Oak regeneration at the arid boundary of the temperate deciduous forest biome: insights from a seeding and watering experiment

Abstract

Previous studies found that pedunculate oak, one of the most widespread and abundant species in European deciduous forests, regenerates in open habitats and forest edges, but not in closed forest interiors. However, these observations usually come from the core areas of the biome, and much less is known about such processes at its arid boundary, where limiting factors may be different. In a full factorial field experiment, we tested the effects of different habitats (grassland, forest edge, forest interior) and increased growing season precipitation on the early regeneration of pedunculate oak in a forest-steppe ecosystem in Central Hungary, at the arid boundary of temperate deciduous forests. In the grassland habitat, seedling emergence was very low, and no seedlings survived by the fourth year. In contrast, seedling emergence was high and similar at forest edges and forest interiors, and was not affected by water addition. Most seedlings survived until the fourth year, with no difference between forest edge and forest interior habitats in numbers, and only minor or transient differences in size. The lack of oak regeneration in the grassland differs from previous reports on successful oak regeneration in open habitats, and may be related to a shift from light limitation to other limiting factors, such as moisture or microclimatic extremes, when moving away from the core of the deciduous forest biome towards its arid boundary. The similar number and performance of seedlings in forest edges and forest interiors may also be related to the decreasing importance of light limitation.

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European Journal of Forest Research (2021) 140:589–601
https://doi.org/10.1007/s10342-020-01344-x
ORIGINAL PAPER
Oak regeneration atthearid boundary ofthetemperate deciduous
forest biome: insights fromaseeding andwatering experiment
LászlóErdős1,2 · KatalinSzitár1 · KingaÖllerer1,3 · GáborÓnodi1 · MiklósKertész1 · PéterTörök2 ·
KornélBaráth4· CsabaTölgyesi5 · ZoltánBátori5 · LászlóSomay1· IldikóOrbán6 · GyörgyKröel‑Dulay1
Received: 14 August 2020 / Revised: 26 November 2020 / Accepted: 4 December 2020 / Published online: 23 January 2021
© The Author(s) 2021
Abstract
Previous studies found that pedunculate oak, one of the most widespread and abundant species in European deciduous forests,
regenerates in open habitats and forest edges, but not in closed forest interiors. However, these observations usually come
from the core areas of the biome, and much less is known about such processes at its arid boundary, where limiting factors
may be different. In a full factorial field experiment, we tested the effects of different habitats (grassland, forest edge, forest
interior) and increased growing season precipitation on the early regeneration of pedunculate oak in a forest-steppe ecosystem
in Central Hungary, at the arid boundary of temperate deciduous forests. In the grassland habitat, seedling emergence was
very low, and no seedlings survived by the fourth year. In contrast, seedling emergence was high and similar at forest edges
and forest interiors, and was not affected by water addition. Most seedlings survived until the fourth year, with no difference
between forest edge and forest interior habitats in numbers, and only minor or transient differences in size. The lack of oak
regeneration in the grassland differs from previous reports on successful oak regeneration in open habitats, and may be related
to a shift from light limitation to other limiting factors, such as moisture or microclimatic extremes, when moving away from
the core of the deciduous forest biome towards its arid boundary. The similar number and performance of seedlings in forest
edges and forest interiors may also be related to the decreasing importance of light limitation.
Keywords Pedunculate oak· Quercus robur· Forest-steppe· Seedling emergence· Temperate deciduous forest
Introduction
Temperate deciduous forests characterised by various oak,
hornbeam, linden, maple, ash, and beech species cover vast
areas in Europe (Schultz 2005). They harbour high species
richness at the local scale show high net primary produc-
tion, and possess considerable carbon sequestration capac-
ity (Pfadenhauer and Klötzli 2014). Though the composi-
tion, structure, and abiotic parameters of these forests are
well studied (Pfadenhauer and Klötzli 2014), considerable
debates regarding their dynamics still exist (e.g., Vera 2000;
Svenning 2002; Szabó 2009; Gillian 2016). Uncertainties
about the dynamics and especially the natural regeneration
of temperate deciduous forests are at least partly due to the
fact that most of these forests have been heavily modified
by human use during the last couple of millennia, severely
compromising natural processes (Ellenberg 1988; Walter
and Breckle 1989; Schultz 2005; Kirby and Watkins 2015;
Gillian 2016).
Communicated by Christian Ammer.
* László Erdős
erdos.laszlo@ecolres.hu
1 Institute ofEcology andBotany, MTA Centre forEcological
Research, Vácrátót, Hungary
2 MTA-DE Lendület Functional andRestoration Ecology
Research Group, Debrecen, Hungary
3 Institute ofBiology Bucharest, Romanian Academy,
Bucharest, Romania
4 Department ofBiology, Savaria University Centre, Eötvös
Loránd University, Szombathely, Hungary
5 Department ofEcology, University ofSzeged, Szeged,
Hungary
6 Department ofPlant Systematics, Ecology andTheoretical
Biology, Eötvös Loránd University, Budapest, Hungary
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590 European Journal of Forest Research (2021) 140:589–601
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Pedunculate oak (Quercus robur) is one of the most
important tree species in European temperate deciduous for-
ests, dominating lowland forests in a huge belt from Britain
to the Ural Mts (Walter and Breckle 1989; Bohn etal. 2004).
However, it has been recognised that the natural regeneration
of this species is frequently deficient (Shaw Shaw 1968a, b;
Reif and Gärtner 2007; Annighöfer etal. 2015). It is well-
known that pedunculate oak is a light-demanding species
(Annighöfer etal. 2015; Leuschner and Ellenberg 2018).
Therefore, its regeneration depends on open or semi-open
sites with relatively high light availability, such as forest
edges, hedges, shelterwoods, openings, and grasslands, and
it is not successful in forest interiors (Reif and Gärtner 2007;
Leuschner and Ellenberg 2018; reviewed by Bobiec etal.
2018).
Besides light availability, other key factors influencing
the regeneration of pedunculate oak include water supply,
competition from ground vegetation, zoochory, grazing
and browsing (Vander Wall 2001; Annighöfer etal. 2015,
Schäfer etal. 2019). Water supply is a critical factor during
oak germination and seedling development (Dreyer etal.
1991, Bobiec etal. 2018). While water scarcity is relatively
rare in Western Europe and in partially shaded habitats, its
effect may be much more important in drier regions and in
open habitats (Löf etal. 1998; Reif and Gärtner 2007). Com-
petition heavily influences the survival of seedlings (Jensen
and Löf 2017), but it may be reduced in sites where the herb
layer is sparse or where ungulates open up the dense sward
(Reif and Gärtner 2007). Grazing and browsing can affect
seedling survival and performance negatively, but the nutri-
ent reserves of the cotyledon enable oak seedlings to with-
stand a certain level of defoliation (Frost and Rydin 1997),
while thorny shrubs and the high abundance of other, more
palatable species can protect oak seedlings from grazing and
browsing (Bakker etal. 2004; Jensen etal. 2012). To sum it
up, an area ideal for pedunculate oak regeneration has been
described as providing sufficient moisture and consisting of
a mosaic of forests, thickets, shrubs, solitary trees, grass-
lands, and the ecotones between these habitats (Vera 2000;
Bakker etal. 2004; Bobiec etal. 2018).
Biome boundaries are regions where several species
reach their distributional limits, and there is a major shift
in the physiognomy of the vegetation (Walter 1985; Gosz
and Sharpe 1989, Neilson 1993; Peters etal. 2006, Pinto-
Ledezma etal. 2018). In these transitional zones, patches
from both adjoining biomes form a mosaic pattern. Con-
straints operating in the transitional zones are typically
different from those operating within the core areas of the
biomes (Gosz and Sharpe 1989; Risser 1995). In addition,
species that are dominant in the core area of the biome may
become limited to specific habitats (with special micro-
climates) towards the biome boundary (Gosz 1992, 1993;
Neilson 1993). Environmental changes, including climate
change, are likely to substantially affect biome boundaries
(Gosz and Sharpe 1989; Allen and Breshears 1998, Frelich
and Reich 2010). Germination and establishment may be
critically affected, resulting in altered dynamic processes
in biome boundaries (Gosz 1992; Risser 1995; Erdős etal.
2018a).
The forest-steppe zone is at the arid boundary of the tem-
perate deciduous forest biome: as, largely due to climatic
constraints, closed-canopy forests open up and gradually
give way to grasslands, a mosaic of woody and herbaceous
habitats emerges (Wesche etal. 2016; Erdős etal. 2018a).
Pedunculate oak is a major constituent not only in the decid-
uous forest biome of Europe, but also in these mosaic eco-
systems (Molnár etal. 2012; Erdős etal. 2018a). While the
regeneration of pedunculate oak has been intensively studied
within the core areas of the deciduous forest biome, oak
regeneration patterns at the arid boundary of the biome are
mostly unstudied (Bobiec etal. 2018).
In this study, our objective was to understand the effects
of different habitats (forest interior, forest edge, and grass-
land) and watering on oak germination and early seedling
performance. The experimental area lies at the arid bound-
ary of the deciduous forest biome, where growing season
precipitation strongly constrains woody vegetation, there-
fore, we expected that the natural regeneration of oak heav-
ily depends on the amount of precipitation. Accordingly,
our hypothesis was that oak seedling emergence and growth
would be positively affected by water addition, especially in
grasslands, where evapotranspiration and thus water limita-
tion is highest. Furthermore, in line with previous studies,
we also hypothesised that seedling emergence and perfor-
mance would be high in grasslands (only when watered)
and in forest edges, but lower and declining through time in
forest interiors, because of light limitation.
Materials andmethods
Study area
The Kiskunság Sand Ridge in Central Hungary lies at the
arid boundary of the temperate deciduous forest biome. The
area is the most arid part of the Carpathian Basin, with a
mean annual temperature of 10.5 °C (17.4 °C in the grow-
ing season from April to September), and a mean annual
precipitation of 530mm (310mm in the growing season)
(Dövényi 2010). The area is characterised by stabilised cal-
careous sand dunes, with humus-poor sandy soils (Várallyay
1993). Due to a combination of semiarid climate and coarse-
textured sandy soil, forests open up and the potential vegeta-
tion is forest-steppe, with both forests and grasslands being
natural and permanent elements of the landscape, and form-
ing a mosaic (Erdős etal. 2018a).
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591European Journal of Forest Research (2021) 140:589–601
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Pedunculate oak, a characteristic species of the temper-
ate deciduous forests, is also present in this forest-steppe
mosaic (Rédei etal. 2020), although its abundance is highly
variable and is strongly affected by land use in the past cen-
turies (Biró etal 2013, Erdős etal. 2015). The study area
is located near Fülöpháza, Central Hungary; N 46°52’, E
19°25’) (Fig.1a), where pedunculate oak is currently rela-
tively rare, most likely due to previous land use, but the
species is a typical component in several forest-steppe areas
in the region.
The forest component of the vegetation mosaic at the
study area is represented by the juniper-poplar forest Juni-
pero-Populetum albae. The canopy layer is formed mainly
by 12–15m tall Populus alba individuals. For trees with
DBH over 5cm, stand density is 1450 trees/ha (Erdős etal.
2018b). The shrub layer is dominated by Juniperus com-
munis and Crataegus monogyna. The most frequent species
of the herb layer are Asparagus officinalis, Carex flacca, C.
liparicarpos, Poa angustifolia, and the seedlings of trees
and shrubs.
Among the various grassland communities of the study
area, the open perennial sand grassland Festucetum vagina-
tae is the most widespread. Its dominant species are Fes-
tuca vaginata, Stipa borysthenica, and S. capillata, while
Alkanna tinctoria, Dianthus serotinus, Euphorbia seguie-
riana, Fumana procumbens, and Poa bulbosa are also
common.
The contact zones of the forest patches and the grasslands
host specific edge communities with various shrubs (e.g.
Berberis vulgaris, Crataegus monogyna, Juniperus com-
munis) and a high density of Populus alba saplings. The
most frequent and abundant species of the herb layer include
Calamagrostis epigeios, Festuca rupicola, Pimpinella saxi-
fraga, and Taraxacum laevigatum.
Fig. 1 The position of the study area (black dot) in the Kiskunság
Sand Ridge (grey shading) (a), the experimental design with oak
acorns (black dots) in the 0.5 m × 0.5 m plots in the three habitats
under study (C: control plots, W: watered plots) (b), the grassland
habitat (c), the forest edge habitat (d), and the forest interior habitat
(e)
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592 European Journal of Forest Research (2021) 140:589–601
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The study area belongs to the Kiskunság National Park; it
is strictly protected, and every major human activity except
research and controlled tourism has been banned since 1975.
The browsing pressure by native ungulates (mostly roe deer)
is relatively low, but no particular study assessed this issue
in the region. The study area is part of the KISKUN Long-
term Ecological Research platform (KISKUN LTER, https ://
deims .org/124f2 27a-787d-4378-bc29-aa94f 29e17 32).
The plant species names follow Király (2009), while the
plant community names are used according to Borhidi etal.
(2012).
Experimental design
Quercus robur acorns were collected in October 2015 from
a nearby patch of seed producing oaks. To exclude acorns
with reduced viability, we carried out visual inspection and a
float test. The float test is reliable in identifying aborted, dis-
eased, insect-infested or otherwise damaged acorns (Gribko
and Jones 1995).
Sixteen sites were selected within a ca. 400m × 1100m
area in a natural forest-grassland mosaic. For each site, three
habitats were defined: forest interior (within the forest patch,
10m from the forest edge), forest edge (the zone outside of
the outermost tree trunks but still under the canopy, on the
northern side of forest patches), and grassland (a neighbour-
ing treeless area, 10m from the edge). At each habitat, two
0.5m × 0.5m plots were designated in a row parallel to the
forest edge. Within both plots, three acorns were planted at a
depth of 2cm in November 2015 (Fig.1b-e). A total of 288
acorns was used in the experiment (16 sites × 3 habitats × 2
plots × 3 acorns).
At each site and habitat, we applied two precipitation
treatments in the two plots: one plot received ambient pre-
cipitation (control), while the other plot received additional
watering ten times between 5 April and 6 September in their
first year (2016). Watering was started in April, because
temperature is low until March (ca. 6 °C mean temperature
in March) and no water limitation occurs during wintertime.
For watering, we used rainwater collected nearby, and the
amount added corresponded to 15mm precipitation each
time, resulting in a total of 150mm watering during the
year. The additional watering was 36.5% of the natural pre-
cipitation in the growing season and 20.2% of the yearly
precipitation in 2016.
Seedlings were individually censused every two or 3
weeks in the first year. The performance of the seedlings
was measured near the end of the growing season of the first
and the fourth years (19 September 2016 and 25 September
2019, respectively), by registering the following parameters
for each plot: (1) the number of living seedlings, (2) the
number of leaves per living seedling, and (3) the height of
the living seedlings.
During the growing season of 2016, we measured the
volumetric soil moisture content of the upper 20cm every
2 or 3 weeks from 5 April till 6 September, using FieldS-
cout TDR300 Soil Moisture Meter (Spectrum Technologies
Inc). Since soil texture is very similar across the different
vegetation types in the study area including grasslands and
woodlands (Kröel-Dulay etal. 2019), soil water content is
a good measure of soil water availability for plants in the
different habitats. We measured soil water content before
watering at each site and 5h after watering in three a priori
chosen sites. These two measurements aimed at assessing
the longer (ca. 2-week-long) and the short-term (right after
watering) effects of watering on the soil moisture content.
For each 0.5m × 0.5m plot, three measurements were done
and then averaged. Means for the whole growing season
were calculated for each plot.
The Leaf Area Index (LAI) of the woody canopy was esti-
mated above the herbaceous layer (25cm) using a LAI 2000
Plant Canopy Analyser instrument (LI-COR, Inc., Lincoln,
Nebraska). The measurements were conducted in each plot
at peak canopy coverage, 30 July 2016, under clear weather
conditions. The total cover of the herb layer (percentage of
the 0.5m × 0.5m plot) was estimated visually on 19 Sep-
tember 2016.
Statistical analyses
All statistical analyses were carried out using the R envi-
ronment version 3.4.3. (R Core Team 2017). We compared
the abiotic conditions of the treated and untreated plots in
the three habitat types by using linear mixed-effects (LME)
models (nlme package; Pinheiro etal. 2017). We built indi-
vidual models for soil moisture content before and after
watering, LAI, and total herb cover. In the models, habitat
type and treatment, and their interaction were used as fixed
effects, while site was used as a random effect. As the soil
water was measured at only three sites after watering, we
analysed the short-term effect of watering by using a linear
model where habitat type, watering, and site were all used
as fixed effects.
A generalised mixed-effects model (GLMM) with bino-
mial distribution was applied to assess seedling numbers.
In these models, the germination success or failure of each
acorn was treated as a binary response variable, while habi-
tat type and watering were used as fixed variables, and site
as a random variable. Individual models were built for each
time. As no seedling survived in the grassland till the fourth
year, we did not consider the effect of this habitat type in the
respective model.
The effect of habitat type and watering treatment on the
leaf number and height of the oak seedlings in both 2016
and 2019 were assessed by applying LME models. In these
models, we did not consider the grassland habitat type, as
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593European Journal of Forest Research (2021) 140:589–601
1 3
too few seedlings survived in the grassland plots (only 4
individuals by the end of 2016 and none till 2019). Leaf
numbers and height data were square-root transformed to
meet the homogeneity and normality assumptions of the
tests.
We made visual assessments of the residual diagnostic
plots to check the assumptions of the tests. For post hoc
pairwise comparisons, we performed Tukey tests using the
multcomp package (Hothorn etal. 2016).
Results
Inherent differences amongthestudied habitats
The cover of the herb layer was similar in the grassland
and the forest edge habitats, while it was much lower in
the forest interior habitat (Table1, Fig.2a). Note that the
cover of the herb layer was relatively low (below 50%)
even in the grassland and the forest edge habitats. The LAI
of the overstorey vegetation showed marked differences
among the habitats, with the lowest value in grasslands,
intermediate values at the forest edges, and the highest
values in the forest interiors (Fig.2b). Average growing
season soil moisture content was the lowest in grasslands,
while it was higher and similar at the forest edge and the
forest interior habitats (Fig.2c, d; control plots).
Effect ofwatering treatment onsoil moisture
content
Watering substantially increased soil moisture content in all
the three habitats right after watering (Fig.2c), and some of
this effect remained even ca. 2 weeks after watering (before
the next watering), although post hoc tests showed that this
was only significant in the forest interior habitats (Fig.2d).
Seedling emergence andsurvival
Seedling emergence rate was very low in grassland habitats
(on average 0.3 acorns germinated out of 3), but was high
(on average 2.5 out of 3) and similar in forest edges and
forest interiors (Table2, Fig.3a). Water addition did not
affect the emergence rate (Table2, Fig.3a). Even the few
seedlings that emerged in grasslands died by the fourth year,
September 2019 (Fig.3c). Seedling number remained high
(on average 2) in forest edge and forest interior habitats until
September 2019, and was affected neither by habitat (for-
est edge vs. forest interior) nor by water addition (Table2,
Fig.3b–c).
Seedling performance
In September 2016, there was no difference in the leaf num-
ber of the seedlings between the forest edge and the forest
interior habitats (Table2, Fig.4a), while in September 2019,
seedlings in forest edges had more leaves than seedlings in
forest interiors (Table2, Fig.4b). Seedlings were taller in
the forest interior habitat in 2016 (Fig.4c), but there was
no difference in plant height between the habitats in 2019
(Fig.4d). Watering had no effect on leaf number and plant
height at either time (Table2, Fig.4). In general, oak seed-
lings grew very little from 2016 to 2019, and were still very
short and had few leaves at the age of 4years (Fig.4).
Discussion
In contrast to our first hypothesis, watering throughout the
growing season did not improve oak seedling emergence and
subsequent seedling performance, and this was consistent
across all habitat types. Oak seedling emergence and seed-
ling survival were extremely low in the grassland habitat,
which is in contrast to previous reports from the core areas
of the deciduous forest biome, where pedunculate oak most
often regenerates in open or semi-open habitats (Bakker
etal. 2004; Bobiec etal. 2018). We did not find a nega-
tive effect of the forest interiors compared to forest edges
Table 1 Linear mixed-effects and linear model results of the effects
of habitat type, watering on the total cover of the herb layer, soil
moisture content before and 5h after watering, and leaf area index
(LAI)
P values are rounded to three digits
(P<0.05) values are shown in bold
Variables and effects df F P
Total herb cover
Habitat type 2 16.9 0.000
Watering 1 0.9 0.350
Habitat type × watering 2 0.1 0.891
LAI
Habitat type 2 318.7 0.000
Watering 1 1.0 0.344
Habitat type × watering 2 0.2 0.844
Soil moisture content right after watering
Habitat type 2 66.2 0.000
Watering 1 315.1 0.000
Site 2 0.3 0.774
Habitat type × watering 2 14.4 0.001
Soil moisture content ca. 2 weeks after watering
Habitat type 2 86.2 0.000
Watering 1 12.1 0.000
Habitat type × watering 2 2.6 0.080
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594 European Journal of Forest Research (2021) 140:589–601
1 3
on seedling numbers and performance throughout the four
years of the study, while previous studies reported that the
shade tolerance of oak seedlings is very low (Lorimer etal.
1994; Welander and Ottosson 1998; Leuschner and Ellen-
berg 2018). These results suggest that patterns of early oak
regeneration at this site at the arid boundary of the temper-
ate deciduous forest biome substantially differ from those
previously reported from the core area of the biome. This is
most likely related to a shift in oak regeneration from light
limitation in the core zone to other limiting factors at the
biome boundary.
Effect ofwatering
Even though we managed to substantially increase soil
moisture content during the experiment, excess water had
no effect on oak regeneration, which is in striking contrast
to our expectation. The pot experiment of van Hees (1997)
showed that moist conditions positively affect the height,
biomass, and leaf area of Q. robur seedlings. The study of
Urli etal. (2015) revealed that Q. robur seedlings and sap-
lings react sensitively to drought stress in Southwest France
and are not able to survive under very dry circumstances.
In a Mediterranean mountain environment, Mendoza etal.
(2009) found that watering increased the survival of Q. ilex
and Q. pyrenaica seedlings in open and shrubby habitats,
while it was not affected under tree canopies, where sur-
vival was high even in the absence of watering. In a similar
study conducted in Mediterranean ecosystems, Matías etal.
(2012a, b) showed that additional watering during the sum-
mer is able to increase the survival of Q. ilex seedlings in
open, shrubby, and forest habitats.
Fig. 2 The cover of the herb layer (a), leaf area index (b), soil moisture content 5h after watering (c), and soil moisture content 2 weeks after
watering (d) in the three habitats (grassland, forest edge, and forest interior). C: control plots, W: watered plots
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595European Journal of Forest Research (2021) 140:589–601
1 3
The lack of response to watering in our experiment
may be related to the fact that 2016 was an unusually
wet year. Yearly total precipitation in 2016 was 742mm,
compared to the long-term mean of 530mm; and grow-
ing season precipitation was 410mm, compared to the
long-term mean of 310mm. The fact that even a year of
above-average precipitation combined with excess water
resulted in very low emergence and no survival in grass-
land patches suggests that grasslands are truly incapable
of supporting oak regeneration in this ecosystem.
In our experiment, watering lasted throughout the
growing season, from early April to September. Although
we did not assess potential effect of water limitation
outside the growing season, the cool temperature com-
bined with usually substantial water in this period (an
average 30–50mm per month, Kovács-Láng etal 2000)
makes water limitation unlikely.
Effect ofhabitat type
In contrast to our hypothesis that the forest edge would rep-
resent the best habitat for seedlings while the grassland (due
to drought) and the forest interior (due to shade) habitats
would be less suitable, we found that seedling emergence
and performance were extremely poor in grasslands while
they were high in forest edges and forest interiors. Thus,
forest edges and forest interiors proved to be similarly suit-
able for early oak regeneration, despite the strong differ-
ences regarding abiotic parameters in these two habitats.
It is possible that increased soil moisture in forest interiors
and forest edges compensate seedlings for the shady condi-
tions; a similar compensatory effect has been described by
Mellert etal. (2018).
Oak regeneration was absent in the grassland habitat:
seedling emergence was extremely low and the few seedlings
that did emerge died by September 2019. This finding differs
from earlier studies conducted in the temperate deciduous
forest biome. For example, Bakker etal. (2004) found that
the survival and performance of pedunculate oak seedlings
was better in grasslands than in forest interiors in riverine
floodplains of western Europe (Germany, the Netherlands,
and Great Britain). Similarly, Q. robur is able to colonise
abandoned ploughlands and pastures as shown in France
(Onaindia etal. 2001) and Poland (Bobiec etal. 2011b).
The study of Olrik etal. (2012) showed successful colonisa-
tion by pedunculate oak in a heathland in Denmark, while
oak can occupy abandoned pastures in Poland and Ukraine
(Ziobro etal. 2016). In Belgium, several non-woody vegeta-
tion types such as grasslands, ruderal fields, and bramble
thickets proved to be appropriate for Q. robur emergence
(Van Uytvanck etal. 2008). Thus, it seems that Q. robur can
easily regenerate in open (i.e. non-woody) habitats in the
core areas of the temperate deciduous forest biome (Bobiec
etal. 2018).
However, studies from Mediterranean habitats with
oak species other than pedunculate oak indicated that oak
regeneration may be limited in open habitats. For example,
Mendoza etal. (2009) reported from southern Spain that the
seedling survival of two Mediterranean oak species, Q. ilex
and Q. pyrenaica, was the lowest in open habitats, while it
was much higher under shrubs and in woodlands. Matías
etal. (2012b) found that the emergence of Q. ilex was very
good in open habitats, but the survival of the seedlings was
poor in the same habitat, presumably due to drought stress.
Similarly, in southern France, Rousset and Lepart (2000)
showed that the germination and survival of Q. humilis was
Table 2 Results of generalised linear mixed-effects model and linear
mixed-effects models of habitat type and watering treatment on ger-
minated seedling number, leaf number, and plant height
P values are rounded to three digits
(P<0.05) values are shown in bold
Variables and effects df Chisq P
Germinated seedlings
Habitat type 2 34.09 0.000
Watering 1 0.04 0.841
Habitat type × watering 2 0.94 0.625
Seedling number in September 2016
Habitat type 2 28.86 0.000
Watering 1 0.01 0.937
Habitat type × watering 2 1.18 0.553
Seedling number in September 2019
Habitat type 1 0.04 0.832
Watering 1 0.04 0.832
Habitat type × watering 1 0.39 0.532
Leaf number in September 2016
Habitat type 1 2.44 0.118
Watering 1 0.03 0.872
Habitat type × watering 1 0.45 0.504
Leaf number in September 2019
Habitat type 1 6.14 0.013
Watering 1 0.78 0.378
Habitat type × watering 1 0.24 0.622
Plant height in September 2016
Habitat type 1 5.60 0.018
Watering 1 3.00 0.083
Habitat type × watering 1 0.01 0.937
Plant height in September 2019
Habitat type 1 0.73 0.393
Watering 1 1.18 0.277
Habitat type × watering 1 0.15 0.703
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596 European Journal of Forest Research (2021) 140:589–601
1 3
better under shrubs than in the neighbouring grassland, as
shrubs protected the seedlings from drought. In Mediterra-
nean California, the seedling transplantation study of López-
Sánchez etal. (2019) revealed that almost all seedlings of
Q. lobata and Q. agrifolia died in the open grassland, while
they had significantly higher survival rates under trees and
shrubs, where they were more protected from drought stress.
Desiccation is a critical factor during oak germination
and seedling growth (Bobiec etal. 2018). Low soil moisture
seems to be the most likely cause of poor seedling emer-
gence and performance in the grassland habitat in our study,
besides other factors, discussed below. Water limitation is
the most prominent ecological constraint in the centre of
the Carpathian Basin, with a semi-arid period during the
summer months according to the long-term climate records
(Borhidi 1993; Kun 2001). In addition, the sandy soils of the
study site have very poor water retention capacity (Várallyay
1993), further decreasing water availability. While water
limitation is relatively rare in the western and northern parts
of Europe (within the core area of the temperate deciduous
forest biome) (Reif and Gärtner 2007), it seems to be of
primary importance at the arid boundary of the biome. How-
ever, the overriding role of water limitations in grasslands
could only be proved by a more intense watering treatment
(e.g. watering more frequently, or with higher amount, or
starting already in autumn).
Competition with ground vegetation is usually considered
one of the most important factors limiting oak regeneration
(e.g. Vander Wall 2001; Reif and Gärtner 2007; Annighöfer
etal. 2015). However, we think it cannot explain the strik-
ingly poor oak regeneration in grasslands. First, the total
cover of the herb layer was very low (40% or even less) in
the grasslands of the study. Thus, there was ample space
for oak seedlings to establish. Second, the cover of the herb
layer was similar in the grasslands and the forest edges, yet
forest edges had much higher seedling emergence and per-
formance rates.
The poor oak germination and performance of the grass-
land habitat cannot be explained by browsing or predation
either (Bobiec etal. 2018). Browsing pressure is generally
low in the area, and we did not see signs of heavy brows-
ing pressure on the seedlings during our regular surveys.
Seed predation is also unlikely to differ substantially among
the three habitats, due to the small distances (few metres)
between the forest interior, forest edge, and grassland plots,
and we did not see signs of predation (e.g. soil disturbance).
Further factors potentially limiting oak regeneration
include high solar radiation and the lack of a humus layer
Fig. 3 The number of germinated oak individuals (a), individuals that
survived until September 2016 (b), and until September 2019 (c) in
the three habitats (grassland, forest edge, and forest interior). C: con-
trol plots, W: watered plots
▸
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597European Journal of Forest Research (2021) 140:589–601
1 3
(Nilsson etal. 1996), both of which might have affected
seedling emergence and survival in our study. The influ-
ence of high solar radiation may be amplified by the very
sparse herb layer, and may contribute to the drying of the
soil. Regarding the humus layer, the sandy soil of the grass-
land habitat in the study site is extremely poor in humus: the
humus content of the upper 10cm soil layer can be as low
as 0.6%, while it is considerably higher in the forest patches
(Bodrogközy 1982; Várallyay 1993; Kröel-Dulay etal. 2019;
Tölgyesi etal. 2020).
Microclimatic extremes may also contribute to the poor
oak emergence and survival in the grassland habitat. High
air temperatures measured near the soil surface in the grass-
land habitat during summer days (compared to the much
cooler forest edges and forest interiors) (e.g. Erdős etal.
2014; Tölgyesi etal. 2020) may damage the tissues and
physiological processes of pedunculate oak (Cuza 2018),
thus preventing oak regeneration in this habitat.
Our study revealed similarly high early oak regenera-
tion in forest edges and forest interiors. Good oak regen-
eration within the forest edge habitat fits our hypothesis
and is in line with earlier observations regarding habitats
optimal for oak regeneration (e.g. Vera 2000; Reif and
Gärtner 2007; Bobiec etal. 2018). For example, Herlin
and Fry (2000) showed that Q. robur is able to establish in
forest edges and hedgerows in southern Sweden. Similarly,
Bakker etal. (2004) found that edges are optimal habitats
for Q. robur regeneration throughout northwestern Europe.
We found only small and transient differences between
forest edge and forest interior habitats. Seedlings in the
forest interiors had fewer leaves than seedlings in for-
est edges, although the difference was significant only in
2019. This result is in line with earlier studies reporting
Fig. 4 The number of leaves in September 2016 (a), the number of leaves in September 2019 (b), the height of the seedlings in September 2016
(c), and the height of the seedlings in September 2019 (d) in the forest edge and forest interior habitats. C: control plots, W: watered plots
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598 European Journal of Forest Research (2021) 140:589–601
1 3
reduced leaf number in seedlings under shady conditions
(e.g. Ziegenhagen and Kausch 1995; Welander and Ottos-
son 1998). Seedlings were higher in forest interiors than
in forest edges in 2016, while no significant difference
was found in 2019. Seedlings are usually higher in shady
than in sunny habitats (e.g. Ziegenhagen and Kausch
1995; Nilsson etal. 1996; van Hees 1997; Ammer 2003).
The overall similarity of forest interiors and for-
est edges is surprising given the reported high light
requirements of pedunculate oak seedlings. According to
Leuschner and Ellenberg (2018), the shade tolerance of
Q. robur seedlings is very low. Indeed, the regeneration
of pedunculate oak depends primarily on non-forest habi-
tats (Bakker etal. 2004; Bobiec etal. 2018). However,
it has also been shown that seedlings do tolerate shady
conditions during the first few years; that is, their light
demand starts to increase only after those initial years
(e.g. Welander and Ottosson 1998; Vander Wall 2001;
Annighöfer etal. 2015). Von Lüpke and Hauskeller-Bull-
erjahn (2004) and Bobiec etal. (2011a) found that young
oak individuals are increasingly dependent on clearings
as they grow up. Ziegenhagen and Kausch (1995) argued
that the starch reserves of the young seedlings enable
them to survive in shade for a couple of years. Although
a negative effect of shading in the forest interiors may
easily be seen in the future, the lack of such difference in
the first four years is interesting given the above reports
on low shade tolerance of pedunculate oak. One possible
explanation may be that forest interiors at our site are not
as closed as forests in the biome interior (see picture in
Fig.1e). Indeed, the LAI of 3–3.5 measured at our forest
interiors is lower than that reported for several temperate
oak forests in Europe (e.g. Bréda and Granier 1996; Le
Dantec etal. 2000; Soudani etal. 2006; Thimonier etal.
2010). Another explanation for the similar performance of
oak seedlings at forest edges and forest interiors is that a
factor other than light limits growth. A major candidate in
these ecosystems can be soil moisture (Várallyay 1993),
which may also explain the extremely small size of the
4-year old oak seedlings (14–16cm).
Differences inoak regeneration betweenthecore
area andthearid boundary ofthebiome
Towards the arid boundary of the temperate deciduous
forest biome, the competitive vigour of the woody life-
forms decreases (Walter and Breckle 1989; Erdős etal.
2018a). As a consequence, forests gradually open up,
enabling the emergence of the forest-steppe zone with
alternating forest and grassland patches. The poor perfor-
mance of our seedlings, especially regarding their height,
also indicates that conditions are suboptimal for oak
regeneration at our site. Seedling height has been reported
to reach 13–20cm after one (Giertych and Suszka 2010;
Devetaković etal. 2019), and 30–60cm after only two
growing seasons (Ammer 2003; Cabral and O’Reilly
2008; Andersen 2010).
Conclusions
Our study suggests that oak regeneration pattern in this tran-
sitional zone differs markedly from what has been described
in the core areas of the temperate deciduous forest biome.
When one moves from the core areas of the deciduous forest
biome towards the arid boundary of the biome, there seems
to be a shift from light limitation to other limiting factors,
which prevent oak regeneration in grassland patches and
restrict it to forest edges, and, potentially, to forest interiors.
In conclusion, our results emphasise that oak regeneration
and thus forest dynamics may be limited by different factors
at a biome boundary compared to the biome core. Indeed,
the lack of tree regeneration in grassland patches may con-
tribute to the opening up of the closed forest biome, and the
emergence of the forest-steppe zone.
Acknowledgements The authors are thankful for the support of the
‘Momentum’ Program of the Hungarian Academy of Sciences.
Funding Open Access funding provided by ELKH Centre
for Ecological Research. This work was supported by the
Hungarian Scientific Research Fund (Grant Number OTKA
PD 116114 for László Erdős), the National Research, Devel-
opment and Innovation Office (Grant Numbers NKFIH K
119225 and NKFIH KH 129483 for Péter Török, NKFIH
K 124796 for Zoltán Bátori, NKFIH PD 132131 for Csaba
Tölgyesi, NKFIH K 129068 for György Kröel-Dulay). Kinga
Öllerer received further support from the Romanian Acad-
emy (Grant Number RO1567 IBB03/2019).
Compliance with ethical standards
Conflicts of interest The authors declare that they have no conflict of
interest.
Open Access This article is licensed under a Creative Commons Attri-
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tion, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article’s Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
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