Skip to main content
Log in

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

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

Abstract

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.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Åhlund M, Andersson M (2001) Female ducks can double their reproduction. Nature 414:600–601

    Article  PubMed  Google Scholar 

  • Alves MAS, Bryant DM (1998) Brood parasitism in the sand martin, Riparia riparia: evidence for two parasitic strategies in a colonial passerine. Anim Behav 56:1323–1331

    Article  PubMed  Google Scholar 

  • Amos W, Hoffman JI, Frodsham A, Zhang L, Best S, Hill AVS (2007) Automated binning of microsatellite alleles: problems and solutions. Mol Ecol Notes 7:10–14

    Article  CAS  Google Scholar 

  • Andersson M (1984) Brood parasitism within species. In: Barnard CJ (ed) Producers and scroungers. Croom Helm, London, pp 195–228

    Chapter  Google Scholar 

  • Andersson M, Åhlund M (2001) Protein fingerprinting: a new technique reveals extensive conspecific brood parasitism. Ecology 82:1433–1442

    Article  Google Scholar 

  • Andersson M, Eriksson MOG (1982) Nest parasitism in Goldeneyes Bucephala clangula: some evolutionary aspects. Am Nat 120:1–16

    Article  Google Scholar 

  • Ar A, Yom-Tov Y (1978) The evolution of parental care in birds. Evolution 32:655–669

    Article  Google Scholar 

  • 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 269:1263–1269

    Article  Google Scholar 

  • Baillie SR, Milne H (1982) The influence of female age on breeding in the Eider Somateria mollissima. Bird Study 29:55–66

    Article  Google Scholar 

  • Bennett PM, Owens IPF (2002) Evolutionary ecology of birds. Oxford University Press, Oxford

    Google Scholar 

  • 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 17:131–140

    Article  Google Scholar 

  • Boonekamp JJ, Salomons M, Bouwhuis S, Dijkstra C, Verhulst S (2014) Reproductive effort accelerates actuarial senescence in wild birds: an experimental study. Ecol Lett 17:599–605

    Article  PubMed  Google Scholar 

  • Brown CR (1984) Laying eggs in a neighbor’s nest: benefit and cost of colonial nesting in swallows. Science 224:518–519

    Article  CAS  PubMed  Google Scholar 

  • Brown CR, Brown MB (1988) The costs and benefits of egg destruction by conspecifics in colonial cliff swallows. Auk 105:737–748

    Google Scholar 

  • Brown CR, Brown MB (1989) Behavioural dynamics of intraspecific brood parasitism in colonial cliff swallows. Anim Behav 37:777–796

    Article  Google Scholar 

  • Brown CR, Brown MB (1991) Selection of high-quality host nests by parasitic cliff swallows. Anim Behav 41:457–465

    Article  Google Scholar 

  • Crawley MJ (2007) The R Book. Wiley, West Sussex

    Book  Google Scholar 

  • Dawkins R (1980) Good strategy or evolutionarily stable strategy. In: Barlow GW, Silverberg J (eds) Sociobiology: beyond nature/nurture? Westview Press, Boulder, pp 331–367

    Google Scholar 

  • 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, Vancouver

  • 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 66:1709–1721

    Article  Google Scholar 

  • Emlen ST, Wrege PH (1986) Forced copulations and intra-specific parasitism: two costs of social living in the White-fronted Bee-eater. Ethology 71:2–29

    Article  Google Scholar 

  • Erikstad KE, Bustnes JO (1994) Clutch size determination in common eiders: an egg removal and egg addition experiment. J Avian Biol 25:215–218

    Article  Google Scholar 

  • Fujita G, Higuchi H (2007) Barn swallows prefer to nest at sites hidden from neighboring nests within a loose colony. J Ethol 25:117–123

    Article  Google Scholar 

  • Gibbons DW (1986) Brood parasitism and cooperative nesting in the moorhen, Gallinula-chloropus. Behav Ecol Sociobiol 19:221–232

    Google Scholar 

  • Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212

    Article  CAS  PubMed  Google Scholar 

  • Griffith SC, Lyon B, Montgomerie R (2004) Quasi-parasitism in birds. Behav Ecol Sociobiol 56:191–200

    Article  Google Scholar 

  • 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 40:337–341

    Article  Google Scholar 

  • Hoi H, Darolová A, Krištofík J (2010) Conspecific brood parasitism and anti-parasite strategies in relation to breeding density in female bearded tits. Behaviour 147:1533–1549

    Article  Google Scholar 

  • Jackson WM (1993) Causes of conspecific nest parasitism in the northern masked weaver. Behav Ecol Sociobiol 32:119–126

    Article  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  • Kendra PE, Roth RR, Tallamy DW (1988) Conspecific brood parasitism in the house sparrow. Wilson Bull 100:80–90

    Google Scholar 

  • Kleven O, Jacobsen F, Robertson RJ, Lifjeld JT (2005) Extrapair mating between relatives in the barn swallow: a role for kin selection? Biol Lett 1:389–392

    Article  PubMed Central  PubMed  Google Scholar 

  • Krakauer AH (2008) Sexual selection and the genetic mating system of wild turkeys. Condor 110:1–12

    Article  Google Scholar 

  • 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 67:301–309

    Article  Google Scholar 

  • 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 45:19–30

    Google Scholar 

  • 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, e7895

    Article  Google Scholar 

  • 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 67:913–918

    Article  Google Scholar 

  • 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 24:217–223

    Article  Google Scholar 

  • Lyon BE (1993) Conspecific brood parasitism as a flexible female reproductive tactic in American coots. Anim Behav 46:911–928

    Article  Google Scholar 

  • Lyon BE, Eadie JM (2008) Conspecific brood parasitism in birds: a life-history perspective. Annu Rev Ecol Evol Syst 39:343–363

    Article  Google Scholar 

  • Lyon BE, Everding S (1996) High frequency of conspecific brood parasitism in a colonial waterbird, the Eared Grebe Podiceps nigricollis. J Avian Biol 27:238–244

    Article  Google Scholar 

  • 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 56:1253–1256

    Article  PubMed  Google Scholar 

  • MacWhirter RB (1989) Minireview: on the rarity of intraspecific brood parasitism. Condor 91:485–492

    Article  Google Scholar 

  • McRae SB (1997) A rise in nest predation enhances the frequency of intraspecific brood parasitism in a moorhen population. J Anim Ecol 66:143–153

    Article  Google Scholar 

  • Møller AP (1987) Intraspecific nest parasitism and anti-parasite behaviour in swallows, Hirundo rustica. Anim Behav 35:247–254

    Article  Google Scholar 

  • Møller AP (1994) Sexual selection and the barn swallow. Oxford University Press, Oxford

    Google Scholar 

  • 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 14:707–712

    Article  Google Scholar 

  • 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 18:159–167

    Article  Google Scholar 

  • Nielsen CR, Parker PG, Gates RJ (2006) Intraspecific nest parasitism of cavity-nesting wood ducks: costs and benefits to hosts and parasites. Anim Behav 72:917–926

    Article  Google Scholar 

  • Payne RB (1977) The ecology of brood parasitism in birds. Annu Rev Ecol Syst 8:1–28

    Article  Google Scholar 

  • Primmer CR, Møller AP, Ellegren H (1995) Resolving genetic relationships with microsatellite markers: a parentage testing system for the swallow Hirundo rustica. Mol Ecol 4:493–498

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Rohwer FC, Freeman S (1989) The distribution of conspecific nest parasitism in birds. Can J Zool 67:239–253

    Article  Google Scholar 

  • Safran RJ, Neuman CR, McGraw KJ, Lovette IJ (2005) Dynamic paternity allocation as a function of male plumage color in barn swallows. Science 309:2210–2212

    Article  CAS  PubMed  Google Scholar 

  • Saino N, Primmer CR, Ellegren H, Møller AP (1997) An experimental study of paternity and tail ornamentation in the barn swallow (Hirundo rustica). Evolution 51:562–570

    Article  Google Scholar 

  • 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 290–322

    Google Scholar 

  • Semel B, Sherman PW (2001) Intraspecific parasitism and nest-site competition in wood ducks. Anim Behav 61:787–803

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (2012) Biometry. W. H. Freeman & Co, New York

    Google Scholar 

  • Sorenson MD (1991) The functional significance of parasitic egg laying and typical nesting in redhead ducks: an analysis of individual behaviour. Anim Behav 42:771–796

    Article  Google Scholar 

  • Sorenson MD (1992) Comment: why is conspecific nest parasitism more frequent in waterfowl than in other birds? Can J Zool 70:1856–1858

    Article  Google Scholar 

  • Spurr EB, Milne H (1976) Factors affecting laying date in the Common Eider. Wildfowl 27:107–110

    Google Scholar 

  • Svensson L (1984) Identification guide to European passerines, 2nd edn. Svensson, Stockholm

    Google Scholar 

  • 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 7:833–835

    Article  CAS  Google Scholar 

  • 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 4:535–538

    Article  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, New York

    Book  Google Scholar 

  • Vortman Y, Lotem A, Dor R, Lovette I, Safran R (2013) Multiple sexual signals and behavioral reproductive isolation in a diverging population. Am Nat 182:514–523

    Article  PubMed  Google Scholar 

  • Waldeck P, Öst M, Kilpi M, Andersson M (2004) Brood parasitism in a population of common eider (Somateria mollissima). Behaviour 141:725–739

    Article  Google Scholar 

  • Wang JL (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979

    Article  PubMed Central  PubMed  Google Scholar 

  • Wrege PH, Emlen ST (1987) Biochemical determination of parental uncertainty in white-fronted bee-eaters. Behav Ecol Sociobiol 20:153–160

    Article  Google Scholar 

  • Yom-Tov Y (1980) Intraspecific nest parasitism in birds. Biol Rev 55:93–108

    Article  Google Scholar 

  • Yom-Tov Y (2001) An updated list and some comments on the occurrence of intraspecific nest parasitism in birds. Ibis 143:133–143

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgments

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).

Authorship

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tomáš Albrecht.

Additional information

Communicated by M. Soler

Adéla Petrželková and Romana Michálková contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Petrželková, A., Michálková, R., Albrechtová, J. et al. Brood parasitism and quasi-parasitism in the European barn swallow Hirundo rustica rustica . Behav Ecol Sociobiol 69, 1405–1414 (2015). https://doi.org/10.1007/s00265-015-1953-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-015-1953-6

Keywords

Navigation