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Journal of Ornithology

, Volume 159, Issue 3, pp 793–804 | Cite as

Plumage pigmentation patterns of diurnal raptors in relation to colour ornamentation and ecology

  • Ana Cristina R. Gomes
  • Renato Silva
  • Gonçalo C. Cardoso
Original Article

Abstract

While sexual signalling often compromises camouflage, some traits, including avian barred plumage, have been suggested to function simultaneously in camouflage and sexual signalling. Compared to coloration without pigmentation patterns, visual patterns are often beneficial for camouflage, and the precise arrangement of parallel bars in the pigmentation patterns of barred plumage may, at close range, provide cues on plumage quality useful for signalling. We used diurnal raptors, which benefit from camouflage for hunting in daylight, to test whether the evolution of some pigmentation patterns is associated with traits indicative of sexual selection. Phylogenetic regressions showed a negative association between the extent of barred and mottled plumage. There was also a negative association between the extent of ornamental colours and mottled plumage, thought to function mostly for camouflage, indicating a compromise between ornamentation and camouflage. The trade-off between ornamental colours and barred plumage was weaker than the one with mottled plumage, consistent with the hypothesis that barred plumage at times evolves for camouflage, similarly to mottled plumage, but at times can be co-opted for signalling together with ornamental colours. However, both barred plumage and ornamental coloration were only weakly related to socioecological traits suggestive of increased sexual selection. Therefore, despite differences in evolution between mottled and barred plumage in raptors, suggesting that the latter has more diverse functions than camouflage alone, behavioural research is needed to confirm the possible dual function of barred plumage as an ornamental trait.

Keywords

Camouflage Signalling Plumage bars Visual communication Phylogenetic regression Ornamental coloration 

Zusammenfassung

Muster der Gefiederpigmentierung bei tagaktiven Greifvögeln in Relation zu farblicher Ornamentierung und Ökologie

Während sexuelle Signale oft die Tarnung beeinträchtigen, wird vermutet, dass manche Merkmale, darunter auch die Sperberung beim Vogelgefieder, gleichzeitig der Tarnung als auch als Signal ans andere Geschlecht dienen können. Im Vergleich zur Färbung ohne Pigmentierungsmuster sind optische Muster oft hilfreich für die Tarnung und die genaue Anordnung der Parallelstreifen im Pigmentierungsmuster gesperberten Gefieders kann aus der Nähe Hinweise auf die Gefiederqualität geben, welche nützliche Signale darstellen. Um zu überprüfen, ob die Evolution mancher Pigmentierungsmuster mit Merkmalen zusammenhängt, welche auf sexuelle Selektion hindeuten, wählten wir tagaktive Greifvögel, für die eine Tarnfärbung auf der Jagd bei Tageslicht vorteilhaft ist. Phylogenetische Regressionsanalysen zeigten einen negativen Zusammenhang zwischen dem Ausmaß gesperberten beziehungsweise gefleckten Gefieders. Außerdem bestand ein negativer Zusammenhang zwischen dem Ausmaß an Farbornamenten und der Gefiederfleckung, bei der man hauptsächlich einen Tarneffekt annimmt, was auf einen Kompromiss zwischen Schmuck- und Tarnwirkung hindeutet. Der Kompromiss zwischen Farbornamenten und Gefiedersperberung war weniger deutlich als der bei Gefiederfleckung, was sich mit der Hypothese deckt, dass gesperbertes Gefieder manchmal – ähnlich wie geflecktes Gefieder - zu Tarnzwecken entwickelt wird, manchmal aber auch in Kombination mit Farbornamenten zur Signalübermittlung hinzugezogen werden kann. Allerdings standen sowohl Gefiedersperberung als auch Farbornamente nur in einem schwachen Zusammenhang mit sozioökologischen Merkmalen, die auf eine verstärkte sexuelle Selektion hinweisen. Trotz evolutiver Unterschiede zwischen geflecktem und gesperbertem Gefieder bei Greifvögeln, welche nahelegen, dass letzteres vielseitigere Funktionen hat, als nur der Tarnung zu dienen, sind weitere Verhaltensstudien notwendig, um eine eventuelle Doppelfunktion der Gefiedersperberung als Schmuckmerkmal zu bestätigen.

Notes

Acknowledgements

We thank Frank Shufelt and Sage Kadow for permission to use the photographs in this article. This work was supported by grant PTDC/BIA-EVF/116758/2010 and fellowships SFRH/BPD/46873/2008 and SFRH/BPD/110165/2015 from the Fundação para a Ciência e a Tecnologia. This comparative study was based on the literature and did not use live animals, and thus did not require legal permits.

Supplementary material

10336_2018_1550_MOESM1_ESM.pdf (238 kb)
Supplementary material 1 (PDF 237 kb)
10336_2018_1550_MOESM2_ESM.xls (96 kb)
Supplementary material 2 (XLS 96 kb)

References

  1. Albrecht T, Schnitzer J, Kreisinger J, Exnerová A, Bryja J, Munclinger P (2007) Extrapair paternity and the opportunity for sexual selection in long-distant migratory passerines. Behav Ecol 18:477–486CrossRefGoogle Scholar
  2. Andersson MB (1994) Sexual selection. Princeton University Press, Princeton, NJGoogle Scholar
  3. Armenta JK, Dunn PO, Whittingham LA (2008) Quantifying avian sexual dichromatism: a comparison of methods. J Exp Biol 211:2423–2430CrossRefPubMedGoogle Scholar
  4. Badyaev AV (1997a) Altitudinal variation in sexual dimorphism: a new pattern and alternative hypotheses. Behav Ecol 8:675–690CrossRefGoogle Scholar
  5. Badyaev AV (1997b) Covariation between life history and sexually selected traits: an example with cardueline finches. Oikos 80:128–138CrossRefGoogle Scholar
  6. Badyaev AV, Ghalambor CK (1998) Does a trade-off exist between sexual ornamentation and ecological plasticity? Sexual dichromatism and occupied elevational range in finches. Oikos 82:319–324CrossRefGoogle Scholar
  7. Badyaev AV, Hill GE (2002) Paternal care as a conditional strategy: distinct reproductive tactics associated with elaboration of plumage ornamentation in the House Finch. Behav Ecol 13:591–597CrossRefGoogle Scholar
  8. Badyaev AV, Hill GE (2003) Avian sexual dichromatism in relation to phylogeny and ecology. Annu Rev Ecol Evol Syst 34:27–49CrossRefGoogle Scholar
  9. Bailey SF (1978) Latitudinal gradients in colors and patterns of passerine birds. Condor 80:372–381CrossRefGoogle Scholar
  10. Baker RR, Parker G (1979) The evolution of bird coloration. Philos Trans R Soc B 287:63–130CrossRefGoogle Scholar
  11. Bergeron ZT, Fuller RC (2018) Using human vision to detect variation in avian coloration: how bad is it? Am Nat 191:269–276CrossRefPubMedGoogle Scholar
  12. Bonser RH (1995) Melanin and the abrasion resistance of feathers. Condor 97:590–591CrossRefGoogle Scholar
  13. Bortolotti GR, Blas J, Negro JJ, Tella JL (2006) A complex plumage pattern as an honest social signal. Anim Behav 72:423–430CrossRefGoogle Scholar
  14. Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595CrossRefPubMedGoogle Scholar
  15. Cardoso GC, Hu Y, Mota PG (2012) Birdsong, sexual selection, and the flawed taxonomy of canaries, goldfinches and allies. Anim Behav 84:111–119CrossRefGoogle Scholar
  16. Cuervo J, Møller A (1999) Ecology and evolution of extravagant feather ornaments. J Evol Biol 12:986–998CrossRefGoogle Scholar
  17. Dale J, Dey CJ, Delhey K, Kempenaers B, Valcu M (2015) The effects of life history and sexual selection on male and female plumage colouration. Nature 527:367–370CrossRefPubMedGoogle Scholar
  18. Drury JP, Burroughs N (2016) Nest shape explains variation in sexual dichromatism in New World blackbirds. J Avian Biol 47:312–320CrossRefGoogle Scholar
  19. Dunning JB (2008) CRC handbook of avian body masses. Taylor & Francis, Boca RatonGoogle Scholar
  20. Ferguson-Lees J, Christie DA (2001) Raptors of the world. Houghton Mifflin Harcourt, BostonGoogle Scholar
  21. Fitzpatrick S (1994) Colourful migratory birds: evidence for a mechanism other than parasite resistance for the maintenance of ‘good genes’ sexual selection. Proc R Soc B 257:155–160CrossRefGoogle Scholar
  22. Fitzpatrick S (1998) Intraspecific variation in wing length and male plumage coloration with migratory behaviour in continental and island populations. J Avian Biol 29:248–256CrossRefGoogle Scholar
  23. Freckleton R (2011) Dealing with collinearity in behavioural and ecological data: model averaging and the problems of measurement error. Behav Ecol Sociobiol 65:91–101CrossRefGoogle Scholar
  24. Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726CrossRefPubMedGoogle Scholar
  25. Garamszegi LZ, Mundry R (2014) Multimodel-inference in comparative analyses. In: Garamszegi LZ (ed) Modern phylogenetic comparative methods and their application in evolutionary biology. Springer, Berlin, pp 305–331Google Scholar
  26. Germain RR, Reudink MW, Marra PP, Ratcliffe LM (2010) Carotenoid-based male plumage predicts parental investment in the American Redstart. Wilson J Ornithol 122:318–325CrossRefGoogle Scholar
  27. Gladbach A, Gladbach DJ, Kempenaers B, Quillfeldt P (2010) Female-specific colouration, carotenoids and reproductive investment in a dichromatic species, the Upland Goose Chloephaga picta leucoptera. Behav Ecol Sociobiol 64:1779–1789CrossRefPubMedPubMedCentralGoogle Scholar
  28. Gluckman T-L, Cardoso GC (2009) A method to quantify the regularity of barred plumage patterns. Behav Ecol Sociobiol 63:1837–1844CrossRefGoogle Scholar
  29. Gluckman TL, Cardoso GC (2010) The dual function of barred plumage in birds: camouflage and communication. J Evol Biol 23:2501–2506CrossRefPubMedGoogle Scholar
  30. Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Kin-Lan H, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768CrossRefPubMedGoogle Scholar
  31. Hammers M, von Engelhardt N, Langmore NE, Komdeur J, Griffith SC, Magrath MJ (2009) Mate-guarding intensity increases with breeding synchrony in the colonial Fairy Martin, Petrochelidon ariel. Anim Behav 78:661–669CrossRefGoogle Scholar
  32. Hasson O (1991) Sexual displays as amplifiers: practical examples with an emphasis on feather decorations. Behav Ecol 2:189–197CrossRefGoogle Scholar
  33. Hastad O, Odeen A (2008) Different ranking of avian colors predicted by modeling of retinal function in humans and birds. Am Nat 171:831–838CrossRefPubMedGoogle Scholar
  34. Hu Y, Cardoso GC (2009) Are bird species that vocalize at higher frequencies preadapted to inhabit noisy urban areas? Behav Ecol 20:1268–1273CrossRefGoogle Scholar
  35. Jetz W, Thomas G, Joy J, Hartmann K, Mooers A (2012) The global diversity of birds in space and time. Nature 491:444–448CrossRefPubMedGoogle Scholar
  36. Lind O, Mitkus M, Olsson P, Kelber A (2013) Ultraviolet sensitivity and colour vision in raptor foraging. J Exp Biol 216:1819–1826CrossRefPubMedGoogle Scholar
  37. Marques CI, Batalha HR, Cardoso GC (2016) Signalling with a cryptic trait: the regularity of barred plumage in common waxbills. R Soc Open Sci 3:160195CrossRefPubMedPubMedCentralGoogle Scholar
  38. Marshall NJ (2000) Communication and camouflage with the same ‘bright’ colours in reef fishes. Philos Trans R Soc B 355:1243–1248CrossRefGoogle Scholar
  39. Marshall KL, Gluckman TL (2015) The evolution of pattern camouflage strategies in waterfowl and game birds. Ecol Evol 5:1981–1991CrossRefPubMedPubMedCentralGoogle Scholar
  40. Martin TE, Badyaev AV (1996) Sexual dichromatism in birds: importance of nest predation and nest location for females versus males. Evolution 50:2454–2460CrossRefPubMedGoogle Scholar
  41. McNaught MK, Owens IP (2002) Interspecific variation in plumage colour among birds: species recognition or light environment? J Evol Biol 15:505–514CrossRefGoogle Scholar
  42. Mitchell DP, Dunn PO, Whittingham LA, Freeman-Gallant CR (2007) Attractive males provide less parental care in two populations of the Common Yellowthroat. Anim Behav 73:165–170CrossRefGoogle Scholar
  43. Mundry R (2014) Statistical issues and assumptions of phylogenetic generalized least squares. In: Garamszegi LZ (ed) Modern phylogenetic comparative methods and their application in evolutionary biology. Springer, Berlin, pp 131–153Google Scholar
  44. O’brien R (2007) A caution regarding rules of thumb for variance inflation factors. Qual Quant 41:673–690CrossRefGoogle Scholar
  45. Orme D (2013) The caper package: comparative analysis of phylogenetics and evolution in R. http://cranr-project.org/web/packages/caper/vignettes/caperpdf5
  46. Östman Ö, Stuart-Fox D (2011) Sexual selection is positively associated with ecological generalism among agamid lizards. J Evol Biol 24:733–740CrossRefPubMedGoogle Scholar
  47. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884CrossRefPubMedGoogle Scholar
  48. Perez-Rodriguez L, Jovani R, Stevens M (2017) Shape matters: animal colour patterns as signals of individual quality. Proc R Soc B 284:20162446CrossRefPubMedGoogle Scholar
  49. Price JJ (1996) An association of habitat with color dimorphism in finches. Auk 113:256–257CrossRefGoogle Scholar
  50. R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0Google Scholar
  51. Riegner MF (2008) Parallel evolution of plumage pattern and coloration in birds: implications for defining avian morphospace. Condor 110:599–614CrossRefGoogle Scholar
  52. Rubolini D, Liker A, Garamszegi LZ, Møller AP, Saino N (2015) Using the BirdTree.org website to obtain robust phylogenies for avian comparative studies: a primer. Curr Zool 61:959–965CrossRefGoogle Scholar
  53. Ruxton GD, Speed MP, Kelly DJ (2004) What, if anything, is the adaptive function of countershading? Anim Behav 68:445–451CrossRefGoogle Scholar
  54. Shultz AJ, Burns KJ (2013) Plumage evolution in relation to light environment in a novel clade of Neotropical tanagers. Mol Phylogenet Evol 66:112–125CrossRefPubMedGoogle Scholar
  55. Singh P, Price TD (2015) Causes of the latitudinal gradient in birdsong complexity assessed from geographical variation within two Himalayan warbler species. Ibis 157:511–527CrossRefGoogle Scholar
  56. Somveille M, Marshall KL, Gluckman TL (2016) A global analysis of bird plumage patterns reveals no association between habitat and camouflage. PeerJ 4:e2658CrossRefPubMedPubMedCentralGoogle Scholar
  57. Spottiswoode C, Møller AP (2004) Extrapair paternity, migration, and breeding synchrony in birds. Behav Ecol 15:41–57CrossRefGoogle Scholar
  58. Spottiswoode CN, Tøttrup AP, Coppack T (2006) Sexual selection predicts advancement of avian spring migration in response to climate change. Proc R Soc B 273:3023–3029CrossRefPubMedGoogle Scholar
  59. Stevens M (2007) Predator perception and the interrelation between different forms of protective coloration. Proc Biol Sci B 274:1457–1464CrossRefGoogle Scholar
  60. Stevens M, Merilaita S (2009) Animal camouflage: current issues and new perspectives. Philos Trans R Soc B 364:423–427CrossRefGoogle Scholar
  61. Swaddle JP, Cuthill IC (1994) Female Zebra Finches prefer males with symmetric chest plumage. Proc R Soc B 258:267–271CrossRefGoogle Scholar
  62. Tate GJ, Bishop JM, Amar A (2016) Differential foraging success across a light level spectrum explains the maintenance and spatial structure of colour morphs in a polymorphic bird. Ecol Lett 19:679–686CrossRefPubMedGoogle Scholar
  63. Tobias J, Seddon N (2009) Sexual selection and ecological generalism are correlated in antbirds. J Evol Biol 22:623–636CrossRefPubMedGoogle Scholar
  64. Troscianko T, Benton CP, Lovell PG, Tolhurst DJ, Pizlo Z (2009) Camouflage and visual perception. Philos Trans R Soc B 364:449–461CrossRefGoogle Scholar
  65. Vergara P, Fargallo JA (2011) Multiple coloured ornaments in male Common Kestrels: different mechanisms to convey quality. Naturwissenschaften 98:289–298CrossRefPubMedGoogle Scholar
  66. Vergara P, Fargallo JA, Martinez-Padilla J (2015) Genetic basis and fitness correlates of dynamic carotenoid-based ornamental coloration in male and female Common Kestrels Falco tinnunculus. J Evol Biol 28:146–154CrossRefPubMedGoogle Scholar
  67. West-Eberhard MJ (1983) Sexual selection, social competition, and speciation. Q Rev Biol 58:155–183CrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2018

Authors and Affiliations

  • Ana Cristina R. Gomes
    • 1
  • Renato Silva
    • 1
  • Gonçalo C. Cardoso
    • 1
    • 2
  1. 1.CIBIO-Centro de Investigação em Biodiversidade e Recursos GenéticosUniversidade do PortoVairãoPortugal
  2. 2.Behavioural Ecology Group, Department of BiologyUniversity of CopenhagenCopenhagen ØDenmark

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