, Volume 173, Issue 4, pp 1661–1668 | Cite as

Density effect on great tit (Parus major) clutch size intensifies in a polluted environment

  • Tapio EevaEmail author
  • Esa Lehikoinen
Conservation ecology - Original research


Long-term data on a great tit (Parus major) population breeding in a metal-polluted zone around a copper–nickel smelter indicate that, against expectations, the clutch size of this species is decreasing even though metal emissions in the area have decreased considerably over the past two decades. Here, we document long-term population-level changes in the clutch size of P. major and explore if changes in population density, population numbers of competing species, timing of breeding, breeding habitat, or female age distribution can explain decreasing clutch sizes. Clutch size of P. major decreased by one egg in the polluted zone during the past 21 years, while there was no significant change in clutch size in the unpolluted reference zone over this time period. Density of P. major nests was similar in both environments but increased threefold during the study period in both areas (from 0.8 to 2.4 nest/ha). In the polluted zone, clutch size has decreased as a response to a considerable increase in population density, while a corresponding density change in the unpolluted zone did not have such an effect. The other factors studied did not explain the clutch size trend. Fledgling numbers in the polluted environment have been relatively low since the beginning of the study period, and they do not show a corresponding decrease to that noted for the clutch size over the same time period. Our study shows that responses of commonly measured life-history parameters to anthropogenic pollution depend on the structure of the breeding population. Interactions between pollution and intrinsic population characters should therefore be taken into account in environmental studies.


Density-dependent regulation Life-history parameters Metal pollution Population number Reproduction 



We thank Jorma Nurmi and all the other persons involved in the field work over the past years. Three anonymous referees are acknowledged for their help in correcting the manuscript. This study was financed by the Academy of Finland (project 265859).


  1. Ahola MP, Laaksonen T, Eeva T, Lehikoinen E (2009) Great tits lay increasingly smaller clutches than selected for: a study of climate- and density-related changes in reproductive traits. J Anim Ecol 78:1298–1306PubMedCrossRefGoogle Scholar
  2. Belskii EA, Bezel VS, Lyakhov AG (1995) Characteristics of the reproductive indices of birds nesting in tree hollows under conditions of technogenic pollution. Russ J Ecol 26:126–131Google Scholar
  3. Berglund ÅMM, Koivula MJ, Eeva T (2011) Species- and age-related variation in metal exposure and accumulation of two passerine bird species. Environ Pollut 159:2368–2374PubMedCrossRefGoogle Scholar
  4. Berglund ÅMM, Rainio M, Eeva T (2012) Decreased metal accumulation in passerines as a result of reduced emissions. Environ Toxicol Chem 31:1317–1323PubMedCrossRefGoogle Scholar
  5. Both C (1998) Density dependence of clutch size: habitat heterogeneity or individual adjustment? J Anim Ecol 67:659–666CrossRefGoogle Scholar
  6. Both C, Tinbergen JM, Visser ME (2000) Adaptive density dependence of avian clutch size. Ecology 81:3391–3403CrossRefGoogle Scholar
  7. Cooke AS (1973) Shell thinning in avian eggs by environmental pollutants. Environ Pollut 4:85–152CrossRefGoogle Scholar
  8. Cramp S, Perrins CM (1993) The birds of the Western Palearctic, vol VII. Oxford University Press, OxfordGoogle Scholar
  9. Dhondt AA (1989) The effect of old age on the reproduction of Great Tits Parus major and Blue Tits Parus caeruleus. Ibis 131:268–280CrossRefGoogle Scholar
  10. Dhondt AA, Kempenaers B, Adriaensen F (1992) Density-dependent clutch size caused by habitat heterogeneity. J Anim Ecol 61:643–648CrossRefGoogle Scholar
  11. Eeva T, Lehikoinen E (1995) Egg shell quality, clutch size and hatching success of the great tit (Parus major) and the pied flycatcher (Ficedula hypoleuca) in an air pollution gradient. Oecologia 102:312–323CrossRefGoogle Scholar
  12. Eeva T, Lehikoinen E (1996) Growth and mortality of nestling great tits (Parus major) and pied flycatchers (Ficedula hypoleuca) in a heavy metal pollution gradient. Oecologia 108:631–639CrossRefGoogle Scholar
  13. Eeva T, Lehikoinen E (2000) Improved breeding success in forest passerines after decreased emissions of heavy metals. Nature 403:851–852PubMedCrossRefGoogle Scholar
  14. Eeva T, Lehikoinen E, Pohjalainen T (1997) Pollution-related variation in food supply and breeding success in two hole-nesting passerines. Ecology 78:1120–1131CrossRefGoogle Scholar
  15. Eeva T, Lehikoinen E, Rönkä M (1998) Air pollution fades the plumage of the Great Tit. Funct Ecol 12:607–612CrossRefGoogle Scholar
  16. Eeva T, Ojanen M, Räsänen O, Lehikoinen E (2000) Empty nests in the great tit (Parus major) and the pied flycatcher (Ficedula hypoleuca) in a polluted area. Environ Pollut 109:303–309PubMedCrossRefGoogle Scholar
  17. Eeva T, Lehikoinen E, Nikinmaa M (2003) Pollution-induced nutritional stress in birds: an experimental study of direct and indirect effects. Ecol Appl 13:1242–1249CrossRefGoogle Scholar
  18. Eeva T, Ryömä M, Riihimäki J (2005) Pollution-related changes in diets of two insectivorous passerines. Oecologia 145:629–639PubMedCrossRefGoogle Scholar
  19. Eeva T, Sillanpää S, Salminen J-P, Nikkinen L, Tuominen A, Toivonen E, Pihlaja K, Lehikoinen E (2008) Environmental pollution affects the plumage color of Great tit nestlings through carotenoid availability. EcoHealth 5:328–337Google Scholar
  20. Eeva T, Ahola M, Lehikoinen E (2009) Breeding performance of blue tits (Cyanistes caeruleus) and great tits (Parus major) in a heavy metal polluted area. Environ Pollut 157:3126–3131PubMedCrossRefGoogle Scholar
  21. Eeva T, Belskii E, Gilyazov AS, Kozlov MV (2012) Pollution impacts on bird population density and species diversity at four non-ferrous smelter sites. Biol Conserv 150:33–41CrossRefGoogle Scholar
  22. Hörnfeldt B, Nyholm NEI (1996) Breeding performance of Tengmalm’s owl in a heavy metal pollution gradient. J Appl Ecol 33:377–386CrossRefGoogle Scholar
  23. Kiikkilä O (2003) Heavy-metal pollution and remediation of forest soil around the Harjavalta Cu-Ni smelter, in SW Finland. Silva Fennica 37:399–415Google Scholar
  24. Klomp H (1970) The determination of clutch size in birds. A review. Ardea 58:1–124Google Scholar
  25. Klomp H (1972) Regulation of the size of bird populations by means of territorial behaviour. Neth J Zool 22:456–488CrossRefGoogle Scholar
  26. Kluyver HN (1951) The population ecology of the Great Tit, Parus m. major L. Ardea 39:1–135Google Scholar
  27. Kozlov M, Zvereva EL, Zverev V (2009) Impacts of point polluters on terrestrial biota. Springer, BerlinGoogle Scholar
  28. Krebs JR (1970) Regulation of numbers in the Great tit (Aves: Passeriformes). J Zool (Lond) 162:317–333CrossRefGoogle Scholar
  29. Krebs JR (1971) Territory and breeding density in the Great Tit, Parus major L. Ecology 52:2–22CrossRefGoogle Scholar
  30. Krebs CJ (1989) Estimating abundance: distance methods and removal methods. Ecological methodology. Harper & Row, New York, pp 125–166Google Scholar
  31. Lack D (1955) British tits (Parus spp.) in nesting boxes. Ardea 43:50–84Google Scholar
  32. Lack D (1966) Population studies of birds. Clarendon, OxfordGoogle Scholar
  33. Lambrechts MM, Adriaensen F, Ardia DR, Artemyev AV, Atiénzar F, Banbura J, Barba E, Bouvier J-C, Camprodon J, Cooper CB, Dawson RD, Eens M, Eeva T, Faivre B, Garamszegi LZ, Goodenough AE, Gosler AG, Grégoire A, Griffith SC, Gustafsson L, Johnson LS, Kania W, Keišs O, Llambias PE, Mainwaring M, Mänd R, Massa B, Mazgajski TD, Møller AP, Moreno J, Naef-Daenzer B, Nilsson JÅ, Norte AC, Orell M, Otter K, Park CR, Perrins CM, Pinowski J, Porkert J, Potti J, Remes V, Richner H, Rytkönen S, Shiao M-T, Silverin B, Slagsvold T, Smith HG, Sorace A, Stenning MJ, Stewart I, Thompson CF, Tryjanowski P, Török J, van Noordwijk AJ, Winkler DW, Ziane N (2010) The design of artificial nest boxes for the study of secondary hole-nesting birds: a review of methodological inconsistencies and potential biases. Acta Ornithol 45:1–26CrossRefGoogle Scholar
  34. Mänd R, Leivits A, Leivits M, Rodenhouse NL (2009) Provision of nest boxes raises the breeding density of Great tits Parus major equally in coniferous and deciduous woodland. Ibis 151:487–492CrossRefGoogle Scholar
  35. Mineau P (2005) A review and analysis of study endpoints relevant to the assessment of “long term” pesticide toxicity in avian and mammalian wildlife. Ecotoxicology 14:775–799PubMedCrossRefGoogle Scholar
  36. Nilsson J-E (2011) Talgoxens Parus major antal och häckningsbiologi–resultat av 25 års holkstudier. Ornis Svecica 21:123–132Google Scholar
  37. Nyholm NEI, Myhrberg HE (1977) Severe eggshell defects and impaired reproductive capacity in small passerines in Swedish Lapland. Oikos 29:336–341CrossRefGoogle Scholar
  38. Ormerod SJ, Tyler SJ (1993) The adaptive significance of brood size and time of breeding in the dipper Cinclus cinclus (Aves: Passeriformes) as seen from post-fledging survival. J Zool 231:371–381CrossRefGoogle Scholar
  39. Ormerod SJ, O’Halloran J, Gribbin SD, Tyler SJ (1991) The ecology of dippers Cinclus cinclus in relation to stream acidity in upland Wales—breeding performance, calcium physiology and nestling growth. J Appl Ecol 28:419–433Google Scholar
  40. Perrins CM (1965) Population fluctuations and clutch-size in the Great Tit, Parus major L. J Anim Ecol 34:601–647CrossRefGoogle Scholar
  41. Pettifor RA, Perrins CM, McCleery RH (2001) The individual optimization of fitness: variation in reproductive output, including clutch size, mean nestling mass and offspring recruitment, in manipulated broods of great tits Parus major. J Anim Ecol 70:62–79CrossRefGoogle Scholar
  42. Ratcliffe DA (1970) Changes attributable to pesticides in egg breakage frequency and eggshell thickness in some British birds. J Appl Ecol 7:67–107CrossRefGoogle Scholar
  43. Sasvári L, Orell M (1992) Breeding success in a North and a Central European population of the Great Tit Parus major. Ornis Scand 23:96–100CrossRefGoogle Scholar
  44. Svensson L (1992) Identification guide to European passerines. Fingraf AB, StockholmGoogle Scholar
  45. Väisänen RA (2006) Monitoring population changes of 84 land bird species breeding in Finland in 1983–2005 (in Finnish with English summary). Linnut-vuosikirja 200583-98Google Scholar
  46. von Haartman L (1973) Talgmespopulationen på Lemsjöholm. Lintumies 8:7–9Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Section of Ecology, Department of BiologyUniversity of TurkuTurkuFinland

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