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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 vi

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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 nestlings

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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

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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 fledging success in the polluted area Our results suggest that humoral immune response of birds may

News!

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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)

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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 fluctuating asymmetry as indicators of pollution induced stress in two hole-nesting

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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 plumage colour and success of great tit (Parus

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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)

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