Dendrochronologia 79 (2023) 126072

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Dendrochronologia
journal homepage: www.elsevier.com/locate/dendro

Differences in climate-growth relationships between two tree species that

co-occur in a seasonally dry tropical forest in Northeastern Brazil
Clayane Matos Costa a, Mariana Alves Pagotto a, José Roberto Vieira Aragão b,
Claudio Sergio Lisi a, *
a
Plant Anatomy and Dendrochronology Laboratory, Department of Biology, Federal University of Sergipe, Av. Marechal Rondon s/n, Rosa Elze, São Cristóvão, Sergipe
49100-000, Brazil
b
Department of Plant Biology, Institute of Biology, University of Campinas – UNICAMP, P.O. Box 6109, 13083-970 Campinas, SP, Brazil

A R T I C L E I N F O A B S T R A C T

Keywords: Seasonally dry tropical forests are an important global climate regulator and represent one of main drivers of
Tree rings carbon sink dynamics. However, projections of climate change suggest future productivity losses and negative
Seasonal forests impacts on forest functioning. Understanding the interaction between climate variability and tree growth re­
Drought effects
sponses between species with different growth strategies represents a crucial challenge to forecast ecosystem
Climate change
functioning in the future. Here we used tree ring chronology to evaluate changes in growth and climate sensi­
Growth strategies
tivity of two tropical tree species that co-occur in a seasonally dry tropical forest in Brazil: Cedrela odorata and
Ceiba glaziovii. Using Pearson correlations and linear regressions we explored how growth variability is correlated
with local (precipitation, temperature) and global (ocean temperature and El Niño Southern Oscillation - ENSO)
climatic factors. Tree growth was closely related with precipitation in C. odorata (r = 0.59) and C. glaziovii (0.24).
Differences were found at monthly level, which C. odorata showing greater sensitivity in the beginning of rainy
season. The South Atlantic Temperature was positively correlated with C. odorata, while ENSO was negatively
correlated. Our results showed a dominant effect of precipitation on tree growth and suggest that are different
growth strategies among species, which C. odorata being the most sensitive to drought and C. glaziovii more
adapted with parenchyma in trunk. Therefore, C. odorata is probably more vulnerable to the deleterious effects of
future climate change than C. glaziovii. Our findings highlight the importance of understanding the climate
sensitivity of different seasonally dry tropical forest species, which is critical to predicting carbon dynamics in
tropical regions. These also reveal that differences in sensitivity must be considered when prioritizing conser­
vation measures for seasonally dry tropical forests.

1. Introduction is still scarce (Frank et al., 2015; Pennington et al., 2018).

Seasonally dry tropical forests represent a key factor in global
climate regulation (Piao et al., 2020a) since they act as carbon sinks that
occur in seasonal cycles of productivity (Linscheid et al., 2020; Piao
et al., 2020b, 2020a; Sitch et al., 2003). Despite this importance, these
forests are one of the regions that will lose the most carbon over the
coming years with climate change-induced temperature increased and
droughts (Frank et al., 2015). Temperature and precipitation are the
main modulating agents of tree growth variability of these regions
(Linscheid et al., 2020; Piao et al., 2020a; Zuidema et al., 2020). How­
ever, detailed information on climate effects on seasonal forests growth
Recent findings show that seasonally dry tropical forests of North­
eastern Brazil are considered one of the threatened due to climate
change and intensification of drought stress (Zhao et al., 2018). In this
forest, tree growth is fully associated with seasonal rainfall of the region
(Aragão et al., 2019a, 2022; Nogueira Jr. et al., 2018) which in turn is
modulated mainly by the Intertropical Convergence Zone (ITCZ)
(Marengo et al., 2018). Oscillations in sea surface temperatures (SST) in
the Atlantic Ocean (Correia filho et al., 2019; Jimenez et al., 2019; Utida
et al., 2019) act on the ITCZ, promoting climate variability in the region.
Also, the El Niño events that occur in Pacific Ocean are the main envi­
ronmental factors that impact this seasonality (Stan and

* Correspondence to: Department of Biology, Federal University of Sergipe, Av. Marechal Rondon s/n, Rosa Elze, São Cristóvão, Sergipe 49100-000, Brazil.
E-mail addresses: clayane_matos@hotmail.com (C.M. Costa), maripagotto07@gmail.com (M.A. Pagotto), j211463@dac.unicamp.br (J.R.V. Aragão), cslisi@
academico.ufs.br (C.S. Lisi).

https://doi.org/10.1016/j.dendro.2023.126072
Received 5 December 2022; Received in revised form 1 March 2023; Accepted 1 March 2023
Available online 3 March 2023
1125-7865/© 2023 Elsevier GmbH. All rights reserved.
C.M. Costa et al.
Sanchez-Azofeifa, 2019; Zhao et al., 2018). In El Niño years, seasonal
drought in Northeastern Brazil is amplified (Marengo et al., 2018), as
well as its severe effects on dynamic vegetation (Zhao et al., 2018). In
addition, El Niño may amplify the adverse effect of temperature on
species productivity (Linscheid et al., 2020) and weaken its carbon
sequestration (Piao et al., 2020a). Events like these are expected to occur
more frequently (Stan and Sanchez-Azofeifa, 2019), and may affect the
growth and resilience of the species (Gao et al., 2018).
These is an urgent need to understand forest dynamics in relation to
climatic variability, especially tree growth response of tropical dry forest
(Babst et al., 2018). In this sense, tree rings study is a useful tool for
clarify how climate effects act on tree growth fluctuations in regions
such as seasonal forests (Aragão et al., 2022; Zuidema et al., 2022). In
seasonally tropical dry forests of Northeastern Brazil, despite the low
number of records on international platforms (Babst et al., 2017), recent
researches with tree rings have shown great potential to be explored
(Aragão et al., 2019a, 2022; Lisi et al., 2020; Menezes et al., 2022;
Pagotto et al., 2021). However, when compared to temperate regions,
there are considerable gap of tropical tree growth knowledge (Pearl
et al., 2020).
One way to fill this gap is to explore tree growth of different species
in order to evaluate the plastic responses of xylem growth to water
deficit conditions (Deslauriers et al., 2017; Steppe et al., 2015). In this
sense, it is possible to identify different drought survival strategies be­
tween species (Balducci et al., 2015; McDowell et al., 2018) and to
develop effective and appropriate protection tools for specific needs of
each species (Hennon et al., 2012). The study of tree rings can be applied
to numerous species and has the potential to reveal changes in growth
over time caused by extreme environmental pressures, such as drought
(Gao et al., 2018; Kannenberg et al., 2020).
In this context, we present a tree ring analyses in two tropical tree
species found in Brazilian seasonally dry tropical forest (Aragão et al.,
LISI, 2019a; Aragão et al., 2022) to provide an understanding of radial
growth patterns and growth-climate relationships. We chose Cedrela
odorata L. (Meliaceae) and Ceiba glaziovii (Kuntze) K.Schum. (Malva­
ceae) since they co-occurring in an unexplored seasonal forest of
Northeastern Brazil, with wide distribution and high
ecological-economic relevance (Queiroz et al., 2017), and also consid­
ering their dendrochronological potential (Brienen et al., 2009; Lisi
et al., 2020; Menezes et al., 2022; Quintilhan et al., 2021; Vasconcellos
et al., 2019). As a first step, the dendrochronological potential of these
species was confirmed by examining the macroscopic anatomical
structures that delimit their tree rings, and considering the strong
growth synchronicity between individuals and their climate-growth
relationship. Growth variability was correlated with local meteorolog­
ical data (precipitation and temperature) and large-scale climate vari­
ables (e. g. global sea surface temperatures, El Niño indices). Finally,
climate-growth relationships of two species were validated by simple
and multiple linear regressions, as well as spatial correlations.
Given the seasonal variations in water availability modulate not only
similarities in climate-growth responses, but also affect tree sensitivity
in different ways and in different types of seasonally dry tropical forests
(López et al., 2019), our hypotheses were: 1) Tree growth of each species
is synchronous and varies over time according to local water availabil­
ity; 2) The climate-growth relationship differs between species; 3) The
sea surface temperature of Atlantic Ocean modulates tree growth of both
species; 4) El Niño events promote adverse effects on tree growth
species.
2. Material and methods
2.1. Studied species
In Northeastern Brazil, the largest dry tropical forests system is
known as the Caatinga, which is characterized as a spiny deciduous
savanna and is considered one of the 10 most species-richness forest in
2
Dendrochronologia 79 (2023) 126072
the world, with high ecological and economic relevance for the region
(Queiroz et al., 2017). Cedrela odorata L. (Meliaceae) and Ceiba glaziovii
(Kuntze) K.Schum. (Malvaceae) are thornless, endemic deciduous tree
species that co-occur in Caatinga forest and belong to families with
distinct phenological and functional characteristics (Butz et al., 2018).
These two species were chosen because they are widely distributed in
several regions of the Caatinga forest and present visible tree-rings. In
addition, recent studies have shown the dendrochronological potential
of C. odorata (Lisi et al., 2020; Menezes et al., 2022; Quintilhan et al.,
2021), as well as several species of the genus Ceiba (Brienen et al., 2009;
Vasconcellos et al., 2019).
2.2. Study site
The study area is a forest fragment of a private farm with approxi­
mately 12 ha (10º08’05.8” S; 37º03’21.1” W) (Fig. 1). The site is located
on the right margin of the São Francisco River, in Sergipe State, Brazil.
This region is characterized by a semi-arid tropical climate with shrub-
tree vegetation and a great diversity of cactus species and deciduous
angiosperms (Jacomine et al., 1975).
The soil is an association of Eutrophic Litholics with medium texture
and non-Calcic Brown soil with medium/clayey texture (Santos et al.,
2018). The semi-arid climate (BSh) (Köppen, 1948) shows an annual
average temperature of 26ºC, and total annual rainfall between 550 and
800 mm concentrated between April to July (Jacomine et al., 1975)
(Fig. 1).
2.3. Dendrochronological and statistics analyzes
The samples were collected by guided tour (Williams and Brown,
2019), in which individuals of different sizes were selected among the
populations of the intended species. A total of 35 C. odorata trees were
sampled in January 2018 while 10 C. glaziovii trees were sampled in
January 2021. For C. glaziovii, the tree sampled corresponds to the total
number of specimens founded in the studied forest. We used a manual
increment borer from Suunto and Haglof, with 5.15-mm-diameter, and
extracted, at least, two cores per tree. The circumference at breast height
(C.A.P. = 1.30 m) of the trees and the geographic coordinates were
recorded.
These samples had a varied length between bark and pith. Some
radial samples, despite being ruptured due to the collection procedure,
were carefully aligned and used to this study. The samples were dried at
air temperature and fixed on wooden supports. Then, they were polished
with increasingly finer sandpaper (60–2000 grit) to allow good visual­
ization of tree ring boundaries under a stereomicroscope (Gärtner et al.,
2015; Orvis and Grissino-Mayer, 2002). Subsequently, the wood sur­
faces were digitized with a high-resolution scanner (EPSON® Expression
12,000 XL) with a resolution of 1200 dpi and “.tif” format. After, we
used a stereomicroscope to compare the wood anatomy with the digital
images. Some radial samples supported as basis for the macroscopic
anatomical description of growth layers (cf Aragão et al., 2019; Aragão
et al., 2022). This procedure was useful to understand the tree ring
boundaries and to aid in the interpretation of the possible false rings,
which is very frequent in tropical trees (Brienen et al., 2016).
Based on the digital image, tree-ring width was determined using the
Image Pro-Plus software with a precision of 0.01 mm. Ring width data
were exported to Excel software for graphic comparison. The ring-width
measurements were cross-correlated using visual (correlation curves)
and statistical techniques, such as the COFECHA software (Holmes,
1983), which allow the quality control of cross-dating.
Chronologies were computed for each species using the ARSTAN
software (Cook, 1985; Cook and Kairiukstis, 1990). The detrend was
applied to measurements series from negative exponentials and/or
linear regression applied to standardized series (Hughes et al., 2011;
Speer, 2010) and the standard version of each chronology was used for
climate-growth analysis and species comparisons. To understand
C.M. Costa et al. Dendrochronologia 79 (2023) 126072

Fig. 1. Location map of the studied forest fragment. Local climate diagram for the period 1956–2017 (cf. WALTER; LIETH, 1960): mean monthly temperatures (grey
lines), mean precipitation (black lines), months with water deficit (when the precipitation curve < temperature curve; dotted areas), rainy season (precipitation >
temperature; area with vertical lines), period with precipitation> 100 mm; black area.
Source: SEMARH/SE and AGRITEMPO.

variations in growth between species, differences and similarities be­
tween chronologies were tested using the Wilcoxon test and Pearson
correlation.
To detect the climatic signal in tree growth, we correlated the tree
ring chronologies with local climate, using Pearson’s correlation co­
efficients. In this step, the Treeclim package was used in the R 3.6.3
software (Zang and Biondi, 2015). Total annual precipitations, as well as
mean monthly precipitation from March to August of the current year
(which correspond to tree ring formation) were used. Likewise, inter­
polated temperature data obtained through the KNMI Climate Explorer
platform were used (Trouet and Van Oldenborgh, 2013) for calculating
correlations and linear regressions.
Additionally, the relationship between growth and global climate
records was analyzed. First, correlations maps between chronologies
and sea surface temperature (SST) reconstructions were produced using
the KNMI Climate Explorer (Trouet and Van Oldenborgh, 2013). Next, it
was possible to identify which regions of the ocean affected tree growth.
Sea surface temperature reconstructions with optimal interpolation of
0.25◦ were used through Version 4 of the CRU TS (Harris et al., 2020).
These correlations were performed by month, but with rolling averages
of up to 7 months for SST data (between March and August).
We also used Pearson correlations between chronologies and South
Atlantic Temperature (SAT) and El Niño Southern Oscillation (ENSO).
Both represent large-scale climate indices that are often used in
dendrochronological studies (Aragão et al., 2019a; Schöngart et al.,
2017). SAT comprises sea surface temperatures between 0◦ − 20◦ S and
10◦ E–30◦ W. For ENSO, El Niño 3 was used, which consists of ocean
temperature anomalies in the Pacific between 90◦ − 150◦ W and
5◦ N–5◦ S. The Treeclim package was used in R 3.6.3 software (Zang and
Biondi, 2015).
Similar to local climate analysis, growth correlations with monthly
precipitation values were used (up to 7 months). To identify the com­
bination of months in which tree rings chronologies significantly
responded to climate, combined single and multiple linear regression
models were applied (Hughes et al., 2011; Speer, 2010), correlating the
growth of both species with environmental data (local and global).
Combining single and multiple regression models was useful to under­
stand tree ring patterns (Aragão et al., 2022). In addition, they
contribute to the evaluation of relationship between chronology and
climatic factors related to tropical species (Aragão et al., 2019a;

3
C.M. Costa et al.
Nogueira Jr. et al., 2018). All analyzes between growth and climate were
calculated using Pearson’s correlations (r; 95% significance level), sin­
gle and multiple regressions (p and R2; 95% significance level 95%)
(Hughes et al., 2011; Speer, 2010), over the period 1950–2019 (variable
according to chronologies), using the software R 3.6.3 (R Core Team,
2019).
2.4. Climate data collection
The monthly precipitation data used were obtained from local
meteorological stations and close to the study site: from the munici­
palities of Nossa Senhora de Lourdes, Itabi, and Aquidabã. These data
are from five weather stations: (i) Aquidabã Semarh/INPE, 217 m a.s.l.
(data of 1955–2009), (ii) Aquidabã Agritempo/TRMM 5237, 13 m a.s.l.
(2000–2017), (iii) Itabi Semarh/CEMADEN, 187 m a.s.l. (1963–2005),
(iv) Nossa Senhora de Lourdes Semarh, 200 m a.s.l. (1985–2005), (v)
Nossa Senhora de Lourdes Agritempo/ TRMM 5368, 453 m a.s.l.
(2000–2017). Monthly temperature information indices (maximum and
minimum) were obtained using Version 4 of the CRU TS (Harris et al.,
2020) from Climate Explorer platform - KNMI (www.climex.knmi.nl) for
the coordinates of study region. Monthly data on a global scale, such as
SST and ENSO events, were obtained through the North American
Monitoring Agency’s digital platforms – NOAA (https://www.esrl.noaa.
gov/psd/forecasts/sstlim/timeseries/) and also through Version 4 of the
CRU TS (Harris et al., 2020) on the KNMI platform (www.climex.knmi.
nl).
3. Results
Tree rings of C. odorata and C. glaziovii were visible under a stereo­
microscope with 10x magnification. In C. odorata, tree rings were
delimited by the marginal parenchyma, associated with larger diameter
vessels, characterizing the semi-porous rings. In C. glaziovii, however,
tree rings were characterized by delimitation with marginal paren­
chyma, preceded by fibers with thick cell walls in the latewood of the
previous ring (Fig. 2). False tree rings were observed in both species,
consisting mainly of variations in wood color, fibrous zones and
confluent axial parenchyma.
We dated a total of 20 radii of C. odorata and 19 radii of C. glaziovii,
with tree ages ranged from 35 to 58 and 25–53 years, respectively
(Table 1). C. odorata showed inter-correlation value of 0.65 and C. gla­
ziovii 0.51, with average EPS between 0.90 and 0.97, respectively
(Table1). Synchronization of tree ring series showed similar growth
variability between species (Fig. 3a), which was confirmed by Wilcoxon
test (Fig. 3b). Although a few broken samples (without bark or pith)
were possible to crossdated, some non-broken samples showed anoma­
lous growth (around 10% of the samples/species – 6–8 radii) which
were, therefore, disregarded from the analyzes.
Correlations between species chronologies and total annual precip­
itation were r = 0.59 for C. odorata and r = 0.24 for C. glaziovii (Fig. 4).
Monthly analysis also showed a positive correlation between growth and
precipitation, in which the most significant months for radial growth
were April through August (rainy season period) of the current year
(Fig. 5). Comparison between chronologies and temperature, however,
did not showed any significant correlation for both species (Fig. 5).
Fig. 2. : Macroscopic cross-sectional images of wood from (a) Cedrela odorata
and (b) Ceiba glaziovii. Dark arrows indicate the tree rings boundaries ( 1 mm).
4
Dendrochronologia 79 (2023) 126072
During the monthly analyses, we observed that five months were
positive and significant in C. odorata growth, in contrast to C. glaziovii
which showed a significant response only in one month (Fig. 5). Linear
regressions showed the rainiest months (April to June) was determinant
for C. odorata growth (Table 2), while for C. glaziovii, tree growth was
determined only by rainfall of April (Table 2).
Correlation maps between chronologies and SST showed that species
growth correlates most in Equatorial Pacific and South Atlantic (Table 2;
Fig. 6). The strongest correlations (highest r values) were observed for
the March-August period. Such correlations coincide with the rainy
season of the study site and shows the influence of teleconnections on
the growth of tropical forests.
ENSO showed negative monthly correlations with species growth,
however, a stronger relationship with C. odorata than C. glaziovii was
noted (Table 2; Fig. 6). On the other hand, SAT showed positive corre­
lations with C. odorata chronologies and no apparent effect on
C. glaziovii was observed (Fig. 6).
The difference in the precipitation-growth relationship between
C. odorata (Fig. 6b) and C. glaziovii (Fig. 6d) was confirmed, with
C. odorata growth being most dependent of the rainy season. Through
the results of the multiple regressions, SAT and ENSO effect on
C. odorata growth was observed for the rainiest months March and April,
respectively (Table 2). However, for C. glaziovii these effects were not
significant on multiple regressions.
4. Discussion
In this study, we evaluated how environmental conditions influence
the interannual growth variation of two tree species (C. odorata and
C. glaziovii) from different families that co-occur in a seasonally dry
tropical forest in Northeastern Brazil. Both species form annual tree
rings and their growth variations was associated with local precipitation
and surface temperatures in Equatorial Pacific and South Atlantic.
However, C. odorata showed high correlation values with climate than
C. glaziovii, which probably indicate a greater climate sensitivity. In
other worlds, C. odorata growth appears to be closely synchronized with
rainfall patterns of the study site. C. glaziovii, in turn, stores water in the
trunk to use in the dry season, which probably reflect this adaptation on
their growth. However, to our knowledge, this is the first study reporting
tree-ring chronology of C. glaziovii. These results reveal the potential of
both species for dendroecological studies in tropical forests and
emphasize variations in growth sensitivity of different species in
seasonally dry tropical forests.
4.1. Tree ring chronology and its relationship with precipitation
The two species showed different types of tree ring boundaries
(Brienen et al., 2016; Fichtler; Worbes, 2012), that coincided with the
descriptions from previous studies of C. odorata (Espinoza et al., 2014;
Lisi et al., 2020; Menezes et al., 2022; Pagotto et al., 2021) and for other
species of the genus Ceiba (Brienen et al., 2009; Vasconcellos et al.,
2019). The macroscopical anatomical characterization of tree rings
boundaries reduced identification errors during radial measurements
and aided for effectiveness of crossdating process in both tropical species
(Aragão et al., 2019a, 2022; Brienen et al., 2016; López and Villalba,
2020). Although the species belong to different botanical families,
similar growths were observed (Fig. 3), showing the site effect on tree
growth, which was mentioned in other studies in tropical dry forests
(Aragão et al., 2022; López et al., 2019). This effect can also be observed
in correlations analysis between chronologies and precipitation (total
annual and seasonal; Fig. 4) and confirm the climatic influence on the
cambium rate seasonality of seasonally dry tropical forests (Aragão
et al., 2022; Lisi et al., 2020; Menezes et al., 2022; Pagotto et al., 2021;
Zuidema et al., 2022).
Although these similarities were observed (Figs. 3 and 4), rainfall
monthly effect on growth variability between species was different
C.M. Costa et al. Dendrochronologia 79 (2023) 126072

Table 1
Summary of dendrochronological features for the tree ring chronology of C. odorata and C. glaziovii from a seasonal tropical dry forest, Northeast Brazil. N trees:
number of analysed trees; N radii: number of analysed radii; Intercorr: intercorrelation between series; Rbar: correlation between trees; EPS: expression population
signal.
Species N trees N radii Ages Intercorr. Rbar EPS Period

Cedrela odorata 21 30 35–58 0.65 0.53 0.97 1957–2017

Ceiba glaziovii 10 19 25–53 0.51 0.37 0.90 1967–2020

Fig. 3. (a) Pearson correlations of tree ring width chronologies (RWI) of Cedrela odorata (sampled in 2018) and Ceiba glaziovii (sampled in 2021); (b) comparison
between growth variability of C. odorata and C. glaziovii. Significance of p < 0.05.

bulging appearance). This may be a low-cost adaptation to avoid water

Fig. 4. Temporal relationship between standard chronologies (grey lines) and
total annual precipitation (black lines) for (a) Cedrela odorata and (b) Ceiba
glaziovii from a seasonally dry tropical forest, Northeastern Brazil. The precip­
itation represents the mean of three local meteorological stations for the
period 1957–2020.
(Fig. 5), indicating that the studied species are showing different stra­
tegies to support water deficit (Anderegg and Meinzer, 2015; Aragão
and Lisi, 2019b; Baas et al., 2013; Battipaglia et al., 2010; Gleason et al.,
2016). One possible reason for that is the ability of C. glaziovii to store
water in the cortical cells of trunk (which gives the trunk a swollen or
deficits during drought periods (Lorenzi, 2009). Similar situation was
verified for oak trees growing in a semi-arid forest of Mexico, with deep
roots reaching the water in fractures or fissures of rocks and also with
the presence of water reserve in their trunk (Rodriguez-Robles et al.,
2020). In this sense, C. glaziovii is a less sensitivity species to seasonality
when compared with C. odorata.
The high sensitivity of C. odorata growth to water deficit was also
observed in previous tropical dry forests studies (Lisi et al., 2020;
Menezes et al., 2022; Pagotto et al., 2021). Furthermore, other studies
have shown that tree ring formation of tree species in the tropical dry
forest of Brazil is strongly correlated with the rainy season (Pagotto
et al., 2015; Nogueira et al., 2017). Our results corroborate with these
studies and highlight the importance of the rainiest months for C.
odorata growth.
Species with high sensitivity to climate variations, as C. odorata, are
subject to reduced growth and reproduction, increased mortality and are
considered most vulnerable to climate change (Powers et al., 2020).
However, the high sensitivity of tropical dry forest species is worrying
(Kannenberg et al., 2020; Wang et al., 2016), since climate change
forecasts indicate a reduction in the ecosystem services provided by
them (Allen et al., 2017). It is therefore relevant to identify the different
drought survival strategies (Balducci et al., 2015; McDowell et al., 2018)
and, in this way, structure conservation mechanisms appropriate to the
needs of each species (Hennon et al., 2012).
Trees in seasonally dry tropical forests generally face with high
temperatures, but are especially limited by variations in water avail­
ability (Allen et al., 2017). Increased temperature and reduced precip­
itation during the growing season are the main threats to carbon
sequestration and the maintenance of tropical forests (Zuidema et al.,
2022). In Northeastern Brazil, drought and high temperatures are a
common climate situation (Marengo et al., 2018; Pereira et al., 2014).
Although our results did not show any temperature effect on tree growth
for both species, high temperatures combined with the increase of
droughts period can cause cumulative effects on tree growth, with
possibly long-term effect, as well as a decrease in species resilience
related to such events (Kannenberg et al., 2020). The results of this study
corroborate with the understanding of seasonal growth of tree species

5
C.M. Costa et al. Dendrochronologia 79 (2023) 126072

Fig. 5. Results of the correlation function between species growth and monthly precipitation, monthly maximum temperature, South Atlantic temperature and El
Niño 3 between March-August. (a) and (b) Cedrela odorata, (c) and (d) Ceiba glaziovii. Filled lines indicate significant relationships at 95% and dashed lines are
non-significant.

are associated with the seasonality of rainfall in Northeastern Brazil,

Table 2
which is strongly influenced by the ITCZ (Jimenez et al., 2019; Marengo
Results of multiple regression analysis between chronology (dependent variable)
et al., 2018; Pereira et al., 2014).
and historical monthly average values of environmental variables, for each
species. The multiple regression coefficient “b”, standard error, and “p” values
The ITCZ acts as one of the main teleconnection systems that
are shown. determine rainfall in the seasonal forests of Northeastern Brazil
(Marengo et al., 2018). Changes in SST can influence the position and
Species Variables b ± SE
the effect of ITCZ, modifying the rainfall patterns in Brazilian seasonal
Cedrela odorata intercept 0.3919 ± 0.1229 * * forests (Correia Filho et al., 2019; Jimenez et al., 2019; Pereira et al.,
1. R2 = 0.34 (F = 15.07; df = 58) Prec. April 0.0036 ± 0.0008 * **
2014; Wu et al., 2020). In other words, this influence can reduce
2. R2 = 0.22 (F = 7.99; df = 58) Prec. June 0.0015 ± 0.0008.
intercept 9.4141 ± 2.8962 * * (Jimenez et al., 2019; Martins, 2018; Pereira et al., 2014) or increase the
TSA March 0.4082 ± 0.163 * precipitation in Brazilian Northeastern (Utida et al., 2019), which in
El Niño 3 April -0.3116 ± 0.1056 * * turn, can modify tree growth of species that occur in this region (Aragão
Ceiba glaziovii intercept 0.7577 ± 0.1133 * ** et al., 2022). The growth variability of the studied species coincides with
1. R2 = 0.08 (F = 4.19; df = 52) Prec. April 0.0019 ± 0.0009 *
variations in SSTs and their effect on rainfall in Northeastern Brazil, as
described by Jimenez et al. (2019).
from Northeastern Brazil in relation to precipitation, especially for The growth variability of C. odorata and C. glaziovii showed corre­
C. odorata, which is more sensitive to the environment and more lations with SAT. Both were positive and in the same period (Fig. 5). This
vulnerable to climate change (Menezes et al., 2022; Pagotto et al., 2021; similarity is common in seasonally tropical dry forests of Northeastern
Powers et al., 2020). Brazil, even when dealing with species from different families, once it is
mainly linked to tree phenology (Amorim et al., 2009). In these envi­
ronments, tree phenology is directly related to precipitation (Amorim
4.2. Growth responses to the surface temperature of the South Atlantic et al., 2009), which is strengthened by SAT through trade winds incident
Ocean on the ITCZ (Utida et al., 2019). In this case, some species that occur in
Northeastern Brazil have growth variability associated with precipita­
The strong relationship between precipitation and tree growth may tion and SAT, even with differences in the duration of this relationship
be linked to the deciduousness and demonstrates the dependence of (Aragão et al., 2019a, 2022; Menezes et al., 2022). The results of mul­
species growth on the annual rainy season (Aragão et al., 2019a, 2022; tiple regressions (Table 2) and spatial correlations with the SSTs (Fig. 6)
Lisi et al., 2020). However, differences in climate sensitivity between also showed divergences between C. odorata and C. glaziovii responses to
species of the same site may indicate different strategies to withstand SAT. This large-scale climatic phenomenon affects the climate at the
environmental changes (McDowell et al., 2008, 2018). Such differences region (Utida et al., 2019) and hence, the tree growth of C. odorata

6
C.M. Costa et al. Dendrochronologia 79 (2023) 126072

Fig. 6. Spatial correlations between tree ring width index (RWI) chronologies of two tree species from a seasonally dry tropical forest with gridded sea surface
temperatures (SSTs) in the Atlantic and Pacific oceans and total annual precipitation. Gridded data from 0.25◦ optimal interpolation sea surface temperature re­
constructions from Version 4 of the CRU TS (HARRIS et al., 2020). The 7-month periods with the highest correlations for each species are shown. Colors indicate
Pearson correlation coefficients. (a) Cedrela odorata growth vs. SSTs between 1957 and 2017; (b) C. odorata growth vs. precipitation between 1957 and 2017; (c)
Ceiba glaziovii growth vs. SSTs between 1967 and 2020; (d) C. glaziovii growth vs. precipitation between 1967 and 2020.

during the rainy season (Aragão et al., 2022). In the specific case of
C. glaziovii, changes in SAT did not significantly modify tree growth, as
was observed in other seasonally dry tropical forests (Aragão et al.,
2019a; Menezes et al., 2022). Overall, the climate sensitivity can vary
between species (Aragão et al., 2022; Powers et al., 2020) and distinct
seasonal forest types (Da Silva et al., 2022; López et al., 2019), as they
also indicate different strategies to withstand global climatic pressures
(Balducci et al., 2015; McDowell et al., 2018).
4.3. Growth responses to El Niño events
Of all the variations in SSTs studied recently, none affected tropical
forest growth more then ENSO (Aragão et al., 2022; Garreaud et al.,
2020; Miranda et al., 2020; Spannl et al., 2016; Zhang; Jia, 2020; Zui­
dema et al., 2022). El Niño events negatively influenced tree-ring widths
of the two species from the seasonally dry tropical forests studied here
(Figs. 5, 6 and Table 2), corroborating their strong action on growth in
forests of Northeastern Brazil (Aragão et al., 2019a, 2022; Menezes
et al., 2022; Nogueira Jr. et al., 2018). However, the determining effect
of ENSO was observed only on C. odorata population (Figs. 5, 6 and
Table 2), specifically in April (Table 2).
The seasonality of these environments, which is strongly influenced
by the ITCZ, is the main explanation for the effectiveness of the ENSO on
the seasonal forests of Northeastern Brazil (Correia Filho et al., 2019;
Jimenez et al., 2019; Pereira et al., 2020). During El Niño years, the
annual rainfall volume is reduced and seasonal variability of growth
forest increases (Linscheid et al., 2020; Zhao et al., 2018). In seasonal
forest with litholic soils (FAO, 2014; Santos et al., 2011, 2018), the
drought caused by ENSO can limit its ability to retain water and, as a
result, can influence tree growth (Liu et al., 2020). The different re­
sponses observed between species and ENSO may be associated with the
hydraulic characteristics of the wood (Anderegg and Meinzer, 2015;
Aragão and Lisi, 2019b; Baas et al., 2013; Battipaglia et al., 2010;
Gleason et al., 2016), that limit growth in years of severe drought
(Aragão et al., 2022; Garreaud et al., 2020; Miranda et al., 2020; Spannl
et al., 2016; Zhang and Jia, 2020; Zuidema et al., 2022). This was
corroborated that the growth of C. odorata is sensitive to the negative
effects caused by El Niño events (Menezes et al., 2022). The sensitivity of

7
C.M. Costa et al.
seasonal forests in Northeastern Brazil to El Niño and the forest
vulnerability to this global event are in line with the prediction of
climate change (Allen et al., 2017; Babst et al., 2019; Frank et al., 2015;
Pennington et al., 2018).
Future research should focus on expanding knowledge about other
species of seasonally dry tropical forests, and should incorporate longer
series of tree rings through long-lived individuals, creating more infor­
mation to mitigate actions against the effects of climate changes.
5. Conclusions
The present study confirmed the annual formation of tree rings for
two species of seasonally dry tropical forests in Northeastern Brazil and
its potential for dendrochronological analysis. The annual growth re­
sponses of C. odorata and C. glaziovii showed that rainfall seasonality is
the main limiting factor for tree growth and which can be aggravated by
other factors, such as El Niño events. Differences were observed in
climate-growth relationship between C. odorata and C. glaziovii, which
confirms that water stress modulates the different strategies to with­
stand drought (Balducci et al., 2015; McDowell et al., 2018; Powers
et al., 2020). C. odorata showed the greatest sensitivity to annual pre­
cipitation and rainy season, and therefore is more vulnerable to the ef­
fects of climate change (Allen et al., 2017; Brodribb et al., 2020; Frank
et al., 2015). C. glaziovii also showed sensitivity to climate (precipita­
tion), but with a lower correlation value than C. odorata, possibly due to
its adaptation to store water in the trunk. The climate sensitivity for both
species was reflected in tree growth relationships with fluctuations in
the South Atlantic Temperature and El Niño events.
Hence, the dendroecological study showed that these two species
have different strategies to resist droughts periods that occur in these
seasonally dry tropical forests, contributing to a better understanding of
their growth dynamics, in consonance with Aragão et al. (2022) and
Zuidema et al. (2022). This knowledge is relevant for understanding
carbon sequestration in tropical regions and offers opportunities for
conservation and decision-making on the effects of global climate
change on forests and more sensitive species.
Funding
This work was supported by the Conselho Nacional de Desenvolvi­
mento Científico-CNPQ, Brasil (grant number: 449668/2014–2).
Declaration of Competing Interest
The authors declare the following financial interests/personal re­
lationships which may be considered as potential competing interests:
CLAYANE MATOS COSTA reports financial support was provided by
National Council for Scientific and Technological Development.
Data availability
No data was used for the research described in the article.
Acknowledgments
We would like to thank the Federal University of Sergipe (UFS) for
their institutional support for the development of this research, espe­
cially the technical-scientific group of the Department of Biology and the
Post Graduate Program in Ecology (PPEC) at UFS. We would like to
thank Mr. José da Silva Matos, Mr. Éric Gabriel Antério Costa, Mr.
Hudson Matos Silva, Mr. Clemesson Matos Costa, Mrs. Luzinete dos
Santos and MSc. Ítallo Romany Nunes Menezes for your collaboration.
8
Dendrochronologia 79 (2023) 126072
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