, Volume 101, Issue 5, pp 417–426 | Cite as

Host genotype and age have no effect on rejection of parasitic eggs

  • Petr ProcházkaEmail author
  • Hana Konvičková-Patzenhauerová
  • Milica Požgayová
  • Alfréd Trnka
  • Václav Jelínek
  • Marcel Honza
Original Paper


Egg rejection belongs to a widely used host tactic to prevent the costs incurred by avian brood parasitism. However, the genetic basis of this behaviour and the effect of host age on the probability of rejecting the parasitic egg remain largely unknown. Here, we used a set of 15 polymorphic microsatellite loci, including a previously detected candidate locus (Ase64), to link genotypes of female great reed warblers (Acrocephalus arundinaceus), a known rejecter, with their egg rejection responses in two host populations. We also tested whether host female age, as a measure of the experience with own eggs, plays a role in rejection of common cuckoo (Cuculus canorus) eggs. We failed to find any consistent association of egg rejection responses with host female genotypes or age. It seems that host decisions on egg rejection show high levels of phenotypic plasticity and are likely to depend on the spatiotemporal variation in the parasitism pressure. Future studies exploring the repeatability of host responses towards parasitic eggs and the role of host individual experience with parasitic eggs would greatly improve our understanding of the variations in host behaviours considering the persistence of brood parasitism in host populations with rejecter phenotypes.


Avian brood parasitism Cuckoo Egg recognition Genetic association Host responses Microsatellites 



We thank T. Bolcková, M. Čapek, M. Kašová, K. Morongová, P. Prokop, Z. Šebelíková, M. Šulc, M. Trnka and B. Trnková for their invaluable assistance in the field. We are obliged to the management of the Fish Farm Hodonín, the Slovak Fishing Association and local conservation authorities for permissions to conduct the fieldwork. This work was supported by the Grant Agency of the Academy of Sciences of the Czech Republic (grant number IAA600930903), Czech Science Foundation (grant number P506/12/2404) and by the institutional support (RVO: 68081766). The manuscript benefited from comments of four anonymous referees.

Ethical standards

The experiments comply with the current laws of the countries in which they were performed. The fieldwork in the Czech Republic adhered to the Animal Care Protocol of the Academy of Sciences of the Czech Republic (licence number 0008/98-M103) and the current Czech Law on the Protection of Animals Against Mistreatment. Licences to perform the research and bird ringing in Slovakia were issued by the Ministry of Environment of the Slovak Republic (licence numbers 269/132/05-5.1pil and 7230/2008-2.1pil).

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Amundsen T, Brobakken PT, Moksnes A, Røskaft E (2002) Rejection of common cuckoo Cuculus canorus eggs in relation to female age in the bluethroat Luscinia svecica. J Avian Biol 33:366–370CrossRefGoogle Scholar
  2. Avilés JM (2008) Egg colour mimicry in the common cuckoo Cuculus canorus as revealed by modelling host retinal function. Proc R Soc B 275:2345–2352PubMedCentralPubMedCrossRefGoogle Scholar
  3. Avilés JM, Vikan JR, Fossøy F, Antonov A, Moksnes A, Røskaft E, Stokke BG (2010) Avian color perception predicts behavioral responses to experimental brood parasitism in chaffinches. J Evol Biol 23:293–301PubMedCrossRefGoogle Scholar
  4. Bán M, Moskát C, Barta Z, Hauber ME (2013) Simultaneous viewing of own and parasitic eggs is not required for egg rejection by a cuckoo host. Behav Ecol 24:1014–1021CrossRefGoogle Scholar
  5. Bártol I, Karcza Z, Moskát C, Røskaft E, Kisbenedek T (2002) Responses of great reed warblers Acrocephalus arundinaceus to experimental brood parasitism: the effects of a cuckoo Cuculus canorus dummy and egg mimicry. J Avian Biol 33:420–425CrossRefGoogle Scholar
  6. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300Google Scholar
  7. Bensch S, Hasselquist D, Nielsen B, Hansson B (1998) Higher fitness for philopatric than for immigrant males in a semi-isolated population of great reed warblers. Evolution 52:877–883CrossRefGoogle Scholar
  8. Brooke ML, Davies NB, Noble DG (1998) Rapid decline of host defences in response to reduced cuckoo parasitism: behavioural flexibility of reed warblers in a changing world. Proc R Soc B 265:1277–1282PubMedCentralCrossRefGoogle Scholar
  9. Cracraft J, Barker FK, Braun M, Harshman J, Dyke GJ, Feinstein J, Stanley S, Cibois A, Schikler P, Beresford P, Garcia-Moreno J, Sorenson MD, Yuri T, Mindell DP (2004) Phylogenetic relationships among modern birds (Neornithes): toward an avian tree of life. In: Cracraft J, Donoghue MJ (eds) Assembling the tree of life. Oxford University Press, Oxford, pp 468–489Google Scholar
  10. Crawley MJ (2007) The R book. Wiley, ChichesterCrossRefGoogle Scholar
  11. Davies NB (2000) Cuckoos, cowbirds and other cheats. T and AD Poyser, LondonGoogle Scholar
  12. Davies NB (2011) Cuckoo adaptations: trickery and tuning. J Zool 284:1–14CrossRefGoogle Scholar
  13. Davies NB, de Brooke ML (1988) Cuckoos versus reed warblers: adaptations and counteradaptations. Anim Behav 36:262–284CrossRefGoogle Scholar
  14. Davies NB, de Brooke ML, Kacelnik A (1996) Recognition errors and probability of parasitism determine whether reed warblers should accept or reject mimetic cuckoo eggs. Proc R Soc B 263:925–931CrossRefGoogle Scholar
  15. Dawson DA, Åkesson M, Burke T, Pemberton JM, Slate J, Hansson B (2007) Gene order and recombination rate in homologous chromosome regions of the chicken and a passerine bird. Mol Biol Evol 24:1537–1552PubMedCrossRefGoogle Scholar
  16. Dawson DA, Burke T, Hansson B, Pandhal J, Hale MC, Hinten GH, Slate J (2006) A predicted microsatellite map of the passerine genome based on chicken–passerine sequence similarity. Mol Ecol 15:1299–1320PubMedCrossRefGoogle Scholar
  17. Fitzpatrick MJ, Ben-Shahar Y, Smid HM, Vet LEM, Robinson GE, Sokolowski MB (2005) Candidate genes for behavioural ecology. Trends Ecol Evol 20:96–104PubMedCrossRefGoogle Scholar
  18. Fregin S, Haase M, Olsson U, Alström P (2009) Multi-locus phylogeny of the family Acrocephalidae (Aves: Passeriformes)—the traditional taxonomy overthrown. Mol Phylogen Evol 52:866–878CrossRefGoogle Scholar
  19. Gärtner K (1981) Das Wegnehmen von Wirtsvogeleiern durch den Kuckuck (Cuculus canorus). Ornithol Mitt 33:115–131Google Scholar
  20. Gehringer F (1979) Étude sur le pillage par le coucou, Cuculus canorus, des oeufs de la rousserolle effarvatte. Nos Oiseaux 35:1–16Google Scholar
  21. Gomez D (2010) AVICOL v5. a program to analyse spectrometric data. Available from
  22. Grim T (2002) Why is mimicry in cuckoo eggs sometimes so poor? J Avian Biol 33:302–305CrossRefGoogle Scholar
  23. Hansson B, Åkesson M, Slate J, Pemberton JM (2005) Linkage mapping reveals sex-dimorphic map distances in a passerine bird. Proc R Soc B 272:2289–2298PubMedCentralPubMedCrossRefGoogle Scholar
  24. Hansson B, Bensch S, Hasselquist D, Lillandt B-G, Wennerberg L, Von Schantz T (2000) Increase of genetic variation over time in a recently founded population of great reed warblers (Acrocephalus arundinaceus) revealed by microsatellites and DNA fingerprinting. Mol Ecol 9:1529–1538PubMedCrossRefGoogle Scholar
  25. Honza M, Požgayová M, Procházka P, Tkadlec E (2007) Consistency in egg rejection behaviour: responses to repeated brood parasitism in the blackcap (Sylvia atricapilla). Ethology 113:344–351CrossRefGoogle Scholar
  26. Honza M, Procházka P, Morongová K, Čapek M, Jelínek V (2011) Do nest light conditions affect rejection of parasitic eggs? A test of the light environment hypothesis. Ethology 117:539–546CrossRefGoogle Scholar
  27. Honza M, Šulc M, Požgayová M, Jelínek V, Procházka P (2014) Brood parasites lay eggs matching the appearance of host clutches. Proc R Soc B 281:20132665. doi: 10.1098/rspb.2013.2665 PubMedCrossRefGoogle Scholar
  28. Hauber ME, Moskát C, Bán M (2006) Experimental shift in hosts’ acceptance threshold of inaccurate-mimic brood parasite eggs. Biol Lett 2:177–180PubMedCentralPubMedCrossRefGoogle Scholar
  29. Hauber ME, Sherman PW (2001) Self-referent phenotype matching: theoretical considerations and empirical evidence. Trends Neurosci 24:609–616PubMedCrossRefGoogle Scholar
  30. Kalinowski ST, Wagner AP, Taper ML (2006) ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6:576–579CrossRefGoogle Scholar
  31. Krüger O (2007) Cuckoos, cowbirds and hosts: adaptations, trade-offs and constraints. Phil Trans R Soc B 362:1873–1886PubMedCentralPubMedCrossRefGoogle Scholar
  32. Lahti DC, Lahti AR (2002) How precise is egg discrimination in weaverbirds? Anim Behav 63:1135–1142CrossRefGoogle Scholar
  33. Lindholm AK, Thomas RJ (2000) Differences between populations of reed warblers in defences against brood parasitism. Behaviour 137:25–42CrossRefGoogle Scholar
  34. Lotem A, Nakamura H, Zahavi A (1992) Rejection of cuckoo eggs in relation to host age: a possible evolutionary equilibrium. Behav Ecol 3:128–132CrossRefGoogle Scholar
  35. Lotem A, Nakamura H, Zahavi A (1995) Constraints on egg discrimination and cuckoo–host co-evolution. Anim Behav 49:1185–1209CrossRefGoogle Scholar
  36. Marchetti K (2000) Egg rejection in a passerine bird: size does matter. Anim Behav 59:877–883PubMedCrossRefGoogle Scholar
  37. Martín-Gálvez D, Soler JJ, Martínez JG, Krupa AP, Richard M, Soler M, Møller AP, Burke T (2006) A quantitative trait locus for recognition of foreign eggs in the host of a brood parasite. J Evol Biol 19:543–550PubMedCrossRefGoogle Scholar
  38. Martín-Gálvez D, Soler JJ, Martínez JG, Krupa AP, Soler M, Burke T (2007) Cuckoo parasitism and productivity in different magpie subpopulations predict frequencies of the 457 bp allele: a mosaic of coevolution at a small geographic scale. Evolution 61:2340–2348PubMedCrossRefGoogle Scholar
  39. Martínez JG, Soler JJ, Soler M, Møller AP, Burke T (1999) Comparative population structure and gene flow of a brood parasite, the great spotted cuckoo (Clamator glandarius), and its primary host, the magpie (Pica pica). Evolution 53:269–278CrossRefGoogle Scholar
  40. Moksnes A (1992) Egg recognition in chaffinches and bramblings. Anim Behav 44:993–995CrossRefGoogle Scholar
  41. Moksnes A, Røskaft E, Hagen LG, Honza M, Mørk C, Olsen PH (2000) Common cuckoo Cuculus canorus and host behaviour at reed warbler Acrocephalus scirpaceus nests. Ibis 142:247–258CrossRefGoogle Scholar
  42. Moskát C, Bán M, Székely T, Komdeur J, Lucassen RWG, van Boheemen LA, Hauber ME (2010) Discordancy or template-based recognition? Dissecting the cognitive basis of the rejection of foreign eggs in hosts of avian brood parasites. J Exp Biol 213:1976–1983PubMedCrossRefGoogle Scholar
  43. Moskát C, Hauber ME (2007) Conflict between egg recognition and egg rejection decisions in common cuckoo (Cuculus canorus) hosts. Anim Cogn 10:377–386PubMedCrossRefGoogle Scholar
  44. Moskát C, Hauber ME, Elek Z, Gommers M, Bán M, Groenewoud F, Versluijs TSL, Hoetz CWA, Komdeur J (2014) Foreign egg retention by avian hosts in repeated brood parasitism: why do rejecters accept? Behav Ecol Sociobiol 68:403–413CrossRefGoogle Scholar
  45. Moskát C, Honza M (2002) European cuckoo Cuculus canorus parasitism and host’s rejection behaviour in a heavily parasitized great reed warbler Acrocephalus arundinaceus population. Ibis 144:614–622CrossRefGoogle Scholar
  46. Moskát C, Takasu F, Muñoz AR, Nakamura H, Bán M, Barta Z (2012) Cuckoo parasitism on two closely-related Acrocephalus warblers in distant areas: a case of parallel coevolution? Chinese Birds 3:320–329CrossRefGoogle Scholar
  47. Nishiumi I, Yamagishi S, Maekawa H, Shimoda C (1996) Paternal expenditure is related to brood sex ratio in polygynous great reed warblers. Behav Ecol Sociobiol 39:211–217CrossRefGoogle Scholar
  48. Øien IJ, Moksnes A, Røskaft E, Honza M (1998) Costs of cuckoo Cuculus canorus parasitism to reed warblers Acrocephalus scirpaceus. J Avian Biol 29:209–215CrossRefGoogle Scholar
  49. Otsuka R, Nishiumi I, Wada M (2003) Characterization of 12 polymorphic microsatellite loci in the Japanese bush warbler Cettia diphone. Mol Ecol Notes 3:44–46CrossRefGoogle Scholar
  50. Planqué R, Britton NF, Franks NR, Peletier MA (2002) The adaptiveness of defence strategies against cuckoo parasitism. Bull Math Biol 64:1045–1068PubMedCrossRefGoogle Scholar
  51. Požgayová M, Procházka P, Honza M (2009) Sex-specific defence behaviour against brood parasitism in a host with female-only incubation. Behav Process 81:34–38CrossRefGoogle Scholar
  52. Pritchard JK, Rosenberg NA (1999) Use of unlinked genetic markers to detect population stratification in association studies. Am J Hum Genet 65:220–228PubMedCentralPubMedCrossRefGoogle Scholar
  53. Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000) Association mapping in structured populations. Am J Hum Genet 67:170–181PubMedCentralPubMedCrossRefGoogle Scholar
  54. Procházka P, Honza M (2003) Do common whitethroats (Sylvia communis) discriminate against alien eggs? J Ornithol 144:354–363CrossRefGoogle Scholar
  55. Procházka P, Jelínek V, Požgayová M, Honza M (2012) How to age great reed warblers (Acrocephalus arundinaceus) after complete moult. Sylvia 48:57–73Google Scholar
  56. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from:
  57. Rensch B (1925) Verhalten von Singvögeln bei Aenderung des Geleges. Ornithol Monatsber 33:169–173Google Scholar
  58. Richardson DS, Jury FL, Dawson DA, Salgueiro P, Komdeur J, Burke T (2000) Fifty Seychelles warbler (Acrocephalus sechellensis) microsatellite loci polymorphic in Sylviidae species and their cross-species amplification in other passerine birds. Mol Ecol 9:2226–2232PubMedCrossRefGoogle Scholar
  59. Rodríguez-Gironés MA, Lotem A (1999) How to detect a cuckoo egg: a signal-detection theory model for recognition and learning. Am Nat 153:633–648CrossRefGoogle Scholar
  60. Rothstein SI (1974) Mechanisms of avian egg recognition: possible learned and innate factors. Auk 91:796–807CrossRefGoogle Scholar
  61. Rothstein SI (1978) Mechanisms of avian egg recognition: additional evidence for learned components. Anim Behav 26:671–677CrossRefGoogle Scholar
  62. Rothstein SI (1990) A model system for co-evolution: avian brood parasitism. Annu Rev Ecol Syst 21:481–508CrossRefGoogle Scholar
  63. Rothstein SI, Robinson SK (eds) (1998) Parasitic birds and their hosts: studies in coevolution. Oxford University Press, New YorkGoogle Scholar
  64. Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Res 8:103–106CrossRefGoogle Scholar
  65. Saladin V, Bonfils D, Binz T, Richner H (2003) Isolation and characterization of 16 microsatellite loci in the great tit Parus major. Mol Ecol Notes 3:520–522CrossRefGoogle Scholar
  66. Samaš P, Hauber ME, Cassey P, Grim T (2011) Repeatability of foreign egg rejection: testing the assumptions of co-evolutionary theory. Ethology 117:606–619CrossRefGoogle Scholar
  67. Schulze-Hagen K (1992) Parasitierung und Brutverluste durch den Kuckuck (Cuculus canorus) bei Teich- und Sumpfrohrsänger (Acrocephalus scirpaceus, A. palustris) in Mittel- und Westeuropa. J Ornithol 133:237–249CrossRefGoogle Scholar
  68. Sealy SG (1995) Burial of cowbird eggs by parasitized yellow warblers: an empirical and experimental study. Anim Behav 49:877–889CrossRefGoogle Scholar
  69. Soler JJ, Martínez JG, Soler M, Møller AP (1999) Genetic and geographic variation in rejection behaviour of cuckoo eggs by European magpie populations: an experimental test of rejecter-gene flow. Evolution 53:947–956CrossRefGoogle Scholar
  70. Soler M, Martín-Vivaldi M, Fernández-Morante J (2012) Conditional response by hosts to parasitic eggs: the extreme case of the rufous-tailed scrub robin. Anim Behav 84:421–426CrossRefGoogle Scholar
  71. Soler M, Palomino JJ, Martín-Vivaldi M, Soler JJ (2000) Lack of consistency in the response of rufous-tailed scrub robins Cercotrichas galactotes towards parasitic common cuckoo eggs. Ibis 142:139–158Google Scholar
  72. Soler M, Ruiz-Castellano C, Carra LG, Ontanilla J, Martín-Gálvez D (2013) Do first-time breeding females imprint on their own eggs? Proc R Soc B 280:20122518PubMedCentralPubMedCrossRefGoogle Scholar
  73. Stokke BG, Hafstad I, Rudolfsen G, Moksnes A, Møller AP, Røskaft E, Soler M (2008) Predictors of resistance to brood parasitism within and among reed warbler populations. Behav Ecol 19:612–620CrossRefGoogle Scholar
  74. Stokke BG, Moksnes A, Røskaft E (2005) The enigma of imperfect adaptations in hosts of avian brood parasites. Ornithol Sci 4:17–29CrossRefGoogle Scholar
  75. 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 B 266:1483–1488PubMedCentralCrossRefGoogle Scholar
  76. Stokke BG, Rudolfsen G, Moksnes A, Røskaft E (2004) Rejection of conspecific eggs in chaffinches: the effect of age and clutch characteristics. Ethology 110:459–470CrossRefGoogle Scholar
  77. Stokke BG, Takasu F, Moksnes A, Røskaft E (2007) The importance of clutch characteristics and learning for antiparasite adaptations in hosts of avian brood parasites. Evolution 61:2212–2228PubMedCrossRefGoogle Scholar
  78. Storey JD (2002) A direct approach to false discovery rates. J R Stat Soc B 64:479–498CrossRefGoogle Scholar
  79. Takasu F (1998) Modelling the arms race in avian brood parasitism. Evol Ecol 12:969–987CrossRefGoogle Scholar
  80. Trnka A, Požgayová M, Procházka P, Prokop P, Honza M (2012) Breeding success of a brood parasite is associated with social mating status of its host. Behav Ecol Sociobiol 66:1187–1194CrossRefGoogle Scholar
  81. Welbergen JA, Davies NB (2009) Strategic variation in mobbing as a front line of defence against brood parasitism. Curr Biol 19:235–240PubMedCrossRefGoogle Scholar
  82. Wyllie I (1975) Study of cuckoos and reed warblers. Brit Birds 68:369–378Google Scholar
  83. Zondervan KT, Cardon LR (2004) The complex interplay among factors that influence allelic association. Nature Rev Genet 5:89–101PubMedCrossRefGoogle Scholar
  84. Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data. SpringerGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Petr Procházka
    • 1
    Email author
  • Hana Konvičková-Patzenhauerová
    • 1
  • Milica Požgayová
    • 1
  • Alfréd Trnka
    • 2
  • Václav Jelínek
    • 1
  • Marcel Honza
    • 1
  1. 1.Institute of Vertebrate BiologyAcademy of Sciences of the Czech RepublicBrnoCzech Republic
  2. 2.Department of BiologyUniversity of TrnavaTrnavaSlovakia

Personalised recommendations