Download The importance of hunting pressure, habitat preference and life

Eur J Wildl Res
DOI 10.1007/s10344-012-0673-8
ORIGINAL PAPER
The importance of hunting pressure, habitat preference
and life history for population trends of breeding waterbirds
in Finland
Hannu Pöysä & Jukka Rintala & Aleksi Lehikoinen &
Risto A. Väisänen
Received: 21 May 2012 / Revised: 18 September 2012 / Accepted: 27 September 2012
# Springer-Verlag Berlin Heidelberg 2012
Abstract Populations of migratory species have undergone
dramatic changes in recent decades, but little is known about
the factors actually driving those changes. Of particular
concern are quarry species such as migratory ducks
(Anatidae), many of which have an unfavourable conservation status in Europe. By including both quarry and nonquarry species, as well as habitat preference and life history
characteristics of the species, we investigated the relative
importance of hunting pressure, both in Finland and at the
European level, in explaining population changes of 16
species of migratory waterbirds in Finland during 1986–
2011. Ban of lead shot in 1996 resulted in considerably
lower annual hunting bags in Finland thereafter. Species
which had the highest hunting pressure had the most negative slopes in population trends from 1986 up to 1997,
suggesting that hunting probably limited those populations.
However, in general population trends of the species were
not strongly associated with hunting pressure in Finland or
in Europe. Nor were basic life history characteristics (body
mass and clutch size) associated with population trends of
the species. In contrast, recent population declines were
Communicated by C. Gortázar
H. Pöysä (*)
Finnish Game and Fisheries Research Institute,
Joensuu Game and Fisheries Research,
Yliopistokatu 6,
FI-80100 Joensuu, Finland
e-mail: [email protected]
J. Rintala
Finnish Game and Fisheries Research Institute,
P.O. Box 2, FI-00791 Helsinki, Finland
A. Lehikoinen : R. A. Väisänen
Finnish Museum of Natural History, University of Helsinki,
P.O. Box 17, FI-00014 Helsinki, Finland
associated with habitat preferences of the species: those
breeding mainly in eutrophic lakes had more negative population trends than those breeding in oligotrophic lakes or
generalist species. Reasons for the relatively poor status of
species preferring eutrophic lakes probably include overeutrophication of nutrient-rich lakes, resulting in less abundant food resources, and increased nest depredation.
Keywords Body mass . Clutch size . Habitat preference .
Hunting impact . Migratory species . Waterbirds
Introduction
Population change in migratory species has been a focus of
considerable research during the last few decades. One
reason for the increased research activity is the notion that
climate change has negatively affected bird migration phenology and breeding performance, which in turn may have
contributed to long-term population declines of several species (reviews by Møller et al. 2010; Knudsen et al. 2011).
Populations of migrants breeding at northern latitudes have
been thought to be under particular threat because individuals that migrate longer distances have to cope with climate
change effects in geographically widely separated areas
during their annual cycle.
While climate change undoubtedly has affected population trends of some bird species, there are other anthropogenic factors that also influence population size, such as
hunting. At the extreme end of effects, hunting by prehistoric humans contributed significantly to the extinction of
several birds (e.g., Duncan et al. 2002), while more recently,
less extreme effects of hunting on bird abundance have been
reported frequently (e.g., Newton 1998). Considering all
European breeding birds, recent reports imply alarmingly
Eur J Wildl Res
high total hunting kills in relation to population size for
several species listed in Annex II (i.e., hunted species) of
the EU Birds Directive (Hirschfeld and Heyd 2005; Mooij
2005). Many of these heavily hunted species have an unfavourable conservation status at the European level (BirdLife
International 2004). In this context, it is particularly worrying how little we know about the role of hunting pressure in
driving population trends of quarry species in Europe (e.g.,
Elmberg et al. 2006; Devineau et al. 2010). For example,
many Anatidae (ducks and geese) are important quarry
species in Europe and elsewhere, yet apart from the
information-based management of waterfowl harvest in
North America (e.g., Nichols 1991; Nichols et al. 2007),
we are aware only of two quantitative analyses addressing
the impact of hunting on the status of Anatidae populations.
Green (1996) focused on globally threatened Anatidae species and concluded that hunting was an important determinant of the threat category of the species included in the
analysis. Long et al. (2007) studied 154 species of Anseriformes (Anatidae and screamers) and did not find hunting
to be an important factor influencing the population trends
of the species concerned. However, both of these analyses
were undertaken at a global scale and were based on a very
crude classification of hunting impact (a given species was
classified as hunted or not) without considering speciesspecific differences in harvest rate, i.e., how big a proportion
of the population was annually taken. However, estimation
of total hunting kill for quarry species at the European scale
is problematic (see Hirschfeld and Heyd 2005; Mooij 2005),
and we urgently need more robust analyses of hunting
impacts on Anatidae and other waterbird populations in
Europe.
In addition, some recent studies suggest that habitat type
may also play a role in population declines of migratory
species, but their results are divergent. The intensification of
agriculture has had negative effects on many farmland bird
species (Herzon et al. 2008, 2011), and this intensification
has also increased the eutrophication of wetlands in agricultural environments (Stoate et al. 2009). Sanderson et al. (2006)
analysed population trends of European breeding birds and
found that, in closely related pairs of species, negative trends
were more frequent in long-distance migrants than in shortdistance migrants or residents, irrespective of breeding habitat.
On the other hand, Both et al. (2010) showed that longdistance migrants breeding in seasonal temperate forests in
The Netherlands have declined more than long-distance
migrants breeding in less seasonal marshes, while no difference in population trends between habitats was found for
residents and short-distance migrants. Cormont et al. (2011)
also studied population trends of Dutch breeding birds and
showed that species breeding in the same habitat (forest or
marshland) may differ in terms of weather-correlated population dynamics depending on life-history traits.
Recent analyses of habitat dependence of bird population
trends have been based on rather crude habitat categories.
For example, in Sanderson et al.’s (2006) study, the category
‘inland wetland’ pools together species breeding in any type
of wetland (lakes, ponds, rivers, etc.). This approach certainly is useful for continent-wide analyses incorporating all
migratory species but it may mask important differences
between species specialized to different types of wetlands.
In his review of factors explaining an increase phase of the
breeding bird fauna in northern Europe, von Haartman
(1973) listed several examples of habitat specialists that
increased in eutrophic lakes only; the author mentioned that
the avifauna of oligotrophic lakes had suffered simultaneous
reductions in numbers. Because divergent trends may occur
even within same habitat type (e.g., eutrophic lakes), we
need to consider differences in species’ habitat specialisation when analysing population trends.
Here, we focus on the importance of hunting pressure and
habitat specialisation in explaining long-term (1986–2011)
trends in numbers of breeding waterbirds (i.e., ducks, divers,
grebes and common coot Fulica atra) in Finland. Standardized monitoring of the numbers of breeding waterbirds in
Finland started in 1986 (Koskimies and Väisänen 1991;
Pöysä et al. 1993, 2011). For six out of the 16 species
included in the present study, the estimated breeding numbers in Finland represent over half of the European breeding
population, as defined and reported by Hagemeijer and Blair
(1997), and for the other species the proportion of birds
breeding in Finland from the total European breeding population is also high (see Hagemeijer and Blair 1997). Hence,
the population trends based on the Finnish long-term monitoring data should have significance at the European level.
In addition, a considerable proportion of waterbirds harvested each year in Europe are shot in Finland (Hirschfeld
and Heyd 2005; Mooij 2005), meaning that changes in
waterbird harvest in Finland may bring about considerable
changes in overall hunting impact at the European level.
We will first describe population changes for 16 species
differing in hunting status and breeding habitat specialization. Then we study whether differences between the species’ long-term trends can be explained by differences in
hunting pressure and habitat specialization. The species
studied here include both protected (i.e., no legal hunting)
and quarry species. We use two approaches to assess the
impact of hunting. First, we estimate overall harvest rate,
both in Finland and at the European level, for each of the
quarry species. Using this information, and by also including protected species, we test if there is an association
between population trend and hunting pressure. Second,
the ban of lead shot in Finland in 1996 resulted in a considerable reduction in waterbird harvest. For example, the
mean annual total kill of waterbirds (ducks breeding in
inland waters and the common coot) decreased by about
Eur J Wildl Res
27 % from the period of 1990–1994 to the period of 1996–
2000, and has remained at a low level since 2000 (see
Materials and methods). This magnitude of permanent
change in harvest rate sets up a unique opportunity to study
the impact of hunting on duck populations. Hence, we test
the prediction that, assuming hunting mortality before 1996
has not been completely compensatory (a reasonable assumption, e.g., Smith and Reynolds 1992; Nichols 1991;
Pöysä et al. 2004) in Finland, populations of the quarry
species should show a more positive or less negative trend
after 1996 as compared with the trend before 1996, if
hunting is an important factor driving population trends of
the quarry species in Finland. Corresponding change in
trend should not occur in non-quarry species. Evidence from
North America suggests that duck populations respond rapidly to changes in harvest rate (e.g., Patterson 1979; Reynolds
and Sauer 1991). As life-history traits such as body size and
clutch size potentially are important components in determining species’ vulnerability to over exploitation and other types
of threat (e.g., Patterson 1979; Owens and Bennett 2000;
Olden et al. 2007), we also examine if long-term population
trends of waterbirds are associated with these life-history
traits.
Materials and methods
Fig. 1 Distribution of waterbird census sites totaled according to 20km uniform grid squares
Census data
The Finnish Game and Fisheries Research Institute (FGFRI,
in 1988–2011) and the Finnish Museum of Natural History
(FMNH, in 1986–2011) have coordinated monitoring of
breeding waterfowl numbers in Finland (Pöysä et al. 1993).
In our dataset, the total number of monitored sites is 3,431and
the annual mean number of sites containing pair estimates is
740. Point counts are the basic method used in pair surveys,
but round counts encircling wetlands are also used (methods
explained by Koskimies and Väisänen 1991). The censuses
are carried out in May (generally two visits per site to cover
both early and late nesting species). Spatial distribution of the
census sites is shown in Fig. 1.
Trend indices
The estimation of annual population change indices of the 16
species (see Table 1; common names are according to BirdLife International 2012) was based on log-linear modelling on
site-by-year count data (TRIM; Pannekoek and van Strien
2005) of breeding pairs in 1986–2011. TRIM bases on generalized linear models as the framework of the estimation of
model parameters (McCullagh and Nelder 1989), and it is a
commonly used tool in European bird monitoring schemes
(see www.ebcc.info). In the estimation of standard errors of
the slopes of index trends, over-dispersion in counts was
controlled for in order to reduce the risk of type I statistical
error (rejecting correct null hypothesis). All possible change
points were allowed in the description of the annual variations
in population change indices. Our main purpose was to compare index trends of the species estimated over the periods
1986–1997 and 1997–2011 (see below).
Estimation of hunting pressure
Estimates of species-specific hunting bags, especially at the
European level (see Hirschfeld and Heyd 2005; Mooij
2005), and population sizes are crude and sensitive to errors.
Therefore, instead of using actual harvest rate estimates, we
ranked the species in terms of harvest rate, separately at the
European and Finnish level, and used the ranks in the analyses
as explained below.
The most recent and comprehensive estimates of annual
bag size for ducks and other waterbird species in Europe are
provided by Hirschfeld and Heyd (2005) and Mooij (2005).
Species-specific estimates differ between these two sources
(discussed by Hirschfeld and Heyd 2005) but in general
there is a strong correlation between the estimates for the
species included in this study (r00.994, p<0.001, n012 duck
species; note that Mooij 2005 does not give bag statistics for
Eur J Wildl Res
Table 1 Body mass in grams
(BO), clutch size (CL),
breeding habitat preference (HA)
(G generalist, E eutrophic lakes,
O oligotrophic lakes)
and hunting pressure rank
(EU Europe, FI Finland)
of study species
Species
Latin name
BO
CL
HA
EU
FI
Mallard
Common teal
Eurasian wigeon
Common goldeneye
Northern Pintail
Northern shoveler
Garganey
Tufted duck
Common pochard
Common merganser
Red-breasted merganser
Arctic diver
Great crested grebe
Red-necked grebe
Anas platyrhynchos
Anas crecca
Anas penelope
Bucephala clangula
Anas acuta
Anas clypeata
Anas querquedula
Aythya fuligula
Aythya ferina
Mergus merganser
Mergus serrator
Gavia arctica
Podiceps cristatus
Podiceps grisegena
1077
326
699
858
838
635
384
737
921
1438
1091
2389
937
835
8.9
8.7
7.8
9.0
8.1
9.6
9.0
9.7
7.3
9.2
9.1
2.0
4.2
4.0
G
G
E
G
E
E
E
E
E
O
O
O
E
E
11
12
8
6
9
10
4
5
7
2
1
0
0
0
11
8
10
6
9
7
12
3
2
5
1
0
0
0
Horned grebe
Common coot
Podiceps auritus
Fulica atra
403
782
4.5
7.7
E
E
0
3
0
4
the common coot). We calculated the mean of the values
provided by the two sources and used the mean values when
estimating harvest rate (estimate of the annual bag for the
common coot was taken from Hirschfeld and Heyd 2005).
Information about autumn or winter population (hereafter,
hunted population) size for each species was derived from
BirdLife International (2004) and Delany and Scott (2006).
Again, the estimates vary depending on the source. Because of
this, and because we do not know to what extent birds originating from different non-breeding ranges (see Delany and
Scott 2006) constitute the bag at the European level, we
related the estimated annual bags to three different estimates
of the hunted population for each species, i.e., the EU25
wintering population estimate from BirdLife International
(2004), the non-breeding population estimate for North-west
Europe from Delany and Scott (2006) and the non-breeding
population estimate for North-west, Central and Eastern
Europe from Delany and Scott (2006). For example, the
estimated annual bag for the Eurasian wigeon (Anas penelope)
was 621,278 individuals (i.e., the mean of the estimates from
Hirschfeld and Heyd 2005; Mooij 2005) and the estimated
non-breeding population size for North-west Europe was
1,500,000 individuals according to Delany and Scott (2006),
resulting in a harvest rate of 41.4 % (621,278/1,500,000×100).
The procedure gave us three estimates of harvest rate for each
quarry species at the European level. We calculated the mean
of the three harvest rate values, ranked the species-specific
mean values and used the mean rank in the analyses. In
addition, our analysis included four protected species at the
European level, representing ‘zero’ hunting pressure (Table 1).
Considering harvest rate in Finland, we used annual
species-specific bag statistics from the period 2003–2009
compiled by the Finnish Game and Fisheries Research
Institute (Finnish Game and Fisheries Research Institute
2009, 2010) and calculated mean annual kill for each quarry
species. The period considered is the only period from
which the annual kill has been reported for all the species
included in this study. Based on wing samples of duck bag
from Finland in 1969–1970 (Pirkola and Lindén 1972) and
2005–2007 (Alhainen et al. 2010) the proportions of different species have remained remarkably similar between
1969–1970 and 2005–2007 (r00.985, p<0.001, n09 duck
species), implying that relative annual kill of the species has
been stable over the past few decades. To estimate the
population size at the beginning of the hunting season in
Finland (20 August) for each of the quarry species, we
multiplied the number of breeding pairs reported in the latest
Finnish bird atlas (Väisänen et al. 2011) by 3; this procedure
aims to include immature birds in the population (see
Delany and Scott 2006). Species-specific estimates of harvest
rate in Finland were calculated as explained above at the
European level, except that we needed to calculate only one
estimate. We ranked the species-specific harvest rates and
used the ranks in the analyses. There were four protected
species also at the level of Finland, and these species were
assigned to ‘zero’ hunting pressure (Table 1).
The ban of lead shot in Finland in 1996 (before the 1996
hunting season) resulted in an abrupt reduction in waterbird
harvest: the mean annual total kill of waterbirds (ducks breeding in inland waters and the common coot) was estimated at
801,150 individuals (range 734,500–850,850) during 1990–
1994 (Finnish Game and Fisheries Research Institute 1998),
while it was only 586,120 individuals (range 526,700–
636,500) during 1996–2000 (Finnish Game and Fisheries
Research Institute 2002; note that bag statistics are not available for 1995), i.e., a reduction of about 27 % in total
Eur J Wildl Res
waterbird harvest. The decrease was consistent across species:
the corresponding change for individual species or species
group (at that time, annual bags were not reported for all
species separately) was 28.6 % for mallard (Anas platyrhynchos), 25.9 % for common goldeneye (Bucephala clangula),
18.8 % for common teal (Anas crecca) and garganey (Anas
querquedula) combined, 31.5 % for red-breasted merganser
(Mergus serrator) and common merganser (Mergus merganser) combined, and 36.5 % for other species combined. Moreover, except in 1 year since 2000, the annual total kill has been
below the mean value for the period 1996–2000 (Finnish
Game and Fisheries Research Institute 2007, 2011). Considering the magnitude and consistency of the decrease in waterbird harvest in Finland, we expect it to be reflected in the
population trends of the quarry species, if hunting pressure is
an important driver of population dynamics of these species.
We would like to note that the reduction in hunting mortality may not have been the only positive effect resulting from
the ban of lead shot. Indeed, it may also have had direct
positive effects on waterbird populations through reduction
in lead poisoning (e.g., Pain 1990; Mateo 2009; MartinezHaro et al. 2011). However, it seems unlikely that these effects
would override changes in hunting mortality. More important,
changes in both mortality factors (i.e., hunting mortality and
mortality due to lead poisoning) should have affected trends in
the same direction in the present study.
Habitat specialization and life history
To characterise habitat specialization, we divided the species
into three groups: (1) species breeding mainly in eutrophic
lakes, (2) species breeding mainly in oligotrophic lakes and
(3) generalists which can be found in considerable numbers in
both types of lakes. Eutrophic lakes included both naturally
eutrophic lakes as well as formerly oligotrophic lakes that
have been eutrophicated by agriculture during recent decades.
The species-specific classification (Table 1) was based on
breeding densities and habitat distribution of the species, as
documented in Kauppinen (1993) and Kauppinen and
Väisänen (1993), updated with information from Väisänen et
al. (1998). The habitat definition (i.e., eutrophic lakes or
oligotrophic lakes) used by these authors was based on midsummer coverage of dominant helophytes at the lakes (for
more details, see Kauppinen and Väisänen 1993). We used
body size (body mass) and clutch size as life history variables
(Table 1). Mean body mass values were taken from Cramp
and Simmons (1977). Clutch size information of Finnish birds
was taken from Solonen (1985).
Statistical analyses
Clutch size (CL), adult body mass (BO), habitat preference
(HA), and Finnish and European hunting pressure (FI and
EU, respectively) were used as explanatory variables (Table 1)
for the species-specific slopes estimating mean annual population change from 1986 up to 1997 and from 1997 up to 2011
(Fig. 2). Thus, one slope for each period and species was
estimated. The period effect was indicated by a factorial
variable (PE). For statistical analyses, natural logarithms of
the life history (CL and BO) as well as of the hunting
(EU and FI; 1 was added to each hunting variable
before log transformation) variables were taken. Normally distributed additive slopes, indicating trends in
log population index, were estimated using TRIM software (Pannekoek and van Strien 2005); two change-points
(1986 and 1997) were set to modelling options. Note that, as
an example, the index of 1997 is the result of addition of the
slope value of 1996 to the index of 1996. The ban of lead shot
took effect in 1996 before the start of hunting season. We set
the change-point of population indices at the year 1997,
assuming a delayed (1 year) population dynamical response
(e.g., Newton 1998) of quarry population recovery to the
decreased hunting pressure. Assuming no delayed dynamics,
our experimental set-up should be conservative for the effect
of hunting pressure during the first period as it includes
population census from the spring 1997. In any case, the
shifting of the change point by 1 year would not have apparent
effects on the slope values (cf. Fig. 2).
We used Bayesian mixed modelling and Markov chain
Monte Carlo (MCMC) posterior sampling (Brown and Zhou
2010) in the estimation of generalized linear mixed models.
Species identifier was set as random variable, controlling for
between cluster (species) variation in slopes and the dependency of slopes within the clusters. Fifteen competing models were estimated using all possible combinations of the
following factors or factor combinations: (1) CL + BO, (2)
EU, (3) HA, and (4) the interaction and main effects of FI ×
PE. In particular, our aim was to investigate if the ban of
lead shot (in 1996) had had effect on slopes; thus, we
designed the analysis in order to probe primarily the interaction term (4; i.e., FI × PE). In order to reduce the number of
models, we analysed the joint effect of the life history parameters (1). In MCMC posterior sampling, non-informative priors were used. A total of 10,000 burn-in iterations (up to
convergence of coefficients) and additive 90,000 iterations
were run in order to estimate the posterior distribution of
model parameters. Posterior distributions were derived from
thinned iteration chains (every 50th iteration recorded).
We conducted the Bayesian analyses with the R (R
Development Core Team 2012) interfaces glmmBUGS
(Brown and Zhou 2010) and R2WinBUGS (Sturtz et al.
2005) (for WinBUGS 1.4.3; Spiegelhalter et al. 2003). For
details of MCMC posterior sampling, see, e.g., Gelman et al.
(2003) and Lunn et al. (2000; 2009). The differences of
deviance information criterion ΔDICi values (Spiegelhalter
et al. 2002) were estimated for models (i); DIC weights wi
Eur J Wildl Res
Common Teal
Eurasian Wigeon
Common Goldeneye
ANACRE 863
ANAPEN 531
BUCCLA 1539
1.1
0.6
0.8
Tufted Duck
ANAQUE 47
AYTFUL 547
0.5
1.5
1.0 1.5 2.0
1.0
0.6
0.5 1.0 1.5 2.0
Garganey
ANACLY 141
Red−br. Merganser
Arctic Diver
MERMER 175
MERSER 89
GAVARC 88
1.0
1.1
0.6
0.9
0.7
0.5
0.7 0.9 1.1 1.3
Common Merganser
AYTFER 225
1.4
Common Pochard
Common Coot
PODAUR 57
FULATR 516
1.0
1.0
0.6
0.6
0.9
0.7
0.5 1.0 1.5 2.0
Horned Grebe
PODGRI 173
1.4
Red−necked Grebe
PODCRI 607
1.4
Great Crested Grebe
1.1
1.3
0.9
0.9
1.2
1.0
1.0
0.8
Northern Shoveler
ANAACU 113
1.4
Northern Pintail
1.5
2.5
1.2
Mallard
ANAPLA 1074
1990
2010
Fig. 2 Population change indices as estimated with TRIM. Thin line
shows index series based on all possible change-points and imputation,
which notifies both estimated and observed counts as the basis of index
calculus. Bold line expresses model based indices (based on only
estimated counts) and allowing two change-points, at 1986 and 1997.
The mean of each index series is scaled at one. Horizontal dash line is
placed at index values 0.5, 1.0, and 1.5. Numbers after scientific name
abbreviations (first three letters from genera and species names, see
Table 1) indicate mean number of pairs per study year
(Wagenmakers and Farrell 2004; Lunn et al. 2009) were
calculated as
models in which that factor was included, ji 01 (otherwise,
ji 00).
expð$DICi =2Þ
wi ¼ P
expð$DICi =2Þ
Results
i
Over all competing models, ∑wi 01. We used the DIC
weights for each model as the indication of how well that
model was supported, and model averaging to determine the
relative importance of factors (1–4 above) in models by
summing, ∑wiji, which is the sum of DIC weights from all
The trend analysis based on two change-points at 1986 and
1997 revealed significant long-term trends (Fig. 2, Table 2).
Seven out of the 16 species increased and two species (common teal and northern pintail) decreased statistically significantly (t-test, p<0.05) during the period 1986–1997, whereas
Eur J Wildl Res
Table 2 Additive slopes of indices (slope), their standard errors (SE) and statistical significances (p) based on two change-points at 1986 and 1997
in 16 waterbird species in Finland (Fig. 2)
1986–1996
1997–2011
Species
Latin name
Slope
SE
p
Slope
SE
p
Mallard
Common teal
Eurasian wigeon
Common goldeneye
Northern pintail
Northern shoveler
Garganey
Tufted duck
Common pochard
Common merganser
Anas platyrhynchos
Anas crecca
Anas penelope
Bucephala clangula
Anas acuta
Anas clypeata
Anas querquedula
Aythya fuligula
Aythya ferina
Mergus merganser
0.002
−0.013
−0.001
0.022
−0.039
−0.016
−0.004
0.002
0.038
0.026
0.004
0.004
0.005
0.003
0.010
0.008
0.012
0.006
0.008
0.010
0.636
0.002
0.814
<0.001
<0.001
0.051
0.730
0.747
<0.001
0.007
0.009
−0.002
−0.029
−0.017
−0.033
−0.0002
−0.087
−0.065
−0.121
−0.020
0.003
0.003
0.004
0.002
0.008
0.007
0.013
0.006
0.009
0.007
<0.001
0.605
<0.001
<0.001
<0.001
0.976
<0.001
<0.001
<0.001
0.004
Red-breasted merganser
Arctic diver
Great crested grebe
Red-necked grebe
Horned grebe
Common coot
Mergus serrator
Gavia arctica
Podiceps cristatus
Podiceps grisegena
Podiceps auritus
Fulica atra
0.046
0.041
0.001
0.075
0.010
0.011
0.015
0.012
0.005
0.007
0.011
0.005
0.002
0.001
0.756
<0.001
0.405
0.042
−0.035
0.003
−0.025
−0.059
−0.070
−0.072
0.012
0.008
0.004
0.007
0.014
0.005
0.003
0.698
<0.001
<0.001
<0.001
<0.001
Here, slope estimates mean annual population change and it is derived from the trend-line of logarithmic indices (indexyear+1 0 slope + indexyear)
estimated for each of the two periods. Mean annual multiplicative change is calculated as exp(slope)
seven species showed no significant trend (Table 2). During
the period 1997–2011, 12 species declined significantly, three
species showed no significant trend and the mallard increased
significantly. The northern pintail decreased significantly during the first and second period. Six species increased significantly during the first period and then declined significantly
during the second period (Table 2).
On the basis of the Bayesian analysis and DIC weights, the
model that contained only the habitat preference (HA) and the
interaction term (FI × PE) with the main effects was superior
compared to the other models, and the relative importance of
those factors scored highest values (Table 3). Slopes were less
positive, indicating more declining or less increasing trends,
among the species of eutrophic waters than among the habitatgeneralist species. The slopes among the species preferring
oligotrophic waters were not different from those of habitatgeneralist species (Table 4). Slopes tended to be smaller
during the second period than during the first period (Table 4,
cf. Table 2). Hunting pressure in Finland (FI) had a negative
effect on slopes, but the positive interaction term (FI × PE)
suggests that the negative effect was compensated for during
the second period (Table 4, Fig. 3). This indicates that the ban
of lead shot, resulting in a smaller national bag, may have had
positive effects on population trends of some species. In
particular, the less-hunted species tended to decline more than
the more-hunted species during the second period, i.e. being
opposite to the pattern observed in the first period (Fig. 3).
Discussion
The findings of this study indicate that the breeding populations of seven out of the 16 species examined increased
during the first period (1986–1997), but three quarters of the
species declined significantly during the second period
(1997–2011).
The role of hunting
The population trends during the first period (1986–1997)
and alarming population declines in many waterbird species
during the second period (1997–2011) were not associated
with the average hunting pressure in Europe. However,
hunting in Finland seems to have affected the population
trends during the first period, i.e., before the decrease in
hunting bag size due to the ban of lead shot. Species that had
the highest hunting pressure had the lowest slopes of population trend during the first period, suggesting that hunting
probably limited those populations at that time. After the
ban of lead shot, such an effect was no longer observed. We
would like to note, however, that the drastic change in
population trend (from positive to negative slope) from the
first to the second period in some of the non-hunted species
(e.g., red-necked grebe Podiceps grisegena) and in species
with relatively low hunting pressure (e.g., red-breasted merganser and common pochard Aythya ferina) (see Table 1 and
Eur J Wildl Res
Table 3 Model weights (wi) and
averaging based on deviance
information criterion (DIC)
The lower/higher DIC/w, the
more supported model
CL clutch size, BO body mass,
EU European hunting pressure,
FI Finnish hunting pressure, HA
habitat preference, PE study
period; for further information
see Materials and methods
Model (i)
Factor1
Factor2
Factor3
1
2
3
4
5
6
7
8
9
10
11
12
13
14
CL + BO
CL + BO
CL + BO
CL + BO
EU
EU
HA
15
Relative importance
CL + BO
0.196
EU
0.259
HA
0.857
Factor4
EU
HA
FI × PE
CL + BO
CL + BO
CL + BO
EU
HA
FI × PE
EU
EU
EU
Fig. 2) have had a strong effect on the interaction between
hunting pressure and period (i.e., the FI × PE term). The
change to a positive direction from the first to the second
period was relatively small or did not exist in species ranked
as having relatively high hunting pressure (e.g., garganey,
mallard, Eurasian wigeon and common teal; Table 2). Thus
we suggest that, in general, hunting in Europe and in Finland
is unlikely to have been the major driver of the observed
recent large-scale population declines of breeding waterbirds
in Finland.
HA
FI
FI
FI
FI
FI
HA
HA
HA
× PE
× PE
× PE
× PE
× PE
FI × PE
1.000
DICi
ΔDICi
wi
−106.5
−106.6
−107.8
−124.2
−104.1
−104.7
−123.9
−106.5
−122.7
−128.8
−126.7
−125.5
−121.8
−102.7
22.3
22.2
20.9
4.6
24.7
24.1
4.9
22.3
6.1
0.0
2.1
3.3
6.9
26.1
7.75E−06
8.24E−06
1.52E−05
0.05
2.35E−06
3.18E−06
0.05
7.76E−06
0.03
0.54
0.19
0.10
0.02
1.15E−06
−123.0
5.8
0.03
Our indices of hunting pressure at the European level
were based on incomplete bag statistics. For example information on bag statistics from European countries outside the
EU, notably Russia, was missing (see Hirschfeld and Heyd
2005; Mooij 2005). Also, we were not able to examine the
hunting pressure outside Europe, and yet hunting in Africa
could be significant for some species. However, only two of
the study species, garganey and northern pintail, are mainly
wintering in Africa, and thus hunting outside Europe cannot
explain the generally declining pattern. Interestingly, both of
Table 4 Bayesian analysis based on MCMC posterior sampling
(A)
(B)
Parameter
Mean
SD
2.5 %
50 %
97.5 %
BO
CL
HA_oligotrophic
HA_eutrophic (0a)
FI (0b)
EU
PE_97_11 (0c)
FI × PE_97_11 (0d)
HA_oligotrophic
0.0115
−0.0076
−0.0031
−0.0094
−0.0302
−0.0132
−0.0864
0.0248
0.0004
0.0184
0.0251
0.0153
0.0283
0.0178
0.0159
0.0196
0.0114
0.0209
−0.0245
−0.0577
−0.0339
−0.0652
−0.0649
−0.0456
−0.1250
0.0024
−0.0413
0.0116
−0.0077
−0.0030
−0.0096
−0.0300
−0.0131
−0.0864
0.0248
0.0007
0.0475
0.0425
0.0260
0.0459
0.0059
0.0187
−0.0480
0.0476
0.0412
HA_eutrophic (0a)
FI (0b)
PE_97_11 (0c)
FI × PE_97_11 (0d)
−0.0306
−0.0197
−0.0863
0.0249
0.0158
0.0086
0.0186
0.0108
−0.0620
−0.0372
−0.1230
0.0035
−0.0307
−0.0196
−0.0862
0.0250
0.0012
−0.0033
−0.0498
0.0460
Degree of belief
Pr.(a<0)00.954
Pr.(b<0)00.816
Pr.(c<0)01.000
Pr.(d>0)00.985
Pr.(a<0)00.970
Pr.(b<0)00.988
Pr.(c<0)01.000
Pr.(d>0)00.989
Posterior mean, standard deviation and limits from lower to upper 95 % credible interval. Degree of belief is the probability that a hypothesis is true.
Posteriors reported for (A) the model with all parameters, and (B) the most supported model by DIC (Table 3)
CL clutch size, BO body mass, EU European hunting pressure, FI Finnish hunting pressure, HA habitat preference, PE study period; for further
information, see Materials and methods
0.02 0.06
−0.04
Slope (1986−1996)
Eur J Wildl Res
1.0
1.5
2.0
2.5
−0.06
0.00
0.5
The role of life history parameters and habitat type
−0.12
Slope (1997−2011)
0.0
considered in the present study, despite legislative requirements for the collection of such data (e.g., in the African–
Eurasian Migratory Waterbird Agreement). Reasonably
long series on annual breeding numbers, reproductive output and bag statistics in Finland are presently available for
mallard, common teal and common goldeneye, and we will
address the effects of hunting pressure on breeding numbers
of these species in more detail elsewhere (Pöysä et al., in
preparation).
0.0
0.5
1.0
1.5
2.0
2.5
Hunting pressure (Finland)
Fig. 3 Effect of hunting pressure (Finland) on species specific slopes
of 1986–1996 (upper panel) and 1997–2011 (lower panel) (Table 2)
based on Bayesian analysis. Mean of estimated slopes (open circles)
with Bayesian 95 % confidence intervals (credible intervals). Dots
denote observed slopes. Regression line is drawn on the basis of
estimated mean values. Hunting pressure values of 0 have been slightly
random jittered in order to help distinction between species. Hunting
pressure values have been transformed as log(FI + 1) (for original
values, see Table 1)
the trans-African migrants did show a rapid population decline
during the second period, and similar declines have been
observed in many other long-distance migrants during recent
decades (Sanderson et al. 2006; Brommer 2008). Thus, the
decline of garganey and northern pintail could be partly linked
with the general trend of deteriorating conditions along the
migration route and/or on wintering grounds (Sanderson et al.
2006; Pearce-Higgins et al. 2009). On the other hand, Rendón
et al. (2008) did not find any long-term changes (from 1978 to
2005) in the numbers of northern pintail wintering in Doñana,
south-west Spain. From the other six Anatidae species included
in both Rendón et al. (2008) and this study only the common
teal and Eurasian wigeon showed a long-term decline in wintering numbers at Doñana.
Due to limited sample sizes, our analysis omitted geese
which generally have been increasing in Finland, except the
bean goose Anser fabalis whose population is most probably declining (Valkama et al. 2011). Hunting pressure towards the bean goose is high in Finland (Finnish Game and
Fisheries Research Institute 2011) especially considering its
low population size (Väisänen et al. 2011). Finally, whilst
our study is the first quantitative analysis of hunting impacts
on waterbird populations in Europe, our study design has
shortcomings due to limitations in data availability. A more
powerful approach for exploring the effects of hunting pressure might be to study directly the effect of annual harvest
rate on annual changes in population size (e.g., Nichols
1991; Reynolds and Sauer 1991). Unfortunately, such data
are not available at the European level for any of the species
Neither the clutch size nor the body mass of the study
species were associated with the observed population trends.
However, habitat type had a clear effect: species that prefer
eutrophic lakes had generally declined more as compared
with generalist species or species preferring oligotrophic
lakes. This finding is in line with that observed in wetlands
classified as Important Bird Areas (IBA) in Finland. The
conservation value of several important wetlands has been
decreasing significantly since the early 1980s, but the decline has been much weaker in areas where notable
improvements to management actions have been made
(Ellermaa and Lindén 2011). Since the areas from which
the present data come are not part of the Finnish IBA network,
our findings, together with those of Ellermaa and Lindén
(2011), suggest that the status of breeding waterbirds in eutrophic wetlands in Finland has generally been impaired.
Several reasons have been proposed to explain the declining trend of waterbirds in eutrophic lakes. One of the
suggested causes is further eutrophication of the water systems (Ellermaa and Lindén 2011) that has been going on for
decades (Kauppi et al. 1993; Simola et al. 1995; Ekholm and
Mitikka 2006). Such development should have been more
pronounced in naturally eutrophic lakes and hence affected
especially those species that prefer those habitats. Eutrophication has been suggested to cause population declines of common goldeneye, common coot and velvet scoter Melanitta
fusca in the Archipelago Sea in SW Finland (Rönkä et al.
2005), but its effects on waterbird populations has not been
directly examined at inland lakes.
Most of the eutrophic lakes in Finland are situated on
lowlands in the southern part of the country, where agriculture is also at its most intensive (von Haartman 1973).
Ekholm and Mitikka (2006) studied 20 lakes situated in
agricultural landscapes in south and central Finland and
found six of them to be eutrophic and 14 to be hypertrophic.
Over half of the same lakes also showed signs of increasing
eutrophication during 1976–2002, supporting the idea that
nutrient inputs from agriculture have also continued during
our study period. Eutrophication has been shown to cause
increases of phytoplankton, turbidity and cyprinid populations (Olin et al. 2002; Ekholm and Mitikka 2006), which all
Eur J Wildl Res
can affect negatively the abundance of underwater vegetation
and invertebrates (Giles 1994; Hanson and Butler 1994).
Hence, strong eutrophication can decrease food availability
for waterbirds, which may lead to population decline. Indeed,
food abundance has been shown to be the key factor determining species number and density of waterfowl communities
in Northern Europe (Elmberg et al. 1993). On the other hand,
eutrophication of nutrient-poor oligothrophic lakes may improve breeding opportunities for dabbling ducks, such as the
mallard (Sjöberg et al. 2000), that prefer moderately eutrophic
wetlands. Interestingly, Hilli-Lukkarinen et al. (2011) found
that the decrease of agricultural areas around their study lakes
in central Finland from 1955–56 to 2002–2003 did not have
clear effects on waterfowl populations. It is also important to
keep in mind that climate change may enhance eutrophication.
In Northern Europe, warming climate will likely increase
rainfall especially during winter time (Jylhä et al. 2004),
which increases nutrient flow to the water systems from the
catchment area (Meier et al. 2012). This highlights, that both
direct and indirect consequences of climate change on waterbird populations should be examined in the near future.
Additional reasons for declining waterfowl numbers may
be increasing abundance of invasive predators (Mikkola-Roos
et al. 2010) such as the raccoon dog Nyctereutes procyonoides
and American mink Mustela vison (Nordström et al. 2002,
2003; Väänänen et al. 2007) and the decline of a keystone
species, the black-headed gull Larus ridibundus (MikkolaRoos et al. 2010; Väänänen 2011). Indeed, several duck species are known to have higher breeding densities in blackheaded gull colonies (Cramp and Simmons 1977; Cramp
1985) and there is experimental evidence that the breeding
colonies provide safety from nest predators (Väänänen 2000).
Increased nest predation may have decreased the breeding
success of waterbirds and resulted in population declines.
However, the gull population has been declining since the
1970s (Valkama et al. 2011), whereas the majority of the
waterbird populations have shown negative trends only in
more recent years. While the decrease of gull populations
mostly has been gradual and lags of several years may occur
in the response of duck populations to changes in predation
pressure, these findings suggest that other factors are behind
the overall decline of waterbirds in Finland. Finally, changes in
fish–duck interactions may be one of the potential causes of
waterbird population declines, as fish may affect waterbirds
through both competitive and predatory effects (e.g., Elmberg
et al. 2010; Nummi et al. 2012; Väänänen et al. 2012 and
references therein).
Conclusions
We examined the importance of hunting pressure in explaining long-term trends of breeding numbers of waterbirds in
Finland by analyzing simultaneously population trends of
quarry and non-quarry species. Our findings indicate that
hunting pressure in Finland may have limited the abundance
of some species during the period of high hunting pressure,
though the evidence was not strong. However, in general the
present analysis indicates more strongly that hunting pressure in Finland or in Europe does not explain the general
declining trend of most breeding waterbirds during the last
15 years. These declines were most severe in species that
prefer eutrophic lakes for breeding. One potential reason for
this is over-eutrophication of naturally nutrient-rich lakes,
but the pattern should be studied in more detail. We encourage further investigation into the effects of exploitation on
population sizes of quarry species and into the connection
between water quality and waterbird populations. To that
end, we urgently need more accurate and up-to-date hunting
bag data from all countries along the main European flyways
of waterfowl. And combining data on waterbird numbers with
information on fish abundance and water quality using extensive lake-specific data (e.g., Rask et al. 2010) would help to
elucidate the role of over-eutrophication in affecting waterbird
populations.
Acknowledgments We would like to thank all the hundreds of
hunters and bird watchers that have participated in waterbird surveys
in Finland. We also thank Pirjo Hätönen, Ritva Koivunen, Heikki
Koivunen, Esa Lammi, Petri Timonen and Marcus Wikman for processing census forms and for computerizing the data and Eija Nylander
for compiling the Finnish hunting bag statistics. Comments by two
anonymous reviewers greatly improved the text. The Nordic Waterbirds
And Climate Network (NOWAC) provided inspiring atmosphere that
boosted the writing of this manuscript.
References
Alhainen M, Väänänen V-M, Pöysä H, Ermala A (2010) Duck hunting
bag in Finland – what do wing samples tell us about the species
composition and age structure in a bag? Suomen Riista 56:40–47,
in Finnish with English summary
BirdLife International (2004) Birds in the European Union: A status
assessment. BirdLife International, Wageningen
BirdLife International (2012) The BirdLife checklist of the birds of the
world, with conservation status and taxonomic sources. Version 5.
http://www.birdlife.info/im/species/checklist.zip. Accessed 6
September 2012
Both C, van Turnhout CAM, Bijlsma RG, Siepel H, van Strien AJ,
Foppen RPB (2010) Avian population consequences of climate
change are most severe for long-distance migrants in seasonal
habitats. Proc R Soc B 277:1259–1266
Brommer JE (2008) Extent of recent polewards range margin shifts in
Finnish birds depends on their body mass and feeding ecology.
Ornis Fenn 85:109–117
Brown P, Zhou L (2010) MCMC for Generalized Linear Mixed Models
with glmmBUGS. R J 2:13–17
Cormont A, Vos CC, van Turnhout CAM, Foppen RPB, ter Braak CJF
(2011) Using life-history traits to explain bird population responses
to changing weather variability. Clim Res 49:59–71
Eur J Wildl Res
Cramp S (ed) (1985) The birds of the Western Palearctic, vol. IV.
Oxford University Press, Oxford
Cramp S, Simmons KEL (eds) (1977) The birds of the Western Palearctic, vol. I. Oxford University Press, Oxford
Delany S, Scott D (2006) Waterbird population estimates, 4th edn.
Wetlands International, Wageningen
R Development Core Team (2012) R: A language and environment for
statistical computing. http://www.r-project.org. Accessed 16
September 2012
Devineau O, Guillemain M, Johnson AR, Lebreton J-D (2010) A
comparison of green-winged teal Anas crecca survival and harvest between Europe and North America. Wildl Biol 16:12–24
Duncan RP, Blackburn TM, Worthy TH (2002) Prehistoric bird extinctions and human hunting. Proc Royal Soc Lond B 269:517–521
Ekholm P, Mitikka S (2006) Agricultural lakes in Finland: current
water quality and trends. Environ Monit Assess 116:111–135
Ellermaa M, Lindén A (2011) IBA-monitoring tells us: birds are not
taken seriously in Finnish bird protection areas. Yearb Linnut
Mag 2010:143–168, in Finnish with English summary
Elmberg J, Nummi P, Pöysä H, Sjöberg K (1993) Factors affecting
species number and density of dabbling duck guilds in North
Europe. Ecography 16:251–260
Elmberg J, Nummi P, Pöysä H, Sjöberg K, Gunnarsson G, Clausen P,
Guillemain M, Rodrigues D, Väänänen V-M (2006) The scientific
basis for new and sustainable management of migratory European
ducks. Wildl Biol 12:121–127
Elmberg J, Dessborn L, Englund G (2010) Presence of fish affects lake
use and breeding success in ducks. Hydrobiologia 641:215–223
Finnish Game and Fisheries Research Institute (1998) Annual game bag
1996. Official Statistics of Finland – Agriculture, Forestry and Fishery
Finnish Game and Fisheries Research Institute (2002) Annual game bag
2001. Official Statistics of Finland – Agriculture, Forestry and Fishery
Finnish Game and Fisheries Research Institute (2007) Annual game
bag 2006. Riista-ja kalatalous – Tilastoja 5/2007. Official Statistics
of Finland – Agriculture, Forestry and Fishery
Finnish Game and Fisheries Research Institute (2009) Hunting 2008.
Riista-ja kalatalous – Tilastoja 5/2009. Official Statistics of Finland – Agriculture, Forestry and Fishery
Finnish Game and Fisheries Research Institute (2010) Hunting 2009.
Riista-ja kalatalous – Tilastoja 6/2010. Official Statistics of Finland – Agriculture, Forestry and Fishery
Finnish Game and Fisheries Research Institute (2011) Hunting 2010.
Riista-ja kalatalous – Tilastoja 6/2010. Official Statistics of Finland – Agriculture, Forestry and Fishery
Gelman A, Carlin JB, Stern HS, Rubin DB (2003) Bayesian data
analysis, 2nd edn. Chapman & Hall/CRC, Boca Raton
Giles N (1994) Tufted duck (Aythya fuligula) habitat use and brood
survival increases after fish removal from gravel pit lakes. Hydrobiologia 279–280:387–392
Green AJ (1996) Analyses of globally threatened Anatidae in relation
to threats, distribution, migration patterns, and habitat use. Conserv
Biol 10:1435–1445
Hagemeijer WJM, Blair MJ (eds) (1997) The EBCC atlas of European
breeding birds: Their distribution and abundance. T&A D Poyser,
London
Hanson MA, Butler MG (1994) Responses to food web manipulation
in a shallow waterfowl lake. Hydrobiologia 279–280:457–466
Herzon I, Auninš A, Elts J, Preikša Z (2008) Intensity of agricultural
land-use and farmland birds in the Baltic States. Agr Ecosyst
Environ 125:93–100
Herzon I, Ekroos J, Rintala J, Tiainen J, Seimola T, Vepsäläinen V
(2011) Importance of set-aside for breeding birds of open farmland in Finland. Agr Ecosyst Environ 143:3–7
Hilli-Lukkarinen M, Kuitunen M, Suhonen J (2011) The effect of
changes in land use on waterfowl species turnover in Finnis
boreal lakes. Ornis Fenn 88:185–194
Hirschfeld A, Heyd A (2005) Mortality of migratory birds caused by
hunting in Europe: bag statistics and proposals for the conservation of birds and animal welfare. Ber Vogelschutz 42:47–74
Jylhä K, Tuomenvirta H, Ruosteenoja K (2004) Climate change projections for Finland during the 21st century. Boreal Environ Res
9:127–152
Kauppi L, Pietiläinen O-P, Knuuttila S (1993) Impacts of agricultural
nutrient loading on Finnish watercourses. Water Sci Technol
28:461–471
Kauppinen J (1993) Densities and habitat distribution of breeding
waterfowl in boreal lakes in Finland. Finn Game Res 48:24–45
Kauppinen J, Väisänen RA (1993) Ordination and classification of
waterfowl communities in south boreal lakes. Finn Game Res
48:3–23
Knudsen E, Lindén A, Both C, Jonzén N, Pulido F, Saino N, Sutherland
WJ, Bach LA, Coppack T, Ergon T, Gienapp P, Gill JA, Gordo O,
Hedenström A, Lehikoinen E, Marra PP, Møller AP, Nilsson ALK,
Péron G, Ranta E, Rubolini D, Sparks TH, Spina F, Studds CE,
Sæther SA, Tryjanowski P, Stenseth NC (2011) Challenging claims
in the study of migratory birds and climate change. Biol Rev
86:928–946
Koskimies P, Väisänen RA (1991) Monitoring bird populations. Zoological Museum. Finnish Museum of Natural History, Helsinki
Long PR, Székely T, Kershaw M, O’Connell M (2007) Ecological
factors and human threats both drive wildfowl population
declines. Anim Conserv 10:183–191
Lunn DJ, Thomas A, Best N, Spiegelhalter D (2000) WinBUGS – a
Bayesian modelling framework: concepts, structure, and extensibility. Stat Comput 10:325–337
Lunn D, Spiegelhalter D, Thomas A, Best N (2009) The BUGS project:
evolution, critique and future directions. Stat Med 2009:3049–
3067
Martinez-Haro M, Green AJ, Mateo R (2011) Effects of lead exposure
on oxidative stress biomarkers and plasma biochemistry in waterbirds in the field. Environ Res 111:530–538
Mateo R (2009) Lead poisoning in wild birds in Europe and the
regulations adopted by different countries. In: Watson RT, Fuller
M, Pokras M, Hunt WG (eds) Ingestion of lead from spent
ammunition: Implications for wildlife and human. The Peregrine
Fund, Boise, pp 1–28
McCullagh P, Nelder JA (1989) Generalized linear models. Chapman
and Hall, London
Meier HEM, Hordoir R, Andersson HC, Dieterich K, Gustafsson BG,
Höglund A, Schimanke S (2012) Modelling the combined impact
of changing climate and changing nutrient loads on the Baltic Sea
environment in an ensemble of transient simulations for 1961–
2099. Clim Dyn (in press). doi:10.1007/s00382-012-1339-7
Mikkola-Roos M, Tiainen J, Below A, Hario M, Lehikoinen A,
Lehikoinen E, Lehtiniemi T, Rajasärkkä A, Valkama J, Väisänen RA
(2010) Linnut — Birds. In: Rassi P, Hyvärinen E, Juslén A,
Mannnerkoski I (eds) The 2010 red list of Finnish species. Ministry
of the Environment, Finnish Environment Institute, Helsinki, pp
320–321
Møller AP, Fiedler W, Berthold P (eds) (2010) Effects of climate
change on birds. Oxford University Press, Oxford
Mooij JH (2005) Protection and use of waterbirds in the European
Union. Beitr zur Jagd- und Wildforschung 30:49–76
Newton I (1998) Population limitation in birds. Academic Press, San
Diego
Nichols JD (1991) Responses of North American duck populations to
exploitation. In: Perrins CM, Lebreton J-D, Hirons GJM (eds)
Bird population studies: Relevance to conservation and management. Oxford University Press, Oxford, pp 448–525
Nichols JD, Runge MC, Johnson FA, Williams BK (2007) Adaptive
harvest management of North American waterfowl populations: a
brief history and future prospects. J Ornithol 148:343–349
Eur J Wildl Res
Nordström M, Högmander J, Nummelin J, Laine J, Laanetu N,
Korpimäki E (2002) Variable responses of waterfowl breeding populations to long-term removal of introduced American mink. Ecography 25:385–394
Nordström M, Högmander J, Laine J, Nummelin J, Laanetu N,
Korpimäki E (2003) Effects of feral mink removal on seabirds,
waders and passerines on small islands in the Baltic Sea. Biol
Conserv 109:359–368
Nummi P, Väänänen V-M, Rask M, Nyberg K, Taskinen J (2012)
Competitive effects of fish in structurally simple habitats: perch,
invertebrates, and goldeneye in small boreal lakes. Aquatic Sci
74:343–350
Olden JD, Hogan ZS, Zanden MJV (2007) Small fish, big fish, red fish,
blue fish: size-biased extinction risk of the world’s freshwater and
marine fishes. Global Ecol Biogeogr 16:694–701
Olin M, Rask M, Ruuhijärvi J, Kurkilahti M, Ala-Opas P, Ylönen O
(2002) Fish community structure in mesotrophic and eutrophic
lakes of southern Finland: the relative abundances of percids and
cyprinids along a trophic gradient. J Fish Biol 60:593–612
Owens IPF, Bennett PM (2000) Ecological basis of extinction risk in
birds: habitat loss versus human persecution and introduced predators. PNAS 97:12144–12148
Pain DJ (1990) Lead poisoning of waterfowl: A review. In: Matthews
GVT (ed) Managing waterbird populations. Proc IWRB Symp,
Astrakhan, USSR. IWRB Special Publication No. 12, pp 172–181
Pannekoek J, van Strien AJ (2005) Trim 3 manual (Trends and indices
for monitoring data). Statistics Netherlands, Voorburg
Patterson JH (1979) Can ducks be managed by regulation? Experiences
in Canada. Trans North Am Wildl Nat Res Conf 44:130–139
Pearce-Higgins J, Yalden D, Dougall T, Beale C (2009) Does climate
change explain the decline of a trans-Saharan Afro-Palaearctic
migrant? Oecologia 159:649–659
Pirkola MK, Lindén H (1972) Results of duck wing collection surveys
in Finland 1969 and 1970. Suomen Riista 24:97–106, in Finnish
with English summary
Pöysä H, Väisänen RA, Wikman M (1993) Monitoring of waterbirds in
the breeding season: the programme used in Finland in 1986–92.
In: Moser M, Prentice RC, van Vessem J (eds) Waterfowl and
wetland conservation in the 1990s — a global perspective. Proc
IWRB Symp, St Petersburg Beach, FL, USA. IWRB Special Publication No 26, pp 7–12
Pöysä H, Elmberg J, Gunnarsson G, Nummi P, Sjöberg K (2004)
Ecological basis of sustainable harvesting: is the prevailing paradigm of compensatory mortality still valid? Oikos 104:612–615
Pöysä H, Rintala J, Wikman M, Lehikoinen A, Väisänen RA (2011)
RKTL — Vesilinnut 2011. http://www.rktl.fi/riista/riistavarat/
vesilinnut_2.html. Accessed 14 May 2012
Rask M, Olin M, Ruuhijärvi J (2010) Fish-based assessment of ecological status of Finnish lakes loaded by diffuse nutrient pollution
from agriculture. Fish Manage Ecol 17:126–133
Rendón MA, Green AJ, Aguilera E, Almaraz P (2008) Status, distribution and long-term changes in the waterbird community wintering in Doñana, south-west Spain. Biol Conserv 141:1371–1388
Reynolds RE, Sauer JR (1991) Changes in mallard breeding populations in relation to production and harvest rates. J Wildl Manage
55:483–487
Rönkä MTH, Saari CLV, Lehikoinen EA, Suomela J, Häkkilä K (2005)
Environmental changes and population trends of breeding waterfowl in northern Baltic Sea. Ann Zool Fenn 42:587–602
Sanderson FJ, Donald PF, Pain DJ, Burfield IJ, van Bommel FPJ
(2006) Long-term population declines in Afro-Palearctic migrant
birds. Biol Conserv 131:93–105
Simola H, Kukkonen M, Lahtinen J, Tossavainen T (1995) Effects of
intensive forestry and peatland management on forest lake ecosystems in Finland: sedimentary records of diatom floral changes.
In: Marino D (ed) Proceedings of the Thirteenth International
Diatom Symposium, Maratea, Italy, 1–7th September 1994. Biopress. Bristol, pp 121–128
Sjöberg K, Pöysä H, Elmberg J, Nummi P (2000) Response of mallard
ducklings to variation in habitat quality: an experiment of food
limitation. Ecology 81:329–335
Smith GW, Reynolds RE (1992) Hunting and mallard survival, 1979–
88. J Wildl Manag 56:306–316
Solonen T (1985) Suomen linnusto. Lintutieto, Helsinki
Spiegelhalter DJ, Best NG, Carlin BP, Linde AVD (2002) Bayesian
measures of model complexity and fit. J R Statist Soc B 64:583–
639
Spiegelhalter D, Thomas A, Best N, Lunn D (2003) WinBUGS
user manual. http://www.mrc-bsu.cam.ac.uk/bugs/winbugs/
manual14.pdf. Accessed 16 September 2012
Stoate C, Báldi A, Beja P, Boatman ND, Herzon I, van Doorn A, de
Snoo GR, Rakosy L, Ramwell C (2009) Ecological impacts of
early 21st century agricultural change in Europe — a review. J
Environ Manage 91:22–46
Sturtz S, Ligges U, Gelman A (2005) R2WinBUGS: a package for
running WinBUGS from R. J Stat Softw 12:1–16
Väänänen V-M (2000) Predation risk associated with nesting in gull
colonies by two Aythya species: observations and an experimental
test. J Avian Biol 31:31–35
Väänänen V-M (2011) Small colonial larids and waterfowl — the
effect of gull colonies on waterfowl nesting in inland eutrophic
wetlands. Suomen Riista 57:84–91, in Finnish with English
summary
Väänänen V-M, Nummi P, Rautiainen A, Asanti T, Huolman I, MikkolaRoos M, Nurmi J, Orava R, Rusanen P (2007) The effect of raccoon
dog Nyctereutes procyonoides removal on waterbird breeding success. Suomen Riista 53:49–63, in Finnish with English summary
Väänänen V-M, Nummi P, Pöysä H, Rask M, Nyberg K (2012) Fish–
duck interactions in boreal lakes in Finland as reflected by abundance correlations. Hydrobiologia 697:85–93
Väisänen RA, Lammi E, Koskimies P (1998) Distribution, numbers
and population changes of Finnish breeding birds. Finnish Museum
of Natural History, University of Helsinki, Otava, in Finnish with
English summary
Väisänen RA, Hario M, Saurola P (2011) Population estimates of
Finnish birds. In: Valkama J, Vepsäläinen V, Lehikoinen A (eds)
The third Finnish breeding bird atlas. Finnish Museum of Natural
History and Ministry of Environment. http://atlas3.lintuatlas.fi/
english. Accessed 14 May 2012
Valkama J, Vepsäläinen, V, Lehikoinen, A (2011) The third Finnish
breeding bird atlas. Finnish Museum of Natural History and Ministry of Environment. http://atlas3.lintuatlas.fi/english. Accessed 14
May 2012
von Haartman L (1973) Changes in the breeding bird fauna of North
Europe. In: Farnes DS (ed) Breeding biology of birds. National
Academy of Sciences, Washington DC, pp 448–481
Wagenmakers E-J, Farrell S (2004) AIC model selection using Akaike
weights. Psychon B Rev 11:192–196