Why are birds' eggs colourful? Eggshell pigments co-vary with life-history and nesting ecology among British breeding non-passerine birds

Biological Journal of the Linnean Society

Volumn 106, Issue 3, 2012, Pages 657-672

  Cassey, Phillip ^a,b   Thomas, Gavin H ^c   Portugal, Steven J ^b,d   Maurer, Golo ^a,b   Hauber, Mark E ^e   Grim, Tomáš ^f   Lovell, P George ^g   Mikšík, Ivan ^h  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

^d ROYAL VETERINARY COLLEGE   (United Kingdom)

^e CITY UNIVERSITY OF NEW YORK   (United States)

^f PALACKÝ UNIVERSITY   (Czech Republic)

^g UNIVERSITY OF ST ANDREWS   (United Kingdom)

^h INSTITUTE OF PHYSIOLOGY   (Czech Republic)

Author keywords

Biliverdin; Phylogenetically controlled GLM; Protoporphyrin

Indexed keywords

BIOCHEMISTRY; BIRD; COLOR; COMPARATIVE STUDY; EGG; EGGSHELL; LIFE HISTORY TRAIT; MUSEUM; NESTING; PHYLOGENETICS; PHYLOGENY; PIGMENT; REPRODUCTIVE BIOLOGY; RESEARCH WORK;

UNITED KINGDOM;

AVES; PASSERIFORMES;

EID: 84862330278     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2012.01877.x     Document Type: Article

References (86)

1. Avilés JM, Soler JJ, Hart NS. 2011. Sexual selection based on egg colour: physiological models and egg discrimination experiments in a cavity-nesting bird. Behavioral Ecology and Sociobiology 65: 1721-1730.
2. Avilés JM, Stokke BG, Moksnes A, Røskaft E, Møller AP. 2007. Environmental conditions influence egg color of reed warblers Acrocephalus scirpaceus and their parasite, the common cuckoo Cuculus canorus. Behavioral Ecology and Sociobiology 61: 475-485.
3. Bandaranayake WM. 2006. The nature and role of pigments of marine invertebrates. Natural Product Reports 23: 223-255.
4. Beissinger SR, Cook MI, Arendt WJ. 2005. The shelf life of bird eggs: testing egg viability using a tropical climate gradient. Ecology 86: 2164-2175.
5. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL. 2008. GenBank. Nucleic Acids Research 36: D25-D30.
6. Bertram BCR, Burger AE. 1981. Are ostrich Struthio camelus eggs the wrong color? Ibis 123: 207-210.
7. Birkhead TR. 1978. Behavioural adaptations to high density nesting in the common guillemot Uria aalge. Animal Behaviour 26: 321-331.
8. Cassey P, Ewen JG, Blackburn TM, Hauber ME, Vorobyev M, Marshall NJ. 2008. Eggshell colour does not predict measures of maternal investment in eggs of Turdus thrushes. Die Naturwissenschaften 95: 713-721.
9. Cassey P, Hauber ME, Maurer G, Ewen JG. 2011. Sources of variation in reflectance spectrophotometry: a quantitative analysis using avian eggshell colour. Methods in Ecology and Evolution. doi: 10.1111/j.2041-210X.2011.00152.x.
10. Cassey P, Maurer G, Duval C, Ewen JG, Hauber ME. 2010a. Differential impacts of time since collection on avian eggshell color: a comparison of museum and fresh egg specimens. Behavioral Ecology and Sociobiology 64: 1711-1720.
11. Cassey P, Portugal SJP, Maurer G, Ewen JG, Boulton RL, Hauber ME, Blackburn TM. 2010b. Variability in avian eggshell colour: a comparative study of museum eggshells. PLoS ONE 5: e12054.
12. Cherry MI, Gosler AG. 2010. Avian eggshell coloration: new perspectives on adaptive explanations. Biological Journal of the Linnean Society 100: 753-762.
13. CIE. 1986. Colorimetry. Vienna: Bureau Central CIE.
14. Comfort A. 1951. The pigmentation of molluscan shells. Biological Reviews of the Cambridge Philosophical Society 26: 285-301.
15. Cook MI, Beissinger SR, Toranzos GA, Rodriguez RA, Arendt WJ. 2005. Microbial infection affects egg viability and incubation behavior in a tropical passerine. Behavioral Ecology 16: 30-36.
16. Cramp S, Simmons KEL, eds. 19781994. The birds of the Western Palaearctic. Oxford: Oxford University Press.
17. Davies NB. 2000. Cuckoos, cowbirds and other cheats. London: T & AD Poyser.
18. Davies NB, Brooke MDL. 1989. An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. I. Host egg discrimination. Journal of Animal Ecology 58: 207-224.
19. del Hoyo J, Elliott A, Christie DA, eds. 19922002. Handbook of the birds of the world. Barcelona: Lynx Edicions.
20. Drummond AJ, Ashton BMC, Heled J, Kearse M, Moir R, Stones-Havas S, Thierer T, Wilson A. 2010. Geneious v4.8.5. Available at:.
21. Felsenstein J. 1985. Phylogenies and the comparative method. American Naturalist 125: 1-15.
22. Fischer H, Kögl F. 1923. Zur Kenntnis der natürlichen Porphyrine IV. Über das Ooporphyrin. Zeitschrift fur Physiologische Chemie 131: 241-261.
23. Fossøy F, Antonov A, Moksnes A, Røskaft E, Vikan JR, Møller AP, Shykoff JA, Stokke BG. 2011. Genetic differentiation among sympatric cuckoo host races: males matter. Proceedings of the Royal Society of London, Series B: Biological Sciences 278: 1639-1645.
24. Freckleton RP, Harvey PH, Pagel M. 2002. Phylogenetic analysis and comparative data: a test and review of the evidence. American Naturalist 160: 712-726.
25. Gorchein A, Lim CK, Cassey P. 2009. Extraction and analysis of colourful eggshell pigments using HPLC and HPLC/electrospray ionization tandem mass spectrometry. Biomedical Chromatography 23: 602-606.
26. Gosler AG, Higham JP, Reynolds SJ. 2005. Why are birds' eggs speckled? Ecology Letters 8: 1105-1113.
27. Götmark F. 1992. Blue eggs do not reduce nest predation in the song thrush, Turdus philomelos. Behavioral Ecology and Sociobiology 30: 245-252.
28. Hanley D, Doucet S. 2009. Egg coloration in ring-billed gulls (Larus delawarensis): a test of the sexual signaling hypothesis. Behavioral Ecology and Sociobiology 63: 719-729.
29. Hanley D, Doucet S, Dearborn DC. 2010. A blackmail hypothesis for the evolution of conspicuous egg coloration in birds. Auk 127: 453-459.
30. Higham J, Gosler A. 2006. Speckled eggs: water-loss and incubation behaviour in the great tit Parus major. Oecologia 149: 561-570.
31. Hincke MT, Nys Y, Gautron J. 2010. The role of matrix proteins in eggshell formation. Journal of Poultry Science 47: 208-219.
32. Hubbard JK, Uy JAC, Hauber ME, Hoekstra HE, Safran RJ. 2010. Vertebrate pigmentation: from underlying genes to adaptive function. Trends in Ecology and Evolution 26: 231-239.
33. Igic B, Greenwood DR, Palmer DJ, Cassey P, Gill BJ, Grim T, Brennan PL, Bassett SM, Battley PF, Hauber ME. 2010. Detecting pigments from colourful eggshells of extinct birds. Chemoecology 20: 43-48.
34. Ishikawa S, Suzuki K, Fukuda E, Arihara K, Yamamoto Y, Mukai T, Itoh M. 2010. Photodynamic antimicrobial activity of avian eggshell pigments. FEBS Letters 584: 770-774.
35. Jagannath A, Shore RF, Walker LA, Ferns PN, Gosler AG. 2008. Eggshell pigmentation indicates pesticide contamination. Journal of Applied Ecology 45: 133-140.
36. Kennedy GY, Vevers HG. 1976. A survey of avian eggshell pigments. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 55: 117-123.
37. Kilner RM. 2006. The evolution of egg colour and patterning in birds. Biological Reviews 81: 383-406.
38. Krist M, Grim T. 2007. Are blue eggs a sexually selected signal of female collared flycatchers? A cross-fostering experiment. Behavioral Ecology and Sociobiology 61: 863-876.
39. Lack D. 1948. The significance of clutch sizes. Part III - some interspecific comparisons. Ibis 90: 25-45.
40. Lahti DC. 2008. Population differentiation and rapid evolution of egg color in accordance with solar radiation. Auk 125: 796-802.
41. Lemberg R. 1934. Bile pigments. VI. Biliverdin, uteroverdin and oocyan. Biochemical Journal 28: 978-987.
42. Lovell PG, Tolhurst DJ, Párraga CA, Baddeley R, Leonards U, Troscianko J, Troscianko T. 2005. Stability of the color-opponent signals under changes of illuminant in natural scenes. Journal of the Optical Society of America A 22: 2060-2071.
43. Lyon BE. 2003. Egg recognition and counting reduce costs of avian conspecific brood parasitism. Nature 422: 495-499.
44. Maurer G, Portugal SJ, Cassey P. 2011. An embryo's eye view of avian eggshell pigmentation. Journal of Avian Biology 42: 494-504.
45. Maurer G, Portugal SJ, Mikšík I, Cassey P. 2011. Speckles of cryptic black headed gull eggs show no mechanical or conductance structural function. Journal of Zoology 285: 194-204.
46. McGraw KJ, Wakamatsu K, Ito S, Nolan PM, Jouventin P, Dobson FS, Austic RE, Safran RJ, Siefferman LM. 2004. You can't judge a pigment by its color: carotenoid and melanin content of yellow and brown feathers in swallows, bluebirds, penguins, and domestic chickens. Condor 106: 390-395.
47. Mertens K, Vaesen I, Loffel J, Kemps B, Kamers B, Perianu C, Zoons J, Darius P, Decuypere E, De Baerdemaeker J, De Ketelaere B. 2010. The transmission color value: a novel egg quality measure for recording shell color used for monitoring the stress and health status of a brown layer flock. Poultry Science 89: 609-617.
48. Mikšík I, Holan V, Deyl Z. 1996. Avian eggshell pigments and their variability. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology 113: 607-612.
49. Milgrom LR. 1997. The colours of life: an introduction to the chemistry of porphyrins and related compounds. Oxford: Oxford University Press.
50. Monroe BLJ, Sibley CG. 1997. A world checklist of birds. New Haven, CT: Yale University Press.
51. Morales J, Kim S-Y, Lobato E, Merino S, Tomás G, Martínez-de la Puente J, Moreno J. 2010. On the heritability of blue-green eggshell coloration. Journal of Evolutionary Biology 23: 1783-1791.
52. Morales J, Sanz JJ, Moreno J. 2006. Egg colour reflects the amount of yolk maternal antibodies and fledging success in a songbird. Biology Letters 2: 334-336.
53. Morales J, Velando A, Moreno J. 2008. Pigment allocation to eggs decreases plasma antioxidants in a songbird. Behavioral Ecology and Sociobiology 63: 227-233.
54. Morales J, Velando A, Torres R. 2011. Biliverdin-based egg coloration is enhanced by carotenoid supplementation. Behavioral Ecology and Sociobiology 65: 197-203.
55. Moreno J, Lobato E, Morales J. 2011. Eggshell blue-green colouration fades immediately after oviposition: a cautionary note about measuring natural egg colours. Ornis Fennica 88: 51-56.
56. Moreno J, Lobato E, Morales J, Merino S, Tomas G, Martinez-de la Puente J, Sanz JJ, Mateo R, Soler JJ. 2006. Experimental evidence that egg color indicates female condition at laying in a songbird. Behavioral Ecology 17: 651-655.
57. Moreno J, Osorno JL. 2003. Avian egg colour and sexual selection: does eggshell pigmentation reflect female condition and genetic quality? Ecology Letters 6: 803-806.
58. Moreno J, Osorno JL, Morales J, Merino S, Tomás G. 2004. Egg colouration and male parental effort in the pied flycatcher Ficedula hypoleuca. Journal of Avian Biology 35: 300-304.
59. Needham AE. 1974. The significance of zoochromes. Berlin: Springer.
60. Nys Y, Gautron J, Garcia-Ruiz JM, Hincke MT. 2004. Avian eggshell mineralization: biochemical and functional characterization of matrix proteins. Comptes Rendus Pale 3: 549-562.
61. Otsu N. 1979. A threshold selection method from gray-level histograms. IEEE Transactions on Systems, Man, and Cybernetics 9: 62-66.
62. Pagel M. 1999. Inferring the historical patterns of biological evolution. Nature 401: 877-884.
63. Pike TW. 2011. Using digital cameras to investigate animal colouration: estimating sensor sensitivity functions. Behavioral Ecology and Sociobiology 65: 849-858.
64. Poole HK. 1965. Spectrophotometric identification of eggshell pigments and timing of superficial pigment deposition in the Japanese quail. (302M). Proceedings of the Society for Experimental Biology and Medicine 119: 547-551.
65. Purcell R, Hall LS, Corado R. 2008. Egg and nest. Cambridge, MA: Harvard University Press.
66. Rambaut A. 2002. Se-Al v.2.0a11: sequence alignment program. Available at:.
67. Rambaut A, Drummond A. 2007. Tracer v.1.3. Available at:.
68. Reynolds SJ, Martin GR, Cassey P. 2009. Is sexual selection blurring the functional significance of eggshell coloration hypotheses? Animal Behaviour 78: 209-215.
69. Ricklefs RE. 1968. Patterns of growth in birds. Ibis 110: 419-451.
70. Riehl C. 2011. Paternal investment and the 'sexually selected hypothesis' for the evolution of eggshell coloration: revisiting the assumptions. The Auk 128: 175-179.
71. Russell DGD, White J, Maurer G, Cassey P. 2010. Data-poor egg collections: tapping an important research resource. Journal of Afrotropical Zoology Special Issue: 77-82.
72. Sorby HC. 1875. On the colouring-matters of the shells of birds' eggs. Proceedings of the Zoological Society of London 23: 351-365.
73. Sparks NHC. 2011. Eggshell pigments from formation to deposition. Avian Biology Research 4: 162-167.
74. Starling M, Heinsohn R, Cockburn A, Langmore NE. 2006. Cryptic gentes revealed in pallid cuckoos Cuculus pallidus using reflectance spectrophotometry. Proceedings of the Royal Society of London, Series B: Biological Sciences 273: 1929-1934.
75. Stevens M, Parraga CA, Cuthill IC, Partridge JC, Troscianko TS. 2007. Using digital photography to study animal coloration. Biological Journal of the Linnean Society 90: 211-237.
76. Thomas GH. 2008. Phylogenetic distributions of British birds of conservation concern. Proceedings of the Royal Society of London, Series B: Biological Sciences 275: 2077-2083.
77. Tinbergen N, Broekhuysen GJ, Feekes F, Houghton JCW, Kruuk H, Szulc E. 1962. Egg shell removal by the black-headed gull, Larus ridibundus L.; a behaviour component of camouflage. Behaviour 19: 74-116.
78. Underwood TJ, Sealy SG. 2002. Adaptive significance of egg colouration. In: Deeming DC, ed. Avian incubation: behaviour, environment and evolution. Oxford: Oxford University Press, 280-298.
79. Wallace AR. 1889. Darwinism: an exposition of the theory of natural selection with some of its applications. London: Macmillan.
80. Walters LA, Getty T. 2010. Are brighter eggs better? Egg color and parental investment by House Wrens. Journal of Field Ornithology 81: 155-166.
81. Wang XT, Deng XM, Zhao CJ, Li JY, Xu GY, Lian LS, Wu CX. 2007. Study of the deposition process of eggshell pigments using an improved dissolution method. Poultry Science 86: 2236-2238.
82. Wang XT, Zhao CJ, Li JY, Xu GY, Lian LS, Wu CX, Deng XM. 2009. Comparison of the total amount of eggshell pigments in Dongxiang brown-shelled eggs and Dongxiang blue-shelled eggs. Poultry Science 88: 1735-1739.
83. Wang ZP, Liu RF, Wang AR, Li JY, Deng XM. 2011. Expression and activity analysis reveal that heme oxygenase (decycling) 1 is associated with blue egg formation. Poultry Science 90: 836-841.
84. Weidinger K. 2001. Does egg colour affect predation rate on open passerine nests? Behavioral Ecology and Sociobiology 49: 456-464.
85. Wyszecki G, Stiles WS. 1982. Color science. New York: John Wiley & Sons.
86. Zimmerman K, Hipfner JM. 2007. Egg size, eggshell porosity, and incubation period in the marine bird family Alcidae. Auk 124: 307-315.