Behavioral Ecology and Sociobiology

, Volume 67, Issue 6, pp 913–918 | Cite as

Avoiding parasitism by breeding indoors: cuckoo parasitism of hirundines and rejection of eggs

  • Wei Liang
  • Canchao Yang
  • Longwu Wang
  • Anders Pape MøllerEmail author
Original Paper


Brood parasitism is costly to hosts, and, therefore, a number of anti-parasite defenses have evolved. Surprisingly, several high-quality hosts such as martins and swallows are rarely parasitized, raising the question why that is the case. We hypothesize that martins and swallows may avoid parasitism by breeding in close association with humans, and by building nests that are inaccessible for common cuckoos Cuculus canorus and other brood parasites. Here we show using egg rejection experiments that red-rumped swallows Hirundo daurica, house martins Delichon urbica, and barn swallows Hirundo rustica in Europe do not reject foreign eggs placed in their nests, while barn swallows in China often reject foreign eggs. The frequency of parasitism of barn swallows in Europe was significantly higher than in house martins relative to the expectation based on the abundance of the two species. Barn swallows in Europe that were parasitized by cuckoos more often placed their nests outdoors than expected by chance, suggesting that avoidance of cuckoo parasitism can be achieved by breeding indoors. These findings suggest that barn swallows in China have gained egg rejection behavior because they cannot avoid parasitism when breeding outdoors.


Cuckoo Hirundinidae Human–animal interactions Indoor breeding Parasitism Protection by humans 



W. C. Årestrup and P. Tryjanowski kindly provided the unpublished information. Numerous colleagues and institutions provided invaluable help in creating the databases on cuckoo parasitism of hirundines. We thank F. Li and Zalong National Reserve for support and permission to carry out this study, and L. Liu, S. Cai, H. Wu, W. Lv, M. Chen, and S. Li for their assistance with field work. This work was supported by the National Natural Science Foundation of China (nos. 31071938 and 31272328 to WL, 31101646 and 31260514 to CY), Program for New Century Excellent Talents in University (NCET-10-0111 to WL), and Key Project of Chinese Ministry of Education (No. 212136 to CY). T. Grim and an anonymous reviewer provided helpful comments. The studies reported in this paper conform to the laws in the countries in which they were performed.


  1. Antonov A, Stokke BG, Moksnes A, Røskaft E (2009) Evidence for egg discrimination preceding failed rejection attempts in a small cuckoo host. Biol Lett 5:169–171PubMedCrossRefGoogle Scholar
  2. Antonov A, Stokke BG, Ranke PS, Fossøy F, Moksnes A, Røskaft E (2010) Absence of egg discrimination in a suitable cuckoo Cuculus canorus host breeding away from trees. J Avian Biol 41:11–14CrossRefGoogle Scholar
  3. Burfield I, van Bommel F (2004) Birds in Europe. BirdLife International, CambridgeGoogle Scholar
  4. Campobello D, Sealy SG (2009) Avian brood parasitism in a Mediterranean region: hosts and habitat preferences of common cuckoos Cuculus canorus. Bird Study 56:399–400CrossRefGoogle Scholar
  5. Combes C (2001) Parasitism. University of Chicago Press, ChicagoGoogle Scholar
  6. Cramp S, Perrins CM (eds) (1986) The birds of the Western Palearctic, vol 5. Oxford University Press, OxfordGoogle Scholar
  7. Davies NB (2000) Cuckoos, cowbirds and other cheats. T and AD Poyser, LondonGoogle Scholar
  8. Davies NB, Brooke M de L (1989) An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. I. Host egg discrimination. J Anim Ecol 58:207–224Google Scholar
  9. Davis KE (2008) Reweaving the tapestry: a supertree of birds. PhD thesis, University of GlasgowGoogle Scholar
  10. Dor R, Safran RJ, Sheldon FH, Winkler DW, Lovette IJ (2010) Phylogeny of the genus Hirundo and the barn swallow subspecies complex. Mol Phylogenet Evol 56:409–418PubMedCrossRefGoogle Scholar
  11. Ellegren H, Lindgren G, Primmer CR, Møller AP (1997) Fitness loss and germline mutations in barn swallows breeding in Chernobyl. Nature 389:593–596PubMedCrossRefGoogle Scholar
  12. Grim T (2006a) Low virulence of brood parasitic chicks: adaptation or constraint? Ornithol Sci 5:237–242Google Scholar
  13. Grim T (2006b) Cuckoo growth performance in parasitized and unused hosts: not only host size matters. Behav Ecol Sociobiol 60:716–723CrossRefGoogle Scholar
  14. Hasegawa M, Arai E, Kojima W, Kitamura W, Fujita G, Higuchi H, Watanabe M, Nakamura M (2010) Low level of extra-pair paternity in a population of the barn swallow Hirundo rustica gutturalis. Ornithol Sci 9:161–164CrossRefGoogle Scholar
  15. Kleven O, Jacobsen F, Robertson RJ, Lifjeld JT (2005) Extrapair mating between relatives in the barn swallow: a role for kin selection? Biol Lett 1:389–392PubMedCrossRefGoogle Scholar
  16. Krüger O, Davies NB (2002) The evolution of cuckoo parasitism: a comparative analysis. Proc R Soc Lond B 269:375–381CrossRefGoogle Scholar
  17. Martín-Vivaldi M, Soler JJ, Møller AP, Pérez-Contreras SM (2013) The importance of nest site and habitat in egg recognition ability of potential hosts of the common cuckoo Cuculus canorus. Ibis 155:140–155CrossRefGoogle Scholar
  18. Moksnes A, Røskaft E, Braa AT, Korsnes L, Lampe HM, Pedersen HC (1991) Behavioural responses of potential hosts towards artificial cuckoo eggs and dummies. Behaviour 116:64–89CrossRefGoogle Scholar
  19. Møller AP (1987) Intraspecific nest parasitism and anti-parasite behaviour in swallows, Hirundo rustica. Anim Behav 35:247–254CrossRefGoogle Scholar
  20. Møller AP (1989) Intraspecific nest parasitism in swallows, Hirundo rustica: the importance of neighbours. Behav Ecol Sociobiol 25:33–38CrossRefGoogle Scholar
  21. Møller AP (2010) The fitness benefit of association with humans: elevated success of birds breeding indoors. Behav Ecol 21:913–918CrossRefGoogle Scholar
  22. Møller AP, Brohede J, Cuervo JJ, de Lope F, Primmer CR (2003) Extrapair paternity in relation to sexual ornamentation, arrival date and condition in a migratory bird. Behav Ecol 14:707–712CrossRefGoogle Scholar
  23. Møller AP, Saino N, Adamík P, Ambrosini R, Antonov A, Campobello D, Stokke BG, Fossøy F, Lehikoinen E, Martin-Vivaldi M, Moksnes A, Moskat C, Røskaft E, Rubolini D, Schulze-Hagen K, Soler M, Shykoff JA (2011) Rapid change in host use of the common cuckoo Cuculus canorus linked to climate change. Proc R Soc Lond B 278:733–738CrossRefGoogle Scholar
  24. Moskát C, Karcza Z, Csörgö T (2003) Egg rejection in European blackbirds (Turdus merula): the effect of mimicry. Ornis Fenn 80:86–91Google Scholar
  25. Øien IJ, Honza M, Moksnes A, Røskaft E (1996) The risk of parasitism in relation to the distance from reed warbler nests to cuckoo perches. J Anim Ecol 65:147–153CrossRefGoogle Scholar
  26. Safran RJ, Neumann CR, McGraw KJ, Lovette IJ (2005) Dynamic paternity allocation as a function of male plumage color in barn swallows. Science 309:2210–2212PubMedCrossRefGoogle Scholar
  27. Saino N, Primmer CR, Ellegren H, Møller AP (1997) An experimental study of paternity and tail ornamentation in the barn swallow (Hirundo rustica). Evolution 51:562–570CrossRefGoogle Scholar
  28. Saino N, Primmer CR, Ellegren H, Møller AP (1999) Breeding synchrony and paternity in the barn swallow (Hirundo rustica). Behav Ecol Sociobiol 45:211–218CrossRefGoogle Scholar
  29. SAS Institute Inc (2012) JMP version 10.0. SAS Institute Inc., CaryGoogle Scholar
  30. Sheldon FH, Whittingham LA, Moyle RG, Slikas B, Winkler DW (2005) Phylogeny of swallows (Aves: Hirundinidae) estimated from nuclear and mitochondrial DNA sequences. Mol Phylogenet Evol 35:254–270PubMedCrossRefGoogle Scholar
  31. Soler JJ, Møller AP, Soler M (1999) A comparative study of host selection in the European cuckoo. Oecologia 118:265–276CrossRefGoogle Scholar
  32. Turner AK, Rose C (1989) Swallows and martins of the world. Christopher Helm, LondonGoogle Scholar
  33. von Vietinghoff-Riesch A (1955) Die rauchschwalbe. Duncker and Humblot, BerlinGoogle Scholar
  34. Vortman Y, Lotem A, Dor R, Lovette IJ, Safran RJ (2011) The sexual signals of the East-Mediterranean barn swallow: a different swallow tale. Behav Ecol 22:1344–1352CrossRefGoogle Scholar
  35. Winkler DW, Sheldon FH (1993) The evolution of nest construction in swallows (Hirundinidae): a molecular phylogenetic perspective. P Natl Acad Sci USA 90:5705–5707CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Wei Liang
    • 1
  • Canchao Yang
    • 1
  • Longwu Wang
    • 1
    • 3
  • Anders Pape Møller
    • 2
    Email author
  1. 1.Ministry of Education Key Laboratory for Tropical Plant and Animal Ecology, College of Life SciencesHainan Normal UniversityHaikouPeople’s Republic of China
  2. 2.Laboratoire Ecologie, Systematique et Evolution, UMR 8079 CNRS-Université Paris-Sud XIOrsay CedexFrance
  3. 3.College of Life SciencesWuhan UniversityWuhanPeople’s Republic of China

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