Skip to main content
Log in

How many color metrics do we need? Evaluating how different color-scoring procedures explain carotenoid pigment content in avian bare-part and plumage ornaments

  • Methods
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

For a variety of technical and conceptual reasons, biologists have come to use several different methods to quantify the colors of animals. However, the relative abilities of these different color-scoring procedures to capture variation in the actual color-generating mechanisms—pigment or structural composition of the integument—have never been tested systematically. Here, we examined which commonly employed color metrics predict carotenoid content of ornaments in three avian species (house finch Carpodacus mexicanus, mallard duck Anas platyrhynchos, and zebra finch Taeniopygia guttata). We used spectrophotometry to measure reflectance spectra from beak and feather tissue, calculated numerous color metrics (e.g., hue, chroma, brightness, principal components, and tetrahedral color space position) from these spectra, and determined carotenoid content at the site of color measurement with high-performance liquid chromatography. We found that several principal component, tristimulus, and avian visual model metrics significantly correlated with carotenoid content of house finch feathers and duck beaks. Carotenoid content of mallard beaks was most closely correlated with brightness and saturation metrics, whereas in house finch feathers, carotenoid concentration was best captured by hue and saturation metrics. According to tristimulus scores and visual models, we found that the ultraviolet portion of the spectrum was not an essential predictor of variation in carotenoid content. Also, visual model chromatic contrasts generally were not significant predictors of carotenoid content, although some achromatic contrasts and tetrahedral color space vector parameters were. Our results indicate that numerous methods, especially tristimulus scores, are suitable for capturing pigment-based color variation in two carotenoid-containing ornaments, and we discuss the merits and shortcomings of these different approaches. In contrast, there were no significant relationships between any color metrics and the carotenoid content of zebra finch beaks, suggesting that other color-generating mechanisms besides carotenoids may contribute to color variability in this species.

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

Similar content being viewed by others

Abbreviations

B:

Brightness

H:

Hue

HPLC:

High-performance liquid chromatography

LWS:

Long wavelength sensitive

MWS:

Medium wavelength sensitive

PC:

Principal component

PCA:

Principal components analysis

S:

Saturation

SWS:

Short wavelength sensitive

UV:

Ultraviolet

UV-Vis:

Ultraviolet and human-visible

UVS:

Ultraviolet sensitive

VS:

Violet sensitive

θ:

Theta in visual model; relative stimulation of SWS, MWS, and LWS photoreceptors

φ:

Psi in visual model: stimulation of the UV/V sensitive photoreceptors

r :

R in visual model: chromaticity or spectral purity

References

  • Andersson S, Prager M (2006) Quantifying colors. In: Hill GE, McGraw KJ (eds) Bird coloration, vol I, Mechanisms and measurements. Harvard University Press, Boston, pp 41–89

    Google Scholar 

  • Armenta JK, Dunn PO, Whittingham LA (2008) Quantifying avian sexual dichromatism: a comparison of methods. J Exp Biol 211:2423–2430

    Article  PubMed  Google Scholar 

  • Avilés JM, Perez-Contreras T, Navarro C, Soler JJ (2008) Dark nests and conspicuousness in color patterns of nestlings of altricial birds. Am Nat 171:327–338

    Article  PubMed  Google Scholar 

  • Bleiweiss R (2005) Variation in ultraviolet reflectance by carotenoid-bearing feathers of tanagers (Thraupini: Emberizinae: Passeriformes). Biol J Linn Soc 84:243–257

    Article  Google Scholar 

  • Bowmaker JK, Heath LA, Wilkie SE, Hunt DM (1997) Visual pigments and oil droplets from six classes of photoreceptor in the retinas of birds. Vis Res 37:2183–2194

    Article  CAS  PubMed  Google Scholar 

  • Bowmaker JK, Hunt DM (1999) Molecular biology of photoreceptor spectral sensitivities. In: Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S (eds) Adaptive Mechanisms in the Ecology of Vision. Kluwer Academic Publishers, London, pp 439–462

    Google Scholar 

  • Bright A, Waas JR, King CM, Cuming PD (2004) Bill colour and correlates of male quality in blackbirds: an analysis using canonical ordination. Behav Proc 65:123–132

    Article  CAS  Google Scholar 

  • Butler MW, McGraw KJ (2009) Indoor housing during development affects moult, carotenoid circulation, and beak colouration of mallard ducks (Anas platyrhynchos). Avian Biol Res 2:203–211

    Article  Google Scholar 

  • Cohen AA, McGraw KJ, Wiersma P, Williams JB, Robinson WD, Robinson TR, Brawn JD, Ricklefs RE (2008) Interspecific associations between circulating antioxidant levels and life-history variation in birds. Am Nat 172:178–193

    Article  PubMed  Google Scholar 

  • Cuthill IC, Bennett ATD, Partridge JC, Maier EJ (1999) Plumage reflectance and the objective assessment of avian sexual dichromatism. Am Nat 160:183–200

    Article  Google Scholar 

  • Das D, Wilkie SE, Hunt DM, Bowmaker JK (1999) Visual pigments and oil droplets in the retina of a passerine bird, the canary Serinus canaria: microspectrophotometry and opsin sequences. Vis Res 39:2801–2815

    Article  CAS  PubMed  Google Scholar 

  • Delhey K, Peters A (2008) Quantifying variability of avian colours: are signalling traits more variable? PLoS ONE 3:e1689

    Article  PubMed  Google Scholar 

  • Eaton MD (2005) Human vision fails to distinguish widespread sexual dichromatism among sexually “monochromatic” birds. Proc Natl Acad Sci USA 102:10942–10946

    Article  CAS  PubMed  Google Scholar 

  • Endler JA, Mielke PW (2005) Comparing entire colour patterns as birds see them. Biol J Linn Soc 86:405–431

    Article  Google Scholar 

  • Forstmeier W, Schielzeth H, Schneider M, Kempenaers B (2007) Development of polymorphic microsatellite markers for the zebra finch (Taeniopygia guttata). Molec Ecol Notes 7:1026–1028

    Article  CAS  Google Scholar 

  • Gomez D, Théry M (2007) Simultaneous crypsis and conspicuousness in color patterns: comparative analysis of a neotropical rainforest bird community. Am Nat 169:42–61

    Article  Google Scholar 

  • Grill CP, Rush VN (2000) Analysing spectral data: comparison and application of two techniques. Biol J Linn Soc 69:121–138

    Article  Google Scholar 

  • Grimm CP, Arnold PY (1995) Reading and understanding multivariate statistics. Volume 1. American Psychological Association, Washington DC

  • Hart N, Hunt D (2007) Avian visual pigments: characteristics, spectral tuning, and evolution. Am Nat 169:S7–S26

    Article  PubMed  Google Scholar 

  • Håstad O, Victorsson J, Ödeen A (2005) Differences in color vision make passerines less conspicuous in the eyes of their predators. Proc Natl Acad Sci USA 102:6391–6394

    Article  PubMed  Google Scholar 

  • Hill GE (1998) An easy, inexpensive means to quantify plumage coloration. J Field Ornithol 69:353–363

    Google Scholar 

  • Hill GE (2002) A red bird in a brown bag: the function and evolution of colorful plumage in the House Finch. Oxford University Press, New York

    Google Scholar 

  • Inouye CY, Hill GE, Stradi RD, Montgomerie R (2001) Carotenoid pigments in male house finch plumage in relation to age, subspecies, and ornamental coloration. Auk 118:900–915

    Article  Google Scholar 

  • Jane SD, Bowmaker JK (1988) Tetrachromatic colour vision in the duck (Anas platyrhynchos L.): microspectrophotometry of visual pigments and oil droplets. J Comp Physiol A 162:225–235

    Article  CAS  Google Scholar 

  • Lessels CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Google Scholar 

  • Li Q, Gao KQ, Vinther J, Shawkey MD, Clarke JA, D’Alba L, Meng Q, Briggs DEG, Prum RO (2010) Plumage color patterns of an extinct dinosaur. Science 327:1369–1372

    Article  CAS  PubMed  Google Scholar 

  • Lind O, Kelber A (2009) Avian colour vision: effects of variation in receptor sensitivity and noise data on model predictions as compared to behavioural results. Vis Res 49:1939–1947

    Article  PubMed  Google Scholar 

  • Loyau A, Gomez D, Moureau B, Thery M, Hart NS, Jalme MS, Bennett ATD, Sorci G (2007) Iridescent structurally based coloration of eyespots correlates with mating success in the peacock. Behav Ecol 18:1123–1131

    Article  Google Scholar 

  • Mahler B, Kempenaers B (2002) Objective assessment of sexual plumage dichromatism in the Picui dove. Condor 104:248–254

    Article  Google Scholar 

  • Maney DL, Davis AK, Goode CT, Reid A, Showalter C (2008) Carotenoid-based plumage coloration predicts leukocyte parameters during the breeding season in northern cardinals (Cardinalis cardinalis). Ethol 114:369–380

    Article  Google Scholar 

  • Mays HL Jr, McGraw KJ, Ritchison G, Cooper S, Rush V, Parker RS (2004) Sexual dichromatism in the yellow-breasted chat Icteria virens: spectrophotometric analysis and biochemical basis. J Avian Biol 35:125–134

    Article  Google Scholar 

  • McGraw KJ (2005) Interspecific variation in dietary carotenoid assimilation in birds: links to phylogeny and color ornamentation. Comp Biochem Physiol B 142:245–250

    Article  CAS  PubMed  Google Scholar 

  • McGraw KJ (2006) The mechanics of carotenoid coloration in birds. In: Hill GE, McGraw KJ (eds) Bird coloration, vol I, mechanisms and measurements. Harvard University Press, Boston, pp 177–242

    Google Scholar 

  • McGraw KJ, Toomey MB (2010) Carotenoid accumulation in the tissues of zebra finches: predictors of integumentary pigmentation and implications for carotenoid allocation strategies. Phys Biochem Zool 83:97–109

    Article  CAS  Google Scholar 

  • McGraw KJ, Adkins-Regan E, Parker RS (2002) Anhydrolutein in the zebra finch: a new, metabolically derived carotenoid in birds. Comp Biochem Physiol B 132:811–818

    Article  CAS  PubMed  Google Scholar 

  • McGraw KJ, Safran RJ, Wakamatsu K (2005) How feather colour reflects its melanin content. Funct Ecol 19:816–821

    Article  Google Scholar 

  • McGraw KJ, Nolan PM, Crino OL (2006) Carotenoid accumulation strategies for becoming a colourful House Finch: analyses of plasma and liver pigments in wild moulting birds. Funct Ecol 20:678–688

    Article  Google Scholar 

  • McGraw KJ, Tourville EA, Butler MW (2008) A quantitative comparison of the commonly used methods for extracting carotenoids from avian plasma. Behav Ecol Sociobiol 62:1991–2002

    Article  Google Scholar 

  • Montgomerie R (2006) Analyzing Colors. In: Hill GE, McGraw KJ (eds) Bird coloration, vol I, Mechanisms and measurements. Harvard University Press, Boston, pp 90–147

    Google Scholar 

  • Montgomerie R (2008) CLR, version 1.05. Queen’s University, Kingston, Canada. Available at: http://post.queensu.ca/~mont/color/analyze.html. Accessed 18 September 2009

  • Mougeot F, Martínez-Padilla J, Pérez-Rodríguez L, Bortolotti GR (2007) Carotenoid-based colouration and ultraviolet reflectance of the sexual ornaments of grouse. Behav Ecol Sociobiol 61:741–751

    Article  Google Scholar 

  • Ödeen A, Håstad O (2003) Complex distribution of avian color vision systems revealed by sequencing the SWS1 opsin from total DNA. Molec Biol Evol 20:855–861

    Article  PubMed  Google Scholar 

  • Omland KE (1996) Female mallard mating preferences for multiple male ornaments. I. Natural Variation. Behav Ecol Sociobiol 39:353–360

    Google Scholar 

  • Parker TH, Stansberry BM, Becker CD, Gipson PS (2003) Do melanin- or carotenoid-pigmented plumage ornaments signal condition and predict pairing success in the Kentucky warbler? Condor 105:663–671

    Article  Google Scholar 

  • Peters A, Denk AG, Delhey K, Kempenaers B (2004a) Carotenoid-based bill colour as an indicator of immunocompetence and sperm performance in male mallards. J Evol Biol 17:1111–1120

    Article  CAS  PubMed  Google Scholar 

  • Peters A, Delhey K, Denk AG, Kempenaers B (2004b) Trade-offs between immune investment and sexual signaling in male mallards. Am Nat 164:51–59

    Article  PubMed  Google Scholar 

  • Quesada J, Senar JC (2006) Comparing plumage colour measurements obtained directly from live birds and from collected feathers: the case of the great tit Parus major. J Avian Biol 37:609–616

    Article  Google Scholar 

  • Reudink MW, Studds CE, Marra PP, Kyser TK, Ratcliffe LM (2009) 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 

  • Saino N, Møller AP (1996) Sexual ornamentation and immunocompetence in the barn swallow. Behav Ecol 7:227–232

    Article  Google Scholar 

  • Saks L, McGraw KJ, Hõrak P (2003) How feather colour reflects its carotenoid content. Funct Ecol 17:555–561

    Article  Google Scholar 

  • Shawkey MD, Hill GE, McGraw KJ, Hood WR, Huggins K (2006) An experimental test of the contributions and condition dependence of microstructure and carotenoids in yellow plumage coloration. Proc Roy Soc Lond B 273:2985–2991

    Article  CAS  Google Scholar 

  • Solís E, Avilés JM, De La Cruz C, Valencia J, Sorci G (2008) Winter male plumage coloration correlates with breeding status in a cooperative breeding species. Behav Ecol 19:391–397

    Article  Google Scholar 

  • Stoddard MC, Prum RO (2008) Evolution of avian plumage color in a tetrahedral color space: a phylogenetic analysis of new world buntings. Am Nat 171:755–776

    Article  PubMed  Google Scholar 

  • Toomey MB, McGraw KJ (2009) Seasonal, sexual, and quality related variation in retinal carotenoid accumulation in the house finch (Carpodacus mexicanus). Funct Ecol 23:321–329

    Article  Google Scholar 

  • Toral GM, Figuerola J, Negro JJ (2008) Multiple ways to become red: pigment identification in red feathers using spectrometry. Comp Biochem Physiol B 150:147–152

    Article  CAS  PubMed  Google Scholar 

  • Uy JAC, Endler JA (2004) Modification of the visual background increases the conspicuousness of golden-collared manakin displays. Behav Ecol 15:1003–1010

    Article  Google Scholar 

  • Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc Roy Soc Lond B 265:351–358

    Article  CAS  Google Scholar 

  • Vorobyev M, Osorio D, Bennett ATD, Marshall NJ, Cuthill IC (1998) Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A 183:621–633

    Article  CAS  PubMed  Google Scholar 

  • Wyszecki G, Stiles WS (1982) Color Science: concepts and methods, quantitative data and formulae. Wiley, New York, p 950

    Google Scholar 

  • Zar JH (1999) Biostatistical Analysis, 4th edn. Prentice-Hall, Upper Saddle River, NJ

    Google Scholar 

  • Zuk M, Johnson K, Thornhill R, Ligon JD (1990) Parasites and male ornaments in free-ranging and captive red jungle fowl. Behav 114:232–248

    Article  Google Scholar 

  • Zuk M, Decruyenaere JG (1994) Measuring individual variation in colour: a comparison of two techniques. Biol J Linn Soc 53:165–173

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank E. Tourville, A. Bascuñán, and V. Peng with laboratory and animal assistance, and several anonymous reviewers for comments that greatly improved the manuscript. Funding was provided to KJM by the National Science Foundation (IOS-0746364, IOS-0910357, IOS-0923694, and IOS-0925633).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael W. Butler.

Additional information

Communicated by E. Fernandez-Juricic

Electronic supplementary materials

Below is the link to the electronic supplementary material.

ESM 1

(PDF 135 kb)

ESM 2

(PDF 164 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Butler, M.W., Toomey, M.B. & McGraw, K.J. How many color metrics do we need? Evaluating how different color-scoring procedures explain carotenoid pigment content in avian bare-part and plumage ornaments. Behav Ecol Sociobiol 65, 401–413 (2011). https://doi.org/10.1007/s00265-010-1074-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-010-1074-1

Keywords

Navigation