Abstract
Among the heavy metals (HMs) whose concentrations in natural environments have risen considerably in the last era, chromium (Cr) is one of the most toxic. Because of the risks it poses to human and environmental health, it is of great importance to screen the variation in Cr contamination in the atmosphere and decrease the pollution. This study aimed to determine the proper tree species that can be used to monitor and reduce Cr contamination. For this aim, studies were conducted on Tilia tomentosa, Robinia pseudoacacia, Cedrus atlantica, Pseudotsuga menziesii, and Fraxinus excelsior species growing in Düzce, which is among the 5 most contaminated European towns according to the World Air Pollution report. Samples taken from these trees were examined, and changes in Cr concentration depending on species, organs, compass direction, and age range in the last 60 years were evaluated. Results indicated higher Cr pollution in recent years, consistent with higher traffic density, but that there was no consistent effect of compass direction. It was also determined that the tree species most appropriate for screening the variation in Cr contamination in the airborne were Tilia tomentosa, and the most appropriate species for decreasing pollution were Robinia pseudoacacia and Cedrus atlantica.
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Using Trees to Monitor Airborne Cr Pollution: Effects of Compass Direction and Woody Species on Cr Uptake during Phytoremediation
Ayse Ozturk Pulatoglu,a,* İsmail Koç,b Halil Barış Özel,c Hakan Şevik,d and Yafes Yıldız c
Among the heavy metals (HMs) whose concentrations in natural environments have risen considerably in the last era, chromium (Cr) is one of the most toxic. Because of the risks it poses to human and environmental health, it is of great importance to screen the variation in Cr contamination in the atmosphere and decrease the pollution. This study aimed to determine the proper tree species that can be used to monitor and reduce Cr contamination. For this aim, studies were conducted on Tilia tomentosa, Robinia pseudoacacia, Cedrus atlantica, Pseudotsuga menziesii, and Fraxinus excelsior species growing in Düzce, which is among the 5 most contaminated European towns according to the World Air Pollution report. Samples taken from these trees were examined, and changes in Cr concentration depending on species, organs, compass direction, and age range in the last 60 years were evaluated. Results indicated higher Cr pollution in recent years, consistent with higher traffic density, but that there was no consistent effect of compass direction. It was also determined that the tree species most appropriate for screening the variation in Cr contamination in the airborne were Tilia tomentosa, and the most appropriate species for decreasing pollution were Robinia pseudoacacia and Cedrus atlantica.
DOI: 10.15376/biores.20.1.121-139
Keywords: Air pollution; Heavy metal; Biomonitor; Bioaccumulator; Chromium
Contact information: a: Department of Forest Engineering, Faculty of Forestry, Kastamonu University, Türkiye; b: Department of Forest Engineering, Faculty of Forestry, Düzce University, Türkiye;
c: Department of Forest Engineering, Faculty of Forestry, Bartın University, Türkiye; d: Department of Environmental Engineering Faculty of Engineering and Architecture, Kastamonu University;
* Corresponding author: ayseozturk@kastamonu.edu.tr
INTRODUCTION
Global climate change, urbanization, and pollution, which are among the most critical and irreversible problems on a global scale today, have emerged because of the developments in industry and technology in the last century (Gur et al. 2024; Özel et al. 2024). In the last century, the workforce needed in the industrial field caused the population to migrate from rural to urban areas and gather in certain areas, which has led to various problems (Dogan et al. 2022; Cetin et al. 2023a). Excessive use of fossil fuels to produce the energy needed to meet the needs of industry and people has led to an increase in various gases in the atmosphere, disruption of atmospheric gas balance, and ultimately, global climate change (Tekin et al. 2022; Ozel et al. 2024). Mining activities and processing products to provide the raw materials needed for industrial activities have rapidly increased environmental pollution (Key et al. 2023; Kuzmina et al. 2023).
Urbanization and global climate change have become seemingly irreversible concerns in this era (Arıcak et al. 2024). Pollution has become a global problem that threatens all living things and ecosystems. Air pollution has reached such severe levels that it was reported that 99% of the worldwide population is subjected to low air quality; outdoor air pollution is estimated to have caused 6.7 million premature deaths annually (WHO 2022; Ghoma et al. 2023).
Among the categories of air pollutants, heavy metals (HMs) pose the most severe threat to human and environmental health. It is stated that HMs, some of which can be detrimental, poisonous, and lethal to people even in low amounts, can be dangerous at high concentrations, even those that are necessary as nutrients for living things (Ucun Ozel et al. 2019; Istanbullu et al. 2023). Among HMs, Cr is one of the most dangerous, and Cr contamination extremely disturbs ecosystems and environmental reserves, especially soil and water (Prasad et al. 2021).
Cr, a naturally occurring element in volcanic dust and rocky soils, is categorized as a carcinogen, according to the IARC (International Agency for Research on Cancer) (Sharma et al. 2020). Cr usually exists in two oxidative states, Cr(III) and Cr(VI). Cr(III) is harmful at high levels surpassing the limit, but Cr(VI) is 100 times more poisonous and 1000 times more mutagenic than Cr(III). Cr(VI) is a natural carcinogen, even in trace amounts. Cr(III) present in the soil is naturally oxidized to Cr(VI) during alkaline conditions or the presence of increased manganese contents (Benimeli et al. 2011; Suzuki et al. 2020). Due to its potential harm, it is included in the priority toxin catalog of ATSDR (Agency for Toxic Substances and Disease Registry) (Savas et al. 2021). Cr is released from numerous natural and anthropogenic activities (Hossini et al. 2022; Ullah et al. 2023). In the last 40 to 50 years, its contamination in aquatic and terrestrial biomes has become elevated due to several anthropogenic actions, which are influential environmental threats that utterly affect the environment and natural reserves, especially water and soil (Koç et al. 2024). Overexposure may lead to accumulation at higher levels in human and animal tissues, resulting in toxic and harmful health effects. Numerous studies have revealed that Cr is a noxious element that unfavorably affects plant metabolic behaviors (Prasad et al. 2021). Chronic exposure and bioaccumulation of Cr induces toxicity. It causes numerous pathophysiological defects such as allergic reactions, anemia, burns, and wounds, particularly in the stomach and small intestine, and damage to sperm and the male reproductive system (Hossini et al. 2022), lung cancer, stomach, liver, and kidney injury and epidermal irritation and sensitivity (Kimbrough et al. 1999).
Monitoring and reducing the levels of Cr pollution are priority research topics. Monitoring and reducing the change in airborne concentrations of Cr is vital, since the metal is extremely dangerous, particularly if absorbed into human tissue via inhalation (Yayla et al. 2022; Koc et al. 2024).
Trees exposed to air pollution for a long time can absorb pollutants with their roots, leaves, and bark, and transport them to the wood. Tree annual rings formed every year in wood can provide clues about the effects of atmospheric pollution. Many trials have been conducted to detect HM pollution in polluted areas and monitor the history of pollution using tree wood (Edusei 2021; Isinkaralar 2022; Cuciurean et al. 2024). Studies in recent years have shown the correlation between urban and industrial areas and the chemical content of tree rings, showing that tree annual rings can be used as biomonitors in monitoring HM concentrations (Chen et al. 2021; Savas et al. 2021; Key et al. 2023; Cobanoglu et al. 2023).
The region where the research was performed is the 5th most unclean city in Europe and has attracted the attention of many researchers due to its high pollution level. In the studies conducted in the region, the usability of Cupressus arizonica, Pseudotsuga menziesii, Cedrus atlantica, Picea orientalis, and Pinus pinaster species, which are widely grown in the region, were examined as potential biomonitors. In these studies, the highest values in wood were obtained on average in Picea orientalis with 1848 ppb for Cr (Koc et al. 2024) and 5323 ppb for Sr (Erdem 2023), in Cupressus arizonica with 11065 ppb for Pd (Sevik et al. 2024), 53000 ppb for Bi (Isinkaralar et al. 2023), 2105 ppb for Sn (Cetin et al. 2023b), and 4672 ppb for Tl (Canturk 2023).
For many years, plants have been used to screen the shifts in HM contamination in the airborne and phytoremediation studies aimed at diminishing pollution (Sulhan et al. 2023). However, different characteristics are required in both the species used as biomonitors and the plants used in phytoremediation studies. For plants to be used for both purposes, the plants must be able to absorb and accumulate HMs, but they must not die due to the effects of pollution. While the allocation of HM in wood should be limited in species that will be used as biomonitors (Canturk 2023; Key et al. 2023), in species that will be used to decrease pollution, it is desired that HM accumulate as much as possible, especially in wood, which is the main organ of the tree in terms of mass (Sevik et al. 2024; Koç et al. 2024). Therefore, choosing the proper trees for biomonitoring and phytoremediation analyses is essential. The current study aimed to define Cr concentration variation in the atmosphere over the last 60 years in Düzce, Türkiye, one of the uppermost air-polluted European towns, and to conclude the most appropriate tree species that can be used to lessen contamination. The main hypothesis of the research is that the accumulation of Cr in the organs of the studied species varies based on the direction of the compass.
EXPERIMENTAL
Düzce province, where the study samples were collected, has Europe’s 5th highest pollution level, based on the World Air Pollution Report 2021 (Koc et al. 2024). The topography and meteorological parameters of Düzce province, located in the Western Black Sea province of Türkiye, play a part in the increased air pollution. The primary pollutants that cause air pollution in Düzce arise from industrial facilities, domestic fuel use, and vehicle traffic load (Key et al. 2023).
The log samples used in this study were obtained from the trunks of Tilia tomentosa (linden), Robinia pseudoacacia (acacia), Cedrus atlantica (cedar), Pseudotsuga menziesii (Douglas fir), and Fraxinus excelsior (ash) trees, which are widely used in landscaping in Düzce province. Log samples were taken at a thickness of 10 cm from a height of approximately 40 to 50 cm above the ground in late autumn of 2022. When taking log samples of these species, directions (North, South) were indicated on the logs. Samples taken from the trunk stumps were first sanded in the laboratory to smooth the upper surface so that the annual rings could be seen more clearly.
Annual rings were grouped according to their width and the tree’s age. For this reason, trees that were approximately 60 years old were divided into 5-year age groups. Then, using a stainless-steel drill, samples from the wood (WD) of each age range, as well as outer bark (OB) and inner bark (IB), were taken and placed in glass Petri dishes. Samples were turned into sawdust without using any tools made of the metals examined in the research. After the samples were placed in glass containers without closing their lids, they were left room-dried in the laboratory for 15 days until they were completely dried, followed by drying for another week in an oven set at 45 °C. Then, 0.5 g of the dried samples were taken, and 6 mL 65% nitric acid (HNO3) and 2 mL 30% hydrogen peroxide (H2O2) were added and positioned in the microwave oven. The microwave oven was set to reach 200 °C within 15 min and kept at 200 °C for 15 min. After the samples were burned, the obtained samples were transferred to volumetric bottles, and the final volume was completed at 50 mL with ultrapure water. Samples were analyzed using the ICP-OES (Inductively Coupled Plasma-Optic Emission Spectrometer; GBC Scientific Equipment Pty Ltd., Melbourne, Australia) instrument, and Cr concentrations were determined by multiplying the results by the corresponding dilution factor. This procedure has been commonly used in earlier studies (Isinkaralar et al. 2022; Erdem et al. 2023).
An analysis of variance (ANOVA) was used to analyze the data using the SPSS 22.0 package program. The Duncan test was also applied for factors indicating statistically significant differences at the minimum 95% confidence level (p < 0.05).
RESULTS AND DISCUSSION
The results regarding the detected Cr concentrations based on tree species and direction are illustrated in Fig. 1.
Fig. 1. Cr concentration variations based on tree species and direction
The ANOVA results indicate that the Cr concentration variation in all directions was statistically significant. The Cr concentration change based on direction was determined to be statistically significant in all species except linden. According to the mean concentrations, the uppermost value was found in acacia and the lowest in Douglas fir, ash, and linden. According to the average values, the highest (22400 ppb) was 92 times more than the lowest (242 ppb). The Cr concentration variation based on tree and age period is presented in Fig. 2.
Fig. 2. Cr Concentration levels by tree species and period
Cr concentration differences were statistically noteworthy based on a species in all periods and a period basis in all species except acacia. While the uppermost value for linden was obtained in the 1988-1992 period, the highest value for cedar was obtained in the 2013-2017 and 2018-2022 periods. According to the mean concentrations, the uppermost value is in acacia, while the lowest was in linden, Douglas fir, and ash tree. Based on average concentrations, the value obtained in acacia wood was 200 times higher than in ash wood. The Cr concentration variation by organ and species is presented in Fig. 3.
Fig. 3. Cr concentration variation by organ and tree species
Cr concentration level was statistically significant based on a species in all organs and an organ basis in all species except acacia. In linden, Douglas fir, and ash, the uppermost value was acquired in the outer bark, while in cedar, the maximum concentration was in the inner bark. According to the mean values based on species, the highest value is in acacia, while the lowest is in linden, Douglas fir, and ash. The Cr concentration variation in the linden tree based on organ, direction, and period is presented in Table 1.
Table 1. Cr Concentration Variation in Linden Tree Based on Organ, Direction, and Period
Based on Duncan’s analysis results, numbers followed by the same letters are not statistically significant at P > 0.05. Capital letters indicate horizontal direction, while lower-case letters are vertical. Avg: Average; OB: Outer bark; IB: Inner bark; WD: Wood; BDL: Below detectable limit. Significant levels such as * = 0.05; ** = 0.01; *** = 0.001. These explanations are valid for all tables.
Cr concentration change in linden was statistically significant based on the direction in all organs except wood and on an organ basis in all directions. The uppermost value in the outer bark was observed in the north direction, while the lowermost value was obtained in the south. The uppermost value was achieved in the south direction in the inner bark, while the lowermost was in the east. The uppermost value was seen in the outer bark when considering the organs based on the means. While the value achieved in the outer bark in other directions was between 567 ppb and 847 ppb, it was seen at 2867 ppb in the north. This value was more than 16 times the value determined in the wood. The difference between the wood and the outer bark was less than 5 times in other directions.
According to the ANOVA results, Cr concentration differences in the linden tree were statistically significant based on direction in all periods and on a period basis in all routes. The maximum value in the north was achieved in the 2013-2017 period, the uppermost value in the south and east was in the 1988-1992 period, and the uppermost value in the west was in the 1998-2002 period. The 1978-1982 period in the north, the 2018-2022 period in the east, the 1983-1987 period in the north, and the 1963-1967 period in the west direction under the determinable limits. When the average values are examined according to the periods, the highest value was found in 1988-1992. The Cr concentration variation in the acacia tree based on plant organ, direction, and period is presented in Table 2.
Table 2. Cr Concentration Variation in Acacia Tree Based on Organ, Direction, and Period
Cr concentration in acacia was not statistically significant based on tree organs in all routes except the east. It was found to be statistically significant regarding direction in all organs. The uppermost value in the east direction was found in the inner bark. In the north direction, the inner bark remained under measurable limits. When looking at the directions according to the mean concentrations, the highest Cr concentrations were achieved in the south and the lowermost in the north and west.
Cr concentration in acacia was not statistically significant based on a period in all directions except the west. Cr concentration change was statistically meaningful based on the direction in 1963-1967, 1968-972, 1973-1977, 1978-1982, 1993-1997, and 1998-2002. The uppermost value in the western direction was achieved in the 2013-2017. In the northern direction, the periods 2008-2012, 2013-2017, and 2018-2022 remained under the determinable limits. Based on averages, the maximum Cr concentrations were achieved in the south, while the lowermost values were in the north and west. The Cr concentration difference in cedar tree based on tree organ, direction, and period is presented in Table 3.
Cr concentration variation in cedar tree was statistically significant based on organs in the north and south directions and a direction basis in all organs. While the uppermost value in the north was achieved in the inner bark, in the south, the uppermost value was acquired in the outer bark and wood. The highest Cr concentration was found in the north direction when looking at the directions according to the average values. Unlike other species, the cedar tree obtained the highest Cr concentration in the north route in the inner bark, more than twice that acquired in the outer bark.
Table 3. Cr Concentration Variation in Cedar Tree Based on Organ, Direction, and Period
Table 4. Cr Concentration Variation in Douglas Fir Tree by Organ, Direction, and Period
Cr concentration change in cedar was statistically significant in all routes based on period and in all periods based on direction. The highest value in the eastern and southern directions was obtained in 1963-1967. When one looks at the mean concentrations according to the periods, the maximum value was achieved in the 2013-2017 and 2018-2022 periods. Again, based on the directions, the uppermost average value is in the north. In the eastern direction, the 2013-2017 period remained under the determinable limits. The Cr concentration variation in Douglas fir tree by organ, direction, and period is presented in Table 4.
Cr concentration change in Douglas fir was statistically significant in all directions based on tree organs and in all organs based on route. It is possible to arrange wood < inner bark < outer bark for east and west directions. In the south direction, on the contrary, the ranking is outer bark < inner bark < wood. The uppermost value was achieved in the north according to the mean concentrations. In the north direction, the inner bark remained under measurable limits. The most notable result in Douglas fir was the significant difference between the values obtained in the outer bark. The value obtained in the north direction in the outer bark was more than 30 times the value obtained in the south direction.
According to the ANOVA results, Cr concentration variation in Douglas fir was determined to be statistically meaningful in all directions based on period. Cr concentration was at a statistically noteworthy level on a directional basis in all periods except the 1983-1987, 1998-2002, and 2003-2007 periods. While the uppermost value in the north was seen in the 1973-1977 period, the maximum value in the south was in 1993-1997. The uppermost value in the east was seen in the 2008-2012, while the highest value in the west was seen in the 2018-2022 period. According to the averages, the uppermost Cr was achieved in 1973-1977.
Table 5. Cr Concentration Variation in Ash Tree Based on Organ, Direction, and Period
Cr concentration change remained under the measurable limits in the north direction in periods other than 1963-1977 and 1993-1997, in the south in 1968-1992 and 1998-2007 periods, and in the west in 1973-1977, 1983-1987, and 1993-2012 periods. The Cr concentrations change in the Ash tree based on organ, direction, and period is presented in Table 5.
Cr concentration changes in ash tree samples were statistically significant on a directional basis in the outer and inner bark and on an organ basis in all directions. The uppermost value in all directions was obtained in the outer bark. The highest value was achieved in the north according to the mean concentrations. The Cr concentration change in the inner bark in the south and west remained under measurable limits. It is seen that the concentrations achieved in the outer bark were much higher than the concentrations found in the wood in all directions. Even in the east, where this difference was the least, the value obtained in the outer bark was more than 15 times that in the wood. This difference exceeded 33 times in the north direction. Considering the results, it was defined that the Cr concentration variation in the ash tree was statistically significant on a directional basis in periods other than the 1973-1977 and 2018-2022 periods. The highest value was achieved in 1968-1972 according to mean values. In the northern direction, the Cr concentration change remained under measurable limits in all periods except 1998-2002, 2008-2012, and 2013-2017. The Cr concentration change remained under the measurable limits in the south in the 1963-1977 and 2008-2017 periods and in the west direction in the 1973-1977, 1993-1997, and 2013-2022 periods.
According to the current study, the highest values based on a species were obtained in acacia and cedar. When the values are examined, the average Cr concentration was 22400 ppb in acacia and 11460 ppb in cedar, while it varied between 240 ppb and 390 ppb in other species. The species’ biology and interaction with HMs explain the large difference between species. Many studies have determined that HM concentrations vary significantly from species to species (Karacucuk et al. 2022; Yayla et al. 2022). The average Cr concentrations obtained in the studies were also quite different. While Savas et al. (2021) stated that the Cr concentration in Cedrus atlantica ranged between 923.3 ppb and 1588.4 ppb in the outer bark and 445.1 ppb and 765.8 ppb in the wood, Isinkaralar (2024) reported that the Cr concentration in Ailanthus altissima was 34480 ppb in the outer bark and 940 ppb in the wood. In the current study, there were significant differences between organs. For example, while the Cr concentration determined in the wood of linden was 180 ppb, this value was 370 ppb in the inner bark and 1240 ppb in the outer bark. Similarly, while the Cr concentration determined in the wood of linden was 110 ppb, this value was 120 ppb in the inner bark and 2610 ppb in the outer bark.
As can be seen, the Cr concentration variation on both species and organ basis was as high as 10-fold. Variation based on a species was mainly shaped by plant physiology and anatomy and the plant’s interaction with HMs. Studies have determined that each plant’s HM uptake and accumulation levels are different, and the change in HM concentration on a species basis can vary greatly (Koç et al. 2024; Öztürk Pulatoğlu et al. 2024). For this reason, it is frequently stated that bioaccumulator species should be determined separately for each HM (Sulhan et al. 2023; Sevik et al. 2024).
As a result, it was determined that the Cr concentrations in the outer bark were much higher than those in the wood and that the Cr concentration was generally in the order outer bark > inner bark > wood. Most studies obtained similar results (Key et al. 2022; Koc et al. 2024). This situation is primarily related to the structure of the outer bark and the contamination of particulate matter with HMs. After HMs are dispersed from their source, they adhere to particulate matter, which becomes a sink for HMs to collect. Afterward, contaminated particulate matter in the atmosphere sticks to the bark of trees, and the rougher the bark, the more particulate matter can adhere. Thus, HM concentrations in the outer bark can reach very high levels (Cesur et al. 2022). Afterward, these HMs can pass into the wood because HMs have three pathways to penetrate the plant tissue. These pathways are direct from the leaf through stomata, soil through the roots, and stem parts, namely the bark (Cobanoglu et al. 2023). If one accepts that all three routes are variable, then it can be expected that the higher the amount of HM accumulated in the outer bark, the higher the HM accumulation in the inner bark and the wood.
This study obtained the highest values for cedar, Douglas fir, and ash trees in the north direction. In fact, in these species, as a result of the Duncan test, the values obtained in other directions formed the first group, while those obtained in the north direction formed the second group. In studies with similar results, these findings were often interpreted as a direct result of heavy metal accumulation in roadside woods caused by traffic (Sulhan et al. 2023; Yayla et al. 2022; Canturk et al. 2024). However, the reality is far more complex. A multitude of studies have indicated that traffic and vehicles are indeed significant sources of heavy metals (Aricak et al. 2019; Kuzmina et al. 2023). Yet, when one delves into the subject, it is found that a highly intricate mechanism governs the entry of heavy metals into the plant body. According to Ejaz et al. (2023), heavy metals can translocate from the roots via the stem or enter the leaf through the stomata. Metals are usually transferred by active transport via the symplastic pathway inside cells after diffusion or penetration. Plant biochemical and metabolic activities play a pivotal role in the active transport of heavy metals inside plants (Shahid et al. 2017). The current understanding of the mechanism of Cr absorption and transport by plants in the soil is still in its infancy. Sulfate transporters have been identified as crucial for the movement of Cr in roots, as several recent studies have shown (Xu et al. 2023). The simultaneous occurrence of the two absorption pathways near urban and industrial locations makes it extremely challenging to discern whether the metal concentration within internal plant tissues is taken up by root cells from the soil or leaf surfaces from the atmosphere (Shahid et al. 2017).
The main hypothesis of the research is that the distribution of Cr accumulation in the organs of the studied species relies on the direction of the compass. It could have concluded that, despite the study’s findings highlighting variations in the directions, there was no consistent pattern in the data about compass directions. The distribution and accumulation of Cr in plants differed among species and was impacted by plants’ morphological and genetic traits. Furthermor