Behavioral Ecology and Sociobiology

, Volume 69, Issue 9, pp 1405–1414 | Cite as

Brood parasitism and quasi-parasitism in the European barn swallow Hirundo rustica rustica

  • Adéla Petrželková
  • Romana Michálková
  • Jana Albrechtová
  • Jaroslav Cepák
  • Marcel Honza
  • Jakub Kreisinger
  • Pavel Munclinger
  • Martina Soudková
  • Oldřich Tomášek
  • Tomáš AlbrechtEmail author
Original Paper


We studied patterns of extra-pair maternity (EPM) in 245 nests (225 nests belonging to 120 females of known identity) of sexually promiscuous European barn swallows (Hirundo rustica rustica) over a 3-year period. At least one EPM nestling was identified in 54 nests (22.0 %), representing 5.7 % of a total of 1060 nestlings. Up to 28.3 % of all EPM nestlings resulted from quasi-parasitism (QP), whereby nest-attending males sired parasitic offspring. Nests of quasi-parasitic females were never in close proximity to the host nest. Our data thus indicate nonrandom QP patterns in our population suggesting that QP can be considered a third alternative reproductive strategy alongside extra-pair paternity (EPP) and intraspecific brood parasitism (IBP). Of several socioecological factors evaluated, only number of simultaneous egg-laying females in the population proved a good predictor for EPM occurrence. Whereas parasitic females produced more offspring per breeding attempt than was the population average, both QP and IBP affected host female reproductive output, being associated with a reduced number of her offspring produced from the nest. On the contrary, QP resulted in an increase in the number of offspring produced by nest-attending males, suggesting that males may benefit from cooperating with parasitic females at the expense of their social partners.


Altricial birds Colonial breeding Conspecific brood parasitism Egg dumping Host fitness Parasite fitness 



We would like to thank all of our field assistants. Kevin Roche, Rebecca J. Safran, Nicola Saino, and one anonymous reviewer provided valuable comments on the manuscript. This study would not have been possible without the collaboration of local farm owners, specifically the Kotrba family at Hamr farm, the Kraus family at Šaloun farm, the Pulec family, and the staff of the Obora Stables in Třeboň. This research was funded through project 146213 of the Grant Agency of Charles University (to AP) and project P506/12/2472 of the Czech Science Foundation (to TA).


The project was designed by TA, JC, RM, and AP; data was collected by all authors; paternity and maternity analysis was conducted by JK, RM, and PM; TA and AP analyzed the data for this paper; TA, RM, and AP wrote the manuscript with contributions from all coauthors.

Ethical standards

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All protocols were noninvasive and adhered to the laws and guidelines of the Czech Republic (Czech Research Permit numbers 6628/2008-10001). All protocols were approved by the Animal Care and Use Committees at the Czech Academy of Sciences (041/2011), and Charles University in Prague (4789/2008-30).

Supplementary material

265_2015_1953_MOESM1_ESM.docx (20 kb)
ESM 1 (DOCX 20 kb)


  1. Åhlund M, Andersson M (2001) Female ducks can double their reproduction. Nature 414:600–601CrossRefPubMedGoogle Scholar
  2. Alves MAS, Bryant DM (1998) Brood parasitism in the sand martin, Riparia riparia: evidence for two parasitic strategies in a colonial passerine. Anim Behav 56:1323–1331CrossRefPubMedGoogle Scholar
  3. Amos W, Hoffman JI, Frodsham A, Zhang L, Best S, Hill AVS (2007) Automated binning of microsatellite alleles: problems and solutions. Mol Ecol Notes 7:10–14CrossRefGoogle Scholar
  4. Andersson M (1984) Brood parasitism within species. In: Barnard CJ (ed) Producers and scroungers. Croom Helm, London, pp 195–228CrossRefGoogle Scholar
  5. Andersson M, Åhlund M (2001) Protein fingerprinting: a new technique reveals extensive conspecific brood parasitism. Ecology 82:1433–1442CrossRefGoogle Scholar
  6. Andersson M, Eriksson MOG (1982) Nest parasitism in Goldeneyes Bucephala clangula: some evolutionary aspects. Am Nat 120:1–16CrossRefGoogle Scholar
  7. Ar A, Yom-Tov Y (1978) The evolution of parental care in birds. Evolution 32:655–669CrossRefGoogle Scholar
  8. Arnold KE, Owens IPF (2002) Extra-pair paternity and egg dumping in birds: life history, parental care and the risk of retaliation. Proc R Soc Lond B 269:1263–1269CrossRefGoogle Scholar
  9. Baillie SR, Milne H (1982) The influence of female age on breeding in the Eider Somateria mollissima. Bird Study 29:55–66CrossRefGoogle Scholar
  10. Bennett PM, Owens IPF (2002) Evolutionary ecology of birds. Oxford University Press, OxfordGoogle Scholar
  11. Berger I, Dvir Y, Leshem Y, Yom-Tov Y, Markman S (2013) Extra-pair copulations, intra-specific brood parasitism, and quasi-parasitism in birds: a theoretical approach. Acta Ethol 17:131–140CrossRefGoogle Scholar
  12. Boonekamp JJ, Salomons M, Bouwhuis S, Dijkstra C, Verhulst S (2014) Reproductive effort accelerates actuarial senescence in wild birds: an experimental study. Ecol Lett 17:599–605CrossRefPubMedGoogle Scholar
  13. Brown CR (1984) Laying eggs in a neighbor’s nest: benefit and cost of colonial nesting in swallows. Science 224:518–519CrossRefPubMedGoogle Scholar
  14. Brown CR, Brown MB (1988) The costs and benefits of egg destruction by conspecifics in colonial cliff swallows. Auk 105:737–748Google Scholar
  15. Brown CR, Brown MB (1989) Behavioural dynamics of intraspecific brood parasitism in colonial cliff swallows. Anim Behav 37:777–796CrossRefGoogle Scholar
  16. Brown CR, Brown MB (1991) Selection of high-quality host nests by parasitic cliff swallows. Anim Behav 41:457–465CrossRefGoogle Scholar
  17. Crawley MJ (2007) The R Book. Wiley, West SussexCrossRefGoogle Scholar
  18. Dawkins R (1980) Good strategy or evolutionarily stable strategy. In: Barlow GW, Silverberg J (eds) Sociobiology: beyond nature/nurture? Westview Press, Boulder, pp 331–367Google Scholar
  19. Eadie JM (1989) Alternative female reproductive tactics in a precocial bird: The ecology and evolution of brood parasitism in goldeneyes. PhD Thesis, University of British Columbia, VancouverGoogle Scholar
  20. Eadie JM, Kehoe FP, Nudds TD (1988) Pre-hatch and post-hatch brood amalgamation in North American Anatidae: a review of hypotheses. Can J Zool 66:1709–1721CrossRefGoogle Scholar
  21. Emlen ST, Wrege PH (1986) Forced copulations and intra-specific parasitism: two costs of social living in the White-fronted Bee-eater. Ethology 71:2–29CrossRefGoogle Scholar
  22. Erikstad KE, Bustnes JO (1994) Clutch size determination in common eiders: an egg removal and egg addition experiment. J Avian Biol 25:215–218CrossRefGoogle Scholar
  23. Fujita G, Higuchi H (2007) Barn swallows prefer to nest at sites hidden from neighboring nests within a loose colony. J Ethol 25:117–123CrossRefGoogle Scholar
  24. Gibbons DW (1986) Brood parasitism and cooperative nesting in the moorhen, Gallinula-chloropus. Behav Ecol Sociobiol 19:221–232Google Scholar
  25. Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212CrossRefPubMedGoogle Scholar
  26. Griffith SC, Lyon B, Montgomerie R (2004) Quasi-parasitism in birds. Behav Ecol Sociobiol 56:191–200CrossRefGoogle Scholar
  27. Griffith SC, Barr I, Sheldon BC, Rowe LV, Burke T (2009) Egg patterning is not a reliable indicator of intraspecific brood parasitism in the blue tit Cyanistes caeruleus. J Avian Biol 40:337–341CrossRefGoogle Scholar
  28. Hoi H, Darolová A, Krištofík J (2010) Conspecific brood parasitism and anti-parasite strategies in relation to breeding density in female bearded tits. Behaviour 147:1533–1549CrossRefGoogle Scholar
  29. Jackson WM (1993) Causes of conspecific nest parasitism in the northern masked weaver. Behav Ecol Sociobiol 32:119–126CrossRefGoogle Scholar
  30. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106CrossRefPubMedGoogle Scholar
  31. Kendra PE, Roth RR, Tallamy DW (1988) Conspecific brood parasitism in the house sparrow. Wilson Bull 100:80–90Google Scholar
  32. Kleven O, Jacobsen F, Robertson RJ, Lifjeld JT (2005) Extrapair mating between relatives in the barn swallow: a role for kin selection? Biol Lett 1:389–392PubMedCentralCrossRefPubMedGoogle Scholar
  33. Krakauer AH (2008) Sexual selection and the genetic mating system of wild turkeys. Condor 110:1–12CrossRefGoogle Scholar
  34. Laskemoen T, Albrecht T, Bonisoli-Alquati A, Cepák J, de Lope F et al (2013) Variation in sperm morphometry and sperm competition among barn swallow (Hirundo rustica) populations. Behav Ecol Sociobiol 67:301–309CrossRefGoogle Scholar
  35. Laurila T, Hario M (1988) Environmental and genetic factors influencing clutch size, egg volume, date of laying and female weight in the common eider Somateria mollissima. Finn Game Res 45:19–30Google Scholar
  36. Li MH, Välimäki K, Piha M, Pakkala T, Merilä J (2008) Extrapair paternity and maternity in the Three-toed Woodpecker, Picoides tridactylus: insights from microsatellite-based parentage analysis. PLoS ONE 4, e7895CrossRefGoogle Scholar
  37. Liang W, Yang CC, Wang LW, Møller AP (2013) Avoiding parasitism by breeding indoors: cuckoo parasitism of hirundines and rejection of eggs. Behav Ecol Sociobiol 67:913–918CrossRefGoogle Scholar
  38. Lombardo MP, Power HW, Stouffer PC, Romagnano LC, Hoffenberg AS (1989) Egg removal and intraspecific brood parasitism in the European starling (Sturnus vulgaris). Behav Ecol Sociobiol 24:217–223CrossRefGoogle Scholar
  39. Lyon BE (1993) Conspecific brood parasitism as a flexible female reproductive tactic in American coots. Anim Behav 46:911–928CrossRefGoogle Scholar
  40. Lyon BE, Eadie JM (2008) Conspecific brood parasitism in birds: a life-history perspective. Annu Rev Ecol Evol Syst 39:343–363CrossRefGoogle Scholar
  41. Lyon BE, Everding S (1996) High frequency of conspecific brood parasitism in a colonial waterbird, the Eared Grebe Podiceps nigricollis. J Avian Biol 27:238–244CrossRefGoogle Scholar
  42. Lyon BE, Hochachka WM, Eadie JM (2002) Paternity-parasitism trade-offs: a model and test of host-parasite cooperation in an avian conspecific brood parasite. Evolution 56:1253–1256CrossRefPubMedGoogle Scholar
  43. MacWhirter RB (1989) Minireview: on the rarity of intraspecific brood parasitism. Condor 91:485–492CrossRefGoogle Scholar
  44. McRae SB (1997) A rise in nest predation enhances the frequency of intraspecific brood parasitism in a moorhen population. J Anim Ecol 66:143–153CrossRefGoogle Scholar
  45. Møller AP (1987) Intraspecific nest parasitism and anti-parasite behaviour in swallows, Hirundo rustica. Anim Behav 35:247–254CrossRefGoogle Scholar
  46. Møller AP (1994) Sexual selection and the barn swallow. Oxford University Press, OxfordGoogle Scholar
  47. Møller AP, Brohede J, Cuervo JJ, de Lope F, Primmer C (2003) Extrapair paternity in relation to sexual ornamentation, arrival date, and condition in a migratory bird. Behav Ecol 14:707–712CrossRefGoogle Scholar
  48. Moskát C, Barta Z, Hauber ME, Honza M (2006) High synchrony of egg laying in common cuckoos (Cuculus canorus) and their great reed warbler (Acrocephalus arundinaceus) hosts. Ethol Ecol Evol 18:159–167CrossRefGoogle Scholar
  49. Nielsen CR, Parker PG, Gates RJ (2006) Intraspecific nest parasitism of cavity-nesting wood ducks: costs and benefits to hosts and parasites. Anim Behav 72:917–926CrossRefGoogle Scholar
  50. Payne RB (1977) The ecology of brood parasitism in birds. Annu Rev Ecol Syst 8:1–28CrossRefGoogle Scholar
  51. Primmer CR, Møller AP, Ellegren H (1995) Resolving genetic relationships with microsatellite markers: a parentage testing system for the swallow Hirundo rustica. Mol Ecol 4:493–498CrossRefPubMedGoogle Scholar
  52. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  53. Rohwer FC, Freeman S (1989) The distribution of conspecific nest parasitism in birds. Can J Zool 67:239–253CrossRefGoogle Scholar
  54. Safran RJ, Neuman CR, McGraw KJ, Lovette IJ (2005) Dynamic paternity allocation as a function of male plumage color in barn swallows. Science 309:2210–2212CrossRefPubMedGoogle Scholar
  55. 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
  56. Sayler RD (1992) Ecology and evolution of brood parasitism in waterfowl. In: Batt BDJ, Afton AD, Anderson MG, Ankney CD, Johnson DH, Kadlec JA, Krapu GL (eds) Ecology and management of breeding waterfowl. University of Minnesota Press, Minneapolis, pp 290–322Google Scholar
  57. Semel B, Sherman PW (2001) Intraspecific parasitism and nest-site competition in wood ducks. Anim Behav 61:787–803CrossRefGoogle Scholar
  58. Sokal RR, Rohlf FJ (2012) Biometry. W. H. Freeman & Co, New YorkGoogle Scholar
  59. Sorenson MD (1991) The functional significance of parasitic egg laying and typical nesting in redhead ducks: an analysis of individual behaviour. Anim Behav 42:771–796CrossRefGoogle Scholar
  60. Sorenson MD (1992) Comment: why is conspecific nest parasitism more frequent in waterfowl than in other birds? Can J Zool 70:1856–1858CrossRefGoogle Scholar
  61. Spurr EB, Milne H (1976) Factors affecting laying date in the Common Eider. Wildfowl 27:107–110Google Scholar
  62. Svensson L (1984) Identification guide to European passerines, 2nd edn. Svensson, StockholmGoogle Scholar
  63. Tsyusko OV, Peters MB, Hgen C, Tuberville TD, Mousseau TA, Møller AP, Glenn TC (2007) Microsatellite markers isolated from barn swallows (Hirundo rustica). Mol Ecol Notes 7:833–835CrossRefGoogle Scholar
  64. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  65. Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, New YorkCrossRefGoogle Scholar
  66. Vortman Y, Lotem A, Dor R, Lovette I, Safran R (2013) Multiple sexual signals and behavioral reproductive isolation in a diverging population. Am Nat 182:514–523CrossRefPubMedGoogle Scholar
  67. Waldeck P, Öst M, Kilpi M, Andersson M (2004) Brood parasitism in a population of common eider (Somateria mollissima). Behaviour 141:725–739CrossRefGoogle Scholar
  68. Wang JL (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979PubMedCentralCrossRefPubMedGoogle Scholar
  69. Wrege PH, Emlen ST (1987) Biochemical determination of parental uncertainty in white-fronted bee-eaters. Behav Ecol Sociobiol 20:153–160CrossRefGoogle Scholar
  70. Yom-Tov Y (1980) Intraspecific nest parasitism in birds. Biol Rev 55:93–108CrossRefGoogle Scholar
  71. Yom-Tov Y (2001) An updated list and some comments on the occurrence of intraspecific nest parasitism in birds. Ibis 143:133–143CrossRefGoogle Scholar
  72. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Adéla Petrželková
    • 1
    • 2
  • Romana Michálková
    • 1
  • Jana Albrechtová
    • 1
    • 2
  • Jaroslav Cepák
    • 3
  • Marcel Honza
    • 2
  • Jakub Kreisinger
    • 1
  • Pavel Munclinger
    • 1
  • Martina Soudková
    • 1
  • Oldřich Tomášek
    • 1
    • 2
  • Tomáš Albrecht
    • 1
    • 2
    Email author
  1. 1.Faculty of ScienceCharles University in PraguePraha 2Czech Republic
  2. 2.Institute of Vertebrate BiologyAcademy of Sciences of the Czech RepublicBrnoCzech Republic
  3. 3.Bird Ringing StationNational MuseumPraha 10Czech Republic

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