Delayed maturation of multiple signals in a migratory songbird

Abstract

Many animals use multiple signals in sexual communication, but our understanding of the interactions between multiple signals, particularly in inexperienced breeders, is limited. In birds, delayed plumage maturation (DPM) is well documented; young birds appear duller than adults, despite reaching sexual maturity. Age-related changes in song structure are also common in songbirds, though the extent to which songs of yearling males differ from those of adults (delayed song maturation, DSM) and its prevalence in species with DPM is unknown. We tested for DSM in the mate-attraction (repeat) song of a species with dramatic DPM, the American redstart (Setophaga ruticilla). Repeat song structure of territorial yearling and adult males differed significantly, based on discriminant analysis of nine non-collinear song features. Combined with previous evidence of delayed maturation in territorial (serial) song, we provide the first evidence for DSM in different song types used in different behavioral contexts during the breeding season of a migratory songbird. Within adults, variation in repeat song was associated with pairing, earlier onset of breeding, and number of offspring sired, suggesting a potential benefit for expressing more adult-like song. We found no relationship between the expression of adult-like repeat song and plumage in either age class. These results indicate that delayed maturation of repeat song in yearling redstarts is not due to a generalized delay in signal development, and suggest further work is needed to determine whether mate attraction (for both yearling and adult males) provides greater pressure to sound more “adult-like” than to look more “adult-like”.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  2. Badyaev AV, Hill GE, Weckworth BV (2002) Species divergence in sexually selected traits: increase in song elaboration is related to decrease in plumage ornamentation in finches. Evolution 56:412–419

    PubMed  Google Scholar 

  3. Burt J (2005) Syrinx, version 2.6. University of Washington, Seattle. Available at http://www.syrinxpc.com

  4. Cucco M, Malacarne G (1999) Is the song of black redstart males an honest signal of status? Condor 101:689–694

    Article  Google Scholar 

  5. Cucco M, Malacarne G (2000) Delayed maturation in passerine birds: an examination of plumage effects and some indications of a related effect in song. Ethol Ecol Evol 12:291–308

    Article  Google Scholar 

  6. Dawson RJG, Gibbs HL, Hobson KA, Yezerinac SM (1997) Isolation of microsatellite DNA markers from a passerine bird, Dendroica petechia (the yellow warbler), and their use in population studies. Heredity 79:506–514

    PubMed  Article  CAS  Google Scholar 

  7. de Repentigny Y, Ouellet H, McNeil R (2000) Song versus plumage in some North American oscines: testing Darwin's hypothesis. Ecoscience 7:137–148

    Google Scholar 

  8. Dunn PO (2004) Breeding dates and reproductive performance. In: Møller AP, Fiedler W, Berthold P (eds) Birds and climate change. Advances in ecological research, vol. 35. Academic, London, pp 69–87

    Google Scholar 

  9. Ficken MS (1962) Agonistic behavior and territory in the American redstart. Auk 79:607–632

    Google Scholar 

  10. Ficken MS, Ficken RW (1965) Comparative ethology of the chestnut-sided warbler, yellow warbler, and American redstart. Wilson Bull 77:363–375

    Google Scholar 

  11. Ficken MS, Ficken RW (1967) Age-specific differences in breeding behavior and ecology of American redstart. Wilson Bull 79:188–199

    Google Scholar 

  12. Foote JR, Fitzsimmons LP, Mennill DJ, Ratcliffe LM (2008) Male chickadees match neighbors interactively at dawn: support for the social dynamics hypothesis. Behav Ecol 19:1192–1199

    Article  Google Scholar 

  13. Foster MS (1987) Delayed maturation, neoteny, and social system differences in two manakins of the genus Chiroxiphia. Evolution 41:547–558

    Article  Google Scholar 

  14. Germain RR, Marra PP, Kyser TK, Ratcliffe LM (2010a) Adult-like plumage coloration predicts winter territory quality and timing of arrival on the breeding grounds of yearling male American redstarts. Condor 112:676–682

    Article  Google Scholar 

  15. Germain RR, Reudink MW, Marra PP, Ratcliffe LM (2010b) Carotenoid-based male plumage predicts parental investment in the American redstart. Wilson J Ornithol 122:318–325

    Article  Google Scholar 

  16. Greene E, Lyon BE, Muehter VR, Ratcliffe L, Oliver SJ, Boag PT (2000) Disruptive sexual selection for plumage coloration in a passerine bird. Nature 407:1000–1003

    PubMed  Article  CAS  Google Scholar 

  17. 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

    Article  CAS  Google Scholar 

  18. Hebets EA, Papaj DR (2005) Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 57:197–214

    Article  Google Scholar 

  19. Herring G, Gawlik DE, Beerens JM (2008) Sex determination for the great egret and white ibis. Waterbirds 31:298–303

    Article  Google Scholar 

  20. SAS Institute (2009) JMP version 8.0.1. Duxbury, Pacific Grove

  21. Iwasa Y, Pomiankowski A (1994) The evolution of mate preferences for multiple sexual ornaments. Evolution 48:853–867

    Article  Google Scholar 

  22. Karubian J (2002) Costs and benefits of variable breeding plumage in red-backed fairy-wren. Evolution 56:1673–1682

    PubMed  Google Scholar 

  23. Karubian J, Sillett TS, Webster MS (2008) The effects of delayed plumage maturation on aggression and survival in male red-backed fairy-wrens. Behav Ecol 19:508–516

    Article  Google Scholar 

  24. Kiefer S, Spiess A, Kipper S, Mundry R, Sommer C, Hultsch H, Todt D (2006) First-year common nightingales (Luscinia megarhynchos) have smaller song-type repertoire sizes than older males. Ethology 112:1217–1224

    Article  Google Scholar 

  25. Kiefer S, Sommer C, Scharff C, Kipper S, Mundry R (2009) Tuning towards tomorrow? Common nightingales Luscinia megarhynchos change and increase their song repertoires from the first to the second breeding season. J Avian Biol 40:231–236

    Article  Google Scholar 

  26. Kipper S, Kiefer S (2010) Age-related changes in birds' singing styles: on fresh tunes and fading voices? Adv Study Behav 41:77–118

    Article  Google Scholar 

  27. Kroodsma DE (1981) Variation and functions of song types in warblers (Parulidae). Auk 98:743–751

    Google Scholar 

  28. Kroodsma DE, Bereson RC, Byers BE, Minear E (1989) Use of song types by the chestnut-sided warbler: evidence for both intra- and inter-sexual functions. Can J Zool 67:447–456

    Article  Google Scholar 

  29. Lemon RE, Cotter R, MacNally RC, Monette S (1985) Song repertoires and song sharing by American redstarts. Condor 87:457–470

    Article  Google Scholar 

  30. Lemon RE, Monette S, Roff D (1987) Song repertoires of American warblers (Parulinae): honest advertising or assessment? Ethology 74:265–284

    Article  Google Scholar 

  31. Lemon RE, Weary DM, Norris KJ (1992) Male morphology and behavior correlate with reproductive success in the American redstart (Setophaga ruticilla). Behav Ecol Sociobiol 29:399–403

    Article  Google Scholar 

  32. Lemon RE, Perreault S, Weary DM (1994) Dual strategies of song development in American redstarts, Setophaga ruticilla. Anim Behav 47:317–329

    Article  Google Scholar 

  33. Lozano GA, Perreault S, Lemon RE (1996) Age, arrival date and reproductive success of male American redstarts Setophaga ruticilla. J Avian Biol 27:164–170

    Article  Google Scholar 

  34. Lyon BE, Montgomerie RD (1986) Delayed plumage maturation in passerine birds: reliable signaling by subordinate males. Evolution 40:605–615

    Article  Google Scholar 

  35. Martín J, Forsman A (1999) Social costs and development of nuptial coloration in male Psammodromus algirus lizards: an experiment. Behav Ecol 10:396–400

    Article  Google Scholar 

  36. McGarigal K, Cushman S, Stafford S (2000) Multivariate statistics for wildlife and ecology research. Springer, New York

    Book  Google Scholar 

  37. McGraw KJ, Hudon J, Hill GE, Parker RS (2005) A simple and inexpensive chemical test for behavioral ecologists to determine the presence of carotenoid pigments in animal tissues. Behav Ecol Sociobiol 57:391–397

    Article  Google Scholar 

  38. Møller AP, Pomiankowski A (1993) Why have birds got multiple sexual ornaments? Behav Ecol Sociobiol 32:167–176

    Google Scholar 

  39. Møller AP, Saino N, Taramino G, Galeotti P, Ferrario S (1998) Paternity and multiple signaling: effects of a secondary sexual character and song on paternity in the barn swallow. Am Nat 151:236–242

    PubMed  Article  Google Scholar 

  40. Montgomerie R (2006) Analyzing colors. In: Hill GE, McGraw KJ (eds) Bird coloration, vol 1, Mechanisms and measurements. Harvard University Press, Cambridge, pp 90–147

    Google Scholar 

  41. Montgomerie R (2008) CLR, version 1.03. Queen's University, Kingston. Available at http://post.queensu.ca/~mont/color/

  42. Muehter VR, Greene E, Ratcliffe L (1997) Delayed plumage maturation in lazuli buntings: tests of the female mimicry and status signalling hypotheses. Behav Ecol Sociobiol 41:281–290

    Article  Google Scholar 

  43. Noon BR (1981) The distribution of an avian guild along a temperate elevational gradient: the importance and expression of competition. Ecol Monogr 51:105–124

    Article  Google Scholar 

  44. Norris DR, Marra PP, Kyser TK, Sherry TW, Ratcliffe LM (2004) Tropical winter habitat limits reproductive success on the temperate breeding grounds in a migratory bird. Proc R Soc Lond B 271:59–64

    Article  Google Scholar 

  45. Omland KE, Sherry TW (1994) Parental care at nests of two age classes of male American redstart: implications for female mate choice. Condor 96:606–613

    Article  Google Scholar 

  46. Ornelas JF, Gonzalez C, Espinosa de los Monteros A (2009) Uncorrelated evolution between vocal and plumage coloration traits in the trogons: a comparative study. J Evol Biol 22:471–484

    PubMed  Article  CAS  Google Scholar 

  47. Partan SR, Marler P (2005) Issues in the classification of multimodal communication signals. Am Nat 166:231–245

    PubMed  Article  Google Scholar 

  48. Payne RB (1982) Ecological consequences of song matching: breeding success and intraspecific song mimicry in indigo buntings. Ecology 63:401–411

    Article  Google Scholar 

  49. Payne RB, Payne LL, Doehlert SM (1988) Biological and cultural success of song memes in indigo buntings. Ecology 69:104–117

    Article  Google Scholar 

  50. Perreault S, Lemon RE, Kuhnlein U (1997) Patterns and correlates of extrapair paternity in American redstarts (Setophaga ruticilla). Behav Ecol 8:612–621

    Article  Google Scholar 

  51. Procter-Gray E, Holmes RT (1981) Adaptive significance of delayed attainment of plumage in male American redstarts: tests of two hypotheses. Evolution 35:742–751

    Article  Google Scholar 

  52. Pyle P (1997) Identification guide to North American birds, part I. Braun-Brumfield Inc, Ann Arbor

    Google Scholar 

  53. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, New York

    Google Scholar 

  54. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  55. Read AF, Weary DM (1992) The evolution of bird song: comparative analyses. Philos Trans R Soc Lond B 338:165–187

    Article  Google Scholar 

  56. Reudink MW, Marra PP, Boag PT, Ratcliffe LM (2009a) Plumage coloration predicts paternity and polygyny in the American redstart. Anim Behav 77:495–501

    Article  Google Scholar 

  57. Reudink MW, Marra PP, Kyser TK, Boag PT, Langin KM, Ratcliffe LM (2009b) Non-breeding season events influence sexual selection in a long-distance migratory bird. Proc R Soc Lond B 276:1619–1626

    Article  Google Scholar 

  58. Reudink MW, Studds CE, Marra PP, Kurt Kyser T, Ratcliffe LM (2009c) Plumage brightness predicts non-breeding season territory quality in a long-distance migratory songbird, the American redstart Setophaga ruticilla. J Avian Biol 40:34–41

    Article  Google Scholar 

  59. Rohwer S, Fretwell SD, Niles DM (1980) Delayed maturation in passerine plumages and the deceptive acquisition of resources. Am Nat 115:400–437

    Article  Google Scholar 

  60. Rohwer S, Klein WP, Heard S (1983) Delayed plumage maturation and the presumed prealternate molt in American redstarts. Wilson Bull 95:199–208

    Google Scholar 

  61. Schluter D, Price T (1993) Honesty, perception and population divergence in sexually selected traits. Proc R Soc Lond B 253:117–122

    Article  CAS  Google Scholar 

  62. Setchell JM (2003) Behavioural development in male mandrills (Mandrillus sphinx): puberty to adulthood. Behaviour 140:1053–1089

    Article  Google Scholar 

  63. Sherry TW, Holmes RT (1997) American redstart (Setophaga ruticilla). In: Poole A (ed) The birds of North America. No. 277. Cornell Lab of Ornithology, Ithaca. Retrieved from the Birds of North America Online: http://bna.birds.cornell.edu/bna/species/277. doi:10.2173/bna.277

  64. Shutler D (2011) Sexual selection: when to expect trade-offs. Biol Lett 7:101–104

    PubMed  Article  Google Scholar 

  65. Shutler D, Weatherhead PJ (1990) Targets of sexual selection: song and plumage of wood warblers. Evolution 44:1967–1977

    Article  Google Scholar 

  66. Staicer CA, Ingalls V, Sherry TW (2006) Singing behavior varies with breeding status of American Redstarts (Setophaga ruticilla). Wilson J Ornithol 118:439–451

    Article  Google Scholar 

  67. Studd MV, Robertson RJ (1985) Life-span, competition, and delayed plumage maturation in male passerines: the breeding threshold hypothesis. Am Nat 126:101–115

    Article  Google Scholar 

  68. Tabachnick B, Fidell L (1996) Using multivariate statistics. Harper & Row, New York

    Google Scholar 

  69. Tourangeau L (2002) Correlates of age and pairing success in male American redstarts (Setophaga ruticilla). B.Sc. Honour's thesis, Queen's University

Download references

Acknowledgments

We thank R. Montgomerie and T. Murphy for providing color-analysis equipment and support, C. Scott for paternity analysis, J. Foote for support in song analysis, and C. Toth, M. Osmond, and many capable assistants in the field. We thank K. Delmore, R. Robertson, P. Martin, W. Plaxton, and K. Munhall for useful discussion and helpful comments on this manuscript. Funding for this work was provided by Queen's University, Natural Sciences and Engineering Research Council, National Science Foundation, Ontario Government (MTCU), American Ornithologists' Union, Society of Canadian Ornithologists, Sigma Xi, and the American Museum of Natural History.

Ethical standards

Experiments in this study comply with the current laws of the countries in which they were performed.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ryan R. Germain.

Additional information

Communicated by T. Bakker

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Germain, R.R., Reudink, M.W., Marra, P.P. et al. Delayed maturation of multiple signals in a migratory songbird. Behav Ecol Sociobiol 66, 419–431 (2012). https://doi.org/10.1007/s00265-011-1288-x

Download citation

Keywords

  • Delayed song maturation
  • Delayed plumage maturation
  • Multiple signals
  • Mate choice
  • American redstart