Conspicuous eggs and colourful hypotheses: Testing the role of multiple influences on avian eggshell appearance

Avian Biology Research

Volumn 4, Issue 4, 2011, Pages 185-195

  Cassey, Phillip ^a   Maurer, Golo ^a   Lovell, P George ^b   Hanley, Daniel ^c  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c UNIVERSITY OF GUELPH   (Canada)

Author keywords

Eggshell colour; Maculation; Pigments; Porphyrins; Reproductive ecology

Indexed keywords

BIRD; CHICKEN; CHLAMYDERA LAUTERBACHI; DUMETELLA CAROLINENSIS; EGG SHELL; EMBRYO DEVELOPMENT; GUIRA GUIRA; NONHUMAN; PARADISEA APODA; PIGMENTATION; REVIEW; SPECTROPHOTOMETER; TINAMOTIS PENTLANDII; ULTRAVIOLET B RADIATION;

AVES;

EID: 84855529156     PISSN: 17581559     EISSN: None     Source Type: Journal    
DOI: 10.3184/175815511X13207699868421     Document Type: Review

References (104)

1. Akins, J.M., Hooper, M.J., Miller, H. and Woods, J.S. (1993) Porphyrin profiles in the nestling European starling (Sturnus vulgaris) - a potential biomarker of field contaminant exposure. J. Toxicol. Env. Health, 40, 47-59. (Pubitemid 23285897)
2. Arendt, W.J. (2004) A quarter century of variation in color and allometric characteristics of eggs from a rain forest population of the Pearly-eyed Thrasher (Margarops fuscatus). Caribb. J. Sci., 40, 204-217.
3. Avilés, J.M., Stokke, B.G., Moksnes, A., Røskaft, E. and Møller, A.P. (2006) Nest predation and the evolution of egg appearance in passerine birds in Europe and North America. Evol. Ecol. Res., 8, 493-513.
4. Avilés, J.M., Stokke, B.G., Moksnes, A., Røskaft, E. and Møller, A.P. (2007) Environmental conditions influence egg color of reed warblers Acrocephalus scirpaceus and their parasite, the common cuckoo Cuculus canorus. Behav. Ecol. Sociobiol., 61, 475-485.
5. Baicich, P.J. and Harrison, C.J.O. (1997) A guide to the nests, eggs, and nestlings of North American birds, 2nd edn. Academic Press, San Diego.
6. Bakken, G.S., Vanderbilt, V.C., Buttemer, W.A. and Dawson, W.R. (1978) Avian eggs - thermoregulatory value of very high near-IR reflectance. Science, 200, 321-323. (Pubitemid 8326062)
7. Bandaranayake, W.M. (2006) The nature and role of pigments of marine invertebrates. Nat. Product Rep., 23, 223-255.
8. Berg, E.C., McCormack, J.E. and Smith, T.B. (2009) Test of an adaptive hypothesis for egg speckling along an elevational gradient in a population of Mexican jays Aphelocoma ultramarina. J. Avian Biol., 40, 448-452.
9. Bertram, B.C.R. (1979) Ostriches recognise their own eggs and discard others. Nature, 279, 233-234.
10. Blumthaler, M., Ambach, W. and Ellinger, R. (1997) Increase in solar UV radiation with altitude. J. Photochem. Photobiol., B39, 130-134. (Pubitemid 27289157)
11. Bosque, C. and Bosque, M.T. (1995) Nest predation as a selective factor in the evolution of developmental rates in altricial birds. Am. Nat., 145, 234-260.
12. Buschmann, J.-U.F., Manns, M. and Güntürkün, O. (2006) "Let There be Light!" pigeon eggs are regularly exposed to light during breeding. Behav. Proc., 73, 62-67. (Pubitemid 43766291)
13. Casini, S., Fossi, M.C., Leonzio, C. and Renzoni, A. (2003) Review: Porphyrins as biomarkers for hazard assessment of bird populations: Destructive and non-destructive use. Ecotoxicology, 12, 297-305. (Pubitemid 36398838)
14. Cassey, P. (2009) Seeing colours in the dark. Curr. Biol., 19, 1083-1084.
15. Cassey, P., Portugal, S.J.P., Maurer, G., Ewen, J.G., Boulton, R.L., Hauber, M.E. and Blackburn, T.M. (2010) Variability in avian eggshell colour: A comparative study of museum eggshells. PLoS one, 5, e12054.
16. Cherry, M.I. and Bennett, A.T.D. (2001) Egg colour matching in an African cuckoo, as revealed by UV-visible reflectance spectrophotometry. Proc. R. Soc. B, 268, 565-571. (Pubitemid 32269844)
17. Cherry, M.I. and Gosler, A.G. (2010) Avian eggshell colouration: new perspectives on adaptive explanations. Biol. J. Linn. Soc., 100, 753-762.
18. Coleman, M.A. and Mc\nab, R.A. (1975) Photo acceleration of development in depigmented Japanese quail eggs. Poult. Sci., 54, 1849-1855.
19. Comfort, A. (1951) The pigmentation of molluscan shells. Biol. Rev., 26, 285-301.
20. Conry, P.J. (1988) High nest predation by brown tree snakes on Guam. Condor, 90, 478-482.
21. Davies, N.B. (2000) Cuckoos, Cowbirds and Other Cheats. T. &A. D. Poyser, London.
22. Davies, N.B. and Brooke, M.D.L. (1989) An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. I. host egg discrimination. J. Anim. Ecol., 58, 207-224. (Pubitemid 19325334)
23. De Gruijl, F.R., Van Kranen, H.J. and Mullenders, L.H.F. (2001) UV-induced DNA damage, repair, mutations and oncogenic pathways in skin cancer. J. Photochem. Photobiol., B63, 19-27. (Pubitemid 33040719)
24. Deeming, D.C. (2002) Behaviour patterns during incubation. In: Deeming, D.C. (ed.), Avian incubation:behaviour, environment and evolution, pp. 63-87. Oxford University Press,
25. Deeming, D.C. (2006) Ultrastructural and functional morphology of eggshells supports the idea that dinosaur eggs were incubated buried in a substrate. Palaeontology, 49, 171-185.
26. Deeming, D.C. (2011) A review of the relationship between eggshell colour and water vapour conductance. Avian Biol. Res., 4, 224-230.
27. Endler, J.A. and Mielke, P.W. (2005) Comparing entire colour patterns as birds see them. Biol. J. Linn. Soc., 86, 405-431. (Pubitemid 41783968)
28. Fischer, H. and Kögl, F. (1923) Zur Kenntnis der natürlichen Porphyrine IV. Über das Ooporphyrin. Zeit. Physiol. Chemie, 131, 241-261.
29. Gorchein, A., Lim, C.K. and Cassey, P. (2009) Extraction and analysis of colourful eggshell pigments using HPLC and HPLC/electrospray ionization tandem mass spectrometry. Biomed. Chromatography, 23, 602-606.
30. Gosler, A.G., Oliver, R., Connor, O.R. and Bonser, R.H.C. (2011) Protoporphyrin and eggshell strength: preliminary findings from a passerine bird. Avian Biol. Res., 4, 214-223.
31. Gosler, A.G., Higham, J. and Reynolds, S.J. (2005) Why are birds' eggs speckled? Ecol. Lett., 8, 1105-1113. (Pubitemid 41345841)
32. Götmark, F. (1992) Blue eggs do not reduce nest predation in the song thrush, Turdus philomelos. Beh. Ecol. Sociobiol., 30, 245-252.
33. Hanley, D. and Doucet, S. (2009) Egg colouration in ring-billed gulls (Larus delawarensis): a test of the sexual signaling hypothesis. Beh. Ecol. Sociobiol., 63, 719-729.
34. Hanley, D., Doucet, S. and Dearborn, D.C. (2010) A blackmail hypothesis for the evolution of conspicuous egg colouration in birds. Auk, 127, 453-459.
35. Hart, N.S. and Hunt, D.M. (2007) Avian visual pigments: characteristics, spectral tuning, and evolution. Am. Nat., 169, S7-S26. (Pubitemid 46094996)
36. Hobson, K.A. (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia, 120, 314-326.
37. Ishikawa, S., Suzuki, K., Fukuda, E., Arihara, K., Yamamoto, Y., Mukai, T. and Itoh, M. (2010) Photodynamic antimicrobial activity of avian eggshell pigments. FEBS Lett., 584, 770-774.
38. Jagannath, A., Shore, R.F., Walker, L.A., Ferns, P.N. and Gosler, A.G. (2008) Eggshell pigmentation indicates pesticide contamination. J. Appl. Ecol., 45, 133-140.
39. Kelber, A., Vorobyev, M. and Osorio, D. (2003) Animal colour vision: behavioural tests and physiological concepts. Biol. Rev., 78, 81-118. (Pubitemid 36253947)
40. Kelly, S.T. and Decapita, M.E. (1982) Cowbird control and its effect on kirtland's warbler reproductive success. Wilson Bull., 94, 363-365.
41. Kennedy, G.Y. and Vevers, H.G. (1976) A survey of avian eggshell pigments. Comp. Biochem. Physiol., B55, 117-123.
42. Kennedy, S.W., Fox, G.A., Trudeau, S., Bastien, L.J. and Jones, S.P. (1998) Highly carboxylated porphyrin concentration: a biochemical marker of PCB exposure in herring gulls. Mar. Environ. Res., 46, 65-69. (Pubitemid 28434801)
43. Kilner, R.M. (2006) The evolution of egg colour and patterning in birds. Biol. Rev., 81, 383-406.
44. Lack, D. (1958) The significance of the colour of turdine eggs. Ibis, 100, 145-166.
45. Lahti, D.C. (2008) Population differentiation and rapid evolution of egg color in accordance with solar radiation. Auk, 125, 796-802.
46. Lang, M.R. and Wells, J.W. (1987) A review of eggshell pigmentation. World's Poult. Sci. J., 43, 238-246.
47. Langmore, N.E., Stevens, M., Maurer, G., Heinsohn, R., Hall, M.L., Peters, A. and Kilner, R.M. (2011) Visual mimicry of host nestlings by cuckoos. Proc. R. Soc. B, Biol. Sci., 278, 2455-2463.
48. Lauber, J.K. (1975) Photoacceleration of avian embryogenesis. Comp. Biochem. Physiol., A51, 903-907.
49. Lemberg, R. (1934) Bile pigments. VI. Biliverdin, uteroverdin and oocyan. Biochem. J., 28, 978-987.
50. Liebermann, C. (1878) Ueber die Färbungen der Vogeleierschalen. Ber. Deutsch. Chem. Ges., 11, 606-610.
51. Lopez-Rull, I., Mikšík, I. and Gil, D. (2008) Egg pigmentation reflects female and egg quality in the spotless starling Sturnus unicolor. Beh. Ecol. Sociobiol., 62, 1877-1884.
52. Lovell, P.G., Tolhurst, D.J., Párraga, C.A., Baddeley, R., Leonards, U., Troscianko, J. and Troscianko, T. (2005) Stability of the color-opponent signals under changes of illuminant in natural scenes. J. Opt. Soc. Am., A22, 2060-2071. (Pubitemid 41715818)
53. Magige, F., Moe, B. and Røskaft, E. (2008) The white colour of the Ostrich (Struthio camelus) egg is a trade-off between predation and overheating. J. Orn., 149, 323-328.
54. Magrath, R. (1990) Hatching asynchrony in altricial birds. Biol. Rev., 65, 587-622.
55. Martin, T.E. and Ghalambor, C.K. (1999) Males feeding females during incubation. I. Required by microclimate or constrained by nest predation? Am. Nat., 153, 131-139. (Pubitemid 29284830)
56. Mateo, R., Beyer, W.N., Spann, J.W., Hoffman, D.J. and Ramis, A. (2003) Relationship between oxidative stress, pathology, and behavioral signs of lead poisoning in mallards. J. Toxicol. Env. Health, 66, 1371-1389. (Pubitemid 36918672)
57. Mateo, R., Castells, G., Green, A.J., Godoy, C. and Cristofol, C. (2004) Determination of porphyrins and biliverdin in bile and excreta of birds by a single liquid chromatography-UV detection analysis. J. Chromatography B, 810, 305-311. (Pubitemid 39243319)
58. Maurer, G. (2008) Who cares? Males provide most parental care in a monogamous nesting cuckoo. Ethology, 114, 540-547.
59. Maurer, G., Portugal, S.J. and Cassey, P. (2011a) An embryo's eye view of avian eggshell pigmentation. J. Avian Biol., doi:10.1111/j.1600-0587.2011. 05368.x.
60. Maurer, G., Portugal, S.J. and Cassey, P. (2011b) Speckles of cryptic black headed gull eggs show no mechanical or conductance structural function. J. Zool., doi:10.1111/j.1469-7998.2011.00830.x.
61. Mcaldowie, A.M. (1886) Observations on the development and the decay of the pigment layer on birds' eggs. J. Anat. Physiol., 20, 225-237.
62. Mikšík, I., Holán, V. and Deyl, Z. (1996) Avian eggshell pigments and their variability. Comp. Biochem. Physiol., B113, 607-612. (Pubitemid 26135427)
63. Mikšík, I., Holán, V. and Deyl, Z. (1994) Quantification and variability of eggshell pigment content. Comp. Biochem. Physiol., A109, 769-772. (Pubitemid 24335348)
64. Morales, J., Kim, S.-Y., Lobato, E., Merino, S., Tomás, G., Martínez-De La Puente, J. and Moreno, J. (2010a) On the heritability of blue-green eggshell colouration. J. Evol. Biol., 23, 1783-1791.
65. Morales, J., Torres, R. and Velando, A. (2010b) Parental conflict and blue egg colouration in a seabird. Naturwissenschaften, 97, 173-180.
66. Morales, J., Velando, A. and Moreno, J. (2008) Pigment allocation to eggs decreases plasma antioxidants in a songbird. Beh. Ecol. Sociobiol., 63, 227-233.
67. Morales, J., Velando, A. and Torres, R. (2011) Biliverdin-based egg colouration is enhanced by carotenoid supplementation. Beh. Ecol. Sociobiol., 65, 197-203.
68. Moreno, J., Lobato, E., Morales, J., Merino, S., Tomás, G., Martínez-De La Puente, J., Sanz, J.J., Mateo, R. and Soler, J.J. (2006) Experimental evidence that egg color indicates female condition at laying in a songbird. Behav. Ecol., 17, 651-655. (Pubitemid 43992434)
69. Moreno, J. and Osorno, J.L. (2003) Avian egg colour and sexual selection: does eggshell pigmentation reflect female condition and genetic quality? Ecol. Lett., 6, 803-806. (Pubitemid 37105908)
70. Olson, C.R., Vleck, C.M. and Vleck, D. (2006) Periodic cooling of bird eggs reduces embryonic growth efficiency. Physiol. Biochem. Zool., 79, 927-936. (Pubitemid 44412216)
71. Parsons, J. (1970) Relationship between egg size and posthatching chick mortality in the Herring Gull (Larus argentatus). Nature, 228, 1221-1222.
72. Patent, D.H. (1977) Reptiles and how they reproduce. Holiday House Inc., New York.
73. Pike, T.W. (2011) Using digital cameras to investigate animal colouration: estimating sensor sensitivity functions. Beh. Ecol. Sociobiol., 65, 849-858.
74. Pounds, J.A., Fogden, M.P.L. and Campbell, J.H. (1999) Biological response to climate change on a tropical mountain. Nature, 398, 611-615. (Pubitemid 29183687)
75. Ratcliffe, D.A. (1967) Decrease in eggshell weight in certain birds of prey. Nature, 215, 208-210.
76. Reynolds, S.J., Martin, G.R. and Cassey, P. (2009) Is sexual selection blurring the functional significance of eggshell colouration hypotheses? Anim. Behav., 78, 209-215.
77. Riehl, C. (2011) Paternal investment and the 'sexually selected hypothesis' for the evolution of eggshell coloration: revisiting the assumptions. Auk, 128, 175-179.
78. Rozenboim, I., Biran, I., Uni, Z., Robinzon, B. and Halevy, O. (1999) The effect of monochromatic light on broiler growth and development. Poult. Sci., 78, 135-138. (Pubitemid 129554732)
79. Sanz, J.J. and García-Navas, V. (2009) Eggshell pigmentation pattern in relation to breeding performance of blue tits Cyanistes caeruleus. J. Anim. Ecol., 78, 31-41.
80. Schönwetter, M. (1960-1992) Handbuch der Oologie. Akademie Verlag.
81. Shafey, T.M., Al-Batshan, H.A., Ghannam, M.M. and Al-Ayed, M.S. (2005) Effect of intensity of eggshell pigment and illuminated incubation on hatchability of brown eggs. Brit. Poult. Sci., 46, 190-198. (Pubitemid 40764352)
82. Shafey, T.M. and Al-Mohsen, T.H. (2002) Embryonic growth, hatching time and hatchability performance of meat breeder eggs incubated under continuous green light. Asian -Austr. J. Anim. Sci., 15, 1702-1707. (Pubitemid 35419931)
83. Shafey, T.M., Al-Mohsen, T.H., Al-Sobayel, A.A., Alhassan, M.J. and Ghannam, M.M. (2002) Effects of eggshell pigmentation and egg size on the spectral properties and characteristics of eggshell of meat and layer breeder eggs. Asian-Austr. J. Anim. Sci., 15, 297-302. (Pubitemid 35003066)
84. Shafey, T.M., Ghannam, M.M., Al-Batshan, H.A. and Al-Ayed, M.S. (2004) Effect of pigment intensity and region of eggshell on the spectral transmission of light that passes the eggshell of chickens. Int. J. Poult. Sci., 3, 228-233.
85. Siefferman, L., Navara, K. and Hill, G. (2006) Egg colouration is correlated with female condition in eastern bluebirds (Sialia sialis). Beh. Ecol. Sociobiol., 59, 651-656. (Pubitemid 43209140)
86. Skutch, A.F. (1976) Parent birds and their young. University of Texas Press.
87. Soler, J.J., Moreno, J., Avilés, J.M. and Møller, A.P. (2005) Blue and green egg-color intensity is associated with parental effort and mating system in passerines: Support for the sexual selection hypothesis. Evolution, 59, 636-644. (Pubitemid 40441329)
88. Sorby, H.C. (1875) On the colouring-matters of the shells of birds' eggs. Proc. Zool. Soc. Lond., 23, 351-365.
89. Stevens, M., Parraga, C.A., Cuthill, I.C., Partridge, J.C. and Troscianko, T.S. (2007) Using digital photography to study animal colouration. Biol. J. Linn. Soc., 90, 211-237. (Pubitemid 46192765)
90. Stoddard, M.C. and Stevens, M. (2010) Pattern mimicry of host eggs by the common cuckoo, as seen through a bird's eye. Proc. R. Soc. B, 277, 1387-1393.
91. Stokke, B.G., Moksnes, A. and Røskaft, E. (2002) Obligate brood parasites as selective agents for evolution of egg appearance in passerine birds. Evolution, 56, 199-205. (Pubitemid 34243811)
92. Tschanz, B. (1959) Zur Brutbiologie der Trottellumme (Uria aalge aalge Pont.). Behaviour, 14, 1-100.
93. Underwood, T.J. and Sealy, S.G. (2002) Adaptive significance of egg colouration. In: Deeming, D.C. (ed.), Avian incubation: behaviour, environment and evolution, pp. 280-298. Oxford University Press.
94. Verbeek, N.A.M. (1988) Differential predation of eggs in clutches of Glaucous-winged Gulls Larus glaucescens. Ibis, 130, 512-518.
95. Veterany, L., Hluchy, S. and Veteranyova, A. (2004) The influence of ultra-violet radiation on chicken hatching. J. Env. Sci. Health, A39, 2333-2339. (Pubitemid 39244861)
96. Vorobyev, M. and Osorio, D. (1998) Receptor noise as a determinant of colour thresholds. Proc. R. Soc. B, 265, 351-358. (Pubitemid 28111918)
97. Wallace, A.R. (1889) Darwinism: An exposition of the theory of natural selection with some of its applications. Macmillan, London.
98. Wang, X.T., Zhao, C.J., Li, J.Y., Xu, G.Y., Lian, L.S.,Wu, C.X. and Deng, X.M. (2009) Comparison of the total amount of eggshell pigments in Dongxiang brown-shelled eggs and Dongxiang blue-shelled eggs. Poult. Sci., 88, 1735-39.
99. Wang, Z.P., Liu, R.F., Wang, A.R., Li, J.Y. and Deng, X.M. (2011) Expression and activity analysis reveal that heme oxygenase (decycling) 1 is associated with blue egg formation. Poult. Sci., 90, 836-841.
100. Weidinger, K. (2001) Does egg colour affect predation rate on open passerine nests? Beh. Ecol. Sociobiol., 49, 456-464.
101. Weidinger, K. (2004) Relative effects of nest size and site on the risk of predation in open nesting passerines. J. Avian Biol., 35, 515-523.
102. Westmoreland, D. and Best, L.B. (1986) Incubation continuity and the advantage of cryptic egg colouration to Mourning Doves. Wilson Bull., 98, 297-300
103. Westmoreland, D. and Kiltie, R.A. (1996) Egg crypsis and clutch survival in three species of blackbirds (Icteridae). Biol. J. Linn. Soc., 58, 159-172. (Pubitemid 126564384)
104. Westmoreland, D. and Kiltie, R.A. (2007) Egg colouration and selection for crypsis in open-nesting blackbirds. J. Avian Biol., 38, 682-689. (Pubitemid 350132053)