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Shell thickness and pore density in relation to shell colouration, female characteristics, and environmental factors in the Collared Flycatcher Ficedula albicollis

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An Erratum to this article was published on 12 February 2011

Abstract

Avian eggshell structure may have important consequences for embryonic growth and development, but relatively little is known about the factors responsible for variation in eggshell characteristics of wild birds. In this paper, we explored potential causes of variation in eggshell colour and structure (shell thickness and porosity) in the Collared Flycatcher (Ficedula albicollis). We analysed if eggshell colour is affected by shell structure or pigment level, and whether female traits, laying date, local breeding density, and clutch size affect shell thickness and pore density. We found that eggshell blue-green and UV colours were unrelated to shell thickness, pore density and egg size. Eggs with higher concentration of biliverdin showed lower UV reflection and higher reflection in the blue-green part of the spectrum. We found that females in better nutritional condition, indicated by their higher mass controlled for tarsus length, laid eggs with thicker shells. It is possible that females in better condition have more time available for searching calcium-rich food, and thus could produce eggs with stronger shells. However, female physical characteristics had no significant relationships with shell porosity. In contrast to our expectation, shell thickness and pore density were unrelated to local breeding density and laying date, though very late and repeat clutches were not sampled in our study. However, we found that eggs in larger clutches had lower pore density than eggs in smaller clutches, which may be expected if the rate of water loss and nest humidity are to remain constant in clutches of different egg numbers.

Zusammenfassung

Die Struktur der Eischale von Vögeln kann wichtige Folgen für das Wachstum und die Entwicklung der Embryonen haben, doch über die Faktoren, die für Variation in den Eigenschaften der Eischale bei freilebenden Vögeln verantwortlich sind, ist relativ wenig bekannt. In diesem Artikel haben wir mögliche Gründe für die Variation in Eischalenfarbe und -struktur (Schalendicke und Porosität) beim Halsbandschnäpper (Ficedula albicollis) untersucht. Wir haben analysiert, ob die Eischalenfarbe von der Schalenstruktur oder dem Pigmentgehalt beeinflusst wird und ob Weibchenmerkmale, Legedatum, lokale Brutpaardichte und Gelegegröße die Schalendicke und Porendichte beeinflussen. Wir fanden, dass blaugrüne und ultraviolette Farben der Eischale nicht mit der Schalendicke, Porendichte und Eigröße zusammenhingen. Eier mit einer höheren Biliverdinkonzentration zeigten eine geringere UV-Reflexion und stärkere Reflexion im blaugrünen Bereich des Spektrums. Wir fanden, dass Weibchen in besserem Ernährungszustand, angezeigt durch ihre höhere Körpermasse korrigiert für Tarsuslänge, Eier mit dickerer Schale legten. Es ist möglich, dass Weibchen in besserer Kondition mehr Zeit haben, kalziumreiche Nahrung zu suchen, und daher Eier mit stärkerer Schale produzieren. Die Körpermerkmale der Weibchen standen jedoch in keiner signifikanten Beziehung zu der Schalenporosität. Entgegen unserer Erwartung standen Schalendicke und Porendichte nicht mit der lokalen Brutpaardichte und dem Legedatum in Zusammenhang, obwohl sehr späte Gelege und Nachgelege in unserer Studie nicht beprobt wurden. Wir fanden jedoch, dass Eier in größeren Gelegen eine geringere Porendichte hatten als Eier in kleineren Gelegen, was zu erwarten wäre, wenn die Wasserverlustrate und die Nestfeuchte in Gelegen mit unterschiedlicher Eizahl konstant blieben.

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References

  • Alatalo RV, Lundberg A (1984) Density-dependence in breeding success of the pied flycatcher (Ficedula hypoleuca). J Anim Ecol 53:969–977

    Google Scholar 

  • Ar A, Rahn H (1985) Pores in avian eggshells: gas conductance, gas exchange and embryonic growth rate. Resp Physiol 61:1–20

    CAS  Google Scholar 

  • Ar A, Paganelli CV, Reeves RB, Greene DG, Rahn H (1974) The avian egg: water vapor conductance, shell thickness, and functional pore area. Condor 76:153–158

    Google Scholar 

  • Ar A, Rahn H, Paganelli CV (1979) The avian egg: mass and strength. Condor 81:331–337

    Google Scholar 

  • Avilés JM, Soler JJ, Pérez-Contreras T (2006) Dark nests and egg colour in birds: a possible functional role of ultraviolet reflectance in egg detectability. Proc R Soc Lond B 273:2821–2829

    Google Scholar 

  • Boersma PD, Rebstock GA (2009) Magellanic Penguin eggshell pores: does number matter? Ibis 151:535–540

    Google Scholar 

  • Bureš S, Weidinger K (2003) Sources and timing of calcium intake during reproduction in flycatchers. Oecologia 137:634–647

    PubMed  Google Scholar 

  • Burton FG, Tullett SG (1983) A comparison of the effects of eggshell porosity on the respiration and growth of domestic fowl, duck and turkey embryos. Comp Biochem Physiol A 75:167–174

    Google Scholar 

  • Castilla AM, Herrel A, Van Dongen S, Furio N, Negro JJ (2009) Determinants of eggshell strength in endangered raptors. J Exp Zool 311A:303–311

    Google Scholar 

  • Cherry MI, Bennett ATD (2001) Egg colour matching in an African cucko, as revealed by ultraviolet-visible reflectance spectrophotometry. Proc R Soc Lond B 268:565–571

    CAS  Google Scholar 

  • Cuthill IC, Partridge JC, Bennett ATD, Church SC, Hart NS, Hunt S (2000) Ultraviolet vision in birds. Adv Stud Behav 29:159–214

    Google Scholar 

  • Dauwe T, Janssens E, Kempenaers B, Eens M (2004) The effect of heavy metal exposure on egg size, eggshell thickness and the number of spermatozoa in blue tit Parus caeruleus eggs. Environ Pollut 129:125–129

    CAS  PubMed  Google Scholar 

  • Doliguez B, Paert T, Danchin E, Clobert J, Gustafsson L (2004) Availability and use of public information and conspecific density for settlement decisions in the collared flycatcher. J Anim Ecol 73:75–87

    Google Scholar 

  • Eeva T, Lehikoinen E (1995) Egg shell quality, clutch size and hatching success of the great tit (Parus major) and the pied flycatcher (Ficedula hyoleuca) in an air pollution gradient. Oecologia 102:312–323

    PubMed  Google Scholar 

  • Eichholz MW, Sedinger JS (1998) Factors affecting duration of incubation in black brant. Condor 100:164–168

    Google Scholar 

  • Falchuk KH, Contin JM, Dziedzic TS, Feng ZL, French TC, Heffron GJ, 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garamszegi LZ, Török J, Michl G, Møller AP (2004a) Female survival, lifetime reproductive success and mating status in a passerine bird. Oecologia 138:48–56

    PubMed  Google Scholar 

  • Garamszegi LZ, Török J, Tóth L, Michl G (2004b) The effect of timing and female quality on clutch size in the collared flycatcher Ficedula albicollis. Bird Study 51:270–277

    Google Scholar 

  • Gosler AG, Higham JP, Reynolds SJ (2005) Why are birds’ eggs speckled? Ecol Lett 8:1105–1113

    Google Scholar 

  • Graveland J, Berends JE (1997) Timing of the calcium intake and effect of calcium deficiency on behaviour and egg laying in captive great tits Parus major. Physiol Zool 70:74–84

    CAS  PubMed  Google Scholar 

  • Graveland J, van Gijzen T (1994) Arthropods and seeds are not sufficient as calcium sources for shell formation and skeletal growth in passerines. Ardea 82:299–314

    Google Scholar 

  • Graveland J, van der Wal R, van Balen JH, van Noordwijk AJ (1994) Poor reproduction in forest passerines from decline of snail abundance in acidified soils. Nature 368:446–448

    Google Scholar 

  • Gross WB, Siegel HS (1983) Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Dis 27:972–979

    CAS  PubMed  Google Scholar 

  • Hargitai R, Török J, Tóth L, Hegyi G, Rosivall B, Szigeti B, Szöllősi 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

    Google Scholar 

  • Hargitai R, Herényi M, Török J (2008) Eggshell colouration in relation to female condition, male attractiveness and egg quality in the collared flycatcher (Ficedula albicollis). J Avian Biol 39:413–422

    Google Scholar 

  • Hargitai R, Arnold KE, Herényi M, Prechl J, Török J (2009) Egg composition in relation to social environment and maternal physiological condition in the collared flycatcher. Behav Ecol Sociobiol 63:869–882

    Google Scholar 

  • 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 41:177–185

    Google Scholar 

  • Herényi M, Hegyi G, Garamszegi LZ, Hargitai R, Michl G, Rosivall B, Török J (2010) Lifetime offspring production in relation to attractiveness, breeding lifespan and mating status in male collared flycatchers. Oecologia (in press)

  • Higham JP, Gosler AG (2006) Speckled eggs: water-loss and incubation behavior in the great tit Parus major. Oecologia 149:561–570

    PubMed  Google Scholar 

  • Hipfner JM, Gaston AJ, Mardin DL, Jones IL (2001) Seasonal declines in incubation periods of Brünnich’s guillemots Uria lomvia: testing proximate causes. Ibis 143:92–98

    Google Scholar 

  • Hoyt DF (1979) Practical methods of estimating volume and fresh weight of bird eggs. Auk 96:73–77

    Google Scholar 

  • Jagannath A, Shore RF, Walker LA, Ferns PN, Gosler A (2008) Eggshell pigmentation indicates pesticide contamination. J Appl Ecol 45:133–140

    Google Scholar 

  • Kennedy GY, Vevers HG (1976) A survey of avian eggshell pigments. Comp Biochem Physiol 55B:117–123

    Google Scholar 

  • Kilner RM (2006) The evolution of egg colour and patterning in birds. Biol Rev 81:383–406

    CAS  PubMed  Google Scholar 

  • Král M, Sætre G-P, Bicík V (1996) Intrasexual aggression of female collared flycatchers (Ficedula albicollis): competition for male parental care? Folia Zool 45:153–159

    Google Scholar 

  • Lang MR, Wells JW (1987) A review of eggshell pigmentation. World Poult Sci J 43:238–246

    Google Scholar 

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

    Google Scholar 

  • López-Rull I, Mikšík I, Gil D (2008) Egg pigmentation reflects female and egg quality in the spotless starling Sturnus unicolor. Behav Ecol Sociobiol 62:1877–1884

    Google Scholar 

  • Mänd R (1996) Increased eggshell porosity in replacement clutches of the black-headed gull Larus ridibundus. Ornis Fenn 73:131–136

    Google Scholar 

  • Mänd R, Tilgar V (2003) Does supplementary calcium reduce the cost of reproduction in the pied flycatcher Ficedula hypoleuca? Ibis 145:67–77

    Google Scholar 

  • Massaro M, Davis LS (2004) The influence of laying date and maternal age on eggshell thickness and pore density in yellow-eyed penguins. Condor 106:496–505

    Google Scholar 

  • Massaro M, Davis LS (2005) Differences in egg size, shell thickness, pore density, pore diameter and water vapour conductance between first and second eggs of Snares penguins Eudyptes robustus and their influence on hatching asynchrony. Ibis 147:251–258

    Google Scholar 

  • Massaro M, Davis L, Darby JT, Robertson GJ, Setiawan AN (2004) Intraspecific variation in incubation periods in yellow-eyed penguins (Megadyptes antiopes): testing the influence of age, laying date and egg size. Ibis 146:526–530

    Google Scholar 

  • Mateo R, Castells G, Green AJ, Godoy C, Cristòfol C (2004) Determination of porphyrins and biliverdin in bile and excreta of birds by a single liquid chromatography-ultraviolet detection analysis. J Chromatogr B 810:305–311

    CAS  Google Scholar 

  • Maxwell MH (1993) Avian blood leucocyte responses to stress. World Poult Sci J 49:34–43

    Google Scholar 

  • Mikšík I, Holáň V, Deyl Z (1996) Avian eggshell pigments and their variability. Comp Biochem Physiol 113B:607–612

    Google Scholar 

  • Moreno J, Osorno JL (2003) Avian egg colour and sexual selection: does eggshell pigmentation reflect female condition and genetic quality? Ecol Lett 6:803–806

    Google Scholar 

  • 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 egg laying in a songbird. Behav Ecol 17:651–655

    Google Scholar 

  • Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Res 82:591–605

    Google Scholar 

  • Norris K (1993) Seasonal variation in the reproductive success of blue tits: an experimental study. J Anim Ecol 62:287–294

    Google Scholar 

  • Nys Y, Hincke MT, Arias JL, Garcia-Ruiz JM, Solomon SE (1999) Avian eggshell mineralization. Poult Avian Biol Rev 10:143–166

    Google Scholar 

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

    PubMed  Google Scholar 

  • Packard MJ, Packard GC (1984) Comparative aspects of calcium metabolism in embryonic reptiles and birds. In: Seymour RS (ed) Respiration and metabolism of embryonic vertebrates. Junk, Dordrecht, pp 155–180

    Google Scholar 

  • Paganelli CV (1980) The physics of gas exchange across the avian eggshell. Am Zool 20:329–338

    Google Scholar 

  • Pahl R, Winkler DW, Graveland J, Batterman BW (1997) Songbirds do not create long-term stores of calcium in their legs prior to laying: results from the high-resolution radiography. Proc R Soc Lond B 264:239–244

    Google Scholar 

  • Prum RO, Torres R (2003) Structural colouration of avian skin: convergent evolution of coherently scattering dermal collagen arrays. J Exp Biol 206:2409–2429

    PubMed  Google Scholar 

  • Prum RO, Torres RH, Kovach C, Williamson S, Goodman SM (1999) Two-dimensional Fourier analysis of the spongy medullary keratin of structurally coloured feather barbs. Proc R Soc Lond B 266:13–22

    CAS  Google Scholar 

  • Rahn H, Paganelli CV (1982) Role of diffusion in gas exchange of the avian egg. Fed Proc 41:2134–2136

    CAS  PubMed  Google Scholar 

  • Rahn H, Paganelli CV (1989) Shell mass, thickness and density of avian eggs derived from the tables of Schonwetter. J Ornithol 130:59–68

    Google Scholar 

  • Rätti O (2000) Characteristics and level of aggression by female pied flycatchers at different distances from the nest hole. Ornis Fenn 77:11–16

    Google Scholar 

  • Sanz JJ, García-Navas V (2009) Eggshell pigmentatioin pattern in relation to breeding performance of blue tits Cyanistes caeruleus. J Anim Ecol 78:31–41

    PubMed  Google Scholar 

  • Shawkey MD, Estes AM, Siefferman LM, Hill GE (2003) Nanostructure predicts intraspecific variation in ultraviolet-blue plumage colour. Proc R Soc Lond B 270:1455–1460

    Google Scholar 

  • Siefferman L, Navara KJ, Hill GE (2006) Egg coloration is correlated with female condition in eastern bluebirds (Sialia sialis). Behav Ecol Sociobiol 59:651–656

    Google Scholar 

  • Simkiss K (1967) Calcium in reproductive physiology. Chapman and Hall, London

    Google Scholar 

  • Slagsvold T (1986) Asynchronous versus synchronous hatching in birds: experiments with the pied flycatcher. J Anim Ecol 55:1115–1134

    Google Scholar 

  • Slagsvold T, Amundsen T, Dale S, Lampe H (1992) Female-female aggression explains polyterritoriality in male pied flycatchers. Anim Behav 43:397–407

    Google Scholar 

  • Soliman FN, Rizk RE, Brake J (1994) Relationship between shell porosity, shell thickness, egg weight loss, and embryonic development in Japanese quail eggs. Poult Sci 73:1607–1611

    CAS  PubMed  Google Scholar 

  • Solomon SE (1997) Egg and eggshell quality. Iowa State University Press, Ames

    Google Scholar 

  • Szegedi A, Rosivall B, Szöllősi E, Hegyi G, Török J (2009) The effect of environmental conditions on hatching asynchrony in the collared flycatcher. In: 2nd European congress of conservation biology, Prague

  • Tilgar V, Mänd R, 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

    Google Scholar 

  • Török J, Tóth L (1988) Density dependence in reproduction of the collared flycatcher (Ficedula albicollis) at high population levels. J Anim Ecol 57:251–258

    Google Scholar 

  • Török J, Hegyi G, Tóth L, Könczey R (2004) Unpredictable food supply modifies costs of reproduction and hampers individual optimization. Oecologia 141:432–443

    PubMed  Google Scholar 

  • Tullett SG, Board RG (1977) Determinants of avian eggshell porosity. J Zool 183:203–211

    Google Scholar 

  • Underwood TJ, Sealy SG (2002) Adaptive significance of egg coloration. In: Deeming DC (ed) Avian incubation, behaviour, environment and evolution. Oxford University Press, Oxford, pp 280–298

    Google Scholar 

  • Verhulst S, Nilsson J-Å (2008) The timing of birds’ breeding season: a review of experiments that manipulated timing of breeding. Philos Trans R Soc Lond B 363:399–410

    Google Scholar 

  • von Haartman L (1956) Territory in the pied flycatcher Muscicapa hypoleuca. Ibis 98:460–475

    Google Scholar 

  • Wiggins DA, Pärt T, Gustafsson L (1994) Seasonal decline in collared flycatcher Ficedula albicollis reproductive success: an experimental approach. Oikos 70:359–364

    Google Scholar 

  • Zimmermann K, Hipfner JM (2007) Egg size, eggshell porosity, and incubation period in the marine bird family Alcidae. Auk 124:307–315

    Google Scholar 

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Acknowledgments

We are grateful to R. Főző, L.Z. Garamszegi, G. Hegyi, M. Herényi, M. Laczi, G. Nagy, B. Rosivall, B. Szigeti and E. Szöllősi for assistance during fieldwork. We are indebted to P. Camarero, M. Martínez-Haro and J. Moreno for suggestions and help in the laboratory analyses. We thank two anonymous referees for their constructive comments. This study was supported by the Hungarian Scientific Research Fund (OTKA, grants no. T49650 and K75618), the Hungarian Ministry of Education (FKFP 0021/2002), the Eötvös Loránd University, and the Pilis Park Forestry. The Hungarian Ministry of Environment and Water provided permissions for the collection of Collared Flycatcher eggs for this study (permission no. 15951/2005). This research received support from the SYNTHESYS Project (http://www.synthesys.info/), which is financed by European Community Research Infrastructure Action under the FP6 “Structuring the European Research Area” Programme. The study complied with the current laws of Hungary.

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Correspondence to Rita Hargitai.

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Communicated by C. G. Guglielmo.

An erratum to this article can be found at http://dx.doi.org/10.1007/s10336-011-0665-6

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Hargitai, R., Mateo, R. & Török, J. Shell thickness and pore density in relation to shell colouration, female characteristics, and environmental factors in the Collared Flycatcher Ficedula albicollis . J Ornithol 152, 579–588 (2011). https://doi.org/10.1007/s10336-010-0627-4

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