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Air pollution impacts on birds and insects Project leader: Tapio Eeva, docent Ph.D. students: Jouni Sorvari, Saila Sillanpää ; M.Sc. student: Ville Vähä-Iitu Collaborators: Mikko Nikinmaa (Univ. Turku), Marcel Eens (Univ. Antwerp), Markus Rantala (Univ. California), Juha-Pekka Salminen (Univ. Turku), Eugen Belskii (Russian Acad. Sci) Background Effects of air pollution on the Pied Flycatcher( Ficedula hypoleuca ) and the Great Tit ( Parus major )has been studied in the surroundings of a copper smelter of Harjavalta (SW Finland) since 1991. Our aim has been to find out how atmospheric emissions of heavy metals (especially copper, nickel and lead) and acidic substances affect the breeding success and survival of birds. The main results One of the main interests in our project has been whether the detrimental effects are direct toxic effects or indirect effects (e.g. due to decreased amount of food). We have found both. The two bird species respond differently to pollution. The pied flycatcher suffers from poor quality egg shells and growth abnormalities of nestlings, but these effects are restricted only to relatively small area (1 - 2 km) around the factory complex. The great tit suffers most in late nestling stage, when the growth of nestling is retarded and mortality increased. In summary, the pied flycatcher seems to suffer more from the direct toxic effects whereas the great tit suffers more from the reduced amount of suitable food for nestlin g s. Background The main results Future work The latest results Media Publications Great tits in the polluted area are fading We have found that the air pollution can cause changes in the plumage colour of great tits. The breast feathers of the great tit are normally yellow, but the yellow plumage of young great tits is significantly paler the closer to the pollution source they live (Functional Ecology 12: 607-612). Read articles: The Economist, Priroda [Nature, Moscow] (In Russian) and Helsingin Sanomat (In Finnish). The pigments responsible for colouring feathers yellow are derived from chemicals called carotenoids. Birds cannot make these chemicals themselves and so must obtain them indirectly through what they eat. The problem is that pollutants emitted from the smelting plant are causing a decrease in the number of green caterpillars , an important component of the great tit diet generally and a vital source of carotenoids. The plumage colour study will continue next summer. Future work Birds’ defence mechanisms against environmental stress can be behavioural, physiological or biochemical. Often, they are related to the quality of birds’ diet. For example, recent studies have revealed the importance of dietary carotenoids on the immunocompetence of birds. An analogous, but less studied, is the role of carotenoids (i.e. antioxidants) in defence against toxic substances (heavy metals, PCBs, PAHs and brominated flame retardants). In our future study we want to examine how these defence mechanisms are dependent on the diet of wild bird populations. The main issues in our study area: z Food quality and defence mechanisms z Does air pollution cause genetic changes? z Interspecific differences in defence ability Birds' diet is studied by collecting food samples and by following nestling feeding with video cameras attached into nest-box roof. Look yourself how a pied flycatcher male brings a green caterpillar and a cockroach to nestlings and takes a faecal sac away. Video (wmv), 1.8 mb The most recent results Breeding success was improved after decreased emissions Breeding success of the great tit and pied flycatcher has markedly improved in the vicinity of the copper smelter during 1991 - 1997, when heavy metal emissions markedly decreased. Lead concentrations in nestling bones tissues were decreased about 90% and the number of fledglings increased by about 1.6 chicks in both species. The results suggest that even in an area with decades long heavy metal pollution history, positive results of reduced pollution loads on wild bird populations can be observed over a relatively short time period. (Nature 403: 851-852) Birds did not show reduced immunocompetence in the polluted area We investigated whether heavy metal pollution changed the immunocompetence of the pied flycatcher. We measured humoral and T-cell mediated immune responses in two study areas: a polluted area in the vicinity of a copper smelter and a control area far from the smelter. The immunocompetence of F. hypoleuca was not suppressed by pollution stress. In contrast, we found that F. hypoleuca males showed stronger humoral immune responses to a novel antigen (tetanus toxoid) in the polluted environment than in the unpolluted one. No significant pollution-related effects were found in humoral immune response of females or T-cell mediated immune response of nestlings, despite the lower fled g in g success in the p olluted area. Our results su gg est that humoral immune res p onse of birds ma y News! actually be enhanced, or hyper-activated, under moderate levels of heavy metal pollution. This may cause some extra costs for birds during breeding. Our study and media Newspaper and magazine articles on bird study in Harjavalta: Talitiaiset tarkkailussa Harjavallan seudulla - Satakunnan Kansa 1991 Kirjosieppo ja talitiainen kärsivät ilmansaasteista - Turun Sanomat 1996 Kirjosieppo ja talitiainen kärsivät ilmansaasteista eri tavoin - Lapin Kansa 1996 Ilmansaasteiden vaikutukset väitöskirjan aiheina - Vakka-Suomen Sanomat 1996 Fading signals - The Economist 1998 Ilmansaasteet haalistavat talitiaisen rintahöyhenet - Helsingin Sanomat 1998 Kirjosieppo kärsii ilman saasteista - Maaseudun Tulevaisuus 1998 Smog casts a pall over sex life of birds - New Scientist 1998 Great tits in polluted area are fading fast - BBC Wildlife Magazine 1999 Feedback - New Scientist 1999 Great Tit is Voting for Clean Air - Priroda [Nature, Moscow] 1999 Kirjosieppo riutuu Harjavallan tehtaan varjossa - Helsingin Sanomat 1999 Artikkeli Harjavallan lintututkimuksista - Keski-Pohjanmaa 1999 Koikkalaisen pakina - Seura 1999 Tehtaiden naapurissa asustaa kalvakkaita talitinttejä - Kemia 26/99 Linnut kertovat ympäristön muutoksista - TV-2, EKOISTI 1999 Pollution’s True Colours - Nature Australia 2000 Linnusto toipuu luonnon puhdistuessa - Turun Sanomat 2000 Flying comeback - New Scientist 2000 Komea isä saa poikia - Satakunnan Kansa 2000 Enemmän poikasia, vähemmän raajarikkoja - Helsingin Sanomat 2000 Links Ilmansuojelu (2/98):Effects of heavy metal emissions in forests around Harjavalta Publications , reprint requests to Tapio Eeva Eeva, T., Lehikoinen, E. and Nurmi, J. 1994: Effects of ectoparasites on breeding success of great tit ( Parus major ) and pied flycatcher ( Ficedula hypoleuca ) in an air pollution gradient. - Canadian Journal of Zoology 72: 624-635. Abstract (PDF) Eeva, T., & Lehikoinen, E. 1994: Effects of Air Pollution on the Breeding of Pied Flycatcher Ficedula hypoleuca and Great Tit Parus major . - Journal für Ornithologie 135: 236 (Abstract). 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: 312-323. Abstract ( PDF ) 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: 631-639. Abstract (PDF) Eeva, T. 1996: Direct and indirect effects of air pollution on two hole-nesting bird species. - Annales Universitatis Turkuensis Ser. A. Tom. 83 (doctoral dissertation). Eeva, T. & Lehikoinen, E. 1997: Talitiainen ja kirjosieppo kärsivät eri tavoin ilmansaasteista. - Luonnon Tutkija 3: 79-82. Eeva, T., Lehikoinen, E. & Pohjalainen, T. 1997: Pollution-related variation in food supply and breeding success in two hole-nestong passerines. - Ecology 78: 1120-1131. Full text (PDF) Eeva, T., Lehikoinen, E. & Sunell C. 1997: The quality of pied flycatcher ( Ficedula hypoleuca ) and great tit ( Parus major ) females in an air pollution gradient. - Annales Zoologici Fennici 34: 61-71. Full text (PDF) Eeva, T. & Lehikoinen, E. 1998: Local survival rates of the pied flycatchers ( Ficedula hypoleuca ) and the great tits ( Parus major ) in an air pollution gradient. - Ecoscience 5: 46-50. Eeva, T., Lehikoinen, E. & Rönkä, M. 1998: Air pollution fades the plumage of the great tit. - Functional Ecology 12: 607-612. Full text (PDF) Lehtiniemi, T. 1998: Kirjosiepon värimuodoista. - M.Sc. Thesis . University of Turku. 56 pp. Sarholm, E. 1998: Talitiaisen ( Parus major ) ja kirjosiepon ( Ficedula hypoleuca ) ravinto ja ruokailukäyttäytyminen tunnetussa ilmansaastegradientissa. - M.Sc. Thesis . University of Turku. 42 pp. Bojarinova, J. G., Lehikoinen, E. & Eeva, T. 1999: Dependence of postjuvenile moult on hatching date, condition and sex in the Great Tit. - Journal of Avian Biology 30: 437-446. Full text (PDF) Tanhuanpää, S., Eeva, T., Lehikoinen, E. & Nikinmaa, M. 1999: Developmental changes in 7- ethoxyresorufin-O-deethylase (EROD) and -aminolevulinic acid dehydratase (ALA-D) activities in three passerines. - Comparative Biochemistry and Physiology : Part C 124: 197-202. Full text (PDF) 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. - Environmental pollution 109: 303- 309. Full text (PDF) Lehikoinen, E. 1999: Talitiaisen puku haalistuu Harjavallassa. - Aurora 3: 16-17. Lehikoinen, E., Eeva, T. & Rönkä, M. 1999: Harjavallan pönttölinnut ilman saastumisen vaikutuksen mittareina. - Linnut 3: 12-16. Lehikoinen, E. (1999): Ilmansaasteet haalistuttavat talitiaiset. - Suomen Luonto 2/99: 18. Rönkä, M. 1999: Talitiaisen ( Parus major ) poikasten höyhenpuvun väritys ilmansaastegradientilla. - M.Sc. Thesis . University of Turku. 76 pp. Eeva, T., Tanhuanpää, S., Råbergh, C., Airaksinen, S., Nikinmaa, M. & Lehikoinen E. 2000: Biomarkers and fluctuatin g as y mmetr y as indicators of p ollution induced stress in two hole-nestin g passerines. - Functional Ecology 14: 235-243. Full text (PDF) Eeva, T. & Lehikoinen, E. (2000): Pollution and breeding success in wild birds. - Nature 403: 851-852. Full text (PDF) Lehikoinen, E. & Eeva, T. (2000): Tunne tuttu talvilintu. - Tiede 2000 2/2000. Ilmonen, P., Taarna, T. & Hasselquist, D. (2000): Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. - Proceedings of the Royal Society of London B 267: 1-6. Full text (PDF) Taarna, T. 2000: Haudonnan kustannukset ja taudinvastustuskyky kirjosiepolla ( Ficedula hypoleuca ). - M.Sc. Thesis . University of Turku. 50 pp. Viljanen, M. 2000: Kirjosiepon ( Ficedula hypoleuca ) lisääntymismenestys erilaisissa elinympäristöissä. - M.Sc. Thesis . University of Turku. 31 pp. Eeva, T., Lehikoinen, E., Rönkä, M., Lummaa, V. & Currie, D. (2002): Different responses to cold weather in two pied flycatcher populations. - Ecography 25: 705-713. Full text (PDF) Eeva, T., Hakkarainen, H. & Koivunen, V. (2003): Population densities of forest birds in a heavy metal pollution gradient. - Avian Science 2: 227-236. Full text (PDF) Ryömä, M. (2003): Ravinnon laadun vaikutus talitiaisen ( Parus major ) ja kirjosiepon ( Ficedula hypoleuca ) poikasten raskasmetallialtistukseen. - M.Sc. Thesis . University of Turku. 54 pp. Eeva, T., Lehikoinen, E. and Nikinmaa, M. (2003): Pollution-induced nutritional stress in nestling birds: an experimental study of direct and indirect effects. - Ecological Applications 13: 1242-1249. Full text (PDF) Eeva, T. & Lehikoinen, E. (2004): Rich calcium availability diminishes heavy metal toxicity in Pied flycatcher. – Functional Ecology 18: 548-553. Full text (PDF) Ahola, M., Laaksonen, T., Sippola, K., Eeva, T., Rainio, K. and Lehikoinen, E. 2004 Variation in climate warming along the migration route uncouples arrival and breeding dates. – Global Change Biology 10: 1610-1617. Full text (PDF) Eeva, T., Sorvari, J. & Koivunen, V. (2004): Effects of heavy metal pollution on red wood ant ( Formica s.str.) populations . – Environmental Pollution 132: 533-539. Full text (PDF) Both, C., Artemyev, A. V., Blaauw, B., Cowie, R. J., Dekhuijzen, A. J., Eeva, T., Enemar, A., Gustafsson, L., Ivankina, E. V., Jarvinen, A., Metcalfe, N. B., Nyholm, N. E. I., Potti, J., Ravussin, P. A., Sanz, J. J., Silverin, B., Slater, F. M., Sokolov, L. V., Torok, J., Winkel, W., Wright, J., Zang, H. and Visser, M. E. 2004 Large-scale geographical variation confirms that climate change causes birds to lay earlier. – Proceedings of the Royal Society of London Series B - Biological Sciences 271: 1657- 1662. Full text (PDF) Eeva, T., Hasselquist, D., Langefors, Å., Tummeleht, L., Nikinmaa, M. and Ilmonen, P. (2005): Pollution related effects on immune function and stress in a free-living population of pied flycatcher. – Journal of Avian Biology 36: 1-8. Full text (PDF) Nikkinen, L. ( 2005 ) : The effect of carotenoids on p luma g e colour and success of g reat tit ( Parus major ) in a polluted environment. – M.Sc. Thesis . University of Turku. 53 pp. ( In Finnish ) Full text (PDF) Eeva, T., Ryömä, M. and Riihimäki, J. 2005. Pollution-related changes in diets of two insectivorous passerines. – Oecologia 145: 629-639. Full text (PDF) Eeva, T., Belskii, E. & Kuranov, B. (2006): Environmental pollution affects genetic diversity in wild bird populations. – Mutation Research 608: 8 - 15. Full text (PDF). Eeva, T., Hakkarainen, H., Laaksonen, T. & Lehikoinen, E. (2006): Environmental pollution has sex- dependent effects on local survival. B Biology Letters 2: 298-300. Full text (PDF) Laaksonen, T., Ahola, M., Eeva, T., Väisänen, R. and Lehikoinen, E. (2006) Climate change, migratory connectivity and changes in laying date and clutch size of the Pied flycatcher. B Oikos ( In press ). Sorvari, J., Rantala, L.M., Rantala, M.J., Hakkarainen, H. and Eeva T. (2006): Heavy metal pollution disturbs immunity: toxic effects in wild ant populations. B Environmental Pollution ( In press ). Full text (PDF) | Section of Ecology | Department of Biology | | University of Turku | . text (PDF) Eeva, T., Hasselquist, D., Langefors, Å., Tummeleht, L., Nikinmaa, M. and Ilmonen, P. (2005): Pollution related effects on immune function and stress in a free-living population of. 1610-1617. Full text (PDF) Eeva, T., Sorvari, J. & Koivunen, V. (2004): Effects of heavy metal pollution on red wood ant ( Formica s.str.) populations . – Environmental Pollution 132: 533-539 Air pollution impacts on birds and insects Project leader: Tapio Eeva, docent Ph.D. students: Jouni Sorvari,

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