Skip to main content

Advertisement

SpringerLink
Log in

Egg composition in relation to social environment and maternal physiological condition in the collared flycatcher

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Offspring survival can be influenced by resources allocated to eggs, which in turn may be affected by the environmental factors the mother experiences during egg formation. In this study, we investigated whether experimentally elevated social interactions and number of neighbouring pairs influence yolk composition of collared flycatchers (Ficedula albicollis). Social challenge was simulated by presentation of a conspecific female. Experimental females spent more time near the cage and produced eggs with higher androgen concentration, but local breeding density did not affect yolk androgen level. Moreover, we found that females exposed to more intra-specific interactions and those that bred at higher density produced eggs with smaller yolk. These females may be more constrained in foraging time due to more frequent social encounters, and there might be increased competition for food at areas of higher density. In contrast, the present study did not reveal any evidence for the effect of social environment on yolk antioxidant and immunoglobulin levels. However, we found that yolk lutein and immunoglobulin concentrations were related to the female’s H/L ratio. Also, yolk lutein and α-tocopherol levels showed a seasonal increase and were positively related to the female’s plasma carotenoid level. Mothers may incur significant costs by transferring these compounds into the eggs, thus only females in good physiological condition and those that lay eggs later, when food is probably more abundant, could allocate higher amounts to the eggs without compromising their defence mechanisms. Our results suggest that environmental circumstances during egg formation can influence conditions for embryonic development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

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 

  • Alonso-Alvarez C, Bertrand S, Devevey G, Gaillard M, Prost J, Faivre B, Sorci G (2004) An experimental test of the dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. Am Nat 164:651–659

    PubMed  Google Scholar 

  • Alonso-Alvarez C, Bertrand S, Faivre B, Chastel O, Sorci G (2007) Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc R Soc Lond B Biol Sci 274:819–825

    CAS  Google Scholar 

  • Alonso-Alvarez C, Pérez-Rodriguez L, Mateo R, Chastel O, Viñuela J (2008) The oxidation handicap hypothesis and the caroteniod allocation trade-off. J Evol Biol 21:1789–1797

    PubMed  CAS  Google Scholar 

  • Andersson S, Uller T, Löhmus M, Sundström F (2004) Effects of egg yolk testosterone on growth and immunity in a precocial bird. J Evol Biol 17:501–505

    PubMed  CAS  Google Scholar 

  • Badyaev AV, Schwabl H, Young RL, Duckworth RA, Navara KJ, Parlow AF (2005) Adaptive sex differences in growth of pre-ovulation oocytes in a passerine bird. Proc R Soc B 272:2165–2172

    PubMed  Google Scholar 

  • Bertrand S, Alonso-Alvarez C, Devevey G, Faivre B, Prost J, Sorci G (2006) Carotenoids modulate the trade-off between egg production and resistance to oxidative stress in zebra finches. Oecologia 147:576–584

    PubMed  Google Scholar 

  • Besedovsky HO, del Rey AE (1996) Immune-neuroendocrine interactions: facts and hypotheses. Endocr Rev 17:64–97

    PubMed  CAS  Google Scholar 

  • Biard C, Surai PF, Møller AP (2005) Effects of carotenoid availability during laying on reproduction in the blue tit. Oecologia 144:32–44

    PubMed  Google Scholar 

  • Blas J, Pérez-Rodriguez L, Bortolotti GR, Viñuela J, Marchant TA (2006) Testosterone increases bioavailability of carotenoids: insights into the honesty of sexual signaling. Proc Natl Acad Sci USA 103:18633–18637

    PubMed  CAS  Google Scholar 

  • Blomqvist D, Johansson OC, Götmark F (1997) Parental quality and egg size affect chick survival in a precocial bird, the Lapwing Vanellus vanellus. Oecologia 110:18–24

    Google Scholar 

  • Blount JD, Houston DC, Møller AP (2000) Why egg yolk is yellow. Trends Ecol Evol 15:47–49

    PubMed  Google Scholar 

  • Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127

    PubMed  CAS  Google Scholar 

  • Boulinier T, Staszewski V (2008) Maternal transfer of antibodies: raising immuno-ecology issues. Trends Ecol Evol 23:282–288

    PubMed  Google Scholar 

  • Breiehagen T, Slagsvold T (1988) Male polyterritoriality and female–female aggression in pied flycatchers Ficedula hypoleuca. Anim Behav 36:604–605

    Google Scholar 

  • Britton G (1995) UV/visible spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids: Spectroscopy. Birkhäuser Verlag, Basel, pp 13–63

    Google Scholar 

  • Buchanan KL, Evans MR, Goldsmith AR, Bryant DM, Rowe LV (2001) Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling? Proc R Soc B 268:1337–1344

    PubMed  CAS  Google Scholar 

  • Chainy GBN, Samantaray S, Samanta L (1997) Testosterone-induced changes in testicular antioxidant system. Andrologia 29:343–349

    Article  PubMed  CAS  Google Scholar 

  • Chapple ILC (1997) Reactive oxygen species and antioxidants in inflammatory diseases. J Clin Periodontol 24:287–296

    PubMed  CAS  Google Scholar 

  • Christians JK (2002) Avian egg size: variation within species and inflexibility within individuals. Biol Rev 77:1–26

    PubMed  Google Scholar 

  • Clotfelter ED, O’Neal DM, Gaudioso JM, Casto JM, Parker-Renga IM, Snajdr EA, Duffy DL, Nolan V Jr, Ketterson ED (2004) Consequences of elevating plasma testosterone in females of a socially monogamous songbird: evidence of constraints on male evolution? Horm Behav 46:171–178

    PubMed  CAS  Google Scholar 

  • Cohen AA, Hau M, Wikelski M (2008) Stress, metabolism, and antioxidants in two wild passerine bird species. Physiol Biochem Zool 81:463–472

    PubMed  Google Scholar 

  • Constantini D, Møller AP (2008) Carotenoids are minor antioxidants for birds. Funct Ecol 22:367–370

    Google Scholar 

  • Daan S, Dijkstra C, Drent R, Meijer T (1988) Food supply and the annual timing of avian reproduction. In: Ouellet H (ed) Acta XIX Congressus Internationalis Ornithologici. National Museum of Natural Sciences, Ottawa, pp 392–407

    Google Scholar 

  • Dale S, Slagsvold T (1995) Female contests for nest sites and mates in the pied flycatcher Ficedula hypoleuca. Ethology 99:209–222

    Article  Google Scholar 

  • Dale S, Rinden H, Slagsvold T (1992) Competition for a mate restricts mate search of female pied flycatchers. Behav Ecol Sociobiol 30:165–176

    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 

  • Eising CM, Groothuis TGG (2003) Yolk androgens and begging behaviour in black-headed gull chicks: an experimental field study. Anim Behav 66:1027–1034

    Google Scholar 

  • Eising CM, Eikenaar C, Schwabl H, Groothuis TGG (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc Lond B Biol Sci 268:839–846

    CAS  Google Scholar 

  • Eising CM, Müller W, Groothuis TGG (2006) Avian mothers create different phenotypes by hormone deposition in their eggs. Biol Lett 22:20–22

    Google Scholar 

  • Elekonich MM, Wingfield JC (2000) Seasonality and hormonal control of territorial aggression in female song sparrows (Passeriformes: Emberizidae: Melospiza melodia). Ethology 106:493–510

    Google Scholar 

  • Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247

    PubMed  CAS  Google Scholar 

  • Galbraith H (1988) Effects of egg size and composition on the size, quality and survival of Lapwing Vanellus vanellus chicks. J Zool 214:383–398

    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 

  • Gasparini J, McCoy KD, Haussy C, Tveraa T, Boulinier T (2001) Induced maternal response to the Lyme disease spirochaete Borrelia burgdorferi sensu lato in a colonial seabird, the kittiwake Rissa tridactyla. Proc R Soc Lond B Biol Sci 268:647–650

    CAS  Google Scholar 

  • Goodwin TW (1984) The Biochemistry of the carotenoids, vol. 2. Animals. Chapman and Hall, London

    Google Scholar 

  • Graczyk TK, Cranfield MR, Shaw ML, Craig LE (1994) Maternal antibodies against Plasmodium spp. in African black-footed penguin (Sphenicus demersus). J Wildl Dis 30:365–371

    PubMed  CAS  Google Scholar 

  • Grindstaff JL, Brodie EDIII, Ketterson ED (2003) Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc R Soc B 270:2309–2319

    PubMed  Google Scholar 

  • Groothuis TGG, Schwabl H (2002) Determinants of within- and among-clutch variation in levels of maternal hormones in black-headed gull eggs. Funct Ecol 16:281–289

    Google Scholar 

  • Groothuis TGG, Schwabl H (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Phil Trans R Soc B 363:1647–1661

    PubMed  CAS  Google Scholar 

  • Groothuis TGG, Eising CM, Dijkstra C, Müller W (2005a) Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biol Lett 1:78–81

    PubMed  CAS  Google Scholar 

  • Groothuis TGG, Müller W, von Engelhardt N, Carere C, Eising C (2005b) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 29:329–352

    PubMed  CAS  Google Scholar 

  • Groothuis TGG, Eising CM, Blount JD, Surai P, Apanius V, Dijkstra C, Müller W (2006) Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment. J Evol Biol 19:1304–1313

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Hackl R, Bromundt V, Daisley J, Kotrschal K, Möstl E (2003) Distribution and origin of steroid hormones in the yolk of Japanese quail eggs (Coturnix coturnix japonica). J Comp Physiol B 173:327–331

    PubMed  CAS  Google Scholar 

  • 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. Poult Sci 75:1092–1097

    PubMed  CAS  Google Scholar 

  • Hargitai R, Matus Z, Hegyi G, Michl G, Gy Tóth, Török J (2006a) Antioxidants in the egg yolk of a wild passerine: differences between breeding seasons. Comp Biochem Physiol B 143:145–152

    PubMed  Google Scholar 

  • Hargitai R, Prechl J, Török J (2006b) Maternal immunoglobulin concentration in collared flycatcher (Ficedula albicollis) eggs in relation to parental quality and laying order. Funct Ecol 20:829–838

    Google Scholar 

  • Harrison GJ, Harrison LR (1986) Clinical avian medicine and surgery. W.B. Saunders, London

    Google Scholar 

  • Hegner RE, Wingfield JC (1986) Behavioral and endocrine correlates with multiple brooding in the semicolonial house sparrow Passer domesticus. Horm Behav 20:313–326

    PubMed  CAS  Google Scholar 

  • Hoi-Leitner M, Romero-Pujante M, Hoi H, Pavlova A (2001) Food availability and immune capacity in serin (Serinus serinus) nestlings. Behav Ecol Sociobiol 49:333–339

    Google Scholar 

  • Hõrak P, Ots I, Murumägi A (1998) Haematological health state indices of reproducing great tits: a response to brood size manipulation. Funct Ecol 12:750–756

    Google Scholar 

  • Hõrak P, Saks L, Zilmer M, Karu U, Zilmer K (2007) Do dietary carotenoids alleviate the cost of immune activation? An experiment with greenfinches. Am Nat 170:625–635

    PubMed  Google Scholar 

  • Ilmonen P, Hasselquist D, Langefors Å, Wiehn J (2003) Stress, immunocompetence and leukocyte profiles of pied flycatchers in relation to brood size manipulation. Oecologia 136:148–154

    PubMed  Google Scholar 

  • Jawor JM, Young R, Ketterson ED (2006) Females competing to reproduce: dominance matters but testosterone may not. Horm Behav 49:362–368

    PubMed  CAS  Google Scholar 

  • Karlsen R, Slagsvold T (1997) Aggression of female pied flycatchers Ficedula hypoleuca towards caged conspecific female intruders. Fauna Norv C 20:39–47

    Google Scholar 

  • Ketterson ED, Nolan V Jr, Wolf L, Ziegenfus C, Dufty AM, Ball GF Jr, Johnsen TS (1991) Testosterone and avian life histories: the effect of experimentally elevated testosterone on corticosterone and body mass in dark-eyed juncos. Horm Behav 25:489–503

    PubMed  CAS  Google Scholar 

  • Klasing KC (1998) Nutritional modulation of resistance to infectious diseases. Poult Sci 77:1119–1125

    PubMed  CAS  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 

  • Lifjeld JT, Slagsvold T (1990) Manipulations of male parental investment in polygynous pied flycatchers, Ficedula hypoleuca. Behav Ecol 1:48–54

    Google Scholar 

  • Lipar JL, Ketterson ED (2000) Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc R Soc Lond B Biol Sci 267:2005–2010

    CAS  Google Scholar 

  • Löhrl H (1976) Studies of less familiar birds. Collared flycatcher. Br Birds 69:20–26

    Google Scholar 

  • Lundberg A, Alatalo RV, Carlson A, Ulfstrand S (1981) Biometry, habitat distribution and breeding success in the pied flycatcher Ficedula hypoleuca. Ornis Scand 12:68–79

    Google Scholar 

  • MacGregor NA, Cockburn A (2002) Sex differences in parental response to begging nestlings in superb fairy-wrens. Anim Behav 63:923–932

    Google Scholar 

  • Marshall RC, Leisler B, Catchpole CK, Schwabl H (2005) Male song quality affects circulating but not yolk steroid concentrations in female canaries (Serinus canaria). J Exp Biol 208:4593–4598

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Mazuc J, Bonneaud C, Chastel O, Sorci G (2003) Social environment affects female and egg testosterone levels in the house sparrow (Passer domesticus). Ecol Lett 6:1084–1090

    Google Scholar 

  • McGraw KJ, Ardia DR (2005) Sex differences in carotenoid status and immune performance in zebra finches. Evol Ecol Res 7:251–262

    Google Scholar 

  • 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 92:375–380

    PubMed  CAS  Google Scholar 

  • McGraw KJ, Correa SM, Adkins-Regan E (2006) Testosterone upregulates lipoprotein status to control sexual attractiveness in a colorful songbird. Behav Ecol Sociobiol 60:117–122

    Google Scholar 

  • Meijer T, Drent R (1999) Re-examination of the capital and income dichotomy in breeding birds. Ibis 141:399–414

    Google Scholar 

  • Møller AP, Erritzøe J (1996) Parasite virulence and host immune defence: Host immune response is related to nest reuse in birds. Evolution 50:2066–2072

    Google Scholar 

  • Møller AP, Biard C, Blount JD, Houston DC, Ninni P, Saino N, Surai PF (2000) Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Avian Poult Biol Rev 11:137–159

    Google Scholar 

  • Mousseau TA, Fox CW (1998) Maternal effects as adaptations. Oxford University Press, Oxford

    Google Scholar 

  • Müller W, Eising CM, Dijkstra C, Groothuis TGG (2002) Sex differences in yolk hormones depend on maternal social status in leghorn chickens (Gallus gallus domesticus). Proc R Soc Lond B Biol Sci 269:2249–2255

    Google Scholar 

  • Müller W, Groothuis TGG, Dijkstra C, Siitari H, Alatalo RV (2004) Maternal antibody transmission and breeding densities in the black-headed gull Larus ridibundus. Funct Ecol 18:719–724

    Google Scholar 

  • Müller W, Groothuis TGG, Kasprzik A, Dijkstra C, Alatalo RV, Siitari H (2005) Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks. Proc R Soc Lond B Biol Sci 272:1971–1977

    Google Scholar 

  • Navara KJ, Hill GE, Mendonça MT (2005) Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Phys Biochem Zool 78:570–578

    CAS  Google Scholar 

  • Navara KJ, Siefferman LM, Hill GE, Mendonça MT (2006a) Yolk androgens vary inversely to maternal androgens in eastern bluebirds: an experimental study. Funct Ecol 20:449–456

    Google Scholar 

  • Navara KJ, Badyaev AV, Mendonça MT, Hill GE (2006b) Yolk antioxidants vary with male attractiveness and female condition in the house finch (Carpodacus mexicanus). Physiol Biochem Zool 79:1098–1105

    PubMed  CAS  Google Scholar 

  • Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514

    Google Scholar 

  • Ottoson H, Backman J, Smith HG (1997) Begging affects parental effort in the pied flycatcher, Ficedula hypoleuca. Behav Ecol Sociobiol 41:381–384

    Google Scholar 

  • Parsons J (1970) Relationship between egg size and post-hatching chick mortality in the Herring Gull Larus argentatus. Nature 228:1221–1222

    PubMed  CAS  Google Scholar 

  • Pilz KM, Smith HG (2004) Egg yolk androgen levels increase with breeding density in the European starling (Sturnus vulgaris). Funct Ecol 18:58–66

    Google Scholar 

  • Pilz KM, Smith HG, Sandell MI, Schwabl H (2003) Interfemale variation in egg yolk androgen allocation in the European starling: do high-quality females invest more? Anim Behav 65:841–850

    Google Scholar 

  • Porter TE, Hargis BM, Silsby JM, El Halawani ME (1989) Differential steroid production between theca interna and theca externa cells: a three cell model for follicular steroidogenesis in avian species. Endocrinology 125:109–116

    Article  PubMed  CAS  Google Scholar 

  • Råberg L, Grahn M, Hasselquist D, Svensson E (1998) On the adaptive significance of stress-induced immunosuppression. Proc R Soc Lond B Biol Sci 265:1637–1641

    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 

  • Reed WL, Vleck CM (2001) Functional significance of variation in egg-yolk androgens in the American coot. Oecologia 128:164–171

    Google Scholar 

  • Roberts ML, Buchanan KL, Hasselquist D, Evans MR (2007) Effects of testosterone and corticosterone on immunocompetence in the zebra finch. Horm Behav 51:126–134

    PubMed  CAS  Google Scholar 

  • Royle NJ, Surai PF, Hartley IR (2001) Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav Ecol 12:381–385

    Google Scholar 

  • Rubolini D, Romano M, Martinelli R, Saino N (2006) Effects of elevated yolk testosterone levels on survival, growth and immunity of male and female yellow-legged gull chicks. Behav Ecol Sociobiol 59:344–352

    Google Scholar 

  • Ruff MD, Reid WM, Johnson JK (1974) Lowered blood carotenoid levels in chickens infected with coccidia. Poult Sci 53:1801–1809

    PubMed  CAS  Google Scholar 

  • Rutkowska J, Cichoń M, Puerta M, Gil D (2005) Negative effects of elevated testosterone on female fecundity in zebra finches. Horm Behav 47:585–591

    PubMed  CAS  Google Scholar 

  • Safran RJ, Pilz KM, McGraw KJ, Correa SM, Schwabl H (2008) Are yolk androgens and carotenoids in barn swallow eggs related to parental quality? Behav Ecol Sociobiol 62:427–438

    Google Scholar 

  • Saino N, Stradi R, Ninni P, Pini E, Møller AP (1999) Carotenoid plasma concentration, immune profile, and plumage ornamentation of male barn swallows (Hirundo rustica). Am Nat 154:441–448

    PubMed  Google Scholar 

  • Saino N, Martinelli R, Møller AP (2001) Immunoglobulin plasma concentration in relation to egg laying and mate ornamentation of female barn swallows (Hirundo rustica). J Evol Biol 14:95–109

    CAS  Google Scholar 

  • Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, Stradi R (2002) Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proc R Soc Lond B 269:1729–1733

    CAS  Google Scholar 

  • 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 Biol Sci 270:2485–2489

    Google Scholar 

  • Salvante KG, Williams TD (2002) Vitellogenin dynamics during egg-laying: daily variation, repeatability and relationship with egg size. J Avian Biol 33:391–398

    Google Scholar 

  • Sandell MI (1998) Female aggression and the maintenance of monogamy: female behaviour predicts male mating status in European starlings. Proc R Soc Lond B Biol Sci 265:1307–1311

    Google Scholar 

  • Sapolsky RM (1992) Neuroendocrinology of the stress response. In: Becker JB, Breedlove SM, Crews D (eds) Behavioural endocrinology. MA: MIT Press, Cambridge, pp 287–324

    Google Scholar 

  • Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90:11446–11450

    PubMed  CAS  Google Scholar 

  • Schwabl H (1996a) Maternal testosterone in avian egg enhances postnatal growth. Comp Biochem Physiol A 114:271–276

    CAS  Google Scholar 

  • Schwabl H (1996b) Environment modifies the testosterone levels of a female bird and its eggs. J Exp Zool 276:157–163

    PubMed  CAS  Google Scholar 

  • Schwabl H (1997) The contents of maternal testosterone in the house sparrow Passer domesticus eggs vary with breeding conditions. Naturwissenschaften 1984:1–3

    Google Scholar 

  • Senar JC, Polo V, Uribe F, Camerino M (2000) Status signalling, metabolic rate and body mass in the siskin: the cost of being subordinate. Anim Behav 59:103–110

    PubMed  Google Scholar 

  • Slagsvold T, Lifjeld JT (1994) Polygyny in birds: the role of competition between females for male parental care. Am Nat 143:59–94

    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 

  • Smith HG, Ottoson U, Sandell MI (1994a) Intrasexual competition among polygynously mated female starlings (Sturnus vulgaris). Behav Ecol 5:57–63

    Google Scholar 

  • Smith NC, Wallach M, Miller CMD, Morgenstern R, Braun R, Eckert J (1994b) Maternal transmission of immunity to Eimeria maxima: enzyme-linked immunosorbent assay analysis of protective antibodies induced by infection. Infect Immun 62:1348–1357

    PubMed  CAS  Google Scholar 

  • Sockman KW, Schwabl H (2000) Yolk androgens reduce offspring survival. Proc R Soc Lond B Biol Sci 267:1451–1456

    CAS  Google Scholar 

  • Staub N, De Beer M (1997) The role of androgens in female vertebrates. Gen Comp Endocrinol 108:1–24

    PubMed  CAS  Google Scholar 

  • Strasser R, Schwabl H (2004) Yolk testosterone organises behavior and male plumage coloration in house sparrows (Passer domesticus). Behav Ecol Sociobiol 56:491–497

    Google Scholar 

  • Surai PF, Speake BK (1998) Distribution of carotenoids from the yolk to the tissues of the chick embryo. J Nutr Biochem 9:645–651

    CAS  Google Scholar 

  • Surai PF, Noble RC, Speake BK (1999) Relationship between vitamin E content and susceptibility to lipid peroxidation in tissues of the newly hatched chick. Br Poult Sci 40:406–410

    PubMed  CAS  Google Scholar 

  • Svensson E, Merilä J (1996) Molt and migratory condition in blue tits: a serological study. Condor 98:825–831

    Google Scholar 

  • Tanvez A, Parisot M, Chastel O, Leboucher G (2008) Does maternal social hierarchy affect yolk testosterone deposition in domesticated canaries? Anim Behav 75:929–934

    Google Scholar 

  • Tella JL (2002) The evolutionary transition to coloniality promotes higher blood parasitism in birds. J Evol Biol 15:32–41

    Google Scholar 

  • Török J (1986) Food segregation in three hole-nesting bird species during the breeding season. Ardea 74:129–136

    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 

  • Tschirren B, Richner H (2008) Differential effects of yolk hormones on maternal and paternal contribution to parental care. Anim Behav 75:1989–1994

    Google Scholar 

  • Tschirren B, Saladin V, Fitze PS, Schwabl H, Richner H (2005) Maternal yolk testosterone does not modulate parasite susceptibility or immune function in great tit nestlings. J Anim Ecol 74:675–682

    Google Scholar 

  • Tummeleht L, Mägi M, Kilgas P, Mänd R, Hõrak P (2006) Antioxidant protection and plasma carotenoids of incubating great tits (Parus major L.) in relation to health state and breeding conditions. Comp Biochem Physiol 144C:166–172

    CAS  Google Scholar 

  • Verboven N, Evans NP, D’Alba L, Nager RG, Blount JD, Surai PF, Monaghan P (2005) Intra-specific interactions influence egg composition in the lesser black-backed gull (Larus fuscus). Behav Ecol Sociobiol 57:357–365

    Google Scholar 

  • von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proc R Soc Lond B Biol Sci 266:1–12

    Google Scholar 

  • Whittingham L, Schwabl H (2002) Maternal testosterone in tree swallow eggs varies with female aggression. Anim Behav 62:63–67

    Google Scholar 

  • Williams TD (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev 68:35–59

    Google Scholar 

  • Wingfield JC (1994) Hormone-behavior interactions and mating systems in male and female birds. In: Short RV, Balaban E (eds) The differences between the sexes. Cambridge University Press, Cambridge, pp 303–330

    Google Scholar 

  • Woodall AA, Britton G, Jackson MJ (1996) Dietary supplementation with carotenoids: effects on α-tocopherol levels and susceptibility of tissues to oxidative stress. Br J Nutr 76:307–317

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to R. Főző, L.Z. Garamszegi, G. Hegyi, M. Laczi, G. Nagy, B. Rosivall, B. Szigeti and E. Szöllősi for assistance during fieldwork. We are grateful to P. Péczely and Zs. Szőke for laboratory analysis of yolk testosterone. We are indebted to Zs. Greff, S.D. Larcombe, A. Adams and W. Mullen for their invaluable advice and help in the laboratory analyses. We thank G. Hegyi, K.J. Navara, S. Healy, Á. Lendvai and two anonymous reviewers for their helpful comments that greatly improved the manuscript. This study was supported by the Hungarian Scientific Research Fund (OTKA, grants no. T49650 and T49678), the Eötvös Loránd University, the Erdők a Közjóért Alapítvány, and the Pilis Park Forestry. R.H. was supported during her stay at DEEB of the University of Glasgow by an international exchange grant of the Royal Society of Edinburgh. The Hungarian Ministry of Environment and Water provided permissions for the collection of collared flycatcher eggs for this study (permission no. 15951/2005).

Author information

Authors and Affiliations

  1. Behavioural Ecology Group, Department of Systematic Zoology and Ecology, Eötvös Loránd University, Pázmány P. sétány 1/C, H-1117, Budapest, Hungary

    Rita Hargitai, Márton Herényi & János Török

  2. Division of Environmental and Evolutionary Biology, Graham Kerr Building, University of Glasgow, Glasgow, G12 8QQ, Scotland

    Kathryn E. Arnold

  3. Immunology Research Group, Hungarian Academy of Sciences, Pázmány P. sétány 1/C, H-1117, Budapest, Hungary

    József Prechl

  4. Institute of Environmental Sciences, College of Nyíregyháza, Sóstói út 31/B, H-4401, Nyíregyháza, Hungary

    Rita Hargitai

Authors
  1. Rita Hargitai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kathryn E. Arnold
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Márton Herényi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. József Prechl
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. János Török
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rita Hargitai.

Additional information

Communicated by J. Graves

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hargitai, R., Arnold, K.E., Herényi, M. et al. Egg composition in relation to social environment and maternal physiological condition in the collared flycatcher. Behav Ecol Sociobiol 63, 869–882 (2009). https://doi.org/10.1007/s00265-009-0727-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-009-0727-4

Keywords

Search

Navigation