Advertisement

Behavioral Ecology and Sociobiology

, Volume 70, Issue 12, pp 2093–2110 | Cite as

Biliverdin- and protoporphyrin-based eggshell pigmentation in relation to antioxidant supplementation, female characteristics and egg traits in the canary (Serinus canaria)

  • Rita Hargitai
  • Nóra Boross
  • Zoltán Nyiri
  • Zsuzsanna Eke
Original Article

Abstract

Avian eggs exhibit a large variability in coloration and patterns, which are produced by blue-green biliverdin and red-brown protoporphyrin pigments. Several hypotheses have been proposed to explain the function of eggshell coloration. In this experimental study, we tested two hypotheses (signalling-function hypothesis and structural-function hypothesis) on both eggshell pigment types in an open-nesting songbird, the canary (Serinus canaria). Also, we aimed to examine whether deposition of pigments into the eggshell has any cost in terms of the plasma oxidative status of the female. We found that eggshell average blue-green chroma was increased by antioxidant supplementation, although we note that there had already been a pre-existing bias in plasma antioxidant capacity between the supplemented and control groups. Eggshell average blue-green chroma was positively related to female body condition during egg laying. However, blue-green eggshell colour was not related to female oxidative status during or after the laying period, and blue-green chroma increased with laying order. Accordingly, we found some support for that eggshell blue-green colour could reflect maternal antioxidant availability and body condition, but did not find evidence that it has a cost for the female’s oxidative status. By contrast, eggshell spot brightness was positively related to body condition, suggesting that darker spotting reflected poorer nutritional condition in the canary. Eggshell blue-green pigmentation was not significantly connected to the egg volume or yolk antioxidant level, but we found that eggs with lower yolk antioxidant concentration had higher average eggshell brown chroma. In sum, our results suggest that eggshell colour reflected female antioxidant and nutrient availability. Finally, we found that eggs with thinner eggshells had a more aggregated spot distribution, supporting the view that aggregated spots may help to strengthen eggshells.

Significance statement

Avian eggs have a large variability in colours and patterns, which are due to two pigments: the blue-green biliverdin and the red-brown protoporphyrin. In this study, we tested whether eggshell pigmentation, measured by a spectrophotometer, could reflect female and egg quality in the canary, an open nesting songbird. We found that females supplemented with antioxidants before and during egg-laying laid more intense blue-green eggs. Females in better body condition laid eggs that had a more intense blue-green coloration, but lower intensity of brown coloration. Egg yolk antioxidant level was lower in eggs with more intense brown eggshell coloration. These results suggest that eggshell coloration could reflect the antioxidant and nutrient availability of females. Moreover, we found that eggs with thinner eggshells had a more aggregated spot distribution on the eggshell, supporting the view that aggregated brown pigment spots may help to strengthen eggshells.

Keywords

Eggshell colour Female condition Oxidative status Sexually selected eggshell coloration hypothesis Structural-function hypothesis Yolk antioxidants 

Notes

Acknowledgments

We are grateful to B. Puskás-Farkas for help in the animal care and laboratory analysis of egg yolk antioxidants. We thank A. Simões Souza and G. Dri for help with the animal care and I. Orbán for help in the eggshell pigment concentration analysis. We are grateful to J. Török and G. Nagy for their help in canary purchase. We are indebted to the valuable and constructive comments of D. Hanley and two anonymous reviewers.

Compliance with ethical standards

Funding statement

This study was supported by the Hungarian Scientific Research Fund (OTKA, grant no. PD100304) and the Bolyai János Research Fellowship (MTA) to RH. None of the funders had any input into the content of the manuscript. None of the funders required their approval of the manuscript before submission or publication.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The National Food Chain Safety Office (NÉBIH) provided permissions for this study (PEI/001/824–4/2015). All applicable international, national and institutional guidelines for the care and use of animals were followed.

Supplementary material

265_2016_2214_MOESM1_ESM.doc (30 kb)
ESM 1 (DOC 29 kb)
265_2016_2214_MOESM2_ESM.doc (28 kb)
ESM 2 (DOC 27 kb)
265_2016_2214_MOESM3_ESM.doc (30 kb)
ESM 3 (DOC 27 kb)
265_2016_2214_MOESM4_ESM.doc (26 kb)
ESM 4 (DOC 26 kb)
265_2016_2214_MOESM5_ESM.doc (38 kb)
ESM 5 (DOC 38 kb)

References

  1. Afonso S, Vanore G, Batlle A (1999) Protoporphyrin IX and oxidative stress. Free Radical Res 31:161–170Google Scholar
  2. Alan RR, McWilliams SR (2013) Oxidative stress, circulating antioxidants, and dietary preferences in songbirds. Comp Biochem Physiol B 164:185–193PubMedCrossRefGoogle Scholar
  3. Alvir JMJ (1993) Generating confidence in the SAS system: confidence intervals for commonly used procedures. In: Proceedings of the 18th Annual SAS Users Group International Conference. SAS Institute, Cary, NC, pp 1165–1168Google Scholar
  4. Anwar F, Latif S, Ashraf M (2006) Analytical characterization of hemp (Cannabis sativa) seed oil from different agro-ecological zones of Pakistan. J Am Oil Chem Soc 83:323–329CrossRefGoogle Scholar
  5. Avilés JM, Soler JJ, Hart NS (2011) Sexual selection based on egg colour: physiological models and egg discrimination experiments in a cavity-nesting bird. Behav Ecol Sociobiol 65:1721–1730CrossRefGoogle Scholar
  6. Bakken GS, Vanderbilt VC, Buttemer WA, Dawson WR (1978) Avian eggs: thermoregulatory value of very high near-infrared reflectance. Science 200:321–323PubMedCrossRefGoogle Scholar
  7. Bhatnagar AS, Gopala Krishna AG (2013) Natural antioxidants of the Jaffna variety of Moringa oleifera seed oil of Indian origin as compared to other vegetable oils. Grasas Aceites 64:537–545CrossRefGoogle Scholar
  8. Blount JD, Surai PF, Houston DC, Møller AP (2002) Patterns of yolk enrichment with dietary carotenoids in gulls: the roles of pigment acquisition and utilization. Funct Ecol 16:445–453CrossRefGoogle Scholar
  9. Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127PubMedCrossRefGoogle Scholar
  10. Blount JD, Vitikainen EI, Stott I, Cant MA (2016) Oxidative shielding and the cost of reproduction. Biol Rev 91:483–497Google Scholar
  11. Brulez K, Cassey P, Meeson A, Mikšík I, Webber SL, Gosler AG, Reynolds SJ (2014a) Eggshell spot scoring methods cannot be used as a reliable proxy to determine pigment quantity. J Avian Biol 45:94–102CrossRefGoogle Scholar
  12. Brulez K, Choudhary PK, Maurer G, Portugal SJ, Boulton RL, Webber SL, Cassey P (2014b) Visual scoring of eggshell patterns has poor repeatability. J Ornithol 155:701–706CrossRefGoogle Scholar
  13. Bulla M, Šálek M, Gosler AG (2012) Eggshell spotting does not predict male incubation but marks thinner areas of a shorebird’s shells. Auk 129:26–35CrossRefGoogle Scholar
  14. Bureš S, Weidinger K (2003) Sources and timing of calcium intake during reproduction in flycatchers. Oecologia 137:634–647PubMedCrossRefGoogle Scholar
  15. Butler MW, McGraw KJ (2013) Eggshell coloration reflects both yolk characteristics and dietary carotenoid history of female mallards. Funct Ecol 27:1176–1185CrossRefGoogle Scholar
  16. Butler MW, Waite HS (2016) Eggshell biliverdin concentration does not sufficiently predict eggshell coloration. J Avian Biol published online, doi: 10.5061/dryad.q2t70
  17. Cassey P (2009) Biological optics: seeing colours in the dark. Curr Biol 19:1083–1084CrossRefGoogle Scholar
  18. 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. Naturwissenschaften 95:713–721PubMedCrossRefGoogle Scholar
  19. Cassey P, Mikšík I, Portugal SJ, Maurer G, Ewen JG, Zarate E, Sewell MA, Karadas F, Grim T, Hauber ME (2012) Avian eggshell pigments are not consistently correlated with colour measurements or egg constituents in two Turdus thrushes. J Avian Biol 43:503–512CrossRefGoogle Scholar
  20. Collins EC (1993) Inheritance of egg-color polymorphism in the village weaver (Ploceus cucullatus). Auk 110:683–692CrossRefGoogle Scholar
  21. Costantini D (2016) Oxidative stress ecology and the d-ROMs test: facts, misfacts and an appraisal of a decade’s work. Behav Ecol Sociobiol 70:809–820CrossRefGoogle Scholar
  22. Dearborn DC, Hanley D, Ballantine K, Cullum J, Reeder DM (2012) Eggshell colour is more strongly affected by maternal identity than by dietary antioxidants in a captive poultry system. Funct Ecol 26:912–920CrossRefGoogle Scholar
  23. Deeming DC (2002) Avian incubation: behaviour, environment, and evolution. Oxford University Press, OxfordGoogle Scholar
  24. Dehnhard N, Pinxten R, Demongin L, Van Camp J, Eens M, Poisbleau M (2015) Relationships between female quality, egg mass and eggshell blue-green coloration in southern rockhopper penguins: a test of the sexual signalling hypothesis. Polar Biol 38:1805–1811CrossRefGoogle Scholar
  25. Dutta PC, Helmersson S, Kebedu E, Alema G, Appelqvist LÅ (1994) Variation in lipid composition of Niger seed (Guizotia abyssinica Cass.) samples collected from different regions in Ethiopia. J Am Oil Chem Soc 71:839–843CrossRefGoogle Scholar
  26. Duval C, Cassey P, Mikšík I, Reynolds SJ, Spencer KA (2013) Condition-dependent strategies of eggshell pigmentation: an experimental study of Japanese quail (Coturnix coturnix japonica). J Exp Biol 216:700–708PubMedCrossRefGoogle Scholar
  27. Fargallo JA, López-Rull I, Mikšík I, Eckhardt A, Peralta-Sánchez JM (2014) Eggshell pigmentation has no evident effects on offspring viability in common kestrels. Evol Ecol 28:627–637CrossRefGoogle Scholar
  28. Fecheyr-Lippens DC, Igic B, D’Alba L, Hanley D, Verdes A, Holford M, Waterhouse GIN, Grim T, Hauber ME, Shawkey MD (2015) The cuticle modulates ultraviolet reflectance of avian eggshells. Biol Open 4:753–759PubMedPubMedCentralCrossRefGoogle Scholar
  29. Fechner A, Bohme CC, Gromer S, Funk M, Schirmer RH, Becker K (2001) Antioxidant status and nitric oxide in the malnutrition syndrome kwashiorkor. Pediatr Res 49:237–243PubMedCrossRefGoogle Scholar
  30. Froehling PE, Van Den Bosch G, Boekenoogen HA (1972) Fatty acid composition of carotenoid esters in soybean and rapeseed oils. Lipids 7:447–449CrossRefGoogle Scholar
  31. Fujisawa M, Watanabe M, Choi SK, Teramoto M, Ohyama K, Misawa N (2008) Enrichment of carotenoids in flaxseed (Linum usitatissimum) by metabolic engineering with introduction of bacterial phytoene synthase gene crtB. J Biosci Bioeng 105:636–641PubMedCrossRefGoogle Scholar
  32. Furr HC, Clark RM (1997) Intestinal absorption and tissue distribution of carotenoids. J Nutr Biochem 8:364–377CrossRefGoogle Scholar
  33. García-Navas V, Sanz JJ, Merino S, Martínez-de la Puente J, Lobato E, del Cerro S, Rivero J, Ruiz de Castañeda R, Moreno J (2010) Experimental evidence for the role of calcium in eggshell pigmentation pattern and breeding performance in blue tits Cyanistes caeruleus. J Ornithol 152:71–82CrossRefGoogle Scholar
  34. Gil D, Leboucher G, Lacroix A, Cue R, Kreutzer M (2004) Female canaries produce eggs with greater amounts of testosterone when exposed to preferred male song. Horm Behav 45:64–70PubMedCrossRefGoogle Scholar
  35. Giordano M, Costantini D, Pick JL, Tschirren B (2015) Female oxidative status, egg antioxidant protection and eggshell pigmentation: a supplemental feeding experiment in great tits. Behav Ecol Sociobiol 69:777–785CrossRefGoogle Scholar
  36. Goffman FD, Becker HC (2001) Diallel analysis for tocopherol contents in seeds of rapeseed. Crop Sci 41:1072–1079CrossRefGoogle Scholar
  37. Goffman FD, Velasco L, Thies W (1999) Quantitative determination of tocopherols in single seeds of rapeseed (Brassica napus L.). Fett-Lipid 101:142–145CrossRefGoogle Scholar
  38. Gorchein A, Lim CK, Cassey P (2009) Extraction and analysis of colourful eggshell pigments using HPLC and HPLC/electrospray ionization tandem mass spectrometry. Biomed Chromatogr 23:602–606PubMedCrossRefGoogle Scholar
  39. Gosler AG, Barnett PR, Reynolds SJ (2000) Inheritance and variation in eggshell patterning in the great tit Parus major. Proc R Soc Lond B 267:2469–2473CrossRefGoogle Scholar
  40. Gosler AG, Higham JP, Reynolds SJ (2005) Why are birds’ eggs speckled? Ecol Lett 8:1105–1113CrossRefGoogle Scholar
  41. Gosler AG, Connor OR, Bonser RHC (2011) Protoporphyrin and eggshell strength: preliminary findings from a passerine bird. Avian Biol Res 4:214–223CrossRefGoogle Scholar
  42. Graveland J, van Gijzen T (1994) Arthropods and seeds are not sufficient as calcium sources for shell formation and skeletal growth in passerines. Ardea 82:299–314Google Scholar
  43. Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine, 4th edn. Oxford University Press, OxfordGoogle Scholar
  44. Hanley D, Doucet SM (2009) Egg coloration in ring-billed gulls (Larus delawarensis): a test of the sexual signaling hypothesis. Behav Ecol Sociobiol 63:719–729CrossRefGoogle Scholar
  45. Hanley D, Heiber G, Dearborn DC (2008) Testing an assumption of the sexual-signaling hypothesis: does blue-green egg reflect maternal antioxidant capacity? Condor 110:767–771CrossRefGoogle Scholar
  46. Hanley D, Grim T, Cassey P, Hauber ME (2015) Not so colourful after all: eggshell pigments constrain avian eggshell colour space. Biol Lett 11 20150087Google Scholar
  47. Haq A, Bailey CA, 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 75:1092–1097CrossRefGoogle Scholar
  48. Hargitai R, Herényi M, Török J (2008) Eggshell coloration in relation to female condition, male attractiveness and egg quality in the collared flycatcher (Ficedula albicollis. J Avian Biol 39:413–422Google Scholar
  49. Hargitai R, Moskát C, Bán M, Gil D, López-Rull I, Solymos E (2010) Eggshell characteristics and yolk composition in the common cuckoo Cuculus canorus: are they adapted to brood parasitism? J Avian Biol 41:177–185CrossRefGoogle Scholar
  50. Hargitai R, Mateo R, Török J (2011) Shell thickness and pore density in relation to shell colouration, female characteristics, and environmental factors in the collared flycatcher Ficedula albicollis. J Ornithol 152:579–588CrossRefGoogle Scholar
  51. Hargitai R, Nagy G, Herényi M, Török J (2013) Effects of experimental calcium availability, egg parameters, and laying order on great tit Parus major eggshell pigmentation patterns. Ibis 155:561–570CrossRefGoogle Scholar
  52. Hargitai R, Nagy G, Herényi M, Nyiri Z, Laczi M, Hegyi G, Eke Zs, Török J (2016a) Darker eggshell spotting indicates lower yolk antioxidant level and poorer female quality in the Eurasian great tit (Parus major). Auk 133:131–146CrossRefGoogle Scholar
  53. Hargitai R, Nyiri Z, Eke Zs, Török J (2016b) Effects of temperature and duration of storage on the stability of antioxidant compounds in egg yolk and plasma. Physiol Biochem Zool 89:161–167PubMedCrossRefGoogle Scholar
  54. Hegyi G, Garamszegi LZs (2011) Using information theory as a substitute for stepwise regression in ecology and behavior. Behav Ecol Sociobiol 65:69–76CrossRefGoogle Scholar
  55. Hegyi G, Laczi M (2015) Using full models, stepwise regression and model selection in ecological data sets: Monte Carlo simulations. Ann Zool Fenn 52:257–279CrossRefGoogle Scholar
  56. Holveck M-J, Doutrelant C, Guerreiro R, Perret P, Gomez D, Grégoire A (2010) Can eggs in a cavity be a female secondary sexual signal? Male nest visits and modelling of egg visual discrimination in blue tits. Biol Lett 6:453–457PubMedPubMedCentralCrossRefGoogle Scholar
  57. Holveck M-J, Grégoire A, Staszewski V, Guerreiro R, Perret P, Boulinier T, Doutrelant C (2012) Eggshell spottiness reflects maternally transferred antibodies in blue tits. PLoS One 7 e50389Google Scholar
  58. Honza M, Požgayová M, Procházka P, Cherry MI (2011) Blue-green eggshell coloration is not a sexually selected signal of female quality in an open-nesting polygynous passerine. Naturwissenschaften 98:493–499PubMedCrossRefGoogle Scholar
  59. Hoyt DF (1979) Practical methods of estimating volume and fresh weight of bird egg. Auk 96:73–77Google Scholar
  60. Huopalahti R, Anton M, López-Fandiño R, Schade R (2007) Bioactive egg compounds. Springer, BerlinCrossRefGoogle Scholar
  61. Iamele L, Fiocchi R, Vernocchi A (2002) Evaluation of an automated spectrophotometric assay for reactive oxygen metabolites in serum. Clin Chem Lab Med 40:673–676PubMedCrossRefGoogle Scholar
  62. Igic B, Fecheyr-Lippens D, Xiao M, Chan A, Hanley D, Brennan PRL, Grim T, Waterhouse GIN, Hauber ME, Shawkey MD (2015) A nanostructural basis for gloss of avian eggshells. J R Soc Interface 12 20141210Google Scholar
  63. Ishikawa SI, Suzuki K, Fukuda E, Arihara K, Yamamoto Y, Mukai T, Itoh M (2010) Photodynamic antimicrobial activity of avian eggshell pigments. FEBS Lett 584:770–774PubMedCrossRefGoogle Scholar
  64. Jagannath A, Shore RF, Walker LA, Ferns PN, Gosler AG (2008) Eggshell pigmentation indicates pesticide contamination. J Appl Ecol 45:133–140CrossRefGoogle Scholar
  65. Johnsen A, Delhey K, Andersson S, Kempenaers B (2003) Plumage colour in nestling blue tits: sexual dichromatism, condition dependence and genetic effects. Proc R Soc Lond B 270:1263–1270CrossRefGoogle Scholar
  66. Karadas F, Wood NAR, Surai PF, Sparks NHC (2005) Tissue-specific distribution of carotenoids and vitamin E in tissues of newly hatched chicks from various avian species. Comp Biochem Physiol A 140:506–511CrossRefGoogle Scholar
  67. Kaur H, Hughes MN, Green CJ, Naughton P, Foresti R, Motterlini R (2003) Interactions of bilirubin and biliverdin with reactive nitrogen species. FEBS Lett 543:113–119PubMedCrossRefGoogle Scholar
  68. Kennedy GY, Vevers HG (1976) A survey of avian eggshell pigments. Comp Biochem Physiol B 55:117–123PubMedGoogle Scholar
  69. Kilner RM (2006) The evolution of egg colour and patterning in birds. Biol Rev 81:383–406PubMedCrossRefGoogle Scholar
  70. Lack D (1968) Ecological adaptations for breeding in birds. Methuen, LondonGoogle Scholar
  71. Leitner S, Marshall RC, Leisler B, Catchpole CK (2006) Male song quality, egg size and offspring sex in captive canaries (Serinus canaria). Ethology 112:554–563CrossRefGoogle Scholar
  72. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121CrossRefGoogle Scholar
  73. López-de-Hierro MDG, De Neve L (2010) Pigment limitation and female reproductive characteristics influence egg shell spottiness and ground colour variation in the house sparrow (Passer domesticus). J Ornithol 151:833–840CrossRefGoogle Scholar
  74. López-Rull I, Mikšík I, Gil D (2008) Egg pigmentation reflects female and egg quality in the spotless straling Sturnus unicolor. Behav Ecol Sociobiol 62:1877–1884CrossRefGoogle Scholar
  75. Lovell PG, Ruxton GD, Langridge KV, Spencer KA (2013) Egg-laying substrate selection for optimal camouflage by quail. Curr Biol 23:260–264PubMedCrossRefGoogle Scholar
  76. Martínez-de la Puente J, Merino S, Moreno J, Tomás G, Morales J, Lobato E, García-Fraile S, Martínez J (2007) Are eggshell spottiness and colour indicators of health and condition in blue tits Cyanistes caeruleus? J Avian Biol 38:377–384CrossRefGoogle Scholar
  77. Martínez-Padilla J, Dixon H, Vergara P, Pérez-Rodriguez L, Fargallo JA (2010) Does egg coloration reflect male condition in birds? Naturwissenschaften 97:469–477PubMedCrossRefGoogle Scholar
  78. Maurer G, Portugal SJ, Cassey P (2011) Review: an embryo’s eye view of avian eggshell pigmentation. J Avian Biol 42:494–504CrossRefGoogle Scholar
  79. Maurer G, Portugal SJ, Hauber ME, Mikšík I, Russell DG, Cassey P (2015) First light for avian embryos: eggshell thickness and pigmentation mediate variation in development and UV exposure in wild bird eggs. Funct Ecol 29:209–218CrossRefGoogle Scholar
  80. McDonagh AF (2001) Turning green to gold. Nat Struct Biol 8:198–200PubMedCrossRefGoogle Scholar
  81. McGraw KJ, Adkins-Regan E, Parker RS (2005) Maternally derived carotenoid pigments affect offspring survival, sex ratio, and sexual attractiveness in a colorful songbird. Naturwissenschaften 92:375–380PubMedCrossRefGoogle Scholar
  82. McNeil KA, Newman I, Kelly FJ (1996) Testing research hypotheses with the general linear model. Southern Illinois University Press, CarbondaleGoogle Scholar
  83. Mikšík I, Holáň V, Deyl Z (1996) Avian eggshell pigments and their variability. Comp Biochem Physiol B 113:607–612CrossRefGoogle Scholar
  84. Morales J, Sanz JJ, Moreno J (2006) Egg colour reflects the amount of yolk maternal antibodies and fledging success in a songbird. Biol Lett 2:334–336PubMedPubMedCentralCrossRefGoogle Scholar
  85. Morales J, Velando A, Moreno J (2008) Pigment allocation to eggs decreases plasma antioxidants in a songbird. Behav Ecol Sociobiol 63:227–233CrossRefGoogle Scholar
  86. Morales J, Kim SY, Lobato E, Merino S, Tomás G, Martínez-de la Puente J, Moreno J (2010) On the heritability of blue-green eggshell coloration. J Evol Biol 23:1783–1791PubMedCrossRefGoogle Scholar
  87. Morales J, Velando A, Torres R (2011) Biliverdin-based egg coloration is enhanced by carotenoid supplementation. Behav Ecol Sociobiol 65:197–203CrossRefGoogle Scholar
  88. Morales J, Ruuskanen S, Laaksonen T et al (2013) Variation in eggshell traits between geographically distant populations of pied flycatchers Ficedula hypoleuca. J Avian Biol 44:111–120Google Scholar
  89. Moreno J, Osorno JL (2003) Avian egg colour and sexual selection: does eggshell pigmentation reflect female condition and genetic quality? Ecol Lett 6:803–806CrossRefGoogle Scholar
  90. Moreno J, Morales J, Lobato E, Merino S, Tomás G, Martínez-de la Puente J (2005) Evidence for the signaling function of egg color in the pied flycatcher Ficedula hypoleuca. Behav Ecol 16:931–937CrossRefGoogle Scholar
  91. Moreno J, Lobato E, Morales J, Merino S, Tomás G, Martínez-de la Puente J, Sanz JJ, Mateo R, Soler JJ (2006) Experimental evidence that egg color indicates female condition at laying in a songbird. Behav Ecol 17:651–655CrossRefGoogle Scholar
  92. Moreno J, Morales J, Martínez J (2013) HSP70 level in blood is associated with eggshell blue-green coloration the pied flycatcher. Avian Biol Res 6:297–301CrossRefGoogle Scholar
  93. Moskát C, Avilés JM, Bán M, Hargitai R, Zölei A (2008) Experimental support for the use of egg uniformity in parasite egg discrimination by cuckoo hosts. Behav Ecol Sociobiol 62:1885–1890CrossRefGoogle Scholar
  94. Navarro C, Pérez-Contreras T, Avilés JM, McGraw KJ, Soler JJ (2011) Blue-green eggshell coloration reflects yolk antioxidant content in spotless starlings Sturnus unicolor. J Avian Biol 42:538–543CrossRefGoogle Scholar
  95. Newton A (1896) A dictionary of birds. Adam and Charles Black, LondonGoogle Scholar
  96. Nilsson JA, Råberg L (2001) The resting metabolic cost of egg laying and nestling feeding in great tits. Oecologia 128:187–192CrossRefGoogle Scholar
  97. Nys Y, Gautron J, McKee MD, Garcia-Ruiz JM, Hincke MT (2001) Biochemical and functional characterisation of eggshell matrix proteins in hens. World Poultry Sci J 57:401–413CrossRefGoogle Scholar
  98. Odabaşi AZ, Miles RD, Balaban MO, Portier KM, Sampath V (2006) Vitamin C overcomes the detrimental effect of vanadium on brown eggshell pigmentation. J Appl Poult Res 15:425–432CrossRefGoogle Scholar
  99. Oniki Y (1979) Nest-egg combinations: possible antipredatory adaptations in Amazonian birds. Rev Bras Biol 39:747–767Google Scholar
  100. Oomah BD, Kenaschuk EO, Mazza G (1997) Tocopherols in flaxseed. J Agr Food Chem 45:2076–2080CrossRefGoogle Scholar
  101. Panfili G, Fratianni A, Irano M (2003) Normal phase high-performance liquid chromatography method for the determination of tocopherols and tocotrienols in cereals. J Agr Food Chem 51:3940–3944Google Scholar
  102. Panfili G, Fratianni A, Irano M (2004) Improved normal-phase high-performance liquid chromatography procedure for the determination of carotenoids in cereals. J Agr Food Chem 52:6373–6377CrossRefGoogle Scholar
  103. Peters A, Delhey K, Andersson S, Van Noordwijk H, Förschler MI (2008) Condition-dependence of multiple carotenoid-based plumage traits: an experimental study. Funct Ecol 22:831–839CrossRefGoogle Scholar
  104. Pimentel E, Vidal LM, Cruces MP, Janczur MK (2013) Action of protoporphyrin-IX (PP-IX) in the lifespan of Drosophila melanogaster deficient in endogenous antioxidants, Sod and Cat. Open J Anim Sci 3:1–7CrossRefGoogle Scholar
  105. Ramadan M, Mörsel JT (2002) Direct isocratic normal-phase HPLC assay of fat-soluble vitamins and β-carotene in oilseeds. Eur Food Res Technol 214:521–527CrossRefGoogle Scholar
  106. Ratcliffe DA (1967) Decrease in eggshell weight in certain birds of prey. Nature 215:208–210PubMedCrossRefGoogle Scholar
  107. Remeš V, Krist M, Bertacche V, Stradi R (2007) Maternal carotenoid supplementation does not affect breeding performance in the great tit (Parus major). Funct Ecol 21:776–783CrossRefGoogle Scholar
  108. Reynolds SJ, Martin GR, Cassey P (2009) Is sexual selection blurring the functional significance of eggshell coloration hypotheses? Anim Behav 78:209–215CrossRefGoogle Scholar
  109. Riehl C (2011) Paternal investment and the “sexually selected hypothesis” for the evolution of eggshell coloration: revisiting the assumptions. Auk 128:175–179CrossRefGoogle Scholar
  110. Rindler PM, Plafker SM, Szweda LI, Kinter M (2013) High dietary fat selectively increases catalase expression within cardiac mitochondria. J Biol Chem 288:1979–1990PubMedCrossRefGoogle Scholar
  111. Saino N, Ferrari R, Romano M, Martinelli R, Møller AP (2003) Experimental manipulation of egg carotenoids affects immunity of barn swallow nestlings. Proc R Soc Lond B 270:2485–2489CrossRefGoogle Scholar
  112. Sanz JJ, García-Navas V (2009) Eggshell pigmentation pattern in relation to breeding performance of blue tits Cyanistes caeruleus. J Anim Ecol 78:31–41PubMedCrossRefGoogle Scholar
  113. Scanes CG, Campbell R, Griminger P (1987) Control of energy balance during egg production in the laying hen. J Nutr 117:605–611PubMedGoogle Scholar
  114. Siefferman L, Navara KJ, Hill GE (2006) Egg coloration is correlated with female condition in eastern bluebirds (Sialia sialis). Behav Ecol Sociobiol 59:651–656CrossRefGoogle Scholar
  115. Singleton JW, Laster L (1965) Biliverdin reductase of guinea pig liver. J Biol Chem 240:4780–4789PubMedGoogle Scholar
  116. Slagsvold T, Sandvik J, Rofstad G, Lorentsen Ö, Husby M (1984) On the adaptive value of intraclutch egg-size variation in birds. Auk 101:685–697CrossRefGoogle Scholar
  117. Soler JJ, Soler M, Møller AP (2000) Host recognition of parasite eggs and the physical appearance of host eggs: the magpie and its brood parasite the great spotted cuckoo. Etología 8:9–16Google Scholar
  118. Soler JJ, Navarro C, Contreras TP, Avilés JM, Cuervo JJ (2008) Sexually selected egg coloration in spotless starlings. Am Nat 171:183–194PubMedCrossRefGoogle Scholar
  119. Solomon SE (1997) Egg and eggshell quality. Iowa State University Press, AmesGoogle Scholar
  120. Speakman JR, Garratt M (2014) Oxidative stress as a cost of reproduction: beyond the simplistic trade-off model. BioEssays 36:93–106PubMedCrossRefGoogle Scholar
  121. Stocker R, Yamamaoto Y, McDonagh AF, Glazer AN, Ames BN (1987) Bilirubin as an antioxidant of possible physiological importance. Science 235:1043–1046PubMedCrossRefGoogle Scholar
  122. Stoddard MC, Marshall KLA, Kilner RM (2011) Imperfectly camouflaged avian eggs: artefact or adaptation? Avian Biol Res 4:196–213CrossRefGoogle Scholar
  123. Stoddard MC, Fayet AL, Kilner RM, Hinde CA (2012) Egg speckling patterns do not advertise offspring quality or influence male provisioning in great tits. PLoS One 7 e40211Google Scholar
  124. Stokke BG, Moksnes A, Røskaft E, Rudolfsen G, Honza M (1999) Rejection of artificial cuckoo (Cuculus canorus) eggs in relation to variation in egg appearance among reed warblers (Acrocephalus scirpaceus). Proc R Soc Lond B 266:1483–1488CrossRefGoogle Scholar
  125. Surai PF (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, NottinghamGoogle Scholar
  126. Surai PF, Noble RC, Speake BK (1996) Tissue-specific differences in antioxidant distribution and susceptibility to lipid peroxidation during development of the chick embryo. Biochim Biophys Acta 1304:1–10PubMedCrossRefGoogle Scholar
  127. Surai PF, Royle NJ, Sparks NHC (2000) Fatty acid, carotenoid and vitamin a composition of tissues of free living gulls. Comp Biochem Physiol A 126:387–396CrossRefGoogle Scholar
  128. Tanvez A, Amy M, Chastel O, Leboucher G (2009) Maternal effects and β-carotene assimilation in canary chicks. Physiol Behav 96:389–393PubMedCrossRefGoogle Scholar
  129. 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 Sci 86:2236–2238CrossRefGoogle Scholar
  130. Węgrzyn E, Leniowski K, Rykowska I, Wasiak W (2011) Is UV and blue-green egg coloration a signal in cavity-nesting birds? Ethol Ecol Evol 23:121–139CrossRefGoogle Scholar
  131. Westmoreland D, Schmitz M, Burns KE (2007) Egg color as an adaptation for thermoregulation. J Field Ornithol 78:176–183CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Rita Hargitai
    • 1
  • Nóra Boross
    • 1
  • Zoltán Nyiri
    • 2
  • Zsuzsanna Eke
    • 2
  1. 1.Behavioural Ecology Group, Department of Systematic Zoology and EcologyEötvös Loránd UniversityBudapestHungary
  2. 2.Joint Research and Training Laboratory on Separation TechniquesEötvös Loránd UniversityBudapestHungary

Personalised recommendations