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ORIGINAL PAPER
Habitat selection by breeding waterbirds at ponds
with size-structured fish populations
Janusz Kloskowski &Marek Nieoczym &Marcin Polak &
Piotr Pitucha
Received: 1 April 2010 /Revised: 22 May 2010 /Accepted: 24 May 2010 /Published online: 8 June 2010
#Springer-Verlag 2010
Abstract Fish may significantly affect habitat use by birds,
either as their prey or as competitors. Fish communities are
often distinctly size-structured, but the consequences for
waterbird assemblages remain poorly understood. We
examined the effects of size structure of common carp
(Cyprinus carpio) cohorts together with other biotic and
abiotic pond characteristics on the distribution of breeding
waterbirds in a seminatural system of monocultured ponds,
where three fish age classes were separately stocked. Fish
age corresponded to a distinct fish size gradient. Fish age
and total biomass, macroinvertebrate and amphibian abun-
dance, and emergent vegetation best explained the differ-
ences in bird density between ponds. Abundance of animal
prey other than fish (aquatic macroinvertebrates and larval
amphibians) decreased with increasing carp age in the
ponds. Densities of ducks and smaller grebes were strongly
negatively associated with fish age/size gradient. The
largest of the grebes, the piscivorous great crested grebe
(Podiceps cristatus), was the only species that preferred
ponds with medium-sized fish and was positively associat-
ed with total fish biomass. Habitat selection by bitterns and
most rallids was instead strongly influenced by the relative
amount of emergent vegetation cover in the ponds. Our
results show that fish size structure may be an important
cue for breeding habitat choice and a factor affording an
opportunity for niche diversification in avian communities.
Keywords Common carp .Distant competition .
Habitat selection .Size-structured interactions .
Waterbird assemblages
Introduction
The influence of ecological interactions between distantly
related taxa upon patterns of habitat use is one of the
focuses of ecological and evolutionary research (Levins
1979; Safina and Burger 1985; Englund et al. 1992).
Interactions between fish and bird populations are known to
range from predation to competition. Fish-eating birds
profit from increases in fish populations (Lammens 1999),
while negative effects of fish on waterbird distribution have
been documented and attributed to exploitative competition
(Eriksson 1979; Eadie and Keast 1982; Hurlbert et al. 1986;
van Eerden et al. 1993). Fish communities frequently
exhibit a distinct size structure due either to external
disturbances promoting dominance of single size cohorts
or to inter- and intraspecific trophic interactions between
cohorts (e.g., Tonn and Magnuson 1982; Persson 1988;
McParland and Paszkowski 2006). The variability in size
structure of fish populations may be expected to affect the
habitat choice and reproductive success of many water-
birds, depending on the species involved. Larger fish can be
more profitable prey for avian predators, but on the other
hand, fish susceptibility to predation may decrease with
J. Kloskowski (*):M. Polak
Department of Nature Conservation, Institute of Biology,
Maria Curie-Skłodowska University,
Akademicka 19,
20-033 Lublin, Poland
e-mail: januszkl@hektor.umcs.lublin.pl
M. Nieoczym
Department of Zoology, University of Life Sciences,
Akademicka 13,
20-950 Lublin, Poland
P. Pitucha
Inspectorate for Environmental Protection in Lublin,
Obywatelska 13,
20-092 Lublin, Poland
Naturwissenschaften (2010) 97:673–682
DOI 10.1007/s00114-010-0684-9
growth (Moser 1986). As most fishes are size-limited in
feeding, in species with large terminal body sizes, the
ability to compete with birds may increase over ontogeny.
Fish may also affect the environmental context of inter-
actions with birds, e.g., via bioturbation (Lammens 1999;
Zambrano et al. 2001), and their potential for habitat
alteration can be size dependent (Driver et al. 2005).
However, little is known of size-structured fish–bird
interactions (but see Paszkowski and Tonn 2000), as most
studies have addressed avian habitat selection in relation to
the presence/absence of fish (Eriksson 1979; Hurlbert et al.
1986; Allen et al. 2007) or along a fish density gradient
(Hill et al. 1987; Haas et al. 2007). Since patterns of fish
size structure are predictable in many natural and human-
managed systems (Tonn and Magnuson 1982; Holmgren
and Appelberg 2000), elucidation of size-dependent effects
of fish on birds may be necessary to understand the
functioning of these systems and provide practical solutions
for waterbird conservation strategies.
The aim of this study was to examine how size structure
of fish influences assemblage composition of pond-
breeding waterbirds and what role fish size plays in
determining distribution of waterbirds relative to other
biological and habitat variables. We chose to work on the
common carp (Cyprinus carpio) because carp populations
frequently form strong year classes and consequently
distinct size structure; predation by piscivorous birds is
usually limited to the first- or second-summer cohorts
(Mraz and Cooper 1957; Moser 1986). Moreover, carp
commonly play a key role in structuring aquatic commu-
nities and can negatively affect food resources of waterfowl
(Crivelli 1983; Haas et al. 2007; Bajer et al. 2009). We
predicted that fish size structure would have a strong
influence on habitat selection by some waterbirds, while on
the other hand, we expected certain pond habitat features,
such as emergent vegetation, to affect distribution of
individual bird species among ponds. Therefore, we studied
patterns of habitat selection by waterbirds at the community
and individual species level, taking into account biotic and
abiotic habitat properties that might influence those
patterns, along a gradient of three carp age (size) classes:
young-of-the-year cohorts, 1-year-old fish, and 2-year-old
fish. The study system consisted of open carp ponds where
fish age cohorts were stocked separately and the age of the
cohorts was irregularly rotated between years. As it is
difficult to manipulate habitat choice of birds exploiting
spatially extensive ranges, seminatural systems such as
monoculture pond fisheries offer a valuable alternative
(Suter 1991; Haas et al. 2007) providing conditions for
“natural experiments”sensu Diamond (1986). The clear-cut
size distribution of fish age cohorts among ponds provided
an excellent opportunity to examine size-structured fish–
bird interactions using a whole-system approach.
Methods
Study system
The study was conducted in cooperation with the local
fisheries staff at extensively managed carp ponds in
southeastern Poland. During two breeding seasons, in
2002 and 2004, 39 and 46 ponds were surveyed. The
ponds belonged to five pond complexes (in total 651–
682 ha of water surface area) situated 10–60 km apart. The
eutrophic, typically monoculture ponds in SE Poland are
readily used by breeding birds and are acknowledged
strongholds for waterfowl (Grimmet and Jones 1989).
The privately administered ponds formerly belonged to a
single state-owned fisheries organization; hence, manage-
ment practices were alike for all study sites and all carp
stocks originated from the same hatchery. Three fish age
classes were stocked in separate growing-on ponds, and a
well-defined size gradient of fish cohorts was created.
Before introduction into the ponds, all carp were weighed
to establish the total stock biomass in each pond, and a
large sample of fish was weighed to determine mean
individual biomass. Stocking biomasses were on average
similar in 1+ and 2+ ponds (225±SE 29 vs 224 ± 28 kg/ha)
but were much larger than in 0+ ponds (Table 1), where
carp attained total biomass >50 kg ha only in late June.
During the spring stocking period (April–May), young-
of-the-year (0+; small-sized) carp were stocked at an
individual weight of 1.5–3.0 mg, to reach 5–8g(7to
8 cm in length) within ca. 2 months; 1+ (medium-sized)
carp weighed ca. 30–50 g and 2+ (large-sized) carp ca.
150–250 g. Due to substantial differences in fish size
between year cohorts under pond culture conditions, carp
age and the age-specific size range are considered inter-
changeable here. Potential carry-over effects of cohort
distribution (i.e., the influence of events in pond ecosys-
tems in past breeding seasons on the current habitat choice
of birds) were minimized because in most of the ponds, the
age of the carp stocks was rotated between years (albeit
irregularly, each year in ca. 30–60% of the studied ponds,
depending on the fish farm's current supply of the given
year-class of fish). Age cohorts were alternated either by
stocking different age classes in rotation in subsequent
years or leaving cohorts in the same ponds for 2 years. Carp
densities were within the ranges found in natural systems
(Table 1; Crivelli 1983; Panek 1987). Other fish occurred in
the ponds (small wild-grown and supplemental species,
mainly bleak (Leucaspius delineatus), wels (Silurus glanis),
or pike (Esox lucius)), but carp were overwhelmingly
dominant (95–98% of the total fish biomass per pond; M.
Filipiak and M. Sagan, personal communication). The
proportion of small fish that invaded the ponds despite the
screens at the water inlets was typically visually assessed
674 Naturwissenschaften (2010) 97:673–682
by fish farmers during draining operations because wild
fish were only occasionally collected. However, a few
ponds known to develop noticeable proportions of wild-
grown fish, usually following serious carp mortality
episodes, were excluded from the analyses.
The ponds were similar in depth (mean values 0.7–
1.3 m) but differed in emergent aquatic vegetation cover
along the pond margins (mainly Typha angustifolia and
Phragmites australis) and in surface area (Table 1; see
Kloskowski 2009 for more details on the study system).
Bird surveys
Waterbirds were counted between April and July at ca. 10-
day intervals (each pond was visited 12 times during the
season). The round count method of Koskimies and
Väisänen (1991) was used. We walked around the ponds
and counted birds using binoculars and scopes. We counted
only nonpasserine birds classified as pond breeders (nesting
on ponds or pond levees) and feeding at or beneath the
surface of the water. We used playback of species' calls
(Bibby et al. 2000) to detect territories of little grebe
(Tachybaptus ruficollis) and of rallids other than coot
(Fulica atra). The vocalizations were broadcast using a
tape recorder early in the morning and after sunset.
Numbers of breeding pairs (breeding territories) were
estimated following the method of Koskimies and Väisänen
(1991), with some modifications for pond conditions
(Ranoszek 1983). Analyses were restricted to species
occurring in >5% of the ponds: little grebe, great crested
grebe (Podiceps cristatus), red-necked grebe (Podiceps
grisegena), little bittern (Ixobrychus minutus), great bittern
(Botaurus stellaris), mute swan (Cygnus olor), mallard
(Anas platyrhynchos), garganey (Anas querquedula), po-
chard (Aythya ferina), tufted duck (Aythya fuligula), water
rail (Rallus aquaticus), little crake (Porzana parva),
moorhen (Gallinula chloropus), and coot. Where necessary,
breeding species data were converted to densities (birds/10 ha).
Fish and habitat variables
Data on pond size, carp age, and standing biomass in
individual ponds were provided by the staff of the local
fisheries. Ponds were also classified by hydroperiod (ponds
“wintering”vs flooded in spring). At each pond, a number
of variables were measured for use in analyses predicting
the community structure and responses of individual bird
species. Relative abundances of amphibian larvae and
aquatic invertebrates were estimated from pond surveys
using funnel activity traps. In 2002 and 2004, the study
sites were visited in random order from 27 April to 11 May
and between 19 June and 4 July to collect the spring and
summer fauna. The traps (modeled after Murkin et al. 1983;
Griffiths 1985) were cylindrical with a 23-mm aperture at
the narrow end of the funnel. Trapping is a reliable method
of estimating the availability of nonfish prey taken by
Table 1 Pond habitat variables (mean and range) sampled in 2002 and 2004, selected as potential predictors of breeding bird densities
Variable Description Mean (range)
Pond area Water surface area (ha) 4.8 (0.8–26)
Fish age 0+, 1+, 2+carp cohorts 0+, 51%; 1+, 29%; 2+, 20%
Fish standing biomass Total carp biomass (kg/ha) during the spring
stocking period (April–early May)
0+, negligible at stocking
(ca. 1 kg ha–); 1+, 225
(105–501); 2+, 224 (176–490)
Pond permanence Ponds that held or gathered water over winter
vs ponds which remained dry in winter and
were refilled in late March to early May (treated
as a categorical factor in the analyses)
Ponds wintering, 34%; flooded
in spring 76%
Amphibian abundance Relative wet weight (g/1 trap) 18.4 (0–74.8)
Macroinvertebrate abundance Relative dry weight (mg/1 trap) 0.82 (0–8.1)
Water transparency Secchi disk (26 cm diameter) depth (cm) 102.8 (30–180)
Emergent pond vegetation Proportion of pond surface area covered by emergent
aquatic plants
24.9 (2.5–77)
Shoreline development The ratio of the pond perimeter to the doubled square
root of the product of πand the pond surface area
1.5 (0–2.9)
Urbanized landscape Proportion of the shoreline adjacent to urbanized
habitat, i.e., roads and human settlements
0.2 (0–1.0)
Forest landscape Proportion of the shoreline covered by forest 0.1 (0–1.0)
Agricultural landscape Proportion of the shoreline adjacent to arable fields or pasture 0.2 (0–0.9)
Pond connectivity Proportion of the shoreline adjacent to other ponds 0.5 (0–1.0)
For fish age and pond permanence, the percentage of ponds studied belonging to the given category is presented instead
Naturwissenschaften (2010) 97:673–682 675
waterfowl (Elmberg et al. 1994). Ten traps were set in each
pond for 48 h (see Kloskowski 2009 for details of the
trapping procedure). The traps were approximately evenly
distributed in open water areas close to emergent vegetation
in order to sample both habitats. Invertebrates ≥4mm
(hereafter macroinvertebrates) caught in the traps were
identified (typically to family or genus). For common taxa,
dry weights were predicted from length–weight regressions
obtained after drying subsamples to stable weight at 50–60°C.
Macroinvertebrates from rare taxa were collected and
weighed after drying. Any tadpoles caught were wet-
weighed in the field after drip drying. During each
sampling visit, Secchi transparency was measured at the
deepest parts of the ponds. The two sampling sessions
spanned the time period used to establish numbers of
breeding birds (Ranoszek 1983; Koskimies and Väisänen
1991), and since data collected at 2-week intervals from a
smaller subset of ponds indicated that the variables
measured (amphibian and macroinvertebrate abundance,
water transparency) either remained stable or showed
monotonic increase over late April–end of June (M.
Nieoczym and J. Kloskowski, unpublished data), we used
averages of the two catches/measurements in the analyses,
on the assumption that they represented the variability
between the ponds over the study period.
During the June–July 2002 sampling sessions, water
chemistry data (electrical conductivity, pH, concentrations of
dissolved oxygen, organic carbon, ammonia nitrogen NH
4
-N,
nitrate nitrogen NO
3
-N, and available phosphate PO
4
-P)
were sampled (see Kloskowski 2009 for a detailed descrip-
tion of the methods). However, in the preliminary analyses
(see “Data analysis”section), which included only the 2002
data, none of the chemical variables had a significant effect
on the composition of bird assemblages or on individual
species. Therefore, the analyses were conducted on data
from both 2002 and 2004, omitting the chemical variables.
Emergent vegetation cover and the shoreline develop-
ment index (Lind 1985) were determined by digitization
from groundproofed (a planimeter was used) aerial photos.
To describe the surrounding landscape characteristics for
each pond, we estimated the proportion of the shoreline
adjacent to urbanized habitat, to forest patches, to arable
fields/pasture, and to other ponds. We restricted the
landscape scale to a ca. 20–30 m buffer because all study
sites were situated in agricultural landscape, with small
patches of woodland (see Table 1for a complete list of
variables collected in both 2002 and 2004).
Data analysis
Canonical correspondence analysis (CCA; CANOCO 4.5;
ter Braak and Šmilauer 2002) was used to determine the
variables that best predicted the composition of the pond-
breeding bird community. CCA is a direct gradient analysis
that iteratively develops an ordination of species and
sampling sites, combined with multiple regression on a
series of environmental gradients. A set of environmental
variables is reduced to a few orthogonal axes as composite
environmental gradients structuring species distribution
patterns. The significance of the relation of each environ-
mental variable to the bird data was determined by the
magnitude of the additional variation the variable explained
(“conditional effects”). Stepwise forward selection was
used to include significant variables (P<0.05) in the model.
The significance of the first canonical axis and of all
canonical axes together was tested by the distribution-free
Monte Carlo simulation (999 permutations). Multicollinear-
ity of the habitat variables was not excessive (variance
inflation factor (VIF) <7; VIF range for variables chosen by
the stepwise forward procedure 1.16–2.32). To partial out
the effects of the year of sampling and study locations
(pond complexes) from the model, they were included in
the ordination as categorical (dummy) covariables. When a
pond was sampled in both study years, we randomly
selected 1 year to be excluded from the model.
Although CCA provides information on the habitat
associations of individual species, its main goal is to
determine the relative effects of environmental variables
on the bird community as a whole. Therefore, generalized
linear mixed models (GLMMs) with Poisson distribution
and logarithmic link (GenStat v. 11.0) were used to identify
the habitat conditions most important in determining the
densities of individual bird species and bird species
richness (the number of avian taxa recorded per pond) at
the ponds. For bitterns, mute swan, little crake, and water
rail, typically represented by no more than one breeding
pair (calling individual) per pond due either to strong
territorial behavior or to relatively low overall abundance,
we considered presence/absence data in binomial models
with logit link to be more appropriate. Also, in two species
that are known to be involved in strong agonistic
interactions with sympatric larger-bodied species, interspe-
cific interactions were considered: great crested grebe
presence was added to the models of red-necked grebe
densities as an explanatory categorical variable and coot
presence to the models of moorhen (Cramp 1985; Fjeldså
2004). The other advantage of the GLMMs was that data
from all ponds surveyed in 2002 and 2004 were used,
including ponds sampled twice. With regard to the close
proximity distribution of the ponds clustered in pond
complexes, we assumed spatial autocorrelation between
data points from the same pond complexes. Therefore, the
random model included year and pond identity nested
within pond complex to account for lack of temporal and
spatial independence of observations. We used a step-down
procedure to select the final models. Starting with a full
676 Naturwissenschaften (2010) 97:673–682
model, the densities of each species were analyzed
including all variables used in the CCA as main effects
and two-way interactions. A quadratic term (fish age
squared) was added to account for potential nonlinear
effects of the fish age gradient. To prevent multicollinearity,
the quadratic term was centered by subtracting the mean of
the variable from each case's value before squaring it. We
used a correlation matrix to test candidate variables for
multicollinearity, and significance of predictor variables
with pair-wise correlation coefficients >0.3 was tested in
our models omitting the correlated variable, i.e., alternative
models were constructed. We progressively simplified the
model by eliminating first interactions and then main terms
that were the furthest from statistical significance. To verify
that significant terms had not been wrongly excluded, each
dropped term was then refitted to the minimal model. Wald
tests were used to assess significance of fixed terms. Fish
age was fitted as a continuous variable in the models;
however, for presentation of the observed patterns, carp age
classes were treated as a nominal term with three levels so
that means and SE could be calculated.
We did not apply the Bonferroni correction when multiple
tests on different response variables (species) addressed the
same hypothesis (Moran 2003). Data were log (x+1) or
arcsin-transformed to improve normality before GLMM
analyses. Data were not transformed for CCA.
Results
The five environmental variables included by the CCA
forward selection as best differentiating habitat preferences
of waterbirds were macroinvertebrate abundance (condi-
tional importance λ
a
=0.12, F=5.17, P=0.002), fish age (as
an ordinal trend; λ
a
=0.11, F=4.78, P=0.002), fish biomass
(λ
a
=0.10, F=4.47, P=0.008), amphibian abundance (λ
a
=
0.06, F=3.25, P=0.014), and emergent vegetation cover
(λ
a
=0.08, F=4.12, P=0.002; Fig. 1). Permutation tests on
the trace value (0.703; F=3.219, P=0.001) and on the value
of axis 1 (eigenvalue=0.234; F=8.95, P=0.001) indicated
that the variables included in the model explained a
significant amount of the variation in the species data. Of
the variables selected by the CCA models, significant
correlations (at P<0.05) were found between fish age and
biomass (r=0.6353); both these variables were negatively
related to macroinvertebrate abundance in activity traps
(r=−0.2408 and r=−0.2707). Abundance of larval amphib-
ians was negatively correlated with fish age (r=−0.2265;
GLMM means of relative amphibian abundance in ponds
with different-aged carp are presented in Table 2), but
the relationship with fish biomass was not significant
(r=−0.1580). Also, amphibian abundance was associated
with emergent vegetation (r=0.2994).
The inertia in the species data after fitting the covariables
was 1.776. Of this, the first axis explained 12% and the
second axis 6.3%. The canonical eigenvalues accounted
together for 26.6% of the total variance. Correlation
coefficients indicated that axis 1 of the CCA reflected
trends across richly vegetated habitats (r=−0.5783) to open
water habitats and those of increasing aquatic macro-
invertebrate abundance (r=0.5944). Axis 2 was largely
defined by the gradient of fish age (r=0.7272) and fish
biomass (r=0.8889).
Individual ordination scores for bird species indicated
that breeding habitat was selected with regard to food
(macroinvertebrate or amphibian abundance, fish age, total
fish biomass) and/or the proportion of emergent vegetation
cover (Fig. 1). Tufted duck (r=0.4942, P< 0.001) and
mallard (r=0.3266, P<0.005) densities were most strongly
correlated with macroinvertebrate relative abundance. The
direction of the environmental vectors revealed that the
presence of larger fish was negatively correlated with larval
amphibian densities. Little grebe densities that correlated
best with amphibian abundance (r=0.3772, P< 0.001) were
also negatively associated with fish age (r=−0.4337, P<
0.001) and fish biomass (r=−0.3164, P<0.004). Great
bittern and rallids (except moorhen) were associated with
abundant emergent vegetation (r≥0.34, all P<0.003). The
most common species in terms of overall occurrence,
mallard (overall pond occupancy 89.4%) and coot
(87.1%), but also mute swan (38.8%), tended to be
clustered around the origin of the ordination, i.e., they
were the most habitat generalist species.
Fig. 1 Results of CCA on avian communities and environmental
variables in 74 carp ponds sampled in 2002 and 2004
Naturwissenschaften (2010) 97:673–682 677
Although some associations determined by CCA were
not detected by the GLMMs, the GLMMs confirmed that
habitat selection by individual species was typically
influenced by either a food-related variable (most frequent-
ly the age of the fish in the pond; Fig. 2) or emergent
vegetation cover (Table 3). Little grebe was the only species
whose habitat selection depended on both fish age and the
vegetation cover of the pond. In the case of grebes, little
grebe preferred ponds with the youngest cohorts, red-
necked grebe occurred in both 0+ and 1+ but was absent
from 2+ ponds, and great crested grebe achieved the
relatively highest breeding densities on 1+ ponds (Table 3;
Fig. 2). No species was found to be positively associated
with 2+ fish. Total fish biomass was correlated with carp
age, but when included in the null models omitting carp
age, it was positively related only to the densities of great
crested grebe and pochard (Table 3). Pond area and water
transparency were not selected by the CCA procedure (λ
a
<
0.06, both P>0.1) but were found significant for individual
distribution patterns of some species by the GLMM. Water
transparency was positively related to densities of coot, red-
necked grebe, and great crested grebe. As indicated by the
CCA correlation matrix, Secchi depth decreased with
increasing fish age and total biomass (r=−0.2969 and
r=−0.3034; Table 2). Also, GLMMs demonstrated the
potential importance of interspecific interactions within
waterbird guilds: Densities of red-necked grebe were
positively related to great crested grebe presence, while
moorhen showed a negative association with coot (Table 3).
Total species richness was negatively related to fish age
(Wald χ
2
=4.42, df=1, P=0.0239) and positively correlated
with pond size and the proportion of emergent vegetation
(χ
2
≥17.0, df=1, both P<0.001).
Discussion
Our results show that waterbirds used two types of general
cues for breeding habitat selection and two groups of
species could be distinguished accordingly, although the
suites of preferred habitat attributes overlapped between the
groups. Densities of grebes and ducks were related to food
availability (fish age and density, invertebrate or amphibian
abundance; cf. Nummi et al. 1994; Haas et al. 2007).
Bitterns and rallids were positively related to the amount of
emergent vegetation, which might function both as shelter
from predators and as a specific feeding habitat for some
species (Jenkins and Ormerod 2002; Gilbert et al. 2003),
while they were generally not correlated with the size
structure of the fish community. The species studied have
varying ability to move their young to another pond
Fig. 2 Breeding densities (pairs or calling males per 10 ha) of grebes,
ducks (a), bitterns, and rallids (b) in carp ponds stocked with different
age cohorts. 0+= young-of-the-year carp, 1+ = 1-year-old carp, 2+ = 2-
year-old carp. GLMM predicted means (+SE) are shown. Note that
GLMM statistics on bitterns and some rallids presented in Table 3are
derived from binomial models using species presence/absence data
(see text for more details). Superscripts denote significant differences.
Garganey was omitted because of its rare occurrence at ponds
Table 2 Effects of fish age/size structure on variables related to food availability for waterbirds (GLMM, normal error and identity link function)
Mean (SE) Wald χ
2
(df=2) P
0+ ponds
(N=37)
1+ ponds
(N=22)
2+ ponds
(N=15)
Amphibian abundance (g/1 trap; wet weight) 9.69
a
(2.76) 1.06
b
(0.61) 0.21
b
(0.15) 6.16 0.050
Macroinvertebrate abundance (mg/1 trap; dry weight) 0.78
a
(0.12) 0.33
b
(0.07) 0.27
b
(0.07) 14.47 <0.001
Water transparency (cm) 125.7
a
(5.6) 92.5
b
(7.2) 77.8
b
(6.6) 10.58 0.007
Unlike superscripts denote significant differences (2 standard errors of the difference=95% confidence limits)
678 Naturwissenschaften (2010) 97:673–682
(reviewed in Elmberg et al. 1994); however, we assume that
even in the “mobile”species (particularly dabbling ducks)
the choice of nesting habitat is critical for breeding success
because chick mortality is the highest in the early
posthatching period when moving the brood seems most
risky (Hill et al. 1987; reviewed by Sargeant and Raveling
1992). In great crested grebe and red-necked grebe, the
preference for the early flooded ponds is probably related to
grebes’inability to walk (Fjeldså 2004). After settling on
ponds that are already filled, the early breeders cannot
choose a different territory until the young have fledged,
unless the clutch/brood fails.
The age/size of carp in the ponds significantly influenced
densities of macroinvertebrates and larval amphibians.
Nonfish prey of waterfowl can be heavily suppressed by
fish predation (Eriksson 1979; Mallory et al. 1994). These
effects may substantially depend on individual fish size due
to fish capability of foraging on progressively larger prey
over ontogeny (Persson 1988; Penttinen and Holopainen
1992). The size-dependent potential for predation on or
competition with fish was apparently decisive for habitat
choice in the “grebe-duck”assemblage. Young ducks and
little and red-necked grebes feed heavily on macroinverte-
brates and larval amphibians (Bandorf 1970; Hill et al.
1987; Kloskowski 2004). Therefore, breeding birds may
avoid resource competition by shunning ponds with large-
sized fish. The affinity to emergent vegetation among
grebes was in inverse order to body size. Little grebe and
red-necked grebe are well adapted for foraging both on
open water and within emergent vegetation (Bandorf 1970;
Table 3 GLMMs (fixed part) for the estimated breeding densities or presence/absence of individual species and avian species richness at the
ponds
Species Effect Estimate ± SE Wald χ
2
(df=1) P
Little grebe Fish age −0.748± 0.274 7.46 0.008
Emergent vegetation 3.265± 1.088 9.00 0.005
Amphibian abundance 0.436±0.203 4.60 0.036
Great crested grebe Pond area 0.965±0.299 10.44 0.002
Water transparency 0.986± 0.355 7.69 0.007
Fish squared age −1.468±0.341 18.56 <0.001
Pond permanence 1.276± 0.528 5.85 0.018
Fish biomass 0.195± 0.046 18.04 <0.001
Red-necked grebe Fish age −0.614±0.296 4.28 0.038
Water transparency 0.719± 0.373 3.74 0.05
Pond permanence 4.906± 1.494 8.48 0.004
Great crested grebe presence 1.616 ± 0.536 9.09 0.003
Little bitern Emergent vegetation 3.396± 1.501 5.12 0.027
Great bittern Emergent vegetation 5.500± 1.530 12.92 0.001
Pond area 1.374±0.435 9.95 0.003
Mute swan Pond area 0.678± 0.228 8.85 0.005
Mallard Fish age −0.344± 0.153 5.09 0.027
Pochard Fish age −0.644± 0.217 8.82 0.003
Tufted duck Fish age −0.781±0.309 6.38 0.013
Fish biomass −0.142±0.059 5.87 0.015
Water rail Emergent vegetation 12.090 ± 3.061 15.61 <0.001
Pond area 2.940±0.838 12.31 0.001
Little crake Emergent vegetation 8.477 ± 3.115 7.41 0.009
Pond area 2.062±0.888 5.39 0.024
Moorhen Shoreline development 1.920 ± 0.577 11.07 0.001
Coot presence −1.352± 0.463 8.54 0.005
Coot Water transparency 0.986± 0.211 8.68 0.004
Emergent vegetation 2.263± 1.065 4.52 0.037
Amphibian abundance 0.620 ± 0.120 5.97 0.017
Garganey was omitted because it occurred in only 7% of the ponds. For the sake of brevity, the reduced models resulting from stepwise backward
dropping of insignificant terms are presented. Statistics and Pvalue of significant terms were taken from the minimal models; in great crested
grebe and tufted duck, they were obtained by entering each of the intercorrelated variables into separate models
Naturwissenschaften (2010) 97:673–682 679
Fjeldså 1982). Great crested grebes may be the least
dependent on emergent vegetation as they pursue prey
while diving in open water and nest even in very sparsely
vegetated places (Fjeldså 2004). Females of the duck
species studied can nest on pond shores or in sparse
vegetation stands and thus rely more on food abundance in
selecting a breeding habitat (see also Giles 1994; Nummi et
al. 1994). Total fish biomass was an important factor
structuring the avian community as a whole, but when
individual patterns of species distribution were analyzed, it
was associated only with great crested grebe and tufted
duck densities. The effects of fish size and total biomass are
difficult to separate in age-structured carp ponds because in
spring, the biomass of young-of-the-year fish, even when
stocked at high numerical densities, is naturally lower than
that of older stocks. Since exceeding a critical density
threshold is a prerequisite of carp impact on aquatic
community (Zambrano et al. 2001; Bajer et al. 2009),
density-dependent effects cannot be neglected. However,
notwithstanding that 1+ and 2+ fish were stocked at similar
levels of total biomass, densities of some bird species
differed significantly between 1+ and 2+ ponds, indicating
that the effect of carp size structure on these species was
stronger than that of density.
Benthivorous fish such as carp can impact birds by
elevating turbidity levels and disturbing submerged vege-
tation, which at high fish density induces an ecosystem shift
to a macrophyte-poor turbid state (Crivelli 1983; Lammens
1999; Zambrano et al. 2001). These effects may be related
to fish body size as well. Larger-sized benthivorous carp are
capable of digging deeper in a substratum (Lammens and
Hoogenboezem 1991) and create more turbidity via
sediment and phosphorus suspension than small fish
(Driver et al. 2005). The loss of macrophytes adversely
affects the density of waterfowl foraging on vegetation and its
associated invertebrates (cf. Hargeby et al. 1994). Elevated
turbidity levels restrict the foraging efficiency of visually
hunting avian predators (Cezilly 1992; Brenninkmeijer et al.
2002). However, even in the 2+ ponds (i.e., the ponds
holding the oldest and largest fish), the average Secchi depth
was still far from the estimated lower acceptable limit of ca.
40 cm for efficient great crested grebe predation on fish (van
Eerden et al. 1993). The negative effects of fish on
vegetation and water clarity can be delayed until summer
(cf. Meijer et al. 1990;Haasetal.2007), and breeding
waterbirds may not be seriously affected, at least during the
early breeding period. In carp ponds, the delay can be
explained by low water temperature and reduced fish feeding
activity in spring (Penttinen and Holopainen 1992; Richardson
and Whoriskey 1992). We observed blue-green algae blooms
in ≥1+ ponds only at the end of July and in August. Therefore,
we suggest that the negative effects of carp on waterbirds were
mainly driven by competition for food. Consequently, fish
species that feed in the water column and are capable of
attaining body size that allows exploitation of resources used
by waterfowl may have no less potential to influence habitat
suitability for birds than benthivorous fish (Eriksson 1979;
Hill et al. 1987).
Bitterns and rallids rely at least in large part on animal
diet, especially in the prefledging period, but only coot,
being the single species that commonly acquires prey by
diving (Cramp 1985), showed association with indices of
food availability. However, our trapping method is likely to
assess abundance of epibenthic and nektonic prey in open
water habitats or open water interspersed with emergent
vegetation stands, while some of the bird species dwelling
in emergent vegetation are adapted for gleaning prey from
emergent plants or gathering food on dry sites (Cramp
1985; Jenkins and Ormerod 2002). The piscivorous great
bittern is a food opportunist that forages chiefly within
dense stands of vegetation (Gilbert et al. 2003) and in pond
conditions takes small wild-grown fish rather than carp
(Polak 2007); thus, it may be independent of carp size
structure. Among rallids, only moorhen was not related to
emergent vegetation, but its distribution may be governed
by agonistic competition with the more dominant coot.
Moorhen is also strongly associated with terrestrial habitats
around the breeding pond (Cramp 1985).
To sum up, fish individual size and factors which interact
with size structure of fish populations, such as macro-
invertebrate and amphibian abundance, water transparency,
and pond permanence (Penttinen and Holopainen 1992;
Driver et al. 2005), can play an important role in shaping
distribution patterns of a significant part of the waterbird
community, while avian guilds strongly associated with
emergent vegetation were little responsive to variability in
both fish size and density. Size structure of fish populations
can also better explain niche diversification between some
bird species than the fish presence/absence dichotomy.
Waterfowl susceptible to competition from fish benefit from
avoiding water bodies containing fish (Eriksson 1979; Giles
1994), and our data suggest that ducks tend to avoid ponds
with larger fish in particular, presumably because they are
more effective competitors than small fish. Small- and
medium-sized piscivorous birds may prefer waters with rich
populations of small-bodied fish over both habitats without
fish and those dominated by large fish, i.e., invulnerable to
predation (Allen et al. 2007; but see Paszkowski and Tonn
2000). Larger-bodied piscivorous species, like great crested
grebe in the present study, are likely to select water bodies
with bigger fish, attempting to align their size-limited
predatory capacity with the better energetic return and
other advantages of larger prey (Moser 1986; van Eerden et
al. 1993; Paszkowski and Tonn 2000). In conditions of
distinct fish size structure, e.g., in northern temperate
shallow water bodies, where fish populations are regularly
680 Naturwissenschaften (2010) 97:673–682
structured by winter hypoxia or drought years (Tonn and
Magnuson 1982; Holopainen and Hyvarinen 1985; Allen et
al. 2007), individual fish size can be more significant than
fish density for avian community composition. However, it
should be recognized that the interplay between relative
densities of fish size cohorts may be foremost in importance
in more speciose assemblages with a mixture of size classes.
From a management perspective, large, heavily vegetat-
ed water bodies with small-bodied fish populations are
likely to host the highest number of avian species (Elmberg
et al. 1994; Weller 1999; Paszkowski and Tonn 2000).
Habitats managed for breeding ducks and the smaller grebe
species should harbor only small-bodied (young) fish or
remain fishless (see also Giles 1994). However, water
bodies dominated by populations of large-bodied fish may
support relatively high avian species richness as well,
provided that a considerable emergent vegetation cover is
preserved. Management of habitats with size-structured fish
communities can be specified to target selected bird species,
e.g., by omitting piscivorous species at fisheries, to accom-
modate both wildlife conservation and economic interests.
Acknowledgments We are grateful to the fish farmers (M. Filipiak,
J. Orzepowski, and M. Sagan) for their help and for regular access to
the ponds. Comments from three anonymous referees greatly
improved the manuscript. This research was funded by grants from
the State Committee for Scientific Research (KBN 6 PO4F 066 20 and
3 PO4F 036 23).
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