Tree Species As Bioaccumulator Of Heavy Metals In Polluted Arid Environments: Samplings Made In Spring, Summer And Autumn

The accumulation of heavy metals (Zn, Cu, Pb and Cd) in leaves and barks of five common tree species in the city of Gabès, Tunisia were investigated for a comparative study. Samplings were performed during spring, summer and autumn. The ability of trees to accumulate a certain HMs from soil, the ability for comprehensive accumulation of multiple HMs and the total metal accumulation capacities were evaluated using bioconcentration factor (BCF), comprehensive bio-concentration index (CBCI), and metal accumulation index (MAI), respectively. The results indicated that all the elements that measured were found to be at high levels in bark samples. Casuarina equisetifolia with the highest accumulation for single metal (BCF) have the highest CBCI but not the highest MAI. According to total accumulation capacities, Eucalyptus occidentalis, Casuarina equisetifolia and Tamarix aphylla can be used as a good bioaccumolator for investigated HMs and a suitable tree species for soil and atmospheric phytoremediation in arid areas subjected to industrial and traffic pollution.

The global industrial revolution has led to an unprecedented dissemination of toxic substances in the environment (Seid Mohammed et al., 2011 book chapter). Contamination of air and soil by toxic heavy metals remains to be the main concern of numerous environmental studies and recieve a great deal of focus worldwide (Pulford and Waston, 2003 review; Ugolini et al., 2013; Janta and Chantara, 2017; Jeddi and Chaieb, 2018). In urban environments, heavy metals like Zn, Cu, Pb and Cd can be generated from different anthropogenic sources including industry, combustion of fossil fuels in vehicular traffic, and energy production (Sawidis et al., 2011). Through the high toxicities at alarming levels, the rapid environmental deterioration of urban areas has already threatened human lives and development in arid regions (El-Hasan et al., 2005; Ben Abdallah et al., 2006a; Al-Khashman et al., 2011; Boukhris et al., 2015; Farahat et al., 2015; Jeddi and Chaieb, 2018). Non-biodegradable HMs, can be transferred into plant tissue from the air and soil, and accumulate in the food chain, even in relatively trace quantities (Shahid et al. 2017). Consequently, these conditions have resulted in enormous deteriorating impacts on human health (Arora et al. 2008).

Extensive research has been conducted on the possibility to use tree plants as effective biomonitors or bioindicators of environmental pollution (Celik et al., 2005; Sawidis et al., 2011; Hu et al., 2014; Norouzi et al., 2015; Alhabadi et al., 2017). In contrast to lower plants (fungi, algae, lichens or mosses), trees can be found growing in a number of different countries as the main plant type of polluted urban areas (Sawidis et al., 2011). These plants are able to absorb and accumulate significant quantities of potentially toxic substances, mostly on their outer organs such as foliage and bark (El-Hasan et al., 2005; Hu et al., 2014; Alahabadi et al., 2017). Celik et al. (2005) noted that elemental analysis of tree bark and leaves can be considered as useful and cost-effective way to protect vulnerable urban areas. Due to the excellent availability and long lifetime of trees, a replication of the examination is possible after a few decades (Pluford and Waston, 2003 review phytorem).

According to the literature, there are numerous examples of tree species that have been used successfully to monitor air and soil pollution of urban environments, e.g. Cupressus sempervirens (El-Hassan et al., 2005; Farahat et al., 2015), Populus tomentosa, Sophora japonica and Catalpa speciose (Liu et al., 2007), Phoenix dactylifera (Al-Khashman et al., 2011), Quercus ilex (Ugolini et al. (2013), Platanus orientalis (Norouzi et al., 2015) and Cassia fistula (Janta and Chantara, 2017). These research findings indicated that the capacity of accumulation through dry or wet deposition or absorption, depends not only on the spatial distribution of the trees, time of exposure and climate, but also on the species features, such as leaf area and surface texture.

Situated in the southeast of Tunisia, Gabès is a typical urban city which suffer from high traffic density. Furthermore, there are medium-sized industrial phosphate activities in the eastern part of the city, which have a local effect on the urban environment pollution. The Gabes region presently is considered one of the most polluted areas in the Mediterranean Basin, according to a recent study carried out by the Facility for Euro-Mediterranean Investment and Partnership (FEMIP) and the World Bank (El Zrelli et al., 2015).

In Gabès city, evergreen trees are a typical urban plants growing over large areas such as roadsides in both industrial and suburban areas. However, to date, the biomonitoring metal pollution approach by using trees has received little attention and most of the investigations conducted are still unpublished reports. With large anthropogenic activities, there is a need to evaluate the potential of tree species to remove HM contaminants from this polluted urban envirenment. Therefore, the purpose of the present study were: 1) to assesss the concentrations of certain HMs (Zn, Cu, Pb and Cd) in the leaves and barks of five common tree species in the city of Gabès, Tunisia, 2) to select the best tree species for single HM accumulation in the leaf and bark using bio-concentration factor (BCF), 3) to evaluate the total accumulation capacities of HMs for selected tree species using comprehensive bio-concentration index (CBCI), and metal accumulation index (MAI) and 4) to propose suitable tree species for soil and atmospheric phytoremediation in arid urban areas.

The concentrations of Zn, Cu, Pb and Cd (mg kg-1 DW) in the tree leaf and bark samples in three seasons are shown in Fig. 2. The highest concentrations of HM were measured in summer compared to spring and autumn (rainy seasons). The seasonal trends for elemental metal concentrations had been reported previously (Nourouzi et al., 2015; Alahabadi et al., 2017). Nourouzi et al. (2015) reported that Pb, Cu and Zn concentrations was added each month to leaf surfaces and persisted unmovable, unless partially or totally removed by the rain event. Similarly, Alahabadi et al. (2017), noted that the atmospheric precipitations in spring and autumn wash out the particulate matters from the surfaces of leaf and bark.

In the current study, the metal concentrations in bark were significantly higher than the concentrations in leaves (PDiverse studied plant species has fluctuating metal concentrations, and no specific species had the highest concentrations for each of the investigated heavy metals. As shown in Table 1 and 2, the maximum seasonal mean concentration of Zn in the leaf and bark were found respectively, in Casuarina and Eucalyptus. For Cu, the maximum concentration in the leaf and bark was measured in Casuarina and Tamarix. For both Zn and Cu, the minimum seasonal mean concentrations in the leaf and bark were associated in Acacia and Cupressus species, respectively. Zn similar to Cu, is a minor trace metal crucial for all organisms and play an important role in biosynthetis (Serbula, 2012). Typically, concentrations of Zn and Cu in plants were less than 150 and 30 mg kg-1, respectively (Kabata-Pendias and Pendias, 2001). In the present study, the concentrations of Zn and Cu in the investigated plants were within the normal range.

For Pb, the maximum concentrations in the leaf and bark were measured in Eucalyptus and Casuarina respectively, while the leaf and bark of the Cupressus have minimum seasonal mean concentrations of Pb. Lead pollution is caused, in a large scale, by emissions from motor vehicules using leaded gasoline (Al-Khashman, 2011 palm). The conventional Pb concentration in plants is in the range of 5 – 10 mg kg -1 and its toxic concentration is from 30 to 300 mg kg -1 (Kabata-Pendias and Pendias, 2001). In this study, none of tree species have Pb concentration outside of the normal range.

Eucalyptus occidentalis showed the maximum seasonal mean concentrations of Cd in leaves and barks when the minimum seasonal mean Cd concentration in leaves and barks was observed to be related to Cupressus sempervirens. According to Hu et al. (2014) there is a close relationship between Cd concentrations and vehicle wheels, combustion of vehicle lubricating oil and usage of waste mud. In our study, Cd show low concentrations, far from the pytotoxic level of 5 mg kg -1 (Kabata-Pendias and Pendias, 2001).

The concentrations of metals measured in the surface soil are given in Table 1. The total contents of HMs varied in the following order : Zn > Pb > Cu > Cd. According to Kabata-Pendias (2011), soils from our study site contained Zn, Pb,Cu and Cd at levels within the normal range.

Bio-concentration factors were calculated in order to evaluate the ability of tree species to uptake single HM (Alagić et al., 2013; Zhai et al., 2016). Mean values of BCF for the leaf and bark samples are given in Fig 3. On the average, all investigated HM had values of BCF for the bark significantly higher than values of BCF for leaf. The maximum BCF of Zn and Cu in leaf samples were related to Casuarina (1.3 and 0.97, respectively) and in bark samples were related to Eucalyptus (2.08) and Tamarix (1.98), respectively. For Pb, the maximum BCF values of both leaves and barks were found respectively, in Eucalyptus (1.88) and Casuarina (2.03). For Cd, Eucalyptus occidentalis showed the maximum BCF in leaves (0.23) and barks (1.52). Due to their large accumulating ability, the following species can be recommended for phytoextraction of investigated HMs. Of the five species assessed, Eucalyptus occidentalis has the maximum capability to accumulate single HM, however, it has not the maximum ability to accumulate multi HMs.

The Bio-concentration factors > 1 shows a special ability of the plant to absorb from soils and transport metals and stock them in their above-ground part (Brown et al., 1995). In this study, and in accordance with several previous works (Farahat and Linderholm, 2015; Janta and Chantara, 2017), most of the investigated tree species showed BCF for Zn, Pb, Cu and Cd > 1 for leaf and/or bark; therefore, they are considered as an accumulator for these metals.

Giving to the calculated BCF mean values, the aptitude of tree species for accumulation of HM was in the order of Pb > Cu > Zn > Cd. Xue et al. (2013) reported that plant species, heavy metal concentrations in the environment, and other environmental factors could collectively influence the accumulation of heavy metals in plants.

Comprehensive bio-concentration index (CBCI) was applied to assess the ability of multi-metal accumulation of plants. In the current study, differences between CBCI values corresponding to all investigated tree species were statistically significant (Table 3). The maximum CBCI of both leaves and barks were related to Casuarina equisetifolia (3.56 and 2.81, respectively) and Tamarix aphylla (2.89 and 2.76, respectively) . These values are higher than those reported by Zhao et al. (2014) for Amorpha fruticosa (2.72 in leaves), but much less than those of Pinus eldarica (6.72 in leaves) and Wistaria sinensis (8.42 in barks; Alahabadi et al., 2017). Zhao et al. (2014) reported that woody species with higher CBCI values should be given serious consideration for phytoremediation.

According to the calculated CBCI values, although Casuarina has the maximum ability to accumulate multi-HMs, it is not the best option for greening urban areas. Tamarix aphylla followed Casuarina as a HM accumulator, however, this native Mediterranean species represents a good alternative when native species are a priority. Fernandez et al. (2016) noted that the best option for every region is to choice native plant species even with lower ability in place of non-native species with higher ability for HMs extraction. Gabes, an arid region, can be characterized as a hostile environment with a fragile ecosystem. The introduction of exotic tree species is common for greening urban landscapes. However the introduction of exotic species has many problems, such as high cost, low survival rates and ecological invasion (Richardson, and Rejmánek, 2011 art allelop).

The MAI values for the studied tree species are resumed in table 3. Significant differences were found between MAI corresponding to leaves and barks for all tree species. The maximum MAI values of leaves displayed in Eucalyptus (7.36) and Casuarina (6.03), and maximum values corresponding to barks were in Tamarix (8.17) and Eucalyptus (7.63). These maximum MAI values are far less than those reported previously by Liu et al. (2007) for Catalpa speciosa (53.8 in leaves), but higher than those of Sabina chinensis and Juniperus formosana (respectively, 3.89 and 3.32 in leaves) as reported by Hu et al. (2014).

Foliar characteristic such as mass, area, as well as surface morphology can affect leaf potential to trap airborne pollutants (Sawidis et al. 2011; Rodriguez et al., 2012): as the larger and rougher the leaf’s surface, the greater the accumulation of HMs. Hu et al. (2014) and Alhabadi et al. (2017) suggested that trees growing low to the ground or broad-leaves ones should be used more frequently as barriers between polluted and susceptible environment. Therefore, tree species such as Eucalyptus occidentalis, with the large surface leaves, and Tamarix aphylla, with leaves more exposed to soil splash, can be used for the bio-monitoring of the HMs contaminations in the urban areas.

In the current study, the MAI values of Cupressus sempervirens, with needle growing high to the ground, were lesser than those in all investigated tree species (2.87 for leaves and 4.56 for barks). Sawidis et al. (2011) noted that leaves of Gymnosperm with a thick impermeable cuticule, which forms a smooth sheet over the epidermal cells, show to some degree a resistance to HM uptake.

In conclusion, according to the values of CBCI, Casuarina equisetifolia had the highest ability to accumulate HMs from soil. Moreover, MAI values indicated that Eucalyptus occidentalis, Casuarina equisetifolia and Tamarix aphylla had the highest ability to accumulate HMs from ambient air. A higher accumulation of HMs was found in bark compared to leaves. The maximum BCF values of Zn, Cu, Pb and Cd for leaves were found in Casuarina equisetifolia and Eucalyptus occidentalis, and for barks the maximum BCF values of Zn, Cu, Pb and Cd were found in Eucalyptus occidentalis, Tamarix aphylla and Casuarina equisetifolia species. Therefore, these tree species can be used as a good bioaccumolator for investigated HMs. Their high accumulation capacity can also indicate their application potential for the bio-monitoring of the HMs contaminations in the urban environment. At last, according to our results, Eucalyptus occidentalis, Tamarix aphylla and Casuarina equisetifolia species can be considered as a suitable tree species for soil and atmospheric phytoremediation in arid urban areas.