Urban Ecosystems

, Volume 20, Issue 5, pp 1035–1043 | Cite as

Spatio-temporal variation in the body condition of female pied flycatcher (Ficedula hypoleuca) in a polluted environment

  • Miia J. Rainio
  • Suvi Ruuskanen
  • Tapio Eeva


Food-chain changes in urban and industrial sites may limit breeding-time resources (e.g. food availability) for small insectivorous passerines. We used a long-term data set of pied flycatchers (Ficedula hypoleuca), collected from one of the most polluted sites in Finland during the past 23 years to study the effects of metal pollution on body condition of breeding females. Our results show that body mass started to decline already some days before hatching, indicating a preparation of females to forthcoming chick feeding period. We did not find long-term temporal trends in female body condition index (BCI) in spite of considerably reduced metal emissions during the study period. However, females had higher BCI in polluted than in unpolluted areas during the incubation period. For both incubation and nestling periods the body condition was lower for later breeders, though the condition index decreased slightly faster in relation to hatching date in polluted areas, which may be due to more drastic decrease in nutrition rich food abundance. Temperature and clutch size were positively associated with BCI during the incubation period, but not in the nestling period. Overall, our data suggest that environmental pollution modifies important life-history traits, potentially via indirect effects of higher environmental variability and changed phenology in polluted environment.


Body condition Body mass Ficedula hypoleuca Metal pollution Pied flycatcher 



We are grateful to Esa Lehikoinen, Jorma Nurmi and all the other persons who have been involved in this project over the past 23 years in Harjavalta. We also thank Kalle Rainio and the anonymous referees for the valuable comments on the manuscript. This study was funded by KONE Foundation (SR, MR), the Finnish Cultural Foundation (MR) and Academy of Finland (TE, project number 265859).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Ackerman JT, Overton CT, Casazza ML, Takekawa JY, Eagles-Smith CA, Keister RA, Herzog MP (2012) Does mercury contamination reduce body condition of endangered California clapper rails? Environ Pollut 162(0):439–448CrossRefPubMedGoogle Scholar
  2. Alatalo RV, Lundberg A, Glynn C (1986) Female pied flycatchers choose territory quality and not male characteristics. Nature 323(6084):152–153CrossRefGoogle Scholar
  3. Askenmo C (1982) Clutch size flexibility in the pied flycatcher Ficedula hypoleuca. Ardea 70(2):189–196Google Scholar
  4. Badzinski SS, Flint PL, Gorman KB, Petrie SA (2009) Relationships between hepatic trace element concentrations, reproductive status, and body condition of female greater scaup. Environ Pollut 157(6):1886–1893CrossRefPubMedGoogle Scholar
  5. Berglund ÅMM, Rainio MJ, Eeva T (2012) Decreased metal accumulation in passerines as a result of reduced emissions. Environ Toxicol Chem 31(6):1317–1323CrossRefPubMedGoogle Scholar
  6. Berglund ÅMM, Rainio MJ, Eeva T (2015) Temporal trends in metal pollution: using bird excrement as indicator. PLoS One 10(2):e0117071Google Scholar
  7. Biebach H, Friedrich W, Heine G (1986) Interaction of body mass, fat, foraging and stopover period in trans-sahara migrating passerine birds. Oecologia 69(3):370–379CrossRefPubMedGoogle Scholar
  8. Bókony V, Seress G, Nagy S, Lendvai ÁZ, Liker A (2012) Multiple indices of body condition reveal no negative effect of urbanization in adult house sparrows. Landsc Urban Plan 104(1):75–84CrossRefGoogle Scholar
  9. Burger J, Gochfeld M (1988) Effects of lead on growth in young herring gulls (Larus argentatus). J Toxicol Environ Health 25(2):227–236CrossRefPubMedGoogle Scholar
  10. Busse P, Kania W (1970) Operation Baltic 1961-1967 - working methods. Acta Ornithol (Warsaw) 12:179–208Google Scholar
  11. Combes C (2001) Parasitism. The ecology and evolution of intimate interactions. Chicago: University of Chicago Press. 728 pGoogle Scholar
  12. Currie D, Valkama J (1998) Limited effects of heavy metal pollution on foraging and breeding success in the curlew (Numenius arquata). Environ Pollut 101(2):253–261CrossRefPubMedGoogle Scholar
  13. Dauwe T, Janssens E, Eens M (2006) Effects of heavy metal exposure on the condition and health of adult great tits (Parus major). Environ Pollut 140(2):71–78CrossRefPubMedGoogle Scholar
  14. 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(3):312–323CrossRefPubMedGoogle Scholar
  15. 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(4):631–639CrossRefPubMedGoogle Scholar
  16. Eeva T, Lehikoinen E (2000) Pollution - recovery of breeding success in wild birds. Nature 403(6772):851–852CrossRefPubMedGoogle Scholar
  17. Eeva T, Lehikoinen E (2004) Rich calcium availability diminishes heavy metal toxicity in pied flycatcher. Funct Ecol 18(4):548–553CrossRefGoogle Scholar
  18. Eeva T, Lehikoinen E (2013) Density effect on great tit (Parus major) clutch size intensifies in a polluted environment. Oecologia 173(4):1661–1668CrossRefPubMedGoogle Scholar
  19. Eeva T, Lehikoinen E (2015) Long-term recovery of clutch size and egg shell quality of the pied flycatcher (Ficedula hypoleuca) in a metal polluted area. Environ Pollut 201(0):26–33.Google Scholar
  20. Eeva T, Lehikoinen E, Pohjalainen T (1997a) Pollution-related variation in food supply and breeding success in two hole-nesting passerines. Ecology 78(4):1120–1131CrossRefGoogle Scholar
  21. Eeva T, Lehikoinen E, Sunell C (1997b) The quality of pied flycatcher (Ficedula hypoleuca) and great tit (Parus major) females in an air pollution gradient. Ann Zool Fenn 34(1):61–71Google Scholar
  22. Eeva T, Lehikoinen E, Rönkä M (1998) Air pollution fades the plumage of the great tit. Funct Ecol 12(4):607–612CrossRefGoogle Scholar
  23. Eeva T, Lehikoinen E, Nikinmaa M (2003) Pollution-induced nutritional stress in birds: an experimental study of direct and indirect effects. Ecol Appl 13(5):1242–1249CrossRefGoogle Scholar
  24. Eeva T, Ryömä M, Riihimäki J (2005) Pollution-related changes in diets of two insectivorous passerines. Oecologia 145(4):629–639CrossRefPubMedGoogle Scholar
  25. 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(11):3126CrossRefPubMedGoogle Scholar
  26. Eeva T, Rainio M, Berglund Å, Stauffer J, Stöwe M, Ruuskanen S (2014) Experimental manipulation of dietary lead levels in great tit nestlings – limited effects on growth, physiology and survival. Ecotoxicology 23:914–928CrossRefPubMedGoogle Scholar
  27. Ekman JB, Hake MK (1990) Monitoring starvation risk: adjustments of body reserves in greenfinches (Carduelis chloris L.) during periods of unpredictable foraging success. Behav Ecol 1(1):62–67CrossRefGoogle Scholar
  28. Freed LA (1981) Loss of mass in breeding wrens: stress or adaptation? Ecology 62(5):1179–1186CrossRefGoogle Scholar
  29. Haywood S, Perrins CM (1992) Is clutch size in birds affected by environmental conditions during growth. Proc R Soc B-Biol Sci 249(1325):195–197CrossRefGoogle Scholar
  30. Hill GE (1990) Female house finches prefer colourful males: sexual selection for a condition dependent trait. Anim Behav 40(3):563–572CrossRefGoogle Scholar
  31. Jakob EM, Marshall SD, Uetz GW (1996) Estimating fitness: a comparison of body condition indices. Oikos 77(1):61–67CrossRefGoogle Scholar
  32. Janssens E, Dauwe T, Pinxten R, Bervoets L, Blust R, Eens M (2003) Effects of heavy metal exposure on the condition and health of nestlings of the great tit (Parus major), a small songbird species. Environ Pollut 126(2):267–274CrossRefPubMedGoogle Scholar
  33. Kiikkilä O (2003) Heavy-metal pollution and remediation of forest soil around the Harjavalta cu-Ni smelter, in SW Finland. Silva Fennica 37(3):399CrossRefGoogle Scholar
  34. Koivula MJ, Kanerva M, Salminen JP, Nikinmaa M, Eeva T (2011) Metal pollution indirectly increases oxidative stress in great tit (Parus major) nestlings. Environ Res 111(3):362–370CrossRefPubMedGoogle Scholar
  35. Kozlov MV, Eränen JK, Zverev VE (2007) Budburst phenology of white birch in industrially polluted areas. Environ Pollut 148:125–131CrossRefPubMedGoogle Scholar
  36. Kozlov MV, Zvereva EL, Zverev VE (2009) Impacts of point polluters on terrestrial biota: comparative analysis of 18 contaminated areas introduction. Springer, Netherland, p 466CrossRefGoogle Scholar
  37. Kubin E, Lippo H, Poikolainen J (2000) Heavy metal loading. In: Mälkönen E, eds. Forest condition in a changing environment- the Finnish case. Kluwer Academic Publishers: Kluwer Academic Publishers. p 60–71Google Scholar
  38. Kullberg C, Metcalfe NB, Houston DC (2002) Impaired flight ability during incubation in the pied flycatcher. J Avian Biol 33(2):179–183CrossRefGoogle Scholar
  39. Labocha MK, Hayes JP (2012) Morphometric indices of body condition in birds: a review. J Ornithol 153(1):1–22CrossRefGoogle Scholar
  40. Laet JFD, Dhondt AA (1989) Weight loss of the female during the first brood as a factor influencing second brood initiation in great tits Parus major and blue tits P. caeruleus. Ibis 131(2):281–289CrossRefGoogle Scholar
  41. Lambrechts MM, Adriaensen F, Ardia DR, Artemyev AV, Atienzar 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, Gregoire A, Griffith SC, Gustafsson L, Johnson LS, Kania W, Keiss O, Llambias PE, Mainwaring MC, Mand R, Massa B, Mazgajski TD, Møller AP, Moreno J, Naef-Daenzer B, Nilsson J-Å, Norte AC, Orell M, Otter KA, Park CR, Perrins CM, Pinowski J, Porkert J, Potti J, Remes V, Richner H, Rytkonen S, Shiao M-T, Silverin B, Slagsvold T, Smith HG, Sorace A, Stenning MJ, Stewart I, Thompson CF, Tryjanowski P, Torok J, van Noordwijk AJ, Winkler DW, Ziane N (2010) The design of artificial nestboxes for the study of secondary hole-nesting birds: a review of methodological inconsistencies and potential biases. Acta Ornithol 45(1):1–26CrossRefGoogle Scholar
  42. Lifjeld JT, Slagsvold T (1986) The function of courtship feeding during incubation in the pied flycatcher Ficedula hypoleuca. Anim Behav 34:1441–1453CrossRefGoogle Scholar
  43. Loman J (1984) Breeding success in relation to parent size and experience in a population of the hooded crow. Ornis Scand 15(3):183–187CrossRefGoogle Scholar
  44. Lundberg A, Alatalo RV (1992) The pied flycatcher. T & AD Poyser, London, 267 pGoogle Scholar
  45. Lyon BE, Montgomerie RD (1985) Incubation feeding in snow buntings: female manipulation or indirect male parental care. Behav Ecol Sociobiol 17(3):279–284CrossRefGoogle Scholar
  46. Moreno J (1989) Strategies of mass change in breeding birds. Biol J Linn Soc 37(4):297–310CrossRefGoogle Scholar
  47. Murphy E, Haukioja E (1986) Clutch size in nidicolous birds. Curr Ornithol 4:141–179Google Scholar
  48. Newton I, Marquiss M, Village A (1983) Weights, breeding, and survival in european sparrowhawks. Auk 100(2):344–354Google Scholar
  49. Norberg RÅ (1981) Temporary weight decrease in breeding birds may result in more fledged young. Am Nat 118(6):838–850CrossRefGoogle Scholar
  50. Nur N (1984) The consequences of brood size for breeding blue tits. I. Adult survival, weight change and the cost of reproduction. J Anim Ecol 53(2):479–496CrossRefGoogle Scholar
  51. Nur N (1988) The cost of reproduction in birds: an examination of the evidence. Ardea 76(2):155–168Google Scholar
  52. Orell M, Koivula K (1988) Cost of reproduction: parental survival and production of recruits in the willow tit Parus montanus. Oecologia 77(3):423–432CrossRefPubMedGoogle Scholar
  53. Rainio MJ, Kanerva M, Salminen J-P, Nikinmaa M, Eeva T (2013) Oxidative status in nestlings of three small passerine species exposed to metal pollution. Sci Total Environ 454-455(0):466–473CrossRefPubMedGoogle Scholar
  54. Ricklefs RE (1974) Avian energetics. Publications of Nuttal Ornithological Club, CambridgeGoogle Scholar
  55. Roff D (2002) Life history evolution: MA: Sinauer. 465 pGoogle Scholar
  56. SAS (2013) Base SAS 9.4 Procedures Guide: Statistical Procedures. Version SAS 9.4: SAS Institute IncGoogle Scholar
  57. Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86(1):155–163CrossRefGoogle Scholar
  58. Silverin B (1980) Seasonal development of reproductive organs in the female pied flycatcher Ficedula hypoleuca and experimental studies on duration of her re-nesting ability. J Zool 190:241–257CrossRefGoogle Scholar
  59. Silverin B (1981) Reproductive effort, as expressed in body and organ weights, in the pied flycatcher. Ornis Scand 12(2):133–139CrossRefGoogle Scholar
  60. Slagsvold T, Johansen MA (1998) Mass loss in female pied flycatchers Ficedula hypoleuca during late incubation: supplementation fails to support the reproductive stress hypothesis. Ardea 86(2):203–211Google Scholar
  61. Svensson L (1992) Identification guide to European passerines. Fingraf AB, SödertäljeGoogle Scholar
  62. Tinbergen JM, Boerlijst MC (1990) Nestling weight and survival in individual great tits (Parus major). J Anim Ecol 59(3):1113–1127CrossRefGoogle Scholar
  63. Väisänen R, Lehikoinen A (2013) Monitoring population changes of land bird species breeding in Finland in 1975-2012. Linnut vuosikirja 2012Google Scholar
  64. Wiebe KL, Vitousek MN (2015) Melanin plumage ornaments in both sexes of northern flicker are associated with body condition and predict reproductive output independent of age. Auk 132(2):507–517CrossRefGoogle Scholar

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© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Department of BiologyUniversity of TurkuTurkuFinland

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