Changes in strontium levels in bark and over the past 40 years in the wood of trees exposed to high levels of air pollution

Erdem, R. (2023). “Changes in strontium levels in bark and over the past 40 years in the wood of trees exposed to high levels of air pollution,” BioResources 18(4), 8020-8036.

Abstract

The present study aims to identify the most suitable tree species for monitoring and reducing strontium (Sr) pollution. Strontium is a heavy metal that is extremely harmful to human and environmental health even at low concentrations and is listed as a priority pollutant by the Agency for Toxic Substances and Disease Registry due to its potential harm. Samples were taken from Pinus pinaster, Cupressus arizonica, Picea orientalis, Cedrus atlantica, and Pseudotsuga menziesii species grown in Düzce, a location reported as one of the top 5 cities having the most polluted air in Europe by the World Air Pollution Report. The changes in Sr concentration over the last 40 years were evaluated by species, organ, direction, and age range. The results indicate that Sr pollution significantly increased due to traffic sources. This study also showed that the transfer of Sr within the wood is limited in all the species under consideration; hence, all these species can be used in monitoring the changes in Sr pollution. The most suitable species for reducing Sr pollution were Cupressus arizonica and Picea orientalis, which have the highest capacity to accumulate the most Sr in their wood.

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Changes in Strontium Levels in Bark and Over the Past 40 Years in the Wood of Trees Exposed to High Levels of Air Pollution

Ramazan Erdem *

DOI: 10.15376/biores.18.4.8020-8036

Keywords: Biomonitor; Strontium; Düzce; Heavy metal

Contact information: Department of Forestry, Kastamonu University, Araç Rafet Vergili Vocational School, Kastamonu, Türkiye; *Corresponding author: rerdem@kastamonu.edu.tr

INTRODUCTION

The industrial revolution over the past century has caused irreversible problems, such as climate change and urbanization, on a global scale (Tekin et al. 2022; Cetin et al. 2023). During this period, the increase in environmental pollution is considered to be one of the most important threats to human health worldwide (Elsunousi et al. 2021). Today, almost the entire global population (99%) breathes air that exceeds WHO air quality limits and threatens their health (WHO 2022). Air pollution is estimated to contribute to 6 million preterm births each year and is stated to result in the death of approximately 7 million people annually (Jo et al. 2020; WHO 2023). Moreover, this change in the atmosphere’s composition also contributes to global climate change, which is considered the most critical issue worldwide (Cobanoglu et al. 2023a; Isinkaralar et al. 2023a,b).

The most harmful and deadly components of air pollution, which is important in terms of causing human death, are heavy metals. Nowadays, air concentrations of heavy metals have increased significantly, especially in urban areas, due to industrial activities and traffic (Istanbullu et al. 2023). These metals can stay undegraded in nature for a long period and bioaccumulate in living organisms; some are toxic and carcinogenic even at low concentrations and their concentrations in the air are constantly increasing (Sulhan et al. 2022; Yayla et al. 2022). Studies revealed that the concentrations of many heavy metals in the air, such as Mn, Cr, Ni, Cu, Zn, Al, Cd, and Fe, have increased significantly in recent years (Isinkaralar et al. 2023b,c). Some of these elements are much more harmful than others regarding human and environmental health. Therefore, they are defined as priority pollutants by international organizations such as ATSDR and EPA (Isinkaralar et al. 2022). One of the most toxic heavy metals in terms of environment and human health is strontium (Sr). Compounds of strontium (Sr), even small amounts of which can be harmful to human health, can cause lung cancer and accumulate in the body over a lifetime, leading to significant problems that can even result in sudden death (Cobanoglu et al. 2022). Moreover, studies show that Sr may be radioactive (Burger and Lichtscheidl 2019; Ivanets et al. 2020; Kwon et al. 2021). For this reason, monitoring and reducing the concentrations of these elements in the air is critical for human health.

In the present study, by reviewing the previous studies on the use of annual rings as biomonitors, gaps in the literature were determined. In the literature to date, many species such as Cupressus arizonica, Platanus orientalis, Robinia pseudoacacia, Corylus colurna, and Cedrus atlantica have been used to monitor the change of more known elements such as Pb, Cr, Ni, Co, Mn (Koc et al. 2023). However, the number of studies on elements such as Tl, V, As, and Sr, which have been proven extremely dangerous for human and environmental health, is much more limited (Canturk 2023). In this study, considering the gaps identified, the changes in the concentrations of Sr, one of the most harmful heavy metals for human and environmental health, were determined by species, year range, organ, and direction. Within the scope of the study, it is aimed to compare the Sr accumulation potential of the species examined here and determine how the accumulation in the trunk organs (outer bark, inner bark, and wood) of the tree varies with the concentrations in the air, how the concentrations in the annual rings change by the year range, the level of transition between organs after being taken into the plant body, and which sources are responsible for the accumulation in the trees. Thus, it was aimed to gather information about both the pollutants with Sr origin and the most suitable species that can be used for monitoring and reducing this pollution.

MATERIALS AND METHODS

This study was carried out in Düzce, a province in the Western Black Sea region of Türkiye, where the level of air pollution is very high. According to the 2021 World Air Pollution Report, Düzce is one of the top five cities with the highest level of air pollution in Europe (IQAir 2021). Within the scope of this study, the trunks of Pinus pinaster (Pp), Cupressus arizonica (Cpa), Picea orientalis (Po), Cedrus atlantica (Cda), and Pseudotsuga menziesii (Pm) species marked on their north sides were cut at approximately 10 cm thickness and approximately 50 cm above the ground. These log samples were then brought to the laboratory, and their surfaces were planed to clearly reveal the annual rings. As a result of the count and investigation, it was determined that the trees were approximately 40 years old. Considering the widths of the annual rings, they were grouped into five-year groups, and, using a steel drill, samples were taken from the outer bark, inner bark, and wood of each age group. The process was carried out in triplicate. The collected samples, in the form of shaving, were placed in glass Petri dishes and left with their lids open for 15 days to air dry. Then, the samples were dried in an oven at 45 °C for a week. From the dried samples, 0.5 g was taken, added with 6 mL of 65% HNO₃ and 2 mL of 30% H₂O₂, and then placed in a microwave oven designed for such analyses. The solution samples were transferred to volumetric flasks and diluted with ultrapure water to 50 mL. The samples prepared were analyzed using an ICP-OES device, and the values obtained were multiplied by the dilution factor to calculate Sr concentrations. The method used in the study has been commonly used in recent studies on this subject (Sevik et al. 2020).

Data were analyzed using the SPSS software package. A variance analysis was conducted for the data, and the Duncan test was applied for factors that had statistically significant differences at a confidence level of at least 95% (P < 0.05). Data were interpreted by simplifying and tabularizing them. Thus, the changes in Sr concentration were separately determined and evaluated by species, direction, organ, and year range.

FINDINGS

The changes in Sr concentration by species and organ are presented in Table 1.

Table 1. Changes in Sr (ppb) Concentration by Species and Organ

According to Duncan’s test results, numbers followed by the same letters (a, b, c, or d) are not statistically different at p > 0.05. Lowercase letters illustrate vertical directions; ***P ≤ 0.001

Table 2. Changes in Sr (ppb) Concentration by Directions and Species

According to Duncan’s test results, numbers followed by the same letters (a, b) are not statistically different at p > 0.05. Lowercase letters illustrate vertical directions, ns = not significant; ***P ≤ 0.001; **P ≤ 0.01

Results of the variance analysis revealed that the Sr concentration was significant in all organs by species. The highest values in the outer and inner bark were found in the Cpa and those in wood were observed in the Po. The lowest average value was found in wood and the highest in the outer bark. Therefore, the results can be ranked as wood < inner bark < outer bark. The changes in Sr concentration by species and direction is shown in Table 2.

Given the results presented in Table 2, it was determined that the changes in Sr concentration were significant in all directions, except for the south. The highest concentrations in the north, south, and east were found in the Cpa, whereas the highest concentration in the west was observed in Cpa and Po. The lowest average values were obtained in the Pp, Cda, and Pm species. The changes in Sr concentration by period and direction are given in Table 3.

Table 3. Changes in Sr (ppb) Concentration by Period and Direction

According to Duncan’s test results, numbers followed by the same letters (A, B, or a, b) are not statistically different at p > 0.05. Lowercase letters illustrate vertical directions, while capital letters indicate horizontal directions; ns = not significant; ***P ≤ 0.001; **P ≤ 0.01; *P ≤ 0.01

Given the values presented in Table 3, the changes in Sr concentration by directions were significant in all periods, except for the period 2018 to 2022. The Sr concentration by period was insignificant in directions other than the north and east. The lowest concentration was found in the period 1998 to 2002, whereas the highest concentration was found in the period 1983 to 1987. The lowest concentration in the north was obtained in the periods 1988 to 1992 and 1998 to 2002, while the highest in the east was obtained in the period 2018 to 2022. The changes in Sr concentration by organ and direction are presented in Table 4.

Table 4. Changes in Sr (ppb) Concentration by Organ and Direction

According to Duncan’s test results, numbers followed by the same letters (A, B, or a, b) are not statistically different at p > 0.05. Lowercase letters illustrate vertical directions, while capital letters indicate horizontal directions. Ns = not significant; ***P ≤ 0.001; *P ≤ 0.01

When examining the results shown in Table 4, it was determined that the changes in Sr concentration in all organs, except the outer bark, by direction were significant. The changes in Sr concentration by organ were significant in all directions. The lowest value in the north was found in wood, whereas the highest value was seen in the outer bark. In the east, the highest value was found in the inner and outer bark and the lowest in the wood. The highest concentration in the south was obtained in the outer bark, whereas the highest concentration in the west was obtained in the outer and inner barks. The changes in Sr concentration in Pp by organ and direction are presented in Table 5.

Table 5. Changes in Sr (ppb) Concentration in Pp by Organ and Direction

Table 6. Changes in Sr (ppb) Concentrations in Pp by Period and Direction

Examining the results of the variance analysis, it was found that the change in Sr concentration in Pp was significant in all organs by direction and in all directions, except the east, by organ. The highest values in the north, south, and west were found in the outer bark. The lowest average value was found in the east and the highest value was in the north, south, and west. The changes in Sr concentration in Pp by period and direction are given in Table 6.

Given the results presented above, the changes in Sr concentration in all woods were significant in all periods by direction and in all directions by period. The highest average values were found in the periods 1983 to 1987 and 1993 to 1997. Considering the average values by direction, the lowest value was obtained in the east and the highest value in the south and west. The changes in Sr concentration in the north for the period 2013 to 2017 and in the south for the period 1988 to 1992 were below the detectable limits. In the east, the changes in Sr concentration in the 1983 to 1987, 1993 to 1997, 1998 to 2002, and 2018 to 2022 periods were also lower than the detectable limits. The changes in Sr concentration in Cpa by organ and direction are presented in Table 7.

Table 7. Changes in Sr (ppb) Concentration in Cpa by Organ and Direction

Table 8. Changes in Sr (ppb) Concentration in Cpa Woods by Period and Direction

Examining the results presented in Table 7, the changes in Sr concentration at T5 were significant in all directions based on the organ and in all organs based on direction. The lowest value in the north, east, and west is seen in wood, while the lowest value in the south is seen in wood and inner bark. The highest values were obtained in the outer bark in the north, east, and south, while the highest value in the west was obtained from the inner bark. Therefore, the average results can be ranked as wood < inner bark < outer bark. The changes in Sr concentration in Cpa by period and direction are shown in Table 8.

Considering the results, it was determined that the changes in Sr concentration in Cpa wood were significant in all periods by directions and in all directions by periods. The highest concentration was observed in the north in the period 2008 to 2012, while the highest value in the east was observed during the 1998 to 2002 period. The highest value in the south was found in the period 2018 to 2022 and the one in the west was found in the period 2003 to 2007. Comparing the average values, the lowest one was found in the east and the highest one in the west. There was no significant difference between the periods by average values. The changes in Sr concentration at Po by organ and direction are presented in Table 9.

Table 9. Changes in Sr (ppb) Concentration in Po by Organ and Direction

Given the results of variance analysis, it was determined that the changes in Sr concentration in Po were significant in all organs by direction and in all directions by organ. The highest concentration in the north and east was found in the outer bark and those in the south and west were found in the inner bark. The lowest average value was observed in the north, east, and south, whereas the highest one was found in the west. The average concentration results for organs can be ranked as wood < inner bark < outer bark. The changes in Sr concentration at T6 by period and direction are presented in Table 10.

Table 10 shows that changes in Sr concentration in Po wood were significant in all periods and all directions. The highest value in the north was in the period 1983 to 1987, whereas the highest value in the east was in the period 2018 to 2022. The highest value in the south was obtained in the period 1983 to 1987 and the one in the west was found in the period 1993 to 1997. Comparing the average values, the lowest value was found in the east and the highest in the west. The changes in Sr concentration in Cda by organ and direction are shown in Table 11.

Table 10. Changes in Sr (ppb) Concentration in Po Woods by Period and Direction

Table 11. Changes in Sr (ppb) Concentration in Cda by Organ and Direction

Considering the results presented in Table 11, it was determined that the changes in Sr concentration were significant in all organs by direction and in all directions by organ. The highest concentration in the outer bark was in the west and the lowest concentration in the east. The highest value in the inner bark was obtained in the west and north, whereas the highest value in wood was obtained in the west. Comparing the average values, the lowest average value was found in the east and the highest value in the west. The changes in Sr concentration in Cda woods by period and direction are presented in Table 12.

Table 12. Changes in Sr (ppb) Concentration in Cda Wood by Period and Direction

Considering the results of the variance analysis, it was determined that the changes in Sr concentration in Cda wood were significant in all periods and all directions. A comparison of average values revealed that the lowest value was found in the east and the highest was found in the west. A further comparison found that the lowest average concentration was obtained in the periods 1983 to 1987 and 1988 to 1992. In the east, the changes in Sr concentration during the periods 1988 to 1992 and 1993 to 1997 were found to be lower than the detectable limits. The changes in Sr concentration in Pm by organ and direction are shown in Table 13.

Table 13. Changes in Sr (ppb) Concentration in Pm by Organ and Direction

Considering the results, the changes in Sr concentration in Pm were significant in all organs by direction. The changes in Sr concentration in all directions, except the east and west, were insignificant. The highest value in the east was observed in the inner bark and the lowest one in the wood and outer bark. In the west, the highest concentration was obtained from the outer bark, whereas the lowest concentration was found in the wood. The changes in Sr concentration in Pm by period and direction are presented in Table 14.

Table 14. Changes in Sr (ppb) Concentration in Pm Woods by Period and Direction

Given the results presented in Table 14, the changes in Sr concentration were significant in all periods by direction and in all directions by period. The highest values were obtained in the period 2008 to 2012 for the north, in the period 1983 to 1987 for the east, in the period 2018 to 2022 for the south, and in the period 2018 to 2022 for the west. Furthermore, the changes in Sr concentration were lower than detectable limits in the north for the period 1988 to 1992 and in the east for the periods 1983 to 1987, 1993 to 1997, 2008 to 2012, and 2013 to 2017.

DISCUSSION AND CONCLUSION

In the present study, the highest Sr values were generally found in Cupressus arizonica (Cpa) and Picea orientalis (Po) species. This result agrees with the data reported by many studies conducted on heavy metals. It has been noted in many studies that the accumulation levels of heavy metals varied among different species, and it has also been emphasized that plant type was the main factor influencing heavy metal accumulation (Karacocuk et al. 2022). This is a result of different physicochemical reactions of species to heavy metals (Isinkaralar et al. 2023c). For instance, when the same species are compared, the highest Cr concentration was obtained in Cupressus arizonica and Pseudotsuga menziesii (Koc et al. 2023), the highest Bi concentration was obtained in Pseudotsuga menziesii (Isinkaralar et al. 2023c), and the highest Tl concentration was obtained in Cupressus arizonica (Canturk 2023).

The results achieved in this study indicated that the Sr concentrations in the organs ranked as wood < inner bark < outer bark. It was reported in previous studies that heavy metal concentrations in the outer bark were high (Cesur et al. 2021). This is generally related with the structure of the outer bark and the adhesion of particulate matter contaminated with heavy metals to the outer bark. Particulates in the air are first contaminated with heavy metals and these particles can adhere to the bark surface because of the rough and cracked surface of the outer bark (Yayla et al. 2022). It was determined in the present study that Sr concentrations in the inner bark were higher than in the wood. This is related to the intake of heavy metals into the plant body.

The heavy metals are taken into the plant body primarily from roots, leaves, and stem parts (Chen et al. 2021). Stemwood, the largest reservoir of aboveground tree biomass, was identified in numerous positions as the primary long-term pool for radiocaesium in forest vegetation despite the relatively low concentration of radiocaesium in woody parts (Calmon et al. 2009). The statistically noteworthy correlation between the transfer elements of Sr to stem wood (sapwood, heartwood) and its vertical allocations in soil profiles have not been observed (Golyaka et al. 2020). As a result of the present study, it can be said that the Sr in the inner bark enters from the stem parts and, therefore, the concentrations in the inner bark, which has no contact with air, were lower than in the outer bark but in comparable to the wood. Kudzin et al. (2019) narrated that the ability of tree organs and tissues of pine plantations to accumulate Sr was declining in the subsequent order: bark > roots > wood. Holiaka et al. (2023) noted that Sr was reasonably stable in the entire trunk except in the oldest annual tree rings, which expanded sharply, likely revealing active radionuclide transport to senescing tissues.

The element transfer in the tree timber part is predominantly associated with the cell wall and structure. The CWPM (cell wall–plasma membrane) interface describes an apoplastic mechanical barrier, and a flexible design takes part in stress signaling, sensing, and perceiving the metalloid and metal stress (Wani et al. 2018; Key et al. 2023). Ion exchange is the primary tool for the adsorption of Sr (II) ions on carboxymethyl groups of the carboxymethylcellulose. At low pH (<2.0), the excess H+ ions compete to the Sr (II) ions, to attach with carboxylate ion (-COO). As the pH of the medium increases, carboxylate sites are unrestricted for exchange with strontium ions (II) due to an increase in polymer hydrolysis. The ionic power of the solution rises with the concentration of KCl, and Sr (II) adsorption in carboxymethylcellulose declines. This indicates that ions’ adsorption is also affected by ionic force from the medium (Jain et al. 2022).

It was also determined in the present study that the Sr concentrations in the wood of the species were different; there were remarkable differences between Sr concentrations in the same period in different directions and in the same direction in different periods. For instance, in Cedrus atlantica (Cda), the Sr concentration determined in the north in the period 2008 to 2012 was 127.5 ppb, whereas the Sr concentration measured in the same direction in the period 2003 to 2007 was 3983.2 ppb. The Sr concentration measured in the east in the period 2003 to 2007 was 30.2 ppb. These results show that there were significant differences in Sr concentration between adjacent wood masses and, thus, the transfer of Sr within the wood was limited.

This finding is important because the main lack of knowledge regarding the usability of biomonitors in monitoring heavy metal pollution has been emphasized to be the transfer of elements within the wood. In fact, it has been reported in previous studies that the transfer potentials of different elements in the wood of different species were different. Thus far, in some studies, it has been determined that Cedrus deodara is suitable for monitoring Cu pollution (Zhang 2019), Cedrus atlantica for Ni, Cr, and Mn (Koç 2021; Savas et al. 2021), Cupressus arizonica for Cd, Ni, Fe, and Zn (Cesur et al. 2021, 2022; Cobanoglu et al. 2023b), and Corylus colurna for Cd, Ni, Zn, Pb, Cr, and Zn (Key et al. 2022; Key and Kulaç 2022), indicating that the transfer of these elements in the wood of these species is limited. However, in the same studies, it has also been stated that Pb and Zn in Cedrus deodara (Zhang 2019), Co in Cedrus atlantica (Koç 2021), and Bi, Li, and Cr in Cupressus arizonica could be transferred within the wood (Zhang 2019; Cesur et al. 2021, 2022; Cobanoglu et al. 2023b).

The transport of elements within the wood part of plants is largely related to cell structure, particularly the cell wall (apoplastic route). In plants, the apoplast between the cell wall and plasma membrane (CWPM) is not only an apoplastic membrane barrier but also a flexible structure that acts as a sensor and signal generator in case of metal/metalloid stress. Cell wall proteins (CWP) that are activated under various abiotic stresses have been extensively identified and characterized among different types of plants (Wani et al. 2018). The tree-related materials studied show a relatively clear selectivity for distinct metal ions. The results from several sorption experiments using various metal ion loading solutions show that the affinity ranking of metal ions to the tree-related materials is altering (Su 2012).

Plants frequently face abiotic stress factors throughout their life cycles. The most common stresses that plants face are drought and frost stress factors, which are related to climatic parameters (Sevik and Karaca 2016; Dogan et al. 2023; Koç and Nzokou 2023). This is because plant development depends on the mutual interaction of genetic structure (Kurz et al. 2023; Tandogan et al. 2023) and environmental conditions (Erdem et al. 2023; Yiğit et al. 2023). Therefore, factors that cause significant and permanent changes in climatic parameters, such as global climate change trigger the stress mechanisms of plants (Varol et al. 2022). In addition, the increase of UV-B stress due to climate change (Ozel et al. 2021a), radiation originating from anthropogenic factors (Ozel et al. 2021b), and heavy metal pollution (Cesur et al. 2022; Erdem 2023) are also significant sources of stress for plants. These stress sources are likely to affect plant metabolism and hence the potential of plants to accumulate heavy metals.

As a result of this study, the highest Sr concentrations were obtained in the west and north. There is a residential area to the north of the study area and a highway to the west. It is stated that Sr is largely released into the atmosphere from anthropogenic sources (Cobanoglu et al. 2022; Cong et al. 2023). This situation is actually valid for many heavy metals. Studies show that the main sources of heavy metals are human activities such as traffic, urbanization, industry, and mining activities (Kuzmina et al. 2023).

SUGGESTIONS

Within the scope of this study, the highest concentrations of strontium (Sr) in the air were generally found in the outer bark of the trees examined. The concentrations of heavy metals in the outer bark usually originate from the heavy metal-contaminated particles. Therefore, it can be stated that there is a high level of Sr pollution in the air in the study area.

Changes in the Sr concentrations in different directions were determined and the highest concentrations were found in the west and north, where the traffic density is high, in almost all species. Therefore, it can be said that the primary sources of Sr pollution are anthropogenic activities, particularly urbanization and traffic.

Within the scope of this study, it was determined that the Sr concentration in all the species examined here significantly varied both between different directions within the same year range and between consecutive year ranges. This finding indicates that the transfer of Sr within the wood of the species examined here is limited. Given this conclusion, it can be said that the species and method used in the present study can effectively be used in monitoring the changes in Sr concentrations.

The usability of plants in phytoremediation studies aiming to reduce heavy metal pollution depends on their capacity to accumulate heavy metals in their bodies. The organ with the highest volume in trees is the wood. Therefore, the most suitable species for phytoremediation studies are the ones that accumulate the most Sr in the wood part. In the present study, the highest Sr concentrations were found in the wood parts of Picea orientalis (Po) and Cupressus arizonica (Cpa) species. Thus, it can be said that these species are the most suitable ones for reducing Sr pollution.

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Article submitted: August 8, 2023; Peer review completed: September 30, 2023; Revised version received and accepted: October 3, 2023; Published: October 11, 2023.

DOI: 10.15376/biores.18.4.8020-8036