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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 Białowieża Primeval 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 significantly 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 significant 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 significantly 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 comparison 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.
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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
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
European bison
Bison bonasus
za Primeval Forest
Tree encroachment
Forest succession
Key species
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 signicantly 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
/ha. We found that increased visitation by European bison resulted in a signicant 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
/ha. In addition, the
density of woody vegetation was related to the level of meadow openness. Less open (smaller) meadows had a
signicantly 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 inuence 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: (R. Kowalczyk).
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Received 9 February 2021; Received in revised form 12 April 2021; Accepted 24 April 2021
Forest Ecology and Management 494 (2021) 119310
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
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 conned 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 inuence 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
In this paper we aimed to investigate the inuence 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
inuences 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
(52355255N, 23302400E) (Fig. 1). The study area included the
Polish part of the BPF (620 km
). 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
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
), followed by wild boar (Sus scrofa, 5.4/km
), roe deer (Cap-
reolus capreolus, 2.0/km
), European bison (Bison bonasus, 0.5/km
), and
moose (Alces alces, 0.08/km
) (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 522578
individuals (European Bison Pedigree Book, 20142015). 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 20062010 aimed at spreading the popu-
lation, and reduction and modication 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
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):
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. 35and 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 (MarchMay),
summer (JuneAugust), autumn (SeptemberNovember), and winter
(DecemberFebruary) 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.,
Camera trap data were organized and classied 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 (BD) on study plots localized in meadows in the Białowie ˙
za Primeval Forest.
R. Kowalczyk et al.
Forest Ecology and Management 494 (2021) 119310
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-inated 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-inated 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
) (Burnham
and Anderson, 2002). All submodels close to the top submodel (lowest
), having ΔAIC 2, were considered to have substantial empirical
support. As the differences between AIC
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:
136213), and the median crown volume of woody vegetation was 61.6
/ha (range: 0.61145). The average volume of a single sapling was
0.8 ±0.3 m
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 signicantly be-
tween seasons (Kruskall-Wallis test:
=24.7, P <0.001). The highest
visitation rate was observed in spring (Fig. 3).
The duration of foraging was signicantly higher in European bison
(55.8 s, CI 95% =36.287.7 s) than in other ungulates (16.3 s, CI
95% =13.020.5 s) (Kruskall-Wallis test:
=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 signicant interaction between species
and the meadow openness index (Table 2, Fig. 4B, P =0.04). Unlike
other ungulates, the foraging duration of bison was signicantly 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 signicantly 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
/ha (Fig. 5C). In addition, the density of woody vegetation differed
signicantly 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
za Primeval Forest.
R. Kowalczyk et al.
Forest Ecology and Management 494 (2021) 119310
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
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 6080% 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 signicant limitation of tree succession in these
Studies on the inuence of large herbivores on tree succession
showed that they could signicantly limit the development of woody
vegetation (Olden et al., 2017; Vald´
es-Correcher et al., 2018; ¨
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 inuence 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 inuence of meadow openness on duration of foraging (B) by
ungulates in Białowie ˙
za Primeval Forest.
Table 2
Model-averaged coefcients of independent variables calculated based on the
condence set of the most parsimonious models (ΔAIC
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
Coefcients Estimate SE z-
Bison, low 4.23 0.17 24.8 <0.001
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
High, bison (low, bison) 0.69 0.28 2.48 0.01
High, other ungulates (low, other
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
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
Coefcients 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
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
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
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 protable
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
efciency. For large herbivores, the spatial distribution of forage and its
nutritive value are the most important factors inuencing 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 protable 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 protable 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 inuenced 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% condence intervals.
R. Kowalczyk et al.
Forest Ecology and Management 494 (2021) 119310
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 efciently inuences 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 50150 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 inuence 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 inuenced 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 inuencing 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,
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 specic 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 inuence
the work reported in this paper.
We would like to thank Prof. Petter Kjellander and two anonymous
reviewers for their useful comments on earlier versions of the
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
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... (6%) and small-leaved lime Tilia cordata (5%) (Modzelewska et al. 2020). Open habitats (6% of BPF area) include river valleys, forest meadows and glades with human settlements (Fig. 1;Sokołowski 2004;Kowalczyk et al. 2013Kowalczyk et al. , 2021. BPF is inhabited by five ungulate species, roe deer, red deer (Cervus elaphus), moose (Alces alces), European bison and wild boar (Sus scrofa), as well as two large predators: grey wolf (Canis lupus) and Eurasian lynx (Lynx lynx). ...
... In the case of European bison, we can expect a limited intake of supplementary fodder and a larger area of the BPF utilized by bison during milder weather conditions. Such changes can have a diverse impact on the ecosystem functioning through their influence on nutrient cycling (Melis et al. 2007;Jaroszewicz et al. 2013), vegetation growth, forest succession (Kowalczyk et al. 2021) and the availability and distribution of carrion (Selva et al. 2003). Furthermore, increased bison mobility seems to be also favourable because smaller bison aggregations may decrease parasite and disease transmission (Kołodziej-Sobocińska 2016a, b) and diffuse browsing from feeding sites areas (Jaroszewicz et al. 2017). ...
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Supplementary feeding is a commonly used wildlife management practice, but while it may bring benefits and fulfil management goals, it can also result in unintended negative consequences. In the temperate zone, winter supplementary feeding may reduce movement of some ungulate species, leading to increased utilization of feeding sites by individuals and, consequently, animal aggregation. However, the intensity of feeding site utilization can vary depending on various extrinsic factors, e.g. habitat type, population density or weather conditions. Here, we predicted that the index of feeding sites utilization, expressed as the distance of European bison (Bison bonasus) to feeding sites, would be positively associated with the severity of winter conditions; thus, bison will be closer to feeding sites on colder days and in the presence of snow cover. We analysed winter (December to March) tracking data of 43 VHF- and GPS-collared European bison (24 males and 19 females) collected from 2005 to 2012 in Białowieża Primeval Forest (NE Poland), where bison are supplementally fed with different intensity throughout winter. Female bison were closer to feeding sites than males throughout winter, and regardless of sex, bison were the closest to feeding sites in mid-winter (January to February) and on colder days independently of the time of the season. Additionally, the distances of bison to feeding sites were significantly related to snow cover and depth; i.e. bison were closer to the feeding sites on days with present snow cover and deeper snow. Hence, the winter area occupied by bison differed with changing weather severity — being 4 and 28 times larger in the warmest periods compared to the coldest days with snow cover (for females and males, respectively). This may have direct and indirect ecological consequences for the ecosystem due to potential impact on nutrient cycling, seed dispersal, interspecific competition, vegetation growth, forest succession and carrion distribution. Given these ecological impacts of bison and weather-dependent utilization of supplementary fodder, we recognize the possible need in the future to revise and adapt winter supplementary feeding to annual and seasonal variation in winter severity to meet management goals while optimizing the costs.
... Although the study did not specifically address the effect of browsing on tree regeneration, in the south-eastern part of the wood-pasture, we observed a "brush" of the middle-aged hornbeam saplings, evenly "coppiced" by cattle, just in the way the wild ungulates browse this species in the Białowieża Forest [46,47]. In general, except for the locally occurring sprouts and saplings, and a small grove of the young alder-birch thicket in the south eastern part of the wood-pasture, the livestock had almost no unaided access to the arboreal forage. ...
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Recent Socio-economic changes resulted to mass abandonment of agricultural lands in Central-Eastern Europe. This leads to landscapes homogenisation, especially the disappearance of semi-open habitats of the farmland-woodland interface. The information on potentials of transforming feral, abandoned landscapes to wood-pastures is limited. We studied the ecological features and silvopastoral benefits of a landscape subjected to intensive cattle grazing after ~20 years of abandonment, i.e. the mosaic of habitats, cattle’s preference for habitats and for arboreal forages. The nutritional characteristics of arboreal forage and herbaceous forage were compared. After the initial increase in the landscape’s woodland share, cattle grazing halted further woody succession and stabilised the landscape structure, with treeless grassland occupying 49% of the landscape (most preferred by cattle with regard to the time spent), followed by treed grassland (19%), pioneering birch/alder groves (13%), riparian vegetation (12%, least preferred by cattle), and close-canopy woods (6%). The consumption intensity of arboreal forages was on about 4.5 folds higher than that of herbaceous forage. Our study proved that the grazing herd of arobust cattle breed can turn a feral, post-agricultural land into a working wood pasture, consisting of interconnected open grasslands and various facets of woodland, which seldom occur in contemporary high forests. We advocate for the transition management of abandoned farmlands towards integrated silvopastoral landscapes for sustainable provision of multiple ecosystem services that cannot be provided by segregated agriculture and forestry.
... The use of "herbivore functional traits" (equivalent to the already accepted concept of plant functional traits) and different ways to incorporate linkages between plant and herbivores into process-based models have been suggested [3••]. This issue is not limited to tropical or natural forests, as the influence of large herbivores on tree and shrub density in boreal [66] and temperate forests [67] has been reported, with or without management. ...
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Purpose of Review: Forest models are becoming essential tools in forest research, management, and policymaking but currently are under deep transformation. In this review of the most recent literature (2018-2022), we aim to provide an updated general view of the main topics currently attracting the efforts of forest modelers, the trends already in place, and some of the current and future challenges that the field will face. Recent Findings: Four major topics attracting most of on current modelling efforts: data acquisition, productivity estimation, ecological pattern predictions, and forest management related to ecosystem services. Although the topics may seem different, they all are converging towards integrated modelling approaches by the pressure of climate change as the major coalescent force, pushing current research efforts into integrated mechanistic, cross-scale simulations of forest functioning and structure. Summary: We conclude that forest modelling is experiencing an exciting but challenging time, due to the combination of new methods to easily acquire massive amounts of data, new techniques to statistically process such data, and refinements in mechanistic modelling that are incorporating higher levels of ecological complexity and breaking traditional barriers in spatial and temporal scales. However, new available data and techniques are also creating new challenges. In any case, forest modelling is increasingly acknowledged as a community and interdisciplinary effort. As such, ways to deliver simplified versions or easy entry points to models should be encouraged to integrate non-modelers stakeholders into the modelling process since its inception. This should be considered particularly as academic forest modelers may be increasing the ecological and mathematical complexity of forest models.
... European bison can have an impact on plant species composition and seed bank through endo-and epizoochory [14][15][16], as well as direct grazing and debarking in the forest habitats [17], which may also lead to significant damage to tree stands [18,19]. The ecological role of the European bison in influencing the biodiversity of open areas [20] and its indirect impact on invertebrates in forest habitats was also indicated [21]. ...
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Despite the growing population of European bison (Bison bonasus), it is necessary to plan the reintroduction of these animals to new areas. Reintroduction of European bison often requires the improvement of natural conditions. Such preparatory activities allow European bison to more easily adapt to new places, but also impact the functioning of animals from other taxa. The aim of the presented study was to examine the impact of waterholes for European bison on the development of local populations of amphibians and dragonflies (Odonata), as well as the creation of new feeding grounds for bats. We examined 15 reservoirs in the Augustów Forest District located in northeastern Poland, of which five were waterholes for European bison built in 2013–2014, four were semi-natural reservoirs transformed into waterholes for European bison in 2018, and six were natural reservoirs. Dragonflies were studied in 2021–2022; amphibians in 2018 and 2020; and bats in 2018, 2019, and 2020. In total, 24 species of dragonflies (Odonata), 10 species of amphibians, and 13 species of bats were found. The results of the inventory of three taxonomic groups using different comparative variants indicate a significant impact of the construction of waterholes for European bison on the biodiversity of the forest ecosystem. We concluded that the waterholes for European bison present better resistance to drying out than natural reservoirs. In addition, waterholes warm up more quickly, supporting better conditions for amphibians. The surface of the reservoirs and their exposed surroundings are favorable for insects (including dragonflies), and these are a source of food for bats, becoming attractive feeding grounds for them.
... Particularly for E. bison conservation, such herds can be highly valuable (Plumb et al., 2020). Given the species' high vulnera- (Dvorský et al., 2022;Kowalczyk et al., 2021) and to wildfire prevention (Rouet-Leduc et al., 2021). Finally, reintroductions, even in isolated patches, will contribute to the global conservation of iconic wildlife and threatened species and can support regional development in rural areas (Helmer et al., 2015;Margaryan & Wall-Reinius, 2017). ...
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Aim Several large‐mammal species in Europe have recovered and recolonized parts of their historical ranges. Knowing where suitable habitat exists, and thus where range expansions are possible, is important for proactively promoting coexistence between people and large mammals in shared landscapes. We aimed to assess the opportunities and limitations for range expansions of Europe's two largest herbivores, the European bison (Bison bonasus) and moose (Alces alces). Location Central Europe. Methods We used large occurrence datasets from multiple populations and species distribution models to map environmentally suitable habitats for European bison and moose across Central Europe, and to assess human pressure inside the potential habitat. We then used circuit theory modeling to identify potential recolonization corridors. Results We found widespread suitable habitats for both European bison (>120,000 km²) and moose (>244,000 km²), suggesting substantial potential for range expansions. However, much habitat was associated with high human pressure (37% and 43% for European bison and moose, respectively), particularly in the west of Central Europe. We identified a strong east–west gradient of decreasing connectivity, with major barriers likely limiting natural recolonization in many areas. Main conclusions We identify major potential for restoring large herbivores and their functional roles in Europe's landscapes. However, we also highlight considerable challenges for conservation planning and wildlife management, including areas where recolonization likely leads to human–wildlife conflict and where barriers to movement prevent natural range expansion. Conservation measures restoring broad‐scale connectivity are needed in order to allow European bison and moose to recolonize their historical ranges. Finally, our analyses and maps indicate suitable but isolated habitat patches that are unlikely to be colonized but are candidate locations for reintroductions to establish reservoir populations. More generally, our work emphasizes that transboundary cooperation is needed for restoring large herbivores and their ecological roles, and to foster coexistence with people in Europe's landscapes.
... In most terrestrial biomes large mammalian herbivores are critical agents shaping and maintaining ecosystem dynamics and heterogeneity of habitats (Jones et al., 1994;Linnell et al., 2020;Pringle, 2008;Waldram et al., 2008). The large size of their bodies and their common tendency to live in groups of variable size, combined with their feeding preferences, metabolic traits, behaviour, movement and other life history traits significantly affect the composition, species turnover, structure, nutrient flows and other ecological characteristics of plant communities (Asner et al., 2009;Boulanger et al., 2018a;Kowalczyk et al., 2021;Olff and Ritchie, 1998;Pringle et al., 2007;Ruifrok et al., 2015;Smit et al., 2015). The strongest effects on vegetation typically arise directly from selective consumption of plants (Asner et al., 2009;Fløjgaard et al., 2018) and trampling damage associated with animal mobility and other behavioural patterns (Schrama et al., 2013). ...
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Many plant species develop fruits to attract animals that will eat them and then disperse the seeds. However, there are many plant species, whose seeds are dispersed endozoochorically, but their fruits are not particularly attractive to animals. The “Foliage is the fruit” (FF) hypothesis proposes that entire biomass of the plant exists to encourage herbivores to eat it, in order to enhance seed intake and dispersal (Janzen, 1984). We tested the FF hypothesis by combining the results from the greenhouse seedling emergence method (GR) and DNA-metabarcoding of plant remnants in faeces of European moose (Alces alces L.). We processed 665 samples by the GR and 429 by the MB method, hypothesizing that if the safe passage of seeds through the gut of a large herbivore is the result of an evolutionary adaptation to endozoochoric dispersal, then the species composition of plants revealed by the two methods should largely overlap and the abundance of seedlings revealed by the GR method should be positively correlated in time with the read abundance of DNA of the same species. The large discrepancy between the lists of species detected by DNA metabarcoding and the GR method argues against the FF hypothesis. However, in the case of Urtica dioica, Lysimachia vulgaris and Lythrum salicaria, some clues of evolutionary adaptation to endozoochoric dispersal were revealed for: 1) their foliage is attractive to herbivores; 2) seeds are small, rounded in shape, yielded in large numbers and pass safely through the herbivore's gut; 3) the abundance of seeds (seedlings) was significantly and strongly influenced by the abundance of the plant biomass (DNA reads) in dung samples; 4) peaks in seed abundance and biomass consumption coincided in time. However, it should be considered that moose's diet is mostly composed of woody browse, which makes this animal not an optimal model for testing the Janzen's hypothesis and studies on typical grazers are needed in this respect.
... Although shrub layer cover increased on average across the sites of our study, herbivory reduced it (Fig. 2a). This finding is consistent with other studies showing that herbivory can reduce the density and volume of woody vegetation 36,53,66 . Changes in tree layer cover, however, did not covary with changes in herbivory, and were furthermore not directional (Fig. 2c). ...
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Ungulate populations are increasing across Europe with important implications for forest plant communities. Concurrently, atmospheric nitrogen (N) deposition continues to eutrophicate forests, threatening many rare, often more nutrient-efficient, plant species. These pressures may critically interact to shape biodiversity as in grassland and tundra systems, yet any potential interactions in forests remain poorly understood. Here, we combined vegetation resurveys from 52 sites across 13 European countries to test how changes in ungulate herbivory and eutrophication drive long-term changes in forest understorey communities. Increases in herbivory were associated with elevated temporal species turnover, however, identities of winner and loser species depended on N levels. Under low levels of N-deposition, herbivory favored threatened and small-ranged species while reducing the proportion of non-native and nutrient-demanding species. Yet all these trends were reversed under high levels of N-deposition. Herbivores also reduced shrub cover, likely exacerbating N effects by increasing light levels in the understorey. Eutrophication levels may therefore determine whether herbivory acts as a catalyst for the “N time bomb” or as a conservation tool in temperate forests.
... Such habitats are still under threat, and together with reductions in greenhouse gas emissions to prevent catastrophic climate change, it is also imperative that we retain these, and other natural and semi-natural habitats in the landscape through the restoration of natural or seminatural grazing regimes. Restoring large grazers back into landscape will not only counteract homogenising woody densification 55,56 , but is also important for enhancing dispersal and facilitating colonisations to track climate warming in many plant species 57,58 . ...
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Serious concerns exist about potentially reinforcing negative effects of climate change and land conversion on biodiversity. Here, we investigate the tandem and interacting roles of climate warming and land-use change as predictors of shifts in the regional distributions of 1701 plant species in Sweden over 60 years. We show that species associated with warmer climates have increased, while grassland specialists have declined. Our results also support the hypothesis that climate warming and vegetation densification through grazing abandonment have synergistic effects on species distribution change. Local extinctions were related to high levels of warming but were reduced by grassland retention. In contrast, colonisations occurred more often in areas experiencing high levels of both climate and land-use change. Strong temperature increases were experienced by species across their ranges, indicating time lags in expected warming-related local extinctions. Our results highlight that the conservation of threatened species relies on both reduced greenhouse gas emissions and the retention and restoration of valuable habitat. Land use change has been the dominant anthropogenic driver of plant distribution change, but climate change has also become a major factor. This analysis of long-term data shows that warming likely reinforced the impact of grassland abandonment on plant species distribution change in Sweden.
Trophic rewilding is increasingly applied in restoration efforts, with the aim of reintroducing the ecological functions provided by large-bodied mammals and thereby promote self-regulating, biodiverse ecosystems. However, empirical evidence for the effects of megafauna introductions on the abundance and richness of other organisms such as plants and invertebrates, and the mechanisms involved still need strengthening. In this study, we use environmental DNA (eDNA) metabarcoding of dung from co-existing feral cattle and horses to assess the seasonal variation in plant diet and dung-associated arthropods and nematodes. We found consistently high diet richness of horses, with low seasonal variability, while the generally lower dietary diversity of cattle increased substantially during summer. Intriguingly, season-specific diets differed, with a greater proportion of trees in the horses' diet during winter, where cattle relied more on shrubs. Graminoids were predominantly found in the diet of horses, but were generally underrepresented compared to previous studies, possibly due to the high prevalence of forbs in the study area. Dung-associated arthropod richness was higher for cattle, largely due to a high richness of flies during summer. Several species of dung-associated arthropods were found primarily in dung from one of the two herbivores, and our data confirmed known patterns of seasonal activity. Nematode richness was constantly higher for horses, and nematode communities were markedly different between the two species. Our results demonstrate complementary effects of cattle and horses through diet differences and dung-associated invertebrate communities, enhancing our understanding of large herbivore effects on vegetation and associated biodiversity. These results are directly applicable for decision-making in rewilding projects, suggesting biodiversity-benefits by inclusion of functionally different herbivores.
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Background: In the past decades, the abandonment of traditional land use practices has determined landscape changes inducing reforestation dynamics. This phenomenon can be contrasted with rewilding practices, i.e., the reintroduction of animals that may promote the recovery of landscape diversity. In this study, we explore the dynamics of expansion of two reintroduced populations of wild ungulates, Italian roe deer (Capreolus capreolus italicus) and red deer (Cervus elaphus), assessing their contribution in the recovery of landscape diversity. Methods: By using direct and indirect information on the two species, collected by nocturnal and diurnal surveys and camera trapping, we modelled a habitat suitability map, and estimated the density and distribution of the populations. We also performed a land use changes analysis, combining the presence of wild ungulates and livestock. Results and Discussion: We demonstrated that deer dispersed gradually from their release location, increasing in population size, and this occurred in the entire study area. Moreover, we show that areas with lower grazing density are significantly affected by forest encroachment. A possible interpretation of this result could be that wild grazers (roe deer and red deer) prefer semi-open areas surrounded by the forest. This, in association with other factors, such as domestic grazing, could be one of the main responsible in maintaining landscape mosaic typical of the Apennine mountain, confirming the value of grazers as a landscape management tool. Moreover, we show the possibility to conserve through reintroduction the vulnerable C.c. italicus.
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Over recent decades, ungulate populations across Europe have undergone a rapid recovery. While this constitutes a conservation success, there is increasing concern about their impacts on shared resources with humans. Understanding ungulate food choices is crucial for predicting such impacts. Numerous studies have focused on single species or communities at narrow spatial scales. Here, we used 265 published diets from 87 European studies to investigate patterns of resource use by four common deer species (moose Alces alces , red deer Cervus elaphus , roe deer Capreolus capreolus , and fallow deer Dama dama ), and wild boar Sus scrofa at the continental scale. On average, deer diets separated mostly along a gradient from grass to browse. Fallow deer diets contained the most and moose diets the least amount of grass, but we also found large intraspecific variation among all deer species. Diets of roe deer, a presumed browser, frequently contained ≥ 25% grass. Wild boar diet contained grass in amounts similar to red deer but otherwise differed strongly from deer diets. All five ungulate species shifted to eating higher proportions of woody browse during winter. Habitat influenced variation in intraspecific diets, but the proportions of key forage types related to feeding type (i.e. grass for intermediate feeders red and fallow deer, and shrubs for the browsers moose and roe deer) remained fairly consisted across habitat types. In northern and central Europe, diet similarity between roe deer and red deer was highest during winter and spring and lowest during summer and autumn but remained constant across the seasons in southern Europe. We foresee that, as interspecific interactions driven by land‐use and climatic changes increase across Europe, further monitoring and testing will be needed to understand the dynamics of dietary niche partitioning among ungulates. This article is protected by copyright. All rights reserved.
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Large herbivores play key roles in terrestrial ecosystems. Continuous defaunation processes have produced cascade effects on plant community composition, vegetation structure, and even climate. Wood-pastures were created by traditional management practices that have maintained open structures and biodiversity for millennia. In Europe, despite the broad recognition of their biological importance, such landscapes are declining due to land-use changes. This calls for finding urgent solutions for wood-pasture conservation. To test whether introducing an ecological replacement of an extinct wild horse could have positive effects on wood-pasture restoration, we designed a 3-year rewilding experiment. Horses created a more open wood-pasture structure by browsing on seedlings and saplings, affected tree composition via selective browsing and controlled the colonization of woody vegetation in grassland-dominated areas. Thus, rewilding could be a potential avenue for wood-pasture restoration and biodiversity conservation. However, such benefits may not materialize without a necessary paradigm and political shift.
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Large herbivores influence ecosystem functioning via their effects on vegetation at different spatial scales. It is often overlooked that the spatial distribution of large herbivores result from their responses to interacting top-down and bottom-up ecological gradients that create landscape-scale variation in the structure of the entire community. We studied the complexity of these cascading interactions using high-resolution camera trapping and remote sensing data in the best-preserved European lowland forest, Białowieża Forest, Poland. We showed that the variation in spatial distribution of an entire community of large herbivores is explained by species-specific responses to both environmental bottom-up and biotic top-down factors in combination with human-induced (cascading) effects. We decomposed the spatial variation in herbivore community structure and identified functionally distinct landscape-scale herbivory regimes ('herbiscapes') which are predicted to occur in a variety of ecosystems and could be an important mechanism creating spatial variation in herbivory maintaining vegetation heterogeneity.
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Information on tree species composition is crucial in forest management and can be obtained using remote sensing. While the topic has been addressed frequently over the last years, the remote sensing-based identification of tree species across wide and complex forest areas is still sparse in the literature. Our study presents a tree species classification of a large fraction of the Białowieża Forest in Poland covering 62 000 ha and being subject to diverse management regimes. Key objectives were to obtain an accurate tree species map and to examine if the prevalent management strategy influences the classification results. Tree species classification was conducted based on airborne hyperspectral HySpex data. We applied an iterative Support Vector Machine classification and obtained a thematic map of 7 individual tree species (birch, oak, hornbeam, lime, alder, pine, spruce) and an additional class containing other broadleaves. Generally, the more heterogeneous the area was, the more errors we observed in the classification results. Managed forests were classified more accurately than reserves. Our findings indicate that mapping dominant tree species with airborne hyperspectral data can be accomplished also over large areas and that forest management and its effects on forest structure has an influence on classification accuracies and should be actively considered when progressing towards operational mapping of tree species composition.
Re-introduction of large herbivores is increasingly used as a tool in nature management and for restoration of more biodiverse habitats. This study investigated the diet of recently introduced European bison, Bison bonasus, in a forest habitat in Bornholm, Denmark, with the purpose of evaluating its adaptation to the new habitat and assessing its potential for facilitating development towards a more open and species-rich forest. Metabarcoding of 39 bison dung samples collected during June–August identified 71 plant taxa belonging to 36 families as diet objects, comprising 56% forbs, 20% trees, 17% graminoids and 7% shrubs. The broad composition of the diet shows the capacity of the bison to adjust to new habitats and exploit a variety of different habitats when foraging, including meadows and other wet areas. Among the most frequently consumed plant taxa were the shrub Rubus idaeus, a number of coarse grass species and most tree species found in the habitat. Rubus idaeus were by far the most abundant taxa, constituting 44% of all the DNA sequences. The results suggest that foraging by bison can contribute towards limiting domination by understory shrubs and high, coarse grasses. Over an extended time period, foraging by bison is expected to promote development towards a lower and more open understory and herbaceous layer in the forest habitats.
Increasing deer populations in many temperate regions can affect tree regeneration, resulting in severe long-term impacts on forest structure, composition and diversity. Of the most common deer species in Europe-red deer (Cervus elaphus) and roe deer (Capreolus capreolus)-roe deer are generally thought to have the highest impact on palatable tree species owing to their feeding niche. Although browsing and its potential consequences are well researched, less is known about the influence of specific deer species within multi-species ungulate communities on specific tree species. Environmental DNA (eDNA) allows the determination of species-specific browsing habits without the need for direct observations, facilitating effective targeting of management interventions. In this study eDNA was used to elucidate the browsing patterns of these two deer species in the temperate forest of the Bavarian Forest National Park, Germany and analysed the influence of tree species, management type and height of browsing, on the success rate of the method. Samples were collected from twigs used in feeding trials from enclosures containing red deer or roe deer and from naturally browsed twigs in three different management types within the national park. eDNA was successfully amplified from 98% of the feeding trial samples, and the correct deer species was identified for all samples. eDNA was successfully amplified from approximately 50% of the naturally browsed samples. Neither management type, tree species, nor height of browsing had any significant influence on the success of the method. For silver fir and rowan, no significant difference was found in the proportion of browsing events attributable to roe or red deer, when the two deer species occur at similar densities. These results indicate that roe deer might not always be disproportionately responsible for the browsing of palatable tree species as expected from its food niche. Roe deer were significantly more responsible for browsing at lower heights than red deer. Although not statistically significant, roe deer were more responsible for browsing in intact forest compared to bark-beetle-impact forest, with the opposite relationship for red deer.
Large herbivores that survived the Pleistocene/Holocene transition are hypothesized to have been forced to take refuge, as a result of environmental changes and human pressure, into forest habitats. Today, there is an open question of the degree to which extant large herbivores are well adapted to the forests that allowed for the herbivores’ persistence. We studied the diet of European bison (Bison bonasus), the largest terrestrial mammal in Europe, to gain insight into the foraging behaviour of a large herbivore, that appears to be primarily adapted to grazing but has been restored to forested habitats. The study population resided in the Białowieża Primeval Forests, Poland. DNA-based analysis of faecal samples revealed strong seasonal and spatial patterns in bison foraging, consistent between sexes. Bison fed on at least 105 different plant taxa. Woody species constituted 59.4% of DNA sequences, and forbs 33.6%. The two most abundant taxa were raspberry (Rubus idaeus) and European hornbeam (Carpinus betulus), which together comprised 31.0% of the dietary sequences and occurred in over 80% of faecal samples. Seasonally, the diversity of plants eaten by bison increased with increasing food availability. During high plant biomass in summer, bison consumed up to 40 different plant taxa. There was little overlap in the composition of the diet from month to month, reflecting the strong seasonality of vegetation abundance and/or its dietary quality. The results indicate high plasticity in bison foraging strategies and response to seasonal changes in biomass and the species composition of plants. Bison are browsers which continuously adjusts their diet with seasonal availability of easily digestible non-grass vegetation. We propose that dietary plasticity and micro-selection for open habitats (gaps and river valleys) within a forested landscape allowed bison to persist in sheltering forest habitats during the Holocene and accommodate to forest environments during species restoration.