Local survival of pied flycatcher males and females in a pollution gradient of a
T. Eevaa,*, H. Hakkarainena, E. Belskiib
aSection of Ecology, University of Turku, FI-20014 Turku, Finland
bInstitute of Plant and Animal Ecology, Russian Acad. Sci., 8th March street, 202, Ekaterinburg 620144, Russia
Female pied flycatchers (Ficedula hypoleuca) show decreased local survival around a copper smelter.
a r t i c l e i n f o
Received 20 October 2008
Received in revised form
19 January 2009
Accepted 23 January 2009
a b s t r a c t
Survival is one of the most central population measures when the effects of the pollution are studied in
natural bird populations. However, only few studies have actually measured rigorous survival estimates
on adult birds. In recent years there has been a methodological advance in survival analyses by mark-
recapture models. We modelled local survival (including mortality and emigration) with the program
MARK in a population of a small insectivorous passerine bird, the pied flycatcher (Ficedula hypoleuca),
around a point source of heavy metals. The local survival of females in the polluted area was about 50%
lower than in the other areas. Males, however, survived relatively well in the heavily polluted area, but
showed somewhat lower survival in the moderately polluted area. Different pollution effects between
two sexes might be due to pollution-related differences in reproductive effort in females and males, and/
or more intensive uptake of heavy metals by laying females.
? 2009 Elsevier Ltd. All rights reserved.
Point sources of heavy metals, such as non-ferrous smelters, are
known to pose a serious hazard for local breeding bird populations.
Decreased breeding success of insectivorous passerines has been
demonstrated at several smelter sites (Belskii et al., 1995a, 2005;
Eeva and Lehikoinen, 1996, 2000; Janssens et al., 2003). Typically
such studies report decreased clutch size, hatchling and nestling
numbers and nestling survival, though the effects depend on study
species and pollution load. Several studies have also shown
decreased population densities and species richness of forest birds
around smelter sites (Gilyazov,1993; Kristı ´n and Zilinec,1997; Eeva
et al., 2002; Belskii and Lyakhov, 2003). Heavy loads of sulphuric
oxides and heavy metals have been shown to cause secondary
effects on birds via changed food chains, such as decreased abun-
dance of invertebrate food and limited Ca availability (Eeva et al.,
1997, 2005; Eeva and Lehikoinen, 2004). Nestling stage is generally
supposed to be the phase most affected by environmental stresses
like pollution (Hoffman, 1995). It is also the phase most easily
studied in birds, and, in migratory birds, the phase which is easiest
to couple with certain environment. There is, however, much less
information on pollution effects on survival of adult birds. This is
partly due to the lack of long-term population data from polluted
areas, but also due to problems to analyse long-term data sets with
yearly variation in recapture rates.
In recent years there has been a methodological advance in
analyses of adult survival by mark-recapture models that take into
account the variation in recapture probabilities. By using such
models in MARK software (White and Burnham, 1999) we
modelled local survival (including mortality and emigration) of
a small migratory insectivorous passerine bird, the pied flycatcher
(Ficedula hypoleuca), around a Russian Cu smelter, a point source
of heavy metals (Vorobeytchik et al., 1994). A few recent studies
have suggested important effects of air pollution on the local
survival of this species. F. hypoleuca females showed decreased
local survival in a study around a Finnish Cu smelter, but there was
no effect on another hole-breeding insectivore, the great tit (Parus
major) (Eeva and Lehikoinen, 1998). Another study suggested that
F. hypoleuca males showed, unexpectedly, increased local survival
in a heavy metal polluted area, as compared to females in the
polluted area or males in the unpolluted area (Eeva et al., 2006b).
Long-term mark-recapture data collected around the Russian
smelter gives a good opportunity to compare survival between the
smelter sites, especially because heavy metal emission levels in
the Russian study area are much higher than in any of the earlier
* Corresponding author.
E-mail address: firstname.lastname@example.org (T. Eeva).
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Environmental Pollution 157 (2009) 1857–1861
2. Materials and methods
2.1. Study area and data collection
The data was collected during 1996–2007 in a pollution gradient of the Middle
Ural copper smelter (56?510N, 59?530E) in Revda, Russia. Heavy metals (mainly Cu,
Pb, Zn and Cd) and sulphuric oxides are the main pollutants of this large chemical
metallurgy complex. The total emissions have decreased from 140,700 tons/year in
1989 to 95,700 tons/year in 1996 and 24,507 tons/year in 2007 (Vorobeytchik et al.,
1994; Podust, 1997; Pakhalchak, 2008). High emission of dust causes considerable
emission of heavy metals, especially lead, to surrounding forests. Study sites with
nest boxes were located in three zones around the smelter: I heavily polluted zone
(5 sites 1–2 km from the smelter), II moderately polluted zone (5 sites 4–8 km from
the smelter) and III unpolluted zone (3 sites 16–27 km from the smelter). Forest
stands in the vicinity of the smelterare sparserand contain moredead trees than the
more distant sites. A more detailed description of habitat types is given by Belskii
and Lyakhov (2003). A long-term pollution by metallic dust combined with sulphur
dioxide has increased soil acidity and metal concentrations in the upper soil layer.
Forexample, soil Cu concentrations decrease fromzone I tozone III from 3770 to862
to 87 mg/g dw, respectively (Belskii et al., 2005). Fledging success of F. hypoleuca is
clearly decreased in the polluted area. During 1989–1993 the average number of
fledglings was 2.0 (zone I), 4.6 (zone II) and 5.3 (zone III) while in 2000–2001 the
figures were 2.8, 5.5 and 5.5 chicks, respectively (Belskii et al., 1995a, 2005).
Nest boxes were regularly checked to record the numbers of eggs, nestlings and
fledglings. About 80–100% of breeding females and 30–90% of breeding males were
yearly captured and marked with an aluminium ring. Adult birds were aged (1 year
vs. ?2 years) according to Karlsson et al. (1986), measured for their wing length
(a measure of body size) and colour morph of males was scored according to the
Drost’s scale (Drost,1936), scoresvarying in this population from3 (dark) to7 (grey).
2.2. Survival models
Survival analyses were performed using mark-recapture histories of 589 males
and 815 females that recruited to the breeding population in 1996–2007. For
modelling we used program MARK that enables separate estimation of survival and
recapture rates (White and Burnham, 1999) based on the capture histories of
a sample of marked individuals. Survival rate (S) describes the local survival of
individuals, including emigration. Recapture rate (P), in turn, decreases with the
number of individuals missed in the trapping process, and is taken into account
when modelling estimates for S. To prevent a possible bias in recapture probabilities
due to varying spatial distribution of study sites among distance zones, we omitted
from all the analyses those 18 individuals (1.3% of all) that changed the study plot
during the study period.
In both sexes, we first analyzed all 25 model combinations inwhich survival and
recapture probability were allowed to vary or to be constant with respect to time (t)
and/or to pollution zone (g). The individual models were ranked on the basis of
Akaike’s information criterion (AICc) to determine which models most parsimoni-
ously fit the data (Akaike, 1973; Hurvich and Tsai, 1995; Burnham and Anderson,
1998). The model with the lowest AICc score was considered to be the best model,
but any models that had AICc scores within two points of the best model were
considered to be competitive with the best model (Burnham and Anderson, 1998;
Cooch and White, 1999). The fit of our data to a general model, i.e. the model con-
taining all the interactions (S(g * t)P(g * t)) was explored with contingency table tests
in program RELEASE (tests T2 and T3) (see Burnham et al., 1987).
Finally, we examined whether parental quality in terms of age, wing length and
plumage colour (males only) or breeding success influenced the survival parame-
ters. All these parameters are known to depend on pollution level on the basis of
earlier studies in the area (Belskii et al., 1995a; Belskii and Lyakhov, 2004). For this
purpose, design matrix was modified byadding separatelyone of the variables tothe
most highly ranked model. Note that in program MARK only individual covariates
are allowed and therefore we used mean values of an individual as individual
covariates, except for age, where age at the first encounter was used as a covariate.
The values of covariates were not available for all the individuals and the sample
sizes in these analyses are consequently somewhat smaller than in the basic models.
All the covariates were further tested for their differences among pollution zones
with mixed linear models (SAS procedures GLIMMIX for age and MIXED for fledgling
number, wing length and plumage colour) by using year as a random factor. Binary
error distribution was used for modelling age distribution and normal error distri-
bution for the other variables. Tukey’s test was used to explore pairwise differences
among the zones.
3.1. Goodness of fit analyses
There was no overdispersion in the data, because the fit of our
general model (S(g * t)P(g * t)) to the data was adequate: for females
RELEASE test T2 (c2¼5.23, df¼11, p¼0.92), and test T3 (c2¼23.2,
df¼36, p¼0.95). The data was adequate also for males: test T2
(c2¼4.09, df¼11, p¼0.97), and test T3 (c2¼17.7, df¼35, p¼0.99)
(see Burnham et al., 1987).
3.2. Survival models
In females the best fit model (S(g)P(g þ t)) included the zone
effect (g) for both survival and recapture rate (Table 1). The best
model also allowed recapture rate to vary annually (t) across the
three distance zones (Table 1). The estimates from the best fit
model showed that survival of females in the polluted zone I was
about 50% lower than in the zones II and III (Fig. 1). On the basis of
earlier studies it was known that fledgling numbers are lowclose to
the Cu smelter (Belskii et al., 1995a, 2005). Fledgling number as
a covariate further increased the fit of the model (LR-test between
the nested models S(g þ fledglings)P(g þ t)vs. S(g)P(g þ t): c2¼5.36,
df¼1, p¼0.021; DAICc¼3.28), because survival probability
increased with the fledgling number (b¼0.24, SE¼0.10). The
model including wing length as a covariate was not highly ranked,
suggesting that female’s survival probability was independent on
its body size. The model including female age did not differ
significantly from the most highly ranked model (LR-test S(g)P(gþt)
vs. S(g þ age)P(g þ t): c2¼0.28, df¼1, p¼0.59; DAICc¼1.79), sug-
gesting that old females show a slightly higher (1.4%) local survival
probability (b¼0.091, SE¼0.17). However, the majority of the
variation in local survival among zones cannot be explained by age
In males the best fit model (S(g þ t)P) showed that survival varied
between the three different pollution zones and annually, whereas
recapture rate was constant over time and space (Table 1). Males
showed about 26% lower survival estimates in the moderately
polluted zone II than in two other zones (Fig. 1). Fledgling number
as a covariate did not increase the fit of the survival model of males.
Furthermore, the models including wing length or plumage colour
as a covariate were not highly ranked, suggesting that male’s
survival did not depend on its body size or colour morph. The
model including male age did not significantly differ from the most
highly ranked model (LR-test S(g þ t)P vs. S(g þ age þ t)P: c2¼0.18,
df¼1, p¼0.67; DAICc¼1.91), suggesting that young males show
a slightly (1.7%) higher local survival (b¼?0.083, SE¼0.20).
Therefore, the majority of the variation in local survival among
zones cannot be explained by age effect in males either.
The fledgling numbers of marked birds were 30–40% lower in
the most polluted zone I than in the other zones in data sets of both
sexes, while the difference was not significant between zones II and
III (Table 2). A larger proportion of breeding birds wereyoung in the
The most parsimonious survival models for females and males (S denotes survival, P
denotes recapture probability), including model deviance, number of parameters
(np) and Akaike’s information criterion (AICc¼devianceþ2np) and the difference
in AICc compared to the most highly ranked model (DAICc). The letter t indicates
time (i.e. annual variation) and g the zone-dependence (i.e. polluted, moderately
polluted and unpolluted zone). The models in boldface, with lowest AICc, were used
for interpretation of results.
DAICc AICc weight
S(g)P(g D t)
S(g D t)P
T. Eeva et al. / Environmental Pollution 157 (2009) 1857–1861 1858
most polluted zone than in the two other zones for both sexes
(Table 2). Both females and males were also smaller (shorter
winged) in the zone I than in zones II and III (Table 2). Furthermore,
males werelightercoloured in the zone I (median score¼6) than in
the other zones (median score ¼5 for both zones; Table 2). A great
deal of the differences in wing length and male colour is explained
by age. When age was added in the models the zone effect was still
significant for female wing length (F2,781¼4.4, p¼0.012) and male
wing length (F2,572¼5.4, p¼0.0047), but not for male colour
(F2,558¼2.2, p¼0.11). The fledgling number of young females was
0.5 fledglings smaller than that of old females (F1,688¼17.3,
p<0.0001), but zone effect still remained strong (F2,695¼96.8,
p<0.0001) after including age into the model. Male age did not
significantly explain the fledgling number (F1,527¼0.23, p¼0.63).
The local survival of F. hypoleuca females was decreased in the
heavily polluted area around the Revda Cu smelter while males
seemed to survive relatively well in the polluted area. The differ-
ences in fledging production, age, bodysize or male plumage colour
could not explain the differences in survival among the pollution
zones. In Revda, heavy metal emissions were very high during the
study period. For example, Revda smelter emitted 170 tons of lead
in 2002 (Lassen et al., 2005). High emission levels in Revda are
likely to explain the stronger negative effect on female survival as
compared to earlier studies (Eeva and Lehikoinen,1998; Eeva et al.,
2006b). The negative effect on survival may be due to direct toxic
effects of heavy metals (Eeva and Lehikoinen, 2004), or indirect
effects, e.g. via changes in food availability (Eeva et al., 1997) or
population structure (Eeva et al., 2006a). High emission levels are
also reflected in relatively poor breeding success in the polluted
sites near the Revda smelter (Belskii et al., 1995a,b, 2005; Bezel
et al., 1998). For example, the average fledgling number in the
whole population of the polluted area in Revda was 2.8 in 2000–
2001, while the corresponding figure was 5.5 in the unpolluted area
(Belskii et al., 2005). In our data set the number of fledglings was
somewhat higher (see Table 2) because parents of the most
unsuccessful nests (i.e. those that fail at early phases of breeding)
may remain untrapped more often than those of more successful
The local survival probability (?SE) of F. hypoleuca males was
relatively high (34% ?6.2) in the polluted area of Revda. Surpris-
ingly, male survival was somewhat lower in the moderately
polluted zone II than in the most distant zone III. A possible reason
to this might be a relativelyhighoccupation rate (71%) of nest boxes
in two study sites in the zone II, which likely indicates increased
competition for nest holes among males. High competition might
lead to decreased local survival probability among males. Male age
distribution, size, colour morph or fledgling production in zone II
were not different from the zone III (Table 2). High female survival
and fledging success further suggest that food resources should be
relatively good in the zone II.
Studies on the effects of air pollution on survival of adult birds
are scarce. Local survival of F. hypoleuca has been studied around an
another Cu smelter in Harjavalta, Finland (Eeva and Lehikoinen,
1998; Eeva et al., 2006b). In the beginning of 1990s local survival of
females was decreased in this heavy metal polluted area, but along
with stronglyreduced emissions
approached the level of an unpolluted control area towards the end
of 1990s. For example, particulate yearly lead emissions from Har-
javalta smelter have decreased from 50 tons in 1991 to 0.4 tons in
2002.Simultaneously, heavy metalresiduesin birds have decreased
and fledgling numbers have increased (Eeva and Lehikoinen, 2000).
Like in Revda, males survived well (42% ?4.0) in the polluted area
around the Harjavalta smelter (Eeva et al., 2006b). Studies at both
locations suggest that the effect of pollution on local survival is sex-
dependent, females being affected more severely by heavy metal
The reasons for sex-dependent pollution effects are unknown,
but we suggest here some ideas for further studies. In F. hypoleuca,
female alone is responsible for nest-building, egg production,
incubation and brooding, which apparently cause reproductive
costs (e.g. Ilmonen et al., 2002). Therefore, females might be more
susceptible to negative health effects of pollution stress due totheir
the female survivalhas
I II III
Fig. 1. Survival probabilities (?95% confidence limits) of F. hypoleuca females (grey
bars; estimates derived from the model S(g)P(g þ t)) and males (white bars, estimates
derived from the model S(g)P) at three distance zones from the Cu smelter.
The average number of fledglings, proportions of young (1 yr) breeding females and males, average wing length and average colour morph of males according to Drost’s scale
(smaller value means darker) in three distance zones around the Cu smelter. Tukey’s test for pairwise differences: means with the same letter are not significantly different.
n Zone I Zone II Zone IIIdfFp
Fledgling number (for females)a
Fledgling number (for males)a
Proportion of young females (%)b
Proportion of young males (%)b
Female wing length (mm)a
Male wing length (mm)a
Male colour morph in Drost’s scalea
aA mixed linear model with normal error distribution and year as a random factor.
bA mixed linear model with binary error distribution and year as a random factor. Note that these covariate values refer to the age at the first encounter. The figures in
parentheses give real proportions of young birds in the whole data set (n\\¼990; n__¼733).
T. Eeva et al. / Environmental Pollution 157 (2009) 1857–1861 1859
higher reproductive effort as compared to males. Furthermore,
many males in the impact zone were observed to became passive
(did not take part in feeding nestlings) towards the end of nesting
period and sometimes they disappeared before nestlings fledged.
The proportion of nests without a male during the nestling period
was almost three times higher in the heavily polluted area than in
the unpolluted area (Zone I: 20.3%; Zone II: 14.1%; Zone III: 7.5%;
E. Belskii, unpublished data). Therefore, males might partly avoid
the pollution stress by withdrawing the breeding, and would thus
further increase females’ load at polluted breeding sites where also
food resources may be limited. Furthermore, during egg laying
females need to collect high amount of calcium-rich food for egg
shell formation (Eeva and Lehikoinen, 2004). Together with Ca they
are likely to accumulate heavy metals, especially lead (Goyer,1997).
More intensive accumulation of heavy metals to breeding females
would mean that detrimental effects would first manifest in this
sex. Snoeijs et al. (2005) showed further that lead exposure
impaired antibody production in non-breeding female zebra
finches (Taeniopygia guttata) while such an effect was not found in
The differences in local survival probabilities might also reflect
different population age structure and/or breeding dispersal. In
Revda population, proportions of young females and males were
higher in the heavily polluted than in moderately polluted or
unpolluted zones. Such a difference could be produced by non-
random settlement of young and old individuals to polluted and
unpolluted environments (Eeva et al., 2006a). Generally, F. hypo-
leuca males are clearly more site tenacious than females and older
birds of both sexes are supposed to move shorter distances
between years than young birds (Lundberg and Alatalo, 1992).
A high tendency of young females to disperse to less polluted areas
(e.g. as a response to low breeding success) would produce similar
survival pattern as we observed. However, although age seemed to
explain some of the variation in survival probabilities in both sexes,
adding age to the survival models did not remove a much stronger
effect of distance zone. Alternatively, poor breeding success could
increase breeding dispersal of females independent of age. In
accordance with this, we found a positive association between the
local survival of females and their fledgling production, while such
an effect was not observed in males. Studies in Harjavalta, however,
suggest that in F. hypoleuca less productive individuals in bothsexes
tend to disperse as far as well producing individuals (Eeva et al.,
2008), independently of pollution levels. Much higher pollution
levels in Revda might, however, produce a stronger success-related
effect on female dispersal. A need to disperse from a breeding area
mayalso be associated with other factorsthan fledgling production,
e.g. with the degree of physiological stress and/or pollution-related
The Revda and Harjavalta populations also seem to differ in their
local female survival even between the unpolluted sites, survival
probabilities in Harjavalta (21% ?5.2) being generally much lower
than those in Revda (36% ?2.8). We don’t know the reason for this
inter-population variation, but for example different breeding
dispersal distances in two populations could produce such a differ-
but our models correct survival estimates by the variation in recap-
ture probabilities. The between-site differences in survival were
smaller in males but to the same direction (Harjavalta: 31% ?3.9;
Revda 38% ?2.6).
The local survival of F. hypoleuca females is decreased in the
heavily polluted area around the Revda Cu smelter while males
seem to survive relatively well in the polluted area. The observed
differences in fledging production, age distribution, body size and
male plumage colour could not explain the differences in survival
among the pollution zones. Possible explanations for decreased
local survival of females in the polluted area could be pollution-
related differences in reproductive effort between females and
males and/or more intensive accumulation of heavy metals to
breeding females. However, further studies are needed to confirm
the mechanisms leading to this kind of pollution-related sex-
specific local survival.
This study was financed by the Russian Foundation for Basic
Research (project 08-04-91766-AF), grant of President of Russia for
support scientific schools (NS-1022.2008.4) and the Academy of
Finland (project 8119367).
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