Introduction

Particulate matter (PM) pollution in the atmosphere is becoming increasingly severe as urbanization and industrialization intensify, which has serious threats to human health and environmental safety, so it has attracted much attention1,2,3,4,5. PM is respirable air-suspended particulate matter, which can be classified as PM2.5 (less than or equal to 2.5Ā Ī¼m), PM10 (greater than 2.5Ā Ī¼m and less than 10Ā Ī¼m), and PM>10 (greater than or equal to 10Ā Ī¼m) based on particle size6,7,8.

Roadside plants have the potential to retain atmospheric particulate matter and improve air quality9,10,11,12. In recent years, researchers focused on the mechanisms of PM retention in plants and the factors affecting PM retention. For the plant itself, the leaf surface micromorphology influenced PM retention capacity13,14. The latest research found that the microclimate change caused by evapotranspiration on the surface of plant leaves had a significant effect on the retention of PM2.515. The ability of plants to retain PM can be affected by planting patterns and three-dimensional configuration structures16. Equally important were the effects of meteorological factors on plant PM retention, for instance, rainfall and wind17.

Except for its ability to retain PM, the role of plants in environmental monitoring cannot be ignored18,19. Large amounts of toxic trace elements are present in atmospheric PM20,21, and PM containing toxic trace elements can float to other ecosystems22, and then be enriched in organisms, thereby jeopardizing their health20. Hence, the investigation of toxic trace elements in PM has significant implications for risk assessment and environmental monitoring. A recent study showed that plant leaf PM can substantially reflect the composition of toxic trace elements in the environment23. Nonetheless, there is still a lot of confusion about foliar PM and associated toxic trace elements. What is the composition of toxic trace elements in PM of different sizes retained by plants? Is it possible that plant species affect PM of different sizes to retain toxic trace elements? Who determines the concentration of toxic trace elements in foliar PM?

In this study, six roadside plants were investigated in Changsha, Hunan Province, a typical subtropical city in China. We measured the content of PM in different size fractions on their leaves and associated toxic trace elements. We also analyzed the association between PM of different sizes and toxic trace elements as well as the correlation among toxic trace elements, which is rarely seen in previous studies. The objectives of this study were to (1) evaluate the ability of different plants to retain particulate matter of different size fractions as well as toxic trace elements, (2) analyze driving factors of toxic trace element content in particulate matter, and (3) reveal potential associations between toxic trace elements from particulate matter. Our results can contribute to the knowledge of the ability of common roadside plants to retain particulate matter, toxic trace elements, and their potential associations in the subtropical area. Simultaneously, our study can provide a theoretical basis for the plant configuration in urban green belts and the application of plants in environmental monitoring. In addition, our work can provide innovative perspectives for the study of foliar PM.

Results

Foliar PM retention

FigureĀ 1 shows the differences among plant species in the retention of PM in different size fractions. The total PM retention capacity of P. macrophyllus was the highest (3.8464Ā g/m2), which was significantly higher than that of the other five plants (Pā€‰<ā€‰0.05). Podocarpus macrophyllus also had the greatest retention of PM10 (0.1426Ā g/m2) and PM>10 (3.5865Ā g/m2). PM2.5 accumulated on the leaf surface of C. camphora was the highest (0.4907Ā g/m2), which accounted for 91.85% of the total PM retention of C. camphora, while C. camphora had the lowest PM>10 retention (0.0160Ā g/m2), and it indicated that C. camphora was much more effective in accumulating fine particulate matter. Although O. fragrans had the lowest retention of total PM (0.3958Ā g/m2), PM2.5 retention of O. fragrans (0.2986Ā g/m2) was only lower than that of C. camphora, and significantly higher than that of P. macrophyllus (0.1174Ā g/m2), L. chinense var. rubrum (0.0254Ā g/m2), M. grandiflora (0.0101Ā g/m2) and P. tobira (0.0004Ā g/m2). PM2.5, PM10, and PM>10 on the leaf surface accounted for 75.43%, 17.60%, and 6.97% of the total PM retention of O. fragrans, which indicated that O. fragrans also was more effective in accumulating fine particulate matter.

Figure 1
figure 1

Particulate matter (PM) retention capacity of different plants. (a) Total PM; (b) PM2.5; (c) PM10; (d) PM>10. Different lowercase letters in the graph represent significant differences in the PM retention ability of tree species (Pā€‰<ā€‰0.05).

Toxic trace elements in foliar PM

FigureĀ 2 shows the toxic trace element concentrations in foliar particulate matter of different plants. The distribution of toxic trace elements in PM of the same particle size was different among the six roadside plants. Cinnamomum camphora carried the most amount of Al, Cu, Zn, Fe, and Pb in foliar PM>10 among the six roadside plants, and there were significant differences in the Al, Cu, Zn, Fe, and Pb concentrations in foliar PM>10 between C. camphora and the other five plant species (Pā€‰<ā€‰0.05). The highest Al, Zn, Cd, Fe, and As concentrations were found in foliar PM10 of P. tobira, which was significantly higher than the other five plant species (Pā€‰<ā€‰0.05). For Al, Zn, Cd, and As, P. tobira had the highest concentration in foliar PM2.5 among the six roadside plants. The highest Fe concentration in foliar PM2.5 was observed in P. macrophyllus, which was significantly higher than C. camphora (Pā€‰<ā€‰0.05).

Figure 2
figure 2

Toxic trace element concentration in foliar particulate matter of different plants. Different colors represent different plants and different shapes represent particulate matter of different sizes.

The distribution of the same element varied with plant species and particle size. For Al, C. camphora [PM>10 (537,825Ā mg/kg)ā€‰>ā€‰PM10 (69,319Ā mg/kg)ā€‰>ā€‰PM2.5 (3506Ā mg/kg)] and O. fragrans [PM>10 (309,648Ā mg/kg)ā€‰>ā€‰PM10 (91,191Ā mg/kg)ā€‰>ā€‰PM2.5 (7293Ā mg/kg)] had the highest content of Al in PM>10; P. tobira [PM10 (324,958Ā mg/kg)ā€‰>ā€‰PM2.5 (81,472Ā mg/kg)ā€‰>ā€‰PM>10 (25,202Ā mg/kg)] had the highest content of Al in PM10; M. grandiflora [PM2.5 (64,998Ā mg/kg)ā€‰>ā€‰PM10 (25,893Ā mg/kg)ā€‰>ā€‰PM>10 (15,055Ā mg/kg)] and P. macrophyllus [PM2.5 (46,844Ā mg/kg)ā€‰>ā€‰PM10 (28,992Ā mg/kg)ā€‰>ā€‰PM>10 (20,169Ā mg/kg)] had the highest content of Al in PM2.5; and there were significant differences among the three particle sizes in the same plant species (Pā€‰<ā€‰0.05), while the Al content of L. chinense var. rubrum had no significant difference among the three particle sizes (Pā€‰>ā€‰0.05). The distribution of Cd and As in the particulate matter of different plant leaves showed almost complete consistency, as evidenced by the highest levels of PM>10 in C. camphora foliage, PM2.5 in M. grandiflora foliage, PM10 in P. tobira and L. chinense var. rubrum foliage, and the Cd and As concentrations of O. fragrans and P. macrophyllus showed no significant difference among the three particle sizes (Pā€‰>ā€‰0.05) (Table S1).

The results of two-way ANOVA (Table 1) showed that most of the toxic trace elements were significantly influenced by plant species, PM size, and their interactions. Al (Fā€‰=ā€‰36.19, Pā€‰<ā€‰0.001), Cd (Fā€‰=ā€‰6.64, Pā€‰<ā€‰0.001), and As (Fā€‰=ā€‰7.63, Pā€‰<ā€‰0.001) were more driven by the interaction of plant species and PM size, while some elements were also significantly influenced by these factors but were dominated by PM size, such as Cu (Fā€‰=ā€‰8.70, Pā€‰<ā€‰0.001), Pb (Fā€‰=ā€‰11.63, Pā€‰<ā€‰0.001), and Fe (Fā€‰=ā€‰6.53, Pā€‰<ā€‰0.01). More interestingly, there was no significant effect of PM size on Zn (Pā€‰>ā€‰0.05). There was a highly significant effect of plant species on Zn in the particulate matter (Pā€‰<ā€‰0.01).

Table 1 Two-way ANOVA of toxic trace elements influenced by plant species, PM size, and their interactions.

Correlation analysis of toxic trace elements

Linear regression analysis of toxic trace element concentrations in foliar PM and the ability of foliar PM retention showed that there was a significant correlation between Al, As, Cd, and Zn in PM2.5 and foliar PM2.5 retention (Pā€‰<ā€‰0.05). However, there was no significant correlation between the seven elements and foliar PM10, PM>10 retention (Fig.Ā 3).

Figure 3
figure 3

Regression analysis of toxic trace element concentrations with foliar PM retention. Different colors are used in the figure to distinguish the different toxic trace elements. Significance levels are indicated by Pā€‰<ā€‰0.05, Pā€‰<ā€‰0.01, and Pā€‰<ā€‰0.001.

Most of the toxic trace elements in the particulate matter showed a highly significant correlation (Pā€‰<ā€‰0.05), except Pb and Cd (Rā€‰=ā€‰0.259, Pā€‰>ā€‰0.05). However, the correlation between toxic trace elements was affected by particle size. Al and Cu were significantly correlated only at PM>10 (Rā€‰=ā€‰0.780, Pā€‰<ā€‰0.001), similarly for Al and Pb (Rā€‰=ā€‰0.765, Pā€‰<ā€‰0.001), Pb and Zn (Rā€‰=ā€‰0.963, Pā€‰<ā€‰0.001), Pb and Cd (Rā€‰=ā€‰0.567, Pā€‰<ā€‰0.05), and Pb and As (Rā€‰=ā€‰0.629, Pā€‰<ā€‰0.01). Fe and Al were not significantly correlated only at foliar PM2.5 (Rā€‰=ā€‰0.308, Pā€‰>ā€‰0.05), analogously for Cd and Cu (Rā€‰=ā€‰0.073, Pā€‰>ā€‰0.05), As and Cu (Rā€‰=ā€‰0.119, Pā€‰>ā€‰0.05), Fe and Cd (Rā€‰=ā€‰0.260, Pā€‰>ā€‰0.05), and Fe and As (Rā€‰=ā€‰0.286, Pā€‰>ā€‰0.05) (Fig.Ā 4).

Figure 4
figure 4

Correlation analysis between toxic trace elements. Different colors represent different sizes of particulate matter. Significance levels are indicated by *Pā€‰<ā€‰0.05, **Pā€‰<ā€‰0.01 and ***Pā€‰<ā€‰0.001.

Discussion

Particulate matter retention among plant species

Urbanization has accelerated and increased the pressure on transportation, which has also led to a rapid escalation of particulate matter from roads24,25,26. Numerous studies have demonstrated that the roadside plant species can effectively adsorb and remove particulate matter of different sizes, which to a certain extent alleviates the environmental pollution caused by urban transportation27,28,29. In our study, P. macrophyllus had the highest retention of total PM, especially much more effective in accumulating large PM particles, which was consistent with previous research30,31,32. It has been proved that coniferous species can retain particulate matter more effectively than broadleaf species due to their unique leaf structure and microscopic characteristics. The microstructure of coniferous species is neat "ridged" stripes and well-arranged stomatal strips, with a large number of wrinkles and fluffy structures in the stomatal area, and the size of the fluff is nanoscale, which increases the surface area and surface roughness and is more conducive to the deposition of intercepted particles30. Narrow needles may be more easily hit by particles in the air than large flat leaves, compared to flattened leaves, narrow conifer needles have a much larger Stokes number and therefore have higher capture efficiency31. Podocarpus macrophyllus was not considered outstanding in its ability to retain PM2.5 as there were physiological differences between different conifer species32, and an appropriate selection of conifer species can lead to better air quality improvement12. Besides, we found C. camphora was preferable to P. macrophyllus and other plants in terms of their ability to retain PM2.5. Current studies on foliar PM2.5 capture capacity for evergreen broad-leaved trees (C. camphora) are inconclusive. Some researchers found that C. camphora did not effectively capture small-size particulate matter33,34. But others proved that evergreen broad-leaved trees had greater adsorption capacity of PM2.5 than coniferous trees31, and this is consistent with our results. The reason was that the leaf stomata can adsorb PM2.531, and the broad-leaved trees (C. camphora) have more stomatal density than coniferous trees (P. macrophyllus)35,36,37, so C. camphora showed very high adsorption capacity of PM2.5. In addition, the subtle changes in ambient water vapor brought by the evapotranspiration of plant leaves would also be effective in retaining PM2.515. In our study, P. macrophyllus had the highest ability to retain PM, and C. camphora excelled in retaining PM2.5. Therefore, our results suggest that the combination of P. macrophyllus and C. camphora was highly recommended to be planted in the subtropical city to effectively reduce PM from the air.

Toxic trace elements in foliar particulate matter

Previous studies mainly focused on the adsorption of particulate matter by plants and the factors influencing the reduction of PM31, but the relationship between PM of different sizes and toxic trace elements in foliar PM remains unclear. Our results demonstrated that there was a "particle size effect" for most toxic trace elements in foliar PM. All of the trace element was influenced by particle size except Zn. However, the mechanism of the effects of particle size on trace elements is still unclear, which can be a direction of future research. Additionally, the different content of the same elements in particulate matter of the same particle size indicates that the particulate matter may be from different sources, such as the elemental composition of particulate matter originating from industrial areas and non-industrial areas and their content was completely different34. To avoid the influence of environmental factors, all the trees studied were in the same road adjacent area. Therefore, the most likely reason is that different plant leaves absorb toxic trace elements from the same source of particulate matter, leading to variations in their concentrations. There was further evidence from the two-way ANOVA results that plant species and the interaction of plant species and particle size had a highly significant effect on the seven toxic trace elements, which has rarely been proved by such methods in previous studies38,39. Different plants generally have different foliar microstructures, i.e., some plants are more likely to absorb trace elements from large particulate matter on the leaf surface40,41, while others are more inclined to fine particulate matter, such as PM2.542. All toxic trace elements in PM>10 on C. camphora foliage in our study were higher than those in other particle-size particulate matter. Some plants are selective in the adsorption of particulate matter due to their leaf physicochemical factors, thus explaining why C. camphora has the worst PM>10 adsorption capacity but its ability to retain toxic trace elements is better43.

Association between toxic trace elements and their association with foliar retention capacity of particulate matter

In theory, the more particulate matter retained on the leaf surface, the more toxic trace elements should be accumulated accordingly39,44. However, the linear regression results showed that some toxic trace elements showed a significant negative correlation with the particulate matter content when the particle size was less than 2.5Ā Āµm. This result indicated the toxic trace element may be absorbed by plant leaves. Furthermore, it has been proved that plant species can affect the content of toxic trace elements in foliar particulate matter through their microstructures as well as particulate matter selection33. There is a finding that plant health also affects their ability to retain particulate matter. At the same time, particles can also affect plant growth, photosynthesis, respiration, and transpiration when the particles on the leaf surface reach a certain amount45. Therefore, the differences in foliar PM retention capacity and toxic trace element accumulation in PM can also be attributed to uncertainties associated physical and chemical processes involved in plantā€“particles interactions.

In our study, the phenomenon of a closely association between toxic trace elements in leaf PM was comparable to the results of most studies46,47,48,49. Even though the plant leaf samples were collected in the same timeā€“space, there were some discrepancies in the sources of PM even in the same area, for instance, roadside PM may originate from car exhaust emissions or road PM36. There are records suggesting that Cd, Cu, Pb, and Zn generally originate from road PM50,51, while vehicle exhaust emissions bring As, Cd, and Pb52,53. The highly significant correlation between As and Cd in all particle sizes in this study further confirms the above statement and also illustrates that PM retention on plant foliage can reflect fairly well the sources as well as the distribution of toxic trace elements in the environment of roadsides54,55.

Conclusions

In this study, P. macrophyllus had the strongest ability to retain PM, and C. camphora excelled in retaining PM2.5. The combination of P. macrophyllus and C. camphora is highly recommended to be planted in subtropical cities to effectively reduce PM. PM size and plant species and their interactions played an important role in the toxic trace element concentration of foliar particulate matter. Additionally, the toxic trace element concentration of foliar particulate matter is co-dependent on the physiological characteristics of the plant itself as well as environmental sources. The plants can predict the source of PM by toxic trace elements. This study provides a new reference for city greening and air pollution control.

Materials and methods

Study area

Changsha is located in the eastern part of Hunan Province (111Ā° 53ā€²ā€“114Ā° 15ā€² E, 27Ā° 51ā€²ā€“28Ā° 40ā€² N), which is in the low latitude zone with a subtropical monsoon climate. The annual average temperature is 17.2Ā Ā°C, and the annual precipitation is 1361.6Ā mm in the city. The annual average PM2.5 concentration in 2017 was higher than the limit value of the Chinese Secondary Standard of Environmental Air Quality Standards (GB 3095-2012) (35Ā Ī¼g/m3), and the annual average PM10 concentration is equal to the limit value of the Chinese Secondary Standard of Environmental Air Quality Standards (GB 3095-2012) (70Ā Ī¼g/m3).

Sample collection

By surveying greening tree species in Changsha, we selected six typical evergreen broad-leaved and coniferous greening tree species in Changsha to monitor and analyze their PM retention capacity, including four arbor species: Cinnamomum camphora, Osmanthus fragrans, Magnolia grandiflora and Podocarpus macrophyllus, and two shrub species: Loropetalum chinense var. rubrum and Pittosporum tobira (Table 2). The plants we selected were not listed as national and provincial key protected wild plants in China nor threatened species on the IUCN Red List. Therefore, no specific permissions or licenses were needed for the sampling of plants for research purposes according to the regulations of the Peopleā€™s Republic of China on the protection of wild plants. During the sampling process, we followed the local sampling guideline to ensure no substantial harm to the collecting individual. The plant leaf samples were collected on both sides of the main roads (Shaoshan Road and Furong Road) in Changsha City (Fig.Ā 5) on December 25, 2017, when there was no previous rainfall for more than 7Ā days. The width of the green belt was about 3Ā m, and the plants in the green belt included arbors, shrubs, and herbs with consistent habitat conditions. To avoid the impacts caused by the differences in location and distance, the samples were selected within 3Ā m from the road and all samples were collected within 1Ā day. The height of sampling was 2ā€“6Ā m for arbors and 0.5ā€“3Ā m for shrubs. For each species, ten trees were selected as samples, and the leaves were collected randomly in four different directions (east, west, south, and north) at the upper, middle, and lower positions of the tree canopy. The leaves collected are required to be healthy and free of pests and diseases. After sample collection, the samples were carefully stored in sealed plastic bags and immediately transferred to a refrigerator at 4Ā Ā°C for subsequent experiments and analysis. Meanwhile, the diameter at breast heightĀ (DBH) and basal diameter (BD) of plants were measured with a diameter at breast height ruler, the height of each tree was measured with a height measuring device, and the width of the crowns was measured with a ruler in two directions: northā€“south and eastā€“west.

Table 2 Basic information of the investigated tree species.
Figure 5
figure 5

Location of the research areas. ā€ Software&Versionļ¼šQGIS 3.32.0. URL:https://server.arcgisonline.com/arcgis/rest/services/World_Imagery/MapServer/tile/{z}/{y}/{x}.

Extraction and processing of foliar particulate matter

The retention of particulate matter on the surface of plant leaves was determined by using the microporous membrane weighing method53. The number of test leaves was determined according to leaf size and type to ensure that the experimental leaf samples were adequate and randomized, and three replicates of each plant were required. In general, the larger leaves in broadleaf needed 30ā€“50 pieces, and the smaller leaves needed 150ā€“300 pieces. Put the selected plant leaf samples into a beaker with deionized water for half an hour, and then carefully clean all the PM on the leaves with a small brush. Next, pinch out the leaves with pointed tweezers (be careful not to damage the leaves) and rinse them three times with an appropriate amount of deionized water, then put them on newspaper to dry. Finally, the dried leaves were scanned with a scanner (Epson scanner 11000G) to obtain the leaf projection, and export all the leaf scanned images, then opened Image J software, the edges of the leaves were circled and the leaf area was calculated by the software. To reduce the error, the area of each leaf needed to be calculated three times and get the average value.

The solution was filtered through the dried and weighed microporous membrane of 10Ā Ī¼m pore size, and then the filtrate was filtered through the dried and weighed microporous membrane of 2.5Ā Ī¼m and 0.1Ā Ī¼m pore size to obtain three different particle size levels of PM>10, PM10 and PM2.5 using the same procedure as above. Before and after each filtration, the microporous filter membrane was put in an oven at 60Ā Ā°C31 and dried to a constant mass (two measurementsā€‰ā‰¤ā€‰0.0002Ā g), and weighed on a balance with an accuracy of one ten-thousandth.

The plant leaf PM retention was determined by the mass difference method. The calculation method was as follows:

PM retention per unit leaf area (g/m2):

$${\text{M}} = \left( {{\text{M}}_{{2}} - {\text{M}}_{{1}} } \right)/{\text{S}}$$
(1)

In the formula, M is the retention of particulate matter per unit leaf area (g/m2); M1 is the dried mass of filter membrane before filtration (g); M2 is the dried mass of filter membrane and particulate matter after filtration (g); S is the total area of test leaf samples (m2).

Toxic trace element accumulation of foliar particulate matter

The content of toxic trace elements in PM of plant leaf surface was determined by aqueous solubilization digestion. Approximately 0.2Ā g of filter membranes were digested in a glass tube with HNO3 and HCl mixture (1:3 v/v ratio) using a graphite heater furnace (Polytech PT60, Polytech 3 Instrument, Beijing, China) and kept the mixture in a slightly boiling state for 2Ā h. Then the content of toxic trace elements in the digestion solution was determined by the Inductively coupled plasma optical emission spectrometer (ICP-OES, Optima 8300, USA), and the detection limit of this instrument is 0.001ā€“0.1Ā mg/L. The national standard GSS-5 (Hunan soil) was selected for quality control and the measured standard recoveries ranged from 85.1 to 114%. In this experiment, As, Al, Cu, Zn, Cd, Fe, and Pb, which are common toxic trace elements in PM, were measured. The standard solutions were selected from the national standard samples of single-element standard solutions: As (GSB 04-1714-2004), Al (GSB 04-1713-2004), Cu (GSB 04-1725-2004), Zn (GSB 04-1761-2004), Cd (GSB 04-1721-2004), Fe (GSB 04-1726-2004) and Pb (GSB 04-1742-2004), with the concentration of 1000Ā Ī¼g/ml.

Statistical analysis

One-way ANOVA was used to compare the differences in the PM retention capacity of different plants. Two-way ANOVA was used to reveal the underlying drivers of toxic trace element concentrations in particulate matter. Linear regression was used to explore the relationship between toxic trace element concentrations of particulate matter and the ability of the foliage to retain particulate matter. Correlation analysis based on Pearson's method was used to examine the association among different toxic trace elements. GraphPad Prism 8 as well as the R-based packages "ggplot2" and "GGally" were used for data visualization. All statistical analyses in our work were done in R 4.1.1 (R-Core-Team, 2013).

Ethical approval

All procedures were followed in compliance with institutional, national, and international rules and legislation. The plants we selected were not listed as national and provincial key protected wild plants in China nor threatened species on the IUCN Red List. Therefore, no specific permissions or licenses were needed for the sampling of plants for research purposes according to the regulations of the Peopleā€™s Republic of China on the protection of wild plants.