Skip to main content
SpringerLink
Log in

Environmental conditions influence egg color of reed warblers Acrocephalus scirpaceus and their parasite, the common cuckoo Cuculus canorus

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

Abstract

The outer layer of the eggshell in birds is in many cases covered by pigments that are assumed to be genetically determined traits with a negligible environmental component. To test the hypothesis that spring environmental conditions (i.e., temperature and rainfall) may affect bird egg pigmentation, we measured by spectrophotometry and photography egg coloration and spottiness on reed warbler (Acrocephalus scirpaceus L.) clutches parasitized by the common cuckoo (Cuculus canorus L.) collected over a period of 24 years and preserved in the Zoological Museum, Copenhagen, Denmark. In addition, we investigated whether spring environmental conditions may influence the coevolutionary relationship between the cuckoo and its host via changes in cuckoo–host egg matching. Generalized mixed models revealed that reed warbler eggs were more brilliant in those springs with a higher rainfall and tended to be bluer and greener in springs with a lower relative temperature. On the other hand, cuckoo eggs were bluer and greener in springs with a higher rainfall. Cuckoo–host egg matching in blue-greenness and spottiness was better in springs with a higher rainfall. These results provide support for the existence of an environmental component on bird egg coloration and suggest that environmental factors may potentially affect the outcome of important features of the arms race between cuckoos and reed warblers.

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

  • Antonov A, Stokke BG, Moksnes A, Røskaft E (2006) Egg rejection in marsh warblers (Acrocephalus palustris) heavily parasitized by common cuckoos (Cuculus canorus). Auk 123:419–430

    Article  Google Scholar 

  • Avilés JM, Møller AP (2003) Meadow pipits (Anthus pratensis) egg appearance in cuckoo (Cuculus canorus) sympatric and allopatric populations. Biol J Linn Soc 79:543–549

    Article  Google Scholar 

  • Avilés JM, Møller AP (2004) How is host egg mimicry maintained in the cuckoo (Cuculus canorus)? Biol J Linn Soc 82:57–68

    Article  Google Scholar 

  • Avilés JM, Soler JJ, Soler M, Møller AP (2004) Egg appearance and rejection behaviour in magpies. Anim Behav 67:951–958

    Article  Google Scholar 

  • Avilés JM, Stokke BG, Moksnes A, Røskaft E, Møller AP (2006a) Nest predation and the evolution of egg appearance in passerine birds in Europe and North America. Evol Ecol Res 8:493–513

    Google Scholar 

  • Avilés JM, Stokke BG, Moksnes A, Røskaft E, Åsmul M, Møller AP (2006b) Rapid increase in cuckoo egg matching in a recently parasitized reed warbler population. J Evol Biol 0:000–000

    Google Scholar 

  • Avilés JM, Soler JJ, Pérez-Contreras T, Soler M, Møller AP (2006c) Ultraviolet colour vision of great spotted cuckoo eggs and egg rejection by magpies. Behav Ecol 17:310–314

    Article  Google Scholar 

  • Birkhead T (1978) Behavioural adaptations to high density nesting in the common guillemot Uria aalge. Anim Behav 26:321–331

    Article  Google Scholar 

  • Brooke MDL, Davies NB (1988) Egg mimicry by cuckoos Cuculus canorus in relation to discrimination by hosts. Nature 335:630–632

    Article  Google Scholar 

  • Cherry MI, Bennett ATD (2001) Egg colour matching in an African cuckoo, as revealed by ultraviolet–visible reflectance spectrophotometry. Proc R Soc Lond B 26:565–571

    Article  Google Scholar 

  • Collias EC (1984) Inheritance of egg-color polymorphism in the village weaver (Ploceus cucullatus). Auk 110:683–692

    Google Scholar 

  • Cramp S (1998) Cramp’s the complete birds of the Western Palearctic. Optimedia. Oxford University Press, Oxford

    Google Scholar 

  • Cuthill IC, Bennett ATD, Partridge JC, Maier EJ (1999) Plumage reflectance and the objective assessment of avian sexual dichromatism. Am Nat 153:183–200

    Article  Google Scholar 

  • Davies NB (2000) Cuckoos, cowbirds and other cheats. T & AD Poyser, London

    Google Scholar 

  • Davies NB, Brooke MDL (1988) Cuckoos versus reed warblers: adaptations and counteradaptations. Anim Behav 36:262–284

    Article  Google Scholar 

  • Davies NB, Brooke MDL (1989) An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its host. II. Host egg marking, chicks discrimination and general discussion. J Anim Ecol 58:225–236

    Article  Google Scholar 

  • Dunn PO, Winkler DW (1999) Climate change has affected breeding date of tree swallows throughout North America. Proc R Soc Lond B 266:2487–2490

    Article  Google Scholar 

  • Endler JA, Thery M (1996) Interacting effects of lek placement, display behavior, ambient light, and color patterns in three neotropical forest-dwelling birds. Am Nat 148:421–452

    Article  Google Scholar 

  • Gosler AG, Barnett PR, Reynolds SJ (2000) Inheritance and variation in eggshell patterning in the great tit Parus major. Proc R Soc Lond B 267:2469–2473

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Honza M, Procházka P, Stokke BG, Moksnes A, Røskaft E, Ĉapek Jr M, Mrlík V (2004) Are blackcaps current winners in the coevolutionary struggle against the common cuckoo? J Ethol 22:175–180

    Article  Google Scholar 

  • Hughes BO, Gilbert AB, Brown MF (1986) Categorisation and causes of abnormal eggshells: relationship with stress. Br Poult Sci 27:325–337

    PubMed  CAS  Google Scholar 

  • Jones J, Doran PJ, Holmes RT (2003) Climate and food synchronize regional forest bird abundances. Ecology 84:3024–3032

    Google Scholar 

  • Joseph NS, Robinson NA, Renema RA, Robinson FE (1999) Shell quality and color variation in broiler breeder eggs. J Appl Poult Res 8:70–74

    Google Scholar 

  • Karcza Z, Moskat C, Cherry MI, Kisbenedek T (2003) Experimental manipulation of intraclutch variation in the great reed warbler shows no effect on rejection of parasitic eggs. Ethology 109:15–22

    Article  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 

  • Langmore NE, Hunt S, Kilner R (2003) Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature 422:157–160

    Article  PubMed  CAS  Google Scholar 

  • Lehikoinen E, Sparks TH, Zalakevicius M (2004) Arrival and departure dates. In: Møller AP, Fieldler W, Bethold P (eds) Birds and climate change. Elsevier, Leiden, pp 1–28

    Chapter  Google Scholar 

  • Lotem A, Nakamura H, Zahavi A (1992) Rejection of cuckoo eggs in relation to host age: a possible evolutionary equilibrium. Behav Ecol 3:128–132

    Google Scholar 

  • McDonagh AF (2001) Turning green to gold. Nat Struct Biol 8:198–200

    Article  PubMed  CAS  Google Scholar 

  • Moksnes A, Røskaft E (1995) Egg-morphs and host preference in the common cuckoo (Cuculus canorus): an analysis of cuckoo and host eggs from European museum collections. J Zool 236:625–648

    Article  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, 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 16:931–937

    Article  Google Scholar 

  • Neuzil J, Stocker R (1993) Bilirubin attenuates radical-mediated damage to serum albumin. FEBS Lett 331:281–284

    Article  PubMed  CAS  Google Scholar 

  • Øien IJ, Moksnes A, Røskaft E (1995) Evolution of variation in egg color and marking pattern in European passerines: adaptations in a coevolutionary arms-race with the cuckoo, Cuculus canorus. Behav Ecol 6:166–174

    Google Scholar 

  • Payne RB (1973) Individual laying histories and the clutch size and number of eggs of parasitic cuckoos. Condor 75:414–438

    Google Scholar 

  • Payne RB (1974) The evolution of clutch size and reproductive rates in parasitic cuckoos. Evolution 28:169–181

    Article  Google Scholar 

  • Polis GA, Hurd SD, Jackson CT, Pinero FS (1997) El Niño effects on the dynamics and control of an island ecosystem in the Gulf of California. Ecology 78:1884–1897

    Article  Google Scholar 

  • Punnett RC (1933) Inheritance of egg colour in the “parasitic” cuckoo. Nature 132:892–893

    Google Scholar 

  • Punnett RC, Bailey PG (1920) Genetic studies in poultry. II. Inheritance of colour and broodiness. J Genet 10:277–292

    Article  Google Scholar 

  • Sillett TS, Holmes RT, Sherry TW (2000) Impacts of a global climate cycle on population dynamics of a migratory songbird. Science 288:2040–2042

    Article  PubMed  CAS  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

    Google Scholar 

  • Soler JJ, Moreno J, Avilés JM, Møller AP (2005) Blue and green egg color intensity is associated with parental effort and mating system in passerines: support for the sexual selection hypothesis. Evolution 59:636–644

    Article  PubMed  Google Scholar 

  • Soler M, Møller AP (1990) Duration of sympatry and coevolution between great spotted cuckoo and its magpie host. Nature 343:748–750

    Article  Google Scholar 

  • Solis JC, de Lope F (1995) Nest and egg crypsis in the ground nesting stone curlew Burhinus oedicnemus. J Avian Biol 26:135–138

    Google Scholar 

  • Solomon SE, Bain MM, Cranstoun S, Mascimento V (1994) Hen’s eggshell structure and function. In: Board RG, Fuller R (eds) Microbiology of the Avian Egg. Chapman and Hall, London, pp 1–24

    Google Scholar 

  • 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 266:1483–1488

    Article  Google Scholar 

  • Stokke BG, Moksnes A, Røskaft E (2002) Obligate brood parasites as selective agents for evolution of egg appearance in passerine birds. Evolution 56:199–205

    Article  PubMed  Google Scholar 

  • Stokke BG, Rudolfsen G, Moksnes A, Røskaft E (2004) Rejection of conspecific eggs in Chaffinches: the effect of age and clutch characteristics. Ethology 110:459–470

    Article  Google Scholar 

  • Tinbergen N, Broekhuysen GJ, Feekes F, Houghton JC, Kruuk H, Szulc E (1962) Eggshell removal by the black-headed gull, Larus ridibundus L.: a behaviour component of camouflage. Behaviour 19:74–117

    Google Scholar 

  • Torti VM, Dunn PO (2005) Variable effects of climate change on six species of North American birds. Oecologia 145:486–495

    Article  PubMed  Google Scholar 

  • Underwood TJ, Sealy SG (2002) Adaptive significance of egg coloration. In: Deeming DC (eds) Avian Incubation. Oxford University Press, Oxford, pp 280–298

    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 266:1–12

    Article  Google Scholar 

  • Weidinger K (2001) Does egg colour affect predation rate on open passerine nests? Behav Ecol Sociobiol 49:456–464

    Article  Google Scholar 

  • Wyllie I (1981) The cuckoo. Batsford, London

    Google Scholar 

Download references

Acknowledgements

We thank J. Fjeldså and J. Bolding of the ornithological section of the Zoological Museum of the University of Copenhagen for help and facilities during data collection. M. Åsmul photographed the clutches and J. J. Soler and I. C. Cuthill made very useful suggestions on a previous draft of the manuscript. M. Soler and two anonymous referees also made very useful suggestions on a previous draft of the manuscript. This research was funded by a European Community Postdoctoral Grant (MCFI-2000-00023) to J. M. A. and by the Research Council of Norway (grant no. 151641/432) to B. G. S. The Danish Meteorological Institute kindly provided access to weather data.

Author information

Authors and Affiliations

  1. Estación Experimental de Zonas Áridas (C.S.I.C), General Segura 1, Almería, 04001, Spain

    Jesús M. Avilés

  2. Department of Biology, Norwegian University of Science and Technology, NTNU, 7491, Trondheim, Norway

    Bård G. Stokke, Arne Moksnes & Eivin Røskaft

  3. Laboratorie de Parasitologie Evolutive, CNRS UMR 7103, Université Pierre et Marie Curie, 7 quai St Bernard, Case 237, 75252, Paris Cedex 05, France

    Anders P. Møller

Authors
  1. Jesús M. Avilés
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bård G. Stokke
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arne Moksnes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eivin Røskaft
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anders P. Møller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jesús M. Avilés.

Additional information

Communicated by M. Soler

Rights and permissions

Reprints and permissions

About this article

Cite this article

Avilés, J.M., Stokke, B.G., Moksnes, A. et al. Environmental conditions influence egg color of reed warblers Acrocephalus scirpaceus and their parasite, the common cuckoo Cuculus canorus . Behav Ecol Sociobiol 61, 475–485 (2007). https://doi.org/10.1007/s00265-006-0275-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-006-0275-0

Keywords

Search

Navigation