Xylem growth rings and leaf phenological patterns in tree species of a subtropical seasonal forest

ABSTRACT

Growth rings have been reported for several tropical species under seasonal precipitation regimes and have often been related to leaf phenology. We investigated growth ring distinctiveness, wood markers, and leaf shedding and flushing patterns of 16 tree species from a subtropical seasonal deciduous forest under abundant and well-distributed rainfall regime in southern Brazil. Distinct growth rings were found in 13 species, 10 of which presented clear anatomical boundaries. Seven species were deciduous, five semideciduous and four perennial. Leaf shedding peaked during winter and spring months for the deciduous species, while it peaked during spring and summer months for the perennial and semideciduous species. Leaf flushing peaked in spring and summer for all species. All the deciduous species exhibited growth rings with clear boundaries. Marginal parenchyma, associated or not with other anatomical markers, was present in deciduous species but was not present in species with other leaf shedding patterns. Growth rings in Allophylus edulis, Erythrina falcata, Jacaranda micrantha and Luehea divaricata were described for the first time. The presence of seasonal leaf phenological patterns and growth rings in most of the species suggests that seasonality of the photoperiod and/or temperature influence the development of trees in moist subtropical seasonal deciduous forests.

Keywords:
dendrochronology; phenology; seasonal deciduous forest; subtropical forest; tree rings; wood anatomy

Introduction

Growth rhythms in woody plants usually affect the morphology of their secondary tissues, forming radial anatomical patterns in the xylem, phloem and/or rhytidome known as growth layers or growth rings (Fahn et al. 1981; IAWA Committee 1964; Silva et al. 2019). Growth ring distinctness and periodicity are easier to detect in temperate and boreal floras, where most woody plants produce annual growth rings with conspicuous earlywood and latewood zones because lower temperatures and shorter daylengths toward the winter progressiveely reduce and prevent the mitotic activity of the vascular cambium and affect the differentiation of new cells (Fritts 1976; Schweingruber 2007).

Growth rings that do not follow this periodic and distinct pattern are generally more difficult to detect, especially in tropical floras. The identification of growth rings in taxa from tropical and subtropical regions has been hindered due to conceptual divergences from what is observed in high-latitude floras, which neither incorporate the great diversity of wood anatomy types seen in tropical floras nor their ecological and evolutionary drivers (Worbes 2002; Tarelkin et al. 2016; Silva et al. 2019). Although xylem growth rings in tropical trees were early recognized (see Worbes 2002), investigated and applied in specific disciplines, notably taxonomy, anatomy and dendrochronology (Stahle 1999; Alves & Angyalossy-Alfonso 2000; Callado et al. 2001b; Worbes 2002; Marcati et al. 2006a; Tarelkin et al. 2016; Silva et al. 2017), a definition of growth ring that integrates the anatomical diversity of growth ring distinctness, markers and causal factors of tropical species was only recently proposed (Silva et al. 2019).

Formation of conspicuous annual growth rings has been reported for hundreds of tropical species and attributed to seasonal changes in environmental conditions (Worbes 2002; Brienen et al. 2016; Schöngart et al. 2017), including rainfall in most regions (e.g., Worbes 1995; 1999; Brienen & Zuidema 2005; Marcati et al. 2006b) but also flooding in lowland plains (e.g., Worbes 1985; 1989; Callado et al. 2001a). Tropical taxa that reach subtropical belts find a contrasting climate environment, with more intense cold and frequent mild frosts in winter (Corlett 2013). In this zone, cambial activity is likely influenced by photoperiod and/or temperature, so that cell division and growth is stimulated by the longer and warmer days of summer (Jacoby 1989; Oliveira et al. 2009; Spathelf et al. 2010; Shimamoto et al. 2015; Kanieski et al. 2017; Reis-Ávila & Oliveira 2017). However, other combinations of formation rhythms and distinctness have also been reported for growth rings in tropical and subtropical plants (e.g., Jacoby 1989; Borchert 1999; Alves & Angyalossy-Alfonso 2000; Callado et al. 2001a; Tarelkin et al. 2016; Baker et al. 2017).

Wood formation is a process associated with other vegetative events in a plant because apical and lateral meristems share common and fundamental regulatory mechanisms (Risopatron et al. 2010; Immanen et al. 2016). Thus, growth ring formation and leaf shedding patterns are likely to be associated, as shown in temperate (e.g., Sass-Klassen et al. 2011; Takahashi et al. 2015; Guada et al. 2019) and tropical species (e.g., Borchert 1999; Callado et al. 2001b; Schöngart et al. 2002; Singh & Kushwaha 2005; Callado et al. 2013; Brienen et al. 2016). The cambial activity in deciduous and semideciduous tropical species generally accompanies leaf shedding and flushing, i.e., leaves are shed and the cambium becomes dormant during the dry season, while leaf flushing and cambium activation occur in the rainy season (Borchert 1999; Worbes 1999; Lisi et al. 2008; Marcati et al. 2006a; Callado et al. 2013).

Deciduous and semideciduous forests also occur under ever-wet climate conditions in subtropical belts, such as in southern Brazil (Veloso & Góes Filho 1982; IBGE 2012). In these forests, leaf phenological patterns are associated with seasonal variation in photoperiod and/or temperature, so that leaf shedding is concentrated in the period with shorter days and leaf flushing occurs when photoperiod increases again (Andreis et al. 2005; Athayde et al. 2009; Ferrera et al. 2017). In addition, growth ring formation in subtropical moist forests has been attributed to the same seasonal environmental drivers (Oliveira et al. 2009; Spathelf et al. 2010; Shimamoto et al. 2015; Kanieski et al. 2017; Reis-Ávila & Oliveira 2017; Blagitz et al. 2019).

Here, we adopt the broader concept of growth ring as defined by Silva et al. (2019) to assess and describe the macroscopic features of growth rings in 16 tree species from subtropical deciduous forest and verify relationships between growth ring occurrence and leaf phenological patterns. If subtropical climatic conditions affect the developmental rhythm of trees and/or if this rhythm is conserved in tropical taxa under subtropical conditions, we expect to find distinct growth rings in subtropical trees. Therefore, if leaf phenology is strongly associated with cambium activity, we expect different seasonal leaf phenological patterns to correspond with different incidence and/or anatomical definition of growth rings between species.

Materials and methods

Study area

The study was carried out in a fragment of seasonal deciduous forest in southern Brazil (state of Rio Grande do Sul), within the subtropical belt (Corlett 2013). Due to the mesothermal climatic character, the temperature presents pronounced annual oscillation, with hot summers and cold winters, while the annual rainfall regime has a well-balanced distribution, resulting in high and almost constant humidity throughout the year (Nimer 1989). In this region, the average minimum and maximum temperatures are around 13.7 ºC and 24.3 ºC respectively and the monthly average rainfall is 142.5 mm (IRGA 2017). Day length ranges from 10.13 h to 14.03 h according to the interactive observatory of the Observatório Nacional (ON 2018) (Fig. 1).

Figure 1
Climate diagram for the region of the study area. Data obtained from climatological averages (IRGA 2017).

In Rio Grande do Sul, the seasonal deciduous forest covers the Uruguay River Valley and the southern edge of the Serra Geral (IBGE 2012; Fig. 2). The seasonal deciduous forest is physiognomically defined by tree species that completely shed leaves in a given season of the year, resulting in 50 % or more of the canopy trees to be leafless in autumn and/or winter (Veloso & Góes Filho 1982; IBGE 2012). The seasonal deciduous forest in southern Brazil has been severely devastated since the arrival of European immigrants in 1824 (Rambo 1942) and now consists of fragments in various regeneration stages.

Figure 2
Map of study site location.

The study site is a seasonal deciduous forest fragment that is regenerating without major disturbances after clearcutting in the 1970s. It is located in the Municipality of Nova Petrópolis (29°23'57" S, 51°06'47" W) at an altitude of 170 m (Fig. 2).

Selection of species and preparation of wood samples

Eighty individuals from 16 species and 10 families were sampled in the study site (Tab. 1). The species were selected because they are widely distributed in areas of seasonal deciduous forest in Rio Grande do Sul (Reitz et al. 1988; Sobral et al. 2006) and are abundant in the study site. Five adult trees of each species were selected, preferably with rectilinear trunk and without apparent injuries to the stem and crown. The wood samples (two radial cores per tree) were collected from the trunk using a 5.1-mm-diameter increment borer at a height of 1.3 m from the ground. To complement the sample, we analyzed wood discs from recently cut down trees found in nearby sites or from samples in the xylotheque of Herbarium Anchieta that were collected in areas of seasonal deciduous forest in Rio Grande do Sul.

Table 1
Growth rings, marker type and leaf shedding pattern of 16 species from subtropical seasonal deciduous forest. Growth rings: DCB - distinct with clear boundaries, DFB - distinct with fuzzy boundaries, IND - indistinct. Marker type: A - absent, MP - marginal parenchyma, TW - thick-walled latewood fibers and thin-walled earlywood fibers, RF - radially flattened latewood fibers and radially elongated earlywood fibers, FB - fibrous band, SR - semi-porous ring. Leaf shedding pattern: DEC - deciduous, SDE - semideciduous, PER - perennial.

Taxa	Growth rings	Marker type	Leaf shedding pattern
BIGNONIACEAE
Jacaranda micrantha Cham.	DCB	MP, TW, RF	DEC
EUPHORBIACEAE
Alchornea triplinervia (Spreng.) Müll. Arg.	DFB	RF	SDE
ERYTROXILACEAE
Erythroxylum argentinum O.E. Schulz	IND	A	SDE
FABACEAE
Erythrina falcata Benth. Machaerium stipitatum (DC.) Vogel Parapiptadenia rigida (Benth.) Brenan	DCB DCB DCB	FB MP MP, TW, RF	DEC DEC DEC
LAURACEAE
Nectandra megapotamica (Spreng.) Mez	DCB	TW, RF	PER
Nectandra oppositifolia Nees & Mart. Ocotea puberula (Rich.) Nees	DFB DFB	TW, RF TW, RF	PER SDE
MALVACEAE
Luehea divaricata Mart.	DCB	MP	DEC
MELIACEAE
Cabralea canjerana (Vell.) Mart Cedrela fissilis Vell.	IND DCB	A MP, SR	SDE DEC
MORACEAE
Maclura tinctoria (L.) D. Don. ex Steud.	DCB	MP	DEC
SALICACEAE
Casearia sylvestris Sw.	IND	A	PER
SAPINDACEAE
Allophylus edulis (A. St. Hil., A. Juss. & Cambess.) Hieron. ex Niederl. Cupania vernalis Cambess.	DCB DCB	TW, RF TW, RF	SDE PER

The cores were fixed on wooden supports, identified, dried and polished with sandpaper (grain 80 to 2000) according to the usual methodology for dendrochronological analysis. The disks were polished in the same way. Possible macroscopic features related to the delimitation of growth rings were inspected in the transverse section of the samples under 10 x and 40 x magnifications using a stereomicroscope. Digital photographs of the wood samples were taken using an AxionCam ERc5s camera attached to a Stemi SV6 stereomicroscope under 10 x and 40 x magnifications.

Cell arrangement and anatomical markers of the rings were described according to the IAWA Committee (1989). The classification of the presence of growth rings followed, with adaptations, the proposal of Silva et al. (2017) and we considered the pattern seen in most samples obtained from each species. The rings were classified as: indistinct, when no pattern of radial anatomical variation was observed; distinct with clear boundaries, when there was radial anatomical variation showing growth cycles, usually delimited by abrupt transitions between adjacent growth rings; distinct with fuzzy boundaries, when there was radial anatomical variation showing growth cycles, usually delimited by gradual transitions between adjacent growth rings.

Phenological data were obtained from the observation of 10 to 15 trees of each species. All trees had good crown visibility (Morellato et al. 2010) and were in seasonal deciduous forest fragments located within a 30-km-radius from the study site, in altitudes from 30 m to 500 m. The selected trees were monthly monitored between December 2017 to November 2018. Leaf shedding, flushing and leaf cover were assessed through direct observation and binoculars. The quantification of the leaf phenological events was performed using the Fournier intensity index (Fournier 1974). Based on the observations, the species were classified as: deciduous, when individuals were found leafless in one or more observations; semideciduous (brevideciduous), when they presented leaf shedding with partial canopy suppression and concomitant flushing of new leaves; and perennial (evergreen), when individuals presented continuous leaf replacement throughout the year, without total or partial canopy suppression (adapted from Morellato et al. 1989; Borchert 1999).

Results

The macroscopic anatomical analysis showed that 13 out of 16 species presented distinct growth rings (Tab. 1). Among these, 10 presented distinct growth rings with clear boundaries (63 %) and three presented distinct growth rings with fuzzy boundaries (18 %). Three species showed indistinct growth rings (19 %).

The growth-ring descriptions are presented by species and grouped by family, with emphasis on the anatomical traits that define the boundaries.

Bignoniaceae

Jacaranda micrantha: Growth rings are distinct, with clear boundaries defined by marginal parenchyma and variation in fiber shape and wall thickness (Figs. 3, 4). The boundaries are marked by an abrupt transition zone between radially-flattened thick-walled fibers (typical of latewood) and radially-elongated thin-walled fibers (typical of earlywood), and marginal parenchyma band (Figs. 3A, 4A).

Figure 3
Macroscopic view of transverse xylem sections of tree species from subtropical seasonal deciduous forest. Arrows indicate growth ring boundaries. Magnification: 10x. (A) Jacaranda micrantha; (B) Alchornea triplinervia; (C) Erythroxylum argentinum; (D) Erythrina falcata; (E) Machaerium stipitatum; (F) Parapiptadenia rigida; (G) Nectandra megapotamica; (H) Nectandra oppositifolia. Scale: 0.5 mm

Figure 4
Detail of growth ring with clear boundaries for tree species from subtropical seasonal deciduous forest. Arrows indicate growth ring boundaries. Magnification: 40x. (A) Jacaranda micrantha; (B) Machaerium stipitatum; (C) Parapiptadenia rigida; (D) Nectandra megapotamica; (E) Luehea divaricata; (F) Cedrela fissilis; (G) Maclura tinctoria; (H) Allophylus edulis; (I) Cupania vernalis. Scale: 2 mm

Euphorbiaceae

Alchornea triplinervia: Growth rings are distinct, with fuzzy boundaries defined by variation in fiber shape. The boundaries are marked by a smooth transition zone in the shape of the fibers, which become successively flatter in the radial plane of latewood and then gradually return to the radially and more elongated shape in earlywood (Fig. 3B).

Erytroxilaceae

Erythroxylum argentinum: indistinct growth rings (Fig. 3C).

Fabaceae

Erythrina falcata: Growth rings are distinct, with clear boundaries marked by a continuous fibrous band that is wider than the other bands, and macroscopically characterized as a darker band. Growth-ring boundaries are visible in transverse discs of the trunk but it was not possible to define them in transverse core samples because the continuous dark-colored bands of the growth ring boundaries cannot be differentiated from discontinuous fibrous zones within the growth rings in narrow core samples (Fig. 3D).

Machaerium stipitatum: Growth rings are distinct, with clear boundaries marked by marginal parenchyma. The latewood has axial parenchyma, while the earlywood has winged-aliform axial parenchyma (Figs. 3E, 4B). The innermost growth rings may also have fiber-wall thickening in the latewood.

Parapiptadenia rigida: Growth rings are distinct, with clear boundaries defined by a marginal parenchyma layer and variation in fiber shape and wall thickness between latewood and earlywood. Smaller-diameter vessels are present in latewood (Fig.3F, 4C). Sometimes, the abrupt transition between radially-flattened thick-walled fibers (latewood) and radially-elongated thin-walled fibers (earlywood) was absent.

Lauraceae

Nectandra megapotamica: Growth rings are distinct, with clear boundaries defined by variation in fiber shape and wall thickness. The boundaries are marked by an abrupt transition zone between radially-flattened thick-walled fibers (latewood) and radially-elongated thin-walled fibers (earlywood) (Figs. 3G, 4D).

Nectandra oppositifolia: Growth rings are distinct, with fuzzy boundaries defined by variation in fiber shape and wall thickness. The boundaries are marked by a smooth transition zone between radially-flattened thick-walled fibers (latewood) and radially-elongated thin-walled fibers (earlywood) (Fig. 3H).

Ocotea puberula: Growth rings are distinct, with fuzzy boundaries defined by variation in fiber shape and wall thickness (Fig. 5). The boundaries are marked by a smooth transition zone between radially-flattened thick-walled fibers (latewood) and radially-elongated thin-walled fibers (earlywood) (Fig. 5A).

Figure 5
Macroscopic view of transverse xylem sections of tree species from subtropical seasonal deciduous forest. Arrows indicate growth ring boundaries. Magnification: 10x. (A) Ocotea puberula; (B) Luehea divaricata; (C) Cabralea canjerana; (D) Cedrela fissilis; (E) Maclura tinctoria; (F) Casearia sylvestris; (G) Allophylus edulis; (H) Cupania vernalis. Scale: 0.5 mm

Malvaceae

Luehea divaricata: Growth rings are distinct, with clear boundaries marked by a conspicuous marginal parenchyma band. There is a greater incidence of diffuse axial parenchyma forming aggregates in earlywood compared to latewood (Figs. 5B, 4E).

Meliaceae

Cabralea canjerana: indistinct growth rings (Fig. 5C).

Cedrela fissilis: Growth rings are distinct, with clear boundaries defined by conspicuous marginal parenchyma and semi-porous ring. Larger vessels are present in the earlywood and smaller vessels are present in the latewood (Figs. 5D, 4F).

Moraceae

Maclura tinctoria: Growth rings are distinct, with clear boundaries defined by continuous axial parenchyma in a seemingly marginal band (Figs. 5E, 4G). Growth-ring boundaries are visible in transverse discs of the trunk but it was not possible to define them in transverse core samples because the continuous axial parenchyma bands of growth-ring boundaries cannot be differentiated from discontinuous axial parenchyma bands occurring within the growth rings. Growth rings can be indistinct in the sapwood due to a lack of contrast between parenchyma and fibers.

Salicaceae

Casearia sylvestris: Indistinct growth rings (Fig. 5F).

Sapindaceae

Allophylus edulis: Growth rings are distinct, with clear boundaries defined by variation in fiber shape and wall thickness. The boundaries are marked by an abrupt transition between radially-flattened thick-walled fibers (latewood) and radially-elongated thin-walled fibers (earlywood) (Figs. 5G, 4H).

Cupania vernalis: Growth rings are distinct, with clear boundaries defined by varying fiber shape and wall thickness. The boundaries are marked by an abrupt transition between radially-flattened thick-walled fibers (typical of latewood) and radially-elongated thin-walled fibers (typical of earlywood) (Figs. 5H, 4I).

Regarding leaf-shedding patterns, seven species were deciduous, five were semideciduous and four were perennial (Tab. 1). All species presented a period of more intense leaf loss and replacement in the year of observation and a continuous or discontinuous occurrence of the leaf phenological events (Fig. 6).

Figure 6
(A) Leaf shedding and flushing phenophases of tree species from subtropical seasonal deciduous forest. The lines in the graph indicate the occurrence of the phenophases and the markers indicate the months of greatest event intensity (Fournier Index). (B) Climate diagram for the study area in the period between December 2017 and November 2018. Right axis: photoperiod (h/light/day) and mean temperature; left axis: accumulated monthly rain.

Perennial and semideciduous species showed continuous leaf shedding and flushing through the year, while these phenophases were discontinuous in deciduous species. In E. falcata, all individuals presented discrete periods of leaf shedding and flushing but these phenophases were asynchronous among the trees and, thus, continuous at the population level. Leaf-shedding peaks occurred in late winter or early spring in deciduous species, and in spring or early summer in perennial and semideciduous species. Leaf-flushing peaks occurred in spring or early summer (except in A. edulis) (Fig. 6).

All deciduous species had distinct growth rings with clear boundaries (Tab. 1, Fig. 7). A greater proportion of species with distinct growth rings with clear boundaries was observed in perennial species than in semideciduous species (Fig. 7). Species with indistinct or fuzzy-boundary growth rings seem to have a shorter leaf-exchange period (the time-lapse between the peaks of leaf shedding and leaf flushing) than species showing growth rings with clear boundaries (Fig. 8).

Figure 7
Number of deciduous, semideciduous and perennial species that present growth rings with different degrees of distinctiveness for trees from a subtropical seasonal forest. Growth rings: DCB - distinct with clear boundaries, DFB - distinct with fuzzy boundaries, IND - indistinct.

Figure 8
Leaf exchange time in tree species that present growth rings with different degrees of distinctiveness in a subtropical seasonal forest. Growth rings: DCB - distinct with clear boundaries, DFB - distinct with fuzzy boundaries, IND - indistinct.

Discussion

Distinct growth rings had already been recorded in subtropical species in southern Brazil (Oliveira et al. 2009; Spathelf et al. 2010; Shimamoto et al. 2015; Andreacci et al. 2017; Kanieski et al. 2017; Reis-Ávila & Oliveira 2017; Granato-Souza et al. 2018; Blagitz et al. 2019). In this study, distinct growth rings were also observed in most studied species, being absent only in C. sylvestris, C. canjerana and E. argentinum. This result points to a rhythmic cambium activity in the tree species that is possibly triggered by variations in temperature and/or photoperiod (Morales et al. 2004; Yanez-Espinosa et al. 2006; Figueiredo-Filho et al. 2008; Oliveira et al. 2009; Kanieski et al. 2012; 2013) since regular intra-annual periods of water stress are not observed in this subtropical region (Nimer 1989; Peel et al. 2007).

The presence of distinct growth rings is not directly related to phenology, as rings were observed in species with different leaf-shedding patterns. However, indistinct rings were only observed among semideciduous and perennial species, indicating that the episodic leafless phase (deciduous phenology) is strongly associated with the presence of distinct growth rings in subtropical species (Fig. 7).

In perennial or semi-deciduous species, the greatest intensity of leaf shedding and leaf flushing accompanied the increase in temperature and photoperiod in spring and summer. These species keep their leaves during the annual period of lower temperature and shorter day length and undergo a quick (semideciduous) or a partial replacement (perennial) of the crown when the climatic conditions become more favorable for metabolic activity. The deciduous species showed intense leaf shedding during winter and early spring, with total crown loss in most individuals, and flushing between spring and summer (Fig. 6). Crown loss in deciduous species accompanied the decrease in photoperiod and temperature in the study region. Leaf shedding is a phenological strategy for these species to support physiological drought caused by the decrease in temperature in winter, which causes a stop in growth and photosynthesis (Givnish 2002). Leaf flushing occurs when the length of the day and the temperature increase, leading to photosynthetic activity and growth. Crown reconstitution/replacement after a period with low or no photosynthetic activity results in the resumption of growth, anatomically marking the cellular elements of the earlywood (Fahn et al 1981) and allowing the visualization of the ring boundaries.

In deciduous species, growth-ring markers are defined by marginal parenchyma (except E. falcata) accompanied or not by fiber wall thickness and/or shape or even a semi-porous ring. In perennial or semi-deciduous species, when present, growth rings are defined by wall thickness and shape of the latewood fibers. The species that showed distinct growth rings had marginal parenchyma bands and thickness and/or variation in the fiber shape in the latewood as main markers. These results from subtropical species are similar to the ones described for tropical species where the most common markers of the growth rings are wall thickening and radial flattening of the fibers, which are often associated with the marginal parenchyma (Worbes 1989; Roig 2000). The marginal parenchyma more precisely defines the limit of a growth ring (Lisi et al. 2008) and was the marker observed in most species of the study that showed distinct rings with clear boundaries.

Deciduous species tend to show a better distinctness of the growth rings (Coster 1927; 1928; Tomlinson & Logman 1981; Callado et al. 2001a; Shimamoto et al. 2015; Blagitz et al. 2019) resulting from cambial dormancy caused by leaf loss and consequent reduction in metabolism during the unfavorable period. In tropical regions, the cambial activity of C. fissilis, a deciduous tree, is related to phenology and precipitation. Cambial dormancy occurs during leaf shedding in the dry season and earlywood formation occurs along with leaf flushing during the rainy season (Marcati et al. 2006b). The leaf phenophases presented by C. fissilis in subtropical climatic conditions show a relationship between leaf renewal and increase in photoperiod, and leaf shedding and reduction and photoperiod. In the month following the reduction of the day length by approximately 30 minutes (January) from its maximum (December), senescence and leaf shedding begin, and in the month following the increase of day length by about 2 h (September) from its minimum length (June), leaf flushing begins (Fig. 6). The presence of distinct growth rings combined with this phenological pattern observed in the species reinforce the idea that, in subtropical climatic conditions, day length plays an important role as a seasonal determinant of growth (Andreacci et al. 2017) like that observed in temperate deciduous species (Fu et al. 2019).

Although the presence of distinct growth-ring boundaries is expected in species that have a period of absence of leaves, it is common for species with this phenological leaf pattern not to present distinct growth rings (Coster 1927; 1928; Worbes 1999; Venugopal & Liangkuwang 2007), so that a clear relationship between leaf shedding patterns and distinct tree-ring boundaries was not always observed (Marcati et al. 2006a). However, in this study, all deciduous species showed distinct growth rings with clear boundaries (Fig. 7). This result agrees with previous results (Coster 1927; 1928; Tomlinson & Logman 1981; Callado et al. 2001a; Shimamoto et al. 2015; Blagitz et al. 2019) and indicates that leaf-shedding patterns are linked to wood formation in trees from tropical and subtropical regions and is a good indicator for the distinctness of growth rings. Complementing this idea, it is interesting to note that all species with indistinct growth rings had a short leaf exchange, a phenological behavior that would facilitate a strategy of continuous growth (Fig. 8). Leaf exchange was also associated with growth ring distinctness in the flora of the Cerrado biome (Coradin 2000), where distinct growth layers occurred mainly in species showing one leaf-flushing event per year.

The results found herein for the presence, absence and/or degree of distinctness of the rings agree with those observed in studies with the species M. stipitatum (Alves & Angyalossy-Alfonso 2000), P. rigida (Boninsegna et al. 1989), M. tinctoria (Alves & Angyalossy-Alfonso 2000), C. fissilis (Boninsegna et al. 1989; Alves & Angyalossy-Alfonso 2000; Dunisch 2005; Marcati et al. 2006b; Lopéz & Villalba 2016; Andreacci et al 2017; Pereira et al. 2018), C. canjerana (Alves & Angyalossy-Alfonso 2000 and Tomazello Filho et al. 2004), C. vernalis (Alves & Angyalossy-Alfonso 2000) and O. puberula (Boninsegna et al. 1989; Oliveira et al. 2001). These similar results found in species from subtropical and other climatic conditions suggest that growth rings are typical or genetically fixed for a species and/or that different restrictive climatic factors may act similarly on the growth rate of the trees, anatomically marking the wood.

On the other hand, our results differ from the results obtained in previous studies on growth rings of A. triplinervia (Callado et al. 2001a; Granato-Souza et al. 2018), C. canjerana (Shimamoto et al. 2015; Blagitz et al. 2019), N. megapotamica (Reis-Ávila et al. 2017), N. oppositifolia (Alves & Angyalossy-Alfonso 2000), O. puberula (Alves & Angyalossy-Alfonso 2000; Oliveira et al. 2001; Tomazello Filho et al. 2004; Reis-Ávila et al. 2017) and C. sylvestris (Absy & Scavone 1973, Sonsin et al. 2013, Avila et al. 2017). Several factors can be responsible for these divergences. The distinctness of growth rings may vary depending on the classification criteria adopted by the author, which are usually different, showing the need for uniformity in this sense (Silva et al. 2019). Factors such as the number of sampled specimens, genetic variations, endogenous rhythm, edaphic and local climatic conditions (Fahn et al. 1981; Vetter 2000; Callado et al. 2001a; Tarelkin et al. 2016; Silva et al. 2017; Blagitz et al. 2019; Silva et al. 2019) may influence the anatomy of growth rings and can partly explain the variations observed in the delimitation of rings between different studies. Therefore, the possible influence of sex on the distinction of growth rings in dioecious species, such as O. puberula (Carvalho 2002) and A. triplinervia (Carvalho 2004), should be investigated. In the Atlantic Forest, annual and distinct growth rings were observed in A. triplinervia (Callado et al. 2001a; Granato-Souza et al. 2018) but the studies do not mention whether the analyzed samples were from male or female individuals. In our study, two male and three female individuals from this species were sampled and it was observed that in the latter the boundaries of the rings were more defined.

Besides that, the methodology used for the anatomical analysis must also be considered. The 5-mm wood sections may be inadequate when there is variation in size or distance between the layers (Marcati et al. 2006b; Lisi et al. 2008; Silva et al. 2017), and, for a better view of the cell arrangements and greater precision of the determination and measurement of the growth rings width, cross-sections are more appropriate (López & Villalba 2016). Regarding this aspect, species that initially did not show distinct growth rings in the samples obtained using the Pressler probe (E. falcata, M. tinctoria, C. canjerana, E. argentinum and C. sylvestris) were also analyzed through cross-sections, and E. falcata and M. tinctoria showed distinct boundaries, reinforcing the limitation of the Pressler probes in such cases (Tarelkin et al. 2016).

To the best of our knowledge, this is the first study to describe growth rings and their anatomical characteristics in E. falcata, J. micrantha, L. divaricata (deciduous) and A. edulis (semideciduous), and the first wood anatomical investigation in E. argentinum (semideciduous), which showed indistinct growth rings. These novel results highlight the relevance of conducting basic research with subtropical species.

This study contributes to consolidating the idea that most subtropical trees forma distinct growth rings, which are probably marked when there is a reduction in temperature and photoperiod, considering the climatic conditions of the study area (Alves & Angyalossy-Alfonso 2000; Dünisch et al. 2003; Dünisch 2005; Lisi et al. 2008; Yanez-Espinosa et al. 2006; Venugopal & Liangkuwang 2007; Oliveira et al. 2009; Shimamoto et al. 2015). A periodicity pattern was also observed in the leaf phenophases of the studied species, as all species presented a period of more intense shedding and flushing during the year that was related to the subtropical climatic seasonality.

Although it was not possible to establish a direct relationship between leaf-shedding pattern and the presence of rings, since distinct rings were observed in deciduous, semideciduous and perennial species, leaf loss likely promotes an increase in growth-ring distinctness in deciduous species. Most deciduous species showed tree rings limited by marginal parenchyma, associated or not with other anatomical markers, while semideciduous and perennial species with distinct rings did not show this boundary marker, indicating a possible relationship between the type of ring marker and leaf-shedding pattern presented by the species.

Conclusion

This study confirmed the hypothesis that most tree species sampled from the subtropical seasonal deciduous forest have distinct growth rings, as found in tropical seasonal deciduous forests. It suggests that the widespread growth ring formation in this forest type may emerge under different seasonal climatic conditions, i.e., photoperiod and/or temperature in the subtropics and rainfall in the tropics. The rhythm of growth ring formation (if seasonal or other) and the role of climatic conditions as seasonal growth drivers need to be further investigated.

About the second hypothesis, we did not observe a clear relationship between leaf phenology and the presence of growth rings since growth rings were found in all leaf phenological patterns. However, all deciduous species had distinct growth rings with clear boundaries, suggesting that complete leaf loss has a strong influence on the wood anatomy of subtropical trees, similar to what is observed in tropical and temperate species.

Allophylus edulis, Erythrina falcata, Cedrela fissilis, Cupania vernalis, Jacaranda micrantha, Luehea divaricata, Machaerium stipitatum, Maclura tinctoria, Nectandra megapotamica and Parapiptadenia rigida constitute a group of tree species that can be explored for dendrochronological studies in subtropical moist forests in South America because they were found to have distinct growth rings with clear boundaries. Therefore, further dendrochronological investigations would shed light on the periodicity of growth ring formation and climatic drivers.

Acknowledgement

We thank the support of Coordenação de Aperfeiçoamento de Pessoal de Nível Superior -Brasil (CAPES) - Funding code 001 for the first autor, the support of CNPq for JLS (PQ-308926/2017-0), the Ph.D. student Ilana Rossi, from the Laboratório de Histologia at UNISINOS, for helping with photography, Claudia Fontana for providing bibliography, Giulia F. Santos for making the maps, Carolina Bauer for editing the images, José D. Bauer for the financial support of the fieldwork and an anonymous reviewer for important contributions.

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Publication Dates

• Publication in this collection
  22 Mar 2021
• Date of issue
  Oct-Dec 2020

History

• Received
  11 Dec 2019
• Accepted
  09 Aug 2020