Eggshell coloration in relation to male ornamentation, female condition and egg quality in the collared flycatcher Ficedula albicollis

Journal of Avian Biology

Volumn 39, Issue 4, 2008, Pages 413-422

  Hargitai, Rita ^a   Herényi, Márton ^a   Torok, János ^a  

^a EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

CLUTCH SIZE; COLOR; EGG; EGGSHELL; FEMALE BEHAVIOR; LAYING DATE; MALE BEHAVIOR; ORNAMENTATION; PASSERINE; PIGMENT;

FICEDULA ALBICOLLIS;

EID: 64549120321     PISSN: 09088857     EISSN: 1600048X     Source Type: Journal    
DOI: 10.1111/j.2008.0908-8857.04337.x     Document Type: Article

References (92)

1. Afonso, S., Vanore, G. and Batik, A. 1999. Protoporphyrin IX and oxidative stress. - Free Radic. Res. 31: 161-170.
2. Asad, S. K. Singh, S., Ahmad, A., Khan, N. U. and Hadi, S. M. 2001. Prooxidant and antioxidant activities of bilirubin and its metabolic precursor biliverdin: a structure-activity study. - Chem. Biol. Interact. 137: 59-74.
3. Biard, C., Surai, P. F. and Møller, A. P. 2005. Effects of carotenoid availability during laying on reproduction in the blue tit. - Oecologia 144: 32-44.
4. Blount, J. D., Houston, D. C. and Møller, A. P. 2000. Why egg yolk is yellow. - Trends. Ecol. Evol. 15: 47-49.
5. Blount, J. D., Surai, P. F., Nager, R. G., Houston, D. C., Møller, A. P., Trewby, M. L. and Kennedy, M. W. 2002. Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. - Proc. R. Soc. B 269: 29-36.
6. Britton, G. 1995- UV/Visible spectroscopy. - In: Britton, G., Liaaen-Jensen, S. and Pfander, H. (eds). Carotenoids: spectroscopy. Birkhauser Verlag, Basel, pp. 13-63.
7. Bureš, S. and Weidinger, K. 2003. Sources and timing of calcium intake during reproduction in flycatchers. - Oecologia 137: 634-647.
8. Burley, N. 1986. Sexual selection for aesthetic traits in species with biparenal care. -Am. Nat. 127: 415-445.
9. Cuthill, I. C., Partridge, J. C., Bennett, A. T. D., Church, S. C., Hart, N. S. and Hunt, S. 2000. Ultraviolet vision in birds. -Adv. Study Behav. 29: 159-214.
10. Daan, S., Dijkstra, C., Drent, R. and Meijer, T. 1988. Food supply and the annual timing of avian reproduction. - In: Ouellet, H. (ed.). Acta XIX Congr. Internat. Ornithol. Natl. Mus. Natural Sci., Ottawa, pp. 392-407.
11. Dabrosin, C., Hammar, C. and Ollinger, K. 1998. Impact of oestradiol and progesterone on antioxidant activity in normal human breast epithelial cells in culture. - Free Rad. Res. 28: 241-249.
12. Edge, R., McGarvey, D. J. and Truscott, T. G. 1997. The carotenoids as anti-oxidants - a review. - J. Photochem. Photobiol. 41B: 189-200.
13. Falchuk, K. H., Contin, J. M., Dziedzic, T. S., Feng, Z. L., French, T. C., Heffron, G. J. and Montorzi, M. 2002. A role for biliverdin IX alpha in dorsal axis development of Xenopus laevis embryos. - Proc. Natl. Acad. Sci. USA 99: 251-256.
14. Folstad, I. and Karter, A. J. 1992. Parasites, bright males, and the immunocompetence handicap. -Am. Nat. 139: 603-622.
15. Garamszegi, L. Z., Rosivall, B., Hegyi, G., Szöllösi, E., Török, J. and Eens, M. 2006. Determinants of male territorial behavior in a Hungarian collared flycatcher population: roles for plumage traits of residents and challengers. - Behav. Ecol. Sociobiol. 60: 663-671.
16. Garamszegi, L. Z., Török, J., Tóth, L. and Michl, G. 2004. The effect of timing and female quality on clutch size in the collared flycatcher Ficedula albicollis. - Bird Study 51: 270-277.
17. Gosler, A. G., Higham, J. P. and Reynolds, S. J. 2005. Why are birds' eggs speckled? - Ecol. Lett. 8: 1105-1113.
18. Gotmark, F. 1992. Blue eggs do not reduce nest predation in the song thrush, Turdus philomelos. - Behav. Ecol. Sociobiol. 30: 245-252.
19. Grindstaff, J. L., Brodie, E. D., III and Ketterson, E. D. 2003. Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. - Proc. R. Soc. B 270: 2309-2319.
20. Gustafsson, L., Nordling, D., Andersson, M. S., Sheldon, B. C. and Qyarnström, A. 1994. Infectious diseases, reproductive effort and the cost of reproduction in birds. - Phil. Trans. R. Soc. B 346: 323-331.
21. Gustafsson, L., Qyarnström, A. and Sheldon, B. C. 1995- Tradeoffs between life history traits and a secondary sexual character in male collared flycatchers. - Nature 375: 311-313.
22. Hammond, R. W., Olson, D. M., Frenkel, R. B., Biellier, H. V. and Hertelendy, F. 1980. Prostaglandins and steroid hormones in plasma and ovarian follicles during the ovulation cycle of the domestic hen (Gallus domesticus). - Gen. Comp. Endocrinol. 42: 195-202.
23. Haq, A., Bailey, C. A. and Chinnah, A. 1996. Effect of β-carotene, canthaxanthin, lutein, and Vitamin E on neonatal immunity of chicks when supplemented in the broiler breeder diet. - Poultry Sci. 75: 1092-1097.
24. Hargitai, R., Matus, Z., Hegyi, G., Michl, G., Tóth, Gy. and Török, J. 2006b. Antioxidants in the egg yolk of a wild passerine: differences between breeding seasons. - Comp. Biochem. Physiol. 143B: 145-152.
25. Hargitai, R., Prechl, J. and Török, J. 2006a. Maternal immunoglobulin concentration in collared flycatcher (Ficedula albicollis) eggs in relation to parental quality and laying order. - Funct. Ecol. 20: 829-838.
26. Hargitai, R., Török, J., Toth, L., Hegyi, G., Rosivall, B., Szigeti, B. and Szöllösi, E. 2005. Effects of environmental conditions and parental quality on the inter- and intraclutch egg size variation in the collared flycatcher (Ficedula albicollis). - Auk 122: 509-522.
27. Harrison, G. J. and Harrison, L. R. 1986. Clinical avian medicine and surgery. - W. B. Saunders, London.
28. Hegyi, G., Rosivall, B., Garamszegi, L. Z., Szöllösi, E., Hargitai, R., Eens, M. and Török, J. 2008. Phenotypic plasticity in a female plumage colour: information content and mating patterns. - Anim. Behav. 75: 977-989.
29. Hegyi, G., Rosivall, B., Szöllösi, E., Hargitai, R., Eens, M. and Török, J. 2007. A role for female ornamentation in a facultatively polygynous mating system. - Behav. Ecol. 18: 1116-1122.
30. Hegyi, G., Török, J. and Tóth, L. 2002. Qualitative population divergence in proximate determination of a sexually selected trait in the collared flycatcher. -J. Evol. Biol. 15: 710-719.
31. Hegyi, G., Török, J., Tóth, L., Garamszegi, L. Z. and Rosivall, B. 2006. Rapid temporal change in the expression and age-related information content of a sexually selected trait. - J. Evol. Biol. 19: 228-238.
32. Hoi-Leitner, M., Romero-Pujante, M., Hoi, H. and Pavlova, A. 2001. Food availability and immune capacity in serin (Serinus serinus) nestlings. - Behav. Ecol. Sociobiol. 49: 333-339.
33. Hoyt, D. F. 1979. Practical methods of estimating volume and fresh weight of bird eggs. - Auk 96: 73-77.
34. Hudson, M. F. and Smith, K. M. 1975. Bile pigments. - Chem. Soc. Rev. 4: 363-399.
35. Kaur, H., Hughes, M. N., Green, C. J., Naughton, P., Foresti, R. and Motterlini, R. 2003. Interactions of bilirubin and biliverdin with reactive nitrogen species. - FEBS Lett. 543: 113-119.
36. Kennedy, G. Y. and Vevers, H. G. 1976. A survey of avian eggshell pigments. - Comp. Biochem. Physiol. 55B: 117-123.
37. Kilner, R. M. 2006. The evolution of egg colour and patterning in birds. - Biol. Rev. 81: 383-406.
38. Kim, C.-H., Yamagishi, S. and Won, P.-O. 1995. Egg-color dimorphism and breeding success in the crow tit (Paradoxornis webbiana). -Auk 112: 831-839.
39. Krist, M. and Grim, T. 2007. Are blue eggs a sexually selected signal of female collared flycatchers? A cross-fostering experiment. - Behav. Ecol. Sociobiol. 61: 863-876.
40. Lack, D. 1958. The significance of the colour of turdine eggs. - Ibis 100: 145-166.
41. Löhrl, H. 1976. Studies of less familiar birds. Collared flycatcher. - Brit. Birds 69: 20-26.
42. McDonagh, A. F. 2001. Turning green to gold. - Nat. Struct. Biol. 8: 198-200.
43. McGraw, K. J., Adkins-Regan, E. and Parker, R. S. 2005. Maternally derived carotenoid pigments affect offspring survival, sex ratio, and sexual attractiveness in a colourful songbird. - Naturwiss. 92: 375-380.
44. McPhee, F., Caldera, P. S., Bemis, G. W., McDonagh, A. F., Kuntz, I. D. and Craik, C. S. 1996. Bile pigments as HIV-1 protease inhibitors and their effects on HIV-1 viral maturation and infectivity in vitro. - Biochem. J. 320: 681-686.
45. Merino, S. and Potti, J. 1998. Growth, nutrition and blowfly parasitism in nestling pied flycatchers. - Can. J. Zool. 76: 936-941.
46. Michl, G., Török, J., Griffith, S. C. and Sheldon, B. C. 2002. Experimental analysis of sperm competition mechanisms in a wild bird population. - Proc. Nad. Acad. Sci. USA 99: 5466-5470.
47. Michl, G., Török, J., Péczely, P., Garamszegi, L. Z. and Schwabl, H. 2005. Female collared flycatchers adjust yolk testosterone to male age, but not to attractiveness. - Behav. Ecol. 16: 383-388.
48. Mikšík, I., Holáň, V. and Deyl, Z. 1996. Avian eggshell pigments and their variability. - Comp. Biochem. Physiol. 113B: 607-612.
49. Morales, J., Sanz, J. J. and Moreno, J. 2006. Egg colour reflects the amount of yolk maternal antibodies and fledging success in a songbird. - Biol. Lett. 2:334-336.
50. Moreno, J., Lobato, E., Morales, J., Merino, S., Tomás, G., Martínez-de la Puente, J., Sanz, J. J., Mateo, R. and Soler, J. J. 2006b. Experimental evidence that egg color indicates female condition at egg laying in a songbird. - Behav. Ecol. 17: 651-655.
51. Moreno, J., Morales, J., Lobato, E., Merino, S., Tomás, G. and Martínez-de la Puente, J. 2005- Evidence for the signaling function of egg color in the pied flycatcher Ficedula hypoleuca. - Behav. Ecol. 16: 931-937.
52. Moreno, J., Morales, J., Lobato, E., Merino, S., Tomás, G. and Martinez-de la Puente, J. 2006a More colourful eggs induce higher relative paternal investment in the pied flycatcher Ficedula hypoleuca: a cross-fostering experiment. - J. Avian Biol. 37: 555-560.
53. 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.
54. Moreno, J., Osorno, J. L., Morales, J., Merino, S. and Tomás, G. 2004. Egg coloration and male parental effort in the pied flycatcher Ficedula hypoleuca. - J. Avian Biol. 35: 300-304.
55. Mousseau, T. A. and Fox, C. W. 1998. Maternal effects as adaptations. - Oxford University Press, Oxford.
56. Møller, A. P., Biard, C., Blount, J. D., Houston, D. C., Ninni, P., Saino, N. and Surai, P. F. 2000. Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? - Avian Poult. Biol. Rev. 11: 137-159.
57. Nakagami, T., Taji, S., Takahashi, M. and Yamanishi, K. 1992. Antiviral activity of a bile pigment, biliverdin, against human herpesvirus 6 (HHV-6) in vitro. - Microbiol. Immunol. 36: 381-390.
58. Navara, K. J., Badyaev, A. V., Mendonça, M. T. and Hill, G. E. 2006b. Yolk antioxidants vary with male attractiveness and female condition in the house finch (Carpodacus mexicanus). -Physiol. Biochem. Zool. 79: 1098-1105.
59. Navara, K. J., Hill, G. E. and Mendonça, M. T. 2006a. Yolk androgen deposition as a compensatory strategy. - Behav. Ecol. Sociobiol. 60: 382-398.
60. Olson, V. A. and Owens, I. P. F. 1998. Costly sexual signals: are carotenoids rare, risky or required? - Trends Ecol. Evol. 13: 510-514.
61. Oniki, Y. 1979. Nest-egg combinations: possible antipredatory adaptations in Amazonian birds. - Rev. Bras. Biol. 39: 747-767.
62. Oniki, Y. 1985. Why robin eggs are blue and birds build nests: statistical tests for Amazonian birds. - Orn. Monogr. 36: 536-545.
63. Partali, V., Liaaen-Jensen, S., Slagsvold, T. and Lifjeld, J. T. 1987. Carotenoids in food chain studies - II. The food chain of Parus spp. monitored by carotenoid analysis. - Comp. Biochem. Physiol. 87B: 885-888.
64. Patterson, R., Younger, J. S., Weigle, W. O. and Dixon, F. J. 1962. The metabolism of serum proteins in the hen and chick and secretion of serum proteins by the ovary of the hen. - J. Gen. Physiol. 45: 501-513.
65. Qyarnström, A. 1999. Genotype-by-environment interactions in the determination of the size of a secondary sexual character in the collared flycatcher (Ficedula albicollis). - Evolution 53: 1564-1572.
66. Rosivall, B., Szöllösi, E. and Török, J. 2005. Maternal compensation for hatching asynchrony in the collared flycatcher. - J. Avian Biol. 36: 531-537.
67. Ruff, M. D., Reid, W. M. and Johnson, J. K. 1974. Lowered blood carotenoid levels in chickens infected with coccidia. - Poultry Sci. 53: 1801-1809.
68. Saino, N., Bertacche, V., Ferrari, R. P., Martinelli, R., Møller, A. P. and Stradi, R. 2002. Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection, and paternal ornamentation. - Proc. R. Soc. B 269: 1729-1733.
69. Saino, N., Ferrari, R., Romano, M., Martinelli, R. and Møller, A. P. 2003. Experimental manipulation of egg carotenoids affects immunity of barn swallow nestlings. - Proc. R. Soc. B 270: 2485-2489.
70. Saino, N., Stradi, R., Ninni, P., Pini, E. and Møller, A. P. 1999. Carotenoid plasma concentration, immune profile, and plumage ornamentation of male barn swallows (Hirundo rustica). -Am. Nat. 154: 441-448.
71. Sheldon, B. C. 2000. Differential allocation: tests, mechanisms and implications. -Trends Ecol. Evol. 15: 397-402.
72. Sheldon, B. C. and Ellegren, H. 1999. Sexual selection resulting from extra-pair paternity in collared flycatchers. - Anim. Behav. 57: 285-298.
73. Siefferman, L., Navara, K. J. and Hill, G. E. 2006. Egg coloration is correlated with female condition in eastern bluebirds (Sialia sialis). - Behav. Ecol. Sociobiol. 59: 651-656.
74. Slagsvold, T., Sandvik, J., Rofstad, G., Lorentsen, O. and Husby, M. 1984. On the adaptive value of intra-clutch egg size variation in birds. -Auk 101: 685-697.
75. Soh, T. and Koga, O. 1994. The effects of sex steroid hormones on the pigment accumulation in the shell gland of Japanese quail. - Poultry Sci. 73: 179-185.
76. 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.
77. Stocker, R., Yamamaoto, Y., McDonagh, A. F., Glazer, A. N. and Ames, B. N. 1987. Bilirubin as an antioxidant of possible physiological importance. - Science 235: 1043-1046.
78. Surai, P. F., Noble, R. C. and Speake, B. K. 1996. Tissue specific differences in antioxidant distribution and susceptibility to lipid peroxidation during development of the chick embryo. - Biochim. Biophys. Acta 1304: 1-10.
79. Svensson, E. and Merilä, J. 1996. Molt and migratory condition in blue tits: a serological study. - Condor 98: 825-831.
80. Tilgar, V., Mänd, R. and Leivits, A. 1999. Effect of calcium availability and habitat quality on reproduction in pied flycatcher Ficedula hypoleuca and great tit Parus major. - J. Avian Biol. 30: 383-391.
81. Török, J. 1986. Food segregation in three hole-nesting bird species during the breeding season. - Ardea 74: 129-136.
82. Török, J. and Tóth, L. 1988. Density dependence in reproduction of the collared flycatcher (Ficedula albicollis) at high population levels. -J. Anim. Ecol. 57: 251-258.
83. Török, J., Hargitai, R., Hegyi, G., Matus, Z., Michl, G., Péczely, P., Rosivall, B. and Tóth, Gy. 2007. Carotenoids in the egg yolks of collared flycatchers (Ficedula albicollis) in relation to parental quality, environmental factors and laying order. - Behav. Ecol. Sociobiol. 61: 541-550.
84. Török, J., Hegyi, G. and Garamszegi, L. Z. 2003. Depigmented wing patch size is a condition-dependent indicator of viability in male collared flycatchers. - Behav. Ecol. 14: 382-388.
85. Underwood, T. J. and Sealy, S. G. 2002. Adaptive significance of egg coloration. - In: Deeming, D. C. (ed.). Avian incubation, behaviour, environment and evolution. Oxford University Press, Oxford, pp. 280-298.
86. Verhulst, S., Dieleman, S. J. and Parmentier, H. K. 1999. The tradeoff between immunocompetence and sexual ornamentation in domestic fowl. - Proc. Nad. Acad. Sci. USA 96: 4478-4481.
87. von Schantz, T., Bensch, S., Grahn, M., Hasselquist, D. and Wittzell, H. 1999. Good genes, oxidative stress and conditiondependent sexual signals. - Proc. R. Soc. B 266: 1-12.
88. Wassmann, K., Wassmann, S. and Nickenig, G. 2005. Progesterone antagonizes the vasoprotective effect of estrogen on antioxidant enzyme expression and function. - Circ. Res. 97: 1046-1054.
89. Weidinger, K. 2001. Does egg colour affect predation rate on open passerine nests? - Behav. Ecol. Sociobiol. 49: 456-464.
90. Williams, M., Krootjes, B. B., van Steveninck, J. and van der Zee, J. 1994. The pro- and antioxidant properties of protoporphyrin IX. - Biochim. Biophys. Acta 1211: 310-316.
91. Zahavi, A. 1975- Mate selection - a selection for a handicap. - J. Theor. Biol. 53: 205-214.
92. Zhao, R., Xu, G.-Y., Liu, Z.-Z., Li, J.-Y. and Yang, N. 2006. A study on eggshell pigmentation: biliverdin in blue-shelled chickens. - Poultry Sci. 85: 546-549.