The influence of rainfall and temperature on radial growth of urban trees under the impact of steel industry pollution

Neto, T. C. C., Lousada, J. L. P. C., Fontana C., Moreira, C. G., and Latorraca, J. V. F. (2023). “The influence of rainfall and temperature on radial growth of urban trees under the impact of steel industry pollution,” BioResources 18(3), 4771-4789.

Abstract

The aim of this study was to analyze the growth rings and evaluate the effect of the urban environment on the growth of Terminalia catappa L. under intense industrial activity. At least two wood samples were obtained from each tree with an increment borer. The regions of Volta Redonda (Northwest and Southeast regions) and Resende (used as control) were established for the collection. The dendrochronological potential of T. catappa indicated sensitivity to precipitation and temperature in a more exposed urban and industrial steel pollution area because there were differences in growth when compared to an area less exposed to the same pollution. Thus, it was possible to conclude that this species has the potential to be used as a bioindicator of anthropogenic activities. In addition, the delimitation of the growth rings of the studied species contributes to the realization of future dendrochronological studies, expanding the understanding of the behavior of this species present in urban environments at different regional scales. This study reinforces the importance of rainfall and temperature in regulating radial growth in tropical forests.

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The Influence of Rainfall and Temperature on Radial Growth of Urban Trees Under the Impact of Steel Industry Pollution

Thayanne Caroline Castor Neto,^a José Luis Penetra Cerveira Lousada,^b Cláudia Fontana,^c Carolina Gomes Moreira,^d and João Vicente de Figueiredo Latorraca ^e,*

DOI: 10.15376/biores.18.3.4771-4789

Keywords: Bioindicator; Tree rings; Tropical tree; Urban pollution

Contact information: a: Postgraduate Program in Environmental and Forest Sciences, Federal Rural University of Rio de Janeiro, 23890-000, Seropédica, Rio de Janeiro, Brazil; b: Centre for the Research and Technology of Agro-Environmental and Biological Sciences (CITAB), University of Trás-os-Montes and Alto Douro, 5001-801, Vila Real, Portugal; c: Department of Forest Science, Luiz de Queiroz School of Agriculture, University of São Paulo, 13418-900, Piracicaba, São Paulo, Brazil; d: Department of Environmental Sciences, Federal Rural University of Rio de Janeiro, 23890-000, Seropédica, Rio de Janeiro, Brazil; e: Department of Forest Products, Federal Rural University of Rio de Janeiro, 23890-000, Seropédica, Rio de Janeiro, Brazil; *Corresponding author: latorraca@ufrrj.br

INTRODUCTION

The study of growth dynamics of a woody species leads to a better understanding of specific strategies developed in favor of its adaptation in each environment. Trees react according to environmental variables, which may be reflected in the cambial activity and in the formation of annual rings, expressing events that occurred both in the past and in the present year (Tomazello Filho et al. 2001). Climate, for example, is considered one of the most important modulators of tree growth (Locosselli et al. 2019a), and in this sense, dendrochronology makes it possible not only to determine age, but also to study the performance of trees as a function of factors that made them grow (Fontana et al. 2018b), both in natural and urban environments.

In addition to climate, other variables can affect plant performance, especially those growing in urban environments that have less favorable environmental conditions. The trees that are present in these environments are exposed to thermal stress, soil drought, and low air humidity (Gillner et al. 2014). Therefore, these factors may contribute to the increased vulnerability of tree development (Locosselli et al. 2019a). A first step in predicting forest resistance and resilience to unfavorable conditions is to know how it performed in relation to past climatic conditions. To investigate this issue by dendrochronological methods, it is necessary to identify which species are sensitive to the environmental conditions to the point of influencing annual growth rings. In this context, one of the authors’ goals was to explore the dendrochronological potential of and assess climate influence on radial growth in Terminalia catappa L. (almond tree), growing in urban conditions. The aim was to evaluate the potential of T. catappa as an environmental bioindicator. Furthermore, atmospheric pollution, linked to the urban environment, is considered one of the most important environmental concerns (Volná et al. 2021). The presence of steel industries in urban areas can significantly increase air pollution by emitting toxic heavy metals such as lead, cadmium, mercury, arsenic, chromium, and nickel, as well as various air pollutants such as acid gases (SO₂ and NO_X), incomplete combustion pollutants (CO and HC), and particulate matter (PM) of varying sizes (Wang et al. 2016), which can alter the optical properties of leaf surfaces, leading to a reduction in the amount of light required for photosynthesis (Prajapati 2012). Because it is a critical problem for human health, the monitoring of these pollutants has become essential during urbanization (Isinkaralar 2022).

Considering the sensitivity of species when recording changes in the environment, dendrochronological studies have been conducted to observe the effect of atmospheric pollution on the growth of tree species (Battipaglia et al. 2010; Bartens et al. 2012; Gillner et al. 2014; Sensuła et al. 2017; Kukarskih et al. 2022). Gillner et al. (2014) affirm that tree-ring analyses are a valuable tool for urban forestry to assess the capability of tree species to withstand future climatic conditions that are aggravated in urban heat islands and help in the selection of adapted plantations. The same authors found that two important species of urban forestry in the city of Dresden, in Germany, Acer platanoides L., and Acer pseudoplatanus L., should be planted at urban sites with lower heat and drought stress. Sensula et al. (2017), studying Pinus sylvestris L. growing near sites of chemical factories in Poland, discovered that the effects of industrial pollution have been recorded by this pine species via the long-term reduction in the size of thickness growth, reduction in the level of homogeneity of short-term incremental response, and reduced susceptibility of trees to short-term environmental impulses. The authors concluded that pollution could affect the size of incremental growth and disturbance in the incremental reaction of trees. Kukarskih et al. (2022) after studying P. sylvestris in Russia concluded that environmental pollution negatively affects tree growth. Moreover, the results of climate and historical data analysis suggest that the trees on urban sites were weakened by both climate and air pollution factors after 1941 because of the introduction of more than 60 industrial factories to the studied city, which generated a significant increase in air pollution.

In Brazil, there are still few studies that address the same effect on urban trees (Chagas 2013; Geraldo et al. 2014; Locosselli et al. 2019; Vasconcellos et al. 2019). For example, Chagas (2013) studied the species Tabebuia pentaphylla Hemsley and Poincianella pluviosa (DC.) Queiroz and discovered that changes in the pattern of climatic response can provide evidence regarding the influence of non-climatic factors, such as stress and sources of pollution, on the annual growth rate of trees in urban and peri-urban locations. Locosselli et al. (2019) used Tipuana tipu (Benth.) Kuntze to assess how climate and air pollution affect the development of urban trees and found that climate modulates the growth of these trees in the urban environment. However, the authors also concluded that air pollution has a dramatic influence on tree inter-annual growth variability compared to climate and may be considered a limitation to tree growth. Vasconcellos et al. (2019) found that there is an immediate response of the species Ceiba speciosa (A.St.-Hil., A.Juss. & Cambess.) Ravenna in urban environments in relation to the rainfall and the dry and hot climate, and the absence of natural water reserves in urban soil may explain this more immediate response of urban tree growth to rainfall and temperature indexes. Therefore, the search for varied species can add to the knowledge base and expand the performance of studies on this topic in the country.

In this context, T. catappa, an exotic but quite common species, is found in most cities in Brazil, especially in urban areas (Ribeiro et al. 2020). However, questions remain regarding the growth dynamics of this species in an urban environment and how exposure to atmospheric pollution can interfere with the formation of rings in these environments. Therefore, the present study aimed to analyze the effect of the urban, industrial environment on growth rings of T. catappa. Knowing that this species has dendrochronological potential (Chagas 2009), it is expected to find differences in growth and responses to climatic conditions because of interference from atmospheric pollution. Thus, because it is a consolidated species in urban afforestation, the study of its growth dynamics in an anthropic environment can contribute to future studies being conducted at different regional scales.

EXPERIMENTAL

Study Areas

The study was conducted in the municipalities of Volta Redonda (22º31’23” S, 44º06’15” W) and Resende (22°27’46” S, 44°27’20” W), the latter being for the purpose of controlling the samples, as it is approximately 40 km away from an imposing steel industry in Volta Redonda. Both are in the Middle Paraíba do Sul region, in the state of Rio de Janeiro, Brazil. The altitude in Volta Redonda ranges from 363 m to 707 m a.n.m. on the banks of the Paraíba do Sul River, while in the main area it is 380.3 m (Gioda et al. 2004). According to the Köppen climate classification, the climate is Cwa (humid subtropical zone, with dry winters and hot summers) (Alvares et al. 2013). The average annual precipitation is 1,337 mm and the average temperature is 21 °C (Rocha and Guimarães 2017). February is the hottest month (24 °C), and July is the coldest (17 °C) (Montine et al. 2014). The dry season is from April to September and the wet season is from October to March.

Sampling and Tree Ring Measurements

Initially, a survey of individuals of T. catappa present in the surroundings of the steel mill was conducted, within a radius of 2500 m from the industrial plant. Two regions were also established for collection (Northwest and Southeast) considering the pollution levels in the municipality and the predominant wind direction. Located on the west side of the Paraíba do Sul River, the northwest region exhibits higher levels of pollution, while the southeast region, located on the east side of the same river, has lower levels (Peiter and Tobar 1998). The predominant wind direction is northwestward, according to a survey of data made available by State Institute of the Environment (INEA) between 2001 and 2018. Of the 110 individuals of T. catappa found and georeferenced in Volta Redonda, 86 trees were in good phytosanitary condition and were chosen for the accomplishment of this study: 40 in the southeast region and 35 in the northwest region. In Resende, 11 trees were sampled (used as control, because they were approximately 40 km from the steel factory). The study areas, the collection points, and the climate diagram are illustrated in Fig. 1.

Fig. 1. Representation of study areas; Delimitation of the sampled area, the collection points, and a climatic diagram of the Resende meteorological station.

At least two wood samples, perpendicular to each other, were obtained from each tree using an increment borer in the bark-pith direction at 1.30 m above the ground. After collection, the samples were polished with a sequence of sandpaper (between 80 to 1200 grains/mm²) to highlight the transverse plane. The samples were scanned at 1200 dpi for analysis and counting of annual rings.

The width of the annual rings was measured using CooRecorder version 7.8 (Cybis Elektronik & Data AB, Saltsjöbaden, Sweden) with an accuracy of 0.01 mm in the digitized images. The COFECHA software was used to statistically verify the cross dating and the quality of the measurement of the rings (Holmes et al. 1986; Grissino-Mayer 2001), in which 30-year segments were used with 15-year overlaps. Then, the ARSTAN software was used to remove the biological age trend of individual series and adjust a common growth signal between the trees (Cook and Holmes 1996), therefore, the cubic smoothing spline model (50% of variance maintained in 20-year segments) was used to adjust each series. During this process, an individual series of rings was considered unreliable if it had a low correlation value with all other series and under these circumstances, that series was rejected to improve the common signal (Brienen and Zuidema 2005). Of a total of 172 cores, 38 cores were removed, 32 in the SE region and six in the NW region. No cores were removed from Resende. The chronologies were built with 134 cores.

Data Analysis and Statistics

At each site, the final mean chronology was constructed from the set of all standardized tree-ring width series for their populations. The standard chronology was used to perform Pearson’s correlations, being the most sensitive to the signal of interest between growth and local climatic variables, both for the current and previous year, as well as for the dry and rainy season periods. For this purpose, monthly precipitation, and temperature data between 1961 and 2018 were used and obtained from the nearest meteorological station to the studied locations (Resende station). The data were obtained by the National Institute of Meteorology (INMET). In addition, to evaluate the properties of the chronologies (Cook et al. 1990), the average sensitivity, the correlation between the series, Running Bar (RBar), and the expressed population signal (EPS) (Fritts 1976; Speer 2010) were calculated (in COFECHA and ARSTAN) for each study site. Furthermore, the cumulated radial increment (CRI) was calculated by adding the measurements of each ring and the radial annual increment (RAI) was calculated by dividing the CRI by the number of rings, to verify the performance differences between the sites.

Before performing the statistical analyses, all quantitative results were evaluated for normality and homoscedasticity using the Shapiro-Wilk and Levene tests, respectively. Values that did not follow a normal distribution were submitted to logarithmic transformation. The results of the radial increments were compared with each other by Student’s t test at a confidence level of 95%, following the recommendations of Zar (2010).

RESULTS AND DISCUSSION

Annual Rings Delimitation and Measurements

In the three study sites, the species T. catappa presented distinct annual rings, visible to the naked eye, delimited either by the formation of a thin line of marginal axial parenchyma, or by the confluence of the lozenge aliform paratracheal parenchyma and often associated with vessel alignment, fibrous zones, and slight differences in vessel diameter at the transition to the next ring.

The cumulated radial increment was similar among the population trees in the Volta Redonda regions and higher in the trees in Resende (Fig. 2). Trees in the northwest region exceeded the average value of 200 mm of increment accumulated at approximately 75 years old, while trees in the southeast region reached this value at an approximate age of 60 years. In Resende, trees aged between 60 and 65 years showed a cumulated increase of 200 mm. However, the longest-lived trees were mostly in the most polluted region (northwest), with ages estimated at up to 110 years. The trees in the southeast region were up to 104 years old and the youngest individuals were concentrated in Resende, with a maximum age of 95 years. It is also observed that the maximum average of the accumulated radial increment occurred in the trees of the northwest region, with 266.51 mm at 110 years. The southeastern region had trees with 282.73 mm at 100 years of age and the trees of Resende with 220.44 mm at 95 years of age.

The trees in the northwest region (n = 32) had a mean age of 50 years, radial annual increment (RAI) and, at 45 years old a cumulated radial increment (CRI) of 2.60 mm/year (SD ± 0.58) and 116.78 mm (SD ± 26.16), respectively. In the southeast region (n = 24), the trees had a mean age of 47 years, with an annual radial increment at 45 years old of 2.83 mm/year (SD ± 0.41) and a radial increment of 127.45 mm (SD ± 18.59). In Resende (n = 11), the trees had an average age of 59 years. The radial annual increment at 45 years old was 2.87 mm/year (SD ± 0.29), and the radial increment was 129.02 mm (SD ± 13.13). The values of the annual and radial increments, as well as the dendrometric values of the trees used in the present study, can be requested from the first author.

Fig. 2. Cumulated radial increment (CRI) of the T. catappa species in the study regions: (a) northwest, (b) southeast, and (c) Resende; the dashed line represents average growth.

Both the RAI and the CRI showed significant differences between the trees sampled in Volta Redonda and Resende. The RAI between the northwest region and Resende presented the following statistical values t = – 2.95, p = 0.008; between the southeast region and Resende presented t = – 2.58, p = 0.018. The CRI between the northwest region and Resende presented t = – 4.97, p = 0.000; between the Southeast region and Resende presented t = – 3.90, p = 0.000. However, between the northwest and southeast regions, there was no significant difference between tree growth. The RAI presented t = – 0.42, p = 0.679 and CRI presented t = – 1.34, p = 0.186.

Dendrochronological Analysis

After analyzing the growth rings, it was observed that from a total of 172 samples obtained from 86 trees (35 in the northwest region, 40 in the southeast region, and 11 in Resende), 134 radial samples were used to build the chronology (64 in the region north-west, 48 in the southeast, and 22 in Resende) (Table 1).

Table 1. Statistical Characteristics of the T. catappa Species in the Study Sites

SD: Standard deviation; Min = minimum value; Max = maximum value; Rbar: Correlation coefficient; EPS: Expression of population sign.

The statistical characteristics, presented in Table 1, show that the mean sensitivity values were about 0.40 for the samples from the three study sites. The intercorrelation values of the series were similar for trees from Volta Redonda (northwest and southeast regions) (< 0.30); however, Resende presented a higher value (> 0.50). The values obtained for the variable Rbar varied between 0.123 and 0.265. The population expression signal (EPS) was high in all regions and ranged from 0.902 to 0.926 between study sites.

Figure 3 illustrates the growth rates of rings constructed from the standardized values, as well as the number of samples used during the analyzed period (1909 to 2019) at the study sites. The EPS and Rbar values were highlighted at an interval of 20 years (1950, 1970, 1990, and 2010), and it was found that, for all study sites, the EPS value increased as the number of radial samples increased. The correlation coefficient (Rbar) was higher in the period of 1950 and lower in the year of 1990 for the chronologies of the trees in the northwest region and Resende; and higher in the period of 2010 and lower in the period of 1950 for the chronologies of trees in the Southeast region.

The correlation indices of the width of the rings of the individuals analyzed in the northwest region (NW) are represented in Fig. 4. For the rainfall variable, there was a significant positive correlation in the current year; however, the significance occurred in two months of the dry season (July and September) and one month of the rainy season (October). In other words, the trees in the NW region showed a rapid response to the precipitation rates that occurred in the current year (Fig. 4a). For the temperature variable, there was only a significant negative correlation during the current year, in the month of October, which corresponds to the rainy season (Fig. 4b). In other words, wetter early spring and milder temperatures favor the growth of the species. For the Southeast (SE) region, there was no significant correlation between growth and climatic variables. In Resende, there was no significant correlation for the rainfall variable; however, for the temperature variable, there was a significant negative correlation for the month of September, referring to the previous month, which corresponds per month of the dry season.

Fig. 3. The growth index of T. catappa rings in the study regions (black line): (a) northwest, (b) southeast, and (c) Resende. The gray area shows the number of radial samples used during the analysis period (1909 to 2019).

Considering the dendrochronological potential of the tropical species T. catappa (Chagas 2009), it was possible to describe a new analysis of the annual rings of this species, finding differences in growth and responses to climatic conditions in an environment under intense urban and steel activity. Although T. catappa is abundantly found in anthropic environments (Ribeiro et al. 2020), there are still few studies that address the characteristics of the wood of this species (Van Vliet 1979; Ruwanpathirana 2014), or even the analysis of rings (Chagas 2009).

Fig. 4. Correlations between the width of T. catappa rings and climatic variables (1961 to 2018). The bars represent the correlation indices between the growth of the species in the northwest region and the indices of precipitation (a) and temperature (b). The light gray areas show the rainy season period. DS: Dry season; WS: Wet season. *Significant correlation values, critical correlation value = 0.259, for p < 0.05.

Some species of the genus Terminalia have distinct rings, such as T. bellirica (Gaertn.) Roxburgh, T. myriocarpa Van Heurck & Müll.Arg., T. ivorensis A. Chev, T. superba Engl. & Diels, T. gracilipes Capuron, T. Amazonia Exell in Pulle, and T. oblonga Steud. (Urbinati et al. 2003; Ridder et al. 2013; Singh et al. 2013; Gaspard et al. 2018; Marcelo-Peña et al. 2020). When studying the wood anatomy of several species of the Combretaceae family, Van Vliet (1979) described that the annual rings are distinct for T. catappa. A more recent study by Chagas (2009) reported a similar description, but detailed some more features, stating that the growth layers are distinctly demarcated by a thin band of marginal parenchyma, sometimes associated with confluent paratracheal axial parenchyma, by the thickening and radial flattening of the fiber wall. Additionally, there are observed variations in the diameter of the vessels in the transition of the annual rings. In other words, the description made by the author corroborates the macroscopic characteristics observed in the present study. Therefore, it is understood that T. catappa did not present differences in the forms of delimitation of the annual rings in an urban environment.

In dendrochronological studies of tropical species, the difficulty in delimiting annual rings is a frequent problem (Trouet et al. 2010; Ridder et al. 2013). For this reason, Brienen and Zuidema (2005) recommend the use of trunk discs to facilitate the verification of the discontinuity of rings in these species. In addition, anatomical characterization helps to correctly identify rings during measurements and reduces errors caused by false rings, which are a common feature in tropical species (Aragão et al. 2019), increasing the accuracy of measurements and favoring the construction of reliable chronologies (Fritts 1976; Vaganov et al. 2011; Brienen et al. 2016; López and Villalba 2020). In the present study, the level of difficulty in identifying the rings of T. catappa was high and demanded immense attention during this process, because the species present several forms of ring delimitation. Moreover, it was not possible to obtain an entire disc of the trunk once the samples came from urban afforestation.

The chronologies constructed with the 67 trees of T. catappa indicate that the success of cross-dating between individuals occurred due to a similar variation in growth patterns (Stahle et al. 1999). Some authors, working with species of the same genus, found average sensitivities that ranged from 0.64 for T. gracilipes, in a xerophytic environment in southwestern Madagascar, and 0.16 for T. superba, in lowland tropical forests in the western and in the central African continent (Ridder et al. 2013; Gaspard et al. 2018). Speer (2010) suggests that 0.20 is an accepted value in series that are sensitive enough for climate reconstruction. However, for trees present in urban environments, some authors found values greater than 0.40 (Chagas 2013; Locosselli et al. 2019; Vasconcellos et al. 2019), which is a value considered so sensitive that it may mean that dating is complicated by the frequent presence of narrow or absent rings close to wider rings (Speer 2010). However, the average sensitivities found for urban trees of T. catappa demonstrate year-to-year growth variability and a high common signal, inferring that the growth of trees from Volta Redonda and Resende can be influenced by an environmental, climatic, or non-climatic factor. The average correlation coefficient for all pairs of series described by the value of Rbar, in general, was low for the chronologies of the species T. catappa but like those found for urban trees (Locosselli et al. 2019; Vasconcellos et al. 2019). Furthermore, the correlations varied along the growth of the trees in the different studied places, which makes it possible to assess the period in which growth limitations occurred (Fritts 1976).

The EPS values express the quality that a finite set of radial samples must represent the chronology of the infinite population (Buras 2017); that is, the EPS value is influenced by the size of the sample set (Wigley et al. 1984; Speer 2010; Mérian et al. 2013). According to Buras (2017), the EPS value has been misinterpreted in dendrochronological studies, because the constant arbitrary use of the theoretical threshold above 0.85, suggested by Wigley et al. (1984), refers to the signal strength of the subsample, not the total sample size. Therefore, no specific EPS value can guarantee that the chronology of the growth rings is suitable for climatic reconstructions (Cook et al. 1990; Buras 2017).

Response of Terminalia catappa to Climate Conditions

In species from temperate climates, it is consensual to admit that the climate can significantly influence the tree radial growth (Fritts 1976; Holmes et al. 1986; Schweingruber 1988; Speer 2010; Vaganov et al. 2011). Nevertheless, the use of tropical species in dendrochronological studies was for some time questioned, as some authors assumed that tropical species usually did not produce annual rings. However, the recent work by Zuidema et al. (2022), which brought together the contribution of 53 authors and was based on a new global network consisting of over 14,000 tree-ring data series from 350 locations across the tropics, makes it possible to identify the formation of annual rings in hundreds of tropical species. The research also allowed for the study of climatic phenomena (temperature and precipitation) recorded in tree rings in different tropical environments, suggesting that climate change may increase the sensitivity of tropical trees to climatic fluctuations.

Other works that can be mentioned are those by Fontana et al. (2018) who concluded that Copaifera lucens Dwyer growth is more dependent on precipitation than temperature, being sensitive to drought in cases of extreme water deficit during the late growing season. Campbell et al. (2022), when investigating the dendroclimatological potential of Paratecoma peroba (Record) Kuhlm. occurring in the last remnant of seasonal semi-deciduous forest in Rio de Janeiro, Brazil, found that temperature is the climatic factor with the greatest influence on the growth ring of the species. Likewise, Aragão et al. (2019), evaluated the dendrochronological potential of four Caatinga neotropical dry forest tree species and found that inter-annual growth variation is strongly driven by seasonal rainfall. Moreover, the authors indicated that the strong dependence of trees on precipitation is worrisome, considering that climate change scenarios forecast increased drought conditions in the Caatinga dry forest.

The relationships between climate and growth can also be modulated by non-climatic factors, including those present in microsites (Fang et al. 2015). Urban areas can develop a different microclimate due to the presence of numerous sources of pollutants, both vehicular and industrial, which contribute to excess heat (Kukarskih et al. 2022). In addition, particulate matter (PM) from these emissions can also affect the local climate and intensify heat island and thermal inversion effects, changing the way radiation is transmitted through the atmosphere (Valverde et al. 2020; Kukarskih et al. 2022; Zhang et al. 2022). It is worth mentioning that the retention of pollution occurs as a function of urban size, atmospheric stability, and the intensity and flow of winds (Takebayashi and Senoo 2018; Yun et al. 2020; Abbassi et al. 2022), these considered as the main mechanism that results in greater deposition of particles in trees (Chen et al. 2015). At the same time, the vegetation that makes up urban afforestation is subject to greater stress and can undergo changes in its structure (Rai 2016), such as morphological or anatomical parameters of the leaves (Alves et al. 2008; Costa et al. 2015), in cellular metabolic processes (Sytar 2013) in periods of cambial activity and dormancy (Iqbal et al. 2010a, 2010b; Vasconcellos et al. 2017), or even in xylem anatomy and radial increment (Leonelli et al. 2012; Chagas 2013; Pretzsch et al. 2017; Vasconcellos et al. 2019; Vasconcellos and Callado 2020). In this way, the task of interpreting dendroclimatic reconstructions, for example, can be aided by investigating the influences of non-climatic sources (Fang et al. 2015).

Different responses were observed when relating the growth of T. catappa with the climatic variables in the study sites. Considering that climatic data of precipitation and temperature were the same, it is suggested that factors related to atmospheric pollution may interfere with the growth of this species in an urban environment. In addition, it is possible to infer that the sensitivity of the species to the climate was lower in Resende, because the municipality is far from the urban-industrial center of Volta Redonda and, for this reason, does not receive too much influence from the pollution from this specific location. However, when evaluating the behavior of the species as a function of the climate between the two regions of Volta Redonda (NW and SE), the trees in the northwest region showed greater sensitivity to climatic indices, for precipitation rates. Even though they are close, the trees in the southeast region did not express a significant correlation between the precipitation and temperature indices, that is, the growth of trees in this region was not dependent on the climatic factor. This fact could be explained by the possible interference of the winds throughout the year. These differences in growth between NW and SE, in addition to being explained by the influence of pollution, may also be due to the heat island effect exerted by the industrial unit through the increase in temperature in the northwest region, induced by the wind direction (Abbassi et al. 2022; Song et al. 2022).

It is noteworthy that the tree ring index presented in Fig. 3 all show a decreased trend during the 2000 to 2019 period, which may be related to the increasing climate extremes. Regoto et al. (2021), in an analysis of seasonal and annual trends of extreme indices of air temperature and precipitation over Brazil during the period 1961 to 2018, concluded that, in the Southern region, the climate is becoming wetter, with a reduction in consecutive dry days, especially in spring. Likewise, Córdova et al. (2022), in a study on the dynamics of precipitation anomalies in Tropical South America, found a significant increase in the frequency of climatic extremes occurrence (precipitation) in the south-eastern region of Brazil, which includes the 3 locations sampled in the present work. An identical situation was observed in a humid subtropical zone in the Northern Hemisphere, where climate extremes increased under global warming (Shao et al. 2021).

Urban Pollution Effects

The life expectancy of Terminalia catappa can reach 100 years, and the species can present heights that vary between 15 and 25 meters in the natural environment (Flores 2003; Thomson and Evans 2006). Although the ages of the trees in each region studied were similar, the differences that occurred between the increments of trees from Volta Redonda and trees from Resende may be associated with pollution, because the trees that grew less were those from Volta Redonda. Studies indicate that the effects of atmospheric pollution on urban trees, in general, affect photophysiological mechanisms, causing changes in the optical properties of leaves, the photosynthetic system, and in stomatal functioning (Wigley et al. 1984; Schweingruber 1988; Grantz et al. 2003; Paoletti 2009; Prajapati 2012; Mérian et al. 2013), consequently, interfering with the growth in height and diameter of trees (Marques et al. 2019; Vasconcellos et al. 2019; Zuidema et al. 2022). In addition, frequent reduction pruning, commonly practiced in urban trees that are under power lines (Carvalho Maria et al. 2021), can interfere not only with the canopy architecture, but also reduce the leaf coverage area, reducing the proportion of leaves and, consequently, photosynthetic rates. Therefore, the possibility of relating tree growth with air quality indices, such as the emission of particulate matter and total suspended particles, for example, may be an alternative to better understand the interference of pollution in the growth of urban trees.

The trees in the southeast region may have received less influence from urban and industrial pollution because the predominant wind direction in Volta Redonda was from southeast to northwest, according to the wind rose diagram for the region, built with the available data by INEA, between 2001 and 2018. Gioda et al. (2004), when evaluating the air quality in the city of Volta Redonda between some periods (the years 1995, 1996, and 1999), observed that the wind direction was east to west, so air pollutants would converge from east to west. The same authors also found that the concentration gradient of total suspended particles (TSP) was lower on the windward side of the steel industry than on the leeward side, reinforcing the hypothesis that the trees located in the northwest region would be receiving more interference from atmospheric pollution.

The sensitive behavior of trees in the northwest region as a function of precipitation may be related to the loss of leaves during the dry season. T. catappa trees are briefly deciduous during this season and, in some environments, can lose their leaves twice a year (Stahle 1999). The leaf surface, in turn, works as an efficient device for the deposition of pollutants, as they are highly exposed parts (Sytar 2013). In this sense, precipitation plays a significant role during the rainy season, as it helps to remove pollutants deposited on leaf surfaces, contributing to the effective growth of tree individuals. Therefore, the most expressive results of the growth indices in relation to precipitation observed during the transition from the dry season to the rainy season, may mean that the growth of T. catappa occurred in response to the rainy season of the previous year and that the trees present in the region considered most affected by pollution (NW) may be dependent on this climatic factor.

CONCLUSIONS

The dendrochronological study of the species indicated sensitivity to precipitation and temperature in an area more exposed to steel pollution by the possible interference of winds throughout the year, and it is suggested that factors related to atmospheric pollution may interfere with the growth of this species in an urban environment.
The species can be considered tolerant to the anthropic environment because of the longevity of the individuals analyzed under different environmental conditions.
The delimitation of the annual rings of the species in this research contributes to the realization of future dendrochronological studies, expanding the understanding of the behavior of this species at different regional scales.

ACKNOWLEDGMENTS

The authors are grateful to the Wood Quality Research Center (NPQM) at the Federal Rural University of Rio de Janeiro, in Brazil, and to the Laboratory of Forest Products of the University of Trás-os-Montes and Alto Douro, in Portugal. This article came from the thesis of the first author, in the Postgraduate Program in Environmental and Forestry Sciences (PPGCAF/UFRRJ). This research was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Finance Code 001, by National Funds by FCT, the Portuguese Foundation for Science and Technology, under the project UIDB/04033/2020 and the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) under the project NSF-FAPESP PIRE-CREATE 2017/50085-3 and 2019/27110-7.

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Article submitted: March 29, 2023; Peer review completed: April 29, 2023; Revised version received and accepted: May 9, 2023; Published: May 22, 2023.

DOI: 10.15376/biores.18.3.4771-4789