Ecotoxicology DOI 10.1007/s10646-014-1251-5
Heavy metal concentrations in timberline trees of eastern Tibetan Plateau Ji Luo • Jia She • Peijun Yang • Shouqin Sun Wei Li • Yiwen Gong • Ronggui Tang
•
Accepted: 25 April 2014 Ó Springer Science+Business Media New York 2014
Abstract Concentrations of 14 heavy metals (Ag, As, Cd, Co, Cr, Cu, Hg, Mo, Ni, Pb, Sb, Tl, V, and Zn) in needles, twigs, bark and xylem of spruce and fir collected at the timberline of eight sites along the Hengduan Mountains, eastern Tibetan Plateau, are reported. Twigs had the highest concentration for most of elements, while xylem had the lowest concentration. The connections between elements in twigs were much richer than other organ/tissues. Pb, Ni, As, Sb, Co, Cd, Hg, Cr and Tl which are partly through anthropogenic sources and brought in by monsoon, have been accumulated in twigs and needles by wet or dry deposition in south and east sites where are within or near pollutant sources. Under moderate pollution situation, vegetation are able to adjust the nutrient element (Cu and Zn) cycle rate, thus maintain a stable concentration level. Seldom V, Ag, and Mo are from external anthropogenic sources. Needles and twigs can be used as biomonitors for ecosystem environment when needles can simply distinguish the origin of elements and twigs are more sensitive to extra heavy metal input.
J. Luo J. She (&) S. Sun W. Li Y. Gong R. Tang Key Laboratory of Mountain Surface Processes and Ecological Regulation, Institute of Mountain Hazards and Environment, Chinese Academy of Sciences & Ministry of Water Conservancy, #9, Block 4, Renminnan Road, Chengdu 610041, China e-mail: [email protected] J. She R. Tang University of Chinese Academy of Sciences, Beijing, China P. Yang School of Biological Sciences and Engineering, Shaanxi University of Technology, Hanzhong, Shaanxi, China
Keywords Heavy metals Timberline Eastern Tibetan Plateau Biomonitor Transect Anthropogenic source
Introduction Elements in plant tissues have been a hot topic in many subjects such as plant nutriology, environmental science and ecology (Peterjohn and Correll 1984). With the development of human civilization, human activities brought about the increasingly serious environmental problems, heavy metals emitted into the atmosphere and the resultant hazards to vegetation and human life are becoming a matter of great concern (Sun et al. 2010). Plants may accumulate heavy metals by absorbing them either from airborne contaminants, or soil (Chen and Guan 1998; Markert 1993). Different organs or tissues differ in their capacity to accumulate elements. Sun et al. (2011) have compared concentrations of 23 elements in fir leaves and twigs, they found that most of the elements were more significantly enriched in twigs than in leaves. The study of Fan et al. (2006) have found the similar regular that twigs of Pinus taeda had the strongest accumulation ability than leaves and xylem. While Chen and Guan (1998) found that the general order of organs of seven phytocoenosiums for heavy metal concentration were leaves, bark, twigs and trunk. Tree species play an important role in determining heavy metal distribution in plants. Understanding heavy metal distribution in vegetation is the basis of the study of heavy metal dynamics in plants. Higher plants, particularly spermatophytes, have been frequently used as accumulative bioindicators of heavy metals (Markert 1993). Coniferous needles and bark has the ability to absorb heavy metals immediately from atmosphere, resulting in higher concentrations in places
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with anthropogenic airborne contamination (Chen and Guan 1998). Many studies have found the significant correlations between leaves and the ambient pollutant concentration, but no significantly relationship between leaves and the concentrations in soil (Kord et al. 2010), indicating that leaves are suitable biomonitors of air pollution (Aboal et al. 2004; Tomasˇevicˇ et al. 2008). Twigs are also proved as important indicators for heavy metal pollution (Rossbach and Jayasekera 1996; Wu 2006). Tree bark and trunk must be carefully and skillfully used as indicators for long term air pollution or the history of pollution (Gue´guen et al. 2011; Koma´rek et al. 2008; Patrick and Farmer 2007). A study on Pb concentration in urban forest community in pearl river delta showed that the average concentrations of leaves and twigs in experimental plot were higher than control plot, while that of trunk were similar, proving a representative example for tissues of the different response to pollution and different abilities as biomonitors (Wu 2006). Under natural conditions, few researches about heavy metal contamination press on trees at a large scale (up to n 9 104 km2) have been carried out. A typical series of studies in Europe were carried by Reimann et al. (2001, 2007a, b), who studied on higher plants such as birch, mountain ash, and spruce that were indigenous along certain anthropogenic or geogenic concentration gradients in northern Europe. They found that in the natural conditions, bedrock lithology, ore occurrences, soil pH and urban contamination all have a visible influence on the element concentrations in trees, and it is often impossible to differentiate between all the factors that can influence element concentrations. The eastern Tibetan Plateau, as the border of the first level ladder and second level ladder of China, as well as the transition zone of Pacific Ocean and Mediterranean Sea, presents with series of north–south mountains with special conditions of natural geography and unique topographic features (Zheng and Shen 2002). Though the region is remote from anthropogenic activities, once heavy metals brought into these remote mountain areas by long-range atmospheric transport, the ecosystem stability (especially to the fragile timberline forest) and downstream will be under threat (Begum et al. 2005; Wu et al. 2011). In previous aerosol studies on the Tibetan Plateau, it has been reported that elements in particulate matters, rainwater or soil in Tibetan Plateau with EF values higher than ten for Co, Pb, Ni, As, Sb, Cd, Hg, Cr, Tl, Cu, Zn and Ag were observed, and considered from anthropogenic origin, partly transported from the heavily polluted northeast Indian and central Asia by means of air mass back trajectories analysis during the summer monsoon season (Basha et al. 2010;Cong et al. 2007, 2010; Hopkea et al. 2008; Peterjohn and Correll 1984; Yang et al. 2009; Li et al. 2007; Zhang
123
et al. 2012b). Moreover, southwest China, for example, southeast Sichuan province, is also a strong source of PM10 and PM2.5 (Yang et al. 2009). However, during the nonmonsoon periods, particle-bounded pollutants can be barely transported into the Tibetan Plateau from outside (the Sahara Desert or the Thar Desert) (Li et al. 2012). Most of studies about heavy metals in eastern Tibetan Plateau concentrated on soil and air, how will anthropogenic contaminant influence heavy metals in plants? There have been few studies. The aim of this work is to understand the distribution of different elements in different plant organs and tissues, the contamination press of heavy metals on vegetation, the accumulation way and possible sources of certain element, and the suitability of spruce and fir as biomonitors of anthropogenic influence.
Materials and methods Site description The study area is located in the middle of Hengduan Mountains, eastern Tibetan Plateau, China. Hengduan Mountainous Region is one of the youngest tectonic units of the Tibetan Plateau, and the transitional fringe area from Tibetan Plateau to west Sichuan Basin and center Yunnan Plateau (Gao and Li 2000). Mountains are in the north and south trend, with nearly 900 km long, 4,000 to 5,000 m above sea level, and with commonly 1,000 m or more elevation difference between mountain valleys. It presents complex diversity of natural environment, biology, minority, society, culture and economy. Generally, Hengduan mountains are mainly controlled by two climate systems: one is westerly of the northern hemisphere, carrying less water vapor; the other is monsoon system, including the southwest monsoon of bay of Bengal and Indian Ocean, and the southeast monsoon from western Pacific, which is the main precipitation air mass (Li et al. 2010). What’s more, this area is also affected by the local circulation of plateau monsoon (Li and Su 1996). These climate systems result in two obvious seasons: the dry season and the wet season. The dry season is between the middle of October and the middle of May next year, with scarce rainfall, long sunlight, high evaporation, and dry air, which is mainly dominated by westerly. The wet season is between the middle of May and the middle of October, air mass mainly comes from southeast Sichuan province and northeast India, characterized by relatively higher temperature and humid weather, resulting in above 85 % rainfall (mainly concentrated in June, July, and August) during this period (some regions are even above 90 %) (Cong et al. 2010; Yang et al. 2009). Under its special geographical position and topography, this mountain region forms a
Heavy metal concentrations in timberline trees
Fig. 1 Location of the sampling sites: Transect A (S1, S2, S3, and S4) and Transect B (S5, S6, S7, and S8)
diverse and regular vertical climate change that is ‘‘spring at the foot, ice and snow on the peak, one mountain at four seasons, and different weather within 10 km’’ (Luo et al. 2013a). Sampling sites were selected in timberline of eight sites in Hengduan Mountains (Fig. 1) owing to timberline’s easy contamination acceptance (Takahashi et al. 2012). The dominant species are spruce in S3, S4 and S5, and fir in other sites. At the basis of the eight sites, we set two parallel northwest-southeast belt transects, each parallel belt transect had 4 typical sites, that is Transect A (TA), consisting of S1, S2, S3, and S4, and Transect B (TB), consisting of S5, S6, S7, and S8, to estimate the diversity of north and south; and two clusters of sites, each cluster also had 4 sites, that is the northwest sites (NW), consisting of S3, S4, S5 and S6; and the southeast sites (SE), consisting of S1, S2, S7 and S8, to estimate the diversity of northwest and southeast. Soil types are brown coniferous forest soil for all sites. The pH value of top soil (0–20 cm) were between 3.85 and 5.08. Mt. Gongga (S1) is the main peak of Hengduan mountains, which is close to urban and suburban areas. Sampling and preparation The dominant timberline tree species are fir (in S1, S2, S6, S7, and S8) or spruce (in S3, S4, and S5). Fir and spruce are two species with similar physiology and morphology. Yanai et al. (2009) have found that the Engelmann spruce and subalpine fir were indistinguishable in nutrient uptake, specific root length and diameter distribution, so data from the two species are thought to be comparable. To avoid
possible seasonal influences, all samples were collected within as short a time span as possible in July and August, 2011. Before sampling, preliminary observation on topography and forest form were conducted. In each stand, three 20 9 30 m plots were established. Each plot consisted of twenty-four 5 9 5 m quadrats. Twelve quadrats in each plot were randomly selected for sampling (Luo et al. 2013b). In each plot, mature needles, twigs, xylem and bark from its dominant specie (spruce or fir) were collected separately as four composite samples from twelve quadrats randomly selected. Needles and twigs were collected at the same branches in all directions. Xylem samples were extracted at breast height (approximately 1.5 m) as a chunk of wood and outside portion of the trunk. Bark was carefully removed from the boles of the trees at an average height of 1.5 m above the ground. Trace-element and powder-free vinyl gloves (one new pair per sample material) were used during sample collection (Reimann et al. 2007a). Different trees had almost the same size and age. The total number of collected samples was 96. Samples were separately collected into clean cellulose bags and stored them with cooler. After the samples were brought to the laboratory, they were carefully washed with tap water to remove coarse particles, then were washed with distilled water three times to remove adhering particle. After air drying, all samples were oven dried to a constant weight at 40 °C. Then samples were cut to the length of less than 2 mm and pulverized to pass through a 100-mesh screen in a mild steel mill. Finally, all samples were spread into contamination-free polyethylene plastic bags and labeled respectively.
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Heavy metal analysis Plant samples were dissolved in a microwave-assisted nitric acid, hydrogen peroxide, and hydrofluoric acid digestion (The Analyzing and Testing Center, Nanjing Institute of Geography & Limnology, Chinese Academy of Sciences) (Wu et al., 2011). Then solutions were analyzed using Inductively Coupled Plasma Mass Spectrometry (ICP-MS) (77009, Agilent Technologies, America) for 14 heavy metals (here, we consider As as heavy metal since it has similar damaging effects to environment and humans as that of heavy metals): the essential nutrients Cu, Zn, Ni, and Mo, and nonessential trace elements Ag, As, Cd, Co, Cr, Hg, Mo, Pb, Sb, Tl, and V. The analysis method refers to Inductively Coupled Plasma Mass Spectrometry, USA EPA Method 6020a (Revision 1, February 2007). The detection limits are: Ag (0.005 mg L-1), As (0.01 mg L-1), Cd (0.005 mg L-1), Co (0.001 mg L-1), Cr (0.01 mg L-1), Cu (0.003 mg L-1), Hg (0.01 mg L-1), Mo (0.01 mg L-1), Ni (0.005 mg L-1), Pb (0.01 mg L-1), Sb (0.001 mg L-1), Tl (0.005 mg L-1), V (0.002 mg L-1), Zn (0.003 mg L-1). When calculating, if a value is lower than the detection limit, we use the detected limit value instead. Standard solution SPEXTM (SPEX Certi-Prep) from USA was used as the standard. Quality control was ensured through the triplicate analysis of two reference materials. Plant reference materials were from the National Quality and Technology Supervision Agency of China (GBW07603 and GBW07604). Precision was good with the coefficient of variation (CV) below 5 % for the measurement and recoveries between 90–115 %.
Fig. 2 The weighted average concentration of heavy metals in aboveground part of spruce and fir of the eight sites (n = 8). The weighted average concentration of an element in one site was calculated as the quotient of total element storage and total biomass of aboveground part
organ/tissue biomass. Then the weighted average concentration is calculated as the quotient of total element storage and total biomass of aboveground part (compose of needles, twigs, bark, and xylem) in fir or spruce. Data of organs and tissues biomass were based on Zhong et al. (1997)’s research in a near-mature forest, that the biomass ratio of needles: twigs: bark: xylem was about 2:13: 9: 76. Annual precipitation data of the eight sites were acquired from the local meteorological stations.
Results Statistical analysis Statistical analyses were performed using SAS 9.1 software. Difference analysis of different organs/tissues for certain element concentration were determined by Student– Newman–Keuls (SNK) Test with the significance level set as P \ 0.05. Other difference analysis were carried out using one-way ANOVA followed by LSD. A probability value of less than 0.05 was regarded as significant. Correlation analysis between elements in different organs and tissues were carried out in linear dependence. Cluster analysis of 14 elements in needles and twigs were carried out using PASW Statistics 18.0 software. Before computing proximities, standardization was performed, which can be automatically done by the hierarchical cluster analysis procedure. Cluster analysis was applied to the standardized data using between-groups linkage method. A dendrogram was constructed to assess the cohesiveness of the clusters formed, in which correlations among elements can readily be seen. The storage of an element in certain organ/tissue was calculated as the product of element concentration and
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Concentrations of different elements in aboveground part of spruce and fir As we calculated the weighted average concentration in a certain site, average element concentrations of the eight sites were shown in Fig. 2. Elements ranged as: Zn [ Cu [ Pb [ Ni [ Cr [ V [ Co [ As [ Sb [ Cd [ Mo [ Tl [ Ag [ Hg. In certain tissues and organs, elements ranged as: in leaves: Zn [ Cu [ Pb [ Ni [ V [ Cr [ Sb [ Co [ As [ Mo [ Cd [ Tl [ Hg [ Ag; in twigs: Zn [ Cu [ Pb [ Ni [ Cr [ V [ As [ Co [ Sb [ Cd [ Mo [ Tl [ Ag [ Hg; in bark: Zn [ Cu [ Ni [ Pb [ Cr [ V [ Co [ Cd [ As [ Sb [ Tl [ Mo [ Hg [ Ag; in xylem: Zn [ Cu [ Ni [ Pb [ Cr [ V [ Co [ Sb [ Cd [ Mo [ As [ Tl [ Ag [ Hg. No matter in aboveground part or certain tissue/organ, the nutrient Zn and Cu had the highest concentration. Ni concentration was also much higher than all trace metals except Pb. However, Mo concentration was very low, it was even not detected at four sites in xylem. For trace elements, Pb, Cr and V concentrations were the highest. It
Heavy metal concentrations in timberline trees
Fig. 3 Average concentrations of different heavy metals in different organs and tissues (n = 8). Different letters denote significant differences among means (a = 0.05) as determined by Student–Newman–Keuls (SNK) Test
is noteworthy that Pb concentration in needles, twigs and aboveground part were higher than micronutrient Ni, though Pb is considered as a nonessential element. Co, As, Sb, and Cd concentrations did not have a regular rank, but all higher than Tl. Ag and Hg concentrations were the lowest among all elements. Element concentrations and storages in different organs and tissues Element concentrations in different organs and tissues were presented in Fig. 3. Element concentrations except Tl, Ag, Hg, Cd and Zn in twigs were significantly higher than that in needles, bark and xylem. For unessential trace elements, concentrations in xylem were the lowest, and were significantly lower than other tissues and organs for V, Co and As. For most of elements (Cu, Ni, Cr, V, Co, As, Sb, Tl, Ag and Hg), concentrations in bark and needles were comparable. Moreover, we estimated the proportion of certain element storage in certain organ/tissue on total element storage in aboveground part (Fig. 4). For most of elements (except V, Co and As), heavy metal storage in xylem accounted for higher than 40 % of total storage in
Fig. 4 Proportion of certain element storage in certain organ/tissue on element storage in aboveground part of spruce or fir. The storage of certain element was calculated as the product of mean element concentration of the eight sites and biomass of certain organ/tissue. The element storage in aboveground part was the sum of element storage in needles, twigs, bark and xylem
aboveground part. Another important storage place was twigs, with the proportion of higher than 20 % for most of elements (except Ag and Hg). Elements storages in needles and bark were relatively low.
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J. Luo et al. Fig. 5 Correlation analysis between elements in different organs and tissues. Solid line stands for significant correlation (R2 [ 0.5), while dotted line stands for general correlation(0.5 [ R2 [ 0.3). ‘Pre’ stands for precipitation
Furthermore, in order to find out the interrelationships of elements in certain organ/tissue, we performed correlation analysis between element concentrations, and between element concentrations and precipitation in different organs and tissues (Fig. 5). In the case of the very low concentrations of Mo, Hg and Ag in xylem, we didn’t consider any relationships between those elements in xylem. In twigs, all elements except Cu, Zn and Hg were closely correlated directly or indirectly. In needles, Cu, V, Mo and Ag had no relationship with other elements. In bark, Cr had no relationship with other elements. In xylem, when not considering Mo, Hg and Ag, Pb had no relationship with other elements.
Element concentrations in two transects and two clusters of sites Average element concentrations in TA and TB for needles and twigs were shown in Table 1. As a result, in twigs, V, Cr, Co, As, Sb, Hg, Pb and Tl concentrations in TB were higher than that in TA, while Mo and Cd in TA were higher than that in TB; in needles, only Co, As, Sb and Pb showed higher average concentrations in TB than TA. The significant differences in statistics were only detected for As in needles (P = 0.039) and twigs (P = 0.029). Average concentrations of northwest sites (S3, S4, S5 and S6) and southeast sites (S1, S2, S7 and S8) for needles and twigs were shown in Table 2. Result shows that elements except Cu, Zn, V and Sb in needles, and Cu and Zn in twigs, showed higher concentrations in southeast sites. Significant differences were found for Ni, Ag, Cd and Pb in twigs (P = 0.002, 0.006, 0.04 and 0.01 respectively).
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Discussion Heavy metals in aboveground part of spruce and fir The present study indicated large elements-dependent differences. Zn, Cu, and Ni concentrations ranged from 3.26 to 36.48 mg kg-1, 4.48 to 60.07 mg kg-1, and 0.44 to 5.81 mg kg-1 respectively, which is comparable to other studies of fir and spruce (Sun et al. 2011; Reimann et al. 2007a). Same as nutrient element, however, Mo concentration was much lower than above elements. In our study, Mo concentration ranged from 0.01 to 0.53 mg kg-1, which were also similar to Reimann et al. (2007a) and Sun et al. (2011)’s research, but significantly lower than other species of trees (Reimann et al. 2007a) and normal natural Mo concentration in plants(0.2–5 mg kg-1) (Kabata Pendias and Pendias 2001). The abnormal low Mo concentration in spruce and fir reflected the specificity of these species, or ascribed to low soil Mo concentration (\1.3 mg kg-1) in study area (Xie and Cheng 2008), challenging the necessary role of Mo to mature timberline spruce and fir trees. The exposure levels of heavy metals in soil or air, the bioavailability, uptake activity, and efficiency of translocation of metal ions, all determined the nonessential trace element concentrations in vegetation. (Clemens 2006; Nadgo´rska-Socha et al. 2013). It is noteworthy that Pb concentration in needles, twigs and aboveground part were higher than micronutrient Ni. It was reported that in industrial emission impacted areas, Pb concentrations in masson pine needles even exceeded Cu concentrations (Sun et al. 2010). It is true that in heavily polluted environment, plants are able to accumulate heavy metal to a high concentration level.
4.95
34.61–48.41
Sd
Range
21.17–52.39
Range
41.24
11.91
Ave.
35.16
13.87–26.34
Range
Sd
4.55
Ave.
20.77
8.83–36.42
Range
Sd
8.83
Sd
Ave.
22.73
Ave.
7.95–36.49
11.59
17.52
7.67–18.79
4.28
12.91
3.66–7.80
1.58
5.94
4.23–5.81
0.61
5.23
Cu
0.21–14.31
4.649
7.035
0.49–11.00
3.981
4.730
0.93–10.58
3.66
4.83
0.16–2.85
1.08
1.46
Pb
0.86–5.81
2.01
3.42
1.71–4.89
1.24
3.68
0.26–3.06
1.04
1.58
0.91–2.54
0.61
1.64
Ni
0.76–3.46
1.02
1.74
0.44–1.96
0.59
0.97
0.13–0.76
0.23
0.42
0.13–0.76
0.24
0.35
Cr
0.65–3.67
1.11
1.85
0.39–1.61
0.49
0.85
0.06–0.48
0.17
0.26
0.12–0.34
0.09
0.28
V
0.29–0.96
0.24
0.60
0.16–0.56
0.15
0.41
0.03–0.37
0.12
0.18
0.03–0.21
0.06
0.12
Co
b
a
38.83
7.40
27.62–48.84
Range
21.17–52.39
Range
Sd
11.38
Ave.
37.56
13.87–22.27
Range
Sd
3.17
Ave.
19.18
11.83–36.42
Range
Sd
8.79
Sd
Ave.
24.33
Ave.
SE means Southeast sites
NW means Northwest sites
SE
NW
Twigs
SEb
NWa
Needles
Zn
7.95–18.79
4.60
13.60
7.67–36.49
11.70
16.83
3.66–7.80
1.58
5.23
5.37–6.94
0.60
5.94
Cu
5.12–14.31
3.46
9.54
0.49–3.90
1.21
2.23
2.13–10.58
3.31
5.21
0.16–2.54
0.89
1.08
Pb
4.58–5.81
0.46
5.05
0.86–3.54
0.97
2.05
0.91–3.06
0.80
2.11
0.27–1.80
0.56
1.10
Ni
0.86–3.46
0.98
1.91
0.44–1.39
0.36
0.80
0.33–0.76
0.21
0.55
0.13–0.46
0.14
0.23
Cr
0.95–3.67
1.03
1.93
0.39–1.58
0.48
0.77
0.06–0.36
0.12
0.27
0.12–0.48
0.15
0.26
V
0.43–0.96
0.20
0.63
0.16–0.58
0.16
0.38
0.08–0.37
0.10
0.20
0.03–0.17
0.06
0.09
Co
Table 2 Element contents in needles and twigs of Northwest sites and Southeast sites (mg kg-1)
TB
TA
Twigs
TB
TA
Needles
Zn
Table 1 Element contents in needles and twigs of TA and TB (mg kg-1)
0.197–1.799
0.630
0.857
0.139–0.842
0.276
0.418
0.070–0.329
0.104
0.176
0.024–0.180
0.059
0.084
As
0.48–1.80
0.48
1.04
0.14–0.38
0.09
0.23
0.078–0.329
0.089
0.200
0.024–0.092
0.025
0.059
As
0.144–0.388
0.092
0.235
0.049–0.126
0.034
0.083
0.040–0.075
0.015
0.059
0.014–0.060
0.022
0.037
Cd
0.050–0.216
0.067
0.141
0.049–0.388
0.127
0.177
0.016–0.072
0.021
0.048
0.014–0.075
0.023
0.047
Cd
0.082–0.385
0.117
0.216
0.112–0.166
0.022
0.129
0.029–0.163
0.050
0.108
0.081–0.155
0.030
0.105
Sb
0.110–0.385
0.103
0.232
0.082–0.136
0.020
0.113
0.085–0.163
0.030
0.135
0.029–0.104
0.029
0.078
Sb
0.031–0.529
0.198
0.216
0.029–0.127
0.037
0.066
0.015–0.181
0.068
0.075
0.012–0.129
0.048
0.047
Mo
0.04–0.242
0.081
0.103
0.031–0.529
0.206
0.179
0.015–0.181
0.070
0.060
0.012–0.129
0.050
0.061
Mo
0.019–0.168
0.072
0.111
0.011–0.118
0.045
0.039
0.019–0.075
0.022
0.038
0.005–0.049
0.018
0.017
Tl
0.014–0.193
0.067
0.097
0.011–0.168
0.066
0.053
0.005–0.049
0.015
0.028
0.006–0.075
0.028
0.027
Tl
0.021–0.046
0.009
0.032
0.005–0.013
0.003
0.008
0.005–0.020
0.006
0.012
0.005–0.007
0.001
0.006
Ag
0.005–0.034
0.012
0.018
0.005–0.046
0.015
0.021
0.005–0.009
0.002
0.006
0.005–0.020
0.006
0.011
Ag
0.010–0.045
0.014
0.022
0.010–0.030
0.008
0.015
0.014–0.038
0.010
0.025
0.011–0.021
0.004
0.015
Hg
0.010–0.045
0.013
0.026
0.010–0.012
0.001
0.011
0.012–0.038
0.010
0.022
0.011–0.033
0.008
0.018
Hg
Heavy metal concentrations in timberline trees
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Large differences of heavy metals concentration and storage in different organs and tissues were also observed in the present study. In our study, all heavy metals except Hg, Ag and Tl were accumulated in twigs (Fig. 3, significantly difference from other organ and tissues). The concentrations of heavy metals in twigs are approximately twice to triple of those in needles, consistent with previous studies that heavy metal concentration of spruce and fir in twigs were significantly higher than that in leaves, different from other tree species such as willow, birch and mountain ash (Luo et al. 2013a; Reimann et al. 2007b; Nkongolo et al. 2008). Though knowledge about the mechanisms of uptake by roots, translocation, re-translocation and deposition of Cd in plants is still little (Welch and Norvell 1999; Clemens 2006), this distribution pattern most likely depends on species specificity for the detoxification strategy of plants (Reimann et al. 2007b). We noticed that in twigs, most elements bonded together by direct or indirect correlation, but in needles, bark and xylem, elements didn’t show such rich connections (Fig. 5). Such rich connection in twigs may be a result of its important role in nutrient cycle: the passageway for needles and trunk, thus elements can be transported into this part from needles, bark and xylem. This particular position and the rich relationship in twigs, may determine the highest heavy metal concentrations in twigs. Furthermore, as we calculated that over 40 % of element mass stored in xylem and 20 % stored in twigs, it seems that fir and spruce were more likely to allocate elements in wood, resulting in a moderate
Fig. 7 a Trend of Pb, Ni, Co, As and Sb in needles and twigs along c eight sites. These elements in needles and twigs both presented regular trends along sites with the lowest concentrations in northwest sites (S3, S4, S5, and S6) b Trend of Cd, Cr, Hg and Tl in needles and twigs along eight sites. These elements in needles and twigs both presented regular trends along sites with the lowest concentrations in northwest sites (S3, S4, S5, and S6) c Trend of V, Cu, Ag, Zn and Mo in needles and twigs along eight sites. V, Cu, Ag in twigs presented regular trends along sites, while in needles don’t. Zn and Mo in both needles and twigs didn’t present any regular trend
elemental turnover rate. Though element concentrations in xylem were very low, for the reason that the biomass of xylem accounted for a large proportion in the biomass of aboveground part, xylem was the main storage place. Contamination press of heavy metals on vegetation As the special geographical location of our study area, extraneous heavy metals can be brought in our study sites by westerly, southwest monsoon and southeast monsoon, contributing to spatial diversity of element concentrations in trees. In our study, we made the trend of element concentrations in different organs and tissues from S1 to S8. From Fig. 6 where six typical elements were selected, concentrations in xylem and bark were with no obvious distribution pattern. So we just discussed the spatial distribution pattern of element concentrations in twigs and needles. Not like xylem and bark, Co, Pb, Ni, Cd, Hg, Cr and Tl concentrations in needles and twigs showed obviously arch
Fig. 6 Trend of Cu, Pb, Cr, Cd, V, and Ag in xylem and bark along eight sites. These elements in xylem and bark presented no regular trends along sites
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trends with the lowest concentrations in the northwest sites (S3, S4, S5, S6) (Fig. 7a, b). For As and Sb, there were stablethen-increasing trends in twigs and needles (Fig. 7a). For V, Cu and Ag, there were obvious difference in twigs from different sites, but these element concentrations were almost the same in needles for all sites (Fig. 7c). For Zn and Mo, trends of element concentrations in both needles and twigs among all the sites were not observed (Fig. 7c). Specifically, the arch trend can be embodied in the diversity between different positions. Firstly, the difference between north and south was estimated by comparing average concentrations of needles and twigs in TA and TB (Table 1). In twigs, all elements (except Cd and the essential nutrient Ni), which presented regular spatial trends both in needles and twigs, also had the higher average concentrations in TB than TA. Among these element, the higher concentrations in TB were also showed in needles for Co, As, Sb, and Pb. It indicated that these elements may partly come from southern contaminantloaded atmosphere, and mountains may barricade these pollutants from southern monsoon. Secondly, the difference between northwest and southeast was estimated by comparing average concentrations of NW (S3, S4, S5 and S6) and SE (S1, S2, S7 and S8) (Table 2). In both twigs and needles, except Cu and Zn whose concentration in SE were a litter lower than or equal to that in NW, all element concentrations in SE were higher than NW. This difference was greater than that between north and south. In conclusion, the southwest and southeast monsoon have contributed to the high heavy metal concentrations in vegetation in the south and east sites. Accumulation way of certain element in timberline forest and its possible source Different elements behave differently in the vegetation, the environment, and between vegetation and environment. In order to distinguish property of elements, we made the cluster analysis of all metals in organs and tissues. In needles (Fig. 8a), elements can be divided into five clusters: cluster 1: Co, Pb, Ni, As, Sb; cluster 2: Cd, Hg, Cr, Tl; cluster 3: V, Cu; cluster 4: Ag; cluster 5: Zn, Mo. In other organ/tissues such as twigs (Fig. 8b), comparing with tree map of needles, the meaning of the classification of elements were indistinct. In the following paragraphs we discuss cluster in needles. First cluster elements in needles are those which can be absorbed by needles from ambient atmosphere, and possibly partly from anthropogenic sources. Co, Pb and Ni can be trapped by needle wax (He and Shun 1993). Because of the moderate or low allocation ability of Co, Pb and Ni in plant (Markert 1993), absorbed elements from air mainly stay in needles. As and Sb are within the same group in the
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Fig. 8 a Hierarchical dendogram for 14 elements in needles obtained by between-groups linkage method (the distances reflect the degree of correlation between different elements). With dark gray dash line as the boundary, elements can be divided into 5 clusters. b Hierarchical dendogram for 14 elements in twigs obtained by between-groups linkage method (the distances reflect the degree of correlation between different elements). With dark gray dash line as the boundary, elements can be divided into 5 clusters
periodic table and act with similar chemical property, so they often associates with each other in the ore (Wang 2012). Though the absorption, transportation and transformation of these elements in plant are not clear, it was reported that water spinach leaves can absorb As and over 83 % absorbed As stay in aboveground part (Feng 2009; Liu 2009). Interestingly, first cluster elements (except Ni) showed higher concentrations in TB than TA in both needles and twigs, supporting the inference that these elements partly came from southern contaminant-loaded atmosphere. Second cluster elements in needles were mostly related to precipitation, and also partly from anthropogenic sources, according to the relationship between precipitation and
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these elements (Fig. 5). It is also worth noting that the correlation between Cd and precipitation, Hg and precipitation were normally positive but not significant, that is because Cd and Hg can be absorbed by needles from air as well. The last three cluster elements in needles were either nutrient elements (Cu, Zn, Mo), or trace elements related to local soil concentrations. In supergene environment, V, Cu, Zn and Mo are all with high solubility and mobility, and can allocate in plant easily (Zhang 1994). da Souza et al. (2014) have found that the translocation factor of Cu from roots to shoots of L. racemosa was much higher than other elements, becoming 179 times higher in leaves with relation to its content in roots, while the translocation of Ag occurred very low and only in the summer. Specially, when soil pH [ 4, Ag in soil can hardly move, and was hardly absorbed by plant (He and Shun 1993). This was supported by the very low even undetectable concentration of Ag in almost half of plant samples when strong enrichment was found in Mount Gongga atmosphere (Yang et al. 2009). Cycling in the soil-plant system, elements behave inside these two mediums both interrelatedly and differently. Classifications in previous studies about Tibetan top soil were similar (Sheng et al. 2012; Zhang 1994), reflecting certain soil geochemical characteristics. However, our results are obviously different from soil classification, demonstrating that biological actions have obviously changed element connections. The outside anthropogenic source have important effects on the elevated vegetation concentrations in southeast sites for the first two clusters of elements. According to cluster analysis, we inferred that Co, Pb, Ni, As and Sb may more root in dry deposition by the means of needle absorption from air, while Cd, Hg, Cr and Tl may more originate in wet deposition by the means of absorption from soil. Previous studies about heavy metal emission ways have proven that the main elements related to vehicle exhaust are Pb, Zn, Ni, Cu and Sb. Ni is generally regarded as an indicator of emissions from fuel burning and vehicular emissions, and Sb is related to shedding of brake lining materials (Zhang et al. 2012a). Cr, Cd, Hg, Tl, As, Cu and Zn are generally from emissions of exploitation of mineral resources, industrial metallurgical process, fossil fuel combustion, and solid waste dumping (Feng 2009; Nriagu 1996). Noteworthy, though there exist well-known deposits of Chinese iron ores along the border of Yunnan and Sichuan provinces, that numerous mineral elements such as Fe, Cu, Pb, Zn, Cd coexist (Xie and Cheng 2008), and high EF of Cu and Zn in our region were observed (Zhang et al. 2012a), however, for Cu and Zn, there are non-differences between TA and TB, as well as northwest and southeast sites. This is interesting that under natural environment with moderate pollution situation, vegetation are able to
adjust its nutrient elements cycle rate, and maintain a stable concentration level. For V, Ag, and Mo, with the no-regular site trends, as well as the low concentrations or low EF value showed in other researches (Cong et al. 2010), we inferred that they were mainly from soil parent materials. Suitability of spruce and fir as biomonitors of anthropogenic contamination Higher plants, particularly spermatophytes, are frequently used as accumulative indicators of heavy metals (Markert 1993). In our study, concentrations in xylem were very low and with no obvious distribution pattern. Bark of coniferous trees has discrete scale structure, and most of element concentrations in which had no obvious distribution pattern as well. So we just discussed the suitability of needles and twigs. From sites S1 to S8, the arch trends with the lowest concentrations in the northwest sites (S3, S4, S5, S6) for Co, Pb, Ni, Cd, Hg, Cr, Tl, As and Sb were presented in needles and twigs. These elements partly come from outer anthropogenic sources suspended in aerosol, and they can be absorbed by needles and bark or transported to needles and twigs from roots. However, this trend for V, Cu and Ag were only presented in twigs, whereas, for Zn and Mo, there is no trend presented in needles and twigs. We concluded that both needles and twigs can reflect the accumulation of heavy metals in ecosystem even with slight amount. Needles are very suitable for airborne contaminations. By analyzing needles, we can easily distinguish the origin of the elements. Twigs can show more information than needles. It was found to contain more numbers of the observed elements when we were discussing the site trend, as well as the statistical difference between the average concentrations in the two transects (TA and TB), and the two directional sites (NW and SE), especially under relatively pure environment. Because twigs are the passageway for needles and trunk to transport nutrients, elements can be transported into twigs from needles and xylem, and be absorbed from air by their bark, as a result, twigs are more sensitive to extra heavy metals input. Once the ecosystem is polluted, the pollution can be detected from most of the factors belong to the ecosystem, such as water, soil, atmosphere and plant vegetation. Therefore, we suggest that by combining the analysis of elements in needles and twigs of spruce and fir, we can synthetically evaluate the environmental quality of eastern Tibetan Plateau for heavy metals.
Conclusions Nutrient elements (except Mo) had higher concentrations in fir and spruce, while in heavily polluted environment,
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plants are able to accumulate heavy metal to a high concentration level. Twigs of fir and spruce have the highest heavy metal concentrations of almost all elements we studied, when xylem has the lowest concentrations. The connections between elements in twigs were much richer than other organ/tissues. Fir and spruce storage most of heavy metal mass in xylem and twigs, which reduces the biogeochemical cycle rate and plays a positive role in maintaining the ecosystem’s environmental quality. The anthropogenic heavy metals from the heavily loaded central Asia, northeast India, and southwest China have made important effects on alpine vegetation by the southwest and southeast monsoon, and be a threaten to eastern Tibetan Plateau. In timberline forest, heavy metals accumulated in twigs and needles of spruce and fir by different ways. Pb, Ni, As, Sb, Co accumulated in spruce and fir more through dry deposition by the means of needle absorption from air, while Cd, Hg, Cr and Tl more through wet deposition by the means of absorbing from soil. For nutrient elements Cu and Zn, with moderate pollution situation, vegetation are able to adjust the nutrient elements cycle rate, thus maintain a stable concentration level. Seldom V, Ag, and Mo are from external anthropogenic sources. Needles and twigs of fir and spruce can serve as indicators of the environment within the ecosystem under study. These indicators present regular spatial variation with higher element concentration in more heavy metal loaded sites, and present differences between sites by the use of statistical analysis when contrasting environmental quality existing. Needles can be suitable indicator of airborne contamination and to simply distinguish the origin of elements, while twigs are more sensitive to extra heavy metals and present more information. Combining the analysis of elements in needles and twigs of spruce and fir, we can synthetically evaluate the environmental quality of heavy metals in eastern Tibetan Plateau. Acknowledgments The present work received financial support from the Strategic Technology Project of the Chinese Academy of Science (Grant XDA05050207) and the National Natural Science Foundation of China (Grants 41272200 and 40871042). Ethical standards The authors declare that that the experiments comply with the current laws of China in which they were performed. Conflict of interest of interest.
The authors declare that they have no conflict
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Heavy metal concentrations in timberline trees of eastern Tibetan Plateau Ji Luo • Jia She • Peijun Yang • Shouqin Sun Wei Li • Yiwen Gong • Ronggui Tang
•
Accepted: 25 April 2014 Ó Springer Science+Business Media New York 2014
Abstract Concentrations of 14 heavy metals (Ag, As, Cd, Co, Cr, Cu, Hg, Mo, Ni, Pb, Sb, Tl, V, and Zn) in needles, twigs, bark and xylem of spruce and fir collected at the timberline of eight sites along the Hengduan Mountains, eastern Tibetan Plateau, are reported. Twigs had the highest concentration for most of elements, while xylem had the lowest concentration. The connections between elements in twigs were much richer than other organ/tissues. Pb, Ni, As, Sb, Co, Cd, Hg, Cr and Tl which are partly through anthropogenic sources and brought in by monsoon, have been accumulated in twigs and needles by wet or dry deposition in south and east sites where are within or near pollutant sources. Under moderate pollution situation, vegetation are able to adjust the nutrient element (Cu and Zn) cycle rate, thus maintain a stable concentration level. Seldom V, Ag, and Mo are from external anthropogenic sources. Needles and twigs can be used as biomonitors for ecosystem environment when needles can simply distinguish the origin of elements and twigs are more sensitive to extra heavy metal input.
J. Luo J. She (&) S. Sun W. Li Y. Gong R. Tang Key Laboratory of Mountain Surface Processes and Ecological Regulation, Institute of Mountain Hazards and Environment, Chinese Academy of Sciences & Ministry of Water Conservancy, #9, Block 4, Renminnan Road, Chengdu 610041, China e-mail: [email protected] J. She R. Tang University of Chinese Academy of Sciences, Beijing, China P. Yang School of Biological Sciences and Engineering, Shaanxi University of Technology, Hanzhong, Shaanxi, China
Keywords Heavy metals Timberline Eastern Tibetan Plateau Biomonitor Transect Anthropogenic source
Introduction Elements in plant tissues have been a hot topic in many subjects such as plant nutriology, environmental science and ecology (Peterjohn and Correll 1984). With the development of human civilization, human activities brought about the increasingly serious environmental problems, heavy metals emitted into the atmosphere and the resultant hazards to vegetation and human life are becoming a matter of great concern (Sun et al. 2010). Plants may accumulate heavy metals by absorbing them either from airborne contaminants, or soil (Chen and Guan 1998; Markert 1993). Different organs or tissues differ in their capacity to accumulate elements. Sun et al. (2011) have compared concentrations of 23 elements in fir leaves and twigs, they found that most of the elements were more significantly enriched in twigs than in leaves. The study of Fan et al. (2006) have found the similar regular that twigs of Pinus taeda had the strongest accumulation ability than leaves and xylem. While Chen and Guan (1998) found that the general order of organs of seven phytocoenosiums for heavy metal concentration were leaves, bark, twigs and trunk. Tree species play an important role in determining heavy metal distribution in plants. Understanding heavy metal distribution in vegetation is the basis of the study of heavy metal dynamics in plants. Higher plants, particularly spermatophytes, have been frequently used as accumulative bioindicators of heavy metals (Markert 1993). Coniferous needles and bark has the ability to absorb heavy metals immediately from atmosphere, resulting in higher concentrations in places
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with anthropogenic airborne contamination (Chen and Guan 1998). Many studies have found the significant correlations between leaves and the ambient pollutant concentration, but no significantly relationship between leaves and the concentrations in soil (Kord et al. 2010), indicating that leaves are suitable biomonitors of air pollution (Aboal et al. 2004; Tomasˇevicˇ et al. 2008). Twigs are also proved as important indicators for heavy metal pollution (Rossbach and Jayasekera 1996; Wu 2006). Tree bark and trunk must be carefully and skillfully used as indicators for long term air pollution or the history of pollution (Gue´guen et al. 2011; Koma´rek et al. 2008; Patrick and Farmer 2007). A study on Pb concentration in urban forest community in pearl river delta showed that the average concentrations of leaves and twigs in experimental plot were higher than control plot, while that of trunk were similar, proving a representative example for tissues of the different response to pollution and different abilities as biomonitors (Wu 2006). Under natural conditions, few researches about heavy metal contamination press on trees at a large scale (up to n 9 104 km2) have been carried out. A typical series of studies in Europe were carried by Reimann et al. (2001, 2007a, b), who studied on higher plants such as birch, mountain ash, and spruce that were indigenous along certain anthropogenic or geogenic concentration gradients in northern Europe. They found that in the natural conditions, bedrock lithology, ore occurrences, soil pH and urban contamination all have a visible influence on the element concentrations in trees, and it is often impossible to differentiate between all the factors that can influence element concentrations. The eastern Tibetan Plateau, as the border of the first level ladder and second level ladder of China, as well as the transition zone of Pacific Ocean and Mediterranean Sea, presents with series of north–south mountains with special conditions of natural geography and unique topographic features (Zheng and Shen 2002). Though the region is remote from anthropogenic activities, once heavy metals brought into these remote mountain areas by long-range atmospheric transport, the ecosystem stability (especially to the fragile timberline forest) and downstream will be under threat (Begum et al. 2005; Wu et al. 2011). In previous aerosol studies on the Tibetan Plateau, it has been reported that elements in particulate matters, rainwater or soil in Tibetan Plateau with EF values higher than ten for Co, Pb, Ni, As, Sb, Cd, Hg, Cr, Tl, Cu, Zn and Ag were observed, and considered from anthropogenic origin, partly transported from the heavily polluted northeast Indian and central Asia by means of air mass back trajectories analysis during the summer monsoon season (Basha et al. 2010;Cong et al. 2007, 2010; Hopkea et al. 2008; Peterjohn and Correll 1984; Yang et al. 2009; Li et al. 2007; Zhang
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et al. 2012b). Moreover, southwest China, for example, southeast Sichuan province, is also a strong source of PM10 and PM2.5 (Yang et al. 2009). However, during the nonmonsoon periods, particle-bounded pollutants can be barely transported into the Tibetan Plateau from outside (the Sahara Desert or the Thar Desert) (Li et al. 2012). Most of studies about heavy metals in eastern Tibetan Plateau concentrated on soil and air, how will anthropogenic contaminant influence heavy metals in plants? There have been few studies. The aim of this work is to understand the distribution of different elements in different plant organs and tissues, the contamination press of heavy metals on vegetation, the accumulation way and possible sources of certain element, and the suitability of spruce and fir as biomonitors of anthropogenic influence.
Materials and methods Site description The study area is located in the middle of Hengduan Mountains, eastern Tibetan Plateau, China. Hengduan Mountainous Region is one of the youngest tectonic units of the Tibetan Plateau, and the transitional fringe area from Tibetan Plateau to west Sichuan Basin and center Yunnan Plateau (Gao and Li 2000). Mountains are in the north and south trend, with nearly 900 km long, 4,000 to 5,000 m above sea level, and with commonly 1,000 m or more elevation difference between mountain valleys. It presents complex diversity of natural environment, biology, minority, society, culture and economy. Generally, Hengduan mountains are mainly controlled by two climate systems: one is westerly of the northern hemisphere, carrying less water vapor; the other is monsoon system, including the southwest monsoon of bay of Bengal and Indian Ocean, and the southeast monsoon from western Pacific, which is the main precipitation air mass (Li et al. 2010). What’s more, this area is also affected by the local circulation of plateau monsoon (Li and Su 1996). These climate systems result in two obvious seasons: the dry season and the wet season. The dry season is between the middle of October and the middle of May next year, with scarce rainfall, long sunlight, high evaporation, and dry air, which is mainly dominated by westerly. The wet season is between the middle of May and the middle of October, air mass mainly comes from southeast Sichuan province and northeast India, characterized by relatively higher temperature and humid weather, resulting in above 85 % rainfall (mainly concentrated in June, July, and August) during this period (some regions are even above 90 %) (Cong et al. 2010; Yang et al. 2009). Under its special geographical position and topography, this mountain region forms a
Heavy metal concentrations in timberline trees
Fig. 1 Location of the sampling sites: Transect A (S1, S2, S3, and S4) and Transect B (S5, S6, S7, and S8)
diverse and regular vertical climate change that is ‘‘spring at the foot, ice and snow on the peak, one mountain at four seasons, and different weather within 10 km’’ (Luo et al. 2013a). Sampling sites were selected in timberline of eight sites in Hengduan Mountains (Fig. 1) owing to timberline’s easy contamination acceptance (Takahashi et al. 2012). The dominant species are spruce in S3, S4 and S5, and fir in other sites. At the basis of the eight sites, we set two parallel northwest-southeast belt transects, each parallel belt transect had 4 typical sites, that is Transect A (TA), consisting of S1, S2, S3, and S4, and Transect B (TB), consisting of S5, S6, S7, and S8, to estimate the diversity of north and south; and two clusters of sites, each cluster also had 4 sites, that is the northwest sites (NW), consisting of S3, S4, S5 and S6; and the southeast sites (SE), consisting of S1, S2, S7 and S8, to estimate the diversity of northwest and southeast. Soil types are brown coniferous forest soil for all sites. The pH value of top soil (0–20 cm) were between 3.85 and 5.08. Mt. Gongga (S1) is the main peak of Hengduan mountains, which is close to urban and suburban areas. Sampling and preparation The dominant timberline tree species are fir (in S1, S2, S6, S7, and S8) or spruce (in S3, S4, and S5). Fir and spruce are two species with similar physiology and morphology. Yanai et al. (2009) have found that the Engelmann spruce and subalpine fir were indistinguishable in nutrient uptake, specific root length and diameter distribution, so data from the two species are thought to be comparable. To avoid
possible seasonal influences, all samples were collected within as short a time span as possible in July and August, 2011. Before sampling, preliminary observation on topography and forest form were conducted. In each stand, three 20 9 30 m plots were established. Each plot consisted of twenty-four 5 9 5 m quadrats. Twelve quadrats in each plot were randomly selected for sampling (Luo et al. 2013b). In each plot, mature needles, twigs, xylem and bark from its dominant specie (spruce or fir) were collected separately as four composite samples from twelve quadrats randomly selected. Needles and twigs were collected at the same branches in all directions. Xylem samples were extracted at breast height (approximately 1.5 m) as a chunk of wood and outside portion of the trunk. Bark was carefully removed from the boles of the trees at an average height of 1.5 m above the ground. Trace-element and powder-free vinyl gloves (one new pair per sample material) were used during sample collection (Reimann et al. 2007a). Different trees had almost the same size and age. The total number of collected samples was 96. Samples were separately collected into clean cellulose bags and stored them with cooler. After the samples were brought to the laboratory, they were carefully washed with tap water to remove coarse particles, then were washed with distilled water three times to remove adhering particle. After air drying, all samples were oven dried to a constant weight at 40 °C. Then samples were cut to the length of less than 2 mm and pulverized to pass through a 100-mesh screen in a mild steel mill. Finally, all samples were spread into contamination-free polyethylene plastic bags and labeled respectively.
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Heavy metal analysis Plant samples were dissolved in a microwave-assisted nitric acid, hydrogen peroxide, and hydrofluoric acid digestion (The Analyzing and Testing Center, Nanjing Institute of Geography & Limnology, Chinese Academy of Sciences) (Wu et al., 2011). Then solutions were analyzed using Inductively Coupled Plasma Mass Spectrometry (ICP-MS) (77009, Agilent Technologies, America) for 14 heavy metals (here, we consider As as heavy metal since it has similar damaging effects to environment and humans as that of heavy metals): the essential nutrients Cu, Zn, Ni, and Mo, and nonessential trace elements Ag, As, Cd, Co, Cr, Hg, Mo, Pb, Sb, Tl, and V. The analysis method refers to Inductively Coupled Plasma Mass Spectrometry, USA EPA Method 6020a (Revision 1, February 2007). The detection limits are: Ag (0.005 mg L-1), As (0.01 mg L-1), Cd (0.005 mg L-1), Co (0.001 mg L-1), Cr (0.01 mg L-1), Cu (0.003 mg L-1), Hg (0.01 mg L-1), Mo (0.01 mg L-1), Ni (0.005 mg L-1), Pb (0.01 mg L-1), Sb (0.001 mg L-1), Tl (0.005 mg L-1), V (0.002 mg L-1), Zn (0.003 mg L-1). When calculating, if a value is lower than the detection limit, we use the detected limit value instead. Standard solution SPEXTM (SPEX Certi-Prep) from USA was used as the standard. Quality control was ensured through the triplicate analysis of two reference materials. Plant reference materials were from the National Quality and Technology Supervision Agency of China (GBW07603 and GBW07604). Precision was good with the coefficient of variation (CV) below 5 % for the measurement and recoveries between 90–115 %.
Fig. 2 The weighted average concentration of heavy metals in aboveground part of spruce and fir of the eight sites (n = 8). The weighted average concentration of an element in one site was calculated as the quotient of total element storage and total biomass of aboveground part
organ/tissue biomass. Then the weighted average concentration is calculated as the quotient of total element storage and total biomass of aboveground part (compose of needles, twigs, bark, and xylem) in fir or spruce. Data of organs and tissues biomass were based on Zhong et al. (1997)’s research in a near-mature forest, that the biomass ratio of needles: twigs: bark: xylem was about 2:13: 9: 76. Annual precipitation data of the eight sites were acquired from the local meteorological stations.
Results Statistical analysis Statistical analyses were performed using SAS 9.1 software. Difference analysis of different organs/tissues for certain element concentration were determined by Student– Newman–Keuls (SNK) Test with the significance level set as P \ 0.05. Other difference analysis were carried out using one-way ANOVA followed by LSD. A probability value of less than 0.05 was regarded as significant. Correlation analysis between elements in different organs and tissues were carried out in linear dependence. Cluster analysis of 14 elements in needles and twigs were carried out using PASW Statistics 18.0 software. Before computing proximities, standardization was performed, which can be automatically done by the hierarchical cluster analysis procedure. Cluster analysis was applied to the standardized data using between-groups linkage method. A dendrogram was constructed to assess the cohesiveness of the clusters formed, in which correlations among elements can readily be seen. The storage of an element in certain organ/tissue was calculated as the product of element concentration and
123
Concentrations of different elements in aboveground part of spruce and fir As we calculated the weighted average concentration in a certain site, average element concentrations of the eight sites were shown in Fig. 2. Elements ranged as: Zn [ Cu [ Pb [ Ni [ Cr [ V [ Co [ As [ Sb [ Cd [ Mo [ Tl [ Ag [ Hg. In certain tissues and organs, elements ranged as: in leaves: Zn [ Cu [ Pb [ Ni [ V [ Cr [ Sb [ Co [ As [ Mo [ Cd [ Tl [ Hg [ Ag; in twigs: Zn [ Cu [ Pb [ Ni [ Cr [ V [ As [ Co [ Sb [ Cd [ Mo [ Tl [ Ag [ Hg; in bark: Zn [ Cu [ Ni [ Pb [ Cr [ V [ Co [ Cd [ As [ Sb [ Tl [ Mo [ Hg [ Ag; in xylem: Zn [ Cu [ Ni [ Pb [ Cr [ V [ Co [ Sb [ Cd [ Mo [ As [ Tl [ Ag [ Hg. No matter in aboveground part or certain tissue/organ, the nutrient Zn and Cu had the highest concentration. Ni concentration was also much higher than all trace metals except Pb. However, Mo concentration was very low, it was even not detected at four sites in xylem. For trace elements, Pb, Cr and V concentrations were the highest. It
Heavy metal concentrations in timberline trees
Fig. 3 Average concentrations of different heavy metals in different organs and tissues (n = 8). Different letters denote significant differences among means (a = 0.05) as determined by Student–Newman–Keuls (SNK) Test
is noteworthy that Pb concentration in needles, twigs and aboveground part were higher than micronutrient Ni, though Pb is considered as a nonessential element. Co, As, Sb, and Cd concentrations did not have a regular rank, but all higher than Tl. Ag and Hg concentrations were the lowest among all elements. Element concentrations and storages in different organs and tissues Element concentrations in different organs and tissues were presented in Fig. 3. Element concentrations except Tl, Ag, Hg, Cd and Zn in twigs were significantly higher than that in needles, bark and xylem. For unessential trace elements, concentrations in xylem were the lowest, and were significantly lower than other tissues and organs for V, Co and As. For most of elements (Cu, Ni, Cr, V, Co, As, Sb, Tl, Ag and Hg), concentrations in bark and needles were comparable. Moreover, we estimated the proportion of certain element storage in certain organ/tissue on total element storage in aboveground part (Fig. 4). For most of elements (except V, Co and As), heavy metal storage in xylem accounted for higher than 40 % of total storage in
Fig. 4 Proportion of certain element storage in certain organ/tissue on element storage in aboveground part of spruce or fir. The storage of certain element was calculated as the product of mean element concentration of the eight sites and biomass of certain organ/tissue. The element storage in aboveground part was the sum of element storage in needles, twigs, bark and xylem
aboveground part. Another important storage place was twigs, with the proportion of higher than 20 % for most of elements (except Ag and Hg). Elements storages in needles and bark were relatively low.
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J. Luo et al. Fig. 5 Correlation analysis between elements in different organs and tissues. Solid line stands for significant correlation (R2 [ 0.5), while dotted line stands for general correlation(0.5 [ R2 [ 0.3). ‘Pre’ stands for precipitation
Furthermore, in order to find out the interrelationships of elements in certain organ/tissue, we performed correlation analysis between element concentrations, and between element concentrations and precipitation in different organs and tissues (Fig. 5). In the case of the very low concentrations of Mo, Hg and Ag in xylem, we didn’t consider any relationships between those elements in xylem. In twigs, all elements except Cu, Zn and Hg were closely correlated directly or indirectly. In needles, Cu, V, Mo and Ag had no relationship with other elements. In bark, Cr had no relationship with other elements. In xylem, when not considering Mo, Hg and Ag, Pb had no relationship with other elements.
Element concentrations in two transects and two clusters of sites Average element concentrations in TA and TB for needles and twigs were shown in Table 1. As a result, in twigs, V, Cr, Co, As, Sb, Hg, Pb and Tl concentrations in TB were higher than that in TA, while Mo and Cd in TA were higher than that in TB; in needles, only Co, As, Sb and Pb showed higher average concentrations in TB than TA. The significant differences in statistics were only detected for As in needles (P = 0.039) and twigs (P = 0.029). Average concentrations of northwest sites (S3, S4, S5 and S6) and southeast sites (S1, S2, S7 and S8) for needles and twigs were shown in Table 2. Result shows that elements except Cu, Zn, V and Sb in needles, and Cu and Zn in twigs, showed higher concentrations in southeast sites. Significant differences were found for Ni, Ag, Cd and Pb in twigs (P = 0.002, 0.006, 0.04 and 0.01 respectively).
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Discussion Heavy metals in aboveground part of spruce and fir The present study indicated large elements-dependent differences. Zn, Cu, and Ni concentrations ranged from 3.26 to 36.48 mg kg-1, 4.48 to 60.07 mg kg-1, and 0.44 to 5.81 mg kg-1 respectively, which is comparable to other studies of fir and spruce (Sun et al. 2011; Reimann et al. 2007a). Same as nutrient element, however, Mo concentration was much lower than above elements. In our study, Mo concentration ranged from 0.01 to 0.53 mg kg-1, which were also similar to Reimann et al. (2007a) and Sun et al. (2011)’s research, but significantly lower than other species of trees (Reimann et al. 2007a) and normal natural Mo concentration in plants(0.2–5 mg kg-1) (Kabata Pendias and Pendias 2001). The abnormal low Mo concentration in spruce and fir reflected the specificity of these species, or ascribed to low soil Mo concentration (\1.3 mg kg-1) in study area (Xie and Cheng 2008), challenging the necessary role of Mo to mature timberline spruce and fir trees. The exposure levels of heavy metals in soil or air, the bioavailability, uptake activity, and efficiency of translocation of metal ions, all determined the nonessential trace element concentrations in vegetation. (Clemens 2006; Nadgo´rska-Socha et al. 2013). It is noteworthy that Pb concentration in needles, twigs and aboveground part were higher than micronutrient Ni. It was reported that in industrial emission impacted areas, Pb concentrations in masson pine needles even exceeded Cu concentrations (Sun et al. 2010). It is true that in heavily polluted environment, plants are able to accumulate heavy metal to a high concentration level.
4.95
34.61–48.41
Sd
Range
21.17–52.39
Range
41.24
11.91
Ave.
35.16
13.87–26.34
Range
Sd
4.55
Ave.
20.77
8.83–36.42
Range
Sd
8.83
Sd
Ave.
22.73
Ave.
7.95–36.49
11.59
17.52
7.67–18.79
4.28
12.91
3.66–7.80
1.58
5.94
4.23–5.81
0.61
5.23
Cu
0.21–14.31
4.649
7.035
0.49–11.00
3.981
4.730
0.93–10.58
3.66
4.83
0.16–2.85
1.08
1.46
Pb
0.86–5.81
2.01
3.42
1.71–4.89
1.24
3.68
0.26–3.06
1.04
1.58
0.91–2.54
0.61
1.64
Ni
0.76–3.46
1.02
1.74
0.44–1.96
0.59
0.97
0.13–0.76
0.23
0.42
0.13–0.76
0.24
0.35
Cr
0.65–3.67
1.11
1.85
0.39–1.61
0.49
0.85
0.06–0.48
0.17
0.26
0.12–0.34
0.09
0.28
V
0.29–0.96
0.24
0.60
0.16–0.56
0.15
0.41
0.03–0.37
0.12
0.18
0.03–0.21
0.06
0.12
Co
b
a
38.83
7.40
27.62–48.84
Range
21.17–52.39
Range
Sd
11.38
Ave.
37.56
13.87–22.27
Range
Sd
3.17
Ave.
19.18
11.83–36.42
Range
Sd
8.79
Sd
Ave.
24.33
Ave.
SE means Southeast sites
NW means Northwest sites
SE
NW
Twigs
SEb
NWa
Needles
Zn
7.95–18.79
4.60
13.60
7.67–36.49
11.70
16.83
3.66–7.80
1.58
5.23
5.37–6.94
0.60
5.94
Cu
5.12–14.31
3.46
9.54
0.49–3.90
1.21
2.23
2.13–10.58
3.31
5.21
0.16–2.54
0.89
1.08
Pb
4.58–5.81
0.46
5.05
0.86–3.54
0.97
2.05
0.91–3.06
0.80
2.11
0.27–1.80
0.56
1.10
Ni
0.86–3.46
0.98
1.91
0.44–1.39
0.36
0.80
0.33–0.76
0.21
0.55
0.13–0.46
0.14
0.23
Cr
0.95–3.67
1.03
1.93
0.39–1.58
0.48
0.77
0.06–0.36
0.12
0.27
0.12–0.48
0.15
0.26
V
0.43–0.96
0.20
0.63
0.16–0.58
0.16
0.38
0.08–0.37
0.10
0.20
0.03–0.17
0.06
0.09
Co
Table 2 Element contents in needles and twigs of Northwest sites and Southeast sites (mg kg-1)
TB
TA
Twigs
TB
TA
Needles
Zn
Table 1 Element contents in needles and twigs of TA and TB (mg kg-1)
0.197–1.799
0.630
0.857
0.139–0.842
0.276
0.418
0.070–0.329
0.104
0.176
0.024–0.180
0.059
0.084
As
0.48–1.80
0.48
1.04
0.14–0.38
0.09
0.23
0.078–0.329
0.089
0.200
0.024–0.092
0.025
0.059
As
0.144–0.388
0.092
0.235
0.049–0.126
0.034
0.083
0.040–0.075
0.015
0.059
0.014–0.060
0.022
0.037
Cd
0.050–0.216
0.067
0.141
0.049–0.388
0.127
0.177
0.016–0.072
0.021
0.048
0.014–0.075
0.023
0.047
Cd
0.082–0.385
0.117
0.216
0.112–0.166
0.022
0.129
0.029–0.163
0.050
0.108
0.081–0.155
0.030
0.105
Sb
0.110–0.385
0.103
0.232
0.082–0.136
0.020
0.113
0.085–0.163
0.030
0.135
0.029–0.104
0.029
0.078
Sb
0.031–0.529
0.198
0.216
0.029–0.127
0.037
0.066
0.015–0.181
0.068
0.075
0.012–0.129
0.048
0.047
Mo
0.04–0.242
0.081
0.103
0.031–0.529
0.206
0.179
0.015–0.181
0.070
0.060
0.012–0.129
0.050
0.061
Mo
0.019–0.168
0.072
0.111
0.011–0.118
0.045
0.039
0.019–0.075
0.022
0.038
0.005–0.049
0.018
0.017
Tl
0.014–0.193
0.067
0.097
0.011–0.168
0.066
0.053
0.005–0.049
0.015
0.028
0.006–0.075
0.028
0.027
Tl
0.021–0.046
0.009
0.032
0.005–0.013
0.003
0.008
0.005–0.020
0.006
0.012
0.005–0.007
0.001
0.006
Ag
0.005–0.034
0.012
0.018
0.005–0.046
0.015
0.021
0.005–0.009
0.002
0.006
0.005–0.020
0.006
0.011
Ag
0.010–0.045
0.014
0.022
0.010–0.030
0.008
0.015
0.014–0.038
0.010
0.025
0.011–0.021
0.004
0.015
Hg
0.010–0.045
0.013
0.026
0.010–0.012
0.001
0.011
0.012–0.038
0.010
0.022
0.011–0.033
0.008
0.018
Hg
Heavy metal concentrations in timberline trees
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J. Luo et al.
Large differences of heavy metals concentration and storage in different organs and tissues were also observed in the present study. In our study, all heavy metals except Hg, Ag and Tl were accumulated in twigs (Fig. 3, significantly difference from other organ and tissues). The concentrations of heavy metals in twigs are approximately twice to triple of those in needles, consistent with previous studies that heavy metal concentration of spruce and fir in twigs were significantly higher than that in leaves, different from other tree species such as willow, birch and mountain ash (Luo et al. 2013a; Reimann et al. 2007b; Nkongolo et al. 2008). Though knowledge about the mechanisms of uptake by roots, translocation, re-translocation and deposition of Cd in plants is still little (Welch and Norvell 1999; Clemens 2006), this distribution pattern most likely depends on species specificity for the detoxification strategy of plants (Reimann et al. 2007b). We noticed that in twigs, most elements bonded together by direct or indirect correlation, but in needles, bark and xylem, elements didn’t show such rich connections (Fig. 5). Such rich connection in twigs may be a result of its important role in nutrient cycle: the passageway for needles and trunk, thus elements can be transported into this part from needles, bark and xylem. This particular position and the rich relationship in twigs, may determine the highest heavy metal concentrations in twigs. Furthermore, as we calculated that over 40 % of element mass stored in xylem and 20 % stored in twigs, it seems that fir and spruce were more likely to allocate elements in wood, resulting in a moderate
Fig. 7 a Trend of Pb, Ni, Co, As and Sb in needles and twigs along c eight sites. These elements in needles and twigs both presented regular trends along sites with the lowest concentrations in northwest sites (S3, S4, S5, and S6) b Trend of Cd, Cr, Hg and Tl in needles and twigs along eight sites. These elements in needles and twigs both presented regular trends along sites with the lowest concentrations in northwest sites (S3, S4, S5, and S6) c Trend of V, Cu, Ag, Zn and Mo in needles and twigs along eight sites. V, Cu, Ag in twigs presented regular trends along sites, while in needles don’t. Zn and Mo in both needles and twigs didn’t present any regular trend
elemental turnover rate. Though element concentrations in xylem were very low, for the reason that the biomass of xylem accounted for a large proportion in the biomass of aboveground part, xylem was the main storage place. Contamination press of heavy metals on vegetation As the special geographical location of our study area, extraneous heavy metals can be brought in our study sites by westerly, southwest monsoon and southeast monsoon, contributing to spatial diversity of element concentrations in trees. In our study, we made the trend of element concentrations in different organs and tissues from S1 to S8. From Fig. 6 where six typical elements were selected, concentrations in xylem and bark were with no obvious distribution pattern. So we just discussed the spatial distribution pattern of element concentrations in twigs and needles. Not like xylem and bark, Co, Pb, Ni, Cd, Hg, Cr and Tl concentrations in needles and twigs showed obviously arch
Fig. 6 Trend of Cu, Pb, Cr, Cd, V, and Ag in xylem and bark along eight sites. These elements in xylem and bark presented no regular trends along sites
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Heavy metal concentrations in timberline trees
123
J. Luo et al.
trends with the lowest concentrations in the northwest sites (S3, S4, S5, S6) (Fig. 7a, b). For As and Sb, there were stablethen-increasing trends in twigs and needles (Fig. 7a). For V, Cu and Ag, there were obvious difference in twigs from different sites, but these element concentrations were almost the same in needles for all sites (Fig. 7c). For Zn and Mo, trends of element concentrations in both needles and twigs among all the sites were not observed (Fig. 7c). Specifically, the arch trend can be embodied in the diversity between different positions. Firstly, the difference between north and south was estimated by comparing average concentrations of needles and twigs in TA and TB (Table 1). In twigs, all elements (except Cd and the essential nutrient Ni), which presented regular spatial trends both in needles and twigs, also had the higher average concentrations in TB than TA. Among these element, the higher concentrations in TB were also showed in needles for Co, As, Sb, and Pb. It indicated that these elements may partly come from southern contaminantloaded atmosphere, and mountains may barricade these pollutants from southern monsoon. Secondly, the difference between northwest and southeast was estimated by comparing average concentrations of NW (S3, S4, S5 and S6) and SE (S1, S2, S7 and S8) (Table 2). In both twigs and needles, except Cu and Zn whose concentration in SE were a litter lower than or equal to that in NW, all element concentrations in SE were higher than NW. This difference was greater than that between north and south. In conclusion, the southwest and southeast monsoon have contributed to the high heavy metal concentrations in vegetation in the south and east sites. Accumulation way of certain element in timberline forest and its possible source Different elements behave differently in the vegetation, the environment, and between vegetation and environment. In order to distinguish property of elements, we made the cluster analysis of all metals in organs and tissues. In needles (Fig. 8a), elements can be divided into five clusters: cluster 1: Co, Pb, Ni, As, Sb; cluster 2: Cd, Hg, Cr, Tl; cluster 3: V, Cu; cluster 4: Ag; cluster 5: Zn, Mo. In other organ/tissues such as twigs (Fig. 8b), comparing with tree map of needles, the meaning of the classification of elements were indistinct. In the following paragraphs we discuss cluster in needles. First cluster elements in needles are those which can be absorbed by needles from ambient atmosphere, and possibly partly from anthropogenic sources. Co, Pb and Ni can be trapped by needle wax (He and Shun 1993). Because of the moderate or low allocation ability of Co, Pb and Ni in plant (Markert 1993), absorbed elements from air mainly stay in needles. As and Sb are within the same group in the
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Fig. 8 a Hierarchical dendogram for 14 elements in needles obtained by between-groups linkage method (the distances reflect the degree of correlation between different elements). With dark gray dash line as the boundary, elements can be divided into 5 clusters. b Hierarchical dendogram for 14 elements in twigs obtained by between-groups linkage method (the distances reflect the degree of correlation between different elements). With dark gray dash line as the boundary, elements can be divided into 5 clusters
periodic table and act with similar chemical property, so they often associates with each other in the ore (Wang 2012). Though the absorption, transportation and transformation of these elements in plant are not clear, it was reported that water spinach leaves can absorb As and over 83 % absorbed As stay in aboveground part (Feng 2009; Liu 2009). Interestingly, first cluster elements (except Ni) showed higher concentrations in TB than TA in both needles and twigs, supporting the inference that these elements partly came from southern contaminant-loaded atmosphere. Second cluster elements in needles were mostly related to precipitation, and also partly from anthropogenic sources, according to the relationship between precipitation and
Heavy metal concentrations in timberline trees
these elements (Fig. 5). It is also worth noting that the correlation between Cd and precipitation, Hg and precipitation were normally positive but not significant, that is because Cd and Hg can be absorbed by needles from air as well. The last three cluster elements in needles were either nutrient elements (Cu, Zn, Mo), or trace elements related to local soil concentrations. In supergene environment, V, Cu, Zn and Mo are all with high solubility and mobility, and can allocate in plant easily (Zhang 1994). da Souza et al. (2014) have found that the translocation factor of Cu from roots to shoots of L. racemosa was much higher than other elements, becoming 179 times higher in leaves with relation to its content in roots, while the translocation of Ag occurred very low and only in the summer. Specially, when soil pH [ 4, Ag in soil can hardly move, and was hardly absorbed by plant (He and Shun 1993). This was supported by the very low even undetectable concentration of Ag in almost half of plant samples when strong enrichment was found in Mount Gongga atmosphere (Yang et al. 2009). Cycling in the soil-plant system, elements behave inside these two mediums both interrelatedly and differently. Classifications in previous studies about Tibetan top soil were similar (Sheng et al. 2012; Zhang 1994), reflecting certain soil geochemical characteristics. However, our results are obviously different from soil classification, demonstrating that biological actions have obviously changed element connections. The outside anthropogenic source have important effects on the elevated vegetation concentrations in southeast sites for the first two clusters of elements. According to cluster analysis, we inferred that Co, Pb, Ni, As and Sb may more root in dry deposition by the means of needle absorption from air, while Cd, Hg, Cr and Tl may more originate in wet deposition by the means of absorption from soil. Previous studies about heavy metal emission ways have proven that the main elements related to vehicle exhaust are Pb, Zn, Ni, Cu and Sb. Ni is generally regarded as an indicator of emissions from fuel burning and vehicular emissions, and Sb is related to shedding of brake lining materials (Zhang et al. 2012a). Cr, Cd, Hg, Tl, As, Cu and Zn are generally from emissions of exploitation of mineral resources, industrial metallurgical process, fossil fuel combustion, and solid waste dumping (Feng 2009; Nriagu 1996). Noteworthy, though there exist well-known deposits of Chinese iron ores along the border of Yunnan and Sichuan provinces, that numerous mineral elements such as Fe, Cu, Pb, Zn, Cd coexist (Xie and Cheng 2008), and high EF of Cu and Zn in our region were observed (Zhang et al. 2012a), however, for Cu and Zn, there are non-differences between TA and TB, as well as northwest and southeast sites. This is interesting that under natural environment with moderate pollution situation, vegetation are able to
adjust its nutrient elements cycle rate, and maintain a stable concentration level. For V, Ag, and Mo, with the no-regular site trends, as well as the low concentrations or low EF value showed in other researches (Cong et al. 2010), we inferred that they were mainly from soil parent materials. Suitability of spruce and fir as biomonitors of anthropogenic contamination Higher plants, particularly spermatophytes, are frequently used as accumulative indicators of heavy metals (Markert 1993). In our study, concentrations in xylem were very low and with no obvious distribution pattern. Bark of coniferous trees has discrete scale structure, and most of element concentrations in which had no obvious distribution pattern as well. So we just discussed the suitability of needles and twigs. From sites S1 to S8, the arch trends with the lowest concentrations in the northwest sites (S3, S4, S5, S6) for Co, Pb, Ni, Cd, Hg, Cr, Tl, As and Sb were presented in needles and twigs. These elements partly come from outer anthropogenic sources suspended in aerosol, and they can be absorbed by needles and bark or transported to needles and twigs from roots. However, this trend for V, Cu and Ag were only presented in twigs, whereas, for Zn and Mo, there is no trend presented in needles and twigs. We concluded that both needles and twigs can reflect the accumulation of heavy metals in ecosystem even with slight amount. Needles are very suitable for airborne contaminations. By analyzing needles, we can easily distinguish the origin of the elements. Twigs can show more information than needles. It was found to contain more numbers of the observed elements when we were discussing the site trend, as well as the statistical difference between the average concentrations in the two transects (TA and TB), and the two directional sites (NW and SE), especially under relatively pure environment. Because twigs are the passageway for needles and trunk to transport nutrients, elements can be transported into twigs from needles and xylem, and be absorbed from air by their bark, as a result, twigs are more sensitive to extra heavy metals input. Once the ecosystem is polluted, the pollution can be detected from most of the factors belong to the ecosystem, such as water, soil, atmosphere and plant vegetation. Therefore, we suggest that by combining the analysis of elements in needles and twigs of spruce and fir, we can synthetically evaluate the environmental quality of eastern Tibetan Plateau for heavy metals.
Conclusions Nutrient elements (except Mo) had higher concentrations in fir and spruce, while in heavily polluted environment,
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plants are able to accumulate heavy metal to a high concentration level. Twigs of fir and spruce have the highest heavy metal concentrations of almost all elements we studied, when xylem has the lowest concentrations. The connections between elements in twigs were much richer than other organ/tissues. Fir and spruce storage most of heavy metal mass in xylem and twigs, which reduces the biogeochemical cycle rate and plays a positive role in maintaining the ecosystem’s environmental quality. The anthropogenic heavy metals from the heavily loaded central Asia, northeast India, and southwest China have made important effects on alpine vegetation by the southwest and southeast monsoon, and be a threaten to eastern Tibetan Plateau. In timberline forest, heavy metals accumulated in twigs and needles of spruce and fir by different ways. Pb, Ni, As, Sb, Co accumulated in spruce and fir more through dry deposition by the means of needle absorption from air, while Cd, Hg, Cr and Tl more through wet deposition by the means of absorbing from soil. For nutrient elements Cu and Zn, with moderate pollution situation, vegetation are able to adjust the nutrient elements cycle rate, thus maintain a stable concentration level. Seldom V, Ag, and Mo are from external anthropogenic sources. Needles and twigs of fir and spruce can serve as indicators of the environment within the ecosystem under study. These indicators present regular spatial variation with higher element concentration in more heavy metal loaded sites, and present differences between sites by the use of statistical analysis when contrasting environmental quality existing. Needles can be suitable indicator of airborne contamination and to simply distinguish the origin of elements, while twigs are more sensitive to extra heavy metals and present more information. Combining the analysis of elements in needles and twigs of spruce and fir, we can synthetically evaluate the environmental quality of heavy metals in eastern Tibetan Plateau. Acknowledgments The present work received financial support from the Strategic Technology Project of the Chinese Academy of Science (Grant XDA05050207) and the National Natural Science Foundation of China (Grants 41272200 and 40871042). Ethical standards The authors declare that that the experiments comply with the current laws of China in which they were performed. Conflict of interest of interest.
The authors declare that they have no conflict
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