Behavioral Ecology and Sociobiology

, Volume 56, Issue 4, pp 360–365 | Cite as

Manipulation of nest-box density affects extra-pair paternity in a population of blue tits (Parus caeruleus)

Original Article


We tested the effect of manipulation of breeding density on the occurrence of extra-pair paternity in a blue tit (Parus caeruleus) population during two consecutive years. In a homogeneous oak forest, nest-box manipulation provided a high density plot (plot A, 1.10 and 1.32 pairs/ha) and a low density plot (plot B, 0.43 and 0.46 pairs/ha). Microsatellite analysis on 91 broods revealed a higher proportion of extra-pair paternity in broods in plot A (mean of 17.2%) than in plot B (mean of 11.4%). A correlative approach showed that the proportion of extra-pair young in broods was affected by the number of breeding neighbours within 100 m around the nest-box, by the distance to the nearest breeding neighbour and by an additional plot effect. However, the nearest neighbours accounted for only 39.3% of extra-pair paternities and distance to extra-pair fathers was significantly higher than the nearest neighbour distance in both plots. This implies that the effect of density on the occurrence of extra-pair paternities is associated with active female choice to enhance the brood fitness. Although there were more extra-pair young in broods when density was high, the number of extra-pair fathers did not increase and stayed close to one. We suggest that density increases the cost of mate guarding by males, thereby increasing the possibility for females to solicit extra-pair paternities to the cuckolding male they have chosen. Finally, we discuss why correlatives approaches do not always show evidence for an effect of breeding density on extra-pair paternity occurrence.


Breeding density Extra-pair paternity Intra-specific variation Parus caeruleus 



We thank Anne Barrabé for her help in the microsatellite genotyping. Thank you also to Jacques Blondel, Paula Dias and Marcel Lambrechts for constructive advice on the manuscript. A.C. was supported by a grant from the Ministère Français de l’Education Nationale, de l’Enseignement et de la Recherche, a European Network grant (EKVL-CT-1999–0017) and a grant from the Bureau des Ressources Génétiques, France. Bird rings were provided by CRBPO-France. The manipulation of birds comply with the current laws in France.


  1. Alatalo RV, Lundberg A (1984) Density-dependence in breeding success of the Pied Flycatcher (Ficedula hypoleuca). J Anim Ecol 53:967–977Google Scholar
  2. Bensch S, Price T, Khon J (1997) Isolation and characterization of microsatellite loci in a Phylloscopus warbler. Mol Ecol 6:91–92CrossRefPubMedGoogle Scholar
  3. Birkhead T, Møller AP (1992) Sperm competition in birds: evolutionary causes and consequences. Academic Press, LondonGoogle Scholar
  4. Blondel J, Farré H (1988) The convergent trajectories of bird communities along ecological successions in European forests. Oecologia 75:83–93Google Scholar
  5. Charmantier A, Blondel J (2003) A contrast in extra-pair paternity levels on mainland and island populations of Mediterranean blue tits. Ethology 109:351–364Google Scholar
  6. Charmantier A, Blondel J, Perret P, Lambrechts MM (2004) Do extra-pair paternities provide genetic benefits for female blue tits (Parus caeruleus) J Avian Biol (in press)Google Scholar
  7. Chuang HC, Webster MS, Holmes RT (1999) Extrapair paternity and local synchrony in the Black-throated blue warbler. Auk 116:726–736Google Scholar
  8. Dawson DA, Hanotte O, Greig C, Stewart IRK, Burke T (2000) Polymorphic microsatellites in the blue tit Parus caeruleus and their cross-species utility in 20 songbird families. Mol Ecol 9:1919–1952CrossRefPubMedGoogle Scholar
  9. Dias PC, Blondel J (1996) Local specialization and maladaptation in the Mediterranean blue tit (Parus caeruleus). Oecologia 107:79–86Google Scholar
  10. Dunn PO, Whittingham LA, Lifjeld JT, Robertson RJ, Boag PT (1994) Effects of breeding density, synchrony, and experience on extrapair paternity in tree swallows. Behav Ecol 5:123–129Google Scholar
  11. Foerster K, Delhey K, Johnson A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717CrossRefPubMedGoogle Scholar
  12. Fridolfsson A-K, Gyllensten UB, Jakobsson S (1997) Microsatellite markers for paternity testing in the Willow warbler Phylloscopus trochilus: high frequency of extra-pair young in an island population. Hereditas 126:127–132Google Scholar
  13. Gelter HP, Tegelström H (1992) High frequency of extra-pair paternity in Swedish pied flycatchers revealed by allozyme electrophoresis and DNA fingerprinting. Behav Ecol Sociobiol 31:1–7Google Scholar
  14. Gibbs HL, Weatherhed PJ, Boag PT, White BN, Tabak LM, Hoysak DJ (1990) Realized reproductive success of polygynous red-winged blackbirds revealed by DNA markers. Science 250:1394–1396Google Scholar
  15. Goldstein DB, Schlötterer C (1999) Microsatellites: evolution and applications. Oxford University Press, OxfordGoogle Scholar
  16. Gowaty PA, Bridges WC (1991) Nestbox availability affects extra-pair fertilizations and conspecific nest parasitism in eastern bluebirds, Sialia sialis. Anim Behav 41:661–675Google Scholar
  17. Griffith SC, Stewart IRK, Dawson DA, Owens IPF, Burke T (1999) Constrasting levels of extra-pair paternity in mainland and island populations of the house sparrow (Passer domesticus): is there an ‘island effect’? Biol J Linn Soc 68:303–316CrossRefGoogle Scholar
  18. 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
  19. Gullberg A, Tegelström H, Gelter HP (1992) DNA fingerprinting reveals multiple paternity in families of Great and Blue Tits (Parus major and P. caeruleus). Hereditas 117:103–108Google Scholar
  20. Hasselquist D, Bensch S, von Schantz T (1995) Low frequency of extrapair paternity in the polygynous great reed warbler, Acrocephalus arundinaceus. Behav Ecol 6:27–39Google Scholar
  21. Hill GE, Montgomerie R, Roeder C, Boag P (1994) Sexual selection and cuckoldry in a monogamous songbird: implications for sexual selection theory. Behav Ecol Sociobiol 35:193–199CrossRefGoogle Scholar
  22. Hoi H, Hoi-Leitner M (1997) An alternative route to coloniality in the bearded tit: females pursue extra-pair fertilizations. Behav Ecol 8:113–119Google Scholar
  23. Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211Google Scholar
  24. Jamieson A (1994) The effectiveness of using co-domimant polymorphic allelic series for (1) checking pedigrees and (2) distinguishing full-sib pair members. Anim Genet 25:37–44Google Scholar
  25. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev Cambridge Philos Soc 75:21–64CrossRefGoogle Scholar
  26. Kempenaers B (1997) Does reproductive synchrony limit male opportunities or enhance female choice for extra-pair paternity? Behaviour 134:551–562Google Scholar
  27. Kempenaers B, Dhondt AA (1993) Why do females engage in extra-pair copulations? A review of hypothesis and their predictions. Belg J Zool 123:93–103Google Scholar
  28. Kempenaers B, Verheyen GR, Dhondt AA (1995) Mate guarding and copulation behaviour in monogamous and polygynous blue tits: do males follow a best-of-bad-job strategy? Behav Ecol Sociobiol 36:33–42CrossRefGoogle Scholar
  29. Kempenaers B, Verheyen GR, Dhondt AA (1997) Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492Google Scholar
  30. Krebs JR (1971) Territory and breeding density in the great tit, Parus major L. Ecology 52:2–22Google Scholar
  31. Krokene C, Lifjeld JT (2000) Variation in the frequency of extra-pair paternity in birds: a comparison of an island and a mainland population of Blue Tits. Behaviour 137:1317–1330CrossRefGoogle Scholar
  32. Lambrechts MM, Dias PC (1993) Differences in the onset of laying between island and mainland Mediterranean Blue Tits Parus caeruleus : phenotypic plasticity or genetic differences? Ibis 135:451–455Google Scholar
  33. Langefors A, Hasselquist D, von Schantz T (1998) Extra-pair fertilizations in the sedge warbler. J Avian Biol 29:134–144Google Scholar
  34. Leisler B, Beier J, Staudter H, Wink M (2000) Variation in extra-pair paternity in the polygynous Great Reed Warbler (Acrocephalus arundinaceus). J Ornithol 141:77–84CrossRefGoogle Scholar
  35. Lifjeld JT, Slagsvold T, Lampe HM (1991) Low frequency of extra-pair paternity in the pied flycatchers revealed by DNA fingerprinting. Behav Ecol Sociobiol 29:95–101Google Scholar
  36. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655PubMedGoogle Scholar
  37. Møller AP (1987) Advantages and disadvantages of coloniality in the swallow Hirundo rustica. Anim Behav 35:819–832Google Scholar
  38. Møller AP (1991) Density-dependent extra-pair copulations in the Swallow Hirundo rustica. Ethology 87:316–329Google Scholar
  39. Møller AP (1992) Nest boxes and the scientific rigour of experimental studies. Oikos 63:309–311Google Scholar
  40. Møller AP, Birkhead TR (1993) Cuckoldry and sociality—a comparative study of birds. Am Nat 142:118–140CrossRefGoogle Scholar
  41. Møller AP, Ninni P (1998) Sperm competition and sexual selection: a meta-analysis of paternity studies of birds. Behav Ecol Sociobiol 43:345–358Google Scholar
  42. Moore OR, Stutchbury BJM, Quinn JS (1999) Extrapair mating system of an asynchronously breeding tropical songbird: the mangrove swallow. Auk 116:1039–1046Google Scholar
  43. Rätti O, Lundberg A, Tegelström H, Alatalo RV (2001) No evidence for effects of breeding density and male removal on extrapair paternity in the pied flycatcher. Auk 118:147–155Google Scholar
  44. Richardson DS, Burke T (1999) Extra-pair paternity in relation to male age in Bullock’s orioles. Mol Ecol 8:2115–2126CrossRefPubMedGoogle Scholar
  45. SAS Institute (1992) SAS user’s guide, statistics. SAS Institute, Cary, N.C.Google Scholar
  46. Stutchbury BJM, Morton ES (1995) The effect of breeding synchrony on extra-pair mating systems in songbirds. Behaviour 132:675–690Google Scholar
  47. Stutchbury BJM, Rhymer JM, Morton ES (1994) Extrapair paternity in hooded warblers. Behav Ecol 5:384–392Google Scholar
  48. Sundberg J, Dixon A (1996) Old, colourful male yellowhammers, Emberiza citrinella, benefit from extra-pair copulations. Anim Behav 52:113–122CrossRefGoogle Scholar
  49. Tarof SA, Stutchbury JM, Piper WH, Fleischer RC (1998) Does breeding density covary with extra-pair fertilizations in hooded warblers? J Avian Biol 29:145–154Google Scholar
  50. Veiga JP, Boto L (2000) Low frequency of extra-pair fertilisations in house sparrows breeding at high density. J Avian Biol 31:237–244CrossRefGoogle Scholar
  51. Verboven N, Mateman AC (1997) Low frequency of extra-pair fertilizations in the great tit Parus major revealed by DNA fingerprinting. J Avian Biol 28:231–239Google Scholar
  52. Westneat DF (1993) Polygyny and extrapair fertilizations in eastern red-winged blackbirds (Agelaius phoeniceus). Behav Ecol 4:49–60Google Scholar
  53. Westneat DF, Sherman PW (1997) Density and extra-pair fertilizations in birds: a comparative analysis. Behav Ecol Sociobiol 41:205–215CrossRefGoogle Scholar
  54. Yezerinac SM, Gibbs HL, Briskie JV, Whittam R, Montgomerie R (1999) Extrapair paternity in a far northern population of yellow warblers Dendroica petechia. J Avian Biol 30:234–237Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.CEFE-CNRSMontpellier Cedex 5France

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