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DIRECT AND INDIRECT EFFECTS OF AIR POLLUTION
ON TWO HOLE-NESTING BIRD SPECIES
by
TAPIO EEVA
TURUN YLIOPISTO
Turku 1996
This thesis is a summary of the following articles which are referred to in the text by
their Roman numerals:
I.
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 102:312323.
II.
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.
III.
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.
IV.
Eeva, T., Lehikoinen, E. & Nurmi, J. 1994: Effects of ectoparasites on
breeding success of great tits (Parus major) and pied flycatchers
(Ficedula hypoleuca) in an air pollution gradient. - Canadian Journal of
Zoology 72:624-635.
V.
Eeva, T., Lehikoinen, E. & Pohjalainen, T. 1997: Pollution-related
variation in food supply as a determinant of breeding success in two
hole-nesting passerines. - Ecology 78: 1120-1131.
VI.
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.
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 . . . . . . . . . . . . . . . . . . . . . . . .
4.2. Nestling growth and mortality . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.3. Growth abnormalities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.4. Survival and recruitment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3
3
4
5
5. MECHANISMS OF AIR POLLUTION EFFECTS ON BIRDS . . . . . . . . . . . . . . 5
5.1. Heavy metals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.2. Calcium deficiency . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.2.1. Natural availability of calcium . . . . . . . . . . . . . . . . . . . .
5.2.2. Calcium manipulation experiment . . . . . . . . . . . . . . . . .
5.3. The quality of females . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.4. Food abundance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.5. Ectoparasites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5
5
5
6
7
9
9
6. CONCLUSIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
ACKNOWLEDGEMENTS
REFERENCES
1
Introduction
1. INTRODUCTION
A
ir pollution has become a widespread and
expanding environmental problem in this
century (Holdgate 1979, Postel 1984, Hutchinson
& Meema 1987, Pitelka 1994). Air pollutants are
generally defined as aerial substances that have
some adverse effects on plants, animals or
materials (Treshow 1984). Environmental
pollution studies made during the last few
decades have largely concerned the toxic levels
of pollutants in organisms or the abundance of
certain pollution-sensitive species, “biomonitors”. In recent years, there has been an
increasing demand to direct environmental
studies towards giving information about the
larger ecological processes. Also a greater
emphasis on individual based parameters is
called for in field assessments of environmental
impacts (Osenberg et al. 1994).
To understand larger ecological processes we
need information from various trophic levels.
Although the literature regarding pollutant levels
in wildlife is extensive, there are only few studies
concerning the ecological consequences of
environmental pollution on higher trophic levels.
Small insectivorous passerines are considered to
be good candidates for such studies in terrestrial
ecosystems. In addition to being ubiquitous,
intensively studied, and high in the food chain,
they are considered good biomonitors due to their
high metabolic rate (Morrison 1986, Root 1990).
On the other hand, birds may respond similarly to
different kinds of pollutants or their secondary
effects, which sometimes makes it difficult to
reveal causal relations without detailed studies
(Morrison 1986).
Environmental stress gradients are universal
in all habitat types (Menge & Sutherland 1987).
Perhaps the best opportunities to conduct
detailed impact studies in nature are offered by
well-defined pollution gradients around
point-source discharges. Because rigorous
before-after-type studies (Green 1979, Osenberg
et al. 1994) are often out of the question due to
their sampling scheme, the distribution between
anthropogenic and “natural” sources of variation
must usually be made afterwards by spatial
comparisons. Even then a careful control over
natural sources of variation is needed (Green
1979, Dutilleul 1993, Posthumus 1984).
The aim of this thesis is to measure
individual and population level effects of air
pollution, both heavy metal contamination and
acidification, on breeding performance and
survival of two passerine bird species. My
experimental field consisted of 14 study sites
around a polluting factory complex. In terms of
Eberhard and Thomas (1991), the sampling
design is observational, i.e. selected
subpopulations subjected to different levels of
pollution are compared. I have carried out
bottom-up breeding performance analyses, i.e.
from analyses of egg quality (I), nestling
mortality (II) and female quality (III) to
secondary effects of parasites (IV) and food
abundance (V), and finally to recruitment and
survival of adult birds (VI). This study clarifies
the interactions between natural and anthropogenic effects on breeding performance and the
importance of direct vs. indirect effects.
2. STUDY AREA, POLLUTION SOURCE
AND MAIN POLLUTANTS
The study was carried out in the surroundings of
the town of Harjavalta (61°20'N, 22°10'E), SW
Finland (Fig. 1) during 1991 - 1994. Twelve
study sites, each with 30 - 50 nest boxes, were
established early in spring 1991 in the air
pollution gradient in three main directions (SW,
SE and NW) from the centre of town, the most
distant site (60°53'N, 22°6'E) being 48 km from
the centre. Two more sites were established in
spring 1992 at 64 km (60°44'N, 21°59'E) and 74
km (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.
2
Introduction
The main source of air pollutants in this area
is a factory complex producing copper, nickel
and fertilizers in the centre of Harjavalta.
Especially zinc, copper, lead, and nickel are
common pollutants in the area (Kubin 1990,
Jussila & Jormalainen 1991). Copper
concentrations of 650 mg/kg have been measured
in soil close to the factories (Hyvärinen et al.
1993). During the early activity of the factory in
the 1940's, sulphurdioxide produced in the
process was not made use of, but emitted into the
surroundings. This led to decline in the forest and
loss of most ground vegetation in the
surroundings of the town. Later on, most SO2
was utilized to produce sulphuric acid. Emissions
have clearly decreased also during the course of
this study (Table 1).
In general, southerly winds prevail in the
area. However, the shape of the pollution field is
an ellipse in the direction of the river valley
(southeast to northwest). This has been confirmed by analyses of SO2 content of pine
needles and species number of bark lichen
(Laaksovirta & Silvola 1975), analyses of heavy
metals with the moss bag method (Hynninen
1986), and analyses of moss and rain water
samples from the forest floor (Jussila et al.
1991). This information was used in planning the
location of study sites. Metal contents decrease in
an exponential manner with increasing distance
from the factory complex, approaching the
background level 5 - 10 km away from the
factory. Weather data come from the Peipohja
meteorological station, 8.6 km (ESE) from the
factories.
The forests in the area are dominated by Scots
pine (Pinus sylvestris), which forms mixed
stands with spruce (Picea abies) and birch (Betula spp.). The proportion of spruce increases away
from the center of town. In the field layer, dwarf
shrubs Vaccinium vitis-idaea and V. myrtillus
dominate. In the three study sites closest to the
factory complex, field layer vegetation is almost
absent 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 of
northern and eastern Europe (Cramp & Perrins
1993). The species winters in tropical West
Africa. Males generally arrive in my study area in
May, about 1 week ahead of females. Laying
starts in the end of May. The diet consists of
various arthropods. F. hypoleuca obtains food
from trees or ground or by darting out from the
perch after flying prey. Both sexes feed the
nestlings. A part of males are polygynous, and
such males mainly help in feeding their primary
brood (Lundberg & Alatalo 1992).
Table 1. Particulate atmospheric emissions (t/a) of sulphuric oxide and heavy metals from
Outokumpu copper smelter in Harjavalta (source: annual reports from Outokumpu
Harjavalta 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
1.0
0.9
0.7
Cadmium
Arsenic
4.2
28
1.6
18
12
11
5
Introduction
The Great Tit (Parus major L.) is a
monogamous and resident species extending over
the whole of Europe (Cramp & Perrins 1993).
This implies that in my study area this species is
susceptible to pollution effect all year round
whereas the migrant, F. hypoleuca, is only
susceptible three months during the breeding
time. P. major starts laying in the beginning of
May. During breeding time P. major feed on a
variety of insects, especially Lepidoptera larvae.
Both sexes feed the nestlings.
F. hypoleuca and P. major are found in a
variety of forest habitats from luxuriant
deciduous woodlands and subalpine birch forest
to coniferous forest. Both species nest in tree
holes but also readily accept nest-boxes. The
breeding biology of these birds has been
intensively studied during the past 40 years
(Lundberg & Alatalo 1992, Cramp & Perrins
1993, Glutz von Blotzheim & Bauer 1993,
Gosler 1993). The numbers of breeding pairs in
the study area in 1991 - 1994 are shown in paper
VI, Table 1.
4. EFFECTS OF AIR POLLUTION
3
Especially in F. hypoleuca, the egg shell surface
was more rough and porous near the factory.
4.2. Nestling growth and mortality
Nestling growth, growth abnormalities, mortality
and breeding success were studied in 1991 - 1993
(II). Exposure of birds to heavy metals was
studied by fecal concentrations (Fig. 2). The
growth of F. hypoleuca nestlings was poorer and
they suffered higher mortality very close to the
factory complex, but did relatively well in all
other sites. Decreased nestling growth and
fledging success of P. major extended farther
from the factory than in F. hypoleuca. I suggest
that the strong response of F. hypoleuca is related
to the increased amount of heavy metals in diet
near the factory complex (Fig. 2), but synergistic
effects of a low amount of calcium in food are
also probable (chapter 5.2.). The response of P.
major is rather a consequence of habitat change,
that has taken place during the activity of the
factory complex. The main reason for the
different responses in these two bird species is
probably their different foraging habits (II, V).
ON BIRDS
4.1. Egg shell quality and hatchability
Egg shell thickness, egg volume, clutch-size and
hatching success were studied in 1991 - 1993 (I).
Unhatched eggs were collected for measuring
shell quality. In general, F. hypoleuca was more
susceptible to pollutants than P. major. Egg
shells of F. hypoleuca were about 17 % thinner
and eggs were about 8 % smaller in volume near
the factory than at a distance of 10 km. Clutchsize of F. hypoleuca was significantly smaller
and hatching success markedly reduced at a study
site next to the factory complex.
In P. major, variation in shell thickness or
egg volume was not significantly related to the
distance from the pollution source. Clutch-size
and hatching success of P. major did not
significantly differ among study sites, although
there was a similar tendency in hatching success
as in F. hypoleuca. Clutches of both species
contained less shell material and both species had
more eggless nests near the factory than further
away. The surface structure of the eggshells was
studied by scanning electron microscope.
Figure 2. Copper concentration (dry weight, d.w.) in
faeces of F. hypoleuca (a) and P. major (b) nestlings in
different distances from the factory (sampling and
analyses described in paper II).
4
Introduction
Although the emissions have decreased during
the course of this study (Table 1), neither the
clutch-size nor breeding success have essentially
improved in polluted area in either species (Figs.
3 and 4).
4.3. Growth abnormalities
Nestlings were checked for any visible
abnormalities in their bodies. The most common
aberrations were defectively developed tibiotarsi
and tarsometatarsi (II). This was evident from the
weak, soft and bent legs of chicks. In some cases,
corresponding abnormalities were also observed
in wings.
Defectively developed legs occurred in F.
hypoleuca nestlings significantly more often near
the factory than farther away. At the most heavily
polluted site, about 27 % of the broods contained
one 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 in
1991 - 1994. Destroyed, second and replacement clutches
omitted. Bars denote standard error.
limbs (II). In many cases these nestlings died.
Although the crippled nestlings sometimes
reached fledging size, they were probably too
weak to leave the nest cavity. In P. major no
corresponding defects were noted. The observed
abnormalities in bone structure of F. hypoleuca
nestlings are likely to arise from the same reason
as abnormal egg-shells, i.e. from the impairing
effect of dietary heavy metals on Ca-metabolism.
4.4. Survival and recruitment
The local survival and recruitment of F. hypoleuca and P. major females were studied with
capture-recapture data from 1991 - 1995 (VI).
The local survival of F. hypoleuca females tended to be reduced near the pollution source, being
7% compared to 23% in most distant areas, but
this 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 pollution
source in 1991 - 1994. Destroyed, second and replacement
clutches omitted. Bars denote standard errors.
5
Introduction
area, but slightly higher survival probabilities
occurred in moderately polluted area than
elsewhere. The slightly higher survival
probability in moderately polluted area may be
related to the availability of ample invertebrate
food for P. major (V). The fact that local survival
of migratory F. hypoleuca, but not of resident P.
major, was decreased in polluted area
emphasizes the importance of diet in determining
the response of a bird to the pollutants. In winter,
the vicinity of the town probably compensates for
the possible detrimental effects of pollution via
an increased amount of winter food and reduced
predation pressure (VI). Differences in
recruitment rates of young birds could not be
confirmed because of the low number of recruits
in both species (VI).
5. MECHANISMS OF AIR POLLUTION
EFFECTS ON BIRDS
5.1. Heavy metals
Exposure of birds to heavy metals was studied by
measuring concentrations in nestling faeces and
in one of their food items, red ants (Formica
rufa) sampled from hills (II). The concentrations
in faeces reflected well the heavy metal gradient
measured in soil, rain water and leaf samples
from the same area (Sippola & Erviö 1986, Fritze
et al. 1989, Jussila & Jormalainen 1991, Koricheva & Haukioja 1992). The gradient in faeces
concentrations was relatively steep for copper,
nickel and lead (II). A less steep gradient was
observed for cadmium and zinc. The same
applies to the concentrations in ants (II). A
summary of components potentially involved in
egg shell and bone abnormalities in Harjavalta is
presented in figure 5.
In general, F. hypoleuca received more heavy
metals in its food than P. major (II). The
difference between species is probably due to
their different diet. In my study area F. hypoleuca
takes about half of its food items from the ground
and air, whereas P. major forages almost
exclusively in tree foliage during the nestling
period (V). Heavy metals probably accumulate
more 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 (see
Hunter & Johnson 1982, Bengtsson & Rundgren
1984, Grue et al. 1986). Food selection is thus of
primary importance in the susceptibility of birds
to heavy metals.
5.2. Calcium deficiency
5.2.1. Natural availability of calcium
In Harjavalta, the amount of exchangeable
calcium in the humus layer is relatively low,
which may partly be explained by natural soil
differences (Jussila et al. 1991). On the other
hand, the amount of Ca in pine needles is
relatively high near the factory complex
(Heliövaara and Väisänen 1989, Jussila &
Jormalainen 1991). This is probably because the
factory complex also emits calcium-rich fertilizer
dust, with a pH varying from 5 to 7.5
(Laaksovirta and Silvola 1975).
The different Ca-gradients in soil and needles
are probably reflected in nestling faeces
concentrations of P. major and F. hypoleuca (II)
via their different foraging behaviour (V). This
may be the reason for the relatively high amount
of Ca in the faeces of P. major nestlings
compared to those of F. hypoleuca at the study
site next to the factory in both study years (I).
Fallen snail shells were frequently found from the
nests of F. hypoleuca in Harjavalta, but there
were almost none in the site closest to the factory
(II). This may stress the importance of certain
Ca-rich food items which are absent from the
most polluted site (see Graveland et al. 1994).
The reduced amount of Ca in the diet probably
makes birds more susceptible to the detrimental
effects of heavy metals (see Six & Goyer 1970).
5.2.2. Calcium manipulation experiment
In summer 1994 I made an experiment in which
calcium carbonate (CaCO3) was artificially added
to 12 territories of F. hypoleuca. Another 12
territories were used as controls. The study was
performed at the site 0.7 km south of the factory
complex. Commercial crushed calcium carbonate
was provided at the time of nest building on the
roof of the nest-box, on the feeder at the ent
6
Introduction
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 and
some 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 calcium
was followed by video cameras (Table 2).
Surprisingly, males ate the calcium pieces more
frequently than females (Table 2). I do not
know the reason for such behaviour but to
ensure that nestlings got their proportions I
daily fed pieces of calcium with tweezers to the
nestlings over 4 days old.
Control and treatment nests were selected
according to randomized four block design to
ensure even spatial distribution of treated nests.
Four blocks were arranged so that they were
equally far from the factory complex. Inside the
blocks, treated and untreated nests were
selected in turn according to the arrival date of
females. This ensured similar temporal
distribution of experimental nests.The
experiment involved two parts. In the first part
I followed the egg characteristics, laying order,
clutch-size and hatching success. In the second
part I studied the growth and developmental
abnormalities of nestlings. Original hatchlings
were removed from the nests at day 0 and new
broods were created by bringing nestlings from
background sites, 10 km from the factory
complex. The new broods of five young were
mixed as regards the origin of nestlings, so that
every brood contained nestlings from three
donor nests. By mixing nestlings I wanted to
avoid genetic effects on growth and
development.
Egg length and breadth were measured on
daily visits. Females were captured after they
had incubated 9 days and again when the
nestlings were 10 days old. Females were
ringed, weighed and their wing length was
measured. Nestlings were weighed and wing
length was measured on days 1, 5 and 10. Each
time nestlings were checked for visible
abnormalities in their legs and wings.
There were no differences in female wing
length (ANOVA, F1,16, P= 0.64), weight at
incubation 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
7
Introduction
differences between groups cannot be
explained by different female quality.
There were no significant differences in egg
size characteristics between treatment and
control groups (Table 3). Although not
significantly, the mean egg volume was about
5% smaller in control nests. Nests with extra
calcium had a one egg larger average clutchsize and 9% better hatching success, but the
differences were not significant (Table 3). No
difference was found in nestling mass between
groups, but their wings seemed to grow more
rapidly in treated nests (Table 3). Mortality was
low in both groups in the beginning of the
nestling period, but at the age of 10 days,
treated nests had, on average, one nestling more
than control nests (Table 3). The extra calcium
most clearly affected the development of
nestling legs. Most of the control broods had
one or more nestlings with defectively
developed legs, whereas in treated nests no
defects were noted (Table 3).
different kind of assortment along the pollution
gradient. Females were of the same size in all
areas. At nestling time, P. major females were
heaviest in the moderately polluted area, but
they were not lighter in polluted area than in
background area.
In both species the female fat reserves were
smaller in polluted area during the cold
breeding season. This emphasizes the effect of
simultaneous stress factors on the female
condition. In the beginning of the study the
proportion of young F. hypoleuca females was
slightly higher in polluted area than elsewhere
but after two years it was the same everywhere.
F. hypoleuca females started laying later,
whereas P. major females laid earlier in
polluted area, but the strength of these effects
also depended on the year. The clearest
difference among distance zones was found in
breeding density. Both species bred more
sparsely in polluted area. I conclude that
females preferred to breed in unpolluted areas,
but differed only marginally in their size and
condition between polluted and unpolluted
habitats.
5.3. The quality of females
Reduced breeding success might result in a
polluted area if, in spring the birds assortatively
settled in areas of different degrees of
pollution. Body size, fat reserves, age
distribution, timing of breeding and breeding
density of females were measured in 1991 1994 (III). I found only few such differences in
female quality which could be caused by a
5.4. Food abundance
Invertebrate abundance was measured along the
pollution gradient in 1992 to study whether the
reduced breeding performance of birds was
caused by pollution-induced alterations in their
food supply (V). At the nestling time of both
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
Stage
female
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
93.6
50
0.53
10
0.10
G
8
Introduction
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 were
formed 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
86.2
6.37
9
79.2
8.42
9
0.373
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
3
16.1
0.61
8
14.2
0.66
7
0.036
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
7
75
8
0.008
Hatching success (%)2
Weight (g), 5 days3
Wing (mm), 5 days
Wing (mm), 10 days3
Leg abnormalities (%)4
1
2
3
4
0
One-way ANOVA, egg volume was calculated using the equation of Ojanen et al. (1978).
Kruskall-Wallis test, only those nests where incubation started were used in calculating clutch size.
Suddenly destroyed nests were omitted when calculating brood size.
ANCOVA, day 1 values were used as covariates, least squares means.
Percentages denote the proportions of broods. Chi-square test.
species, larvae were scarce in Scots pine ) the
dominant species among the trees ) close to the
factory complex, peaked at the moderately
polluted zone, 2 - 4 km from the factory, and
tended to decrease further away. Both bird
species preferred pine, particularly in the
moderately polluted zone, where also the
proportion of larvae in the diet of P. major was
high. Ground-living arthropods were scarce
close to the factory, but among-site variation
was high even in the cleanest area.
The breeding success of both bird species
correlated positively with prey abundance, but
only in P. major did the lack of food retard
nestling growth. Also the productivity of
different sized clutches was affected in P.
major but not in F. hypoleuca. Large F.
hypoleuca clutches produced more fledglings
than smaller clutches at all parts of the
pollution gradient, while this was true for P.
major in the moderately or slightly polluted
parts of the gradient only; in the most polluted
areas clutches comprising 6 to 11 eggs
invariably produced 3 to 4 fledglings. The
stronger impact of food abundance on P. major
probably results from the different diet in two
bird species. P. major, a caterpillar specialist,
suffered from the shortage of larvae in the late
nestling period.
9
Introduction
5.5. Ectoparasites
Ectoparasites are one of the stress factors
encountered by a reproducing bird. To study
the simultaneous effects of ectoparasites and
pollution stress I counted the numbers of larvae
of an ectoparasitic fly, Protocalliphora azurea
(Diptera: Calliphoridae), an adult and larval
Hen fl ea, C er a t o p h y l l u s g a l l i n ae
(Siphonaptera: Ceratophyllidae) and other nest
dwellers from the nests in 1991 and 1992 (IV).
Protocalliphora larvae were more frequently
found in the nests of P. major than in the nests
of F. hypoleuca. The prevalence of
Protocalliphora larvae tended to be smaller in
polluted areas. The number of larvae correlated
positively with the nest size and brood size of
P. major, which may be the result of
difficulties of sanitation in large and crowded
nests.
Nests of F. hypoleuca contained more adult
fleas in polluted areas than in control areas.
This observation supports the idea that
pollution-induced stress makes birds more
susceptible to harm from natural stresses.
Protocalliphora larvae retarded the growth of
P. major nestlings and fleas increased the
nestling mortality of F. hypoleuca, but these
effects were not enhanced by air pollution. I
conclude that the ectoparasites studied, at the
densities observed in our study area, were of
minor importance in determining the breeding
success of these two bird species.
6. CONCLUSIONS
The consequences of air pollution were
different for the two bird species. F. hypoleuca
directly responded to the steep pollution
gradient (1 - 2 km from the pollution source)
and was affected most severely at the egg stage.
The response of P. major extended farther from
the factory complex (up to 3 - 4 km) and was
more obvious at the nestling stage, when the
nestling mortality was increased near the
pollution source.
The results indicate that the reduced
breeding performance of birds in the polluted
area may have various causes: one species may
respond directly to toxicity while the other to
reduced food supply. The strong and steep
response of F. hypoleuca is related to the high
amount of heavy metals in its diet, and this
effect is enhanced by the lack of calcium-rich
food. The decreased amount of invertebrate
food in the polluted area was the main reason
for lowered nestling production in P. major.
The different responses of the two bird species
are related to their different foraging habits.
Due to low fledgling production and decreased
local survival, the most polluted area around
the factory complex is probably a sink area for
the F. hypoleuca population, with continuous
immigration from outside. In P. major, the
survival probability of breeding females did not
differ between polluted and unpolluted areas.
This contrasts with the intuitive idea that
resident species, being exposed to impacts of
pollution all year round, would be more
severely affected than a migrant species which
only arrives to breed in polluted area.
Although anthropogenic, air pollution is
one stress factor among others, and it may have
evolutionary effects similar to more natural
factors. This study demonstrated a reduction in
the optimal clutch size of P. major in polluted
area, whereas in F. hypoleuca such an effect
was not noted. However, adaptations to
pollution or its secondary effects are unlikely
because the impact area is small compared to
the dispersal capacity of birds and the
surrounding gene pool.
Both species can be considered suitable
biomonitors, but they are sensitive to different
factors. A partial ground forager, F. hypoleuca,
is more susceptible to receiving aerially
deposited heavy metals from the environment
than the foliage forager, P. major. Instead, P.
major is probably a more sensitive indicator of
secondary environmental changes than F.
hypoleuca. Species-specific differences in
responses should be carefully considered when
planning projects for air pollution monitoring.
ACKNOWLEDGEMENTS
First but not least I wish to thank my
supervisor, Prof. Esa Lehikoinen, who has
suprisingly many characteristics of a good
supervisor. Esa never hesitated to introduce
new ideas and methods, and sometimes even
succeeded in getting me involved in them. I
10
Introduction
also wish to thank Prof. Erkki Haukioja, who
many times encouraged me in the course of this
study and, somehow, even seemed to believe in
it.
I am also most grateful to Jorma Nurmi, the
most efficient field assistant of the northern
hemisphere. Without his enthusiastic attitude
and enormous contribution in data collection
this study would have been only a reflection of
a study. Simo Veistola, besides helping with
the field work, was invaluable in criticizing my
manuscripts. Luckily, he always understood the
main ideas in them much better than I did.
Several other people took part in the data
collection. Tuija Pohjalainen was responsible
for the invertebrate sampling and dived deeply
into the fascinating world of coprology. Carita
Sunell and Erja Sarholm were fast enough to
follow the birds in order to reveal their foraging
habits. Tapio Aalto, Jari Valkama, Julia
Bojarinova, Petteri Ilmonen, Juha Niemi and
Tapani Lilja helped me in catching the birds
who did not always understand that the work
was done for their good. People in Harjavalta
and surroundings helped me by sending
information on ringed birds.
Many times, people in the Laboratory of
Ecology in Turku University and people in the
Satakunta Environmental Research Center
helped me in the course of the study.
Jürgen Wiehn, Jan-Åke Nilsson and Juha
Tiainen made valuable comments on the earlier
version of this thesis. Jacqueline Välimäki
kindly checked the language.
I also want to thank my wife, Elina, for her
patience in many situations. Thank you (!).
This study was financed by the Academy of
Finland.
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