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Forest Ecology and Management 494 (2021) 119310
Available online 6 May 2021
0378-1127/© 2021 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Do large herbivores maintain open habitats in temperate forests?
Rafał Kowalczyk
*
, Tomasz Kami´
nski , Tomasz Borowik
Mammal Research Institute, Polish Academy of Sciences, 17-230 Białowie˙
za, Poland
ARTICLE INFO
Keywords:
European bison
Bison bonasus
Białowie˙
za Primeval Forest
Tree encroachment
Forest succession
Grazing
Key species
ABSTRACT
In recent decades, grazing by wild and domestic ungulates has become a strategy for conservation management
to restore or maintain open landscapes. One of the species playing an increasing role in ecological restoration is
the European bison – the largest terrestrial mammal in Europe. We studied the impact of this large herbivore and
other ungulates (moose, red deer, and roe deer) on tree encroachment in open habitats in the Białowie ˙
za Pri-
meval Forest (Poland). On 30 study plots located in meadows, we measured crown volume and the density of
woody vegetation and monitored visitation and behavior of ungulates with the use of camera traps. The mean
visitation rate to meadows by European bison was 0.11 ind./day/plot, and 0.22 ind./day/plot by other un-
gulates. The duration of foraging was signicantly higher in European bison (55.8 s) than in other ungulates
(16.3 s). The density of woody vegetation on meadows varied from 13 to 6213 ind./ha and the crown volume
from 0.6 to 1145 m
3
/ha. We found that increased visitation by European bison resulted in a signicant reduction
in the density and volume of woody vegetation in meadows. The reducing effect on woody vegetation was over
eight times higher in frequently visited plots when compared to unvisited plots – the density of woody vegetation
decreased from 879 to 101 saplings/ha, while the crown volume declined from 295 to 35 m
3
/ha. In addition, the
density of woody vegetation was related to the level of meadow openness. Less open (smaller) meadows had a
signicantly higher density of woody vegetation than meadows characterized by high openness. Combined
visitation by other ungulates did not affect either the volume or density of woody vegetation. The most plausible
mechanism of observed patterns can be a remarkably higher foraging activity in meadows by bison in com-
parison to other ungulates. As a consequence, European bison, being adapted to open habitats, can effectively
reduce the growth of tree seedlings and limit tree encroachment at the initial stages of forest succession. Thus,
populations of this wild herbivore can play a role in the restoration or maintenance of open habitats and woody
pastures that serve as an important foraging ground for bison in suboptimal forests, where populations of these
herbivores were restored.
1. Introduction
The majority of large herbivores that inhabited European landscapes
in the late Pleistocene became extinct before the Pleistocene/Holocene
transition (Cooper, et al., 2015; Stuart, 2015). Very few species, such as
European bison and aurochs, survived until the Holocene; however,
forest expansion and human pressure restricted them to forests as refuge
habitats and the latter caused progressive extirpation of their pop-
ulations (Hofman-Kami´
nska et al., 2019). Survival of these open-
adapted species in forest habitats was possible probably because of the
structure of natural forests with numerous gaps, and micro-selection for
openings within forests or on their edges that supported their pop-
ulations (at low densities and tness), and also in periods of winter
vegetation scarcity (Kerley et al., 2012; Hofman-Kami´
nska et al., 2019;
Kowalczyk et al., 2019).
Although the important role of large herbivores in shaping forest
ecosystems was broadly reported (Svenning, 2002; Sandom et al., 2014),
the question of whether populations of large herbivores do indeed play a
key role in maintaining open habitats remains open. The wood-pasture
theory of Vera (2000) attributes an important role to large herbivores
under natural conditions. However, the palynological data indicate that
large herbivores did not inuence the structure of primeval forests, but
quite the opposite; the forest structure limited herbivore carrying ca-
pacity (Mitchell, 2005). Therefore, high densities of large herbivores,
necessary for the transition from woodland to grassland due to tree and
shrub browsing, bark stripping, and trampling (Gill, 2006; Bakker et al.,
2016) were often unlikely. Instead, gaps that ungulates kept open
originated rather from res and windthrows (Bradshaw and Hannon,
* Corresponding author.
E-mail address: rkowal@ibs.bialowieza.pl (R. Kowalczyk).
Contents lists available at ScienceDirect
Forest Ecology and Management
journal homepage: www.elsevier.com/locate/foreco
https://doi.org/10.1016/j.foreco.2021.119310
Received 9 February 2021; Received in revised form 12 April 2021; Accepted 24 April 2021
Forest Ecology and Management 494 (2021) 119310
2
2004).
In recent decades, grazing by wild and domestic ungulates has
become a strategy for conservation management to restore or maintain
open or half-open, structurally diverse, landscapes as substitutes for
extinct wild ancestors (e.g., Olff et al., 1999; Naundrup and Svenning,
2015). Typical non-wild grazers, such as horses and cattle, are used to
reduce tree and shrub succession on meadows (Hall and Bunce, 2019;
Garrido et al., 2021). A lack of wild megaherbivores, however, limits
inference on the impact of large herbivores on the forest structure and
creation or maintenance of open habitats. Recently, the increasing role
of European bison – the last remnant of legendary megafauna – in
ecological restoration has been recognized (Cromsigt et al., 2018). The
species was restored from captive survivors after extirpation in the wild
at the beginning of the 20th century, and successfully introduced to the
wild mainly in forest ecosystems, as the European bison was recognized
as a forest specialist (Kerley et al., 2012). However, very little is known
of its functional role in shaping forest ecosystems and maintaining open
habitats.
Large megafauna in the northern hemisphere were generally linked
to a tundra-steppe environment (Allen et al., 2010; Bocherens et al.,
2015). As shown by historical reconstruction, the remaining mega-
herbivores in the early Holocene were not able to stop forest expansion.
They most probably followed early Holocene environmental changes in
natural vegetation and human-induced transformation initiated by
Neolithic agriculture (Fyfe et al., 2015; Hofman-Kami´
nska et al., 2019).
Due to their morphological adaptations and evolutionary history, large
herbivores such as European bison or aurochs seem anomalous in forest
habitats (Mendoza and Palmqvist, 2008; Kerley et al., 2012) that pre-
disposed the European bison to serve as a model species for the devel-
opment of the refuge species concept (Kerley et al., 2012). This concept
includes species or populations that can no longer access optimal hab-
itats but are conned to suboptimal habitats which could cause
decreased tness and density, and attendant conservation risks (Kerley
et al., 2012; Lea et al., 2016). Thus, it is an unresolved question if large
herbivores, such as European bison – adapted to open or mosaic habitats
– are able to inuence the structure or composition of woody vegetation.
However, in areas where the European bison was restored, it prefers to
forage in forest gaps, clearings, river valleys, and meadows (Kowalczyk
et al., 2019; Zielke et al., 2019), and its diet includes a high proportion of
woody species (Vald´
es-Correcher et al., 2018; Kowalczyk et al., 2019).
This may suggest that bison can play some role in shaping the vegetation
structure both in forest and open habitats such as forest gaps or
meadows.
In this paper we aimed to investigate the inuence of the European
bison – the largest terrestrial herbivore – and other ungulates (moose,
red deer, and roe deer) on the development of woody vegetation in open
habitats in the Białowie˙
za Primeval Forest. We asked whether large
herbivores are able to maintain open habitats and how habitat openness
inuences their use by ungulates and animal foraging activity. We
predicted that: 1) the European bison, due to its adaptation to open
habitats and foraging behavior, including grazing and browsing, would
have a negative effect on both the density and volume of tree recruit-
ment in the open habitats; 2) other species of ungulates, mainly due to
their browsing behavior, would reduce volume, not density, of tree
vegetation only.
2. Materials and methods
2.1. Study area
The study was conducted in the Białowie˙
za Primeval Forest (BPF) –
one of the best-preserved temperate lowland forests in Europe
(52◦35′–52◦55′N, 23◦30′–24◦00′E) (Fig. 1). The study area included the
Polish part of the BPF (620 km
2
). The forest includes a mosaic of fresh
and wet mixed and deciduous forests dominated by Norway spruce Picea
abies (25%), black alder Alnus glutinosa (21%), Scots pine Pinus sylvestris
(19.0%), European hornbeam Carpinus betulus (11%), birches Betula sp.
(7%), oaks Quercus sp. (6%), and Small-leaved lime Tilia cordata (5%)
(Modzelewska et al., 2020). The continuity of the BPF is interrupted by
open river valleys, meadows (created for ungulates mainly in the 19th
century, Samojlik et al., 2019), and glades with settlements and villages
covering 7% of the area in total. The BPF is surrounded by pastures,
meadows, wasteland, and arable land interwoven with small woodlands
(Hofman-Kami´
nska and Kowalczyk, 2012). The meadows within the
forests were utilized until the 1990 s, when they fell into disuse. Some of
them were restored after 2006 in support of the LIFE bison conservation
project and are more regularly mowed. Part of the meadows within the
forest, in river valleys and abandoned meadows on settlement clearings,
are kept in a more natural condition, without mowing.
The climate of the BPF is transitional between Atlantic and conti-
nental types with clearly marked seasons. The mean annual temperature
is 7 ◦C. The coldest month is January (mean temperature −4.8 ◦C) and
the warmest is July (18.4 ◦C) (Jędrzejewska and Jędrzejewski, 1998).
The BPF is inhabited by a natural community of central European
ungulates, with red deer (Cervus elaphus) being the most abundant (6.0
ind./km
2
), followed by wild boar (Sus scrofa, 5.4/km
2
), roe deer (Cap-
reolus capreolus, 2.0/km
2
), European bison (Bison bonasus, 0.5/km
2
), and
moose (Alces alces, 0.08/km
2
) (Bubnicki et al., 2019). There are two
species of large predators present in the area, wolf (Canis lupus) and
Eurasian lynx (Lynx lynx), having a limiting impact on red and roe deer
(Okarma et al., 1997, Jędrzejewski et al., 2002; Kamler et al., 2007).
European bison are rarely predated upon by wolves (Jędrzejewski et al.,
2000, 2002).
The European bison population in the BPF is the largest of the wild
bison populations in Europe. During the study it numbered 522–578
individuals (European Bison Pedigree Book, 2014–2015). It was more
intensively managed until the late 1990s; that included supplementary
feeding in winter in a limited number of feeding sites which caused
increased aggregation of bison and culling up to 17% of the population
aimed at reducing the population and removing invalid individuals
(Hayward et al., 2011; Krasi´
nska and Krasi´
nski, 2013). Actions imple-
mented in European bison management after 2000, especially during the
LIFE conservation project in 2006–2010 aimed at spreading the popu-
lation, and reduction and modication of supplementary feeding, led to
Fig. 1. Distribution of study plots in meadows in the Białowie ˙
za Prime-
val Forest.
R. Kowalczyk et al.
Forest Ecology and Management 494 (2021) 119310
3
a split of large winter aggregations of bison, a drop in the parasitic load,
increased use of open habitats, and reduced culling (Kowalczyk et al.,
2013; Hayward et al., 2015; Kołodziej-Soboci´
nska et al., 2016). Nowa-
days culling is limited to 2% of the population annually and an
increasing proportion of bison do not aggregate in winter feeding sites
and seasonally migrate to open habitats (Kowalczyk et al., 2013; R.
Kowalczyk personal communication on the subject of annual bison
surveys conducted by the Białowie˙
za National Park). Other ungulates in
the BPF are not supplementary fed; red deer and roe deer are the subject
of limited hunting and there has been a ban on moose hunting in Poland
since 2001.
2.2. Forest succession survey
The study was conducted between June 2014 and May 2015. The
tree succession was estimated once, on 30 plots located in meadows
within and on the edges of the forest, which had not been maintained by
human activities since at least the 1990s (Figs. 1 and 2). Due to different
constraints (proximity to the river, irregular shape of mid-forest
meadows), the plots varied in size from 0.04 to 0.25 ha (0.15 ±0.09
ha, on average) and were localized up to 130 m from the forest edge
(mean 72 ±136 m). As we were not able to determine the size of
meadows on which the study plots were located, especially those lying
in the river valleys and on the edges of the forest, for the purposes of
further analysis we divided them into meadows with low (small mid-
forest meadows [<2 ha] and narrow river valleys) and high (wide
river valleys, meadows located on settlement clearings and on the edges
of the forest) openness.
On each plot, the number, species, and crown volume of trees and
shrubs were estimated with the basic ellipsoid volume formula (Thorne
et al., 2002):
2/3
π
H(A/2×B/2)
where:
H – tree or shrub height from the base to the top.
A and B – diameter readings taken perpendicularly at 50% of the
plant crown height.
Single large trees (>4 m) growing on the plots (1.4% of all trees and
shrubs recorded) were excluded from the analysis. On the basis of the
measurements, we estimated the density and total crown volume of
woody vegetation per hectare.
2.3. Ungulate survey
We used digital trail cameras (LTL AcornSGN-5210A) triggered by
passive infrared sensors with a detection angle of c. 35◦and range of
approximately 20 m. After detection, with a time lag of 1 s, a 30 s video
was recorded. When an animal was motionless, this procedure was
repeated without trigger delay. During low-light conditions, cameras
switched to a stealth infrared mode. At each plot cameras were attached
to a tree at a height of 1.5 m with a clear view of at least 20 m. Videos
were downloaded weekly.
We monitored study plots in each season: spring (March–May),
summer (June–August), autumn (September–November), and winter
(December–February) for 30 days (120 days in total). Due to different
reasons (low battery, full memory card), the effective monitoring time of
each plot was 98.2 days on average. The total number of individuals of
different ungulates recorded on each plot was divided by the total
number of monitoring days to estimate a daily visitation index for each
species. On the basis of videos or sequences of videos, the length of the
visits, and duration of foraging and other activities were estimated.
When a group of animals was simultaneously present, we only used data
for one randomly chosen focal animal, as behavior of individuals in a
group is often synchronized (Kuijper et al., 2009). Behavior of the
recorded animals was determined as: grazing, browsing, vigilance,
moving, and other (resting, grooming, wallowing, etc.). The wild boar
was excluded from the analysis because its foraging behavior differs
remarkably from other ungulates (Kuijper et al., 2009; Spitzer et al.,
2020).
Camera trap data were organized and classied using TRAPPER
software (Bubnicki et al., 2016). In total, 552 videos and video se-
quences were analyzed. Cervid species (red deer, roe deer, and moose)
were analyzed jointly, due to a lower number of video records for roe
deer and moose, and their quite similar foraging mode, different than
that of European bison (Hofmann, 1989; Kuijper et al., 2009; Merceron
et al., 2014), and lack of differences in their activity (foraging duration)
on study plots (Table A.1). Finally, as the duration of the animal visits on
Fig. 2. Example distribution (A) and vegetation structure (B–D) on study plots localized in meadows in the Białowie ˙
za Primeval Forest.
R. Kowalczyk et al.
Forest Ecology and Management 494 (2021) 119310
4
the studied plots and foraging duration were highly correlated
(Spearman test; R =0.77, P <0.001), we decided to use foraging
duration exclusively in the further analyses.
2.4. Statistical analyses
We used zero-inated negative binomial generalized linear mixed
models to test the association between foraging duration on the sam-
pling plots and the species (bison vs other ungulates) and openness index
(GLMM1). Zero-inated models account for excessive zeros in response
variables, which was the case for foraging duration (Zuur et al., 2009).
In GLMM1, we included the main effect of species, meadow openness,
and season as well as the interactive effects of the species and meadow
openness index. As the same plots were sampled multiple times, we set
plot ID as a random factor. To verify if the ungulate visitation rate and
the distance to the forest edge affected density and crown volume of
woody vegetation, we applied generalized linear models (GLM1 with
negative binomial error structure and GLM2 with gamma error struc-
ture, respectively). Before modeling we divided the ungulate visitation
rate into two variables: bison visitation rate and other ungulate visita-
tion rate. In GLM1 the response variable was the number of saplings,
while explanatory variables included bison visitation rate, other ungu-
late visitation rate, and meadow openness index (high or low). We used
the same set of independent variables in GLM2, in which the dependent
variable was the tree and shrub crown volume. In GLM1 and GLM2, we
tested the main effects of all explanatory variables and the interactive
effects of the openness index and both bison visitation rate and other
ungulate visitation rate. As the size of plots differed, we offset GLM1 and
GLM2 by adding the logarithm of the plot size to linear predictors (Zuur
et al., 2009). For GLMM1, GLM1, and GLM2, we created sets of sub-
models which were ranked with the Akaike Information Criterion (AIC)
with a second-order correction for small sample size (AIC
c
) (Burnham
and Anderson, 2002). All submodels close to the top submodel (lowest
AIC
c
), having ΔAIC ≤2, were considered to have substantial empirical
support. As the differences between AIC
c
scores among highly ranked
submodels were low for GLMM1 (Table A.2), we applied model aver-
aging on the selected set of submodels (ΔAIC ≤3). All statistical ana-
lyses were done in R (R Core Team, 2018).
3. Results
Saplings of 14 tree and shrub species were recorded on study plots
dominated by silver birch (34.5% of saplings), Norway spruce (20.4%),
pedunculate oak (15.0%), and European hornbeam (12.4%) (Table 1).
The median density of woody vegetation was 289.7 saplings/ha (range:
13–6213), and the median crown volume of woody vegetation was 61.6
m
3
/ha (range: 0.6–1145). The average volume of a single sapling was
0.8 ±0.3 m
3
and the average height was 1.0 ±0.5 m.
The mean (±SD) ungulate visitation rate was the highest in red deer
(0.19 ±0.14 ind./day/plot), followed by European bison (0.11 ±0.13),
roe deer (0.03 ±0.03) and moose (0.01 ±0.01). Combined visitation by
ungulates other than European bison was 0.22 ±0.14 ind./day/plot.
The bison visitation rate on the studied plots varied signicantly be-
tween seasons (Kruskall-Wallis test:
χ
2
=24.7, P <0.001). The highest
visitation rate was observed in spring (Fig. 3).
The duration of foraging was signicantly higher in European bison
(55.8 s, CI 95% =36.2–87.7 s) than in other ungulates (16.3 s, CI
95% =13.0–20.5 s) (Kruskall-Wallis test:
χ
2
=50.58, P <0.001)
(Fig. 4A). Bison were almost exclusively grazing (97.5% of their foraging
activity), while other ungulates were both grazing (68.8% of foraging
activity) and browsing (31.2%) when foraging on the study plots
(Fig. 4A).
Averaged GLMM1 indicated a signicant interaction between species
and the meadow openness index (Table 2, Fig. 4B, P =0.04). Unlike
other ungulates, the foraging duration of bison was signicantly higher
in meadows with low openness compared to meadows with high open-
ness (Table 2, Fig. 4B, P =0.01).
For both the surveyed models (GLM1 and GLM2), among all com-
binations of the submodels considered, the single top-ranked submodels
were the best models (Table A.2). In GLM1, the top-ranked submodel
included the main effect of the bison visitation rate and openness index,
while in GLM2 it was based on the bison visitation rate exclusively
(Table A.2). The results of GLM1 and GLM2 indicated that both tree and
shrub numbers and their crown volume decreased signicantly with an
increasing bison visitation rate (GLM1: P =0.004; GLM2: P =0.03,
Table 3, Fig. 5). With the bison visitation rate increasing from 0 to 0.5/
day/plot the woody vegetation density decreased from 879 to 101
saplings/ha (Fig. 5A) while the crown volume declined from 295 to 35
m
3
/ha (Fig. 5C). In addition, the density of woody vegetation differed
signicantly between the high and low openness index (Table 3,
Fig. 5B). GLM1 predicted 3.3 times more saplings per hectare on
meadows with low openness compared to meadows with high openness
(Fig. 5B). The visitation rate of other ungulates and the distance to the
forest edge were not among explanatory variables in the selected sub-
models for either density or crown volume of woody vegetation
(Table A.2).
Table 1
Proportion of saplings of different tree and shrub species succeeding in
the open habitats in the Białowie˙
za Primeval Forest.
Species Proportion of saplings (%)
Betula pendula 34.50
Picea abies 20.44
Quercus robur 15.04
Carpinus betulus 12.36
Alnus glutinosa 7.03
Salix sp. 2.88
Prunus sp. 2.79
Rhamnus catharticus 1.53
Pinus sylvestris 1.10
Corylus avellana 1.07
Populus tremula 0.44
Sorbus aucuparia 0.40
Frangula alnus 0.32
Tilia cordata 0.1
Fig. 3. Seasonal indices of European bison visitation to open habitats in the
Białowie˙
za Primeval Forest.
R. Kowalczyk et al.
Forest Ecology and Management 494 (2021) 119310
5
4. Discussion
Our study shows the clear impact of the largest European herbivore
foraging on tree encroachment in open habitats located within a large
forest complex. As predicted, European bison substantially reduced both
the density and volume of woody vegetation on meadows. Contrary to
our prediction, other ungulates (cervids) did not affect either the volume
or the density of tree recruitment in open habitats. The majority of bovid
species, including European bison, are morphologically adapted to open
habitats (Mendoza and Palmqvist, 2008). Their wide muzzle makes
them less selective when grazing or browsing on the ground (Hofmann,
1989). They usually take large bites of food and their selection is limited
more to food patches than individual plants. The European bison pri-
marily is a grazer or mixed feeder (Hofmann, 1989), however studies of
their diet indicate that they are extensively foraging on browse
(including woody species and forbs), and continuously adjusting their
diet to seasonal availability of easily digestible non-grass vegetation
(Gębczy´
nska et al., 1991; Kowalczyk et al., 2011, 2019; Merceron et al.,
2015). Recent studies using DNA-based analysis of European bison diet
shows that woody vegetation constitutes 60–80% of plant biomass
consumed during the growing season (Kowalczyk et al., 2019; Hartvig
et al., 2021). The majority of woody species recorded on study plots was
previously reported in bison diet (Kowalczyk et al., 2011, 2019). They
forage more frequently on leaves than twigs (Cromsigt et al., 2018).
When foraging on the ground, which was the main behavior of bison in
this study, they are not selective and also take woody seedlings, limiting
their growth and reducing their numbers and related volume.
After extirpation in the wild, European bison populations were
restored mainly in forest habitats (Kerley et al., 2012). However, in this
non-optimal environment, they strongly select for open habitats such as
woody pastures, clearings, and river valleys (Kowalczyk et al., 2013,
2019; Zielke et al., 2019). Thus, their impact on woody vegetation can
be much higher in open areas than in forest habitats. As shown by
studies in the BPF, the impact of ungulate browsing on trees growing in
forest gaps was 1.5 times higher than in closed forest (Kuijper et al.,
2009). This relates mainly to red deer, the most abundant species in the
BPF (Borowik et al., 2016). This difference for bison can be even higher
(Kuijper et al., 2009), due to their strong preference for open habitats,
which may result in signicant limitation of tree succession in these
habitats.
Studies on the inuence of large herbivores on tree succession
showed that they could signicantly limit the development of woody
vegetation (Olden et al., 2017; Vald´
es-Correcher et al., 2018; ¨
Ollerer
et al., 2019; Garrido et al., 2021) or completely remove all tree seedlings
(Smit et al., 2015). However, the majority of these studies related mainly
to domesticated species, often kept at high density in fenced areas. Wild
and domesticated large herbivores may differ in their diets and the way
they inuence vegetation structure (Cromsigt et al., 2018). Our study
has shown that European bison can reduce tree encroachment in open
habitats, and the reducing impact was increasing with the growing
Fig. 4. Duration of foraging (predicted time ±CI 95%) and proportion of grazing and browsing (A) and inuence of meadow openness on duration of foraging (B) by
ungulates in Białowie ˙
za Primeval Forest.
Table 2
Model-averaged coefcients of independent variables calculated based on the
condence set of the most parsimonious models (ΔAIC
c
≤3) investigated to test
the differences in foraging duration of the bison and other ungulates (moose, red
deer, roe deer) on meadows in relation to an index of meadow openness
(GLMM1). Plot ID was set as a random factor. Reference levels are presented in
parenthesis.
Coefcients Estimate SE z-
value
P
Intercept
Bison, low 4.23 0.17 24.8 <0.001
Species
Other ungulates, low (bison, low) −1.42 0.18 7.86 <0.001
Other ungulates, high (bison, high) −0.97 0.32 3.01 0.003
Openness
High, bison (low, bison) −0.69 0.28 2.48 0.01
High, other ungulates (low, other
ungulates)
−0.04 0.18 0.24 0.81
Species ×Openness 0.65 0.31 2.09 0.04
Table 3
Results of the top-ranked (the lowest AIC
c
scores) generalized linear models
GLMs testing association between: the number of saplings and both bison visi-
tation rate and meadow openness index (GLM1); the crown volume of woody
vegetation and bison visitation rate (GLM2). Reference level is presented in
parenthesis.
Coefcients Estimate SE t-value P
GLM1 The number of saplings
(Intercept) 7.37 0.30 24.2 <0.001
Bison visitation rate −4.31 1.49 −2.89 0.004
Openness index
high (low) −1.18 0.39 −3.03 0.002
GLM2
The crown volume
(Intercept) 5.69 0.32 17.8 <0.001
Bison visitation rate −4.24 1.89 −2.24 0.03
R. Kowalczyk et al.
Forest Ecology and Management 494 (2021) 119310
6
visitation rate. As the BPF provides rich habitats with a mosaic structure
and is dominated by deciduous tree stands (Jędrzejewska and Jędrze-
jewski, 1998; Niedziałkowska et al., 2010), European bison densities are
higher here than in other forests, especially coniferous ones (Kerley
et al., 2020). We can only speculate if the same effect could have been
observed at low bison densities or in the past. It was proposed by some
authors that large native herbivores have been key agents in creating or
maintaining open habitats (Svenning, 2002). Historical data indicate
quite low densities of European bison in forests (Samojlik et al., 2019).
Nowadays, in many areas, European bison are supplementary fed
(Kerley et al., 2012), which increases their survival, and probably
reproduction, leading to increased densities. Historical and contempo-
rary analysis of bison habitat use and diet shows that this large herbivore
is tracking habitat structure rather than reducing forest expansion at the
larger scale (Hofman-Kami´
nska et al., 2018, 2019). However, due to the
selection of open habitats by bison (Kowalczyk et al., 2019; Zielke et al.,
2019), their reducing impact on the vitality of woody species is more
pronounced in open habitats and can lead to strong effects on vegetation
structure and composition, including not only removal of tree seedlings
at the initial stage, but also reducing vitality of larger shrubs and trees
(Vald´
es-Correcher et al., 2018). Thus, European bison can play an
important role in the restoration of open habitats, and facilitate biodi-
versity (Svenning, 2002; Sandom et al., 2014).
The visitation of meadows by European bison was highest in spring.
This may result from the availability of easily digestible fresh leaves of
woody vegetation and forbs that start their development earlier in the
open than in forest habitats. Foraging in meadows can be less protable
with the progressing vegetation senescence during summer when bison
can face a trade-off between forage quality and abundance. With
increasing forb biomass, meadows become dominated by tall grasses
which decrease the accessibility of other plants and reduce foraging
efciency. For large herbivores, the spatial distribution of forage and its
nutritive value are the most important factors inuencing foraging
behavior, resource selection, and space use (Bailey et al., 1996; Prins
and van Langevelde, 2008). As large herbivores prefer low or interme-
diate vegetation biomass (Raynor et al., 2016), foraging in forests in
summer on seasonally changing vegetation is more protable than on
meadows with high vegetation biomass of declining digestibility. During
summer, the bison increase foraging on protein-rich plants such as Rubus
ideaus or Urtica dioica (Kowalczyk et al., 2019), readily available in the
forest. Additionally, a declining concentration of leaf nutrients such as
nitrogen, phosphorus, and potassium in summer makes woody vegeta-
tion browsing less protable with leaf senescence (Tamm, 1951). Thus,
the European bison probably adjusts its habitat selection to seasonal
variation of forage biomass and quality. Very low visitation in autumn
and winter may be inuenced by increased use of mowed meadows
offering higher quality vegetation, seasonal migrations to open and
agriculture areas, or use of supplementary feeding sites (Radwan et al.,
Fig. 5. Predicted association between woody vegetation density and both bison visitation rate (A) and meadow openness index (B), and between crown volume and
bison visitation rate (C) in open habitats of the Białowie ˙
za Primeval Forest. Shaded areas show 95% condence intervals.
R. Kowalczyk et al.
Forest Ecology and Management 494 (2021) 119310
7
2010; Kowalczyk et al., 2013).
Ungulate browsing can strongly reduce seedling density, as shown
for some temperate forest ecosystems (Kumar and Shibata, 2007; Long
et al., 2007; Olesen and Madsen, 2008). However, we found no effect of
other ungulate browsing on woody vegetation encroachment in the BPF.
This may be related to relatively low ungulate densities in the BPF
compared to other study areas (Borowik et al., 2016) and high avail-
ability of undergrowth woody vegetation in forest habitats (Kowalczyk
et al., 2011). When emerging into the open, deer have high access to
forbs, and may concentrate their browsing only on palatable species of
trees. However, probably the most plausible mechanism for the
observed pattern is the difference in foraging activity of bison when
compared to other ungulates. Although cervids were visiting the study
plots with higher frequency, the duration of their foraging was nearly
3.5 times shorter than for European bison. Additionally, cervids dedi-
cated a lower proportion of time to foraging on ground vegetation when
compared to bison. The review of the effects of wild ungulates on
regeneration, structure, and functioning of temperate forests showed
that forest regeneration was most sensitive to immediate browsing and
trampling impacts of small seedlings (Ramirez et al., 2018). Thus,
grazing probably more efciently inuences both the abundance and
volume of woody vegetation. The preferred foraging height of red deer,
the most common cervid in the BPF and on our study plots, is 50–150 cm
(Renaud et al., 2003; Kuijper et al., 2010), and their browsing increases
with the height of the trees (van Beeck Calkoen et al., 2019). An
exclosure experiment in the BPF showed that ungulates (mainly red
deer), played a dominant role in affecting tree recruitment only for size
classes >50 cm (Kuijper et al., 2010). Thus, cervids are not able to
effectively limit woody vegetation encroachment at initial phases
compared with the European bison, but may probably reduce its volume
at higher height classes as predicted by us, however it was not observed
during our study. Furthermore, cervids foraged on meadows less than
bison. Earlier studies showed their preference towards gaps in the forest
(Kuijper et al., 2009), however, the duration of their visits to the studied
meadows was much shorter than observed in forest gaps (Kuijper et al.,
2009). Openings in the forest are preferentially used for predation by
Eurasian lynx (Podg´
orski et al., 2008), for which the roe deer and red
deer are their main prey (Okarma et al., 1997). As forest meadows are
characterized by a larger size and higher visibility than forest gaps, they
thus offer lower cover protection against predators. Experimental
studies showed reduced visitation duration for red deer and roe deer
when exposed to predator scent, and a tendency to shorten the visitation
in areas characterized by higher visibility (Kuijper et al., 2014; Wikenros
et al., 2015). For bison, predation from wolves is marginal (Jędrzejewski
et al., 2000, 2002), and most likely does not inuence their behavior as
much as the case of cervids. Interestingly, bison foraging on smaller
meadows was longer than on large meadows, despite higher woody
vegetation density on smaller meadows. This is probably related to the
location of the meadows. Smaller meadows were more often located
within the forest, while larger meadows on the edges of the forest in
closer proximity to human settlements. It was shown that human
avoidance may play some role in European bison behavior and space use
(Hayward et al., 2015; Haidt et al., 2018). We recorded longer foraging
by bison on meadows with low openness (smaller meadows) that were
characterized by higher woody vegetation density than meadows with
high openness. This gives some indication on causality of meadow
visitation by bison, i.e., if increasing meadow openness determines their
use. We found rather the opposite, however this could be inuenced by
factors other than openness, as explained above. It leads to the conclu-
sion that it is the increasing visitation rate that keeps meadows opened,
rather than openness attracting bison and inuencing the higher visi-
tation rate.
We found a higher density of woody vegetation on meadows with
lower openness (smaller meadows). Tree succession in open habitats is a
function of numerous factors including distance to the forest edge, tree
species, and seed adaptations (Clark et al., 1999; Heydel et al., 2014)
and is usually initiated from the edge of the forest-open habitat ecotone
(Copenheaver et al., 2004). Thus, smaller openings should be charac-
terized by a higher density of woody vegetation, as observed on our
study plots. As many as two thirds of recruiting trees were wind-
dispersed species, including the most abundant on the studied
meadows: birch and Norway spruce. The other species, such as oak or
hornbeam, can be dispersed over larger distances (up to 1000 m) by the
European jay, common in the area (G´
omez, 2003; Pons and Pausas,
2007).
5. Conclusions
Our study shows that large herbivore populations can play a role in
open habitat maintenance. As European farmland is now being aban-
doned, especially in remote areas (Alcantara et al., 2013), and strong
environmental change (mainly forest succession) and a shift from live-
stock to wildlife-dominated assemblages is observed (Speed et al.,
2019), the growing global population of bison (5% annually over the last
decade, Plumb et al., 2020), and the increasing role European bison play
in ecological restoration programs, make the species a potential key
agent for shaping vegetation structure in some specic conditions, and a
valuable alternative for livestock – widely used nowadays in maintain-
ing woody pastures and open habitats. However, it is worth emphasizing
that cattle and European bison differ in their impact on woody vegeta-
tion. European bison strip bark more, whereas cattle browse on twigs,
thus bison can have a stronger negative effect on woody plant survival
and may curb or even reverse woody encroachment in areas of intensive
use (Cromsigt et al., 2018).
The European bison is recognized by the IUCN as a near threatened
species (Plumb et al., 2020), thus abandoned farmland (especially in
eastern Europe) and a mosaic of forests and open habitats are suitable
for species restoration (Kerley et al., 2020) but taking into account
conservation regimes and related risks for this unique herbivore. The
maintenance of sustainable wild native ungulate populations is an
important mechanism in both the conservation and restoration of forest
ecosystems (Apollonio et al., 2017). Restoration of large herbivore
populations and the maintenance of open habitats with related biolog-
ical diversity should be recognized by policymakers as one of the
possible land management options in Europe, particularly in marginal
areas (Navarro and Pereira, 2012).
CRediT authorship contribution statement
Rafał Kowalczyk: Conceptualization, Methodology, Supervision,
Formal analysis, Writing - original draft. Tomasz Kami´
nski: Software,
Data curation, Investigation. Tomasz Borowik: Software, Formal
analysis, Visualization.
Declaration of Competing Interest
The authors declare that they have no known competing nancial
interests or personal relationships that could have appeared to inuence
the work reported in this paper.
Acknowledgements
We would like to thank Prof. Petter Kjellander and two anonymous
reviewers for their useful comments on earlier versions of the
manuscript.
Funding
The study was funded by the Mammal Research Institute, Polish
Academy of Sciences budget.
R. Kowalczyk et al.
Forest Ecology and Management 494 (2021) 119310
8
Appendix A. Supplementary material
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.foreco.2021.119310.
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