DIRECT AND INDIRECT EFFECTS OF AIR POLLUTION

ON TWO HOLE-NESTING BIRD SPECIES

by

TAPIO EEVA

TURUN YLIOPISTOTurku 1996

This thesis is a summary of the following articles which are referred to in the text bytheir Roman numerals:

I. Eeva, T. & Lehikoinen, E. 1995: Egg shell quality, clutch size andhatching success of the great tit (Parus major) and the pied flycatcher(Ficedula hypoleuca) in an air pollution gradient. - Oecologia 102:312-323.

II. Eeva, T. & Lehikoinen, E. 1996: Growth and mortality of nestling GreatTits (Parus major) and Pied Flycatchers (Ficedula hypoleuca) in a heavymetal pollution gradient. - Oecologia 108: 631-639.

III. Eeva, T., Lehikoinen, E. & Sunell, C. 1997: The quality of PiedFlycatcher (Ficedula hypoleuca) and Great Tit (Parus major) females inan air pollution gradient - Annales Zoologici Fennici 34: 61-71.

IV. Eeva, T., Lehikoinen, E. & Nurmi, J. 1994: Effects of ectoparasites onbreeding success of great tits (Parus major) and pied flycatchers(Ficedula hypoleuca) in an air pollution gradient. - Canadian Journal ofZoology 72:624-635.

V. Eeva, T., Lehikoinen, E. & Pohjalainen, T. 1997: Pollution-relatedvariation in food supply as a determinant of breeding success in twohole-nesting passerines. - Ecology 78: 1120-1131.

VI. Eeva, T. & Lehikoinen, E. 1998: Local survival rates of the piedflycatchers (Ficedula hypoleuca) and the great tits (Parus major) in anair pollution gradient. - Ecoscience 5: 46-50.

CONTENTS

1. INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1

2. STUDY AREA, POLLUTION SOURCE AND MAIN POLLUTANTS . . . . . . . . . 1

3. STUDY SPECIES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

4. EFFECTS OF AIR POLLUTION ON BIRDS . . . . . . . . . . . . . . . . . . . . . . . . . . 3

4.1. Egg shell quality and hatchability . . . . . . . . . . . . . . . . . . . . . . . . 34.2. Nestling growth and mortality . . . . . . . . . . . . . . . . . . . . . . . . . . . 34.3. Growth abnormalities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44.4. Survival and recruitment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

5. MECHANISMS OF AIR POLLUTION EFFECTS ON BIRDS . . . . . . . . . . . . . . 5

5.1. Heavy metals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55.2. Calcium deficiency . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

5.2.1. Natural availability of calcium . . . . . . . . . . . . . . . . . . . . 55.2.2. Calcium manipulation experiment . . . . . . . . . . . . . . . . . 6

5.3. The quality of females . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75.4. Food abundance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95.5. Ectoparasites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

6. CONCLUSIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

ACKNOWLEDGEMENTS

REFERENCES

Introduction 1

1. INTRODUCTION

Air pollution has become a widespread andexpanding environmental problem in this

century (Holdgate 1979, Postel 1984, Hutchinson& Meema 1987, Pitelka 1994). Air pollutants aregenerally defined as aerial substances that havesome adverse effects on plants, animals ormaterials (Treshow 1984). Environmentalpollution studies made during the last fewdecades have largely concerned the toxic levelsof pollutants in organisms or the abundance ofcertain pollution-sensitive species, “biomoni-tors”. In recent years, there has been anincreasing demand to direct environmentalstudies towards giving information about thelarger ecological processes. Also a greateremphasis on individual based parameters iscalled for in field assessments of environmentalimpacts (Osenberg et al. 1994).

To understand larger ecological processes weneed information from various trophic levels.Although the literature regarding pollutant levelsin wildlife is extensive, there are only few studiesconcerning the ecological consequences ofenvironmental pollution on higher trophic levels.Small insectivorous passerines are considered tobe good candidates for such studies in terrestrialecosystems. In addition to being ubiquitous,intensively studied, and high in the food chain,they are considered good biomonitors due to theirhigh metabolic rate (Morrison 1986, Root 1990).On the other hand, birds may respond similarly todifferent kinds of pollutants or their secondaryeffects, which sometimes makes it difficult toreveal causal relations without detailed studies(Morrison 1986).

Environmental stress gradients are universalin all habitat types (Menge & Sutherland 1987).Perhaps the best opportunities to conductdetailed impact studies in nature are offered bywell-defined pollution gradients aroundpoint-source discharges. Because rigorousbefore-after-type studies (Green 1979, Osenberget al. 1994) are often out of the question due totheir sampling scheme, the distribution betweenanthropogenic and “natural” sources of variationmust usually be made afterwards by spatialcomparisons. Even then a careful control overnatural sources of variation is needed (Green1979, Dutilleul 1993, Posthumus 1984).

The aim of this thesis is to measureindividual and population level effects of airpollution, both heavy metal contamination andacidification, on breeding performance andsurvival of two passerine bird species. Myexperimental field consisted of 14 study sitesaround a polluting factory complex. In terms ofEberhard and Thomas (1991), the samplingdesign is observational, i.e. selectedsubpopulations subjected to different levels ofpollution are compared. I have carried outbottom-up breeding performance analyses, i.e.from analyses of egg quality (I), nestlingmortality (II) and female quality (III) tosecondary effects of parasites (IV) and foodabundance (V), and finally to recruitment andsurvival of adult birds (VI). This study clarifiesthe interactions between natural and anthropoge-nic effects on breeding performance and theimportance of direct vs. indirect effects.

2. STUDY AREA, POLLUTION SOURCE

AND MAIN POLLUTANTS

The study was carried out in the surroundings ofthe town of Harjavalta (61°20'N, 22°10'E), SWFinland (Fig. 1) during 1991 - 1994. Twelvestudy sites, each with 30 - 50 nest boxes, wereestablished early in spring 1991 in the airpollution gradient in three main directions (SW,SE and NW) from the centre of town, the mostdistant site (60°53'N, 22°6'E) being 48 km fromthe centre. Two more sites were established inspring 1992 at 64 km (60°44'N, 21°59'E) and 74km (60°39'N, 22°1'E) south from the center.

Figure 1. Location of the study area and 11 study sites(•) around the factory complex.

Introduction2

Table 1. Particulate atmospheric emissions (t/a) of sulphuric oxide and heavy metals fromOutokumpu copper smelter in Harjavalta (source: annual reports from OutokumpuHarjavalta Metals Oy).

pollutant 1990 1991 1992 1993 1994

SO2 8800 5200 4800 4700 5000

Copper 80 80 60 50 40

Nickel 31 15 10 7 6

Zinc 160 90 12 11 6

Lead 80 45 9 6 3

Cadmium 4.2 1.6 1.0 0.9 0.7

Arsenic 28 18 12 11 5

The main source of air pollutants in this areais a factory complex producing copper, nickeland fertilizers in the centre of Harjavalta.Especially zinc, copper, lead, and nickel arecommon pollutants in the area (Kubin 1990,Jussila & Jormalainen 1991). Copperconcentrations of 650 mg/kg have been measuredin soil close to the factories (Hyvärinen et al.1993). During the early activity of the factory inthe 1940's, sulphurdioxide produced in theprocess was not made use of, but emitted into thesurroundings. This led to decline in the forest andloss of most ground vegetation in thesurroundings of the town. Later on, most SO2

was utilized to produce sulphuric acid. Emissionshave clearly decreased also during the course ofthis study (Table 1).

In general, southerly winds prevail in thearea. However, the shape of the pollution field isan ellipse in the direction of the river valley(southeast to northwest). This has been con-firmed by analyses of SO2 content of pineneedles and species number of bark lichen(Laaksovirta & Silvola 1975), analyses of heavymetals with the moss bag method (Hynninen1986), and analyses of moss and rain watersamples from the forest floor (Jussila et al.1991). This information was used in planning thelocation of study sites. Metal contents decrease inan exponential manner with increasing distancefrom the factory complex, approaching the

background level 5 - 10 km away from thefactory. Weather data come from the Peipohjameteorological station, 8.6 km (ESE) from thefactories.

The forests in the area are dominated by Scotspine (Pinus sylvestris), which forms mixedstands with spruce (Picea abies) and birch (Betu-

la spp.). The proportion of spruce increases awayfrom the center of town. In the field layer, dwarfshrubs Vaccinium vitis-idaea and V. myrtillus

dominate. In the three study sites closest to thefactory complex, field layer vegetation is almostabsent due to the long-term effect of pollution(Salemaa & Vanha-Majamaa 1993).

3. STUDY SPECIES

The Pied Flycatcher (Ficedula hypoleuca Pallas)is a small passerine bird ranging over most ofnorthern and eastern Europe (Cramp & Perrins1993). The species winters in tropical WestAfrica. Males generally arrive in my study area inMay, about 1 week ahead of females. Layingstarts in the end of May. The diet consists ofvarious arthropods. F. hypoleuca obtains foodfrom trees or ground or by darting out from theperch after flying prey. Both sexes feed thenestlings. A part of males are polygynous, andsuch males mainly help in feeding their primarybrood (Lundberg & Alatalo 1992).

Introduction 3

The Great Tit (Parus major L.) is amonogamous and resident species extending overthe whole of Europe (Cramp & Perrins 1993).This implies that in my study area this species issusceptible to pollution effect all year roundwhereas the migrant, F. hypoleuca, is onlysusceptible three months during the breedingtime. P. major starts laying in the beginning ofMay. During breeding time P. major feed on avariety of insects, especially Lepidoptera larvae.Both sexes feed the nestlings.

F. hypoleuca and P. major are found in avariety of forest habitats from luxuriantdeciduous woodlands and subalpine birch forestto coniferous forest. Both species nest in treeholes but also readily accept nest-boxes. Thebreeding biology of these birds has beenintensively studied during the past 40 years(Lundberg & Alatalo 1992, Cramp & Perrins1993, Glutz von Blotzheim & Bauer 1993,Gosler 1993). The numbers of breeding pairs inthe study area in 1991 - 1994 are shown in paperVI, Table 1.

4. EFFECTS OF AIR POLLUTION

ON BIRDS

4.1. Egg shell quality and hatchability

Egg shell thickness, egg volume, clutch-size andhatching success were studied in 1991 - 1993 (I).Unhatched eggs were collected for measuringshell quality. In general, F. hypoleuca was moresusceptible to pollutants than P. major. Eggshells of F. hypoleuca were about 17 % thinnerand eggs were about 8 % smaller in volume nearthe factory than at a distance of 10 km. Clutch-size of F. hypoleuca was significantly smallerand hatching success markedly reduced at a studysite next to the factory complex.

In P. major, variation in shell thickness oregg volume was not significantly related to thedistance from the pollution source. Clutch-sizeand hatching success of P. major did notsignificantly differ among study sites, althoughthere was a similar tendency in hatching successas in F. hypoleuca. Clutches of both speciescontained less shell material and both species hadmore eggless nests near the factory than furtheraway. The surface structure of the eggshells wasstudied by scanning electron microscope.

Especially in F. hypoleuca, the egg shell surfacewas more rough and porous near the factory.

4.2. Nestling growth and mortality

Nestling growth, growth abnormalities, mortalityand breeding success were studied in 1991 - 1993(II). Exposure of birds to heavy metals wasstudied by fecal concentrations (Fig. 2). Thegrowth of F. hypoleuca nestlings was poorer andthey suffered higher mortality very close to thefactory complex, but did relatively well in allother sites. Decreased nestling growth andfledging success of P. major extended fartherfrom the factory than in F. hypoleuca. I suggestthat the strong response of F. hypoleuca is relatedto the increased amount of heavy metals in dietnear the factory complex (Fig. 2), but synergisticeffects of a low amount of calcium in food arealso probable (chapter 5.2.). The response of P.

major is rather a consequence of habitat change,that has taken place during the activity of thefactory complex. The main reason for thedifferent responses in these two bird species isprobably their different foraging habits (II, V).

Figure 2. Copper concentration (dry weight, d.w.) infaeces of F. hypoleuca (a) and P. major (b) nestlings indifferent distances from the factory (sampling andanalyses described in paper II).

Introduction4

Although the emissions have decreased duringthe course of this study (Table 1), neither theclutch-size nor breeding success have essentiallyimproved in polluted area in either species (Figs.3 and 4).

4.3. Growth abnormalities

Nestlings were checked for any visibleabnormalities in their bodies. The most commonaberrations were defectively developed tibiotarsiand tarsometatarsi (II). This was evident from theweak, soft and bent legs of chicks. In some cases,corresponding abnormalities were also observedin wings.

Defectively developed legs occurred in F.

hypoleuca nestlings significantly more often nearthe factory than farther away. At the most heavilypolluted site, about 27 % of the broods containedone or more nestlings with visible defects in their

Figure 3. The mean clutch size of F. hypoleuca (a) and P.

major (b) at two distances from the pollution source in1991 - 1994. Destroyed, second and replacement clutchesomitted. Bars denote standard error.

limbs (II). In many cases these nestlings died.Although the crippled nestlings sometimesreached fledging size, they were probably tooweak to leave the nest cavity. In P. major nocorresponding defects were noted. The observedabnormalities in bone structure of F. hypoleuca

nestlings are likely to arise from the same reasonas abnormal egg-shells, i.e. from the impairingeffect of dietary heavy metals on Ca-metabolism.

4.4. Survival and recruitment

The local survival and recruitment of F. hypo-

leuca and P. major females were studied withcapture-recapture data from 1991 - 1995 (VI).The local survival of F. hypoleuca females ten-ded to be reduced near the pollution source, being7% compared to 23% in most distant areas, butthis difference was not statistically significant. P.

major did not show reduced survival in polluted

Figure 4. The mean breeding success of F. hypoleuca (a)and P. major (b) at two distances from the pollutionsource in 1991 - 1994. Destroyed, second and replacementclutches omitted. Bars denote standard errors.

Introduction 5

area, but slightly higher survival probabilitiesoccurred in moderately polluted area thanelsewhere. The slightly higher survivalprobability in moderately polluted area may berelated to the availability of ample invertebratefood for P. major (V). The fact that local survivalof migratory F. hypoleuca, but not of resident P.

major, was decreased in polluted areaemphasizes the importance of diet in determiningthe response of a bird to the pollutants. In winter,the vicinity of the town probably compensates forthe possible detrimental effects of pollution viaan increased amount of winter food and reducedpredation pressure (VI). Differences inrecruitment rates of young birds could not beconfirmed because of the low number of recruitsin both species (VI).

5. MECHANISMS OF AIR POLLUTION

EFFECTS ON BIRDS

5.1. Heavy metals

Exposure of birds to heavy metals was studied bymeasuring concentrations in nestling faeces andin one of their food items, red ants (Formica

rufa) sampled from hills (II). The concentrationsin faeces reflected well the heavy metal gradientmeasured in soil, rain water and leaf samplesfrom the same area (Sippola & Erviö 1986, Fritzeet al. 1989, Jussila & Jormalainen 1991, Koriche-va & Haukioja 1992). The gradient in faecesconcentrations was relatively steep for copper,nickel and lead (II). A less steep gradient wasobserved for cadmium and zinc. The sameapplies to the concentrations in ants (II). Asummary of components potentially involved inegg shell and bone abnormalities in Harjavalta ispresented in figure 5.

In general, F. hypoleuca received more heavymetals in its food than P. major (II). Thedifference between species is probably due totheir different diet. In my study area F. hypoleuca

takes about half of its food items from the groundand air, whereas P. major forages almostexclusively in tree foliage during the nestlingperiod (V). Heavy metals probably accumulatemore in the ground-living (mobile, often adult)food items of F. hypoleuca (e.g. ants,cockroaches, beetles) than in the foliage-living

(less mobile, often larval) insect food (e.g.caterpillars, spiders, aphids) of P. major (seeHunter & Johnson 1982, Bengtsson & Rundgren1984, Grue et al. 1986). Food selection is thus ofprimary importance in the susceptibility of birdsto heavy metals.

5.2. Calcium deficiency

5.2.1. Natural availability of calcium

In Harjavalta, the amount of exchangeablecalcium in the humus layer is relatively low,which may partly be explained by natural soildifferences (Jussila et al. 1991). On the otherhand, the amount of Ca in pine needles isrelatively high near the factory complex(Heliövaara and Väisänen 1989, Jussila &Jormalainen 1991). This is probably because thefactory complex also emits calcium-rich fertilizerdust, with a pH varying from 5 to 7.5(Laaksovirta and Silvola 1975).

The different Ca-gradients in soil and needlesare probably reflected in nestling faecesconcentrations of P. major and F. hypoleuca (II)via their different foraging behaviour (V). Thismay be the reason for the relatively high amountof Ca in the faeces of P. major nestlingscompared to those of F. hypoleuca at the studysite next to the factory in both study years (I).Fallen snail shells were frequently found from thenests of F. hypoleuca in Harjavalta, but therewere almost none in the site closest to the factory(II). This may stress the importance of certainCa-rich food items which are absent from themost polluted site (see Graveland et al. 1994).The reduced amount of Ca in the diet probablymakes birds more susceptible to the detrimentaleffects of heavy metals (see Six & Goyer 1970).

5.2.2. Calcium manipulation experiment

In summer 1994 I made an experiment in whichcalcium carbonate (CaCO3) was artificially addedto 12 territories of F. hypoleuca. Another 12territories were used as controls. The study wasperformed at the site 0.7 km south of the factorycomplex. Commercial crushed calcium carbonatewas provided at the time of nest building on theroof of the nest-box, on the feeder at the ent

Introduction6

Figure 5. Summary of the major components potentially involved in egg shell and bone defects of F.

hypoleuca around Harjavalta factory complex. Statements both for and against the gilt of each element andsome known symptoms caused by toxic concentrations (gathered from the papers of Evans 1973,Scheuhammer 1991, Outridge & Scheuhammer 1993).

rance, and on the ground. The intake of calciumwas followed by video cameras (Table 2).Surprisingly, males ate the calcium pieces morefrequently than females (Table 2). I do notknow the reason for such behaviour but toensure that nestlings got their proportions Idaily fed pieces of calcium with tweezers to thenestlings over 4 days old.

Control and treatment nests were selectedaccording to randomized four block design toensure even spatial distribution of treated nests.Four blocks were arranged so that they wereequally far from the factory complex. Inside theblocks, treated and untreated nests wereselected in turn according to the arrival date offemales. This ensured similar temporaldistribution of experimental nests.Theexperiment involved two parts. In the first partI followed the egg characteristics, laying order,clutch-size and hatching success. In the secondpart I studied the growth and developmentalabnormalities of nestlings. Original hatchlingswere removed from the nests at day 0 and new

broods were created by bringing nestlings frombackground sites, 10 km from the factorycomplex. The new broods of five young weremixed as regards the origin of nestlings, so thatevery brood contained nestlings from threedonor nests. By mixing nestlings I wanted toavoid genetic effects on growth anddevelopment.

Egg length and breadth were measured ondaily visits. Females were captured after theyhad incubated 9 days and again when thenestlings were 10 days old. Females wereringed, weighed and their wing length wasmeasured. Nestlings were weighed and winglength was measured on days 1, 5 and 10. Eachtime nestlings were checked for visibleabnormalities in their legs and wings.

There were no differences in female winglength (ANOVA, F1,16, P= 0.64), weight atincubation time (ANOVA, F1,16, P= 0.95),weight at nestling time (ANOVA, F1,11, P=0.93) or age distribution (P2= 0.00, df= 1, P=1.00) between the two groups, so possible

Introduction 7

Table 2. Calcium pieces taken in feeding experiment by male and female F. hypoleuca

at different stages of breeding. Hours denote the observation time with video cameras.

male female

Stage hours n freq n freq

Nest building 47.8 15 0.31 4 0.08

Egg laying 31.0 33 1.07 5 0.16

Incubation 7.2 2 0.28 1 0.14

Nestlings 7.6 0 0.00 0 0.00

G 93.6 50 0.53 10 0.10

differences between groups cannot beexplained by different female quality.

There were no significant differences in eggsize characteristics between treatment andcontrol groups (Table 3). Although notsignificantly, the mean egg volume was about5% smaller in control nests. Nests with extracalcium had a one egg larger average clutch-size and 9% better hatching success, but thedifferences were not significant (Table 3). Nodifference was found in nestling mass betweengroups, but their wings seemed to grow morerapidly in treated nests (Table 3). Mortality waslow in both groups in the beginning of thenestling period, but at the age of 10 days,treated nests had, on average, one nestling morethan control nests (Table 3). The extra calciummost clearly affected the development ofnestling legs. Most of the control broods hadone or more nestlings with defectivelydeveloped legs, whereas in treated nests nodefects were noted (Table 3).

5.3. The quality of females

Reduced breeding success might result in apolluted area if, in spring the birds assortativelysettled in areas of different degrees ofpollution. Body size, fat reserves, agedistribution, timing of breeding and breedingdensity of females were measured in 1991 -1994 (III). I found only few such differences infemale quality which could be caused by a

different kind of assortment along the pollutiongradient. Females were of the same size in allareas. At nestling time, P. major females wereheaviest in the moderately polluted area, butthey were not lighter in polluted area than inbackground area.

In both species the female fat reserves weresmaller in polluted area during the coldbreeding season. This emphasizes the effect ofsimultaneous stress factors on the femalecondition. In the beginning of the study theproportion of young F. hypoleuca females wasslightly higher in polluted area than elsewherebut after two years it was the same everywhere.F. hypoleuca females started laying later,whereas P. major females laid earlier inpolluted area, but the strength of these effectsalso depended on the year. The clearestdifference among distance zones was found inbreeding density. Both species bred moresparsely in polluted area. I conclude thatfemales preferred to breed in unpolluted areas,but differed only marginally in their size andcondition between polluted and unpollutedhabitats.

5.4. Food abundance

Invertebrate abundance was measured along thepollution gradient in 1992 to study whether thereduced breeding performance of birds wascaused by pollution-induced alterations in theirfood supply (V). At the nestling time of both

Introduction8

Table 3. Comparison of egg and nestling parameters in calcium manipulation experiment.Original clutches were followed up to hatching, whereafter new broods of 5 nestlings wereformed and followed onwards. All tests are one-tailed.

Treatment Control

Parameter Mean SE n Mean SE n P

Egg length (mm)1 17.4 0.26 12 17.1 0.36 12 0.279

Egg breadth (mm)1 13.2 0.11 12 13.0 0.07 12 0.076

Egg volume (cm3)1 1.52 0.04 12 1.45 0.04 12 0.129

Clutch size2 5.8 0.40 9 4.9 0.54 9 0.089

Hatching success (%)2 86.2 6.37 9 79.2 8.42 9 0.373

Weight (g), 5 days3 7.4 0.44 7 7.4 0.44 7 0.475

Weight (g), 10 days3 12.6 0.54 7 12.4 0.54 7 0.394

Wing (mm), 5 days3 16.1 0.61 8 14.2 0.66 7 0.036

Wing (mm), 10 days3 36.8 1.29 7 33.3 1.29 7 0.060

Brood size, 5 days2 4.9 0.13 8 4.7 0.18 7 0.227

Brood size, 10 days2 4.7 0.18 7 3.7 0.57 7 0.077

Leg abnormalities (%)4 0 7 75 8 0.008

1 One-way ANOVA, egg volume was calculated using the equation of Ojanen et al. (1978).2 Kruskall-Wallis test, only those nests where incubation started were used in calculating clutch size.

Suddenly destroyed nests were omitted when calculating brood size.3 ANCOVA, day 1 values were used as covariates, least squares means.4 Percentages denote the proportions of broods. Chi-square test.

species, larvae were scarce in Scots pine ) thedominant species among the trees ) close to thefactory complex, peaked at the moderatelypolluted zone, 2 - 4 km from the factory, andtended to decrease further away. Both birdspecies preferred pine, particularly in themoderately polluted zone, where also theproportion of larvae in the diet of P. major washigh. Ground-living arthropods were scarceclose to the factory, but among-site variationwas high even in the cleanest area.

The breeding success of both bird speciescorrelated positively with prey abundance, butonly in P. major did the lack of food retardnestling growth. Also the productivity of

different sized clutches was affected in P.

major but not in F. hypoleuca. Large F.

hypoleuca clutches produced more fledglingsthan smaller clutches at all parts of thepollution gradient, while this was true for P.

major in the moderately or slightly pollutedparts of the gradient only; in the most pollutedareas clutches comprising 6 to 11 eggsinvariably produced 3 to 4 fledglings. Thestronger impact of food abundance on P. major

probably results from the different diet in twobird species. P. major, a caterpillar specialist,suffered from the shortage of larvae in the latenestling period.

Introduction 9

5.5. Ectoparasites

Ectoparasites are one of the stress factorsencountered by a reproducing bird. To studythe simultaneous effects of ectoparasites andpollution stress I counted the numbers of larvaeof an ectoparasitic fly, Protocalliphora azurea

(Diptera: Calliphoridae), an adult and larvalHen f lea, Ceratophyl lus gal l inae

(Siphonaptera: Ceratophyllidae) and other nestdwellers from the nests in 1991 and 1992 (IV).Protocalliphora larvae were more frequentlyfound in the nests of P. major than in the nestsof F. hypoleuca. The prevalence ofProtocalliphora larvae tended to be smaller inpolluted areas. The number of larvae correlatedpositively with the nest size and brood size ofP. major, which may be the result ofdifficulties of sanitation in large and crowdednests.

Nests of F. hypoleuca contained more adultfleas in polluted areas than in control areas.This observation supports the idea thatpollution-induced stress makes birds moresusceptible to harm from natural stresses.Protocalliphora larvae retarded the growth ofP. major nestlings and fleas increased thenestling mortality of F. hypoleuca, but theseeffects were not enhanced by air pollution. Iconclude that the ectoparasites studied, at thedensities observed in our study area, were ofminor importance in determining the breedingsuccess of these two bird species.

6. CONCLUSIONS

The consequences of air pollution weredifferent for the two bird species. F. hypoleuca

directly responded to the steep pollutiongradient (1 - 2 km from the pollution source)and was affected most severely at the egg stage.The response of P. major extended farther fromthe factory complex (up to 3 - 4 km) and wasmore obvious at the nestling stage, when thenestling mortality was increased near thepollution source.

The results indicate that the reducedbreeding performance of birds in the pollutedarea may have various causes: one species mayrespond directly to toxicity while the other toreduced food supply. The strong and steep

response of F. hypoleuca is related to the highamount of heavy metals in its diet, and thiseffect is enhanced by the lack of calcium-richfood. The decreased amount of invertebratefood in the polluted area was the main reasonfor lowered nestling production in P. major.The different responses of the two bird speciesare related to their different foraging habits.Due to low fledgling production and decreasedlocal survival, the most polluted area aroundthe factory complex is probably a sink area forthe F. hypoleuca population, with continuousimmigration from outside. In P. major, thesurvival probability of breeding females did notdiffer between polluted and unpolluted areas.This contrasts with the intuitive idea thatresident species, being exposed to impacts ofpollution all year round, would be moreseverely affected than a migrant species whichonly arrives to breed in polluted area.

Although anthropogenic, air pollution isone stress factor among others, and it may haveevolutionary effects similar to more naturalfactors. This study demonstrated a reduction inthe optimal clutch size of P. major in pollutedarea, whereas in F. hypoleuca such an effectwas not noted. However, adaptations topollution or its secondary effects are unlikelybecause the impact area is small compared tothe dispersal capacity of birds and thesurrounding gene pool.

Both species can be considered suitablebiomonitors, but they are sensitive to differentfactors. A partial ground forager, F. hypoleuca,is more susceptible to receiving aeriallydeposited heavy metals from the environmentthan the foliage forager, P. major. Instead, P.

major is probably a more sensitive indicator ofsecondary environmental changes than F.

hypoleuca. Species-specific differences inresponses should be carefully considered whenplanning projects for air pollution monitoring.

ACKNOWLEDGEMENTS

First but not least I wish to thank mysupervisor, Prof. Esa Lehikoinen, who hassuprisingly many characteristics of a goodsupervisor. Esa never hesitated to introducenew ideas and methods, and sometimes evensucceeded in getting me involved in them. I

Introduction10

also wish to thank Prof. Erkki Haukioja, whomany times encouraged me in the course of thisstudy and, somehow, even seemed to believe init.

I am also most grateful to Jorma Nurmi, themost efficient field assistant of the northernhemisphere. Without his enthusiastic attitudeand enormous contribution in data collectionthis study would have been only a reflection ofa study. Simo Veistola, besides helping withthe field work, was invaluable in criticizing mymanuscripts. Luckily, he always understood themain ideas in them much better than I did.

Several other people took part in the datacollection. Tuija Pohjalainen was responsiblefor the invertebrate sampling and dived deeplyinto the fascinating world of coprology. CaritaSunell and Erja Sarholm were fast enough tofollow the birds in order to reveal their foraginghabits. Tapio Aalto, Jari Valkama, JuliaBojarinova, Petteri Ilmonen, Juha Niemi andTapani Lilja helped me in catching the birdswho did not always understand that the workwas done for their good. People in Harjavaltaand surroundings helped me by sendinginformation on ringed birds.

Many times, people in the Laboratory ofEcology in Turku University and people in theSatakunta Environmental Research Centerhelped me in the course of the study.

Jürgen Wiehn, Jan-Åke Nilsson and JuhaTiainen made valuable comments on the earlierversion of this thesis. Jacqueline Välimäkikindly checked the language.

I also want to thank my wife, Elina, for herpatience in many situations. Thank you (!).

This study was financed by the Academy ofFinland.

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