Bottom-up versus top-down control of tree regeneration in the Bialowieza Primeval Forest, Poland

Abstract

1. We tested the interactions between biotic and abiotic factors in structuring temperate forest communities
by comparing tree recruitment after 7 years inside 30 pairs of exclosure (excluding ungulates:
red deer, roe deer, bison, moose, wild boar) and control plots (7 · 7 m each) in one of the
most natural forest systems in Europe, the Białowie_za Primeval Forest (eastern Poland). The strictly
protected part of that forest hosts the complete native variety in trees, ungulates and their carnivores
and excludes human intervention.
2. We analysed whether the exclosure effect interacted with abiotic factors, relevant for tree recruitment
(canopy cover, ground vegetation cover, soil fertility and soil wetness) at different stages of
tree regeneration (seedlings, saplings £ 50 and>50 cm).
3. Contrary to our expectations, a single factor dominated at each stage of tree regeneration.
Herbaceous vegetation cover was the main factor determining the number of seedlings with an
optimum at 38%of cover. Soil fertility determined the density of saplings £ 50 cm, with on average
three times higher density on eutrophic than on oligotrophic soils. Herbivory was the main factor
determining recruitment rate of trees into>50 cm size classes only.
4. The density of saplings that grew into the >50 cm size class was more than three times higher
in the exclosures than in the control plots during 7 years. In the absence of ungulates, on average
3.1 species recruited into the >50 cm size class compared to 1.7 in control plots. Tree species
occurred in more equal proportions inside exclosures, whereas species composition was pushed
towards strong dominance of a preferred forage species, Carpinus betulus, in the presence of ungulates.
This suggests that preference of species by ungulates can coincide with tolerance to browsing.
5. Synthesis. The study showed that abiotic conditions dominated the early stages and ungulate
impact the later stages of tree regeneration, indicating the context-dependence of herbivore top-down
effects. Heterogeneity in abiotic and biotic conditions may, therefore, have an important influence
on the strength of top-down effects and the role that herbivores play in natural ecosystems.

Full text

Bottom-up versus top-down control of tree
regeneration in the Białowie _
za Primeval Forest,
Poland
Dries P. J. Kuijper
1
*, Joris P. G. M. Cromsigt
1,2
, BogumiłaJe˛drzejewska
1
,
Stanisław Mis
´cicki
3
, Marcin Churski
1
,Włodzimierz Je˛drzejewski
1
and Iwona Kweczlich
3
1
Mammal Research Institute, Polish Academy of Sciences, ul. Waszkiewicza 1d, 17-230 Białowie _
za, Poland;
2
Center for Ecological and Evolutionary Synthesis, University of Oslo, PO Box 1066 Blindern, 0316 Oslo, Norway;
and
3
Department of Forest Management, Geomatics and Forest Economics, Forestry Faculty, Warsaw University of
Life Sciences, ul. Nowoursynowska 166, 02-787 Warszawa, Poland
Summary
1. We tested the interactionsbetween biotic and abiotic factors in structuring temperate forestcom-
munities by comparing tree recruitment after 7 years inside 30 pairs of exclosure (excluding ungu-
lates: red deer, roe deer, bison, moose, wild boar) and control plots (7 ·7 m each) in one of the
most natural forest systems in Europe, the Białowie_
za Primeval Forest (eastern Poland). The strictly
protected part of that forest hosts the complete native variety in trees, ungulates and their carnivores
and excludes human intervention.
2. We analysed whether the exclosure effect interacted with abiotic factors, relevant for tree recruit-
ment (canopy cover, ground vegetation cover, soil fertility and soil wetness) at different stages of
tree regeneration (seedlings, saplings £50 and >50 cm).
3. Contrary to our expectations, a single factor dominated at each stage of tree regeneration.
Herbaceous vegetation cover was the main factor determining the number of seedlings with an
optimum at 38% of cover. Soil fertility determined the density of saplings £50 cm, with on average
three times higher density on eutrophic than on oligotrophic soils. Herbivory was the main factor
determining recruitment rate of trees into >50 cm size classes only.
4. The density of saplings that grew into the >50 cm size class was more than three times higher
in the exclosures than in the control plots during 7 years. In the absence of ungulates, on average
3.1 species recruited into the >50 cm size class compared to 1.7 in control plots. Tree species
occurred in more equal proportions inside exclosures, whereas species composition was pushed
towards strong dominance of a preferred forage species, Carpinus betulus, in the presence of ungulates.
This suggests that preference of species by ungulates can coincide with tolerance to browsing.
5. Synthesis. The study showed that abiotic conditions dominated the early stages and ungulate
impact the later stages of tree regeneration, indicating the context-dependence of herbivore top-down
effects. Heterogeneity in abiotic and biotic conditions may, therefore, have an important influence
on the strength of top-down effects and the role that herbivores play in natural ecosystems.
Key-words: bison, exclosure, herbivory, hornbeam, moose, red deer, roe deer, species
diversity, tolerance to browsing, ungulates, wild boar
Introduction
There has been an ongoing debate on the importance of
bottom-up versus top-down forces in structuring plant
communities (McNaughton et al. 1989; Hunter & Price 1992;
Power 1992).
Bottom-up forces are environmental conditions affecting
primary production and, as a result, higher trophic levels. In
contrast, top-down forces are higher trophic levels impacting
lower levels (Fretwell 1987; DeAngelis 1992). There is general
agreement that both factors affect plant communities (Polis &
Strong 1996), but the question remains what the relative
strength of such top-down and bottom-up forces is and if we
can find general patterns in their effects (Gripenberg & Roslin
*Correspondence author. E-mail: dkuijper@zbs.bialowieza.pl
Journal of Ecology 2010, 98, 888–899 doi: 10.1111/j.1365-2745.2010.01656.x
2010 The Authors. Journal compilation 2010 British Ecological Society

2007). Increasing evidence suggests that the balance of top-
down and bottom-up forces varies over environmental or pro-
ductivity gradients (Oksanen et al. 1981; Osem, Perevolotsky
& Kigel 2002; Kuijper & Bakker 2005; Bakker et al. 2006).
Much of this evidence comes from grassland systems. Here,
we investigate the relative effects of both forces on forest
dynamics.
Studies from boreal forest systems illustrate the overriding
importance of abiotic bottom-up factors relative to biotic her-
bivore control (Turkington et al. 2002), whereas others show
that abiotic and biotic factors change in importance during
different stages of boreal forest primary succession (Kielland
& Bryant 1998). Recruitment of trees in mature forest typi-
cally depends on the formation of gaps in the tree canopy
(e.g. Runkle 1981; Bobiec 2007). Most tree species profit from
the enhanced light availability and show higher growth and
recruitment inside gaps. However, enhanced light levels may
also increase herbaceous vegetation cover leading to increased
competition with tree seedlings hampering seedling growth or
establishment (Modry, Hubeny & Rejsek 2004; Van den Ber-
ghe et al. 2006). When light is not limiting, soil productivity
may be an important factor determining sapling growth (Sipe
& Bazzaz 1995; Lusk & Matus 2000), potentially changing
the competitive balance between regenerating tree species
(Latham 1992; Modry, Hubeny & Rejsek 2004). Next to abi-
otic conditions, foraging by large herbivores can top-down
regulate both recruitment rate and species composition of
recruiting trees in temperate forests (Ammer 1996; Van Hees,
Kuiters & Slim 1996; Kriebitzsch et al. 2000; Scott et al.
2000). In the long-term, this browsing may prevent successful
regeneration of some species into the tree canopy and alter
the structure and dynamics of forest ecosystems (Mladenoff
& Stearns 1993; Long, Pendergast & Carson 2007). Recent
studies from temperate North-American forest systems illus-
trate the dominant role of top-down factors. Reintroduction
of large predators in Yellowstone National Park led to cas-
cading effects, modifying plant–herbivore interactions (Ripple
& Larsen 2000). This suggests that herbivores are top-down
regulating tree regeneration in the absence of predators, but
that presence of predators may release trees from this control
(Ripple & Beschta 2007).
Clearly, it is difficult to synthesize general effects of both
bottom-up and top-down factors on tree dynamics, since vari-
ous studies result in quite different outcomes. In addition to
differences in productivity and ungulate density between sys-
tems, one reason for this is that biotic and abiotic factors may
strongly interact. Light conditions may affect forage availabil-
ity but also alter forage chemical quality, both potentially
determining forage patch choice of herbivores (Edenius 1993;
Molvar, Bowyer & Van Ballenberghe 1993; Hartley et al.
1997). Forest gaps may, therefore, preferentially be visited by
ungulates leading to an uneven distribution of ungulate brows-
ing and their effects of browsing in a forest system (Kuijper
et al. 2009). In addition, the abundance and effects of herbi-
vores are predicted to change along gradients of productivity
(Oksanen et al. 1981; Kuijper & Bakker 2005; Melis et al.
2009). Lastly, browsing or grazing may directly or indirectly
change the competitive balance between plant species and
hence change the interaction between tree seedlings and herba-
ceous vegetation (Riginos & Young 2007). These interactions
suggest a strong context-dependence of top-down effects of
herbivores on tree regeneration and a shifting importance
of biotic and abiotic factors during different stages of tree
regeneration.
Although several studies have addressed the relative impor-
tance of bottom-up versus top-down factors in structuring
temperate forest communities, surprisingly little empirical data
are available that show how biotic and abiotic conditions may
interact and how this can modify the importance of top-down
and bottom-up forces (Hunter & Price 1992). Empirical data
are especially lacking from systems with limited human inter-
vention and a complete set of natural processes. The lack of a
complete guild of ungulate species occurring at natural densi-
ties, absence of large predators and rarity of natural tree
recruitment without human manipulation can all be factors
that conceal the role that top-down effects might play in
natural, unmanaged forest ecosystems. In this study, we tested
the interactions between herbivore top-down effects and abi-
otic bottom-up effects during early stages of tree regeneration
in one of the last remaining natural, temperate, lowland forest
systems in Europe, the Białowie_
za Primeval Forest in Poland.
The strictly protected part of this forest still hosts the complete
native variety in both flora and fauna and excludes any human
intervention.
Materials and methods
STUDY SITE
The study site was the strictly protected zone of the Białowie_
za
National Park(BNP) located in the centre of the Białowie_
za Primeval
Forest (BPF). The BPF, situated in eastern Poland (5245¢N,
2350¢E) and western Belarus, is a large continuous forest composed
of multispecies tree stands. The entire BPF covers 1450 km
2
, of which
600 km
2
belong to Poland and the remaining 850 km
2
to Belarus. In
1921, the best preserved central part of the BPF was proclaimed as
the Strict Reserve, which later becameBNP. At present, BNP consists
of a 47.5-km
2
area of strictly protected old-growth forest in which no
human intervention has been allowed since 1921 and tourist access is
only permittedwith a guide. Before 1921, human impact on tree stand
structure and composition was small or minimal (Je˛drzejewska et al.
1997; Samojlik et al. 2007). In 1996, BNP was enlarged to 105.2 km
2
and the strictly protected zone has been surrounded by the partially
protected zone since then (see Fig. 2). The area outside BNP is man-
aged for forestry purposes, and hence wood exploitation and regula-
tion of ungulate numbers is taking place. In the strictly protected
zone, old forest stands prevail. Young stands with dominate trees of
40 years or less account for 2.4% of the area. Mid-aged stands, domi-
nated by trees aged 41–80 years, cover 16.3% and old stands
(81–120 years) cover 41.5%. Very old stands, dominated by trees
aged over 120 years, account for 39%. Only 0.8% of the area is lack-
ing tree cover (Michalczuk 2001). The following main forest types can
be distinguished (with % share of total area and dominant trees in
brackets based on Michalczuk 2001): deciduous forest (54%, Quercus
robur,Tilia cordata and Carpinus betulus), mixed deciduous forest
(23%, Picea abies,Quercus robur,Tilia cordata and Carpinus betulus),
Abiotic and biotic control of tree regeneration 889
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black alder bog forest and streamside alder-ash forest (14%, Alnus
glutinosa and Fraxinus excelsior), mixed coniferous forest (13%, Pi-
nus sylvestris,Picea abies and Quercus robur) and coniferous forest
(9%, Pinus sylvestris and Picea abies). These forest types are situated
along an ecological gradient of soil richness and water availability.
Coniferous forest can be found on the driest, nutrient-poor soils.
Deciduous forest and streamside alder-ash forest occur at productive
soils rich in organic matter but streamside alder-ash forest are inun-
dated (at least part of the year). Mixed coniferous and mixed decidu-
ous forests occupy transitional zones of the soil fertility gradient
(Falin
´ski 1986). The mean altitude of the strictly protected part of
BNP is 158 m a.s.l. and the total altitudinal range is 23 m. Mean
annual air temperature is 6.8 C with the coldest month in January
with on average )4.7 C and the warmest month is July with 17.8 C.
Mean annual precipitation is 641 mm and mean annual snow cover
lasts for 92 days.
HERBIVORES AND THEIR POPULATION DENSITIES
Another unique aspect of BPF is that it is one of the very few Euro-
pean lowland forests that still host the complete native ungulate and
carnivore assemblages. Five ungulate species occur throughout the
forest system. The most abundant species, both in numbers and crude
biomass, is red deer (Cervus elaphus) with a winter density of 3.4
individuals km
)2
in 1999 (Je˛drzejewski et al. 2002) increasing
to 6.0 individuals km
)2
according to the last estimate in 2008
(T. Borowik, J. Borkowski & W. Je˛drzejewski, unpubl. data). The
second-most numerous ungulate is wild boar (Sus scrofa), of which
annual density strongly depends on fluctuations in food availability;
density varied from 3.4 individuals km
)2
in 1999 (Je˛drzejewski et al.
2002) to 5.4 individuals km
)2
in 2008 (T. Borowik, J. Borkowski &
W. Je˛ drzejewski, unpubl. data). Roe deer, Capreolus capreolus,were
present with 2.4 individuals km
)2
in the winter of 1999 (Je˛drzejewski
et al. 2002) and a similar density in 2008. In lower density occur
European bison (Bison bonasus) with 0.49 individuals km
)2
and
moose (Alces alces) with 0.04–0.08 individuals km
)2
during 1993–
2008 (Je˛drzejewska et al. 1997; Mysterud et al. 2007; T. Borowik, J.
Borkowski & W. Je˛drzejewski, unpubl. data). Since human interven-
tion is prohibited in the strictly protected zone of BNP, the ungulates
in that area have not beenhunted for over 80 years. However, the reg-
ulation of ungulate numbers that occurs outside BNP may to some
extent affect the observed numbers inside the protected area. Hunting
activities could increase densities in BNP by displacement of individu-
als to the protected area during the hunting season. However, recent
studies suggest that this probably only affects individuals in areas
directly bordering the non-hunting areas (Tolon et al. 2009). Hunting
outside BNP may also reduce population levels in the protected area
if BNP would act as a source area. However, the observed stability of
the home ranges of the dominant ungulate species (red deer: Kamler,
Je˛drzejewski & Je˛drzejewska 2008; wild boar: T. Podgo
´rski & W.
Je˛drzejewski unpubl. data) inside BNP suggests that there is not a
large movement of individualsto the areas outside the protected zone.
Concluding, we believe that current hunting practices outside BNP
will not strongly influence the ungulate densities inside the protected
area. Natural predators of these ungulates, wolf (Canis lupus)and
lynx (Lynx lynx), are strictly protected since 1989 and are not hunted
throughout Poland. In BPF,they occur with average densities around
0.01–0.05 individuals km
)2
(wolf) and 0.01–0.03 individuals km
)2
(lynx) (Schmidt et al. 2008).
Several medium-sized and small herbivores occur, although reli-
able figures on their abundance are scarce. Both brown hare (Lepus
europaeus) and mountain hare (Lepus timidus) have been recorded
but are very rare. The community of herbivorous–granivorous forest
rodents is dominated by bank vole (Myodes glareolus) and yellow-
necked mouse (Apodemus flavicollis), whereas species such as pine
vole (Microtus subterraneus), field vole (Microtus agrestis) and root
vole (Microtus oeconomus) occur in forests in lower densities (Je˛drze-
jewska & Je˛drzejewski 1998).
EXPERIMENTAL DESIGN
To measure the impact of top-down forces on tree regeneration, 30
paired exclosure–control plots (Fig. 1) were erected in BNP in July
2000 (Kweczlich & Mis
´cicki 2004 following Reimoser & Suchant
1992). The location of each exclosure was chosen randomly by placing
a grid of 460 cells of 100 ·1000 m over the map of the strictly pro-
tected zone, with the shorter side of each cell aligned according to
330azimuth.Each intersection of the raster was given a unique num-
ber and exclosure locations were determined by randomly selecting
intersection numbers (Kweczlich & Mis
´cicki 2004). The minimal dis-
tance between two exclosures was c. 310 m. The resulting locations
(Fig. 2) covered all main soil and forest types, ranging from mesic
coniferous forest to wet deciduous forest (see Table 1). The number
of exclosures per forest type reflects the occurrence of each forest type
inside the strict reserve. Therefore, we see this set of exclosures as a
Fig. 1. Two examples of exclosures, illustrating the variation in the
effect of ungulate exclusion after 7 years of experiment. The upper
photo (exclosure 30) shows higher regeneration of maple (Acer
platanoides) inside (on the right hand) compared to outside the
exclosure, whereas, the photo below (exclosure 23) shows no effect
of ungulate exclusion on tree regeneration. For locations of
exclosures,see Fig. 2.
890 D. P. J. Kuijper et al.
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random sample covering the natural variation which exists in this
diverse forest.
Each exclosure consisted of a 2-m-high fence surrounding the
7·7 m sample plots plus a 50-cm buffer zone along the borders of
the sample plot in which no measurements were taken to prevent
potential fence effects. Fences were constructed of mesh wire with a
mesh size of c. 15 cm (see Fig. 1). This fence effectively excluded all
ungulate species (roe deer,red deer, moose, bison and wild boar) from
entering, while allowing all small (rodents) and medium-sized herbi-
vores (hares) free access. For each exclosure, we set-up a paired con-
trol plot (unfenced) of 7 ·7 m as close as possible to the exclosure
with comparable habitat characteristics at the start of the experiment,
such as canopy tree species composition, forest type, tree sapling den-
sity, herbaceous vegetation cover and canopy openness. Control plots
were situated on average 20 m away from their paired exclosure plot
with a minimum distance of 5 m. Metal sticks marked the corners of
the plots to ensure consecutive measurements were taken at the same
location. The surveyed area in each plot (both control and exclosure)
was 49 m
2
. In 2007, one of the exclosures was destroyed by a fallen
tree covering the entire plot. Hence, we excluded this plot from the
analyses resulting in n=29.
MEASUREMENTS OF TREE REGENERATION
During July–August 2000, 2002, 2004 and 2007, we recorded all
trees occurring in the plots. The first inventory was carried out
just after the exclosures were built. During each inventory,
we counted the number of trees separately for each species. In
addition, individuals per species were assigned to eight different size
classes: seedlings (younger than 1 year, no woody stem), tree saplings
<10, 11–25, 26–50, 51–75, 76–100, 101–130, 131–200 and >200 cm
tall.
Table 1. Description of habitat types in which exclosure–control pairs were established with the number of exclosure plots (and paired control
plots) in each habitat. The main tree canopy species at the location of the exclosures in each habitat at the start of the experiment are indicated
(Picea abies,Pinus sylvestris,Quercus robur,Carpinus betulus,Tilia cordata,Acer platanoides,Populus tremula,Fraxinus excelsior,Betula pendula
in coniferous and Betula pubescensin alder-ash forest)
Forest type Hydrological conditions Dominating tree canopy species Number of exclosures
Coniferous Wet Picea,Pinus 2
Mixed coniferous Mesic ⁄wet Picea,Pinus,Quercus,Betula 2
Mixed deciduous Wet ⁄mesic Carpinus,Quercus,Tilia,Picea,Populus 3
Deciduous Mesic Carpinus,Quercus,Tilia,Picea,Acer 13
Deciduous Wet Carpinus,Quercus,Tilia,Picea,Acer,Fraxinus 8
Streamside alder-ash forest Wet Alnus,Betula,Fraxinus 1
Fig. 2. Location of the study area in Poland, Europe (right panel) and map of paired exclosures–control plots (numbered from 1 to 30) in the
strictly protected part (dark grey) of Białowie_
za National Park (light and dark grey). The surrounding Białowie_
za Primeval Forest is not indi-
cated on the map.
Abiotic and biotic control of tree regeneration 891
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To compare species diversity between treatments, taking the rela-
tive abundances of species into account, we calculated the Shannon
index (Pielou 1975) for each plot for different size classes according
to:
H0¼
X
S
i¼1
piln pi;
where Sis the number of species and pthe proportion of species
iof all tree individuals per height class. The minimum value of
the Shannon index is 0 when there is only one species present,
and the index is highest when each species is present in equal pro-
portions. Low values indicate a high dominance of a single spe-
cies, either due to low number of species or relatively high
abundance of one species. We determined Shannon’s diversity for
the 2000 data at the start of the experiment and for the 2007 data
after 7 years of potential ungulate impact.
MEASUREMENTS OF ABIOTIC FACTORS AT EACH
LOCATION
To test for possible bottom-up effects on tree regeneration, we mea-
sured those abiotic factors that havebeen illustrated by previous stud-
ies to be important for recruitment of trees. Canopy cover determines
the amount of available light on the forest floor and is the prime fac-
tor shaping tree recruitment (Runkle 1981; Bobiec 2007). Herbaceous
vegetation can compete with tree seedlings, retarding their growth
and establishment (Modry, Hubeny & Rejsek 2004; Van den Berghe
et al. 2006), whereas soil fertility and wetness determine growth of
established seedlings and hence recruitment rate in larger size classes
(Sipe & Bazzaz 1995; Lusk & Matus 2000).
As a measure of lightavailability at each plot, we visually estimated
tree canopy cover during each inventory (using 5% classes) and aver-
aged the values per plot. Canopy cover in general was relatively high
in both controls (mean± SE: 73.0± 4.1%) and exclosures
(72.5± 4.7%), typical for this old-growth forest, and ranged in both
treatments from 5% to 100%. In addition, we estimated the total
ground cover of bushes, herbs, grasses and ferns at each plot to the
nearest 5%. The values of ground vegetation cover ranged from 1%
to 96% inside controls (mean 51.9± 4.4%) and exclosures
(59.4± 3.5%) during the study period. Both measures were recorded
at the same time as the tree measurements in July–August, i.e. at time
of peak vegetation biomass. These measurements were conducted at
each plot (controls as well as exclosures) because both factors could
vary considerably at small scale (metres). Moreover, although at the
start of the experiment control plots were selected to havesimilar can-
opy and ground cover to those in exclosure plots, both factors chan-
ged quickly over time and in some cases led to considerable
differences between paired plots.
Data on soil fertility were extracted from a map of soil types in the
strict reserve of BNP (Prusinkiewicz & Michalczuk 1998). Plots
occurred on ninemain soil types (with number ofexclosures in brack-
ets): cambisols (7), phaeosols (6), luvisols (5), epigleysols (3), podzol-
sols (3), gleysols (2), cambiarenosols (1), gleypodzolsols (1) and
eutrohistosols (1). These soil types were further aggregated in two cat-
egories indicating habitat productivity based on Prusinkiewicz &
Michalczuk (1998): eutrophic soils (cambisols, phaeosols, luvisols
and eutrohistosols) and oligotrophic soils (epigleysols, podzolsols,
gleysols, cambiarenosols, gleypodzolsols). As an additional factor
influencing soil productivity, we recorded soil wetness according to
two categories: mesic (15 exclosures) and wet (14 exclosures). Values
for both soil fertility and soil wetness were the same for paired exclo-
sure and control plots due to their proximity.
STATISTICAL ANALYSES
We aggregated tree height classes into three classes: seedlings,
saplings £50 cm and saplings >50 cm. We choose the cut-off
value of 50 cm because red deer have a preferred foraging height
around 50–100 cm (Renaud, Verheyden-Tixier & Dumont 2003)
and hence size classes above and below 50 cm were expected to
show a differential response to ungulate exclusion. As the number
of seedlings showed large year-to-year variation, we calculated the
cumulative amount of seedlings by adding up the counted seedlings
on each plot in 2000, 2002, 2004 and 2007. We chose to analyse
the cumulative number of seedlings because we were not interested
in showing how fluctuations in seedlings affected regeneration of
different species. Instead, we wanted to show how bottom-up
versus top-down factors influenced the net seedling input over
the whole 7-year study period, as part of the forest regeneration
process.
We performed all below-described analyses for each tree size
class separately. First, we used paired-sample t-tests to see if spe-
cies richness and the number of tree seedlings and saplings were
similar in exclosure and control plots at the start of the experi-
ment in 2000. We then tested for effects of top-down and bottom-
up factors on the regeneration of trees in the different height clas-
ses over our 7-year study period. Because all our tree regeneration
data represented count data (number of trees per size class), we
used generalized linear models with a Poisson error distribution
and log-link function. We used a quasipoisson distribution in all
models to correct for overdispersion because the residual deviance
was much larger than the residual degrees of freedom in all cases
(>10, Crawley 2007). As we were interested in the effect of her-
bivory and its potential interaction with abiotic conditions, we
first tested for an overall effect of exclosures on the number of
woody individuals. Then, we tested whether the effect of exclosure
depended on the environmental factors (soil fertility and soil wet-
ness) and covariates (canopy cover and herbaceous vegetation
cover averaged over the study period). As we did not find any sig-
nificant interactions between exclosure and environmental treat-
ments, we continued with testing for effects of environmental
variables without including the exclosure effect.
Soil fertility and wetness did not vary between paired exclosure
and control plots, while canopy and ground cover did because they
varied at much finer spatial scale. Therefore, we tested for an effect
of factors (soil fertility and soil wetness) and covariates (canopy
cover and vegetation cover) in separate models. First, we tested for
an effect of the covariates using all our plots as replicates (n=58).
Secondly, we tested for an effect of the factors using only the control
plots (n= 29). For the latter, we could not use all plots because
paired control and exclosure plots always occurred on the same soil
type, hence representing pseudoreplicates. We then repeated the test
with the exclosure plots to check the robustness of the result.
While testing for effects of environmental variables, westarted with
full models (including interactions) and used likelihood ratio tests to
simplify the full models to find the most parsimonious model (Craw-
ley 2007). Although technically quasi-likelihoods (as used in our mod-
els) are not real likelihoods, the use of F-test-based likelihood ratio
tests is considered appropriate to simplify quasipoisson models
(Crawley 2002;Venables & Ripley 2002; Bolker 2008). For the covari-
ates, we also considered models withquadratic terms of the covariates
to test, whether possible effects were nonlinear rather than linear. In
the Results section, we present statistics for the most parsimonious
models only. We used rversion 2.7.1 for these analyses (R Develop-
ment Core Team 2008).
892 D. P. J. Kuijper et al.
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Ecology,98,888–899

Differences between exclosures and controls in species composition
of trees and Shannon-diversity index were tested pair-wise for cumu-
lative seedlings, saplings <50 cm and saplings >50 cm separately
using nonparametric Wilcoxon signed-rank tests. All percentage data
(canopy cover and vegetation cover) were arcsine-transformed prior
to analyses (Zar 1984). These statistical analyses were performed
using spss 15.0 (SPSS Inc., Chicago, Illinois, USA).
Results
EFFECTS OF UNGULATES AND ABIOTIC FACTORS ON
TREE REGENERATION
The density of trees in three size classes, the number of species
and Shannon’s diversity indices were similar in exclosures and
control plots at the start of the experiment in 2000. After
7 years, exclosures did not show a higher cumulative number
of seedlings than control plots (Table 2). Moreover, we did not
find any interaction between exclosure and environmental fac-
tors (F
1,54
=0.55,P= 0.46 for all factors, Table 3). The most
parsimonious model explaining the variation in cumulative
number of seedlings among the plots and including the
covariates, only showed vegetation cover as explanatory vari-
able with its quadratic term (F
1,55
=20.56, P< 0.001). The
density of seedlings increased with vegetation cover until an
optimum of 7.2 seedlings m
)2
at 38% vegetation cover, and
decreased with increasing vegetation cover (Fig. 3). Soil fertility
and wetness did not affect the density of seedlings in the control
plots (soil fertility: F
1,27
= 2.38, P= 0.13; soil wetness:
F
1,27
=2.37, P= 0.13) or exclosure plots (soil fertility:
F
1,27
=0.61,P= 0.44; soil wetness: F
1,27
=0.59,P=0.45).
Exclusion of ungulates also did not affect the density of tree
saplings shorter than 50 cm, and this effect did not depend on
the environmental factors (effect of exclosure: F
1,56
= 0.60,
P= 0.44; see Table 2 for interaction effects). Canopy and
vegetation cover did not affect the density of saplings £50 cm
in the plots (ground cover: F
1,56
=0.23, P= 0.64; canopy
cover: F
1,56
= 1.10, P= 0.30). While soil wetness did not
affect the density of saplings in control plots (F
1,27
=0.29,
P= 0.60) or exclosures (F
1,27
= 0.022, P= 0.88), soil fertil-
ity did. The density of saplings £50cmwashigheroneutro-
phic soils than on oligotrophic soils in control (F
1,27
=3.61,
P= 0.0068) as well as exclosure plots (F
1,27
=7.93,
Table 2. Density (individuals m
)2
on 49-m
2
plots), number of species and Shannon index of species diversity (mean± SE) of trees in different
size classes in the control and exclosure plots at the start of the experiment (2000) and after 7 years (2007). Seedlings in 2000 refer to seedlings
present in that year, whereas seedlings in 2007 refer to the cumulative number counted during surveys in 2000, 2002, 2004 and 2007. Sample sizes
differ because Shannon indices could only be calculated when trees were present on a plot. Differences between exclosures and controls were
tested by Wilcoxon signed-rank tests.Significant differences are indicated in bold
Size class
Survey in 2000
Control Exclosure znP-value
Density
Seedlings 0.49 ± 0.20 0.44± 0.18 )0.31 29 0.758
Saplings £50 cm 1.59 ± 0.39 1.43± 0.31 )0.38 29 0.707
Saplings > 50 cm 0.07± 0.01 0.12± 0.05 )0.60 29 0.550
Number of species present
Seedlings 1.65 ± 0.21 1.76± 0.18 )0.43 29 0.665
Saplings £50 cm 3.72 ± 0.29 3.51± 0.31 )0.70 29 0.484
Saplings > 50 cm 0.86± 0.18 1.10± 0.17 )1.01 29 0.312
Shannon index
Seedlings 0.48 ± 0.07 0.29± 0.07 )1.85 22 0.064
Saplings £50 cm 0.79 ± 0.08 0.76± 0.08 )0.41 28 0.683
Saplings > 50 cm 0.21± 0.09 0.28± 0.08 )0.25 11 0.799
Survey in 2007
Density
Seedlings 3.89 ± 1.08 3.79± 0.77 )0.65 29 0.516
Saplings £50 cm 1.46 ± 0.34 1.14± 0.24 )0.42 29 0.673
Saplings > 50 cm 0.21± 0.05 0.69± 0.18 )3.32 29 0.001
Number of species present
Seedlings 3.90 ± 0.28 3.93± 0.27 )0.06 29 0.960
Saplings £50 cm 3.72 ± 0.34 4.00± 0.28 )0.74 29 0.458
Saplings > 50 cm 1.72± 0.19 3.07± 0.30 )3.37 29 0.001
Shannon index
Seedlings 0.79 ± 0.08 0.62± 0.08 )2.04 27 0.041
Saplings £50 cm 0.77 ± 0.08 0.89± 0.07 )1.25 28 0.210
Saplings > 50 cm 0.45± 0.06 0.72± 0.08 )2.02 23 0.044
Abiotic and biotic control of tree regeneration 893
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P= 0.0090). Density of saplings was on average three times
higher on eutrophic soils (Fig. 4).
Herbivory clearly affected the density of tree saplings taller
than 50 cm (F
1,56
= 10.20, P= 0.0023) and this effect did not
depend on environmental conditions (see Table 3 for interac-
tions). The density of saplings that grew into the >50 cm size
class was more than three times higher in the exclosures than in
the control plots during 7 years (Table 2). Canopy cover
(F
1,56
=2.05,P= 0.16) or vegetation cover (F
1,56
=0.95,
P= 0.33) had no influence on the density of saplings taller
than 50 cm and neither soil fertility nor soil wetness did influ-
ence density in control (fertility: F
1,27
= 0.064, P= 0.80; wet-
ness: F
1,27
= 0.23, P= 0.88) or exclosure plots (fertility:
F
1,27
=0.14,P= 0.71; wetness: F
1,27
= 0.84, P=0.37).
EFFECTS OF HERBIVORY ON SPECIES COMPOSITION
OF REGENERATING TREES
After 7 years, hornbeam, Carpinus betulus made up the largest
proportion of cumulative seedlings but in general the species
composition of seedlings was similar in exclosure and control
plots (Fig. 5a). Only one species, Tilia cordata,hadasignifi-
cantly higher abundance inside control plots than in exclosures
(z=)2.945, n= 29, P= 0.003). The total number of spe-
cies encountered in the seedling group did not differ between
exclosures and controls. The Shannon index showed a small
but significant difference and was higher in controls than in
exclosures (Table 2).
Unlike the seedling community, the community of tree sap-
lings £50 cm was not dominated by a single species in 2007
(Fig. 5b). Overall, exclosures did not show consistent effects
on species abundances of saplings £50 cm. Occurrence of only
two species significantly differed between exclosures and con-
trols. Quercus robur was found more often inside exclosures
Table 3. Results of quasipoisson regression models that tested for the effect of exclosure or exclosure and one of four environmental factors (soil
fertility, soil wetness, canopy cover and herbaceous vegetation cover) on the number of individuals from three tree size classes. Only the
interaction effect is shown from the analysis of the full model, i.e. including main effects of the factors in the interaction term. Significant effects
are indicated in bold
Size class Models d.f. Residual d.f. FP-value
Seedlings Exclosure 1 56 < 0.01 0.95
Exclosure ·Soil fertility 1 54 0.55 0.46
Exclosure ·Wetness 1 54 0.51 0.48
Exclosure ·Canopy cover 1 54 < 0.01 0.97
Exclosure ·Vegetation cover 1 54 0.03 0.86
Saplings £50 cm Exclosure 1 56 0.60 0.44
Exclosure ·Soil fertility 1 54 0.13 0.72
Exclosure ·Wetness 1 54 0.08 0.77
Exclosure ·Canopy cover 1 54 0.01 0.93
Exclosure ·Vegetation cover 1 54 0.22 0.64
Saplings > 50 cm Exclosure 156 10.20 < 0.01
Exclosure ·Soil fertility 1 54 0.14 0.71
Exclosure ·Wetness 1 54 0.23 0.63
Exclosure ·Canopy cover 1 54 0.09 0.77
Exclosure ·Vegetation cover 1 54 < 0.01 0.97
Herbaceous ve
g
etation cover (%)
020406080100
Cumulative number of seedlings (N m–2)
0.01
0.1
1
10
100
Controls
Exclosures
Fig. 3. The relationship between vegetation cover and cumulative
density of seedlings (in 2000–07) in control and exclosure plots.
The parabolic line shows the fit of the most parsimonious model
(ground cover: F
1,56
=8.15,P= 0.006; vegetation cover
2
:F
1,55
=
20.56, P< 0.001) with the following parameter estimates:
intercept = 0.083±0.73, t=5.58,P< 0.001; effect of vegetation
cover = 0.099± 0.032, t=3.09,P= 0.0031; effect of vegetation
cover
2
=)0.0013± 0.00034, t=)3.80, P< 0.001 (Log(y)=
0.083 + 0.099x)0.0013x
2
).
Eutrophic soil Oligotrophic soils
Density of saplings ≤ 50 cm (N m–2)
0.0
0.5
1.0
1.5
2.0
2.5
Control
Exclosure
Effect of exclosure: ns
*
*
Fig. 4. Density of tree saplings (N m
)2
) shorter than 50 cm on eutro-
phic versus oligotrophic soils for the control and the exclosure plots
in 2007. Significant differences (P< 0.01) are indicated by asterisks.
894 D. P. J. Kuijper et al.
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Ecology,98,888–899

(z=)2.454, n=29,P= 0.014), whereas Fraxinus excelsior
attained higher numbers in controls (z=)2.189, n= 29,
P= 0.029). The mean total number of species of tree saplings
£50 cm and the Shannon-diversity index did not differ
between exclosure and control plots (Table 2).
After 7 years, all species showed on average a higher density
of tree saplings taller than 50 cm inside exclosures than in
controls (Fig. 5c). This difference was significant for Acer plat-
anoides (z=)2.536, n=29,P= 0.011), Sorbus aucuparia
(z=)2.609, n=29,P= 0.009) and marginally significant
for Ulmus glabra (z=)1.904, n=29, P= 0.057). Pinus
sylvestris, although rare, was found only inside exclosures. The
effect of herbivory was also reflected in the number of tree
species present. While species richness in exclosures and
controls was similar at the start of the experiment, a signifi-
cantly higher number of species had recruited into the >50 cm
size class inside exclosures (3.1 ± 0.3) than in the control plots
(1.7 ± 0.2) after 7 years of excluding ungulates (Table 2). Due
to the recruitment of more tree species and the more even dis-
tribution of the species composition of the recruiting trees in
2007, Shannon indices were significantly higher inside exclo-
sures (0.72 ± 0.08) compared to control plots (0.45 ± 0.06,
Table 2). In the presence of ungulates, recruitment of tree
saplings into the >50 cm size class was strongly dominated by
one species, Carpinus betulus, which on average made up
68% of trees >50 cm in control plots, compared to 38% in
exclosures.
Discussion
The present study shows that the relative importance of
top-down biotic and bottom-up abiotic factors changed during
Cumulative seedlings
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
Carpinus betulus
Acer platanoides
Ulmus glabra
Populus tremula
Picea abies
Sorbus aucuparia
Betula pubescens &
B. pendula
Tilia cordata
Fraxinus excelsior
Pinus sylvestris
Alnus glutinosa
Quercus robur
Saplings
≤
50 cm
0.0
0.2
0.4
0.6
0.8
Saplings > 50 cm
Treatment
Control
0.0
0.1
0.2
0.3
0.4
Density (N m–2)Density (N m–2)Density (N m–2)
Exclosure
(a)
(b)
(c)
Fig. 5. Species composition of (a) tree seedlings (cumulative over 2000–07), (b) saplings £50 cm and (c) saplings >50 cm inside exclosures and
control plots in 2007 (mean density± SE). The order oftree species in the graphs is the same as in the legend.
Abiotic and biotic control of tree regeneration 895
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different stages of tree regeneration in an old-growth forest
with a complete native ungulate and carnivore assemblage.
Whereas biotic (vegetation cover) and abiotic factors (soil fer-
tility) determined variation in the numbers of seedlings and
tree saplings £50 cm, top-down effects of ungulates controlled
recruitment into taller size classes. The strength of these top-
down effects differed among tree species and resulted in a shift
in species composition of regenerating trees in the presence of
ungulates compared to plots, where ungulates were excluded.
In general, species diversity was lower in the presence of
ungulates, because of a higher dominance of one species,
Carpinus betulus.
SHIFTING IMPORTANCE OF TOP-DOWN AND BOTTOM-
UP FACTORS AFFECT TREE RECRUITMENT
In the present study, we aimed at studying the interacting
effects between biotic and abiotic factors. On the one hand,
abiotic factors have been shown to be important in determin-
ing tree regeneration (Runkle 1981; Sipe & Bazzaz 1995;
Modry, Hubeny & Rejsek 2004; Van den Berghe et al. 2006;
Bobiec 2007). On the other hand, they influence forage
availability and quality for herbivores (Edenius 1993; Molvar,
Bowyer & Van Ballenberghe 1993; Hartley et al. 1997), which
is likely to result in interacting effects. In contrast to our expec-
tation, we did not find interacting effects of abiotic and biotic
(herbivory) factors. Instead, a single dominant factor deter-
mined recruitment at different stages of tree regeneration.
Abundance of seedlings was reduced at high herbaceous vege-
tation cover, suggesting competitive effects of vegetation on
seedling establishment, which is in line with other studies
(Modry, Hubeny & Rejsek 2004; Van den Berghe et al. 2006).
Interestingly, the number of seedlings showed an optimum at
intermediate herbaceous vegetation cover. Lower seedling
abundance at low vegetation cover could be related to low light
or nutrient availability that limit growth of herbaceous vegeta-
tion and establishment of seedlings. However, we did not find
any effect of canopy cover and soil fertility on seedling density,
suggesting that light and nutrient availability per se are not the
most important factors explaining the low abundance of seed-
lings at low vegetation cover. We suggest that, alternatively,
this pattern could be explained by the process of associative
resistance, where tree seedlings are protected from browsing
because they grow among unpalatable herbaceous cover (Smit,
Ouden den & Mu
¨ller-Scha
¨rer 2006). Hence, a minimum
amount of herbaceous vegetation cover would be needed to
providesafesitesfortreeseedling establishment, which could
explain the low seedling abundance at low vegetation cover in
our study. Whereas several studies have illustrated the impor-
tance of gap formation in the regeneration process (e.g. Runkle
1981; Bobiec 2007), we did not find that canopy cover signifi-
cantly affected the density of seedlings or saplings. In contrast,
the effect of canopy cover was overruled by other factors at all
stages of the tree regeneration process that we studied. In the
case of seedlings, the most influential factor (vegetation cover)
is only indirectly related to canopy cover, and the most influen-
tial factor for saplings £50 cm (soil fertility) is not related to
canopy cover in our study system. The absence of a relation
between canopy cover and recruitment into the larger size clas-
ses (saplings >50 cm) can for a large part be explained by the
relatively closed canopy observed in all our study plots, which
is typical for old-growth forest. Additionally, selective foraging
of ungulates inside forest gaps comparedtoclosedforest(Kuij-
per et al. 2009) may repress enhanced tree regeneration inside
forest gaps.
The effects of ungulates on total tree recruitment depended
on the size class of trees. Neither did they affect the cumulative
number of seedlings throughout the study period nor the num-
ber of trees £50 cm, indicating that the input of seedlings and
saplings in the tree regeneration process is not different in the
presence or absence of ungulates. The lack of effects of ungu-
lates on seedlings and trees in the smallest size class is in con-
trast to results from studies in other temperate forest systems
which illustrated that ungulate browsing can strongly reduce
seedling density (Kumar & Shibata 2007; Long, Pendergast &
Carson 2007; Olesen & Madsen 2008). This may first of all be
related to the large differences in ungulate density between
these areas and our study area. The densities of the dominant
browser in these systems were 2- to 13-fold higher than those in
the present study system (17.5–39.5 sika deer km
)2
:Kumar&
Shibata 2007; 12 white-tailed deer km
)2
: Long, Pendergast &
Carson 2007; 24 roe deer km
)2
: Olesen & Madsen 2008).
These large differences may reflect the dissimilarity in hunting
management, presence of predators or productivity between
their and our study systems. A second important factor
explaining the observed differences in effects of ungulates may
be related to structural diversity of the forest in different study
areas. Naturally developed forests, as in the present study, are
characterized by rich undergrowth and a multi-layered tree
structure, in contrast to managed forests (Je˛drzejewska et al.
1994). Hence, food for browsing ungulates is abundant at dif-
ferent height classes in natural forests, whereas it may comprise
only certain height classes in more even-aged, managed forest
systems. As the preferred foraging height of red deer, the most
abundant ungulate species in our system, is 50–150 cm (Re-
naud, Verheyden-Tixier & Dumont 2003; S. Mis
´cicki, unpubl.
data), a higher food availability at this preferred forage height
may have prevented intense foraging on trees at lower, less pre-
ferred heights.
In the present study, ungulates played a dominant role in
affecting tree recruitment only into size classes >50 cm.
Within this size class, more than three times higher numbers of
trees occurred inside exclosures compared to controls after
7 years. Therefore, the presence of ungulates results in a ‘herbi-
vore trap’ at about 50 cm from which many trees cannot
escape. We suggest that this ‘herbivore trap’ might be function-
ally similar to the ‘fire trap’ that was shown in studies from
African savanna systems (Skowno et al. 1999). The regular
occurrence of fires can prevent trees from regenerating into tal-
ler size classes in which they would be resistant to fire (Skowno
et al. 1999). Constant browsing by ungulates may act in a simi-
lar way, in which small but relatively old trees are being
trapped at a certain height. These suppressed individuals,
called ‘gullivers’ by Bond & van Wilgen (1996), are only able to
896 D. P. J. Kuijper et al.
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Ecology,98,888–899

escape from this herbivore trap once they are released from
herbivore control caused by a population crash of browsing
ungulates (Prins & Van der Jeugd 1993). This illustrates the
important top-down effects that ungulates can have in natural
temperate forest systems in determining the recruitment of
trees and ultimately may affect species composition and age
structure of the tree stand.
UNGULATE IMPACTS ON TREE SPECIES COMPOSITION
In the present study, besides influencing total recruitment,
ungulates affected species composition of trees recruiting into
the >50 cm size classes, whereas they did not affect species
composition in either the seedling or sapling (£50 cm) size
class. Species composition of trees taller than 50 cm was
affected by ungulates in two different ways. On the one hand,
the number of tree species increased inside exclosures. This dif-
ference could not be explained by higher numbers of species
which exclusively occurred inside exclosures, as Pinus sylvestris
was only found inside exclosures. All other species were found
both in exclosures and controls, albeit in lower numbers per
species and in a lower number of plots in the controls. Hence,
the difference in the number of species is mainly the result of
simultaneous occurrence of several species inside exclosures
versus recruitment of a single species in controls. On the other
hand, tree species occurred in more equal proportions inside
exclosures compared to the controls, as indicated by the higher
Shannon index. Whereas Carpinus betulus strongly dominated
the control plots, comprising more than 68% of all present
trees, its dominance was reduced to 38% inside exclosures due
to higher recruitment of other species. The impact of ungulates
on tree species composition shows that apart from an overall
reduction of recruitment, the ‘herbivore trap’ acts as a filter,
which only some species are able to pass so that they can suc-
cessfully regenerate. This results in a higher dominance of only
few or a single species in the presence of ungulates, which has
also been observed in other studies carried out in temperate
forest systems (Ammer 1996; Kriebitzsch et al. 2000; Find’o &
Petra
´s
ˇ2007). Such a shift in species composition of regenerat-
ing trees may affect forest communities and alter species
composition (Kwiatkowska & Wyszomirski 1990).
The higher dominance of Carpinus in the presence of ungu-
latesisinterestingasCarpinus constitutes an important food
plant in the diet of the three most common ungulates (red deer,
roe deer and bison) in the system (Ge˛bczyn
´ska 1980; Ge˛bc-
zyn
´ska, Ge˛bczyn
´ski & Martynowicz 1991). In addition, of all
trees present in BPF Carpinus was shown to have the highest
proportion of individuals in the size class up to 130 cm with its
leader shoot browsed (Mis
´cicki 1996; B. Brzeziecki, unpubl.
data). This indicates the strong selective foraging of ungulates
on this species compared to other species. Hence, the domi-
nance of Carpinus in the recruitment in control plots is not the
result of avoidance by ungulates. Other studies from temperate
forest systems showed that by selective foraging ungulates may
differentially affect the recruitment of tree species, either lead-
ing to a reduction (Horsley, Stout & DeCalesta 2003; Modry,
Hubeny & Rejsek 2004; Long, Pendergast & Carson 2007) or
an increase (Tilghman 1989; Van Hees, Kuiters & Slim 1996)
in relative abundance of the preferred forage species. A possi-
ble mechanism for increasing abundance of preferred species
in the presence of herbivores is that preference coincides with a
high browsing-tolerance (Augustine & McNaughton 1998).
The observed patterns suggest that Carpinus is one of the most
browsing-tolerant species in the studied system and can
regenerate despite high browsing pressure. This might be a
result of ‘apparent competition’, where a high tolerance to
browsing together with a high preference by ungulates favours
Carpinus as long as other potentially competing species are also
browsed but show lower tolerance (see also Kriebitzsch et al.
2000).
How the observed effects of herbivory on the recruitment
and species composition of relatively small trees translate into
later stages and finally into the structure of mature stands
may not be straightforward (Mladenoff & Stearns 1993;
Woodward et al. 1994). Population dynamics of trees are
shaped by inter- and intraspecific competition after the sapling
stage (Hulme 1996). However, the above-mentioned patterns
in species composition are supported by the observed
long-term changes (1936–2002) in tree recruitment rates in
BPFinrelationtochangesinungulate density (D. P. J. Kuijper
et al., unpubl. data) and the observed changes in tree canopy
composition in the same period (Bernadzki et al. 1998).
Periods of several years with low ungulate density resulted in
high recruitment of virtually all tree species. However,
Carpinus was the only species that showedhighregeneration
under levels of high ungulate density. This suggests that the
effects of ungulates during early life stages carry over on
the mature tree stands, and they do play an important role in
tree canopy composition.
BIOTIC AND ABIOTIC INTERACTIONS SHAPE
UNGULATE TOP-DOWN EFFECTS
Most studies on the impact of ungulates in temperate forest
systems have been carried out in single-ungulate-species-domi-
nated systems (see for example Ammer 1996; Van Hees, Kuit-
ers & Slim 1996; Kriebitzsch et al. 2000; Scott et al. 2000;
Long, Pendergast & Carson 2007) mainly because most sys-
tems have a greatly impoverished faunal community. Interac-
tions between multiple ungulate species that co-occur in an
area can alter their net effects on the plant community (Gor-
don 1988; Ritchie & Olff 1997; Latham et al. 1999; Young,
Palmer & Gadd 2005). In addition, the presence of carnivores
can influence behaviour, habitat choice and spatial distribution
of ungulate species (Creel et al. 2005; Fortin et al. 2005; Frair
et al. 2005). Recent studies suggest that these indirect (non-
lethal) effects of carnivores may be as important (Schmitz,
Beckerman & O’Brien 1997) or even more important in
influencing herbivore–plant interactions as the release form
herbivore top-down control by population reduction per
se (Oksanen et al. 1981; Creel & Christianson 2008). The pres-
ent study illustrates the context-dependence of herbivore top-
down effects. It thus shows that besides biotic factors, abiotic
bottom-up factors can shape herbivore top-down effects.
Abiotic and biotic control of tree regeneration 897
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Heterogeneity in abiotic and biotic conditions may, therefore,
have an important influence on the strength of top-down
effects and the role that herbivores play in natural ecosystems
(see also Gilliam 2006). In most managed forest systems, many
natural components, such as diverse tree species composition,
undisturbed forest regeneration, heterogeneous soil condi-
tions, multiple large ungulate species or presence of predators
are missing. In such more homogeneous environments, one
dominant factor is expected to prevail, leading to a directional
selection pressure favouring only a few tree species during the
stages of the regeneration process. The relative lack of hetero-
geneity and stochasticity in managed forest systems may
prevent the alternating effects of biotic and abiotic factors
influencing tree recruitment observed in the present study.
These alternating effects may warrant that most tree species
do show successful recruitment, albeit at a lower rate, in the
presence of ungulates.
There has been a recent paradigm shift in forest
management towards a more ecosystem-oriented approach
(Puettmann & Ammer 2007). However, knowledge on forest
ecosystem functioning is scarce and often based on highly
managed forest systems. Our study area comprises the least
disturbed and most complete temperate forest system in
lowland Europe (Je˛drzejewska et al. 1994). Hence, it offers
insight into the role played by ungulates in an intact
old-growth forest and can serve as a reference for other forest
systems in the temperate region.
Acknowledgements
This study was financed by the grant 5P06H03418 from the Ministry of Science
and Higher Education, Poland.The work of D.P.J.K. and J.P.G.M.C.has been
supported by a Marie Curie Transfer of Knowledge Fellowship BIORESC of
the European Community’s Sixth Framework Programme under contract
number MTKD-CT-2005-029957. We are very thankful to several people who
helped with data collection: Małgorzata Piotrowska, Renata Czarnecka, Edyta
Nowicka, Dariusz Mro
´z, Matt Hayward, Anne Velenturf, Basia Ban
´ka. We
thank Roman Kozakfor his technical help in maintaining the exclosures.
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Handling Editor:Frank Gilliam
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