Accepted Manuscript

Title: Tree rings in tree species of a seasonal semi-deciduous

forest in southern Brazil: wood anatomical markers, annual
formation and radial growth dynamic

Authors: Marcela Blagitz, Paulo C. Botosso, Tomaz

Longhi-Santos, Edmilson Bianchini

PII: S1125-7865(18)30126-7
DOI: https://doi.org/10.1016/j.dendro.2019.04.006
Reference: DENDRO 25592

To appear in:

Received date: 8 August 2018

Revised date: 7 April 2019
Accepted date: 17 April 2019

Please cite this article as: Blagitz M, Botosso PC, Longhi-Santos T, Bianchini E, Tree
rings in tree species of a seasonal semi-deciduous forest in southern Brazil: wood
anatomical markers, annual formation and radial growth dynamic, Dendrochronologia
(2019), https://doi.org/10.1016/j.dendro.2019.04.006

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 1

ORIGINAL RESEARCH ARTICLE

Tree rings in tree species of a seasonal semi-deciduous forest in southern Brazil: wood

anatomical markers, annual formation and radial growth dynamic

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Marcela Blagitza *, Paulo C. Botossob, Tomaz Longhi-Santosc and Edmilson Bianchinid

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a
Universidade Estadual Paulista (UNESP), Faculdade de Ciências Agronômicas, Departamento de

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Ciência Florestal, Rua José Barbosa de Barros 1780, Botucatu 18603-970, SP, Brazil. E-mail-

address: [email protected]
b
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EMBRAPA - Empresa Brasileira de Pesquisa Agropecuária / Embrapa Florestas. Estrada da
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Ribeira km 111, Colombo 83411-000, PR, Brazil. E-mail-address: [email protected]
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c
Universidade Federal do Paraná (UFPR), Setor de Ciências Agrárias, Departamento de Ciências
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Florestais, Av. Prefeito Lothário Meissner, 632, Jardim Botânico, Curitiba 80210-170, PR, Brazil.

E-mail-address: [email protected]
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d
Universidade Estadual de Londrina, Departamento de Biologia Animal e Vegetal, Rodovia Celso
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Garcia Cid km 380, Londrina 86057-970, PR, Brazil. E-mail-address: [email protected]

*
Corresponding author. E-mail-address: [email protected] (M. Blagitz)
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Abstract
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Tree rings provide valid predictions regarding species age and growth rates and, therefore, they can

contribute to understand forest dynamics and ecology. In this work, we evaluated the tree rings of

eight tree species from different successional groups that show distinct degrees of deciduousness in

a seasonal semi-deciduous forest located in a transition zone between subtropical and the tropical
 2

climates in southern Brazil. We focused on wood anatomical markers, the annual nature of tree-ring

formation, the description of false rings, a cross-dating analyses and an interpretation of the radial

increment dynamics of the species. We sampled increment cores at breast height, performed

cambial wounding and measured tree-ring widths. Annual tree rings were found in seven species,

which were confirmed by cambium wounding. Differences in fiber wall thickness between

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latewood and earlywood and the marginal parenchyma were the main anatomical markers observed.

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Deciduous species had better distinction of tree ring boundaries, while the evergreen species had

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slightly distinct tree ring boundaries. False rings were characterized by variations in wood density

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and axial parenchyma bands of different widths within true tree rings. The annual tree ring

confirmation and the anatomical description of the true and false rings are useful for future

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dendroecological research in the area. Considering the cross-dating analyses and tree-ring
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distinctiveness, Chrysophyllum gonocarpum is a recommended species. Regarding radial growth,
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the early secondary species had higher growth rates than the late secondary species. Assessing the
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growth trajectories over time, distinct patterns were observed among the species: a constant growth,

an initial increase followed by a reduction, and oscillations of the growth were observed. As no
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consistent pattern of the growth trajectories was observed among species that belong to the same
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successional groups, they contribute to the explanation of the particular life history of these

individuals in the seasonal semi-deciduous forest.

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Keywords: annual increment; Atlantic Forest; dendrochronology; false rings; seasonality; tropical
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species.

Introduction
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Tree ring analysis is a reliable tool in different research fields. In dendroecology, tree rings

are central components in discussions about the effect of climatic and environmental conditions on

tree growth (Battipaglia et al., 2014; Reis-Avila and Oliveira, 2017; Granato-Souza et al., 2018;

Prestes et al., 2018), and the vulnerability of species to climate change (Natalini et al., 2015;
 3

Rahman et al., 2017). When employed in forest ecology, tree ring widths provide information about

the species’ biomass accumulation and estimations of forest productivity (Mbow et al., 2012;

Shimamoto et al., 2014; Costa et al., 2015). In addition, the use of tree rings is considered the best

method for performing age estimates and assessing long-term growth trends in trees species,

providing valuable information on species life history (Worbes et al., 2003; Brienen and Zuidema,

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2006; Costa et al., 2015). In turn, tree long-term growth trends are used to understand the dynamics

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of forests when describing the rhythms and dynamics of growth (Worbes et al., 2003; Costa et al.,

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2015; Shimamoto et al., 2016; Locosselli et al., 2017), as well as the influence of disturbances on

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tree development (Nock et al., 2016). All of these data can be applied to conservation and

sustainable forest management when used to determine felling cycles for timber extraction in an

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attempt to reduce the impact on species survival (Schöngart, 2008; Rosa et al., 2017; Miranda et al.,
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2018).
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However, tree ring analysis in tropical species demands greater effort, because of the more
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reduced seasonality in the tropics compared to temperate climates or because species don’t form

distinct wood anatomical traits that mark the end of the growth ring, not every tree species produces
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annual tree rings or tree ring boundaries are frequently less than clear (Worbes, 2002). For instance,
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trees from the same species, like Cedrela odorata, may produce annual tree rings in Bolivia and

Venezuela, but not in Suriname where it produces two tree rings per year; and climate seasonality
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and/or tree genotype are considered the drivers of growth periodicity (Baker et al., 2017). So, in
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order to obtain responsive information about tree rings in tropical regions, it is ideal to collect wood

samples in areas that show climatic seasonality (Rozendaal and Zuidema, 2011). In species from
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these areas, the reduction of cambial activity can occur in periods unfavorable to tree growth, which

may be reflected in different features of wood cells and highlighted in tree rings (Wimmer, 2002).

Reduced cambial activity in tropical species has been linked to the seasonality of rainfall (Marcati

et al., 2006a; Lisi et al., 2008; Callado et al., 2013), temperature and/or photoperiod (Callado et al.,
 4

2001a; Bosio et al., 2016; Lara and Marcati, 2016; Marcati et al., 2016), and flooding (Callado et

al., 2001a). Thus, annual tree rings are present in tropical species and climatic factors can be related

to tree ring formation (Callado et al., 2001a; Lisi et al., 2008). Because of the seasonality of these

climate variables in the tropics, annual tree rings have been reported for more than 230 tree species

(Brienen et al., 2016).

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However, cambial activity can result in false tree rings under certain conditions. Fluctuations

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in climatic conditions within a season can trigger the formation of false tree rings in species from

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tropical areas (Venegas-González et al., 2015; Baker et al., 2017), as wells as endogenous factors,

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such as genotype, sex, size, age, photosynthetic activity and carbohydrate reserve (see de Micco et

al., 2016; Baker et al., 2017). False rings can hamper tree ring evaluations because they interfere in

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the cross-dating process, in the dating of tree-ring width curves and in the construction of a reliable
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chronology (de Micco et al., 2016), so to verify the occurrence of false rings is fundamental to
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accomplishment of these studies.
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Therefore, it is still necessary to look for potential tree species for tropical dendrochronology

considering the aforementioned assumptions of distinctiveness, tree ring annuality and the presence
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of false rings. It includes the seasonal semi-deciduous forest of southern Brazil that, besides being
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located in a transition zone between subtropical and the tropical climates, is known for having tree

species with seasonal radial stem growth driven by fluctuations in rainfall, temperature and
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photoperiod (Blagitz et al., 2016), indicating that this is a suitable site for tree ring investigations.
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Thus, in this work, we performed a tree ring study of eight representative tree species of a seasonal

semi-deciduous forest in southern Brazil, focusing on anatomical descriptions, annuality, false rings
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characterization and an evaluation of radial growth dynamics. In order to lead our interpretation, we

raised the following questions: Do tree species from the seasonal semi-deciduous forest in southern

Brazil show distinct tree rings? If they are present, are these tree rings formed annually? Do they
 5

produce false tree rings? What is the life-time growth pattern of the tree species considering tree

ring widths?

Material and methods

Study site and selected species

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Sampling took place at Mata dos Godoy State Park, a fragment of seasonal semi-deciduous

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forest located in Londrina municipality, Paraná State, southern Brazil (Fig. 1). The altitude varies

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from 500 to 600 m above sea level (Bianchini et al., 2003), and the soil is Eutrophic Purple Latosol,

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deep and well-drained in the area of the study site where the trees were sampled (Bianchini et al.,

2006). Although the climate of the region is the Cfa type (humid subtropical with hot summers)

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according to Köppen’s climate classification (Alvares et al., 2013), the study site is crossed by the
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Tropic of Capricorn, so a transition between the humid subtropical and the tropical climates is
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evidenced in the region. This leads to a distinct control of the air masses on the climate of the region
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of the study area, giving to it a transitional character at a zonal level (Nunes et al., 2009). The total

annual rainfall is 1602 mm and the average temperature is 21 ºC. December, January and February
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are the wetter (monthly average of 203 mm) and hotter (monthly average of 23.9 ºC) months, while
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June, July and August are the drier (monthly average of 69 mm) and colder (monthly average of 17

ºC) months. Therefore, two distinct seasons are observed: a wet summer from October to March
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and a dry winter from April to September (Fig. 2). The monthly photoperiod varies by 3 hours
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throughout the year (Fig. 2); the shortest photoperiod is 10.5 h/day in June and the longest is 13.5

h/day in December.
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Tree ring distinctiveness

We obtained radial wood samples from 44 trees of eight species in five botanical families

typical the seasonal semi-deciduous forest (Table 1). We sampled two to four radial wood samples

of the stem at breast height (about 130 cm above ground level) from each tree using a Pressler
 6

increment borer (0.5 cm diameter). The wood samples were fixed in a wooden support and we

polished the transverse section using sandpapers to enhance tree ring visualization. To perform

microscopic analysis, we obtained wood pieces (4 x 4 x 4 cm) from the stem, using a hammer and

chisel, that were fixed in FAA70 (formaldehyde, acetic acid, 70% ethanol). After five days of

fixation, they were transferred to 70% alcohol for storage. We reduced the pieces into small cubes

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(approximately 2 cm3) from which we obtained histological transverse sections (17 μm) using a

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sliding microtome (Leica GMBH). The sections were stained with aqueous Astra blue (1%) and

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aqueous safranin (1%; Bukatsch, 1972) solutions and semi-permanent slides were mounted in

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glycerin (50 %). We followed the terminology of IAWA Committee (1989) for tree ring

descriptions.

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Microscopic and macroscopic images were obtained with a capture camera coupled to an
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optical microscope (Olympus CX21FS1) and a stereomicroscope (Leica Z45V), respectively, using
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the software Motic Image Plus v. 2.0.
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Checking tree ring formation and the presence of false rings

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To verify the annual nature of the tree rings, we performed longitudinal incisions of 0.5 x 5
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cm (width x height) in the stem of four to seven trees per species until reaching the vascular

cambium region (cambial wounding; Mariaux, 1977; Lisi et al., 2008) in 2010 during the dry and
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cold season. In the same season in 2012, two years after marking, we collected wood samples from
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the region of each scar and adjacent areas, using a manual extractor. The samples were fixed in a

support and transverse sections of the wood samples were polished using sandpaper. We confirmed
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the annual formation of tree rings whenever two tree rings were produced by the tree

(corresponding to 2010 and 2011 rings) after the scar formed as a result of the cambial injury. With

this method, we also verified the presence of false rings, i.e. the identification of more than two tree

rings after cambial wounding. In this case, we looked for the anatomical differences between true
 7

and false rings. The structural differences were detected using criteria described by de Micco et al.

(2016): bands of dense wood within the earlywood due to the formation of latewood-like cells,

bands of less dense wood within the latewood due to the formation of earlywood-like cells,

increased incidence of thin-walled parenchymal cells and axial parenchyma bands, and resin canals.

We also sought out false rings in the radial wood samples used to identify and describe the tree

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rings.

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Radial growth dynamics

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Tree rings of the radial samples that had both pith and bark were identified and counted, using

the stereoscopic microscope Leica Z45V. The markers indicated by IAWA Committee (1989) were

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considered as growth layer boundaries. Subsequently, we digitalized the radial samples (resolutions
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of 1200 dpi; .jpeg type) and measured the tree-rings width (mm) using the software Image Pro-Plus
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version 4.5.0.19. We performed cross-dating procedures to check the tree rings dating in each
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species (Speer, 2010). To assess the cross-dating quality, we used the COFECHA software,

considering the values obtained from Pearson’s correlations (p < 0.01) between each chronological
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series of tree rings and the master-dating chronology from COFECHA (Holmes, 1983). The

fragmentation period provided (the size that COFECHA should fragment the samples for
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correlations) was 40 years, with an overlap of 20 years in Aspidosperma polyneuron, Alchornea

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glandulosa, Cedrela fissilis and Chrysophyllum gonocarpum, and 20 years, with an overlap of 10
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years in Croton floribundus, Cabralea canjerana, Trichilia claussenii and Prunus myrtifolia. This

value was chosen considering the criterion that the fragmentation period size is dependent on the
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total sample size, and the selected length is approximately half the total length of the analyzed

series (Grissino-Mayer, 2001). We also considered the EPS (expressed population signal) to assess

a common variability within a species chronology. The EPS values were calculated in ARSTAN.
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After the chronological series synchronization, we calculated the mean cumulative radial

increment (CRI) of each radial sample by adding the width of each tree ring with the width of the

previous rings (Costa et al., 2015). When individuals had more than one radial series sampled, we

estimated an average CRI, considering an average of the measured widths. We also calculated the

mean annual radial increment (ARI) by dividing the cumulative radial increment by the number of

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tree rings of each sample (Costa et al., 2015). We performed an analysis of variance (ANOVA) with

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a Tukey post-hoc test to compare ARI and CRI among the species, considering the significance

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level of 5% (p < 0.05). The dynamics of growth were evaluated in two ways. At first, we plot the

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CRI over the years for each tree of each species, as well as the average curve of the species. In the

second approach, we performed the growth trajectory of each species using the mean ARI, by

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fitting the locally weighted scatterplot smoothing (LOESS; Cleveland, 1979). Statistical analyses
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and fit curve were performed using the base package of R version 3.1.3 (R Core Team, 2015).
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Results

Tree ring markers, analysis of cambial wounding and dating scars

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Annual tree rings were found in seven species. This means that two tree rings were found in
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the secondary xylem produced subsequently the scar resulting from cambial injury (Fig. 3 e, h, k, n,

q, t, w). In Aspidosperma polyneuron, it was not possible to recognize cambial wounding scars in
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the material sampled, preventing the cambial wounding analysis.

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Regarding the distinctiveness of the tree rings, Alchornea glandulosa, Aspidosperma

polyneuron, Cedrela fissilis and Chrysophyllum gonocarpum showed the best distinction of
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boundaries. By contrast, Cabralea canjerana, Croton floribundus, Prunus myrtifolia and Trichilia

claussenii had slightly distinct tree rings boundaries.

Aspidosperma polyneuron showed tree ring boundaries marked by thick-walled and radially

flattened latewood fibers in the latewood versus thin-walled earlywood fibers (Fig. 3 a,b);
 9

eventually, marginal parenchyma bands were associated (Fig. 3 a). Alchornea glandulosa (Fig. 3

c,d) and Croton floribundus (Fig. 3 f,g) showed tree ring boundaries marked by thick-walled and

radially flattened latewood fibers in the latewood versus thin-walled earlywood fibers.

Tree ring boundaries in Cabralea canjerana were marked by a fiber zone; eventually,

marginal parenchyma bands at the beginning of the earlywood were associated (Fig. 3 i,j). Cedrela

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fissilis had semi-porous ring, with a gradual decrease in vessels diameter from earlywood to

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latewood, in combination with marginal parenchyma band (Fig. 3 l,m). Trichilia claussenii (Fig. 3

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o,p) and Prunus myrtifolia (Fig. 3 r,s) showed tree rings marked by marginal parenchyma.

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Chrysophyllum gonocarpum showed tree ring boundaries marked by a distinct fiber zone in

latewood, where axial parenchyma bands were absent (Fig. 3 u,v).

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False rings
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Seven species showed false rings. Alchornea glandulosa (Fig. 3c), Croton floribundus (Fig.
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3f) and Chrysophyllum gonocarpum (Fig. 3u,w) had false rings characterized by bands of latewood-

like cells within the true rings, as a result of thick-walled fibers. In Cabralea canjerana (Fig. 3i),
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Trichilia claussenii (Fig. 3o) and Prunus myrtifolia (Fig. 3r) narrow bands of axial parenchyma
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were produced within the true rings, likely being confluent paratracheal parenchyma. Cedrela

fissilis had false rings characterized by axial parenchyma bands of different widths, that can be
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associated with vessels or with resin canals, produced within the tree rings (Fig. 3l,n).
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Radial growth dynamics: dendrochronological analysis and tree ring widths

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All species had low EPS values (Table 2), but considering the correlations between the series,

Cedrela fissilis and Chrysophyllum gonocarpum had good cross-dating (Fig. 4; Table 2). The

remaining species had low correlations among the radial series (Table 2).
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The age of the studied trees varied considerably (Table 3; Fig. 4), and the trees average age

was approximately 70 years in Aspidosperma polyneuron; 66 years in Alchornea glandulosa; 51

years in Croton floribundus; 29 years in Cabralea canjerana; 45 years in Cedrela fissilis; 37 years

in Trichilia claussenii; 33 years in Prunus myrtifolia; and 53 years in Chrysophyllum gonocarpum.

The maximum ages ranged between 39 and 96 years, respectively, in Cabralea canjerana and

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Aspidosperma polyneuron (Table 3). Aspidosperma polyneuron and Chrysophyllum gonocarpum

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had the oldest trees, at 96 and 94 years, respectively (Fig. 4; Table 3).

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Regarding tree ring widths of the species, the mean ARI was 2.8 mm and the CRI 127 mm.

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Cabralea canjerana had the highest ARI and Aspidosperma polyneuron and Trichilia claussenii

had the lowest ARI (Table 3; Appendix 1). As for CRI, Alchornea glandulosa had the highest value

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and Trichilia claussenii the lowest CRI (Fig. 5; Table 3). We observed variation in intraspecific
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growth rates. Alchornea glandulosa, Cabralea canjerana, Cedrela fissilis and Chrysophyllum
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gonocarpum had trees with high and low growth rates (Fig. 5). In contrast, Aspidosperma
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polyneuron, Croton floribundus, Trichilia claussenii and Prunus myrtifolia had trees growing at

similar rates to each other (Fig. 5).

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The ARI varied over the years, resulting in different growth trajectories (Fig. 6). The
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trajectory showed by Alchornea glandulosa, Croton floribundus, Cedrela fissilis, Prunus myrtifolia

and Chrysophyllum gonocarpum, outlined an initial period of growth rate increase, followed by a
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period of growth reduction (Fig. 6). This period of growth rate reduction started at approximately
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50 years in Alchornea glandulosa, 40 years in Croton floribundus and Cedrela fissilis, 25 years in

Prunus myrtifolia and 30 years in Chrysophyllum gonocarpum (Fig. 6). The trajectory observed in
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Aspidosperma polyneuron and Cabralea canjerana showed an increase in the growth rates over the

years (Fig. 6). The trajectory exhibited by Trichilia claussenii showed a steady growth trend in the

first 17 years, followed by a period of a considerable increase in the growth rate, and a subsequent

period of steady to reduction in growth from the age of 30 years (Fig. 6).
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Discussion

Although tree-rings distinctiveness varied among the studied species, it was possible to

recognize the tree-rings boundaries in all studied species. The variation in fibers wall thickness

between the latewood and earlywood and the presence of marginal parenchyma were the most

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common features that defined the tree-ring boundaries, confirming they are typical anatomical

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markers of Neotropical species (Worbes, 1989; Alves and Angyalossy-Alfonso, 2000; Callado et

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al., 2001b; Marcati et al., 2006b; Shimamoto et al., 2016; Santos-Silva et al., 2017). Furthermore,

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some species showed combinations of tree ring markers, and these anatomical features improve the

identification of tree ring boundaries in tropical species (Roig, 2000; Vetter, 2000).

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Except for Croton floribundus, all deciduous or semi-deciduous species had better distinction
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of the ring boundaries observed macroscopically than evergreen species according to their thick-
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walled fibers in latewood, marginal parenchyma, vessels with different diameters along the same
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ring, and fiber zone. This relationship has already been reported (Worbes, 1999; Callado et al.,

2001b; Tetemke et al., 2016) and can be related to cambial dormancy, resulting in more evident tree
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rings (Worbes, 1999). In this case, shedding leaves during the unfavorable season is a mechanism to
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avoid excessive water loss during drought (Pallardy and Rhoads, 1993), and no assimilation and

transpiration may occur (Givnish, 2002), so growth is limited. Regarding Croton floribundus,
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although some of the leaves are shed and a reduction in cambial activity could occur, this species
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seemed to be plastic, showing a relatively constant growth curve (obtained by dendrometers) even

during the dry season (Blagitz et al., 2016), resulting in slightly distinct tree rings.
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The evergreen species Cabralea canjerana, Prunus myrtifolia and Trichilia claussenii

showed slightly distinct tree rings. In these species, retaining their leaves throughout the year can

provide a longer period of photosynthetic activity, even in the unfavorable season (Givnish, 2002),
 12

providing resources for cambial activity. Thus, growth in evergreen species can be constantly

maintained, reflected in slightly distinct or indistinct tree rings.

We also confirmed the annual formation of tree rings in all species, except for Aspidosperma

polyneuron where for technical reasons, it was not possible to recognize cambial wounding scars in

the sampled material. However, annual tree rings have been reported before for Aspidosperma

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polyneuron in previous analyses of cambial wounding (Lisi et al., 2008; Jímenez, 2017). Annual

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tree rings indicate that these species are useful for dendrochronological studies at the Mata dos

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Godoy State Park. Annual tree rings were also described for different species in a tropical seasonal

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semi-deciduous forest, and, in this case, the lower water availability during the dry season was

considered the only driving of the annual tree-rings formation (Lisi et al., 2008). However, for the

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species from the seasonal semi-deciduous forest located in the transition zone between tropical and
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subtropical climates, not only the reduction of rainfall, but lower temperatures and a shorter
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photoperiod were correlated to the reduction of stem growth, and probably tree ring marking
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(Blagitz et al., 2016). Thus, we must consider a context that involves the seasonality of multiple

environmental factors in the annual tree ring formation of the studied species.
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Intrinsic factors may also be involved in tree ring formation in the studied species. Cabralea
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canjerana (Shimamoto et al., 2016) and Cedrela fissilis (Andreacci et al., 2017) showed seasonality

of stem growth and formed tree rings in tropical rainforests, where no marked dry season occurs. In
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both studies, these processes were associated with foliar phenology. Although leaf sprouting and
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also radial growth can be triggered by high temperature and day length, they had a conservative

nature, since a seasonality of development (e.g. stem growth and phenology phases) occurred even
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under wet conditions (Andreacci et al., 2017). It suggests cambial activity and tree ring formation

are genetically fixed in Cabralea canjerana and Cedrela fissilis. Differently, indistinct tree rings

were described for Aspidosperma polyneuron, Cabralea canjerana (Tomazello Filho et al., 2004)

and Alchornea glandulosa (Alves and Angyalossy-Alfonso, 2000) in seasonal environments, such
 13

as the seasonal semideciduous forest. These species-distinct responses in different habitats require

tree ring studies in different tropical environments.

False rings were found within true tree rings. Bands of thick-walled fibers and narrow

parenchyma bands, that were observed in the species studied, facilitated the identification of false

rings, as predicted by de Micco et al. (2016). As false ring formation is usually linked to

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fluctuations in climatic conditions (Venegas-González et al., 2015; Baker et al., 2017), and since

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droughts at the beginning of the growing season can promote false ring formation in seasonal

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climates (Wimmer et al., 2000), the false ring formation in the wood of species in the seasonal

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semi-deciduous forest may be related to reduced rainfall during the growing season, the so-called

“veranicos”. This is a period of drought accompanied by intense heat and insolation and low

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relative humidity within the rainy season, and is frequent in the region of the study site (Bernardes
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et al., 1988). In these environmental conditions, increased evapotranspiration rates can lead to a
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reduction in cambial activity, producing latewood-like cells, observed as thick-walled fibers and
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bands of axial parenchyma (which would be similar to the marginal parenchyma bands). In addition

to the ecological considerations of false rings, their detection and characterization will facilitate the
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correct demarcation of growth boundaries and their analyses in further dendrochronology studies.
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Regarding the cross-dating analyses, significant series intercorrelation suggests that a

common factor could be driving stem growth, so Cedrela fissilis and Chrysophyllum gonocarpum
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show potential to be used in dendrochronological studies in the seasonal semi-deciduous forest. In

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fact, Cedrela fissilis was widely used in dendrochronological studies in other areas (Dünisch, 2005;

Cusatis et al., 2008; Andreacci et al., 2014; Paredes-Villanueva et al., 2016; Barbosa et al., 2018;
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Pereira et al.; 2018), and climatic factors such as temperature, rainfall, and local conditions are

involved in the radial growth of this species. With the purpose of new insights in Dendrochronology

in the neotropics, Chrysophyllum gonocarpum is a recommended species considering the significant

series intercorrelation and the best tree-ring distinctiveness. Among those species that did not have
 14

significant correlations in cross-dating, Cabralea canjerana, Croton floribundus, Prunus myrtifolia

and Trichilia claussenii showed slightly distinct tree rings, which can promote marking errors. In

addition, tree ring analysis in increment cores that represent small areas of the stem in all species

can increase the probability of erroneous tree ring marking reflecting the low series intercorrelation.

However, these species should not be totally rejected in dendrochronological studies, since they

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form annual tree rings. Additionally, some chronologies have been performed in Brazil for

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Aspidosperma polyneuron (Longhi-Santos, 2017), another species that did not have significant

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correlations in cross-dating, and complementary methodologies, such as X-ray wood densitometry

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(Jacquin et al., 2017), or an analysis in a cross-sectional surface of at least 5 cm (Stahle et al., 1999)

can improve cross-dating of these species.

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Our results indicate early secondary successional species (Alchornea glandulosa, Croton
N
floribundus, Cabralea canjerana and Prunus myrtifolia) tend to have higher ARI, whereas late
A
secondary successional species (Aspidosperma polyneuron, Cedrela fissilis, Trichilia claussenii and
M

Chrysophyllum gonocarpum) tend to have the lower ARI. This explains the succession dynamics,

since growth rate is an important factor in the distinction of ecological groups, and early secondary
ED

species generally have high growth rates, while late secondary species have low growth rates
PT

(Baker et al., 2003; Worbes et al., 2003). Regarding CRI, since the values obtained (Table 3) are

results of the sum of tree ring widths over the years, it also can be related to the longevity of
E

individuals, and not necessarily to the annual growth rates. For example, Aspidosperma polyneuron
CC

had a low ARI but a high CRI, because the sampled individuals were long-lived trees. However, the

cumulative radial increment over the years (Fig. 5) shows the slope of the mean curve is
A

proportional to the annual growth rates, so early secondary species tend to have a steeper slope than

the late secondary ones (Schöngart, 2008; Barbosa et al., 2018).

The high radial growth rate variation observed in Alchornea glandulosa, Cabralea canjerana,

Cedrela fissilis and Chrysophyllum gonocarpum indicates heterogeneity of growth between them
 15

(Costa et al., 2015), and may be associated with site-specific differences, mainly light availability

(Brienen et al., 2006; Schöngart et al., 2015), soil characteristics (Cardoso et al., 2012), individual

features such as crown area (Brienen et al., 2006); and genetic structure variability (Housset et al.,

2016). In this same line of reasoning, the lower variation in the radial growth rate observed among

trees of the other Aspidosperma polyneuron, Croton floribundus, Trichilia claussenii and Prunus

T
myrtifolia is associated with homogeneous conditions to growth or similarity of intrinsic factors,

IP
such crown area or genetic characteristics of the trees. In addition, the lowest radial growth

R
variation, as well as the lowest growth rates shown by Aspidosperma polyneuron and Trichilia

SC
claussenii, are typical of trees species with high wood density (Schöngart, 2008; Barbosa et al.,

2018; wood density: A. polyneuron = 0.76 g.cm-1 and T. claussenii = 0.71 g.cm-1; see Nascimento,

U
2013). Moreover, this same tendency has been found in Aspidosperma species (Barbosa et al.,
N
2018).
A
The studied species showed different growth trajectories, and the curve observed in most
M

species (Alchornea glandulosa, Croton floribundus, Cedrela fissilis, Prunus myrtifolia,

Chrysophyllum gonocarpum) showed a reduction in growth after a period of increasing growth.

ED

This trajectory may be an age-related trend of the trees (Fritts, 1976; Schweingruber, 1988), which
PT

predicts high growth rates at the beginning of life and a growth reduction over time related to the

senescence of individuals. Due to morphological and physiological adjustments related to

E

advancing years, e.g. decreases in leaf area and in photosynthetic rates, a reduction in the available
CC

resources for growth in these trees may occur (see Carrer and Urbinati, 2004; Sala et al., 2012).

Also, the decrease of tree rings widths in the radial samples naturally occur due to the volumetric
A

limitation caused by the high amount of wood that would be deposited if the growth rings of the

same width were continuously deposited (Fritts, 1976). It must be noted that the approximate ages

at which the species started to reduce their growth rates varied among species, and was determined
 16

by one or two long-lived individuals (Fig. 5). Therefore, the timing of reduced growth rates is not

necessarily a trend of the species, but is a tendency of these individuals.

Aspidosperma polyneuron and Cabralea canjerana demonstrated an increase in radial growth

rate over time, and this growth curve may be representing the onset of the development in the

pattern previously described. In other words, these trees probably not yet reached senescence, when

T
then, begin to reduce growth. This is supported by the young ages of sampled trees in Cabralea

IP
canjerana and by the growth reduction of Aspidosperma polyneuron trees from the 120 years

R
(Godoy-Veiga et al., 2018). So, probably, we analyzed very young trees which growth patterns may

SC
reflect these trajectories.

Among the studied species, Trichilia claussenii showed the most variable growth trajectory.

U
The steady growth in the first years can be related to the seedlings initial establishment, when the
N
resources are allocated to root biomass development (Modrzyński et al., 2015). As plants grow, they
A
generally invest in the aerial part development, and for that, an increase in light demand is
M

necessary (Valladares et al., 2016). Understorey tree species, such as Trichilia claussenii in the

seasonal semi-deciduous forest (Silva and Soares Silva, 2000), would have difficult to capture light,
ED

however, this species showed a deeper crown in the juvenile stage (Hertel, 2014), which increases
PT

the lateral light interception in the understorey (Sterck et al., 2001). So, the resource supply is

available, reflecting in the increased stem growth rates in the subsequent years of Trichilia
E

claussenii trajectory. The final period of steady to the reduction in growth rates can represent the
CC

reproductive stage when the resources would be reallocated to the development of structures for

reproduction, and/or to senescence of individuals when physiological adjustments lead to negative

A

impacts on resources necessary for growth. As expected, the evaluation of radial growth trajectories

using tree rings allowed for an interpretation of the life history of the tree. Furthermore, these

findings show evidence of forest dynamics, when the full development of some trees are evaluated

and a period of senescence in others are verified.

 17

Conclusions

Seven tree species from the seasonal semi-deciduous forest in southern Brazil form annual

tree rings demarcated by different anatomical markers. The distinctness of these tree rings is related

to the leaf fall patterns of the species. In addition, false rings are formed, and sometimes they are

T
anatomically distinct from true rings. These findings are essential for further dendrochronological

IP
studies in the region, and considering the cross-dating analysis and tree-ring distinctiveness,

R
Chrysophyllum gonocarpum is a recommended species. The studied species showed different radial

SC
growth trajectories when evaluating tree ring widths over the years. However, no consistent pattern

of the growth trajectories was observed among species that belong to the same successional groups,

U
so they contribute to the explanation of the particular life history of each species.
N
A
Acknowledgements
M

This study was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior -

Brasil (CAPES) - Finance Code 001; and Fundação Araucária (Agreement no. 419/2009; Protocol
ED

no. 15381). M. B. received grants from Conselho Nacional de Desenvolvimento Científico e

PT

Tecnológico (CNPq) for MSc. thesis

E

Declarations of interest: none.

CC
A

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Figure captions

Fig. 1. Location map of the studied area.

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Fig. 2. The mean monthly precipitation, temperature and photoperiod for Londrina, Paraná, Brazil.

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Precipitation and temperature were obtained based on annual means from 1976 to 2011 (data

source: Instituto Agronômico do Paraná - IAPAR) and the monthly photoperiod was calculated

following the indications of Forsythe et al. (1995).

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Fig. 3. Macroscopic (a, c, f, i, l, o, r, u) and microscopic (b, d, g, j, m, p, s, v) wood transverse

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sections showing tree rings and macroscopic wood transverse sections (e, h, k, n, q, t, w) showing
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the tree rings equivalent to the years 2010 and 2011 formed after the cambial wounding scar (*) of

tree species from the seasonal semi-deciduous forest, southern Brazil. Aspidosperma polyneuron
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(a,b); Alchornea glandulosa (c-e); Croton floribundus (f-h); Cabralea canjerana (i-k); Cedrela

fissilis (l-n); Trichilia clausseni (o-q); Prunus myrtifolia (r-t); Chrysophyllum gonocarpum (u-w).

Arrows indicate the tree ring boundaries; arrowheads indicate false tree rings; rc = resin canals.

Scale bars of macroscopic sections = 2 mm and of microscopic sections = 100 µm.

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Fig. 4. Dated individual tree ring-width index series (grey lines) and mean index standard series
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(black lines) of species from seasonal semi-deciduous forest, southern Brazil.

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Fig. 5. Cumulative radial increment over the years of species from seasonal semi-deciduous forest,

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southern Brazil. Gray dotted lines are the individual curves; black solid lines are the average curves
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of the species; and vertical bars indicate the standard deviation.
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Fig. 6. Lifetime growth trajectories of species from seasonal semi-deciduous forest, southern Brazil

originated from the smoothed mean curve of the mean annual radial increment of each species.

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Appendix 1. Dated individual series of tree-ring-width of species from seasonal semi-deciduous forest,
southern Brazil.

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Tables
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Table 1. Number of sampled individuals (n), mean diameter at breast height ± standard deviation

(DBH), mean height ± standard deviation (H), mean age ± standard deviation and ecological

features of the studied species naturally growing in a seasonal semi-deciduous forest, southern

Brazil.

Species n DBH (cm) H (m) Age Leaf fall Leaf fall Successional
pattern period1 category3
Apocynaceae

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Aspidosperma polyneuron Müll. 7 63.05 ± 15.47 ± 3.24 72.3 ± semi- Mar - Dez late

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Arg. 14.19 7.59 deciduous1 secondary
Euphorbiaceae
Alchornea glandulosa Poepp. 4 24.07 ± 11.77 ±1.23 69.5 ± semi- Jul - Nov initial

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22.81 9.26 deciduous1 secondary
Croton floribundus Spreng. 6 36.94 ± 12.52 ± 0.28 54.7 ± 4.1 semi- Jan - Dec initial
deciduous1

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6.80 secondary
Meliaceae
Cabralea canjerana (Vell.) Mart. 5 21.59 ± 13.55 ± 3.41 30.2 ± evergreen1 initial
11.23 3.89 secondary
Cedrela fissilis Vell. 7 58.91 ± 10.72 ± 2.34 44.7 ± 7.7 deciduous1 Feb – Jul late

Trichilia claussenii C. DC. 5

15.62
16.87 ± 9.6 ± 12.37
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37.7 ± evergreen1
secondary
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2.67 5.35 late
secondary
Rosaceae
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Prunus myrtifolia (L.) Urb. 4 44.90 ± 9.66 ± 1.77 33 ± 6.44 evergreen1 initial
13.44 secondary
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Sapotaceae
Chrysophyllum gonocarpum (Mart. 6 50.95 ± 12.49 ± 1.45 47.2 ± semi- May - Oct late
& Eichler ex Miq.) Engl. 10.16 6,18 deciduous2 secondary
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Perina (2011); 2 Bianchini et al. (2006) ; 3 Silva and Soares-Silva (2000)
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Table 2. Statistical description of tree rings cross-dating of tree species from a seasonal semi-

deciduous forest, southern Brazil.

Number of radial series Total of tree Series Critical EPS

Species (number of individuals) rings intercorrelation value
Before§ After§
Aspidosperma polyneuron 16 (7) 8 (5) 555 0.2 0.366 0.27
Alchornea glandulosa 10 (4) 9(4) 613 0.31 0.366 0.53
Croton floribundus 16 (6) 10 (5) 514 0.22 0.515 0.37

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Cabralea canjerana 11 (5) 9 (4) 277 0.24 0.515 0.71
Cedrela fissilis 22 (7) 10 (5) 393 0.38* 0.366 0.45

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Trichilia claussenii 10 (5) 6 (4) 226 0.31 0.515 0.49
Prunus myrtifolia 14 (4) 8 (4) 268 0.31 0.515 0.66

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Chrysophyllum 15 (6) 10 (6) 665 0.4* 0.366 0.57
gonocarpum

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The exclusion of radial series with low correlation; * Significant correlations between radial and master series.

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Table 3. Numbers of tree rings observed, mean annual radial increment (ARI) ± standard deviation

and mean cumulative radial increment (CRI) ± standard deviation of tree species from seasonal

semi-deciduous forest, southern Brazil. Different letters in the columns differ significantly by the

Tukey test (p < 0.05).

Number of rings
Species ARI (mm) CRI (mm)
Minimun Maximum

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Aspidosperma polyneuron 49 96 1.7 ± 0.2 c 126 ± 34 ab
Alchornea glandulosa 53 87 3.3 ± 1 ab 212 ± 59 a

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Croton floribundus 45 68 2.3 ± 0.2 bc 115 ± 9 ab
Cabralea canjerana 19 39 4.5 ± 1 a 131 ± 5 ab

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Cedrela fissilis 24 83 2.9 ± 1 bc 132 ± 84 ab
Trichilia claussenii 22 42 1.7 ± 0.3 bc 63 ± 18 b

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Prunus myrtifolia 25 52 3.4 ± 0.6 ab 108 ± 9 ab
Chrysophyllum gonocarpum 22 96 2.6 ± 0.9 bc 129 ± 55 ab
Mean 32.3 ± 70.1 ± 22.8 2.8 ± 0.8 127 ± 38
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