Breeding bird dynamics in a primaeval temperate forest: long

ECOGRAPHY 20: 432-453. Copenhagen 1997
Breeding bird dynamics in a primaeval temperate forest: long-term
trends in Biatowieza National Park (Poland)
Tomasz Wesoiowskj and Ludwik TomiaJojc
Wesolowski, T and Tomialojc, L 1997 Breeding bird dynamics in a pnmaevdl
temperate forest long-term trends in Bialowieza National Park (Poland) - Ecography
20 432-453
Numencdl vanation of the breeding bird community, its ecological subunits (guilds)
and the 26 most numerous constituent species is analysed over 20 yr penod
(1975-1994), and related to vanation m supply of defoliating caterpillars, tree seed
crop, numbers of rodents and winter weather Maximum rates of increase between two
years were less than twofold in most species Changes in numbers of individual
species/guilds were either independent of each other or in parallel The pattern of
numencal vanation was not related to taxonomic affinities, type of nest site, food
types, or migratory habits Whole bird community and 13 of 26 species showed
long-term increasing trends, only three species dechned Numbers remained basically
stable dunng the first decade, increases were concentrated to the second decade Except
tropical migrants (no long-term change) other migratory groups increased in numbers
None of the measured environmental vanables showed parallel trends, which could
account for the recorded trends Long-term trends and year-to-year fluctuations were
not correlated The short-term vanation in bird numbers was to some extent correlated
with (in decreasing order of importance) abundance of defoliating caterpillars, winter
seventy, and changes in rodent numbers No correlation with tree seed crop was found
Overall, a substantial part of the vanation in breeding bird numbers could not be
explained by that set of factors This could be due to birds using wider spectrum of
food sources than those measured, varying predator pressure and/or strong influences
from outside the forest, swamping local relationships
T Wesolowski and L Tomialojc, Dept of Avian Ecology and Museum of Natural
History, Wroclaw Unw, Sienkiewicza 21, 50 335 Wroclaw, Poland
Temperate lowlatid forests of mainly deciduous character are expected to be a less vanable habitat type than
grasslands, tundra or taiga (Blondel 1979, Jarvmen
1979, Noon et al 1985). So if anywhere, it is in the
former habitat where one should expect to find that
animal communities are most numencally stable, possibly in eqtulibnum with their environment However, to
reveal the patterns of stabihty m temperate forests, and
the ecological processes operating to produce them,
thorough and long-term studies of bird communities
are necessary (Wiens 1984, 1989, Hohnes at al. 1986)
An additional requirement is that such studies should
be earned out under undisturbed natural conditions, in
places free of successional changes
The old-growth primaeval forest stands preserved in
Bialowieza National Park (BNP hereafter) offer such a
place They can be seen as "a window into the past",
since they offer an insight into the ecology of pnstine
temperate plant and animal communities (Falmski
1968, 1986, Wesolowski 1983. Tomialojc 1991,
Wesolowski and Tomi^ojc 1995) The data collected
here may, besides enhancing our understandmg of the
fundamental problems of commumty orgamsation, also
serve as a gauge for the bird community studies made
Accepted 27 January 1997
Copynght ® ECOGRAPHY 1997
ISSN 0906-7590
Pnnted m Ireland - all nghts reserved
432
ECXX3RAPHY 20-5 (1997)
in more transformed woodland habitats Gathenng
such, "control data" from areas least affected by human disturbance has become a goal of utmost importance due to global scale of anthropogenic changes in
the natural environment
For these reasons we launched m 1975 a long-term
program of ornithological studies in the BNP The
program was aimed at descnbing pattems of vanation
in breeding bird community in habitats free of direct
human influence, as well as at understanding the mechanisms of community dynamics Using earlier available
data sets of shorter duration, we have proposed some
tentative explanations (Tomialojc et al 1984, Tomiatojc
and Wesolowski 1990, 1994, Tomialojc 1993,
Wesolowski 1994, Wesoiowski and Tomialojc 1995)
Now, with a 20-yr senes of observations at hand, we
are able to provide more conclusive answers
When we started our studies in the mid-70's the
Unitarian "competitive" view of bird communities (as
equilibnal, stable, strongly interacting units), marshalled by MacArthur (1958) and his followers, prevailed Current views of animal community structure
are much more pluralistic (Mclntosh 1995) TTie equilibnal model IS seen rather as a special case, one end of
the continuum between the "competitive" and the "individualistic" The latter term refers to non-equUibnal
communities, made up of loosely-knitted sets of species,
changing numbers indef)endently of one another, and
responding in an individual manner to a varying array
of factors - see Wiens (1989) for review The problem
now IS not whether communities are "competitive" or
"individualistic", but rather of understanding how different processes interact in shaping the structure and
dynamics of communities
We begm this paper with documentation of numencal vanation of the whole breeding bird community.
Its ecological subunits (guilds) and the 26 most numerous species in the BNP dunng 1975-1994 We also
provide some data on annual vanation in food supply, predation pressure and winter seventy We continue by addressing some specific questions 1) What
IS the overall extent of numencal variation'' 2) What
are the maxmium rates of mcrease between years' 3)
Are changes m numbers of individual sp>ecies/guilds
independent of each other'' 4) Do closely related species, species with similar nest sites, food tyjjes, shanng
their migratory habits also have similar pattem of
numencal change'' 5) Are any long-term numencal
trends in bird numbers discemible'' 6) How smuiar are
the long-term trends among different guilds and co-occumng sjjecies'' 7) Do guilds/species which have similar
long-term trends also have sunilar short-temi fluctuations'' 8) Are trends or fluctuations in numbers dependent on vanation in availability of food Qeaf-eating
caterpillars, tree seeds), predator pressure or winter
seventy''
ECOGRAPHY 20-5 (1997)
Study area
The Bialowieza Forest complex (total area 1250 km^) is
situated on the Polish-Belarussian border Its westem
part (580 km") belongs to Poland The forest represents
a rehc remnant of the vast lowland forests, which once
covered large parts of Europe The majonty of tree
stands in the Polish part are now under management,
but a 47.5 km^ block of the best preserved pnmaeval
stands has been strictly protected within the Bialowieza
National Park (hereafter referred to as BNP - Falmski
1986, Tomialojc et al 1984, Tomialojc and Wesolowski
1990, 1996)
The climate is subcontinental mean annual precipitation 624 (426-857) mm, long-term average annual temperature -f6 6°C, with an average -1-17 6° in July and
- 4 3° in January Snow cover (usually ca 0 5 m) lasts
up to 92 days, moming ground-frosts occur as late as
mid-May, dunng the 197O's even to mid-June Snow
melts between ca 10 March (early spnng) and 20 Apnl
(exceptionally late) See Falmski (1968, 1986), Okarma
et al (1995) for more information
The old-growth stands preserved in BNP are distinguished from those m other temperate forests by the
following features they are multi-stoned, mixed-species, uneven-aged, composed of trees reachmg unusual
heights (the tallest spruces reach 57 m, several other
species 42-45 m) and contam large amount of dead
timber and uprooted trees Upland deciduous woods of
oak-hme-hombeam Tilio-Carpinetum tyjse (44 4%),
swampy deciduous (21 6%) and coniferous stands
(28 1%) cover the majonty of BNP area Detailed descnptions of the habitats and plots studied in BNP are
given m Tomialojc et al (1984) and Tomialojc and
Wesolowski (1990, 1994, 1996), Wesolowski and Tomiatojc (1995).
Material and methods
Bird numbers
The numbers of birds m the breeding season were
estimated using a modified spot-mapping technique,
"combined mapping " (Tomialojc 1980), the method
producing near-absolute estimates of numbers for the
majonty of species (Tomialojc 1980, Tomialojc et al
1984, Tomialojc and Wesolowski 1994, 1996,
Wesolowski and Stawarczyk 1991) Largely the same
team of people earned out censuses durmg the whole
study penod, and interpretations of species maps and
estimates of species numbers were always made by the
same persons
The data were collected within piermanent census
plots, 24-33 ha in size In 1975-1979 their number
vaned, from 9 to 14 plots (jomt area 236-358 ha) were
censused a year In 1980, after checkmg that year-to433
year changes in bird numbers in different plots run m
parallel (Tomiatojc et al 1984), a smaller subset of
tbose plots had been chosen for monitonng Thus, in
1980-1994, only a constant set of seven plots Oomt
area 187 ha) was used Six of those plots were also
censused every year m 1975-1979, while the seventh
was censused 1976-1977 and not m 1975 and 19781979
Tbe plots were situated in three main types of mature
tree stands occumng in the BNP, l e swampy deciduous, oak-hornbeam and coniferous stand types The
proportion of habitat types within tbe study plots corresponded to those found in the BNP and remained
stable dunng the whole study penod Initial data on
number of pairs of individual species breeding in particular plots in consecutive years are given in Tomialojc et
al (1984) Tomialojc and Wesolowski (1994, 1996)
As we were interested in year-to-year changes in the
BNP (and not so much in vanation among individual
patches) it was necessary to produce a single figure
reflecting ntimbers of a species (or guild) in tbe BNP m
a given season Tbe areas censused in each year, though
overlapping to large extent, were not identical, thus, we
could not simply add up numbers of pairs recorded in
individual plots within a season and compare them
among years Therefore, to find a common denominator, we calculated indices of yearly abundance for individual species and guilds This was done as follows
numbers of breeding temtories of a species recorded in
all plots censused in a compared year were summed
The same was done for ntimbers of temtones found in
the same set of plots in tbe base year (1977) Then the
index of abundance was finally achieved by dividmg the
stom of temtories m the compared year by the 1977
sum, and expressed as a percentage of the 1977 value
The index for 1977 was always taken as 100% However, due to varying number of plots used in individual
compansons, tbe absolute value of tbe figure treated as
100% was vanable We chose 1977 as a base of calculations as It was the only year m which all plots were
censused smiultaneously.
To avoid problems with excessive vanability of small
samples due to sampling errors the indices were calculated only for more numerous species, l e those breeding in each season and represented by 10 or more
breeding pairs in all the plots in a season Due to these
restnctions, of 81 species found breedmg m study plots
at least one year the indices could be produced only for
the 26 most numerous ones However, they numencally
made up over 80% of the BNP breedmg bird cotnmunity (Tomialoj6 and Wesolowski 1990, 1996)
Apart from species-sp)ecific mdices, we also calculated
indices for groups (guilds) of birds with common feeding, nesting or migratory habits, as well as for the
whole breeding bird community. In those calculations
we took mto account data on all breeding species,
irrespectively of their abundance. Subsequently to To434
mialojc et al (1984), we distinguished the followmg
groups Foraging - hierarchical classification - birds
foraging outside forest (independently of typ)e of food
taken - O) versus within-forest foragers, predators
(hunting mainly vertebrates - P), vegetanans (including
seed eaters - V), and "msectivores", the last group was
subdivided into ground-feeders (IG), bark-feeders (IB)
and crown-feeders (IC) Nesting - three groups reflecting increasing nest vulnerability grotmd (on tbe ground
or in low vegetation up to 1-1 5 m above the ground G), crown (open or domed nests in high bushes or in
trees - C), hole (H) There were no nest-boxes in our
plots, and hole-nesting birds nested entirely in natural
cavities - Migration - four groups tropical (winter
south of Sahara - T), sbort-distance (winter mainly in
SW Europe and in tbe Mediterranean basm - S),
resident (winter outside the forest itself but still within
the same geographic and clunatic region, also nomadic
species - R), forest resident (stay whole year in their
breeding habitats - RF)
The guilds consist of 8 (IB) to 37 (IL) species Full
list of allocations of individual species to partictilar
guilds IS given in Tomialojc and Wesolowski (1990)
Here we followed those earlier allocations in all but two
cases, namely Sylvia atrtcapilla (formerly short-distance) was moved to the tropical category, whereas
Coccothraustes coctothraustes (formerly resident) was
displaced to the short-distance group, in light of recent
information
To calculate an mdex value for an individual guild in
a single season we summed up tbe total number of pairs
of all species ranked with this group recorded breeding
in all plots censused m that year and compared them
with their number in the same plot in 1977 In cases of
species included simultaneously in more than one guild
(Tomialojc and Wesolowski 1990), we parted their
numbers and included them proportionally to different
categones For example, as Parus major is classified as
half ground lnsectivore and half crown insectivore (Toimalojc and Wesolowski 1990), thus, the total number
of pairs of this species recorded in a given season was
divided by two and one half was included into IG and
other half mto IL foraging guilds Because of too small
sample size (see above) the index for the predator (P)
guild could not be calculated
Environmental variables
Wtnter severtty
Meteorological data were denved from the local
weather station in Bialowieza village, sittiated m the
centre of Bialowieza Forest complex, < 1 km from S
edge of the BNP (Wesolowski and Stawarczyk 1991,
unpubl.). To charactense winter conditions, we tised the
mean temperature m the penod December-March, because It had been shown earlier (Wesolowski 1994) that.
ECXX3RAPHY 20 5 (1997)
due to very strong lntercorrelation between different
weather factors (number of days with snow, minimum
temperatures, temperatures of the coldest months) a
single vanable was sufficient to descnbe winter seventy
in Bialowieza
as well as for hombeam and Norway spruce seeds and
caterpillars and rodents
Results
Seed abundance
Information on amount of hombeam Carptnw, betulus
and Norway spruce Picea abies seeds was from Pucek
et al (1993) Hombeam seeds were counted on photos
of the forest floor taken every year in late October and
early November in the oak-hombeam stands (data for
hombeam and maple Acer platanoides), while spruce
seed data were from forestry sources Abundance of
hombeam seeds did not correlate with that of Norway
spruce, but it was highly synchronised with those of
oak Quercus robur and maple (Pucek et dl 1993)
Therefore the hombeam crop alone could be used to
reflect seed abundance of deciduous trees in general m
the BNP
Caterpillars
Leaf-eating caterpillars (mostly Geometndae and some
Tortncidae) were counted once each season, in May,
depending on the stage of leaf development Each time
50-120 standard twigs (0 25 m-) from the lower parts
of the hombeam undercanopy were searched and the
caterpillars counted (Tomialojc et al 1984, Tomialojc
and Wesolowski 1994, 1996) Onginal values of the
caterpillar index are given m Wesolowski and Stawarczyk (1991)
Rodents
Indices of spnng numbers of rodents were taken from
Pucek et al (1993) and Jgdrzejewski et al (1996) They
show combined numbers of Clethrionomys glareolus
and Apodemus silvaticus caught per 100 trapnights in
permanent plots in spnng (Apnl/May) We used the
vanation in rodent numbers to express changes in
predator pressure, as the rodents themselves were important nest predators (Piotrowska and Wesolowski
1989, Tomialojc 1994), and changes in rodent numbers led to functional and numerical responses in
several middle-sized predators important for birds
(J?drzejewski et al 1993, 1995, 1996, Zalewski et al
1995)
Statistical analysis
All procedures used followed the formulas given in
STATISTICA for Wmdows (Anon 1996) Before running parametnc statistical procedures all vanables had
been checked for normahty and, when necessary, logtransformed to improve the fit This was done for
Carduelts spmus, Ficedula albicollts, Sturnus vulgaris,
Parus caeruleus, and the birds foraging outside forest.
ECOGRAPHY 20-5 (1997)
Amplitude of fluctuations
Taken as a whole the breeding bird community of the
BNP remained relatively stable dunng the whole 20-yr
period (Fig 1) The highest numbers of birds recorded
exceeded the minimum numbers by ca 44%, and the
maximum increase between the two successive seasons
amounted to only 13% (Table 1) Similarly, in the
majonty of guilds, difference between the extreme years
was less than two-fold Only the two resident groups,
bark insectivores (composed of residents) and birds
foraging outside woods showed greater range of vanability, with over twofold differences between the extremes (Table 1) More differentiation was apparent at
the individual species level Carduelts spmus, which
became nearly absent m 1988 (Fig 2), was the most
variable species in the sample, its numbers changing by
more than three orders of magnitude (Table 2) Other
unstable sf)ecies were P sibilatrix and A trwtalts (Fig
2), population maxima of which exceeded minima by
factors of 18 3 and 8 5, respectively Except for these
species, a remarkable stability was recorded - in six
sjjecies, highest numbers did not exceed the lowest by
more than two-fold and in eight additional species the
difference was less than three-fold (Table 2) Population
vanability was not related to taxonomic affinities, for
congenenc species (e g Phylloscopus warblers, woodpeckers) could be found on opposite sides of the stability gradient (Table 2) It was not also hnked to type of
nest site (Kruskall-Wallis ANOVA by ranks, p = 0.35,
NS) but It decreased with increasing population size,
standard deviations of population indices of individual
species were negatively correlated with the number of
pairs in the base year (r, = —0.53, p < 0 01) There was
as well some relationship to wintenng sites, with shortdistance migrants being the least vanable group
(Kruskall-Wallis ANOVA by ranks, with both categories of residents treated as a single group, H = 10.0,
p < 0 01) This relationship remained significant even
after removal of, the possibly distorting, extreme value
of C .spmus (H = 9 4, p < 0 01)
Large differences between the highest and lowest
population level could have ansen either by long-term
directional change in population size, taking place in
small increments (l e low year-to-year vanability) or it
could be the result of high year-to-year numencal variabihty Compansons of the maximum rate of increase
with the max/min ratios (Table 2) revealed that the two
vanables were highly sigmficantly correlated (r, = 0 87,
p < 0 0001), thus the overall high vanabihty was to a
large extent accounted for by high rates of population
435
140
' WHOLE COMM
GROUND NEST
140
-o- TROPICAL
-o- SHORT-DIST
100
60'
1975
1980
1985
1990
1995
60
1975
1980
1985
1990
1995
1980
1985
1990
1995
1985
1990
1995
180
140
140
100
100
1976
1980
1995
1985
180
1975
160
- OL/TSIDE FOR
• VEGETARIAN
- BARK INSECT
GROUND INSECT
140
120
1990
1980
436
1985
1980
1995
1995
1975
1980
Fig 1 Patterns of
year-to-year vanation in the
percentage indices of
abundance of the whole bird
community and of
individual guilds m the
BNP, 1975-1994
Procedures used m
calculating numencal indices
are given in Matenal and
methods Full names of
guilds along with the
minimum number of pairs
constitutmg 100% in 1977
are given in Table 1 Slopes
of regressions lines along
with their significance levels
are given m Table 3
ECOGRAPHY 20-5 (1997)
Table 1 Minimum number of pairs of birds constituting 100% in 1977 (base year m calculation of indices), mean and standard
deviations of numencal indices, ratios of highest to lowest indices' values, and maximum rates of increase between the two
consecutive years (max N,+ ,/N,, where N = index value) for individual guilds and the total breeding bird community of
Biatowieza NaUonal Park in 1975-1994 Procedures used m calculating numencal indices are given in Material and methods
Ecological group
N pairs
Index
Ratio
Mean
SD
Max/mm
Max incr
Foraging
Forage outside forest (O)
Vegetarians (V)
Ground insectivores (IG)
Bark insectivores (IB)
Crown insectivores (IL)
58 7
107 9
340 6
76 2
596 3
71 6
1115
1109
120 7
1116
23 8
160
11 5
23 6
137
3 25
1 66
1 45
2 14
1 55
1 32
1 31
1 15
148
1 19
Nesting
Ground nesters (G)
Crown nesters (C)
Hole nesters (H)
344 7
470 7
362 1
102 4
117 1
108 8
133
14 2
18 1
61
49
76
1 33
120
121
Migration
Tropical migrants (T)
Short-distance migrants (S)
Resident in region (R)
True forest residents (RF)
304 5
637 2
129 5
1138
100 6
110 1
121 9
121 6
136
11 9
30 5
24 7
71
48
2 63
2 37
132
1 18
143
I 47
11850
109 9
11 5
144
1 13
All birds
change between the consecutive seasons The largest
increases between the two seasons were observed in
C spmus (over 130 x ) and F sibtlatrix (over 11 x )
and SIX further species sometimes more than doubled
their numbers from one year to the next (Table 2)
Similarities of numerical variation among species
To check how overall patterns of numencal vanation
of individual species were related to each other we
calculated correlation coefficients for every pair-wise
combmation of species and used them m turn to construct a dendrogram of similanties among species
The dendrogram was drawn using the complete linkage algorithm, according to which the distance between two clusters is determined by the distance of
the two furthest neighbours As can be seen in Fig 3,
patterns of numencal vanation were not strongly dependent on taxonomic affinities Though in some of
the genera (e.g Farus, Fhylloscopus) spwcies showed
similar patterns of numencal change, yet m others
(e.g woodpeckers, Ftcedula) numbers vaned independently However, only in one pair of congeners
were the numbers significantly negatively related
F albicoUts-F parva, r = —0.62
The matnx of correspondence contained 325 correlation coefficients Even if changes in numbers of different species were totally independent of each other,
with that number of compansons and a level set at
0.05, one would expect to obtain 16 significant results, half of which positive and half negative Twelve
significant negative coefficients recorded did not significantly exceed the chance level (x^-test) Moreover,
the negauve correlations, with the above menUoned
ECOGRAPHV 20-5 (1997)
exception, occurred between pairs of spyecies with so
different requirements (eg C sptnus~T tioglodytes.
S europaea-A trwtalts, F coelebs-S vulgarts) that
one would hardly expect them to strongly interact
On the other hand, positive values (N = 89, 27 4% of
all) were much more frequent than expected (x" =
465 3, p < 0 0001) Thus, the numbers of certain species tended to vary in a parallel fashion, suggesting
that they were simultaneously affected by the same
environmental factors If so, then the positive associations should be significantly more frequent within
groups of species shanng the same ecological features
than in the whole sample However, the data did not
confirm this conjecture Though positive values were
slightly more common within groups, in none of the
migratory, nesting or feeding guilds distingtushed (see
Table 1), was the difference significant (
Long-term changes
We calculated long-term population trends for each
species (group of species) by linearly regressing respective indices of abundance as a function of time
Where necessary, the data were log-transformed to
improve their fit (see Matenal and methods) The
slope of regression represented the long-term population trend The trend was calculated over all 20-yr
combined and, to check whether the trend direction
remained stable within the study penod, also separately for the first and second 10-yr penods
Index of numbers of the whole breeding bird commumty showed a sigmficant increasing trend over the
20-yr penod. However, the slope of the trend
changed with time, from no relationship within the
437
240
' C palumbus
T troglodytas
160
200
160
120
120
1975
1980
1985
1990
1995
1975
1980
1985
1990
1995
1980
1985
1990
1995
1980
1985
1990
1995
•>
5
-o- P modulans
-o- E nibecuta
240
160
0)
0.
120
120
40
1975
60
1980
1985
1990
1995
200
1975
200
160
160
80
40
1995
1975
o
-o-F
250
albicollis
hypoleuca
I^
I
/
210
170
130
^
' «
'
P
/
D—O
/
^ .
/
90
\
1975
438
1980
1985
1990
1980
1985
1990
1995
ECOGRAPHY 20 5 (1997)
190
-"- R regulus
-o p palustns
1975
1980
1985
1990
1995
1975
1980
1985
1990
1995
1985
1990
1995
240
' F coulebs
C coccothraustes
140
60
1980
1985
1990
1995
160
-o- S migsns
-o C spmus
120
1975
1980
1985
1990
first 10-yr pienod, to a strong increasing trend in the
second decade (Table 3) Trends in numbers of the
individual guilds, in most cases, followed the above
pattern Their numbers were either mcreasing (most
often) or did not change significantly over the 20-yr
penod The trend in ground nester numbers differed
significantly from those observed in crown or hole
nesters (p < 0.001 for every companson) Similarly,
the inclination of slope of tropical migrants differed
ECOGRAPHY 20-5 (1997)
1995
1975
1980
Fig 2 Patterns of
year-to-year vanation in the
percentage indices of
abundance of 26 most
numerous breeding species
in the BNP, 1975-1994
Procedures used in
calculating numencal indices
are given in Matenal and
methods Full scientific
names of species along with
the minimum number of
pairs constttutmg 100% in
1977 (taken as base year)
are given in Table 2 Slopes
of regressions lines along
with their significance levels
are given m Table 4
significantly from those found in any other migratory
group (p < 0 05) Birds collecting food outside the
forest were the only group which showed a significant
decreasing trend (Table 3) However, this was mostly
due to the decrease in the first decade, as in the
second decade the trend was reversed, there was
rather a (non-significant) tendency to mcrease
(Table 3) Similar changes m slopes of trend lines
between the two penods were also visible in
439
Table 2 Assortment of the more numerous breeding species of Bidlowieia National Park to the major foraging, nesting and
migratory groups distinguished in Table 1, as well as the minimum number of pairs of individual species constituting 100% in
1977 (base year in calculation of population indices), mean and standard deviations of population indices, ratios of highest to
lowest values of population indices, and maximum rates of increase between the two consecutive years in 1975-1994 Species are
listed in the systematic order Procedures used in calculating numencal indices are given m Matenal and methods
Species
Ecological group
N pairs
in
Columha palumbui
Dendrocopos major
Dendrocopos medius
Anthus trwialis
Troglodytes troglodytes
Prunella modularis
Erilhacus rubecula
Turdus merula
Turdus philometos
Sylvia atricapilla
Phylloscopus sibilatrix
Phylloscopus collybtta
Regulus regulus
Muscicapa striata
Ficeduta parva
Ficedula albicollis
Ficedula hypoleuca
Parus palustris
ParW) caeruteus
Parus major
Sitta europaea
Certhia familiaris
Sturnus vulgaris
Frmgilla coelebs
Carduelis spmus
C coccothraustes
Migr
Feed
Nest
S
V
IB
IB
IG
IG
IG
IG
IG
IG
IL
IL
IL
IL
IL
IL
IL
IL
IL
IL
IL
IB
IB
O
IL
V
IL
C
H
H
G
G
G
G
C
C
G
G
G
C
C
C
H
H
H
H
H
H
H
H
C
C
C
R
RF
T
S
S
S
S
S
T
T
S
R
T
T
T
T
RF
R
R
RF
RF
S
S
R
S
other groups, in five cases the differences were significant (Table 3) Whereas, in the first 10 yr numbers
remained rather stable,' in the second decade all
groups tended to increase their numbers m parallel
(Table 3)
Over the 20-yr penod 16 of 26 sjjecies showed significant long-term trends, mostly increases, and only
three declines (A trivtalis, P sthilatrix, S vulgaris Table 4) In some sjjeaes, hke M strtata or F hypoleuca (Fig 2), the angle of trend bne remained the
same dunng the two decades, but in others inclination of slopes differed significantly between the two
periods {A trwialts, T philomelos, F albicollts, S vulgaris - Fig 3, Table 4) There were also species such
as T merula, P collybita or F parva, m which no
long-term hnear trend was visible though slopes of
their trends differed significantly between the penods.
Ficedula parva was extreme m this respect, havmg a
strongly mcreasing (0.77) trend m the first decade, a
strongly decreasing tendency (— 0 70) m the second
decade and no trend overall
Generally, dunng the first 10-yr penod, m contrast
with 1985-1994, there were fewer mcreasing species
(4 vs 10 sigmficant values) and more s{>ecies showed
signs of numencal decrease, though only m two cases
were the negative trends significant
440
Index
Ratios
1077
111 ly 1 /
11 5
105
118
120
34 0
180
1165
46 5
29 5
36 5
89 0
41 0
32 5
136
95
76 5
90
185
28 1
30 0
24 6
34 0
56 0
226 5
10 6
45 1
Mean
SD
Max/min
Max mcr
101 3
127 4
95 9
843
107 8
173 6
103 5
120 8
137 3
126 9
101 0
82 1
1175
146 2
102 7
94 5
147 7
107 1
140 8
138 5
151 7
101 9
59 5
123 2
39 3
102 0
26 2
45 8
22 9
38 6
189
449
160
170
26 5
19 2
342
15 8
442
37 8
25 7
28 9
50 1
30 9
56 0
33 1
50 8
18 1
26 6
157
31 7
24 7
3 49
4 30
2 22
8 49
172
2 67
1 80
165
1 84
181
18 33
2 10
3 71
3 84
2 73
2 73
4 26
364
4 42
2 78
381
2 30
3 63
1 60
1043 50
2 38
2 31
2 57
1 62
2 40
1 51
1 60
1 35
126
1 37
141
1142
1 37
2 10
2 07
197
1 52
2 10
1 65
68
60
96
46
73
28
130 40
1 84
None of the environmental variables recorded (Fig
4) changed significantly in the long run, but angle of
slof)es differed significantly between the two decades
m winter temperatures and numbers of caterpillars
(Table 5) Wmters tended to become milder m the
second decade, though the trend was not significant
(p = 0.06) Also leaf-eating caterpillars showed no
trends in the first 10-yr penod, but their numbers
grew significantly in the second decade This increase,
though, was substantial only m relative terms, as it
largely constituted population recovery from a very
low level (Fig 4) The numbers of caterpillars in the
second penod in all seasons except 1993 did not exceed values recorded m the first decade
Short-term fluctuations
We used residuals from the long-term trends, i.e. the
yearly deviations of the index value of the sp>ecies
(groups of species) from their long-term trends as a
measure of the short-term changes (fluctuations) We
checked then whether the fluctuation patterns of mdividual species (guilds) followed the vanation in wmtermg conditions, food availabihty and numbers of
predators m the BNP.
ECOGRAPHY 20 5 (1997)
Total numbers of the breeding birds were positively
correlated with mildness of the preceding wmter (Table
6) The correlation was strongest in forest residents and
birds wintenng locally, weak in short-distance migrants
and non-existent in tropical migrants (Table 6) At the
species level, however, the situation was more vanable
Numbers of only five of nine species of residents were
positively correlated with winter weather (cf Tables 2
and 7) Insofar wintering conditions changed in parallel
over large areas of Europe, the positive correlations
between winter seventy at Bialowieza and numbers of
the short-distance migrants, such as T troglodytes. S
vulgaris or T merula, could indicate some causal relationship However, the positive correlation with winter
weather recorded in F albicollis, the tropical migrant,
could not denote any direct causal link, unless weather
pattems between Europe and Afnca were correlated
Birds' numbers could be influenced by availability of
leaf-eating caterpillars either directly by adjustment of
numbers of settling birds to caterpillar abundance in
the current season, or with time-lag, via changes in
F parva
E rubacul
S atncapil
P modula
D major
T merula
F albicolli
F coelebs
T Philomel
C coccoth
S europae
M stnata
F hypoleu
P palustn
C palumb
T troglody
P caerule
P major
R regulus
D medius
C familian
C spmus
P sibilatra
P collybita
S vulgans
A tnvialis
00
02
04
06
08
10
12
14
16
18
Dissimilanty
Fig 3 Grouping of 26 most numerous species in the BNP
according to sunilanties (Pearson's r) of pattems of their
numencal vanauon Dendrogram drawn according to the
complete linkage algonthm, dissimilanties (1-r) are shown on
the abscissa Full scientific names of species are given in Table
BCOGRAPHY 20-5 (1997)
birds' productivity and/or survival affecting numbers in
the following season. To account for both these possibilities we correlated the residuals with data on both
current and previous years caterpillar numbers However, due to a strong autocorrelation between the two
measures of caterpillar abundance in our data set (r =
0 72, p < 0 001) differentiating between the relative importance of two mechanisms proved impossible
Short-term changes in numbers of the whole bird
community, and those of crown insectivores, were significantly correlated with both measures of caterpillar
abundance The fluctuations of ground insectivores
were correlated with the caterpillars in the current year,
and those of bark insectivores were correlated with
none of the measures (Table 6) Individual species
fluctuated m a more unpredictable fashion Seven of 26
species showed significant correlations with caterpillar
numbers in both comparisons, but only four of them
were crown insectivores, while the others were ground
{A trwialis, T meiula) or bark (C familiaris) insectivores (Table 7) Fluctuations in numbers of another
crown lnsectivore - F coelebs - were positively correlated with the current season's caterpillar abundance
and the value of the correlation coefficient for the
previous year's abundance approached significance
(p < 0 06) If we include this species, then in five of 13
crown insectivores shon-term numencal fluctuations
were positively correlated with caterpillar abundance
The fluctuations of the remaining eight crown feeders
were either independent or even, contrary to expectations, significantly negatively correlated (F parva.
Table 7) The latter result was most probably a spunous result of the peculiar pattem of numerical changes
m numbers of F parva (Fig 2)
Like the caterpillars, the number of rodents could
affect birds directly and with a time-lag Therefore, we
also used two measures of rodent abundance In contrast to the caterpillars the two measures of rodent
abundance were independent (autocorrelation r = 0 08,
NS) However, neither, the whole bird assemblage, nor
the ground nesting guild showed relationship with any
of them (Table 6) Fluctuations in numbers of one
ground nesting species - P sibilatrtx were negatively
correlated with the current numbers of rodents, while
those of P modulans and E rubecula were positively
correlated Significant negative correlation found in the
crown dwelling C sptnus could be an instance of spunous relationship, as this species could hardly be directly
affected by the changmg rodent numbers
Except for one spunous negative correlation (P stbilatrtx - Table 7), the year-to-year vanation in bird
abundance was independent of crop of tree seeds (Table
6 and 7)
Additionally to running the single factor correlation
analyses descnbed above we also earned out a multiple
regression analyses to check how much of the shortterm vanation could be accounted for by the combina-
441
Table 3 Long-term trends 1975-1984, 1985-1994, 1975-1994, in numbers, of mdividual guilds and of the total breeding bird
community of Bialowieza NaUonal Park in 1975-1994 Standardised regression slopes, their F-values and probabilities are given
for every penod Probabilities that the slopes did not differ between the two decades (Diff) are given as well Slopes diffenng
significantly from zero (at p < 0 05, t-test, two-tailed) are shown in bold type
Slope
F
P
0 16
0 49
0 10
064
0 01
-0.63
0.85
041
0.79
0.58
119
48 3
37
29 1
90
000
0 00
0 07
000
0 01
0 08
000
000
0 07
0 06
0 02
- 0 32
077
0 72
2I
26 4
19 5
0 17
000
000
113
11 8
98
48
0 01
0 01
0 14
0 06
0 02
0 02
046
0 95
- 0 11
0.57
0.63
0.72
02
88
II 8
196
064
0 01
0 00
000
36 8
000
001
0.62
11 5
000
Slope
F
P
Slope
F
P
Foraging
Outside (O)
Veget (V)
Ground (IG)
Bark (IB)
Crown (IL)
-0.63
0.65
- 0 30
0.75
0 15
53
59
08
102
02
004
004
040
001
0 68
0 47
0.82
0 56
0 62
0.93
23
163
37
51
53 7
0 19
000
0 09
0 06
000
Nesting
Ground (G)
Crown (C)
Hole (H)
- 0 36
0 27
0 25
12
07
05
0 31
044
0 49
0 57
0.88
0.92
39
26 3
45 3
Migration
Tropical (T)
Short-dist (S)
Resident (R)
Forest resid (RF)
-0
-0
0
0
33
33
50
59
I0
10
26
42
0 33
0 33
0 15
0 08
0 76
0.77
0 74
0 61
0 03
00
0 98
0.91
All birds
tion of these vanables We used only four independent
vanables, l e winter tetnperatures, caterpillars' numbers
in the ctirrent and the previous year and numbers in the
current year We excluded the previous year rodent
numbers, as well as spruce and hornbeam seeds from
this exercise as they had produced no significant and
reasonable correlation coefficients
As presented in Table 8, ca G^/o of short-term variation in numbers of the whole breeding bird community
of the BNP, as well as 45-74% of short-term changes in
the majority of individual guilds, could be accounted
for by the combmation of those vanables Applying the
same set of vanables to the individual species produced
significant results in nine of 26 sf>ecies (Table 9), with
the maximum value - 68% of explamed fluctuations m
R regulus It should be stressed, however, that the
short term changes of the majonty of species still
remam unexplained This, despite the fact, that using
residuals from the long-term trends alone, ignored any
efiects of positive autocorrelations due to density dependence, what could inflate the number of significant
restilts
To account for possible mfluence of bird densities we
used a different approach for each species, rates of
numencal changes between consecutive years were calculated and compared with the previous spnng caterpillar indices, mean winter temperatures and previous year
numbers. Data on bird and caterpillar ntimbers were
log transformed (natural loganthms). Table 10 shows
percentage vanation accounted for by the overwinter
temperature and caterpillar abtmdance taken on their
own, and after allowing for density. Percentage of
vanation in rates of population change accounted for
by the two vanables taken alone is very low, m no case
442
1975-1994
Diff
1985-1994
1975-1984
Ecological group
statistically significant In most species the percentage
of explained vanation was increased by allowing for
density, but it was still small and not statistically significant Only five species showed a significant increase
with temperature, two species showed a significant increase with caterpillar abundance, while Ficedula parva
showed a significant decline, which seems rather odd
Though this analysis reveals some of the effects
reported in Tables 7 and 9 it does not detect all of the
trends apparent in the analysis based on residuals from
the long-term trends Thus, the former conclusion, of
relative independence of year-to-year vanation m ntimbers of Bialowieza birds from the vanation in environmental variables measured in our study, is further
supported
Similarities of long-term trends and short-term
fluctuations
To make compansons possible, we constructed matnces
of dissimilanties for trends and fluctuations following
procedures proposed by Bohning-Gaese et al. (1994)
We defined the dissimilanty of the long-term trends
among species as the difference in the regression coefficients among each pair of species Thus two sp)ecies
with similar regression slopes had similar population
trends Two species with the identical trends had dissimilanties of 0 If one speaes had slope of — 1, the
other + 1 , the long-term dissimilanty of the two species
was 2.
We expressed the similarity of the yearly fluctuations
among sp>ecies by the Pearson's correlation coefficient
of the residuals among each pair of speaes. Hence, two
ECOGRAPHY 20-5 (1997)
Table 4 Long-term population trendi 1975-1984, 1985-1994, 1975-1994 in 26 most numerous species breeding in Bialowieza
Nationai Park Standardised regression slopes, their F-values and probabilities are given for every penod Probabilities that the
slopes did not differ between the two decades (Diff) are given as well Slopes diffenng significantly from zero (at p < 0 05, t test,
two-tailed) are shown in bold type
Species
Columba palumbus
Dendrocopos major
Dendrocopos medim
Anthus irwiatis
Troglodytes troglodytes
Prunella modularis
Erithacus rubecula
Turdus merula
Turdus philomeloi
Sylvia atricapilla
Phylloscopus sibilatrix
Phylloscopus cotlybita
Regulus regulus
Muscicapa striata
Ficedula paria
Ficedula albicollis
Ficedula hypoleuca
Parus patustris
Parus caeruleui
Parui major
Suta europaea
Certhia famtltaris
Sturnus vulgaris
Frmgilla coelebs
Carduelis spmus
C coccothraustes
1975-1984
1985-1994
Diff
Slope
F
P
Slope
F
P
0 06
0 62
0 24
-0.64
Oil
0 52
- 0 56
- 0 02
- 0 43
0 20
- 0 33
-051
- 0 09
0.74
0.77
- 0 49
0 63
0 09
0 42
0.74
0.76
0 57
-0.63
044
- 0 09
- 0 29
00
50
00
56
0 1
29
36
00
1 8
03
1 0
29
0 1
99
114
25
52
01
1 7
94
107
38
54
1 9
01
08
0 87
0 06
0 94
0 05
0 76
0 12
0 10
0 97
021
0 57
0 34
0 13
0 80
0 01
001
0 14
0 05
081
0 22
0 02
001
0 88
0 05
021
0 80
041
051
0 28
0 50
0 50
0.70
0 19
0 10
0.89
0 70
0 17
0 37
0 69
0 62
0.64
-0.70
0.91
0.64
0 53
0.70
0.66
0 22
0 55
0 19
0.89
0 13
0.65
26
07
27
27
75
03
01
31 1
76
02
1 3
74
49
95 6
77
36 2
56
3 1
77
63
04
35
03
29 4
01
59
0 14
0 43
0 14
0 14
0 03
0 61
0 78
000
0 02
064
0 29
0 03
0 06
0 05
0 02
000
0 05
0 12
0 02
004
0 55
0 10
0 60
0 00
0 73
0 04
0 38
0 43
0 57
0 03
0 18
0 48
0 20
0 02
0 03
0 95
0 19
0 02
015
0 72
0 00
000
0 97
0 36
044
0 77
0 17
0 97
0 01
0 10
0 94
0 06
1975-1994
Slope
F
P
0.53
0.49
0 33
-0.53
0 42
0.65
0 12
044
0.73
0 24
-0.46
- 0 22
0 32
0.80
004
0.59
0 80
0.57
0.62
0.71
0.85
0 09
- 0 67
0.79
0 27
0.49
69
56
2 1
72
37
129
03
43
20 3
1 1
48
09
20
319
00
94
32 3
88
11 1
182
46 8
01
144
29 4
1 5
55
0 02
0 03
0 16
0 02
0 07
000
0 60
0 05
000
0 30
004
034
0 18
000
0 87
001
000
0 01
0 00
000
000
0 72
000
000
0 25
0 03
species which had parallel deviations from their long- birds and their resources were simultaneously moniterm trends had similar fluctuations To make compari- tored Enemar et al (1984) gathered data on birds
sons with the populations trends possible we multiplied along with, information on defoliating caterpillars, seed
the values of correlation coefficients by — 1 and added crop and rodent numbers on several plots in subalpine
-I-1 to them This produced dissimilanty values ranging forest in N Sweden over a 20-yr penod The second
from 0 in the case of exactly parallel fluctuations to 2 m study includes results of work earned out within a
smgle 10 ha plot located in a temperate deciduous
the case of completely dissimilar ones
The dissimilanty indices of the long-term trends and forest in north America Data on birds and defoliating
short-term fluctuations showed no correlation whatso- insects were simultaneously gathered there over a peever (r^ = 0 004, N = 325), two species with the opposite riod of 20 yr (summarised in Holmes et al 1986,
trends, for example A trwtalts and F atbicollts (Table Holmes 1988 1990) This area most closely resembles
4) could have similar short-term fluctuation pattern the BNP in terms of habitat physiognomy, yet the
(Fig 2) and vice versa Thus, by knowing that numbers possibilities for compansons are limited, due to differof two species changed in similar fashion at one tempo- ent scale of the two projects (Wiens 1989), a single
ral scale one could not predict their behaviour at the habitat patch, compared to several large plots, replicated in different habitats
second scale.
Our analysis is based on a correlational approach
When one calculates numerous correlation coefficients,
as we have done, some spunous results will emerge by
Discussion
chance, which are significant in the statistical sense but
Long-term studies of forest bird communities are rela- do not reflect underlining causal relationships Sometively few (review in Enemar et al 1994). The longest times, as when numbers of a tropical migrant positively
senes available are those of Kendeigh (1982) from correlate with the preceding winter temperatures, we
North America (over 50 yr of data) and of Enemar et can detect and reject such spunous relationships, but m
al (1994) from Sweden (40 yr of data) In those studies, cases m which vanables show the predicted correlations
smgle small plots (10-40 ha), often situated m isolated we are unable to differentiate between false and genuine
woodlots, were used. Still less frequent are long-term ones This caveat has always to be kept in mind when
intensive studies in which both vanation m numbers of reading the discussion below
ECOGRAPHY 20 5 (1997)
443
1980
1985
1975
1990
1980
1985
1990
1995
Fig 4 Patterns of
year-to-year vanation in
abundance of defoliating
caterpillars, rodents, seed
crop and mean winter
temperatures in the BNP,
1975-1994 See
Environmental vanables
section for descnption of
measurement methods Note
semi-loganthmic scale in
two graphs
0 01
1975
1980
1985
1990
1995
Patterns of variation
The total breeding bird community of the BNP remained relatively stable dunng the whole 20-yr pienod,
the extreme abundance values diffenng by only 44%
Also Its species richness and composition remained
largely the same (Tomialojc and Wesotowski 1996)
Apparently this situation supported the "competitive"
community model "climax" pnmaeval stands inhabited by stable, saturated bird commumty, composed of
more vanable interacting pans - the species However,
a more thorough look at the data lends no support to
this view (see below), yet the narrow variation lirmts are
remarkable Similar low variability in the total community abundance over the 40-yr penod was also found by
Enemar et al (1994) The numbers of individual spiecies
m the BNP were more vanable, yet if we compare their
variability with the amount of vanation recorded m the
same area in numbers of rodents (over 40 x ) , hornbeam
seed crop (over 900 x ) or numbers of defohatmg caterpillars (ahnost '1500 x ) , then by contrast, even their
populations, with the exception of C sptnus and F
stbtkttrtx, app)eared relatively constant To some extent
these differences were forced by hfe-history limitations,
birds pK>ssessing slower maximum reproductive rates
could not increase that fast The vanation could be
damped additionally by low productivity of birds in the
444
BNP This was due mostly to nest loss to predators In
all species studied so far in the BNP, productivity was
lower or equal to the low values recorded for these
species in other areas (Wesolowski 1983, 1985, 1995a,
Wesolowski and Stawarczyk 1991, Piotrowska and
Wesolowski 1989, Walankiewicz 1991, Tomialojc 1994)
The low productivity could be one of the factors responsible for keeping densities of numerous species in
the BNP so low, that birds were unable to saturate
areas with temtones Consequently, patches of suitable
but unoccupied habitat were frequently observed In
less numerous species, such a condition could be close
to permanent (Wesolowski and Stawarczyk 1991,
Wesolowski and Tomialojc 1995) Terntonal behaviour
was another factor which could damp vanation in bird
numbers in the BNP Removal expenments with T
troglodytes and F major demonstrated that temtory
owners were able to prevent some birds form settling,
and occupied all space already at densities < 3 temtones/10 ha (Wesolowski 1981, Wesolowski et al 1987)
Terntonal behaviour and predation could hmit densities and productivity of birds in the BNP, but could
also act m a density-dependent, regulatory way (Newton 1992, 1993), that would increase their stabihsmg
capacity Even if only limiting, these factors rendered
rapid, large-scale populaUon increases unlikely If such
nses did occur they could not be achieved by the
ECOGRAPHV 20 5 (1997)
Table 5 Long-term trends 1975-1984, 1985-1994, 1975-1994 in winter temperature:,, caterpillar and rodent numbers in
BiaJowieza National Park Trends m crop of hornbeam and spruce seeds 1975-1989 m Bialowieza Nauonal Park are shown as
well Standardised regression slopes, their F-values and probabilities are given for ever> penod Probabilities that the slopes did
not differ between the two decades (Diff) are given as well Slopes diflenng significantly from zero (at p < 0 05, t-test, two-tailed)
are shown in bold type
Factor
Winter temperature
Caterpillars
Rodents
Hornbeam seeds
Spruce seeds
1975-1984
Slope
F
-001
-Oil
00
01
0 08
-on
1985-1994
P
Slope
0 98
0 78
0 78
0 62
0.94
0 23
interplay of local production/mortality - some immigration of birds had to take place from time to time
Immigration had to contnbute, at least in some years,
to numencal increases in highly vanable C spmus and
P sibilatrix, but its impact could also be discernible in
some seasons (when numbers more than doubled from
year-to-year) in several other species
Patterns of changes in numbers of bird sp)ecies found
in our data were mostly independent of one another, or
positively correlated, and thus did not offer much su{>port to the idea of compensatory numencal changes in
saturated, competitively interacting communities (Lack
1971, MacArthur 1972) Similar "individualistic'" responses were found also in other woodland bird community studies (Enemar et al 1984, Holmes et al 1986,
Virkkala 1991, Hogstad 1993, Morozov 1993) One
point needs expansion in this context we found earlier
(Tomialojc and Wesolowski 1990) that during the first
ten years of our study changes in numbers of the
tropical migrant gtuld in the BNP were negatively
related to the numbers of the resident group This result
agreed with the competitive model of Herrera (1978)
According to that hjTsothesis, the tropical migrants
only complement the community, being competitively
lnfenor, and can only use resources left by the residents Sunilar negative relationships between migrants
and residents, explained along those lines, have also
been found elsewhere (O'Connor 1981, Berthold 1990,
Enemar et al 1994). However, the situation in the BNP
reversed dunng the second decade when the numbers of
residents and tropical migrants were both lncreasmg
Overall, the numbers of tropical migrants did not substantially change dtirmg the 20-yr period, while those of
residents mcreased. This could be reconciled with the
Herrera model only if the carrying capacity of the
Bialowieia habitats, total amoimt of resources available
to birds dunng the second decade was much higher
than earher, and additionally strongly lncreasmg This,
however, did not seem to be the case (see below), hence
the negative correlation m the first decade could have
ansen from reasons other than interspecific competition. This IS indirectly supported by the fact that the
predicted negative relationship between numbers of
ECOGRAPHY 20-5 (1997)
F
50
58 9
0 450
Diff
Slope
P
0 06
000
0 52
Whole penod
0 02
0 01
0 54
0 28
0 17
-001
0 03
- 0 16
F
1 6
05
00
0 01
1 6
P
0 23
0 48
0 97
091
0 23
tropical migrants and residents has not been found in
majonty of other studies (Enemar et al 1984, Solonen
1986, Holmes et al 1986, Jarvinen and Rajasdrkka
1992, Hogstad 1993, Morozov 1993), thus giving no
support to the Herrera model
Long-term trends
If the "climax" old-growth stands were in equilibnal
state, saturated with birds, one would rather expect
numbers to fluctuate around some mean values, without long-term directional changes This was largely the
picture of the Biatowieza bird community in the first
decade This caused us to underline the relative stability
of the local avifauna in earlier papers (TomiaJojc and
Wesolows,ki 1990, 1994) However, in the second
decade circumstances changed, when most species increased in numbers, resulting in the significant longterm trends in several breeding species and in the whole
community The tendency towards parallel changes observed in species differing in their food requirements,
nest sites, and migratory patterns suggests rather that a
number of different causal factors had to be involved,
as It would be difficult to find a common denominator,
a single factor which could account for all those increases
Neither crops of major tree seeds nor numbers of
rodents increased progressively over time Also their
year-to-year vanation was not coupled with the changes
m numbers of birds in the BNP Therefore, we have to
dismiss their possible contnbution to the explanation of
the long-term increases Relationships between rodent
numbers and predation pressure were less straightforward than expected (see below), but it would be premature to exclude changes in predation pressure, acting
via changes in productivity, as a factor contnbutmg to
the observed trends Such a relationship between predation and long-term trends in North Amencan insectivorous passennes was detected by Bohmng-Gaese et al
(1993). Unfortunately, there are no data from the BNP
on vanation m predator pressure, nor on long-term
trends in nesting success of any bird, so we cannot test
this hypothesis
445
Table 6 Relationships between mean temperatures of preceding winter, seed crop, numbers of caterpillars, numbers of rodents
and the short-term fiuctuations in ntmibers of individual guilds and of the total breeding bird community of Bialowieza National
Park in 1975-1994 Correlation coefficients - r and their p values are shown Slopes diffenng significantly from zero (at p < 0 05,
two-tailed) are shown in bold type Numbers in parentheses following vanable names denote the number of years for which the
data were available Curr yr - current year, Prev yr - previous year, Homb - hornbeam
Ecological group
Winter
temf >(20)
Curr
yr (20)
Prev
yr (19)
Curr
yr (20)
Prev
yr (20)
Homb
(15)
Spruce
(13)
r
P
r
P
r
P
r
P
r
P
r
P
r
P
Foraging
Outside (O)
Veget (V)
Ground (IG)
Bark (IB)
Crown (IL)
0.64
0 36
0 37
0.47
0.49
0 00
0 12
0 11
004
0 03
0.58
0 42
0.45
0 20
0.76
0 01
0 06
0 05
040
000
0.59
0.51
0 29
0 35
0.82
001
0 03
0 22
0 15
0 00
0 20
0 26
0 43
0 22
- 0 02
0 40
0 27
0 06
0 36
0 92
0 09
0 10
-Oil
018
- 0 20
0 70
0 68
064
044
040
0 01
0 35
- 0 14
004
-031
0 96
0 20
0 62
0 88
0 26
- 0 12
- 0 10
- 0 09
0 06
0 10
0 69
0 76
0 78
0 86
0 75
Nesting
Ground (G)
Crown (C)
Hole (H)
0 09
0.52
0.75
071
0 02
000
0.55
0.58
0.63
0 01
0 01
000
0.52
0.56
0.76
0 02
001
0 00
- 0 05
0 33
0 20
084
0 16
040
- 0 14
- 0 03
- 0 12
054
0 91
0 61
- 0 40
- 0 02
- 0 10
0 14
0 96
0 73
0 13
- 0 16
0 02
0 66
0 60
0 95
on
0 36
0.63
0.51
0.53
021
000
0 02
0 02
0 37
0.70
0 40
0.61
034
0 00
0 10
0 01
0 15
- 0 16
0 40
- 0 13
0 33
051
0 08
0 59
0 15
- 0 23
- 0 07
- 0 13
0 22
0 34
0 78
0 57
0 35
-0
-0
-0
-0
0 14
0 94
0 65
0 70
0 06
- 0 12
0 19
- 0 05
0
0
0
0
0.72
000
0.72
0 00
0 18
0 45
- 0 14
0 56
-023
041
004
Migration
Tropical (T)
Short-dist (S)
Resident (R)
Forest resid (RF)
0.68
0 61
064
0 12
0 00
0 00
All birds
0.55
0 01
Winters did not show any clear-cut tendency to
amehorate with time, so, in spite of some resident
species showing short-term correlations with the conditions m the preceding wmter, wintering conditions m
the BNP gave no valid explanation for the long-term
increases in bird numbers
Caterpillar numbers were steadily growing in the
second decade but it was mostly a process of recovery
from a very low level, and their numbers did not
usually exceed those observed in the first decade Therefore, increases in insectivorous bird abundance in the
second p)enpd could not be explained by this factor
alone However, it is possible that increasing caterpillar
numbers added to a generally higher level of other
invertebrates m the second decade, and that the posiUve
short-term correlations between numbers of several
birds and abundance of caterpillars translated into
long-term increases Yet, only some species showing the
strongest relationships with caterpillars in the short run
manifested also the strong tendencies to mcrease
Responses of birds to changing habitat structure
were observed to be involved m producing the longterm trends even m the old-growth stands (e g Hohnes
et al 1986, Enemar et al 1994) Also in our study plots
several changes of varying magnitude were recorded
dunng the 20-yr penod Mostly their influence was
local, but two large scale trends were detectable as well
(Tomialojc and Wesolowski 1996), namely a steady
slow declme of Norway spruce and some opening of the
canopy followmg formation of gaps. These habitat
changes could be benefiaal to species de])endent on
small gaps, hke M. strtata or A. trtvtalts However,
numbers of these two species showed opposing long446
40
02
13
11
84
69
54
86
091
term trends For the majonty of other species, those
relying on spruce or mature trees in general, the observed changes would mean habitat detenoration, not
improvement quality In spite of this, R regulus - the
Norway spruce specialist, tended to increase in numbers
in the second decade, as did the numbers of crown and
hole nesters Their numbers grew not because of habitat
changes, but in spite of them
Secondary hole-nestmg sjjecies serve as a textbook
example of a group of speaes limited by shortage of
resources (nest sites) and/or interspecific competition
for them (von Haartman 1971, Pemns 1979, van Balen
et al 1982, Newton 1994b) Hence it is tempting to
assume that in the BNP, their numbers were controlled
by the shortage of holes The data at hand do not lend
any support to such a notion All species, except S
vulgarts, showed long-term increasing trends Moreover, data on hole availability in the BNP (Wesolowski
1989, Walankiewicz 1991) demonstrate that the secondary hole nesters were not limited by shortage of
holes even at the high densities found in 199O's
Ftcedula albtcollts was the most numerous member of
the hole nester guild in the BNP (Tomialojc and
Wesolowski 1990, 1994, 1996) and at the same the
latest breeding species of this group, so it should be
most severely affected by any shortage of nest sites Yet
even in 1989, the year m which hole nesters achieved
high densities, Walankiewicz (1991) found that there
were still at least 2 holes/flycatcher female to choose
between The figure was conservative as it includes only
holes offered to females by F albicollts males in that
season, and numerous other holes remam unoccupied
(unpubl.). Also removals of F. major (Wesolowski et al.
ECOGRAPHY 20-5 (1997)
Table 7 Relationships between mean temperatures of preceding winter, seed crop, numbers of caterpillars, numbers of rodents
and the short-term fluctuations in numbers of 26 most numerous species of breeding birds in Bialowieza NaUonal Park in
1975-1994 CorrelaUon coefficients - r and their p values are shown Slopes diffenng significantly from zero (at p < 0 0 5 ,
two-tailed) are shown in bold type Numbers in parentheses following vanable names denote the number of years for which the
data for individual vanables were available Curr yr - current year, Prev yr - previous year, Homb - hornbeam
Speaes
Winter
temp (20)
Caterpillars
Curr
y (20)
r
P
Cotumba palumbus
0 23 0 33
Dendrocopos major
0 03 0 92
Dendrocopos medius
0.62 000
Anthus trivialis
0 29 0 22
0.47 004
Trogtodytes trogtodyles
Prunetta modutaris
0 11 0 65
0 02 0 95
Eritliacus rubecula
0.46 004
Turdus merula
0 29 0 22
Turdus phitometos
Sytvia atricapitta
0 27 0 25
- 0 22 034
Phyttoscopus sibitairix
Phyltoscopus coltyhtta
0.48 0 03
Regulus regulus
0.82 000
Muscicapa striata
- 0 02 0 93
Ficedula parva
- 0 4 3 006
Ficedula albicotlis
0.48 0 03
0 12 0 62
Ficedula hypoleuca
Parus palustris
0.53 0 02
Parus caeruteus
0.53 0 02
0.45 0 05
Parus major
0 12 0 62
Sitta europaea
Certhia familtaris
0 38 0 10
Slurnus vulgaris
0.60 001
Frmgilta coetebs
0 13 0 57
Carduelis spmui
- 0 22 0 35
0 30 0 20
C coccothraustes
r
P
0 03
0 10
0.49
0.59
0.56
- 0 06
0 07
0.62
0 36
0 18
040
0.55
0.50
0 08
- 0 43
0.61
0 01
- 0 07
0.50
0 39
- 0 48
0.55
0 36
0.48
0 09
0 42
0 92
0 68
0 03
0 01
001
0 80
0 78
000
0 12
0 45
0 08
0 01
0 02
0 73
006
000
0 98
0 78
0 02
0 09
0 03
0 01
0 12
0 03
0 70
0 06
Prev
yr(19)
r
P
0 24
0 14
031
0.65
0 36
0 03
- 0 12
0.68
0 06
0 24
0 42
0.56
0.56
0 36
-0.70
0.63
0 42
0 14
0.57
040
- 0 24
0.57
0.46
0 45
031
0 27
Seeds
Rodents
0 32
0 58
0 19
000
0 13
0 90
0 63
0 00
0 80
0 32
0 07
0 01
001
0 13
000
0 00
0 07
0 56
0 01
0 09
0 32
0 01
0 05
0 05
0 19
0 27
Curr
yr (20)
r
P
-001
0 08
0 13
-001
- 0 10
048
0.50
- 0 09
0 27
0 33
-0.55
0 28
0 23
0 13
0 01
0 26
0 12
0 49
- 0 43
- 0 12
0 25
- 0 06
0 25
0 14
-0.49
0 40
0 96
0 73
0 59
0 97
0 66
0 03
0 03
071
0 25
0 15
001
0 23
0 33
0 58
0 95
0 27
061
0 03
0 06
0 62
0 30
0 79
0 29
054
0 03
0 08
Prev
yr (20)
r
P
0 18
- 0 11
- 0 07
-041
- 0 08
0 23
- 0 07
- 0 20
-004
- 0 12
- 0 15
- 0 05
- 0 05
- 0 10
0 12
- 0 16
-021
0 42
- 0 10
- 0 28
0 42
-0.20
0 12
- 0 16
- 0 16
004
0 45
0 65
0 78
0 07
0 72
034
0 79
0 39
0 86
0 62
0 52
0 84
0 84
0 68
0 61
051
0 37
0 06
0 67
0 24
0 07
040
0 62
0 51
0 50
0 87
Homb
(15)
r
P
- 0 05
0 03
- 0 25
- 0 30
- 0 03
0 12
- 0 12
-031
- 0 16
0 04
-0.64
- 0 03
- 0 23
0 33
0 30
0 10
0 32
- 0 II
0 20
- 0 20
0 27
- 0 19
0 22
-004
0 02
0 18
0 85
0 91
0 37
0 27
0 92
0 67
0 66
0 27
0 56
0 89
0 01
0 93
0 41
0 23
0 28
0 72
0 25
071
0 47
0 47
0 32
0 50
044
0 90
0 94
0 52
Spruce
(13)
r
P
-001
0 32
0 23
0 09
044
- 0 40
- 0 10
- 0 11
- 0 10
0 96
0 28
0 45
0 76
0 14
0 18
0 75
0 72
0 75
0 30
-031
0 30 031
001 0 99
0 11 0 73
- 0 3 1 0 30
- 0 3 1 0 30
0 07 081
- 0 47 0 10
- 0 19 0 52
041 0 16
0 19 054
- 0 23 0 46
0 23 0 45
0 15 0 63
- 0 0 1 0 99
0 02 0 96
- 0 06 0 85
1987) revealed that their spnng numbers were controlled by ntimbers of would-be settlers and temtonal
behaviour and not by the shortage of holes Quantitative superabundance of holes did not, however, mean
that that interspecific conflicts over holes did not occur
altogether Interspecific aggressive encounters and hole
usurpation of one species by another were recorded
(Tonualojc et al 1984, Wesolowski 1995a), albeit
rarely
Summing up, the long-term increasing trends observed in several species in the BNP could not be
explained by extensive favourable changes in habitats,
nor by amelioration of wintenng conditions in the
forest With the data m hand, we were unable to
demonstrate that changing food resources and/or predation pressure in the BNP were behind the recorded
population trends, but we have not disproved this
possibihty, either
cies changed in similar fashion at one temporal scale
one could not predict their behaviour at the other scale
Bohmng-Gaese et al (1994), working with North
Amencan data- (mostly) on woodland passennes, arnved at the same conclusion These findings, clearly
demonstrating individualistic reactions of different species to varying environmental conditions, are quite
frustrating - our possibility to generahse, to predict
from results of short-term studies the future course of
events, are severely impaired There are perhaps still
opponunities to forecast the reaction of bird communities to e g the global climatic changes qualitatively at a
very general level (Berthold 1990, 1991) but there is not
much hope for very precise quantitative predictions
Saying this, we do not imply that changes in the bird
community m the BNP were completely chaotic, that
there were no regulanties discemible On the contrary,
pattems of short-term vanation of several species could
be explamed by an interplay of factors acting on the
breeding grounds. They are presented below
Short-term fluctuations
Nesting success of several ground nestmg birds (P
sibilatrix, T troglodytes, P collybtta - recalctilated
from Wesolowski 1983, 1985, Piotrowska and
Wesolowski 1989) in the BNP appeared to be negatively related to the numbers of rodents, though the
Our results indicate that birds that responded to environmental vanabihty on a long-term basis in the same
way could have quite divergmg pattems of short-term
vanation, thus, by knowing that numbers of two speECOGRAPHY 20-5 (1997)
447
Table 8 Multiple regression results for the short-term fluctuations in numbers of individual guilds and of the total breeding
bird community of Bialowieza National Park Multiple correlation coefficients, their F-values and probabilities as well as
the coefficients of multiple determination are given Coefficients differing significantly from zero (at p < 0 05, two-tailed)
are shown in bold type
Ecological group
R
F
P
R-
nsk It would thus seem advantageous for the ground
nesting birds to react to this nsk by avoiding breeding
in rodent plague years. However, only fluctuations in P
sibilatrix numbers were congruent with the possibility
that they were negatively correlated with rodent numbers The fluctuation patterns m other ground nesting
species either did not correlate or even positively corre-
lated (P modularts and E rubecula) with those of the
rodents This discrepancy could be due to mustelid
0.71
36
0 03
0.51
predators switching from concentrating on rodents dur0 62
22
0 12
0 39
ing their outbreaks to hunting birds dunng the rodent
0 66
28
0 07
044
0 55
1 5
0 24
031
crash years (Marcstrom et al 1988, Jarvinen 1990.
0.86
10 1
000
0.74
J?drzejewski et al 1993, Wesolowski 1995a, Zalewski et
Nesting
al 1995) Thus, the joint pressure of all predators on
Ground (G)
0.69
32
0 05
0.47
the low nesting birds dunng the rodent outbreaks could
Crown (C)
0.74
43
0 02
0.55
be no higher than in the crash years, making the
Hole (H)
0.87
11 1
000
0 76
avoidance
of such seasons unprofitable Additionally,
Migration
as found m a Swedish study (Arheimer and Enemar
Tropical (T)
0.81
66
0 00
0.65
Short-dist (S)
0.70
34
004
0.49
1974, Enemar et al 1984), the ground nesters could
Resident (R)
0 77
5 1
0 01
0.59
avoid
rodents by nesting higher dunng the outbreaks
Forest resid (RF)
0 67
28
0 07
0 45
This option was unavailable for P sibilatrix, which
All birds
0.83
76
000
0.69
always bred on the ground (Wesolowski 1985), but
other ground nesters in the BNP could react in this way
short penods of studies precluded formal statistical (Wesolowski 1983, Piotrowska and Wesotowski 1989,
testing of those relationships Enormous fluctuations in Wesolowski and Tomialojc 1995)
abundance of rodents observed m the BNP (Pucek et
Influence of changes in spring food resources on the
al 1993) could lead to the vast vanation in predation breedmg bird numbers seemed to vary widely between
different study sites Holmes et al (1986) and Holmes
(1988, 1990) underlined the importance of leaf-eating
Table 9 Multiple regression results for the short-term fluctuations in numbers of 26 most numerous species breeding m
caterpillars (the mam nestling food of insectivorous
Biaiowieza National Park Multiple correlation coefficients,
birds) m shaping numbers of birds in the North Amertheir F-values and probabilities, as well as the coefficients of
ican study site. The caterpillars affected the birds
multiple determination are given Coefficients diffenng significantly from zero (at p < 0 05, two-tailed) are shown in bold
mostly with a time-lag, l e via demographic effects
type
Holmes et al (1986, 1991) concluded that in their area
"food
resources may be chronically low for several to
Species
R
F
R^
P
many successive years and may become superabundant
Columba palionbus
0 38
06
0 67
0 14
only dunng relatively bnef caterpillar eruptions" In a
Dendrocopos major
0 19
01
0 97
004
Swedish woodland, on the other hand, though numerDendrocopos medius
0 67
28
0 07
0 45
ous bird species also rehed heavily on caterpillars to
Anlhus Irivialii
0.74
42
0 02
0.55
Troglodytes troglodytes
feed their young, only FrmgiUa montifrmgilla increased
060
04
0 16
0 36
Prunella modularis
0 52
13
031
0 27
in numbers m parallel with an outbreak of defoliating
Erithacus rubectila
0.60
20
0 16
0 36
caterpillars
(Enemar et al 1984) In this case the impact
Turdus merula
0.71
35
004
0.50
of msects seemed du-ect, the numbers of birds settling m
Turdus philomelos
0 52
1 3
031
0 27
Sylvia atricaptlla
046
09
0 47
0 21
the spring were adjusted to the caterpillar availability
Phylloscopus sibilatrix
0.78
54
0 01
0.61
Our earher analysis of the first ten-years data proPhylloscopus collybita
0.71
37
0 03
0^1
duced only few mdications of birds tracking resources,
Regulus regulus
0.83
76
000
0.68
of their possible numencal responses to the caterpillar
Musctcapa strtata
0 53
14
0 30
0 28
Ficedula parva
0.73
39
0 02
0.53
ntimbers m the current season but produced some more
Ficedula albicollis
0.76
47
0 01
0.58
indications
of possible lagged effects of caterpillars
Ficedula hypoleuca
0 66
26
0 08
0 43
(Tomialojc and Wesolowski 1990). The present data
Panis palustris
0.72
39
0 03
0.52
Parus caeruleus
0.80
64
000
0.65
offer more support to the possibility that a numencal
Parus major
0 51
1 2
034
0.26
response of birds could have occurred - the short-term
Sttta europaea
0 61
21
0 14
0 37
changes m numbers of the whole bird commumty, of
Certhia famdiaris
066
27
0 08
0 43
the crown lnsectivore guild, as well as of 5 of 13 crown
Stumus vulgaris
0 62
2.2
0.13
0 38
Frmgdla coelebi
0 65
25
0.09
0 42
insectivorous species were all positively correlated with
Carduelis spmus
0 57
17
0 20
0 33
the geometnd caterpillar abundance m the current
C coccothraustes
0 61
21
0 14
0 37
spring. However, due to the strong autocorrelation
Foraging
Outside (O)
Veget (V)
Ground (IG)
Bark (IB)
Crown (IL)
448
ECOORAPHY 20-5 (1997)
Table 10 Percentage vanation m annual changes of log population mdex accounted for by overwinter temperature and log
caterpillar abundance alone, and after allowing for previous year's log mdex Positive and negative signs mdicate increasing and
decreasing tendenaes respectively * - p < 0 05, ** p < 0 01
Species
Overwinter temperature
Alone
Columba palumbus
Dendrocopos major
Dendrocopos mediw,
Antlius trwiatis
Troglodytes troglodytes
Prunella modularis
Eritliacus rubecula
Turdus merula
Turdus philomelos
Sylvia atrtcapilla
Phvtloscopus sibitatrix
Phylloscopus collybita
Regulus regulus
Muscicapa striata
Ficedula parva
Ficedula albicottn
Ficedula hypoleuca
Parus palustris
Parus caeruleus
Parus major
Sttta europaea
Certhia familiaris
Sturnus vulgaris
Fringilla coelebs
Carduelis sptnus
C coccothraustes
+ 45
-09
+ 31
-07
-02
-155
-92
+ 53
-182
After density
+ 92
+ 07
+ 28 9**
+2 1
+ 127
-02
+ 09
+ 164
-93
-31
-68
+ 10
+ 70
+ 116
-2 1
-109
+15
+0 1
+ 37
+ 47
+0 9
+ 00
+ 11 1
+ 14
-4 9
+ 09
-0 3
+ 11 3
+ 47 0*'
-97
-19
-127
+ 89
+3 1
+ 19 2*
+ 19 1*
+ 11 1
+ 36
+ 18 5*
+ 06
-9 1
+ 16
+ 71
between the abundance of caterpillars in the current
and the previous year, it was impossible to say whether
the settling birds really reacted numencally to the current caterpillar level, or whether the positive correlations with caterpillar abundance in the current spnng
were to a large extent due to correlation between
caterpillar mdices of successive springs.
Availability of defoliating caterpillars could easily
influence birds in the BNP as they heavily depended on
caterpillars as a source of nestling food (Tomialojc
1994, WesoJowski and Tomiatojc 1995, unpubl), so
there was an ample opportimity for their productivity
and/ or survival to be affected by food supply The
effect of caterpillars on birds could be also indirect, via
lowenng pressure of nest predators It was observed
that in the outbreak years smaller predators (woodpeckers, Garrulus glandarttis, Scturus vulgar ts, Glindae,
and other small mammals) fed extensively on caterpillars, thus presumably paying less attention to robbing
nests (Pucek 1978, TomiaJojc et al 1984, Tomialojc
1994, unpubl)
Whatever the mechanisms of the caterpillar influence
on bird numbers were, three pomts should be stressed
here. Firstly, annual vanation m the numbers of most
insectivorous species bore no relationship to caterpillar
availabihty Secondly, even if the birds were following
the changmg caterpillar numbers, their numbers vaned
within much narrower limits (doubled or tnpled).
HCOGRAPHY 20:5 (1997)
Caterpillar abundance
Alone
+ 33
+0 1
After density
+ 42
+ 04
-20
-23
+ 19
+ 84
+ 22
+ 10
-1 7
+ 20 1*
-35
+ 08
-26
+ 0.2
-10.3
+ 05
+0 1
+ 00
+ 03
+ 39
-70
+ 04
+ 120
+4 1
-00
+0 1
+4 9
+ 00
+0 3
-00
+ 22
+1 1
-55
+ 27
+ 19
+ 132
+47 9'»
+ 52
-27 8 "
+ 53
+ 120
+ 34
+ 55
+ 26
+ 26
+ 15 1
+3 1
+1 5
+ 33
+ 30
whereas those of caterpillars vaned over three orders of
magnitude Therefore, they could not utilise them fully
at higher caterpillar levels, l e in many years caterpillars were superabundant Thirdly, year-to-year variation in nesting success of msectivores in the BNP was
mostly due to predation on eggs and nesthngs, starvation being unimportant, even in the low-caterpiUar
years (Wesolowski, 1983, 1985, Piotrowska and
Wesoiowski, 1989, Tomiatojc 1994) Therefore, shortage of geometnd caterpillars did not necessanly mean
food hmitation dunng the breeding penod.
Surplus resources m the breedmg season could result
from limitation of ntimbers in the non-breeding season
It has been long proposed (Lack 1966, Fretwell 1972)
that most bird populations of the temperate zone were
limited by conditions at the wintermg grounds In
accordance with this hypothesis, several studies demonstrated that the numbers of resident birds in western
Europe and Fennoscandia were strongly dependent on
the seventy of the previous winter (van Balen 1980,
Cawthome and Marchant 1980, Kallander and
Karlsson 1981, Hilden 1982, Bejer and Rudemo 1985,
Nilsson 1986, Greenwood and Baillie 1991). Taking
into account that wmters m the Bialowieza Forest are
much harsher than in western Europe (forcing many
Bialowieza birds to migrate for wmter to western Europe), weather conditions in winter should strongly
influence birds in this forest as well Changes m num449
bers of the breeding bird community, the ntimbers of
forest residents and birdb wintenng in the vicinity of
Bialowieza Forest were, as predicted, positively correlated with winter temperatures At the species level, the
relationship was upheld in R regulus, D medtus and
three Faru^ spp which corresponds well with data from
elsewhere (reviews in Marchant et al 1990, Glutz von
Blotzheim 1991) Yet, the other four resident species
did not seem to be influenced Sttta europaea, known to
be dependent on winter temperatures in other places
(von Haartman 1971, Kallander and Karlsson 1981.
Svensson 1981, Nilsson 1987, Enoksson 1988), in spite
of having to cope with winters that were equally or
more severe, did not show any relationship with winter
tempwrature in the BNP Similarly, in sharp contrast to
R regulus, another tiny resident species - C famtltarts
did not show any correlation with winter temperatures
However, this species could be more sensitive to prolonged ice coating of bark and not to low temperatures
themselves (Marchant et al 1990) Such circumstances
were probably infrequent in the relatively dry, continental conditions of the Bialowieza Forest
It IS known from other areas that the autiunn seed
supply can interplay with winter weather in controlling
spnng numbers of e g 5 europaea (Enoksson and
Nilsson 1983, Nilsson 1987, Matthysen 1989), D major
(review in Glutz von Blotzheim 1980), Farus spp (review in Pemns 1979, Newton 1994a) and C sptnus
(Newton 1972), while the hombeam seed crop influence
partial migration pattem in C coccothraustes (Kruger
1982) These birds in the BNP were regularly observed
using tree seeds in the autumn-winter penod, as well as
early in the spring, before leaves on trees developed
(but no quantitative data available so far) Thus, the
observed lack of any correspondence between their
numbers in the BNP and seed crop came as a surpnse,
the more so, because changing seed supply has quite
dramatic effects on local mammals, mast years result in
rodent outbreaks there CPucek et al 1993) As C sptnus
forages extensively also on alder and D major uses pine
seeds, for which we have no data, there is still a
possibility that they were actually influenced by seed
supply, but we have failed to detect this However, this
explanation cannot be offered for the other species
Hence, it seems that seeds are much less cntical for
birds in the BNP than m other areas This conclusion is
further strengthened by the results of trials to supplement birds m the BNP with food in wmter, where the
birds largely failed to use the extra food offered
(Wesolowski 1995b) Similarly, as proposed for the
mvertebrate food, this could be due to higher than in
other places diversity of altemative food sources Birds
m these pnmaeval, multi-speaes and multi-aged tree
stands can apparently, in the case of failure of any
single food source, switch to other food types, so no
effect on ntimbers emerged
450
Unexplained variation
Taken together, vanation in caterpillar abundance,
winter seventy and numbers of rodents (in a few species) could explain most pattems of short-term variation in the whole bird community, as well as in several
individual species However, there are also species like
D. major, C palwnbus or 5 atrtcaptlla, m which this
combination of factors has explained only a negligible
part of fluctuations What causes could lay behind this
unexplained vanation'' Likewise a substantial part of
causes of the long-term vanation remains to be elucidated (see above)
As already suggested, there had to be additional food
resources, utilised by birds in the BNP, the abundance
of which was not measured The numbers of birds
could actually have been influenced by variation in
their food supply, but the relationship might have been
blurred by switching of birds between different food
sources Likewise our knowledge of vanation in predator pressure is very approximate, and more precise
measurements might result in more vanability explained These suppositions could be resolved with data
collected in future
An additional source of variability, not considered so
far, are processes occumng outside the forest So far we
have analysed the situauon at a local scale, under the
assumption that either there were no significant external inputs, or the changes of environmental factors in
the forest reflected their variability over larger areas
Among resident species such an assumption seems reasonable, yet even here it need not invanably be true
(Holmes and Sherry 1988, Wiens 1989) If processes
acting outside the forest were independent of the situation within It and were acting so strongly that effects of
local factors were swamp)ed, then one would not be able
to show any relationship of bird numbers with the local
situation As discussed in Wesolowski and Stawarczyk
(1991), this explanation seems to be hardly applicable
to S europaea, as well as to other resident species
spending all year round in the same sites But forest
residents constitute only ca 10% of the breeding bird
community m the BNP (Tonualojc and Wesolowski
1996) and for 90% of birds spending winter outside
their breeding areas such conjecture seems more plausible If conditions in the non-breeding period were of
utmost importance for population dynamics, then one
would expect species wmtenng in the same regions to
have similar pattems of ntimencal change, as found m
at least some studies (Enemar et al 1984, 1994, Burskiy
1993, Morozov 1993) This prediction, though, has not
been corroborated. It would be premature to reject
this hypothesis altogether, as our migratory categones
were quite broad, and speaes ranked among e g tropical migrants could wmter in totally non-overlapping
areas (e.g F parva and F. albicollis). Nevertheless,
there is no evidence at the moment on whether events
ECOGRAPHY 20 5 (1997)
m the non-breeding areas were the most influential in
controlling bird ntimbers in the BNP
Regional processes could be important in another
way as well, namely birds breeding in the BNP, m spite
of Its relatively large area (47 km^) did not constitute
closed demographic units As descnbed earlier the maximum rate of numerical increase between two consecutive seasons recorded in several species could not be due
only to local production, so immigration of birds into
study areas must have occurred We do not know if the
immigrants came from surrounding managed parts of
Bialowieza Forest or from places further away, nor
whether emigration took place in other years An important point to be made here is that the external
processes could modify relationships between local
birds and environmental conditions in the BNP The
preponderance of outside influences is well recognised
in small isolated woodlots, but there might be also
situations when, even m larger tracts of intact boreal
forest, regional processes could overshadow local ones
(Helle 1986, Vaisanen et al 1986, but see Virkkala
1990) Checking the possible role of such regional inputs in the population dynamics of birds in this primaeval forest will constitute the subject of a separate
analysis
Acknowledgements
Collection of data which form the basis
of our analyses would not be possible without a help of several
people We express our gratitude to those who shared over the
years the pains of the field work, J Lontkowski, C Mitrus, T
Stawarczyk, A Szymura and above all to W Walankiewicz
We also thank 1 Newton and P Rothery for constructive
discussion of an earlier draft of the manuscnpt, and linguistic
help We appreciate too remarks of reviewers R T Holmes
and another one with indecipherable signature Preparation of
this paper was financially supported by a grant from the
Scientific Research Committee (KBN)
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