner the European starling: dissociation of imitation and syntactic development. Condor 109:968–976

    Article  Google Scholar 

  • Chaiken M, Bohner J, Marler P (1994) Repertoire turnover and the timing of song acquisition in European starlings. Behaviour 128:25–39

    Article  Google Scholar 

  • Coppens CM, de Boer SF, Koolhaas JM (2010) Coping styles and behavioural flexibility: towards underlying mechanisms. Philos Trans R Soc Lond B Biol Sci 365:4021–4028. doi:10.1098/rstb.2010.0217

    Article  PubMed  PubMed Central  Google Scholar 

  • Cotton S, Small J, Pomiankowski A (2006) Sexual selection and condition-dependent mate preferences. Curr Biol 16:R755–R765. doi:10.1016/j.cub.2006.08.022

    Article  PubMed  CAS  Google Scholar 

  • DeVoogd TJ (2004) Neural constraints on the complexity of avian song. Brain Behav Evol 63:221–232. doi:10.1159/000076783

    Article  PubMed  Google Scholar 

  • Eens M, Pinxten R, Verheyen RF (1992) No overlap in song repertoire size between yearling and older starlings Sturnus vulgaris. Ibis (Lond 1859) 134:72–76. doi: 10.1111/j.1474-919X.1992.tb07233.x

  • Farrell TM, Morgan A, Sarqui-Adamson Y, MacDougall-Shackleton SA (in review) Effects of early-developmental stress on growth rates, body composition and developmental plasticity of the HPG-axis. Gen Comp Endo

  • Farrell TM, Weaver K, An Y-S, MacDougall-Shackleton SA (2011) Song bout length is indicative of spatial learning in European starlings. Behav Ecol 23:101–111. doi:10.1093/beheco/arr162

    Article  Google Scholar 

  • Farrell T, Kriengwatana B, MacDougall-Shackleton SA (2015a) Developmental stress and correlated cognitive traits in songbirds. Comp Cogn Behav Rev 10:1–23. doi:10.3819/ccbr.2015.100001

    Article  Google Scholar 

  • Farrell TM, Neuert MAC, Cui A, MacDougall-Shackleton SA (2015b) Developmental stress impairs a female songbird’s behavioural and neural response to a sexually selected signal. Anim Behav 102:157–167. doi:10.1016/j.anbehav.2015.01.018

    Article  Google Scholar 

  • Feare C (1984) The starling. Oxford University Press, Oxford

    Google Scholar 

  • Fisher MO, Nager RG, Monaghan P (2006) Compensatory growth impairs adult cognitive performance. PLoS Biol 4:e251. doi:10.1371/journal.pbio.0040251

    Article  PubMed  PubMed Central  Google Scholar 

  • Flux JEC, Flux MM (1982) Artificial selection and gene flow in wild starlings, Sturnus vulgaris. Naturwissenschaften 69:96–97. doi:10.1007/BF00441236

    Article  Google Scholar 

  • Gall MD, Lucas JR (2010) Sex differences in auditory filters of brown-headed cowbirds (Molothrus ater). J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196:559–567. doi:10.1007/s00359-010-0543-3

    Article  PubMed  Google Scholar 

  • Gall MD, Brierley LE, Lucas JR (2011) Species and sex effects on auditory processing in brown-headed cowbirds and red-winged blackbirds. Anim Behav 81:973–982. doi:10.1016/j.anbehav.2011.01.032

    Article  Google Scholar 

  • Gentner TQ, Hulse S (2000) Female European starling preference and choice for variation in conspecific male song. Anim Behav 59:443–458. doi:10.1006/anbe.1999.1313

    Article  PubMed  Google Scholar 

  • Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075. doi:10.1046/j.1365-294x.1998.00389.x

    Article  PubMed  CAS  Google Scholar 

  • Guglielmo CG, McGuire LP, Gerson AR, Seewagen CL (2011) Simple, rapid, and non-invasive measurement of fat, lean, and total water masses of live birds using quantitative magnetic resonance. J Ornithol 152:75–85. doi:10.1007/s10336-011-0724-z

    Article  Google Scholar 

  • Hasselquist D, Bensch S, von Schantz T (1996) Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler. Nature 381:229–232. doi:10.1038/381229a0

    Article  CAS  Google Scholar 

  • Hausberger M, Black JM (1991) Female song in European starlings: the case of noncompetitive song-matching. Ethol Ecol Evol 3:337–344

    Article  Google Scholar 

  • Hausberger M, Henry L, Lepage L, Schmidt I (1995a) Song sharing reflects the social organization in a captive group of european starlings (Sturnus vulgaris). J Comp Psychol 109:222–241

    Article  Google Scholar 

  • Hausberger M, Henry L, Richard MA (1995b) Testosterone-induced singing in female European starlings (Sturnus vulgaris). Ethology 99:193–208. doi:10.1111/j.1439-0310.1995.tb00894.x

    Article  Google Scholar 

  • Hulse SH, Page SC, Braaten RF (1990) Frequency range size and the frequency range constraint in auditory perception by European starlings (Sturnus vulgaris). Anim Learn Behav 18:238–245

    Article  Google Scholar 

  • Isden J, Panayi C, Dingle C, Madden J (2013) Performance in cognitive and problem-solving tasks in male spotted bowerbirds does not correlate with mating success. Anim Behav 86:829–838. doi:10.1016/j.anbehav.2013.07.024

    Article  Google Scholar 

  • Keagy J, Savard J-F, Borgia G (2011a) Cognitive ability and the evolution of multiple behavioral display traits. Behav Ecol 23:448–456. doi:10.1093/beheco/arr211

    Article  Google Scholar 

  • Keagy J, Savard J-F, Borgia G (2011b) Complex relationship between multiple measures of cognitive ability and male mating success in satin bowerbirds, Ptilonorhynchus violaceus. Anim Behav 81:1063–1070. doi:10.1016/j.anbehav.2011.02.018

    Article  Google Scholar 

  • Kessel B (1957) A study of the breeding biology of the European starling (Sturnus vulgaris L.) in North America. Am Midl Nat 58:257–331

    Article  Google Scholar 

  • Kriengwatana B, Farrell TM, Aitken SDT et al (2015) Early-life nutritional stress affects associative learning and spatial memory but not performance on a novel object test. Behaviour. doi:10.1163/1568539X-00003239

    Google Scholar 

  • Lee TTY, Charrier I, Bloomfield LL et al (2006) Frequency-range discriminations and absolute pitch in black-capped chickadees (Poecile atricapillus), mountain chickadees (Poecile gambeli), and zebra finches (Taeniopygia guttata). J Comp Psychol 120:217–228. doi:10.1037/0735-7036.120.3.217

    Article  PubMed  Google Scholar 

  • Leitner S, Catchpole CK (2007) Song and brain development in canaries raised under different conditions of acoustic and social isolation over 2 years. Dev Neurobiol 67:1478–1487. doi:10.1002/dneu.20521

    Article  PubMed  Google Scholar 

  • Lynch KS, Kleitz-Nelson HK, Ball GF (2013) HVC lesions modify immediate early gene expression in auditory forebrain regions of female songbirds. Dev Neurobiol 73:315–323. doi:10.1002/dneu.22062

    Article  PubMed  CAS  Google Scholar 

  • Macdougall-Shackleton SA, Hulse SH (1996) Concurrent absolute and relative pitch processing by European starlings (Sturnus vulgaris). J Comp Psychol 110:139–146

    Article  Google Scholar 

  • MacDougall-Shackleton SA, Spencer K (2012) Developmental stress and birdsong: current evidence and future directions. J Ornithol 153:105–117. doi:10.1007/s10336-011-0807-x

    Article  Google Scholar 

  • MacDougall-Shackleton SA, Hulse SH, Gentner TQ, White W (1998) Auditory scene analysis by European starlings (Sturnus vulgaris): perceptual segregation of tone sequences. J Acoust Soc Am 103:3581–3587

    Article  PubMed  CAS  Google Scholar 

  • Mayr E (1939) The sex ratio in wild birds. Am Nat 73:156–179

    Article  Google Scholar 

  • Nelson DA (1989) Song frequency as a cue for recognition of species and individuals in the field sparrow (Spizella pusilla). J Comp Psychol 103:171–176. doi:10.1037/0735-7036.103.2.171

    Article  PubMed  CAS  Google Scholar 

  • Njegovan M, Weisman RG (1997) Pitch discrimination in field- and isolation-reared black-capped chickadees (Parus atricapillus). J Comp Psychol 111:294–301

    Article  Google Scholar 

  • Nowicki S, Searcy WA (2005) Song and mate choice in birds: how the development of behavior helps us to understand function. Auk 1:1–14

    Article  Google Scholar 

  • Nowicki S, Searcy WA (2011) Are better singers smarter? Behav Ecol 22:10–11. doi:10.1093/beheco/arq081

    Article  Google Scholar 

  • Nowicki S, Peters S, Podos J (1998) Song learning, early nutrition and sexual selection in songbirds. Integr Comp Biol 38:179–190. doi:10.1093/icb/38.1.179

    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. doi:10.1007/s00359-002-0361-3

    Article  CAS  Google Scholar 

  • Poirier C, Henry L, Mathelier M et al (2004) Direct social contacts override auditory information in the song-learning process in starlings (Sturnus vulgaris). J Comp Psychol 118:179–193. doi:10.1037/0735-7036.118.2.179

    Article  PubMed  Google Scholar 

  • Reid JM, Arcese P, Cassidy ALEV et al (2005) Fitness correlates of song repertoire size in free-living song sparrows (Melospiza melodia). Am Nat 165:299–310. doi:10.1086/428299

    Article  PubMed  Google Scholar 

  • Riebel K, Smallegange IM, Terpstra NJ, Bolhuis JJ (2002) Sexual equality in zebra finch song preference: evidence for a dissociation between song recognition and production learning. Proc Biol Sci 269:729–733. doi:10.1098/rspb.2001.1930

    Article  PubMed  PubMed Central  Google Scholar 

  • Sandell MI, Smith HG (1997) Female aggression in the European starling during the breeding season. Anim Behav 53:13–23

    Article  Google Scholar 

  • Schew WA, Ricklefs RE (1998) Developmental plasticity. In: Starck JM, Ricklefs RE (eds) Avian growth and development: evolution within the altricial-precocial spectrum. Oxford University Press, Oxford, pp 288–304

    Google Scholar 

  • Schmidt KL, McCallum ES, MacDougall-Shackleton EA, MacDougall-Shackleton SA (2013a) Early-life stress affects the behavioural and neural response of female song sparrows to conspecific song. Anim Behav 85:825–837. doi:10.1016/j.anbehav.2013.01.029

    Article  Google Scholar 

  • Schmidt KL, Moore SD, MacDougall-Shackleton EA, MacDougall-Shackleton SA (2013b) Early-life stress affects song complexity, song learning and volume of the brain nucleus RA in adult male song sparrows. Anim Behav 86:25–35. doi:10.1016/j.anbehav.2013.03.036

    Article  Google Scholar 

  • Searcy WA, Nowicki S (2005) The evolution of animal communication: reliability and deception in signaling systems. Princeton University Press, Princeton

    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. doi:10.1098/rsbl.2013.0344

    PubMed  PubMed Central  Google Scholar 

  • Spencer K, MacDougall-Shackleton SA (2011) Indicators of development as sexually selected traits: the developmental stress hypothesis in context. Behav Ecol 22:1–9. doi:10.1093/beheco/arq068

    Article  Google Scholar 

  • Sturdy CB, Phillmore LS, Sartor JJ, Weisman RG (2001) Reduced social contact causes auditory perceptual deficits in zebra finches, Taeniopygia guttata. Anim Behav 62:1207–1218. doi:10.1006/anbe.2001.1864

    Article  Google Scholar 

  • Weary DM, Lemon RE, Date EM (1986) Acoustic features used in song discrimination by the veery. Ethology 72:199–213. doi:10.1111/j.1439-0310.1986.tb00621.x

    Article  Google Scholar 

  • Weisman RG, Njegovan M, Ito S (1994) Frequency ratio discrimination by zebra finches (Taeniopygia guttata) and Humans (Homo sapiens). J Comp Psychol 108:363–372. doi:10.1037/0735-7036.108.4.363

    Article  Google Scholar 

  • Weisman RG, Njegovan M, Sturdy C et al (1998) Frequency-range discriminations: special and general abilities in zebra finches (Taeniopygia guttata) and humans (Homo sapiens). J Comp Psychol 112:244–258

    Article  PubMed  CAS  Google Scholar 

  • West BT, Welch KB, Galecki AT (2007) Linear mixed models: an overview. Linear mixed models: a pratical guide using statistical software. Taylor and Francis Group, Boca Raton, pp 9–50

  • Wingfield JC, Maney DL, Breuner CW et al (1998) Ecological bases of hormone—behavior interactions: the “Emergency Life History Stage”. Integr Comp Biol 38:191–206. doi:10.1093/icb/38.1.191

    CAS  Google Scholar 

  • Woodgate JL, Bennett ATD, Leitner S et al (2010) Developmental stress and female mate choice behaviour in the zebra finch. Anim Behav 79:1381–1390. doi:10.1016/j.anbehav.2010.03.018

    Article  Google Scholar 

  • Woodgate JL, Leitner S, Catchpole CK et al (2011) Developmental stressors that impair song learning in males do not appear to affect female preferences for song complexity in the zebra finch. Behav Ecol 22:566–573. doi:10.1093/beheco/arr006

    Article  Google Scholar 

  • Woodgate JL, Buchanan KL, Bennett ATD et al (2014) Environmental and genetic control of brain and song structure in the zebra finch. Evol Int J Org Evol Org Evol 68:230–240. doi:10.1111/evo.12261

    Article  Google Scholar 

  • Woolley SMN, Moore JM (2011) Coevolution in communication senders and receivers: vocal behavior and auditory processing in multiple songbird species. Ann N Y Acad Sci 1225:155–165. doi:10.1111/j.1749-6632.2011.05989.x

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tara M. Farrell.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 82 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Farrell, T.M., Morgan, A. & MacDougall-Shackleton, S.A. 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 (2016). https://doi.org/10.1007/s10071-015-0908-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-015-0908-7

Keywords

Navigation