Drought-induced shift in tree response to climate in floodplain forests of Southeastern Europe

Abstract

Floodplain forests are the most rapidly disappearing ecosystem in the world, especially in temperate regions of Europe where anthropogenic influence has been pronounced throughout history. Research on primeval forests is crucial to further our understanding of their natural dynamics and interaction with climate but is limited by the lack of such preserved forests. The aim of this study was to investigate how a primeval floodplain forest in Southeastern Europe has responded to climate variability during the last 250 years through comparison of tree growth and climate, canopy disturbance and recruitment dynamic of two dominant tree species with different tolerances to flooding/drought. Our analysis revealed induced stress caused by several consecutive severe drought events in the 1940s, which led to a significant increase in sensitivity to increasing temperatures and decreasing river water levels. This trend is particularly pronounced in pedunculate oak. Age structure analysis revealed one larger episode of oak regeneration culminating after periods of intense growth release. Such period co-occurs with summer drought, which is part of a complex system of natural disturbances and a significant natural driver of the cyclical regeneration of primeval oak ecosystems.

Full text

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SCientiFiC REPORTS | (2018) 8:16495 | DOI:10.1038/s41598-018-34875-w
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Drought-induced shift in tree
response to climate in oodplain
forests of Southeastern Europe
Stjepan Mikac
1,2, Anja Žmegač1,2, Domagoj Trlin1, Vinko Paulić1, Milan Oršanić1 &
Igor Anić1,3
Floodplain forests are the most rapidly disappearing ecosystem in the world, especially in temperate
regions of Europe where anthropogenic inuence has been pronounced throughout history. Research
on primeval forests is crucial to further our understanding of their natural dynamics and interaction
with climate but is limited by the lack of such preserved forests. The aim of this study was to investigate
how a primeval oodplain forest in Southeastern Europe has responded to climate variability during
the last 250 years through comparison of tree growth and climate, canopy disturbance and recruitment
dynamic of two dominant tree species with dierent tolerances to ooding/drought. Our analysis
revealed induced stress caused by several consecutive severe drought events in the 1940s, which led to
a signicant increase in sensitivity to increasing temperatures and decreasing river water levels. This
trend is particularly pronounced in pedunculate oak. Age structure analysis revealed one larger episode
of oak regeneration culminating after periods of intense growth release. Such period co-occurs with
summer drought, which is part of a complex system of natural disturbances and a signicant natural
driver of the cyclical regeneration of primeval oak ecosystems.
Global forest decline caused by drought has been recorded worldwide and has signicantly increased since
19701,2. Recent changes in climate are associated with increased temperatures and changes in precipitation pat-
terns, with more frequent, prolonged and intense episodes of drought as a consequence. Such events result in
long-lasting changes in ecosystem function, community composition and structure, especially in water sensitive
ecosystems such as oodplain forests3. Lowland oodplain forest ecosystems are characterized by high produc-
tivity, diverse microhabitat conditions and considerable biodiversity4. ey are widespread in all biogeographic
regions of the world on alluvial deposits of large rivers with which they have a constant hydrologic interaction5.
According to a study by Tockner et al. in 20026, the world’s remaining oodplain forests cover an area of approx-
imately 2.24 × 106 km2.
e continuous expansion of settlements and infrastructure, as well as exploitation of natural resources, has
ultimately resulted in the widespread disappearance of primeval lowland oodplain ecosystems7,8. In Europe, nat-
ural lowland oodplain forests have all but vanished, and with them, a very important research reference point for
forestry and ecology. In the last century deforestation due to agriculture has wiped out 90% of Europe’s oodplain
forests9,10. e remnants of relatively natural forest occur mostly in Eastern and Southeastern Europe3,11. Apart from
deforestation, oodplain forests have been impacted by numerous activities, particularly river regulation (con-
struction of dams, dykes, drainage systems, etc.). ese interventions have disrupted the sensitive ood patterns
and assisted the progression of mesohydric species12–14. Regional episode of pedunculate oak (Quercus robur L.)
decline were recorded during the 20th century in oodplain forests in almost all of Europe15. As oak and other
species die out, another problem in lowland oodplain ecosystems is the spread of mesohydric species, such as
hornbeam (Carpinus betulus L.), which are becoming increasingly dominant, especially in drier, oak dominated
habitats. In the last 20 years signicant decline in narrow-leaved ash (Fraxinus angustifolia Vahl) was observed
through the whole landscape. e greatest threat to the stability of forest ecosystems of narrow-leaved ash is cur-
rently posed by the phytopathogen Hymenoscyphus fraxineus T. Kowalski16 but also constant increase of temper-
ature and environment dryness. e continuation of oak and ash decline could have long-lasting consequences
1University of Zagreb, Faculty of Forestry, Department of Forest Ecology and Silviculture, Svetošimunska 25, 10002,
Zagreb, Croatia. 2University of Zagreb, Faculty of Forestry, Croatian Dendroecology Laboratory, Svetošimunska
25, 10002, Zagreb, Croatia. 3Croatian Academy of Sciences and Arts, Zrinski trg 11, 10000, Zagreb, Croatia.
Correspondence and requests for materials should be addressed to S.M. (email: smikac@sumfak.hr)
Received: 25 July 2018
Accepted: 28 October 2018
Published: xx xx xxxx
OPEN
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for biodiversity as well as for the European forestry sector and is a huge challenge for nature conservation. Forest
management in Europe strives to implement a close-to-nature approach based on mimicking natural stand
dynamics17. In order to better understand the dynamics of natural lowland oodplain forests and their interaction
with climate, primeval natural ecosystems need to be studied. However, such studies are lacking in Europe since
it is almost impossible to nd a primeval lowland oodplain area with an exclusively natural composition and
structure. erefore, we carried out this study in an area with one of the best preserved oodplain forest complex
of pedunculate oak and narrow-leaved ash in Europe – Lonjsko Polje Nature park (LPNP)13.
e aims of this study were to: (1) analyze the long-term growth sensitivity of oak and ash to climate variabil-
ity and changes in river water regime; (2) determine if climate is the driver of growth releases in the study area;
(3) reconstruct disturbance history through analysis of the relationship between canopy disturbance, tree growth
and recruitment.
We expect that: (1) oak growing on drier sites is more sensitive to precipitation, PDSI and river water regime
than ash; (2) extreme climatic events drive the growth releases and the establishment of recruitment in these
forests.
Materials and Methods
Research area. e oodplain forests in the lowland part of Croatia occupy an area of about 1,980 km2,
mainly along the Sava, Drava and Danube rivers. One of the best preserved natural oodplain regions in Europe
is the Sava River basin, with an area of 97,713 km2. Geographically, it lies between 13.67E–20.58E longitude
and 42.43N–46.52N latitude. It represents 12% of the Danube River basin, making it the second largest Danube
sub-basin. Its preserved naturalness is the result of historical circumstances. Up to the 19th century the Sava River
was a natural barrier between the Austro-Hungarian and the Ottoman empires. In that period, the forests were
under strict control of the military authorities and were protected. e largest and best preserved oodplains and
forest ecosystems in Europe can be found in the central part of the Sava River basin and make up what is called
“e Blue Heart of Europe” (Lonjsko polje Nature Park, LPNP). e area of approximately 511 km2 hosts a mosaic
of preserved wild lowland oodplain forests and alluvial swamps. e dominant tree species are narrow-leaved
ash (Fraxinus angustifolia Vahl) and pedunculate oak (Quercus robur L.). Ash is found on wet and heavy gley soil
and forms the swamp (“wet”) forest edge which is regularly ooded during the year (spring & autumn), while oak
is found on drier terrain, oen out of the reach of regular annual oods, and it represents the upper (“dry”) edge
of these forests. Oak is the main indicator of mesophilic conditions, but common hornbeam (Carpinus betulus L.)
also occurs and is becoming progressively more dominant in oodplain ecosystems. is kind of mosaic alter-
nates throughout the entire area regardless of the distance from the riverbed due to the specic micro-terrain
(micro-rises and micro-depressions) caused by the settling of alluvial deposits.
is study was conducted on the eastern edges of the LPNP area, which is under the direct inuence of ood-
ing from the Sava River and its tributaries. e area is characterized by a humid continental climate, with an aver-
age annual air temperature of 9.5 °C and total precipitation of 870 mm with a maximum in June and a minimum
in February. Evaporation is estimated in the range of 520–600 mm per year. For the study, two areas (Fig.1a,b)
were chosen as representative of extremely wet habitats (swamp edge) and extremely dry habitats. e areas were
required to be (i) absent of direct anthropogenic inuence (cutting, grazing etc.), (ii) representative of marginal
populations with respect to the wetness of the habitat, (iii) exposed to the same climate conditions (precipitation
and temperature) and (iv) similarly distant from the Sava riverbed. e rst area is a mixed stand of pedunculate
oak and common hornbeam in the Prašnik Forest Reserve (dry site, elevation = 95 m, distance to river = 3,2 km)
and the second is a pure narrow-leaved ash stand that forms the border between the forest and permanent wet-
lands (wet site, elevation = 90.5 m, distance to river = 2,9 km). Prašnik, with an area of 50 ha, is the last representa-
tive example of the primeval lowland forests that encompassed approximately 400 km2 of the research area before
World War I. e wood volume is approximately 550 m3 ha−1 with 24 trees ha−1. Pedunculate oak trees reach
impressive dimensions of up to 260 cm in diameter and 45 m in height. A dramatic change in species composition
has been observed in the last ve decades, with common hornbeam having progressed to the point where it is cur-
rently dominating the understory. e second site consists of pure stands of narrow-leaved ash that grow on the
boundaries of constantly wet alluvial swamps. e wood volume is approximately 320 m3 ha−1 with 160 trees ha−1.
ese narrow-leaved ash stands most probably arose by natural succession during the last 200 years. is was
inferred by studying historical maps from the late 18th century (http://mapire.eu/en/).
Field sampling. In Prašnik (dry site) we established a grid of 10 circular experimental plots, each amounting
to 2500 m2 that were evenly spread through the whole reserve area. Within each plot we positioned and sampled
all trees and dead wood with a diameter over 10 cm (Supplementary Fig.1). At the swamp boundary (wet site)
we established three experimental plots, each amounting to 800 m2, where all of the ash trees were sampled. Two
cores per tree were collected with a Pressler borer at approximately 1.30 m above ground level18. Aer collection,
preparation and drying of the samples, we carried out standard coarse and ne sample processing, incrementally
increasing the sandpaper granulation (granulation of 120 to 600).
Climate data. Climate data (mean monthly air temperature, precipitation and standardized Palmer drought
index – scPDSI) were obtained from the gridded CRU TS3.24.01 database (Fig.2) with a spatial resolution of
0.5° × 0.5° for the 1901–2015 period using the KNMI Climate Explorer platform19 (http://climexp.knmi.nl). For
the long-term climate correlations (>100 years), analysis was done using data (mean monthly temperature and
monthly precipitation sums) from the HISTALP database (http://www.zamg.ac.at/histalp/). e database contains
monthly homogenized precipitation data from 192 weather stations and homogenized air temperature data from
131 weather stations in the broader Alps and Dinarides area (4° to 19°E latitude and 43° to 46°N longitude)20.
We used grid-mode-2 series that represent absolute monthly air temperature and precipitation values in a
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5 × 5 minute resolution (4° to 19°E latitude and 43° to 46°N longitude). Hydrological parameters (mean monthly
water level and river discharge values) for the Sava River in the 1926–2014 period were obtained from the
Croatian Meteorological and Hydrological Service (http://meteo.hr/). e distance between dry site, wet site and
nearest river gauges were 12 km and 7 km, respectively.
Chronology development. Tree-ring width was measured with a LINTAB measuring table with 0.01 mm
precision, equipped with OLYMPUS binoculars and a polarized light source. Cross-dating of samples was done
both visually and using the TSAP-Win™ dendrochronological soware (http://www.rinntech.de). Cross-dating
quality was veried using COFECHA program21,22 by checking the consistency of ring width series among trees
from the same site. We averaged two cores for each tree, thereby obtaining one representative series per tree
(Supplementary Fig.2). For each core cambial age was estimated using concentric circles method. Pith estimates
of 10 missing rings or more were not included in the age data set.
Detrending, that is, removing frequency variability as a consequence of the biological age eect as well as
standardization was done on individual tree-ring width series using the “dplR” package in R23. Several methods
(Negative exponential curve, Regional curve standardization - RCS, Signal-Free RCS - RCSsf, C-method, Spline)
were used (Supplementary Fig.3). Following standardization, individual series were calculated using Tukey’s
biweight robust mean24 to obtain a residual chronology25 (Tree-ring width index - TRWI) which was used in all
subsequent analyses (Fig.3). Since the correlation to climate of chronologies obtained through the mentioned
methods showed almost no dierence (Supplementary Fig.4), the Spline method (frequency response of 0.50 cut
o at 0.67 series length) was chosen.
e quality of the obtained chronology was assessed by using several dendrochronological statistics: mean
sensitivity (MS), which is a measure of year-to-year variability in the tree growth series26 calculated as the dier-
ence between each two successive rings divided by their mean27; rst-order autocorrelation of raw data (AC1),
which determines the variance of the current year’s growth that is explained by the previous year’s growth28; the
expressed population signal (EPS), used to assess chronology reliability where EPS value over 0.85 quanties the
degree to which the constructed chronology represent the hypothetical population29 and mean interseries corre-
lation (Rbar) (Supplementary Table.1).
Climate-growth analysis. Climate–growth relationships were assessed by correlation function as well as
response function analysis. In correlation functions, the coecients calculated between the tree-ring chronology
and monthly climatic variables are univariate estimates of Pearson’s product moment correlation. In response
functions, the coecients are obtained through multiple regression using the principal components of monthly
climatic data to estimate ring-width growth indices. ey are interpreted as average eect of the uctuation of
that monthly climatic variables on tree growth. is regression model is used in tree-ring studies to identify
Figure 1. Location of the study sites. Photographs of oak (dry, Site 1) and ash (wet, Site 2) sampled stands
(a). Positions of sampling areas (black square), the location of the hydrologic water level monitoring station
(white dots) and natural, regularly ooded area (shaded polygon) (b).
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the climate origin of variability in the chronologies through avoidance of intercorrelations between climatic
predictors26.
Analysis was performed with the “treeclim” package in R30 for a period of 16 months (June of the previous
year to September of the current year) between climate and hydrologic data and residual chronology (Fig.4).
e signicance (p-value < 0.05) of each coecient was evaluated using 1000 bootstrap replications mimicking
DENDROCLIM2002 soware31. Analysis was performed for the period of 1950–2014 (determined by the greatest
frequency and quality of meteorological data). Seasonal correlation analysis was done using “treeclim” package30
for a 95% signicance level for dierent season durations from 2 to 6 months in monthly increments. In the
results we show seasonal durations for 2 and 4 months (Fig.4).
Temporal stability of Climate-growth relations. Temporal stability of the climate signal was ana-
lyzed using moving window correlations with a 30-year interval (Fig.5). Analysis was performed with the most
6
8
10
12
Temperature (°C)
50
100
150
Precipitation (mm)
0 500 1000250 Km.
Legend
Sava River
Sava Catchment
R0.70
-0.58
(b)
0 500 1000250 Km.
(a)
Legend
Sava River
Sava Catchment
R0.29
-0.83
−5
0
5
scPDSI
Years
1920 1940 1960 1980 2000
0
200
400
600
River Water Level (cm)
Max.
Min.
86.82 m a.s.l.
−1 −0.8 −0.6 −0.4 −0.20 0.20.4 0.60.8
1
JANt
FEBt
MARt
APRt
MAYt
JUNt
JULt
AUGt
SEPt
OCTt
NOVt
DECt
JANt
FEBt
MARt
APRt
MAYt
JUNt
JULt
AUGt
SEPt
OCTt
NOVt
DECt
JANp
FEBp
MARp
APRp
MAYp
JUNp
JULp
AUGp
SEPp
OCTp
NOVp
DECp
I
II
III
IV
V
VI
VII
VIII
IX
X
XI
XII
S=2082, Z=5.0305, P<0.001
S=-419, Z=1.0104, P=0.3123
S=-962, Z=2.3229, P=0.0202
S=-1163, Z=4.118, P<0.001
(c)
Correlation
Figure 2. Long-term trend of mean annual climate data (Temperature, Precipitation, scPDSI) and River Water
Level. Spatial eld correlation between the mean 12-monthly Sava River Water level with E-OBS 14.0 current
year Tmax (averaged May–August) (a) and gridded precipitation (b) for the period 1950–2014. e correlation
matrix between average monthly water levels (I–XII), temperature (t) and precipitation (p) for the period
1926–2014 (c).
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signicant monthly and seasonal variables for the 1901–2014 period using CRU TS3.24.01 climate data, with
additional analysis of pedunculate oak correlations for a longer period (1800–2014) using HISTALP climate data
(Fig.5e).
Disturbance analysis. We collected documented and archived records of salvage logging (drought induced)
and disturbances for the entire lowland region in Croatia for the past century. We extracted information on the
agent of past disturbances and quantity of salvaged wood (m3 ha−1) (Fig.6).
is data provides information from a large area giving us a useful insight into past disturbance regimes and
general trends in decline, but it should be kept in mind that it is obtained from managed and seminatural forest
which can dier in their resistance to disturbances32.
For disturbance analysis in our study, series from trees older than 150 years were used (80 trees). For each tree,
the percentage change in growth was calculated according to the method proposed by Nowacki and Abrams33.
is method uses a percent growth change equation:
=− ∗%GC ((M2M1)/M1)) 100,
where % GC is percent growth change from preceding to superseding 10-yr radial average, M1 is the preceding
10-yr mean radial growth (exclusive of the current year) and M2 is the superseding 10-yr mean radial growth
(inclusive of the current year). e minimum threshold for release is 25% growth change for moderate and >50%
for major release. e percentage of trees showing releases was plotted against time (Fig.7).
Results
River water level. e analysis of monthly water level data showed a signicant decrease in the Sava River
water level from 1926 to 2014, with the decrease being especially pronounced aer 1980 (Fig.2). is is caused
mostly by recent increases in temperature, especially in the summer period from May to August (r = −0.79,
p-value < 0.001). Individual monthly and average seasonal air temperature and river water level correlations in
July and August exhibit the largest values (R = −0.72, p-value < 0.001) (Fig.2.). Total annual precipitation for the
LPNP area is 870 mm. Of this amount, 450 mm occurs in the vegetation period (May to September), nearly the
total amount of actual evapotranspiration. e total variability of the water level explained through the negative
inuence of summer air temperatures (May–August) and the positive inuence of precipitation (April–August)
is 68% (p-value < 0.001).
Tree-ring statistics. For the climate-growth analysis a total of 215 samples of pedunculate oak and 85 sam-
ples of narrow-leaved ash were dated. Since some of the oak samples were in very poor condition upon extraction,
with visible rot and variable wood consistency, only 208 samples of oak were used for the climate-growth anal-
ysis (Supplementary Fig.2d). In some cases, the oak tree dimensions exceed 2 m in diameter, making sampling
particularly dicult. Bearing in mind that this area is protected, we limited the size of the sample to the smallest
possible. e chronology range is 1732–2017 for oak and 1885–2015 for ash. e oldest cambial age of oak is 285
Figure 3. Residual tree-ring index chronologies smoothed with 10 years low pass lter to highlight decadal
high-frequency variability (violet and red). Running EPS and running Rbt statistics (Inter trees correlation) for
Fraxinus angustifolia (a) and Quercus robur (b). EPS and Rbt was calculated using a 50-year moving window.
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years old, while the oldest ash is 130 years old. Two generations of oak were observed (young <100 years cambial
age, old >100 years cambial age) and separated in further analysis (Supplementary Fig.2c,d).
A high autocorrelation of raw series was found in old pedunculate oak (0.74) in comparison to ash (0.45),
which points to the signicant accumulated inuence of climate conditions in the previous years. Comparison of
standardized chronologies shows that narrow-leaved ash has higher mean sensitivity than old pedunculate oak
(MSAsh = 0.36 vs MSOak_O = 0.21). e interseries correlation (Rbar) is also higher for narrow-leaved ash (0.51)
than for pedunculate oak (0.36). EPS value > 0.85 quanties the degree to which the constructed chronology
represents the hypothetical population (EPSAsh from 1897, EPSOak from 1760).
Climate-growth correlations. Simple linear correlation between residual chronologies of tree ring width
index (TRWI) for ash and oak and monthly climate data showed that narrow-leaved ash was signicantly more
sensitive to the hydrologic component, especially precipitation, than pedunculate oak. A statistically positive
correlation (p-value < 0.05) was determined for precipitation (Prec), river water level (R), river discharge (Q) and
drought index (scPDSI) in individual monthly as well as individual seasonal values for 2- and 4-months intervals
in the 1950–2014 period (Fig.4).
e highest positive correlations were found for river discharge (r = 0.61) and water level (r = 0.52) in May of
the current year as well as seasonal correlations from May to August (rQ = 0.68, rR = 0.52). Precipitation in April
Figure 4. Bootstrapped mean monthly and seasonal correlation between TRWI and climate. F. angustifolia
(blue) and Q. robur (old – red, young - gray) for selected climate factors (Temperature, Precipitation and
scPDSI) and hydrological parameters (Sava River water level and river discharge) for the 1950–2015 period.
Statistically signicant values are marked with a dot (p-value < 0.05) and signicant response coecient with a
black bordered dot. Shaded area highlights the correlation values with months of previous year.
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and July showed a signicant positive correlation (r = 0.38). Highest correlation values were found from April to
July (r = 0.63) for the seasonal values.
Signicant positive correlations between the residual chronology and the drought index (scPDSI) for the
individual month values were determined from February to September of the current year with the highest value
in August (r = 0.61). Due to the high autocorrelation structure of scPDSI monthly values, a response function
analysis that reduces individual month intercorrelation was performed. e results point to a signicant positive
sensitivity of ash to scPDSI values in July of the current year (Fig.4). e seasonal values show the highest corre-
lation from June to September (r = 0.60). Negative correlations for temperature were determined for individual
months in May and June (r = −0.28) and for the seasonal values from May to June (r = −0.35).
Unlike narrow-leaved ash, radial growth in old pedunculate oaks showed signicant sensitivity to scPDSI
and temperature. Positive correlations with scPDSI were determined in July of the current year (r = 0.45). In the
period from June to July, a peak in positive impact of scPDSI was recorded (r = 0.43). In contrast, a signicant
negative air temperature impact was determined for April (r = −0.35) and July (r = −0.39). e negative temper-
ature impact becomes more pronounced looking at the seasonal values from April to July (r = −0.43).
Inuence of the precipitation on radial growth is low but statistically signicant. e highest value was deter-
mined in February of the current year (r = 0.26) and for seasonal values from February to May (r = 0.35). e
same pattern was also observed for river discharge and water level. Both show the highest correlation values for
individual months in May (rQ = 0.31, rR = 0.33) and for the seasonal values from April to July (rQ = 0.35, rR = 0.35)
Young oak trees showed lower climate sensitivity than old oaks, with the most signicant positive correla-
tion for temperature in June of previous year (r = 0.39) and for precipitation in June of current year (r = 0.27)
(Fig.4). We also found signicant raw ring width decrease during drought events in the juvenile growth phase
(Supplementary Fig.5). Interestingly, in 2003 the driest year recorded did not aect the growth rate.
Figure 5. Moving correlation between TRWI and most signicant monthly (a,b) and average seasonal climate
factors from CRU TS4. 01 and HISTALP and hydrological data (river water level - RIVER, and river discharge - Q)
(c,d) using 30 years moving window for F. angustifolia and Q. robur for the period 1901–2014 and longer
(1801–2014) period (e).
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e results indicate signicant dierence in climate response between both species. Narrow-leaved ash exhib-
its a more stable signal for the studied period in comparison to oak. e correlation with the precipitation average
for April–July showed a quite stable signal during the studied period. However, on the individual monthly level
(May), signicant increase in correlation with precipitation, river water level and river discharge were observed
(Fig.5a,c). Sensitivity to precipitation in April and May became more pronounced aer 1950. A noticeable
increase in response to the Sava River water level and river discharge in May was determined aer the 1970s, and
reciprocally there was an increase in the negative signal air temperature values in May (Fig.5a).
Oak had a negative but not statistically signicant signal for temperature until the 1950s, aer which the signal
becomes statistically signicant, especially for April and July (Fig.5b,d). At the same time, there were increases
in the positive response to the precipitation, Sava River water level and river discharge in April, May and July.
is pattern was also observed for the 1801–2014 period using HISTALP climate data. e negative tempera-
ture impact was present during the entire studied period, with an increasing trend that becomes especially pro-
nounced aer 1950 for all months between April and July as well as the seasonal average (April–July) (Fig.5e).
Historical evidence of disturbances and salvage logging data. According to the collected historical
records for the period 1900–2010, 7.8 million m3 of dead oak trees have been salvaged. e rst large dieback
occurred from 1910–1925 (1.73 million m3) with three pronounced peaks in 1911, 1916 and 1924. From the
1950s until 1990s salvaging was low compared to the whole period. Still, two large individual events that were
preceded by long-lasting oods (1965 and 1985) occurred in that period.
Aer the 1990s there is evidence of noticeable increase in salvage logging. During the last twenty years total
salvage logging because of individual tree mortality was signicantly higher than all the salvaged wood from the
disturbance events put together. An increase in windthrow events has also been recorded (430153 m3 in the last
two decades) as well as an increase in mortality for ash from 2010 onwards (Fig.6).
e natural disturbance chronology analysis determined four pronounced periods of growth release in the
pedunculate oak primeval forest (1780s, 1850s, 1890s and 1940s). Decadal peaks were determined for the fol-
lowing years: (I) 1788, (II) 1855, (III and IV) 1891 and 1893, and (V and VI) 1942, 1946 and 1950 (Fig.7f). With
narrow-leaved ash, three decades of growth release were determined (1940s, 1960s and 1980s), with peaks in
1946, 1950, 1966 and 1983 (Fig.7h). ese disturbance chronologies show a co-occurrence of growth release with
summer droughts (Fig.7a), high temperatures (Fig.7b), low water level (Fig.7c) and precipitation decit (Fig.7d)
equally in both species. Co-occurrence of peaks in the chronology for both species was found during the 1940s
when a series of dry years was recorded.
e successional response to natural disturbances in the form of cyclical regeneration was observed only once
in the primeval oak forest, but not in ash stands. Oak age structure analysis showed one large period of recruit-
ment that corresponded to the period of intense growth release in the 1940s (Fig.7e). is age structure partially
explains the sigmoidal shape of the diameter frequency distribution characteristic of primeval forests in the tem-
perate zone. Apart from oak, the primeval forest reserve was found to have a signicant distribution of common
Figure 6. Salvage logging data for the lowland area of Croatia. Black histograms represent sum of drought
induced annual salvage logging of oak (a) and ash (b) and windthrow (blue) with individual high-severity
disturbance events (red). NA- data not available for this period.
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hornbeam with an average age of 45 years (20 cm in diameter). Its abundant occurrence coincides with the 1970s,
that is, approximately 20 years aer the recorded period of oak growth release.
Discussion
Numerous studies in Europe suggest that high precipitation values and lower temperatures in the spring and
summer increase the radial growth of pedunculate oak34–42.
e results of our research indicate that old oak trees are positively sensitive to scPDSI and hydrological
parameters and at the same time limited by high air temperatures from April to July, whereas the role of precip-
itation is not as pronounced as that found in the above-mentioned research. Oak’s positive sensitivity to river
water level & discharge in May could be attributed to more intensive new root hairs (<1 mm in diameter) growth
during June and their abrupt dying in the surface layer of the soil during July and at the start of August43,44. Similar
Figure 7. Disturbances chronology and climate variability. PDSI reconstruction for summer (June–August)
droughts severity (Cook et al., 2015) (a). Mean temperature dierence from April to July (b, most severe
droughts marked with plus signs). Mean Sava river water level from May to August (c). Dierence in
precipitation and potential evapotranspiration (PET) for the period (April–July) calculated using long-term
climate data series received from the HISTALP database for sum for the last two years (d). Recruitment of oak
and hornbeam (e) and ash (g) based on cambial age. Disturbance chronology with moderate (black) and major
releases (red bar) displayed in annual interval for pedunculate oak (f) and narrow-leaved ash (h).
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climate sensitivity was not observed for younger trees (<100 years), which we attribute to high interspecies com-
petition (mainly with hornbeam).
In old oaks (older than 150 years) climate sensitivity is not stable over the analyzed period. e negative
response to temperature (April–July) has become signicantly pronounced in roughly the last seven decades
(Figs5 and 6), while at the same time the positive response to precipitation and hydrological parameters has been
growing. is kind of change in oak’s response can be explained by extraordinary warm and drought years in the
1940s. (Fig.2). Similar temporal instability was observed in central-west Germany where oaks changed from a
precipitation to temperature sensitivity aer a severe drought in the 1940s38.
Unlike oak, ash exhibited a more pronounced sensitivity, especially to precipitation (April, May and July) and
to river water level (May and August) while high temperatures in May and June reduced the radial growth. e
aforementioned climatic signal in ash has been conrmed in rare researches in Europe45,46.
We attribute this pronounced precipitation signal to the extreme conditions of ash distribution in relation to
oak. Ash occurs on heavy clay soil at the edge of alluvial swamps, which is also lower, concave terrain that retains
rainfall longer and consequently increases the possibility of greater soil inltration47. In such extreme conditions
ash develops a specic shallow root system exposed to seasonal oscillations of extremely wet (spring, autumn)
and dry periods (summer). Like other oodplain species, it is well adjusted to high levels of groundwater and
limited by humidity shortage during drought periods48. Ash has a high tolerance for such extreme conditions,
and it has no competition from any other tree species, which gives it the opportunity to dominate at the edges of
wet lowland swamps49,50.
Climate sensitivity of ash is stable for seasonal correlations over the analyzed period but for monthly correla-
tions (May) there is a constant increase of sensitivity to all variables especially hydrological parameters (Fig.5a).
We explain this through increasing temperature and decreasing in moisture (decrease in river water level - declin-
ing trend −2.24 cm*year−1 in May for the 1926–2014 period).
The natural dynamics and structure of lowland floodplain primeval forests is hard to reconstruct due
to the lack of preserved reserves in Europe, most of them are deforested during the end of the 19th century
(Supplementary Fig.6). According to historical data four severe individual events were evident during the past
century (Fig.6). Such events occurred on 5.5% of the whole lowland area. Intensity of this recorded events was
from 46–139 m3 ha−1 (mean 70 m3 ha−1). e most severe dieback was in 1985 with intensity of 139 m3 ha−1.
e main cause for such events was a combination of drought follow by oods of long duration. We also found
an increase of windthrow events especially during last past decades which can be attributed to the dierence in
resistance to natural disturbances of managed and semi-natural forests in contrast to primeval ones32. In our
research three pronounced periods of growth release correspond to droughts. Age structure of these forests shows
only two generations of oak trees revealing the severe drought of 1940s as the only drought that triggered a regen-
eration. Origin of rst generation of oak also corresponds to drought during the 1740s (Fig.7).
is implies the complexity of natural regeneration dynamic in primeval forests and also the signicant role
of drought in development of uniformed age structure of European lowland primeval forests. e lack of regen-
eration aer the disturbances in the 1850s and 1890s (Fig.7e) can be attributed to the fact that oak regenerates
in a small area, is especially dependent on light conditions and is spatially limited by the heavy seed dispersion
mechanism. Another possible factor is high competition with eld elm (Ulmus minor L.) which has been widely
distributed until 1970s in oodplain forests. Also unavoidable is the possible inuence of herbivores (primarily
wild pigs) and birds, which can signicantly decrease abundant seed crops51. Observed growth release of ash trees
did not result in regeneration. Being a pioneer tree species, ash originated through succession on the wetlands
and the structure of these forests are very dense which hinders successful regeneration. erefore, it requires large
scale disturbances for adequate regeneration in contrast to oak.
Rising temperatures and anthropogenic inuence have signicantly changed the hydrologic conditions in
both the river basin area and the river itself52. is study, which was conducted in the still preserved natural reten-
tion area of the Sava River, also found signicant changes. ey manifest in the decline of average, and especially
minimal annual and individual monthly water levels, with particular intensity aer 1980 (Fig.2). Such negative
trends can be explained by increased evaporation due to increases in temperature and evapotranspiration and
have been recorded in most European rivers52. From an ecological standpoint, river water level is an important
indicator of groundwater levels that recharges by inltration from the Sava riverbed during high water levels
(spring and autumn) even up to 5 km from the riverbed53.
e proportion of transpiration in oodplain forests is a high 80% of the total evapotranspiration, and most
of the transpired water originates from underground sources54. In such conditions, climate change together with
the fall of river water levels, increasingly expose oak to unfavorable conditions37,55–58.
e results of this research conrm recent trends that higher air temperatures hasten the long-term decline
of trees and that in the dry conditions of this area, oak might be greatly endangered by changes in climate59–63.
Although some research suggests an increase in oak radial growth due to higher temperatures56,64, CO2 fertili-
zation and increases in N deposition65, we believe this might be possible only in normal hydrologic conditions.
Conclusions
We conclude that pedunculate oak and narrow-leaved ash dier in their sensitivity to climate and hydrological
parameters to which ash is more sensitive. Constant increase of sensitivity to precipitation and river water level of
ash has become more pronounced during the climate warming period. Our results suggest that extreme climatic
events, especially drought are a signicant driver behind growth release but isn’t always followed by successful
recruitment in the studied forests. We also found that oak has an evident shi in sensitivity triggered by severe
droughts in the 1940s. Such shi may have been due to its adaptation strategy to increasing temperature and drier
environment conditions.
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Narrow-leaved ash, as the colonizer of wet swamp edges, could also face the rising pressure of water decit. Its
climate signal is slightly more stable, without the dramatic changes exhibited by oak, but considering the distur-
bance dynamic reconstruction results, it shows greater sensitivity to droughts.
e physiological exibility of oak’s adaptation to drought events was shown to be an optimal survival mecha-
nism in the past. However, it could be expected that in disturbed conditions with declining levels of groundwater,
oak might not be able to utilize this alternative in the future.
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Acknowledgements
S.M., A.Ž., D.T., V.P., M.O. and I.A. were supported by the Croatian National Science Foundation under the
project IP-2014-09-1834, A.Ž. received support from Ministry of Agriculture of the Republic of Croatia. Many
thanks to omas Andrew Nagel for his helpful suggestions and comments as well as Jan Nagel for improving the
translation.
Author Contributions
S.M. and A.Ž. designed the research and prepared the manuscript, D.T., V.P. analyzed data, M.O. and I.A. helped
supervise the project. All authors together contributed to the interpretation of results.
Additional Information
Supplementary information accompanies this paper at https://doi.org/10.1038/s41598-018-34875-w.
Competing Interests: e authors declare no competing interests.
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