Skip to main content
Log in

Egg coloration in ring-billed gulls (Larus delawarensis): a test of the sexual signaling hypothesis

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

Abstract

Although many avian eggs appear to be cryptically colored, many species also lay vibrant blue green eggs. This seemingly conspicuous coloration has puzzled biologists since Wallace, as natural selection should favor reduced egg visibility to minimize predation pressure. The sexual signaling hypothesis posits that blue green egg coloration serves as a signal of female quality and that males exert post-mating sexual selection on this trait by investing more in the nests of females laying more intensely blue green eggs. This hypothesis has received mixed support to date, and most previous studies have been conducted in cavity-nesting species where male evaluation of his partner’s egg coloration, relative to that of other females, may be somewhat limited. In this study, we test the sexual signaling hypothesis in colonially nesting ring-billed gulls (Larus delawarensis) where males have ample opportunity to assess their mate’s egg coloration relative to that of other females. We used correlational data and an experimental manipulation to test four assumptions and predictions of the sexual signaling hypothesis: (1) blue green pigmentation should be limiting to females; (2) extent of blue green egg coloration should relate to female quality; (3) extent of blue green egg coloration should relate to offspring quality; and (4) males should provide more care to clutches with higher blue green chroma. Our data provide little support for these predictions of the sexual signaling hypothesis in ring-billed gulls. In light of this and other empirical data, we encourage future studies to consider additional hypotheses for the evolution of blue green egg coloration.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alonso-Alvarez C, Tella JL (2001) Effects of experimental food restriction and body-mass changes on the avian T-cell-mediated immune response. Can J Zool 79:101–105

    Article  Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Aviles JM, Soler JJ, Perez-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

    Article  Google Scholar 

  • Baicich PJ, Harrison CJO (1997) A guide to the nests, eggs, and nestlings of North American birds, 2ndnd edn. Academic, San Diego

    Google Scholar 

  • Bakken GS, Vanderbilt VC, Buttermer WA, Dawson WR (1978) Avian eggs: thermoregulatory value of very high near-infrared reflectance. Science 200:321–323

    Article  PubMed  CAS  Google Scholar 

  • Boersma D, Ryder JP (1983) Reproductive performance and body condition of earlier and later nesting ring-billed gulls. J Field Ornith 54:374–380

    Google Scholar 

  • Bolton M (1991) Determinants of chick survival in the lesser black-backed gull—relative contributions of egg size and parental quality. J Anim Ecol 60:949–960

    Article  Google Scholar 

  • Brown KM (1995) Does blood-sampling ring-billed gulls increase parental desertion and chick mortality. Colon Waterbird 18:102–104

    Article  Google Scholar 

  • Buck CL, O'Reilly KA, Kildaw SD (2007) Interannual variability of black-legged kittiwake productivity is reflected in baseline plasma corticosterone. Gen Comp Endocrinol 150:430–436

    Article  PubMed  CAS  Google Scholar 

  • 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 95:713–721

    Article  PubMed  CAS  Google Scholar 

  • Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Erlbaum, New York

    Google Scholar 

  • Colegrave N, Ruxton GD (2003) Confidence intervals are a more useful complement to nonsignificant tests than are power calculations. Behav Ecol 14:446–450

    Article  Google Scholar 

  • Conover MR (1989) Parental care by male–female and female–female pairs of ring-billed gulls. Colon Waterbird 2:148–151

    Article  Google Scholar 

  • Conover MR, Miller DE, Hunt GL (1979) Female–female pairs and other unusual reproductive associations in ring-billed and California gulls. Auk 96:6–9

    Google Scholar 

  • Cott HB (1948) Edibility of the eggs of birds. Nature 161:8–11

    Article  PubMed  CAS  Google Scholar 

  • Cuthill IC (2006) Color perception. In: Hill GE, McGraw KJ (eds) Bird coloration, vol I. Harvard University Press, Cambridge, MA, pp 3–40

    Google Scholar 

  • Darwin C (1871) The descent of man, and selection in relation to sex. Murray, London

    Google Scholar 

  • Davis AK (2005) Effect of handling time and repeated sampling on avian white blood cell counts. J Field Ornith 76:334–338

    Google Scholar 

  • Ding ZK, Xu YQ (2002) Purification and characterization of biliverdin IXα from Atlantic salmon (Salmo salar) bile. Biochemistry (Moscow) 67:927–932

    Article  CAS  Google Scholar 

  • Falchuk KH, Contin JM, Dziedzic TS, Feng Z, French TC, Heffron GJ, Montorzi M (2002) A role for biliverdin IXα in dorsal axis development of Xenopus laevis embryos. PNAS 99:251–256

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Grant MC (1991) Relationships between egg size, chick size at hatching, and chick survival in the whimbrel Numenius phaeopus. Ibis 133:127–133

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Hipfner JM, Gaston AJ (1999) The relationship between egg size and posthatching development in the thick-billed murre. Ecology 80:1289–1297

    Article  Google Scholar 

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

    Google Scholar 

  • Jackson WM (1992) Estimating conspecific nest parasitism in the northern masked weaver based on within-female variability in egg appearance. Auk 109:435–443

    Google Scholar 

  • Kaur H, Hughes MN, Green CJ, Naughton P, Foresti R, Motterlini R (2003) Interaction of bilirubin and biliverdin with reactive nitrogen species. FEBS Lett 543:113–119

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kitaysky AS, Wingfield JC, Piatt JF (1999) Dynamics of food availability, body condition and physiological stress response in breeding black-legged kittiwakes. Funct Ecol 13:577–584

    Article  Google Scholar 

  • Krist M, Grim T (2007) Are blue eggs a sexually selected signal of female collared flycatchers? A cross-fostering experiment. Behav Ecol Sociobiol 61:863–876

    Article  Google Scholar 

  • Lack D (1958) The significance of the colour of Turdine eggs. Ibis 100:145–166

    Article  Google Scholar 

  • Lahti DC (2005) Evolution of bird eggs in the absence of cuckoo parasitism. Proc Natl Acad Sci U S A 102:18057–18062

    Article  PubMed  CAS  Google Scholar 

  • Lahti DC (2008) Population differentiation and rapid evolution of egg color in accordance with solar radiation. Auk 125:796–802

    Article  Google Scholar 

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

    Google Scholar 

  • Lopez-Rull I, Celis P, Gil D (2007) Egg colour covaries with female expression of a male ornament in the spotless starling (Sturnus unicolor). Ethology 113:926–933

    Google Scholar 

  • Lundberg CA, Väisänen RA (1979) Selective correlation of egg size with chick mortality in the black-headed gull (Larus ridibundus). Condor 81:146–156

    Article  Google Scholar 

  • Martinez-de la Puente J, Merino S, Moreno J, Tomas G, Morales J, Lobato E, Garcia-Fraile S, Martinez J (2007) Are eggshell spottiness and colour indicators of health and condition in blue tits Cyanistes caeruleus? J Avian Biol 38:377–384

    Google Scholar 

  • McAldowie AM (1886) Observations on the development and the decay of the pigment layer on birds’ eggs. J Anat Physiol 20:225–237

    Google Scholar 

  • Meathrel CE, Ryder JP (1987) Intraclutch variation in the size, mass and composition of ring-billed gull eggs. Condor 89:364–368

    Article  Google Scholar 

  • Monaghan P, Nager RG, Houston DC (1998) The price of eggs: increased investment in egg production reduces the offspring rearing capacity of parents. Proc R Soc Lond B 265:1731–1735

    Article  Google Scholar 

  • Montgomerie R (2006) Analyzing colors. In: Hill GE, McGraw KJ (eds) Bird coloration, vol I. Harvard University Press, Cambridge, MA, pp 90–148

    Google Scholar 

  • Morales J, Sanz JJ, Moreno J (2006) Egg colour reflects the amount of yolk maternal antibodies and fledging success in a songbird. Biol Lett 2:334–336

    Article  PubMed  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

    Article  Google Scholar 

  • Moreno J, Osorno JL, Morales J, Merino S, Tomas G (2004) Egg colouration and male parental effort in the pied flycatcher Ficedula hypoleuca. J Avian Biol 35:300–304

    Article  Google Scholar 

  • Moreno J, Morales J, Lobato E, Merino S, Tomas G, Martinez-de la Puente J (2005) Evidence for the signaling function of egg color in the pied flycatcher Ficedula hypoleuca. Behav Ecol 16:931–937

    Article  Google Scholar 

  • Moreno J, Lobato E, Morales J, Merino S, Tomás G, de la Puente JM, Sanz JJ, Mateo R, Soler JJ (2006a) Experimental evidence that egg color indicates female condition at laying in a songbird. Behav Ecol 17:651–655

    Article  Google Scholar 

  • Moreno J, Morales J, Lobato E, Tomás G, de la Puente JM (2006b) More colorful eggs induce a higher relative paternal investment in the pied flycatcher Ficedula hypoleuca: a cross-fostering experiment. J Avian Biol 37:555–560

    Article  Google Scholar 

  • Moss R, Watson A, Rothery P, Glennie WW (1981) Clutch size, egg size, hatch weight and laying date in relation to early mortality in red grouse Lagopus lagopus scoticus chicks. Ibis 123:450–462

    Article  Google Scholar 

  • Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045

    Article  Google Scholar 

  • Nakagawa S, Foster MT (2004) The case against retrospective statistical power analyses with an introduction to power analysis. Acta Ethol 7:103–108

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11:19–26

    Article  Google Scholar 

  • Ots I, Hõrak P (1996) Great tits Parus major trade health for reproduction. Proc R Soc Lond B 263:1443–1447

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ricklefs RE (1974) Energetics of reproduction. In: Paynter RA (ed) Avian energetics, vol 15. Nuttall Ornithological Club, Cambridge, pp 152–297

    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

    Article  Google Scholar 

  • Ryder JP (1978) Sexing ring-billed gulls externally. Bird-Banding 49:218–222

    Google Scholar 

  • Ryder JP (1993) Ring-billed gull. In: Poole A, Stettenheim P, Gill F (eds) The birds of North America. The National Academy of Sciences, Philadelphia

    Google Scholar 

  • Šálek M, Cepáková E (2006) Do northern lapwings Vanellus vanellus and little ringed plovers Charadrius dubius rely on egg crypsis during incubation? Folia Zool 55:43–51

    Google Scholar 

  • Salvante KG (2006) Techniques for studying integrated immune function in birds. Auk 123:575–586

    Article  Google Scholar 

  • Sánchez JM, Corbacho C, del Viejo AM, Parejo D (2004) Colony-site tenacity and egg color crypsis in the gull-billed tern. Waterbirds 27:21–30

    Article  Google Scholar 

  • Scalise I, Durantini EN (2004) Photodynamic effect of metallo 5-(4-carboxyphenyl)-10,15,20-tris(4-methylphenyl) porphyrins in biomimetic AOT reverse micelles containing urease. J Photochem Photobiol A 162:105–113

    Article  CAS  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

    Article  Google Scholar 

  • Soler JJ, Møller AP (1996) A comparative analysis of the evolution of variation in appearance of eggs of European passerines in relation to brood parasitism. Behav Ecol 7:89–94

    Article  Google Scholar 

  • Soler JJ, Navarro C, Contreras T, Aviles J, Cuervo J (2008) Sexually selected egg coloration in spotless starlings. Am Nat 171:183–194

    Article  PubMed  Google Scholar 

  • Swynnerton CFM (1916) On the coloration of the mouths and eggs of birds. II. On the coloration of eggs. Ibis 4:529–606

    Article  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, New York, pp 280–298

    Google Scholar 

  • Verboven N, Monaghan P, Evans DM, Schwabl H, Evans N, Whitelaw C, Nager RG (2003) Maternal condition, yolk androgens and offspring performance: a supplemental feeding experiment in the lesser black-backed gull (Larus fuscus). Proc R Soc Lond B 270:2223–2232

    Article  Google Scholar 

  • Victoria JK (1972) Clutch characteristics and egg discriminative ability of African village weaverbird Ploceus cucullatus. Ibis 114:367–376

    Article  Google Scholar 

  • Wallace AR (1889) Darwinism: an exposition of the theory of natural selection with some its applications. Macmillan, London

    Google Scholar 

  • Zhao R, Xu GY, Liu ZZ, Li JY, Yang N (2006) A study on eggshell pigmentation: biliverdin in blue-shelled chickens. Poult Sci 85:546–549

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are very grateful to Jim Quinn for the advice, guidance, and logistical support he provided throughout this project. We thank M. Vujacic, S. Mai, and especially A. Mistakidis for their efforts in the field. The Doucet Lab provided insightful comments on the manuscript. We also thank anonymous reviewers and the editorial staff for their helpful suggestions. Our study was funded by an Explorer’s Club grant to D.H. and by research and equipment grants from the Natural Sciences and Engineering Research Council of Canada and the University of Windsor to S.M.D. This study was conducted under compliance of regulations provided by the Canadian Council on Animal Care.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel Hanley.

Additional information

Communicated by K. McGraw

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hanley, D., Doucet, S.M. Egg coloration in ring-billed gulls (Larus delawarensis): a test of the sexual signaling hypothesis. Behav Ecol Sociobiol 63, 719–729 (2009). https://doi.org/10.1007/s00265-008-0705-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-008-0705-2

Keywords

Navigation