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Trees (2023) 37:1657–1669
https://doi.org/10.1007/s00468-023-02450-0
ORIGINAL ARTICLE
Strategies fordifficult times: physiological andmorphological
responses todrought stress inseedlings ofCentral European tree
species
MarzenaNiemczyk1 · BarbR.Thomas2 · SzymonJastrzębowski1
Received: 10 March 2023 / Accepted: 17 August 2023 / Published online: 1 September 2023
© The Author(s) 2023
Abstract
Key message Picea abies and Pinus sylvestris seedlings conserve soil water and are more sensitive to drought show-
ing photoinhibition even under moderate stress, while Quercus robur and Fagus sylvatica seedlings have higher soil
water uptake, they show photoinhibition only under severe drought.
Abstract Drought is an important factor in ecological change and species distribution shifts. We conducted a greenhouse
experiment with seedlings of four Central European tree species: Pinus sylvestris (PS), Picea abies (PA), Fagus sylvatica
(FS), and Quercus robur (QR) to investigate their response to drought. We monitored maximum quantum yield of photo-
system II (Fv/Fm) during a 60-day drought treatment and measured above- and below-ground characteristics as morpho-
physiological responses to drought stress. Due to the fast, juvenile growth of the deciduous species (FS and QR), they had
higher soil water uptake and suffered more quickly from severe drought than conifers (PS and PA). The deciduous species
maintained a higher Fv/Fm, until volumetric water content (VWC) was very low (< 5%), oscillating within a narrow safety
margin. Both conifers PA and PS conserved soil water; photoinhibition in these species occurred at VWC of 14.5% and 5.5%,
respectively. There were no differences in height between drought-stressed and irrigated seedlings, while drought reduced
all root characteristics of the deciduous seedlings. Our study revealed trade-offs between different water management strate-
gies, growth rate, and photoinhibition during the juvenile growth stage of our focal species. For climate change adaptation,
anisohydric deciduous tree species seem to be more suitable. However, PS, with its water-conserving management and low
photoinhibition threshold, holds promise for successful regeneration on drought-prone sites. Since species selection is criti-
cal for forest sustainability, our study contributes to the broader discussion of tree species' drought resistance during the
vulnerable juvenile phase in the face of climate change.
Keywords Drought stress· Isohydric· Anisohydric· Maximum efficiency of PSII· Chlorophyll fluorescence· Root
characteristics
Introduction
The recent general circulation models of the World Climate
Research Programme (CMIP6 models) predict that global
warming will affect the hydrological cycle, and increase the
risk and severity of droughts in some regions of the world,
by the end of the century (Cook etal. 2020). Concomitantly,
soil drying is predicted to become more widespread, with
the severity increasing with rising temperatures (Cook
etal. 2020). Sensitivity to drought, temperature, and other
climatic conditions (e.g., length of the growing season) is
critical to the geographic distribution of individual species
and their communities (Engelbrecht etal. 2007; Dyderski
etal. 2018). The distribution of plants will be significantly
Communicated by Gärtner.
* Marzena Niemczyk
M.Niemczyk@ibles.waw.pl
1 Department ofSilviculture andForest Tree Genetics,
Forest Research Institute, Braci Leśnej 3, Sękocin Stary,
05-090Raszyn, Poland
2 Department ofRenewable Resources, University ofAlberta,
442 Earth Sciences Building, Edmonton, ABT6G2E3,
Canada
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1658 Trees (2023) 37:1657–1669
1 3
impacted by these environmental changes, but the magni-
tude of these effects will vary, depending on the species'
tolerance for water scarcity (Schipper etal. 2020; Sandoval-
Martínez etal. 2023). Nearly half of the Earth's terrestrial
surface is covered by forests (Melillo etal. 1993), and the
dominant forest-forming tree species play a key role by
providing habitat, food, or mutualisms with many animals,
fungi, microorganisms, and other plants (Aitken etal. 2008).
Therefore, a transition in the dominant tree species due to
climate change may lead to changes in the characteristics of
entire ecosystems and dependent organisms (Wulf and Naaf
2009; Lindner etal. 2010; Choat etal. 2012; Ellis 2013;
Dyderski etal. 2018; Remke etal. 2022). Changes in for-
est communities will also affect the various services that
forests provide for humans. Understanding the mechanisms
of drought tolerance/avoidance and the effects of drought
on trees is, therefore, critical for the appropriate manage-
ment of forest resources, selection of the best species and
provenances in planted forests, and conservation of forest
ecosystems (Robakowski etal. 2020).
Given trees' long lifespans, adaptation to a water-scarce
environment was one of the first challenges in their evolu-
tion, leading to the development of strategies and mecha-
nisms to cope with water deficits (Aranda etal. 2012). These
strategies include changes in root systems, hydraulic archi-
tecture, and/or stomata conductance regulation (Martínez-
Sancho etal. 2017). Stomata are the primary regulators of
water fluxes in the soil–plant–atmosphere continuum (Urban
etal. 2017). Stomatal closure leads to an improvement in
the water balance and water status of the plant by limiting
transpiration losses. However, due to drought, the cost of
stomata closure is a limitation of CO2 uptake into chloro-
plasts, a reduction in photosynthesis and growth, and sub-
sequently an increased risk of photooxidative stress (Urban
etal. 2017). In extreme cases, prolonged drought can lead
to tree death due to carbon starvation (long stomata closure)
or hydraulic failure (McDowell etal. 2008).
Recent studies (Salmon etal. 2020) have laid the founda-
tion for incorporating stomatal and non-stomatal limitations
on photosynthesis in response to drought stress. Recently,
a strong relationship between the chlorophyll fluorescence
ratio and net photosynthesis under drought stress was also
established, making chlorophyll fluorescence (ChlF) a pow-
erful tool for monitoring the photosynthetic properties of
terrestrial ecosystems under drought stress (Zhuang etal.
2020), although the kinetics of chlorophyll fluorescence
induction has been routinely used for many years to provide
information on photosynthetic performance (Lichtenthaler
and Rinderle 1988). Measurement of chlorophyll fluores-
cence is rapid, accurate, and non-invasive (Baker 2008),
and the principle of chlorophyll fluorescence analysis is
relatively straightforward (Maxwell and Johnson 2000).
When chlorophyll molecules in a leaf absorb light, the light
photons travel to the reaction centers of photosystems I (PSI)
and II (PSII), where they can be used by photosynthesis
(photochemistry), lost as heat, or re-emitted as light-chlo-
rophyll fluorescence (Maxwell and Johnson 2000; Zhuang
etal. 2020). Because each of these processes competes with
the others, ChlF can be used to provide information on
photosynthesis (Maxwell and Johnson 2000; Murchie and
Lawson 2013). To determine the most important fluores-
cence kinetic parameters, such as the maximum quantum
efficiency of the PSII (Fv/Fm), the polyphasic fluorescence
transient is used (Zhuang etal. 2020). PSII is regarded as a
susceptible component of the photosynthetic machinery and
plays a central role in photoinhibition leading to a decrease
in Fv/Fm (Long etal. 1994). Under stress, a decrease in Fv/Fm
indicates down-regulation of photosynthesis or photoinhibi-
tion (Lichtenthaler and Rinderle 1988).
Despite considerable progress in understanding the
effects of drought stress on photosynthesis and the responses
of aboveground tree components to drought, little is known
about how below-ground tree components respond to
drought and the role roots play under drought stress. This
aspect of climate change research is frequently neglected or
completely ignored and further research is required (Brun-
ner etal. 2015). However, tree root systems, in contrast to
herbaceous plant root systems, are more complex, varying in
morphology, size, and function (Brunner etal. 2015; Mariën
etal. 2021). Coarse roots, for example, with a diameter of
more than 2mm, are responsible for tree stability and act as
organs for transporting water from deeper soil horizons. Fine
roots (< 2mm in diameter), which are often non-woody and
short lived, are important for the uptake of both water and
nutrients (Mariën etal. 2021). In addition, roots can serve
as sensors of water deficit and send signals to aboveground
shoots (Hamanishi and Campbell 2011). In general, roots are
typically described by several different traits such as length
(cm), surface area, diameter, root volume, or lifespan of the
root tips. Evidence continues to increase that drought can
influence the structure and growth of tree roots (Kozlowski
and Pallardy 2002).
In this study, we consider drought stress as a main driver
of singular importance to ecological change and species
distribution shifts. To this end, we conducted a greenhouse
experiment with seedlings, as the most vulnerable stage in
the tree ontogeny (juvenile stage responses), of four forest-
forming tree species for the temperate climate of Central
Europe, including two conifers, Pinus sylvestris (L.) and
Picea abies ((L.) H. Karst), and two broadleaved deciduous
species, Fagus sylvatica (L.) and Quercus robur (L.). We
investigated how these four species responded to drought
stress and duration at both the physiological and morpho-
logical level. We paid particular attention to chlorophyll flu-
orescence measurements to track changes in photosynthetic
efficiency (photoinhibition) of the selected species under
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1659Trees (2023) 37:1657–1669
1 3
drought stress and the duration of exposure to this stressor
while using tree aboveground growth and root responses to
drought as the morphological indicators of stress. Our focal
species differ in their ecological requirements. In short, P.
sylvestris (PS) is the most widespread Eurasian conifer. It is
an early- successional pioneer tree species, light-demanding,
and xerophyte tree; while, P. abies (PA) is a late-succes-
sional conifer species that is considered drought sensitive
(hygrophyte). Both deciduous species, Q. robur (QR) and
F. sylvatica (FS), are late-successional species. FS is con-
sidered a shade tolerant and mezophytic species, while QR
is less shade tolerant and is considered a water demanding
species (hygrophyte). Although the selected species differ
in their soil moisture requirements, recent studies on spe-
cies distribution models for Central Europe under expected
climate change scenarios consider both conifer species as
‘losers’, while the late-successional broadleaf species QR
and FS are among the ‘winner’ species (Dyderski etal.
2018). Because selection of the best species is critical to the
sustainability of managed forests in a rapidly changing cli-
mate (Saxe etal. 2001), our study contributes to the broader
discussion regarding species drought resistance during the
vulnerable juvenile in the face of climate change.
Materials andmethods
Plant material andexperimental design
Seeds of all four species used in this study were collected
from autochthonous stands in Poland. Seeds of the decidu-
ous tree species were sown in spring 2020 at a local for-
est nursery into 265ml Hiko containers with 28 cavities
(Stuewe and Sons., Inc., USA). In the first year of growth,
the seedlings were grown in a commercial nursery under
operational conditions. The conifer seeds were sown at
the end of April 2021 into 120ml Hiko containers with 40
cavities (Stuewe and Sons., Inc., USA). Each container cav-
ity was filled with a substrate consisting of peat (83–85%)
and perlite (12–15%) deacidified with dolomite (pH = 6.5),
and a slow-release fertilizer was added at 3g l−1 (Osmo-
cote Exact Standard 3–4months N:P:K:Mg 15:9:12:2, with
micronutrients). All containers were transported to the
research greenhouse in May 2021 and maintained in a con-
trolled environment. During germination and in the initial
phase of growth (until June), all seedlings in the containers
were irrigated every day up to field capacity. Volumetric
soil water content (VWC) was maintained at field capacity
(0.25–0.30 m3 m−3). To compare species-specific responses
to treatment, we applied the same irrigation regime for each
species.
Experimental design andtreatment
The experiment was established in the research greenhouse
at the Forest Research Institute, Sękocin Stary, Poland, on
June 28, 2021. All containers were arranged in a full facto-
rial, split-plot design with species (PS, PA, QR, FS) and
treatments: control (well watered) and drought as factors.
The experiment was comprised of a total of 732 seedlings
(Table1). The containers with seedlings were divided into
two groups. One group of seedlings (n = 352) was subjected
to drought by withholding irrigation (the irrigation lines
were closed), while the remaining seedlings (n = 380) were
irrigated, maintaining the volumetric soil water content
at ~ 0.25–0.30 m 3 m−3 for the duration of the experiment,
which ran for over 60days. The soil temperature and volu-
metric water content were monitored using Decagon EM50
data loggers with 5TM soil sensors (Decagon Devices, Pull-
man WA, USA). The mean soil moisture at the beginning of
the experiment was 25.3% and decreased to 0.0% at the end
of the experiment in the drought treatment. The soil moisture
and soil temperature monitoring across experimental treat-
ments and time are presented in Electronic supplementary
material (Fig.1S and Fig.2S). During the study period, con-
tainers were re-randomized within treatments every 10days
to avoid bias in growth conditions and edge effects. Monitor-
ing of height growth and maximum quantum yield of PSII
on selected seedlings was treated as repeat measurements.
Physiological responses ofseedlings todrought—
fluorescence chlorophyll
The maximum quantum yield of PSII (Fv/Fm, where
Fv = Fm−F0 represents variable fluorescence in the dark-
adapted state, Fm represents maximum fluorescence in the
Table 1 Species, seedlot code,
number (No.) of seedlings,
container type, and number
of containers used in the
greenhouse drought experiment
Species Certificate of forest reproductive
material (seedlot code)
No. of
seed-
lings
Container type No. of
contain-
ers
Pinus sylvestris MR/58600/20/PL MR/51864/17/PL 320 Hiko HV120SS (40 cavities) 8
Picea abies MR/18209/08/PL 160 Hiko HV120SS (40 cavities) 4
Fagus sylvatica MR/59570/19/PL 112 Hiko V265 (28 cavities) 4
Quercus robur MR/53589/17/PL 140 Hiko V265 (28 cavitites) 5
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1660 Trees (2023) 37:1657–1669
1 3
dark-adapted state, and F0 represents minimum fluores-
cence in the dark-adapted state (Mena-Petite etal. 2000))
was measured seven times during the experiment at 10-day
intervals beginning on 28 June (Day 1 of the experiment) on
fully watered seedlings. The last measurements were per-
formed on August 30 (~ Day 60 of drought).
Five randomly selected seedlings from each conifer spe-
cies per container and four randomly selected seedlings from
each deciduous species per container, in each treatment
(total 96 seedlings), were permanently marked for repeated
measurements. Fv/Fm measurements were performed on
the uppermost whorl of the conifer seedlings and on the
uppermost expanded leaf of the deciduous seedlings. Prior
to measurement, needles and leaves were placed in a clip and
allowed to adjust to darkness for a minimum of 30min. Min-
imum fluorescence (F0) was measured for the dark-adapted
photosynthetic apparatus, and maximum fluorescence (Fm)
was measured after a 0.7-s saturating light pulse. The maxi-
mum variable fluorescence (Fv = Fm—F0) and the maximum
quantum yield of PSII (Fv/Fm) were calculated automatically.
Chlorophyll a fluorescence was evaluated with the Plant Effi-
ciency Analyser (PEA, Hansatech, Norfolk, UK).
Morphological responses ofseedlings todrought—
height androot architecture
Height was measured three times during the experiment with
a ruler from the surface of the soil to the tip of the shoot.
The first measurement was taken four days before the start
of the experiment (24.06.2021), the second measurement at
31days after the start of the experiment (28.07.2022), and
the last one on the last day of the experiment (30.08.2021).
At the end of the growing season (October), 42 seedlings
were randomly selected and harvested to evaluate the root
system parameters of the drought-stressed and well-watered
seedlings. Immediately after harvest, roots were marked and
kept in a cooler (5°C) prior to being soaked in water sev-
eral times to remove the substrate. Rinse water was poured
through sieves to collect any roots that detached during rins-
ing. The cleaned root systems were wrapped in a paper towel
and placed in foil bags in the 5°C cooler until measurements
were taken.
Root systems were scanned for eight characteristics (total
root length, total root area, average root thickness, root sys-
tem volume, number of root tips, number of root forks, num-
ber of root crossings, and number of thickness classes) in a
container filled with water using an Epson Perfection V800
/ V850 scanner (software version 1.9 V3.93 3.9.3.4) adapted
to work with the WinRHIZO software (Regent Instrument
version 2017a). The scan was performed at a resolution of
600 dpi in 16-bit grayscale which made it possible to clearly
separate the root system from the background. The image
was saved in TIFF format.
Statistical analysis
Fv/Fm was plotted on heat maps as a function of soil VWC
and temperature for each species, using a spline function
for smoothing the data. To evaluate the differences in seed-
ling height (measured three times) and the maximum pho-
tochemical efficiency of PS II (measured seven times), we
used a general linear model for repeated measures. The par-
tial Eta squared (
𝜂2
p
%) was used to describe the effect sizes.
Partial eta squared (
𝜂2
p
%) was expressed in per cent as the
sum of squares of the effect (SSeffect) in relation to the sum
of squares of the effect and the sum of squares of the error
associated with the effect (SSerror) (Lakens 2013).
Contrast analysis was performed to further explore the
dataset which allowed testing the statistical significance
of the predicted detailed differences in specific parts of
the complex experimental system (Stanisz and Tadeusie-
wicz 2007). Contrasts between the drought treatment and
the control were determined separately for each species by
measurement dates. This approach made it possible to follow
when seedlings of a given species in the drought treatment
began to deviate in parameters from the control seedlings.
Specifically, we tested the hypotheses H0: μ1−μ2 = 0 vs H1:
μ1−μ2 ≠ 0; where μ1 represents the mean for a given species
in the well-watered treatment at a specific time point and μ2
represents the mean for the same species in the same time
point in the drought condition, which were verified by the
significance of the contrast vector (L). The required vec-
tor with contrast weights was obtained directly from these
hypotheses: L = [-1 1]. The statistical significance of L was
verified by the F-test and the calculated probability (p-value)
of a value of an F (Haans 2018).
For the eight root traits measured at harvest, multivariate
analysis of variance (MANOVA) was used. This analysis
was followed by ANOVA tests for each root trait separately.
An assessment of experimental effect sizes was performed
using η2. Eta squared (
𝜂2%
) was expressed in per cent as
the sum of squares of the effect (SSeffect) in relation to the
total sum of squares (Lakens 2013). Root traits were also
subjected to contrast analysis with contrasts defined for the
treatments (drought and control) separately for each species.
The null hypothesis was rejected if this probability was less
than or equal to 0.05 for all measured characteristics. All
statistical analyses were performed using the Statistica 13.0
statistical package (TIBCO Software Inc. 2017).
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1661Trees (2023) 37:1657–1669
1 3
Results
Maximum quantum yield ofPS II
The trends in the maximum efficiency of PSII as a func-
tion of soil VWC and temperature were nonlinear and
species specific (Fig.1). The photosynthetic capacity of
PSII was largely dependent on water availability and only
slightly dependent on temperature. With the exception of
QR (Fig.1b), which was sensitive to lower temperatures,
all species exhibited a wide range of thermal optimum for
maximum PSII efficiency. For this reason, temperature was
removed from further analyses.
Seedlings of all species were able to maintain relatively
high Fv/Fm values at optimal temperature, even under severe
Fig. 1 Heat maps showing variation in Fv/Fm as a spline function of
soil volumetric water content (VWC) and temperature for Fagus syl-
vatica (a), Quercus robur (b), Pinus sylvestris (c), and Picea abies
(d). Predicted values of species-specific maximal photosynthetic
capacity of PSII are shown as smooth surfaces representing pooled
Fv/Fm data (for all terms and both treatments). Fv/Fm is scaled to a
color gradient ranging from low (green) to high (red)
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1662 Trees (2023) 37:1657–1669
1 3
water stress (less than 10% VWC). However, the deciduous
and coniferous species showed different behavioral patterns
to cope with water deficit. The deciduous species responded
rapidly with photoinhibition in a very narrow range on the
VWC axis when VWC dropped below 10%. In contrast,
maximum PSII efficiency gradually decreased in PA and
PS under increasing water scarcity (Fig.1).
Leaf Fv/Fm showed significant variation between all main
effects: treatment, species, time, and interaction effects
(Table2). The contrast analysis allowed us to track species-
specific changes in Fv/Fm with drought stress over time. The
contrast analysis showed Fv/Fm decreased significantly in
the drought treatment in QR at Day 20 (p = 0.003) of the
experiment compared to well-watered seedlings. After Day
30, significant differences (drought vs. well watered) were
observed in the efficiency of the PSII in FS (p < 0.001).
PA lost photosynthetic capacity after Day 40 compared to
the well-watered seedlings (p = 0.043), while PS signifi-
cantly decreased its photosynthetic capacity after Day 50
(p = 0.001; Fig. 2). Importantly, when we considered the
detailed results of species-specific VWC status over time, we
found that broadleaved deciduous and coniferous species dif-
fered in terms of their soil water conservation strategy. QR
and FS depleted available water resources to 10% (VWC)
very quickly, in 11 and 18days, respectively; while the coni-
fers, PS and PA, maintained higher VWC (above 10%) over a
longer period, 42 and 47days, respectively (ESM, Fig.1S).
Fig. 2 Maximum photosynthetic efficiency of photosystem II (Fv/Fm)
in seedlings from four tested species: Fagus sylvatica (FS), Quercus
robur (QR), Pinus sylvestris (PS), and Picea abies (PA) over time,
taking into account treatment (drought and control (irrigation)). The
horizontal arrows mark the first measurement date from which sta-
tistically significant contrasts between the Fv/Fm of seedlings in the
control and drought treatments occurred. The semi-transparent red
area for each species denotes the period of severe water stress for the
seedlings and begins on the day when the VWC fell below 10%
Table 2 ANOVA with
repeated measurements for
the maximum photochemical
yield of photosystem II (Fv/
Fm) of seedlings over time
and experimental effects:
species and treatment (control
vs. drought) including sums
of squares (SS), degrees of
freedom (Df), mean squares
(MS), f-value (F), p-value (p),
and
𝜼2
p
%
Effects SS Df MS F p
𝜼2
p
%
Treatment 11.5226 1 11.5226 168.745 < 0.001 42
Species 4.3838 3 1.4613 21.400 < 0.001 65
Treatment×Species 2.9704 3 0.9901 14.500 < 0.001 33
Err 6.0090 88 0.0683
Time 10.2726 6 1.7121 77.903 < 0.001 46
Time×Treatment 8.8276 6 1.4713 66.945 < 0.001 24
Time×Species 3.8534 18 0.2141 9.741 < 0.001 43
Time × Treatment × Species 2.6569 18 0.1476 6.716 < 0.001 18
Err 11.6041 528 0.0220
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1663Trees (2023) 37:1657–1669
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However, when the effect of VWC and sensitivity of PSII
to drought were combined, the species ranking changed con-
siderably (Fig.2). Here, PA was the most sensitive species,
responding to water scarcity with photoinhibition when soil
VWC dropped to 14.5%. The second most sensitive spe-
cies was PS, whose Fv/Fm decreased significantly compared
to well-watered seedlings at a VWC status of 5.5%. The
broadleaved deciduous species showed photoinhibition only
at critically low VWC (below 5% VWC), which was particu-
larly evident in QR (3.7%, Fig.2).
Height
The analysis of variance for repeated measurements revealed
significant differences in height among species, over time,
and in the interaction between time and species. QR had the
highest recorded height, followed by FS, while both coni-
fer species were considerably smaller. The seedlings' height
changed significantly over time, which was related to the
natural elongation process during the active growth phase.
This height variation exhibited species-specific growth pat-
terns. Specifically, the growth of the broadleaved species
plateaued midway through the experiment, while conifer
species exhibited a continuous height increment throughout
the entire study period. However, the species-specific height
growth trajectories remained consistent across both control
and drought treatment groups (Table3; Fig.3).
Responses ofroot traits todrought
Multivariate analysis of variance (MANOVA) for root traits
showed differences in tree responses depending on the treat-
ment (control vs. drought) and tree species. The interaction
between tree species and experimental treatment was also
significant, indicating that specific root responses to drought
were also depend on tree species (Table4).
Results from ANOVA, conducted separately for each
root trait (Table5), showed that species-specific responses
explained the greatest part of the variability in the model
(48–60% of the variability according to the Eta squared coef-
ficients, excluding the number of root thickness classes),
while treatment (control vs. drought) explained another
6–12% of the variability described in the model (Table5).
The interaction between species and treatment was not sig-
nificant for most root traits (except for mean diameter), and
explained the smallest part of the variability in the model
(values of the Eta-Squared coefficients ranged from 4 to 8%).
Results of the contrast analysis delineate that the tree
responses to drought stress, as manifest in root morphologi-
cal traits, can be categorized into species-specific and, on a
broader scale, broadleaved deciduous and coniferous species
groupings (Fig.4). The deciduous species were sensitive to
drought stress, particularly FS, which exhibited reduced root
length, thickness, volume, and surface area under drought
conditions and produced significantly fewer forks, tips, and
crossings than roots of seedlings of this species under the
well-watered control conditions. QR, was the second most
sensitive species to drought. Coniferous species appeared
less sensitive to the concomitant phenomenon of drought,
although the PA seedlings produced significantly fewer root
tips under drought conditions than under well-watered con-
ditions (Fig.4).
Discussion
In this study, we investigated the maximum quantum effi-
ciency of PSII (Fv/Fm), height growth, and root morphol-
ogy during soil drying in four woody species selected as
representative of the major forest-forming tree species in
Central Europe. Our focal species showed different strate-
gies to cope with water limitation, including morphological
and physiological changes. The two deciduous tree species
(FS and QR) were characterized by significantly higher soil
water uptake than the conifer species (PS and PA), which
was related to their faster growth rate in the juvenile stage
as an adaptation strategy to successfully compete with
other trees, shrubs, and herbaceous plants for soil and light
resources in nature. As a result, they quickly consumed the
available water resources in the limited space of the nurs-
ery container, experiencing severe drought soon after the
experiment began. This was particularly evident in QR, the
tallest of the four species investigated (11days in QR and
18days in FS).
Leaf Fv/Fm appeared to be an appropriate and sensitive
probe for the rapid assessment of physiological stress levels
in seedlings (Meng etal. 2016; Zhuang etal. 2020). Fv/
Fm decreased significantly under drought stress, indicating
that PSII was damaged under drought stress and the primary
response of photosynthesis was inhibited, which is consist-
ent with Lichtenthaler and Rinderle (1988), and Meng etal.
(2016). In addition, the leaf Fv/Fm response of seedlings to
drought was species-specific and dependent on drought dura-
tion, indicating differential drought susceptibility among the
species studied.
Overall, the physiological patterns of response differed
between the deciduous and conifer species (Figs.1 and 2).
While both conifers conserved soil water resources over a
longer period of time, and thus maintained higher Fv/Fm val-
ues for a longer time period than the deciduous trees, they
showed greater sensitivity to drought-induced photoinhibi-
tion at relatively higher soil moisture (5–15% VWC) than
the deciduous species. The gradual decline in maximum
quantum efficiency of PSII, in response to decreasing VWC
in both coniferous species (Figs.1c and d) indicated their
sensitivity to soil moisture fluctuations, reflecting their
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1664 Trees (2023) 37:1657–1669
1 3
isohydric water management strategy. This increased sensi-
tivity to water scarcity was particularly striking in PA, which
showed photoinhibition at a VWC of 14.5% (moderate water
stress; Fig.2). In contrast, deciduous tree seedlings depleted
soil water quickly, but reduced Fv/Fm only under the adverse
conditions of severe drought (VWC < 5%; Fig.1a and 1b;
Fig.2), operating within a narrow safety margin, charac-
teristic of anisohydric behavior. This behavior was par-
ticularly pronounced in QR, which showed photoinhibition
at a critically low VWC level of 3.7% (see Fig.2). Méthy
etal. (1996) and Epron and Dreyer (1993) also observed
low sensitivity of Fv/Fm to moderate drought stress in sev-
eral European Quercus species, and Fv/Fm decreased only
under severe water stress (at predawn water potentials below
-4MPa). Accordingly, the rapid soil water consumption of
this species in our study could be attributed to its mainte-
nance of high transpiration, stomatal conductance, and pho-
tosynthesis under moderate drought conditions (Epron and
Dreyer, 1993; Aranda etal. 2000), while photoinhibition
occurred within a narrow safety margin under severe stress.
FS similarly displayed anisohydric behavior, albeit conserv-
ing water slightly longer than QR (Fig.2, Fig S1), implying
a lower water use in this species. The variation in Fv/Fm
values, shifting from optimal conditions (Fv/Fm above 0.8)
to adverse conditions (Fv/Fm close to 0), exhibited a broader
safety margin dependent on VWC in FS compared to QR
(cf. Figures1a and 1b). These results may indicate that FS
exhibits transitional behavior on the anisohydric–isohydric
scale. Indeed, FS is frequently described as aniso- or isohy-
dric, which, as Nguyen etal. (2017) noted, depends on site
Table 3 ANOVA with
repeated measurements for
seedling height over time and
experimental effects: species
and treatment (control vs.
drought)
Effects SS Df MS F p-value
𝜼2
p
%
Treatment 8078 1 8078 0.775 0.379 < 0.1
Species 15347160 3 5115720 490.770 < 0.001 68
Treatment×Species 92319 3 30773 2.952 0.032 1
Error 7015264 673 10424
Time 75539 2 37770 315.480 < 0.001 31
Time×Treatment 153 2 77 0.640 0.527 0
Time×Species 37040 6 6173 51.564 < 0.001 18
Time × Treatment × Species 881 6 147 1.226 0.230 < 0.1
Error 161145 1346 120
Fig. 3 Mean seedling height (± SE) of the four studied species:
Fagus sylvatica (FS), Quercus robur (QR), Pinus sylvestris (PS), and
Picea abies (PA). Statistically significant contrast between the height
of seedlings in the drought vs. control treatments marked by ** at
p ≤ 0.05 for a given measurement date
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1665Trees (2023) 37:1657–1669
1 3
conditions and provenance, thus showing large intraspecific
variation in this species.
Our analysis of height growth measurements revealed
no differences in shoot elongation between treatments,
although a reduction in growth due to a decrease in cell
expansion is typically the first morphological and quantifi-
able effect of drought stress (Kramer 1974; Szyp-Borowska
etal. 2022). The lack of significant differences in height
between irrigated and non-irrigated seedlings may be pri-
marily because our study focused on the effects of summer
drought (July–August). The phenology of FS and QR, indi-
cates that both species typically complete shoot elongation
and bud formation for the following year in June in growing
conditions in Poland (before the start of our experiment)
(Chałupka 1990, 2006). Despite the fact that both FS and
QR are capable of producing proleptic shoots in secondary
growth in July (proleptic shoots typically make up 5% of all
shoots in a given year) (Chałupka 1990, 2006), neither spe-
cies demonstrated this behavior in the current study, even
under the well-watered control treatment. In turn, the seed-
lings of the coniferous species, characterized by a longer
elongation period during the growing season (they usually
complete shoot elongation in July) (Chałupka 1977, 1993),
were able to complete their height growth before drought
conditions came into effect, mainly due to a more conserva-
tive management of water resources. The PS and PA species
did not experience the summer drought until 42 and 47days
after the start of the experiment (August), respectively. Thus,
the absence of summer drought effects on height growth in
all species studied can be explained by the earlier timing of
shoot elongation and bud formation phenology (especially
in FS and QR) and by conservative strategies to cope with
water limitation (especially in PS and PA). These results are
consistent with Taeger etal. (2015) but do not rule out nega-
tive consequences in subsequent years (Thiel etal. 2012).
Contrary to the aboveground growth, the below-ground
root systems of the deciduous seedlings were sensitive
and responsive morphological probes of drought severity.
The deciduous tree species exhibited a sensitive morpho-
logical response to soil drying, indicating that they expe-
rienced severe drought stress. The results of meta-analysis
of several studies have shown that root growth response is
strongly influenced by the severity of stress (Poorter etal.
2012). Plants exposed to a moderate water deficit generally
Table 4 MANOVA for eight root traits depending on species and
experimental treatment (drought vs. control)
Wilk Test F Factor Df Err Df p-value
0.005 16.574 24 78.909 < 0.001
0.528 3.016 8 27.000 0.015
0.079 4.606 24 78.909 < 0.001
Table 5 ANOVA for individual root traits for experimental effects: species and treatment (control vs. drought). η2—the proportion of the total variance explained by the experimental effect
Effect DF Length Surface area Average diameter Root volume Tips Forks Crossings Number of diam-
eter classess
F (p-value) η2 [%] F (p-value) η2 [%] F (p-value) η2 [%] F (p-value) η2 [%] F (p-value) η2 [%] F (p-value) η2 [%] F (p-value) η2 [%] F (p-value) η2 [%]
Species 3 17.516
(< 0.001)
50 24.65
(< 0.001)
56 32.433
(< 0.001)
60 26.012
(< 0.001)
57 16.758
(< 0.001)
48 21.262
(< 0.001)
55 19.854
(< 0.001)
56 1.247
(0.308)
8
Treatment 1 10.578
(0.003)
10 10.058
(0.003)
7 4.753
(0.036)
2 8.555
(0.006)
6 12.92
(0.001)
12 8.648
(0.006)
7 6.822
(0.013)
6 3.332
(0.077)
7
Spe-
cies × Treat-
ment
3 1.855
(0.156)
5 2.556
(0.071)
5 4.548
(0.009)
8 2.615
(0.067)
5 2.087
(0.12)
6 2.447
(0.081)
6 1.518
(0.227)
4 1.247
(0.308)
8
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1666 Trees (2023) 37:1657–1669
1 3
show little change in their growth pattern, with only a small
increase in root biomass relative to total biomass, maintain-
ing aboveground growth and thus their competitiveness for
aboveground resources for as long as possible. In contrast,
plants exposed to severe drought typically increase the pro-
portion of root mass, with a concomitant reduction in stem
growth (Brunner etal. 2015). However, despite an increase
in root-to-shoot ratio during drought, fine root biomass, root
length, and root tip frequency are typically reduced (Brunner
and Godbold 2007; Eldhuset etal. 2013; Zang etal. 2014;
Brunner etal. 2015). These results are consistent with our
observations made on deciduous tree species under drought
stress, particularly in FS, which, based on contrast analy-
sis, significantly reduced root length, volume, area, thick-
ness, root tip frequency, forks, and crossings in the drought
treatment compared with the control. Interestingly, FS was
characterized by a greater or comparable number of cross-
ings, forks, and root tip frequency, traits important for water
uptake, in the control treatment compared to QR, although
the latter species was much taller (aboveground) suggest-
ing that FS might outperform QR in mixed stands under
normal or moderate drought stress conditions. This find-
ing is consistent with previous studies indicating that QR
(and Q. petraea) have a lower competitive ability than FS in
sites with moderate or optimal water and mineral supplies
(Kieliszewska-Rokicka 2006). As opposed to the QR and FS
species, root traits of the conifers were largely insensitive to
soil water scarcity, with only a very weak decrease in root
tip frequency in PA under drought treatment. This result
is probably due to a more conservative use of soil water
resources in the juvenile stage, which allowed the conifers
to maintain a higher VWC value for a longer period during
the growing season, thus avoiding a significant loss in root
trait parameters.
Although we maintained uniform soil conditions in
our experiment, it is crucial to acknowledge that our focal
Fig. 4 Means (± SE) for eight root characteristics measured after the
end of the experiment, showing the contrast analysis between the
drought vs. control morphological traits separately for each species.
Markings: *—significant contrast at the level of p ≤ 0.05, **—signifi-
cant contrast at the level of significance of p < 0.01. Fagus sylvatica
(FS), Quercus robur (QR), Pinus sylvestris (PS), and Picea abies
(PA)
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1667Trees (2023) 37:1657–1669
1 3
species inhabit diverse soils in nature in terms of fertil-
ity and texture. The two deciduous species require deep,
fine-textured soils, while the conifers often grow in sandy,
coarse-textured soils, that are expected to experience greater
hydraulic failure during drought (McDowell etal. 2008).
The depth of the water table also affects plant hydraulics
by limiting or allowing plant water uptake during drought
periods (Dawson 1996; Franks etal. 2007). To compensate
for coarse-textured soils, or inaccessible water tables, trees
can increase their soil root or rhizosphere conductance by
adjusting their fine root density (Ewers etal. 2000; Hacke
etal. 2000), fine root hydraulic conductance (McElrone etal.
2007), root depth, and other root characteristics (Stirzaker
and Passioura 1996). However, our results suggest that this
adjustment may occur under moderate drought stress rather
than severe drought, while it remains unclear, to what extent
root characteristics may change depending on soil properties
and water table depth in nature.
Conclusions
In conclusion, our study highlights distinctly different
soil water use strategies and trade-offs during the juvenile
growth stage of our four focal species. Conifers adopted
a water-conserving strategy, while the deciduous species
employed efficient water usage for photosynthesis and
growth, resulting in more rapid soil water depletion. These
responses also reflect different drought tolerance and avoid-
ance behaviors. The two deciduous tree species (FS and
QR) exhibited similar anisohydric responses to drought
stress, indicating a degree of drought tolerance. In con-
trast, ecologically differentiated conifers such as PS and PA
demonstrated isohydric behavior in response to water scar-
city during their juvenile growth phase, indicating a water
stress avoidance strategy. It is worth noting that species
responses to drought and its duration were more nuanced
than these general water management strategies suggest.
Although PA and PS exhibited similar patterns of water
management, photoinhibition in these species occurred at
very different VWC levels, 14.5% and 5.5%, respectively,
demonstrating a wide range of species-specific responses
to water scarcity.
Considering water stress tolerance, the anisohydric decid-
uous tree species seem to be better candidates for forest man-
agement under climate change. On the other hand, PS with
its water-conserving management and relatively low thresh-
old for photoinhibition response (5.5% VWC), in addition to
its minimal morphological responses to drought stress dur-
ing the juvenile stage, promises to be a good alternative for
successful regeneration in drought-prone forest areas under
future climate conditions. However, it is unclear to what
extent the current results on container nursery seedlings can
be extrapolated to older growth stages and growth under
natural conditions. Thus, further research is needed to fill
these knowledge gaps.
In addition to photochemical responses to drought,
which have been shown to be accurate indicators of physi-
ological changes, we also observed distinct morphological
responses to water scarcity in the species studied, particu-
larly in root characteristics, suggesting that broadleaved
species are more sensitive. Nevertheless, our study does
not provide insight into the extent to which our focal spe-
cies can make site-specific adaptations (e.g., root archi-
tecture) or whether they alter their behavioral patterns to
adjust to different site conditions, which seems plausible
given the large intraspecific variation reported among spe-
cies. Consequently, the insights gained in this study con-
tribute to an increase in our understanding of species-spe-
cific responses to drought stress. The results also provide
a solid foundation for further studies that consider these
nuanced strategies and responses in a broader ecological
context, aiming to improve forest management approaches
under changing environmental conditions.
Supplementary Information The online version contains supplemen-
tary material available at https:// doi. org/ 10. 1007/ s00468- 023- 02450-0.
Acknowledgements We wish to express our gratitude to Iwona Szyp-
Borowska, Danuta Garbień-Pieniążkiewicz, Tomasz Wojda and Szy-
mon Krajewski (Department of Silviculture and Forest Tree Genetics,
Forest Research Institute, Poland) for their contributions to data col-
lection in the greenhouse of the Forest Research Institute.
Author contributions Conceptualization: MN; Formal analysis: MN;
Funding acquisition: MN; Investigation: MN and SJ; Methodology:
MN; Writing—original draft preparation: MN; Review and editing:
MN and BRT. All authors have read and agreed to the published ver-
sion of the manuscript.
Funding This research was funded by the State Forests National Forest
Holding (Poland), grant number 500468 (acquisition Marzena Niem-
czyk). This manuscript was developed under a scholarship grant to
Marzena Niemczyk within a Scholarship Fund of the Forest Research
Institute, pursuant to the decision of the Head of the Institute dated
14 April 2022 (based on an agreement concluded on 14 April 2022).
Data availability The datasets generated and/or analyzed during the
current study can be available on request.
Declarations
Conflict of interest The authors declare that they have no conflict of
interest.
Open Access This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
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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1668 Trees (2023) 37:1657–1669
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the article’s Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
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