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Heavy metals in plants in constructed and natural wetlands: concentration, accumulation and seasonality ̌ zinová J. Vymazal and T. Bre
ABSTRACT The accumulation of heavy metals in plants is a function of uptake capacity and intracellular binding sites. The concentrations of heavy metals in plants growing in constructed wetlands vary considerably between species and systems but in general, the concentrations are within the range commonly found in natural stands. The highest concentrations are mostly found in roots, followed by rhizomes, leaves and stems. Unfortunately, concentration values are commonly used to evaluate the
J. Vymazal (corresponding author) ̌ zinová T. Bre Department of Applied Ecology, Faculty of Environmental Sciences, Czech University of Life Sciences in Prague, Kamýcká 129, 165 21 Praha 6, Czech Republic E-mail: [email protected]
‘accumulation’ of heavy metals, but this approach is not correct. In order to evaluate heavy metal accumulation, the biomass of particular plant parts must be taken into consideration. In addition, there are two other factors, which need to be taken into consideration when accumulation is evaluated, namely seasonality and distribution within the plant shoot. It has been found that the seasonal distribution of heavy metals in the biomass varies between heavy metals and mostly does not follow the pattern known for nutrients. In addition, the concentration and accumulation of heavy metals vary considerably within the shoot and this fact should be taken into consideration when analyses are carried out. Key words
| accumulation, constructed wetlands, heavy metals, macrophytes
INTRODUCTION Macrophytes have been shown to play important roles in wetland biogeochemistry through their active and passive circulation of elements (Weis & Weis ). The accumulation of a given metal is a function of uptake capacity and intracellular binding sites and, according to Clemens et al. (), it includes mobilization and uptake from the soil, compartmentalization and sequestration within the root, efficiency of xylem loading and transport, distribution between metals sinks in the aerial parts, sequestration and storage in leaf cells. The two most important soil/sediment factors influencing trace element mobility in wetland soils affected by plants are probably redox potential (Eh) and pH. Wetland plants influence the redox status in the rhizosphere due to their ability to transport oxygen to the roots (e.g., Armstrong ; Brix ; Sorrell & Armstrong ). This often leads to radial oxygen loss, which may depend on many factors, such as root biomass (Chen & Barko ), density (Pedersen et al. ), plant species (Sand-Jensen et al. ), location along the root (Connell et al. ), root age (Bedford et al. ), time of the day (Sand-Jensen et al. ) and season (Jacob & Otte ). doi: 10.2166/wst.2014.507
Metals may become mobilized from associated sulfides upon oxidation in the rhizosphere (Howarth & Teal ; Holmer et al. ) but due to their binding affinity, may adsorb to iron (oxy-)hydroxide (Jacob & Otte ). Rhizosphere pH affects the availability of both soil micronutrients and trace elements that are not essential for plant growth. With decreasing pH, the availability of essential trace elements such as zinc, iron and manganese is enhanced by desorption from soil particles. Furthermore, the availability of non-essential elements, such as cadmium, increases with decreasing pH as a result of increased solubility (Marschner & Römheld ). Acidification of the rhizosphere is very often the result of plant root exudate release that mobilizes sparingly soluble micronutrients (Doyle & Otte ). Of the plant organic acids, citric and malic acids have received particular attention (Brown ; Senden et al. ). Because of the high-binding capacity for metallic micronutrients by soil particles, plants have evolved several strategies for increasing their soil bioavailability. The most important strategy is probably the production of metal-chelating
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compounds (phytometallophores), such as mugenic and avenic acids, which are synthetized in response to iron, zinc and possibly other trace-element deficiencies (Kinnersley ; Cakmak et al. ). In the rhizosphere, phytometallophores chelate and mobilize trace elements and once chelated to phytometallophores, metal ions can be transported across the plasma membrane as a metal–phytomellophore complex via specialized transporters (Römheld ; Vonwiren et al. ; Clemens et al. ). The objective of this paper is to evaluate (1) concentrations of heavy metals in the aboveground biomass of plants growing in constructed wetlands (CWs) and to compare them with natural wetlands, (2) calculation of heavy metal accumulation in plants, (3) seasonal variation in heavy metal concentration in the plant biomass, and (4) distribution of heavy metals in the aboveground plant biomass.
CONCENTRATIONS OF HEAVY METALS IN PLANTS The concentrations of heavy metals in various parts of macrophytes growing in CWs, as well as in natural wetlands, generally decrease in the order of roots >rhizomes leaves > stems (e.g., Schierup & Larsen ; Peverly et al. ; Windham et al. ; Lesage et al. a; Vymazal & Kröpfelová ; Bonano & Lo Guidice ; Table 1). The concentrations of heavy metals in the belowground parts, namely roots, could be affected by heavy metals adsorbed onto the root surface. Before the analysis, the roots and rhizomes must be carefully washed but this procedure should be very gentle to prevent root loss. The amount of heavy metals could be increased in the presence of iron plaque where heavy metals may co-precipitate (Weis & Weis ). In Table 1, concentration ratios between leaves and stems and between roots and leaves of Phragmites australis obtained from four CWs during 2005–2008 are shown. During the peak biomass at the end of August both aboveand belowground biomass was harvested. Aboveground biomass was clipped at the ground level in four replicate quadrants (0.5 × 0.5 m), two of them in the inflow zone Table 1
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Average leaf/stem and root/leaf heavy metal concentration (mg/kg) ratios in Phragmites australis
Cu
Cd
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Cr
Ni
Pb
Zn
Hg
Leaf/stem
2.6
1.7
2.0
6.7
1.6
0.8
4.7
Root/leaf
9.0
18.4
72.7
3.4
37.0
5.5
2.5
̌ hov (4 years), Slavošovice Results from CWs Morǐ na (sampling in 4 consecutive years), Bre (3 years), Radotín (1 year). Total number of sampling events ¼ 12.
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and two of them in the outflow zone. The biomass was divided into stems, leaves (including leaf sheaths) and flowers and dried at 60 C until a constant weight was reached. Belowground biomass was dug out to the depth of 30 cm from all quadrants, carefully washed in tap water, divided into rhizomes and roots, and dried under the same conditions as aboveground biomass. Dried plant material was ground, and mineralized in nitric acid under high pressure and temperature in a microwave. The concentrations of heavy metal were determined using inductively coupled plasma mass spectrometry (ICP-MS). Higher concentrations of heavy metal in leaves than in stems are supposed to be a result of detoxifying/sequestration mechanisms in aerial organs. These mechanisms include complexation with ligands and/or their removal from metabolically active cytoplasm by moving them into inactive compartments, mainly vacuoles and cell walls (Rascio & Navari-Izzo ). It seems, however, that zinc concentration is commonly higher in stems than in leaves (Lehtonen ; Windham et al. ; Du Laing et al. ; Table 1). Schierup & Larsen () suggested that higher zinc concentrations in stems could occur due to its essential function in the formation of the plant hormone, indole acetic acid, which primarily performs its function in stems. The high concentrations of heavy metal in roots results from restricted translocation to the aboveground plant parts. Bragato et al. () pointed out that plants restrict upward movement of heavy metals in order to avoid the potential toxic effect of high metal concentrations on the photosynthetic tissues. In Table 2, examples of heavy metal concentrations in P. australis growing in both natural and CWs are shown. P. australis is probably the most frequently studied wetland plant in both natural and CWs and, therefore, it provides a good comparison. The data indicate that the concentrations in all plant parts vary considerably between studies but in general, concentrations in CWs mostly do not exceed those found in natural wetlands. The concentration of heavy metals in the plant biomass is important information; however, it provides no information about accumulation or translocation. In order to evaluate these parameters, plant biomass must be taken into consideration. W
HEAVY METAL ACCUMULATION IN PLANT TISSUES Total storage of a substance in a particular compartment is called standing stock. Standing stocks in vegetation are
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Examples of heavy metal concentrations (mg/kg) in Phragmites australis in natural and constructed wetlands reported in the literature
Rhizomes
Natural
Cd
0.03–5.0
0.014–0.68
0.04–2.1
0.13–1.13
0.06–1.0
Constructed
Cd
0.01–0.04
0.007–0.04
0.01–5.6
0.21–2.9
0.02–0.1
0.05–2.5
Samecka-Cymerman et al. (), Peverly et al. (), Liu et al. (), Lesage et al. (a), Lesage et al. (b), Khan et al. (), Du Laing et al. (), Vymazal et al. ()
Natural
Cr
0.2–160
0.3–120
1.2–11.4
0.5–65.4
1.4–10.5
3.2–42
Obolewski et al. (), Duman et al. (), Szymanowska et al. (), Samecka-Cymerman & Kempers (), Zhang et al. (); Du Laing et al. (), Baldantoni et al. (), Bonano & Lo Guidice (), Windham et al. (), Wells et al. (), Aksoy et al. (), Baudo et al. (), Du Laing et al. ()
Constructed
Cr
0.2–12.9
0.13–15.5
0.17–12.7
2.3–406
1.60
4.0–22.2
Mant et al. (), Lesage et al. (a), Lesage et al. (b), Khan et al. (), Liu et al. (), Bragato et al. (), Vymazal et al. ()
Natural
Cu
2.1–10.7
0.5–19.2
1.3–12.5
9.0–184
4.3–12.6
1.7–8.9
Peverly et al. (), Obolewski et al. (), Lesage et al. (b), Duman et al. (), Szymanowska et al. (), Samecka-Cymerman & Kempers (), Zhang et al. (), Du Laing et al. (), Baldantoni et al. (), Bonano & Lo Guidice (), Windham et al. (), Aksoy et al. (), Baudo et al. (), Du Laing et al. ()
Constructed
Cu
6.1–15
5.1–25
2.7–33
5.3–64
6.5–33
6.9–44
Yeh et al. (), Samecka-Cymerman et al. (), Peverly et al. (), Lesage et al. (a), Lesage et al. (b), Khan et al. (), Galletti et al. (), Liu et al. (), Bragato et al. (), Vymazal et al. ()
Natural
Ni
0.5–5.8
0.2–10.3
1.1–20.3
7.7–25.5
1.6–3.8
12.2
Obolewski et al. (), Duman et al. (), Szymanowska et al. (), Samecka-Cymerman & Kempers (), Liu et al. (), Du Laing et al. (), Baldantoni et al. (), Bonano & Lo Guidice (), Aksoy et al. (), Du Laing et al. ()
Constructed
Ni
0.47–2.8
0.54–2.0
1.3–2.4
4.9–16.7
1.87
4.2–13
Lesage et al. (a), Lesage et al. (b), Khan et al. (), Galletti et al. (), Bragato et al. (), Vymazal et al. ()
References
Peverly et al. (), Obolewski et al. (), Duman et al. (), Szymanowska et al. (), SameckaCymerman & Kempers (), Du Laing et al. (), Bonano & Lo Guidice (), Aksoy et al. (), Du Laing et al. ()
2015
(continued)
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HM
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BGa
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Table 2
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continued
Location
HM
Leaves
Stems
AGa
Roots
Rhizomes
BGa
Natural
Pb
0.1–22
0.21–9.9
0.12–26
0.3–142
0.3–22.7
Constructed
Pb
0.23–0.69
0.11–0.35
0.1–50
3.8–12.2
0.24–0.52
1.3–20
Samecka-Cymerman et al. (), Peverly et al. (), Liu et al. (), Lesage et al. (a), Lesage et al. (b), Khan et al. (), Vymazal et al. ()
Natural
Zn
11–1,300
10–137
8.6–58
1.3–588
17–66.8
8–30
Peverly et al. (), Obolewski et al. (), Duman et al. (), Szymanowska et al. (), SameckaCymerman & Kempers (), Zhang et al. (), Du Laing et al. (), Baldantoni et al. (), Bonano & Lo Guidice (), Windham et al. (), Wells et al. (), Aksoy et al. (), Baudo et al. (), Estabrook et al. (), Du Laing et al. ()
Constructed
Zn
29–59
18–70
17–65
46–165
12.2–22
32–184
Yeh et al. (), Samecka-Cymerman et al. (), Peverly et al. (), Liu et al. (), Lesage et al. (a), Lesage et al. (b), Galletti et al. (), Bragato et al. (), Vymazal et al. ()
References
Peverly et al. (), Obolewski et al. (), Duman et al. (), Szymanowska et al. (), SameckaCymerman & Kempers (), Du Laing et al. (), Baldantoni et al. (), Bonano & Lo Guidice (), Windham et al. (), Kufel (), Aksoy et al. (), Du Laing et al. ()
Heavy metals in plants in constructed wetlands
Table 2
a
2011), industrial effluent (Khan et al. 2009), landfill leachate (Peverly et al. 1995), swine operations (Yeh et al. 2009).
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AG ¼ aboveground, BG ¼ belowground, the numbers are not a summary for leaves and stems or roots and rhizomes, respectively, the numbers are given for studies where only total concentrations were given. Constructed wetlands
include those for municipal sewage (Samecka-Cymerman et al. 2004; Bragato et al. 2006; Lesage et al. 2007a; Lesage et al. 2007b; Liu et al. 2007; Bragato et al. 2009; Du Laing et al. 2009; Vymazal et al. 2009; Liu et al. 2010; Galletti et al.
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commonly computed by multiplying nutrient concentrations in the plant tissue by biomass per unit area and are expressed as mass per unit area (usually g m2 or kg ha1) ( Johnston ). Therefore, both biomass amount and heavy metal concentration are important for standing stock determination. In temperate and cold climates, the maximum standing stock for nutrients (nitrogen and phosphorus) usually occurs at the time of maximum biomass which, indeed, does not occur during the time of maximum concentration (early in the growing season). The standing stock for heavy metals, however, varies between metals and also between plants (Vymazal & Kröpfelová ) and therefore, there is no clear time pattern. Standing stock, and therefore accumulation of heavy metals, is usually higher in the belowground biomass as compared to aboveground biomass due to high concentrations in roots (Vymazal et al. , ). However, due to lower production of roots in heavily loaded CWs, the high concentrations of heavy metals in roots may not result in higher standing stock as compared to aboveground biomass. Data presented in Figure 1 clearly reveal how misleading it could be to estimate the accumulation of heavy metals in plants according to the concentration only. The results from CW Morǐ na in the Czech Republic (horizontal subsurface flow, in operation since 2001, municipal sewage, surface area 3,500 m2, 700 PE, filtration material: gravel 4/8 mm, planted with a mixture of Phalaris arundinacea and P. australis) show that, despite substantially higher zinc concentration in the roots and the belowground biomass as compared to concentrations in the aboveground parts, the standing stock is about four times higher in the aboveground biomass. The major factor is the low biomass of roots and rhizomes as compared to leaves and stems. The results in Figure 1 also indicate a high level of translocation from belowground to aboveground parts of P. arundinacea. The data were obtained using the same method described in the previous section on concentration.
SEASONALITY OF HEAVY METALS IN PLANT BIOMASS Heavy metal concentrations in the plant biomass of wetland plants vary considerably during the season but unfortunately, they do not follow the well-known pattern for nutrients (Figure 2). The concentrations of nutrients in aboveground biomass are highest during the early growing season and then steadily decrease as the concentration is ‘diluted’ by an increase in dry mass. However, for heavy metals, the seasonal
Figure 1
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Zinc concentration in various parts of Phalaris arundinacea (top), Phalaris biomass (middle) and zinc standing stock (bottom) at constructed wetland Morǐ na, Czech Republic.
pattern is very variable (Figure 2). Data in Figure 2 show three seasonal patterns for copper, zinc and lead in a sedge meadow in Sweden (Tyler ). The concentrations of copper followed the seasonality of nitrogen, zinc concentrations decreased in June but then remained more or less stable, while lead concentration decreased sharply between May and July and remained stable until September following a sharp increase up to the level measured in May. Bragato et al. () observed steady concentrations of Cr and Ni in P. australis during the period June–October followed by an
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shoots in the fall and winter, while concentrations of zinc steadily decreased from spring to winter. Moreover, seasonal patterns for one species may vary among various stands within one water body. This situation was, for example, reported by Baldantoni et al. () for P. australis in south Italy.
HEAVY METAL COMPARTMENTALIZATION WITHIN LEAVES AND STEMS It is generally accepted that concentrations of nutrients and heavy metals differ in the leaves and stems of wetland plants in relation to position on the shoot, but there is limited information available in the literature on this topic (e.g., Schierup & Larsen ). However, should this point be taken into account when measuring heavy metal concentration and calculating standing stocks in plants? For example, to evaluate heavy metal (and nutrient) concentrations and consequently standing stocks in the aboveground biomass, some authors analyzed ‘mature leaves picked randomly from the culm’ or ‘the upper leaves and the whole stem’ or ‘five leaves from the top of the shoot’. In 2014, an experiment was carried out at CW Morǐ na. Fifteen P. australis shoots were clipped at ground level and split into three sub-samples. The shoots were divided into thirds and divided into leaves, including the sheaths, (L) and stems (S). The lower parts were labelled S1/3 and L1/3, middle parts S2/3 and L2/3, and the upper parts of the shoots were labelled S3/3 and L3/3. The samples were dried in the oven at 60 C to a constant weight and analyzed for heavy metal according to the method described in the Concentration section of this paper. In Figure 3, the results of the study aimed at lead compartmentalization in the aboveground shoots of P. australis are shown. The highest concentration of lead was found in the leaves (mostly sheaths only) on the bottom part of the shoot, and lead concentrations in leaves sharply decreased towards the top of the shoot. The concentration of lead in stems followed the opposite distribution, with the highest concentrations in the top parts of the shoot. To calculate the average leaf and stem Pb concentration (CPb), it is necessary to include the biomass dry matter (DM) of individual compartments W
Figure 2
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Nitrogen, copper, zinc and lead concentrations in aboveground biomass of Triglochin maritimum (N) and Juncus gerardi (Cu, Zn, Pb) from sea-shore meadow in Sweden. Data elaborated from Tyler (1971).
extremely sharp increase in December. On the other hand, zinc and copper concentrations fluctuated only a little during the period June–December. Duman et al. () reported a sharp increase of lead concentration in P. australis
CPbleaf ¼ [(CPbleaf 1=3 × DMleaf 1=3 ) þ (CPbleaf 2=3 × DMleaf 2=3 ) þ (CPbleaf 3=3 × DMleaf 3=3 )]=(DMleaf 1=3 þ DMleaf 2=3 þ DMleaf 3=3 )
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in the lower stems resulted in the highest standing stock due to the high biomass of lower stems. Again, this is a clear example of how misleading the estimation of metal accumulation based on concentration only could be. Indeed, it is not possible for every measurement estimation to split shoots into more parts; however, to minimize potential error, for an appropriate estimation of heavy metal standing stock in the plant biomass it is necessary to (a) measure concentration separately in leaves and stems, (b) determine the biomass of stems and leaves separately, and (c) include all leaf and stem biomass in analyses rather than selecting only certain parts of the shoot.
CONCLUSIONS 1. Concentrations of heavy metal in plant biomass are similar in constructed and natural wetlands. 2. Concentrations usually decrease in the order of roots > rhizomes leaves > stems, with the possible exception of zinc, which usually exhibits higher concentrations in stems than in leaves. 3. The information about heavy metal concentrations does not provide any information about translocation and accumulation without knowing the amount of biomass. 4. Seasonal fluctuations of heavy metal concentrations in wetland plants vary between elements and also between stands. 5. Heavy metal standing stock depends both on metal concentration and plant biomass, but biomass is the more important factor. 6. Concentrations of heavy metal in leaves and stems vary in relation to the position within the shoot. 7. For appropriate evaluation of the aboveground standing stock, it is necessary to analyze leaves and stems separately and to use the whole shoot for analysis. Figure 3
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Average concentrations of lead, plant biomass and lead standing stock in leaves and stems in three different parts of Phragmites australis shoots at CW Morǐ na, Czech Republic.
The average lead concentration in the stem was calculated using the concentration and biomass of individual stem parts. The results shown in Figure 3 indicate that the value of the average lead concentration in leaves is more than five times lower than the lead concentration in the lower leaves. The data also revealed that biomass is a more important factor than concentration when calculating standing stocks. The extremely high lead concentration in the lower leaves resulted in a very low standing stock because of the low biomass of lower leaves. On the other hand, very low lead concentration
ACKNOWLEDGEMENT The study was supported by grant TA03030400 ‘Development of technologies for road and other paved areas stormwater runoff cleaning’ from the Technology Agency of the Czech Republic.
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Liu, J. G., Li, G. H., Shao, W. C., Xu, J. K. & Wang, D. K. Variations in uptake and translocation of copper, chromium and nickel among nineteen wetland plant species. Pedosphere 20, 96–103. Mant, C., Costa, S., Williams, J. & Tambourgi, E. Phytoremediation of chromium by model constructed wetland. Bioresource Technology 97, 1767–1772. Marschner, H. & Römheld, V. Root-induced changes in the availability of micronutrients in the rhizosphere. In: Plant Roots: The Hidden Half, (Y. Waisel, A. Eshel & U. Kafkaki, eds). Marcel Decker, Inc., New York, pp. 557–580. Obolewski, K., Skorbilowicz, E., Skorbilowicz, M., Gliň skaLewczuk, M., Astel, A. M. & Strzelczak, A. The effect of metals accumulated in reed (Phragmites australis) on the structure of periphyton. Ecotoxicology and Environmental Safety 74, 558–568. Pedersen, O., Sand-Jensen, H. & Revsbech, N. P. Diel pulses of O2 and CO2 in sandy lake sediments inhabited by Lobelia dortmanna. Ecology 76, 1536–1545. Peverly, J. H., Surface, J. M. & Wang, T. Growth and trace metal absorption by Phragmites australis in wetlands constructed for landfill leachate treatment. Ecological Engineering 5, 21–35. Rascio, N. & Navari-Izzo, F. Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting? Plant Science 180, 169–181. Römheld, V. The role of phytosiderophores in acquisition of iron and other micronutrients in graminaceous species: an ecological approach. Plant and Soil 130, 127–134. Samecka-Cymerman, A. & Kempers, A. J. Concentrations of heavy metals and plant nutrients in water, sediments and aquatic macrophytes of anthropogenic lakes (former open cut brown coal mines) differing in stage of acidification. The Science of the Total Environment 281, 87–98. Samecka-Cymerman, A., Stepien, D. & Kempers, A. J. Efficiency in removing pollutants by constructed wetland purification systems in Poland. Journal of Toxicology and Environmental Health, Part A 67, 265–275. Sand-Jensen, K., Prahl, C. & Stokholm, H. Oxygen release from roots of submerged aquatic macrophytes. Oikos 38, 349–354. Schierup, H.-H. & Larsen, V. J. Macrophyte cycling of zinc, copper, lead and cadmium in the littoral zone of a polluted and non-polluted lake. I. Availability, uptake, and translocation of heavy metals in Phragmites australis (Cav.) Trin. Aquatic Botany 11, 197–210.
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Senden, M. H. M. N., van der Meer, A. J. G. M., Verburg, T. G. & Wolterbeek, H. T. Citric acid in tomato plant roots and its effect on cadmium uptake and distribution. Plant and Soil 171, 333–339. Sorrell, B. K. & Armstrong, W. On the difficulties of measuring oxygen release by root systems of wetland plants. Journal of Ecology 82, 177–183. Szymanowska, A., Samecka-Cymerman, A. & Kempers, A. J. Heavy metals in three lakes in west Poland. Ecotoxicology and Environmental Safety 43, 21–29. Tyler, G. Distribution and turnover of organic matter and minerals in a shore meadow ecosystem. Oikos 22, 265–291. Vonwiren, N., Marshner, H. & Römheld, V. Roots of ironefficient maize also absorb phytosiderophore-chelated zinc. Plant Physiology 111, 1119–1125. Vymazal, J. & Kröpfelová, L. Wastewater Treatment in Constructed Wetlands with Horizontal Subsurface Flow. Springer, Dordrecht, The Netherlands. Vymazal, J., Kröpfelová, L., Švehla, J., Chrastný, V. & Štíchová, J. Trace elements in Phragmites australis growing in constructed wetlands for treatment of municipal wastewater. Ecological Engineering 35, 303–309. Vymazal, J., Kröpfelová, L., Švehla, J. & Štíchová, J. Can multiple harvest of aboveground biomass enhance removal of trace elements in constructed wetlands receiving municipal sewage? Ecological Engineering 36, 939–945. Weis, J. S. & Weis, P. Uptake, transport and release by wetland plants: implications for phytoremediation and restoration. Environment International 30, 685–700. Wells, J. R., Kaufman, P. B. & Jones, J. D. Heavy metal contents in some macrophytes from Saginaw Bay (Lake Huron, U.S.A.). Aquatic Botany 9, 185–193. Windham, L., Weis, J. S. & Weis, P. Uptake and distribution of metals in two dominant salt marsh macrophytes, Spartina alterniflora (cordgrass) and Phragmites australis (common reed). Estuarine Coastal and Shelf Science 56, 63–72. Yeh, T. Y., Chou, C. C. & Pan, C. T. Heavy metal removal within pilot-scale constructed wetland receiving river water contaminated by confined swine operations. Desalination 249, 368–373. Zhang, M, Cui, L., Sheng, L. & Wang, Y. Distribution and enrichment of heavy metals among sediments, water body and plants in Hengshuihu Wetland of Northern China. Ecological Engineering 35, 563–569.
First received 27 August 2014; accepted in revised form 28 November 2014. Available online 11 December 2014
© IWA Publishing 2015 Water Science & Technology
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Heavy metals in plants in constructed and natural wetlands: concentration, accumulation and seasonality ̌ zinová J. Vymazal and T. Bre
ABSTRACT The accumulation of heavy metals in plants is a function of uptake capacity and intracellular binding sites. The concentrations of heavy metals in plants growing in constructed wetlands vary considerably between species and systems but in general, the concentrations are within the range commonly found in natural stands. The highest concentrations are mostly found in roots, followed by rhizomes, leaves and stems. Unfortunately, concentration values are commonly used to evaluate the
J. Vymazal (corresponding author) ̌ zinová T. Bre Department of Applied Ecology, Faculty of Environmental Sciences, Czech University of Life Sciences in Prague, Kamýcká 129, 165 21 Praha 6, Czech Republic E-mail: [email protected]
‘accumulation’ of heavy metals, but this approach is not correct. In order to evaluate heavy metal accumulation, the biomass of particular plant parts must be taken into consideration. In addition, there are two other factors, which need to be taken into consideration when accumulation is evaluated, namely seasonality and distribution within the plant shoot. It has been found that the seasonal distribution of heavy metals in the biomass varies between heavy metals and mostly does not follow the pattern known for nutrients. In addition, the concentration and accumulation of heavy metals vary considerably within the shoot and this fact should be taken into consideration when analyses are carried out. Key words
| accumulation, constructed wetlands, heavy metals, macrophytes
INTRODUCTION Macrophytes have been shown to play important roles in wetland biogeochemistry through their active and passive circulation of elements (Weis & Weis ). The accumulation of a given metal is a function of uptake capacity and intracellular binding sites and, according to Clemens et al. (), it includes mobilization and uptake from the soil, compartmentalization and sequestration within the root, efficiency of xylem loading and transport, distribution between metals sinks in the aerial parts, sequestration and storage in leaf cells. The two most important soil/sediment factors influencing trace element mobility in wetland soils affected by plants are probably redox potential (Eh) and pH. Wetland plants influence the redox status in the rhizosphere due to their ability to transport oxygen to the roots (e.g., Armstrong ; Brix ; Sorrell & Armstrong ). This often leads to radial oxygen loss, which may depend on many factors, such as root biomass (Chen & Barko ), density (Pedersen et al. ), plant species (Sand-Jensen et al. ), location along the root (Connell et al. ), root age (Bedford et al. ), time of the day (Sand-Jensen et al. ) and season (Jacob & Otte ). doi: 10.2166/wst.2014.507
Metals may become mobilized from associated sulfides upon oxidation in the rhizosphere (Howarth & Teal ; Holmer et al. ) but due to their binding affinity, may adsorb to iron (oxy-)hydroxide (Jacob & Otte ). Rhizosphere pH affects the availability of both soil micronutrients and trace elements that are not essential for plant growth. With decreasing pH, the availability of essential trace elements such as zinc, iron and manganese is enhanced by desorption from soil particles. Furthermore, the availability of non-essential elements, such as cadmium, increases with decreasing pH as a result of increased solubility (Marschner & Römheld ). Acidification of the rhizosphere is very often the result of plant root exudate release that mobilizes sparingly soluble micronutrients (Doyle & Otte ). Of the plant organic acids, citric and malic acids have received particular attention (Brown ; Senden et al. ). Because of the high-binding capacity for metallic micronutrients by soil particles, plants have evolved several strategies for increasing their soil bioavailability. The most important strategy is probably the production of metal-chelating
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compounds (phytometallophores), such as mugenic and avenic acids, which are synthetized in response to iron, zinc and possibly other trace-element deficiencies (Kinnersley ; Cakmak et al. ). In the rhizosphere, phytometallophores chelate and mobilize trace elements and once chelated to phytometallophores, metal ions can be transported across the plasma membrane as a metal–phytomellophore complex via specialized transporters (Römheld ; Vonwiren et al. ; Clemens et al. ). The objective of this paper is to evaluate (1) concentrations of heavy metals in the aboveground biomass of plants growing in constructed wetlands (CWs) and to compare them with natural wetlands, (2) calculation of heavy metal accumulation in plants, (3) seasonal variation in heavy metal concentration in the plant biomass, and (4) distribution of heavy metals in the aboveground plant biomass.
CONCENTRATIONS OF HEAVY METALS IN PLANTS The concentrations of heavy metals in various parts of macrophytes growing in CWs, as well as in natural wetlands, generally decrease in the order of roots >rhizomes leaves > stems (e.g., Schierup & Larsen ; Peverly et al. ; Windham et al. ; Lesage et al. a; Vymazal & Kröpfelová ; Bonano & Lo Guidice ; Table 1). The concentrations of heavy metals in the belowground parts, namely roots, could be affected by heavy metals adsorbed onto the root surface. Before the analysis, the roots and rhizomes must be carefully washed but this procedure should be very gentle to prevent root loss. The amount of heavy metals could be increased in the presence of iron plaque where heavy metals may co-precipitate (Weis & Weis ). In Table 1, concentration ratios between leaves and stems and between roots and leaves of Phragmites australis obtained from four CWs during 2005–2008 are shown. During the peak biomass at the end of August both aboveand belowground biomass was harvested. Aboveground biomass was clipped at the ground level in four replicate quadrants (0.5 × 0.5 m), two of them in the inflow zone Table 1
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Average leaf/stem and root/leaf heavy metal concentration (mg/kg) ratios in Phragmites australis
Cu
Cd
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Cr
Ni
Pb
Zn
Hg
Leaf/stem
2.6
1.7
2.0
6.7
1.6
0.8
4.7
Root/leaf
9.0
18.4
72.7
3.4
37.0
5.5
2.5
̌ hov (4 years), Slavošovice Results from CWs Morǐ na (sampling in 4 consecutive years), Bre (3 years), Radotín (1 year). Total number of sampling events ¼ 12.
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and two of them in the outflow zone. The biomass was divided into stems, leaves (including leaf sheaths) and flowers and dried at 60 C until a constant weight was reached. Belowground biomass was dug out to the depth of 30 cm from all quadrants, carefully washed in tap water, divided into rhizomes and roots, and dried under the same conditions as aboveground biomass. Dried plant material was ground, and mineralized in nitric acid under high pressure and temperature in a microwave. The concentrations of heavy metal were determined using inductively coupled plasma mass spectrometry (ICP-MS). Higher concentrations of heavy metal in leaves than in stems are supposed to be a result of detoxifying/sequestration mechanisms in aerial organs. These mechanisms include complexation with ligands and/or their removal from metabolically active cytoplasm by moving them into inactive compartments, mainly vacuoles and cell walls (Rascio & Navari-Izzo ). It seems, however, that zinc concentration is commonly higher in stems than in leaves (Lehtonen ; Windham et al. ; Du Laing et al. ; Table 1). Schierup & Larsen () suggested that higher zinc concentrations in stems could occur due to its essential function in the formation of the plant hormone, indole acetic acid, which primarily performs its function in stems. The high concentrations of heavy metal in roots results from restricted translocation to the aboveground plant parts. Bragato et al. () pointed out that plants restrict upward movement of heavy metals in order to avoid the potential toxic effect of high metal concentrations on the photosynthetic tissues. In Table 2, examples of heavy metal concentrations in P. australis growing in both natural and CWs are shown. P. australis is probably the most frequently studied wetland plant in both natural and CWs and, therefore, it provides a good comparison. The data indicate that the concentrations in all plant parts vary considerably between studies but in general, concentrations in CWs mostly do not exceed those found in natural wetlands. The concentration of heavy metals in the plant biomass is important information; however, it provides no information about accumulation or translocation. In order to evaluate these parameters, plant biomass must be taken into consideration. W
HEAVY METAL ACCUMULATION IN PLANT TISSUES Total storage of a substance in a particular compartment is called standing stock. Standing stocks in vegetation are
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Examples of heavy metal concentrations (mg/kg) in Phragmites australis in natural and constructed wetlands reported in the literature
Rhizomes
Natural
Cd
0.03–5.0
0.014–0.68
0.04–2.1
0.13–1.13
0.06–1.0
Constructed
Cd
0.01–0.04
0.007–0.04
0.01–5.6
0.21–2.9
0.02–0.1
0.05–2.5
Samecka-Cymerman et al. (), Peverly et al. (), Liu et al. (), Lesage et al. (a), Lesage et al. (b), Khan et al. (), Du Laing et al. (), Vymazal et al. ()
Natural
Cr
0.2–160
0.3–120
1.2–11.4
0.5–65.4
1.4–10.5
3.2–42
Obolewski et al. (), Duman et al. (), Szymanowska et al. (), Samecka-Cymerman & Kempers (), Zhang et al. (); Du Laing et al. (), Baldantoni et al. (), Bonano & Lo Guidice (), Windham et al. (), Wells et al. (), Aksoy et al. (), Baudo et al. (), Du Laing et al. ()
Constructed
Cr
0.2–12.9
0.13–15.5
0.17–12.7
2.3–406
1.60
4.0–22.2
Mant et al. (), Lesage et al. (a), Lesage et al. (b), Khan et al. (), Liu et al. (), Bragato et al. (), Vymazal et al. ()
Natural
Cu
2.1–10.7
0.5–19.2
1.3–12.5
9.0–184
4.3–12.6
1.7–8.9
Peverly et al. (), Obolewski et al. (), Lesage et al. (b), Duman et al. (), Szymanowska et al. (), Samecka-Cymerman & Kempers (), Zhang et al. (), Du Laing et al. (), Baldantoni et al. (), Bonano & Lo Guidice (), Windham et al. (), Aksoy et al. (), Baudo et al. (), Du Laing et al. ()
Constructed
Cu
6.1–15
5.1–25
2.7–33
5.3–64
6.5–33
6.9–44
Yeh et al. (), Samecka-Cymerman et al. (), Peverly et al. (), Lesage et al. (a), Lesage et al. (b), Khan et al. (), Galletti et al. (), Liu et al. (), Bragato et al. (), Vymazal et al. ()
Natural
Ni
0.5–5.8
0.2–10.3
1.1–20.3
7.7–25.5
1.6–3.8
12.2
Obolewski et al. (), Duman et al. (), Szymanowska et al. (), Samecka-Cymerman & Kempers (), Liu et al. (), Du Laing et al. (), Baldantoni et al. (), Bonano & Lo Guidice (), Aksoy et al. (), Du Laing et al. ()
Constructed
Ni
0.47–2.8
0.54–2.0
1.3–2.4
4.9–16.7
1.87
4.2–13
Lesage et al. (a), Lesage et al. (b), Khan et al. (), Galletti et al. (), Bragato et al. (), Vymazal et al. ()
References
Peverly et al. (), Obolewski et al. (), Duman et al. (), Szymanowska et al. (), SameckaCymerman & Kempers (), Du Laing et al. (), Bonano & Lo Guidice (), Aksoy et al. (), Du Laing et al. ()
2015
(continued)
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HM
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BGa
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Table 2
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continued
Location
HM
Leaves
Stems
AGa
Roots
Rhizomes
BGa
Natural
Pb
0.1–22
0.21–9.9
0.12–26
0.3–142
0.3–22.7
Constructed
Pb
0.23–0.69
0.11–0.35
0.1–50
3.8–12.2
0.24–0.52
1.3–20
Samecka-Cymerman et al. (), Peverly et al. (), Liu et al. (), Lesage et al. (a), Lesage et al. (b), Khan et al. (), Vymazal et al. ()
Natural
Zn
11–1,300
10–137
8.6–58
1.3–588
17–66.8
8–30
Peverly et al. (), Obolewski et al. (), Duman et al. (), Szymanowska et al. (), SameckaCymerman & Kempers (), Zhang et al. (), Du Laing et al. (), Baldantoni et al. (), Bonano & Lo Guidice (), Windham et al. (), Wells et al. (), Aksoy et al. (), Baudo et al. (), Estabrook et al. (), Du Laing et al. ()
Constructed
Zn
29–59
18–70
17–65
46–165
12.2–22
32–184
Yeh et al. (), Samecka-Cymerman et al. (), Peverly et al. (), Liu et al. (), Lesage et al. (a), Lesage et al. (b), Galletti et al. (), Bragato et al. (), Vymazal et al. ()
References
Peverly et al. (), Obolewski et al. (), Duman et al. (), Szymanowska et al. (), SameckaCymerman & Kempers (), Du Laing et al. (), Baldantoni et al. (), Bonano & Lo Guidice (), Windham et al. (), Kufel (), Aksoy et al. (), Du Laing et al. ()
Heavy metals in plants in constructed wetlands
Table 2
a
2011), industrial effluent (Khan et al. 2009), landfill leachate (Peverly et al. 1995), swine operations (Yeh et al. 2009).
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AG ¼ aboveground, BG ¼ belowground, the numbers are not a summary for leaves and stems or roots and rhizomes, respectively, the numbers are given for studies where only total concentrations were given. Constructed wetlands
include those for municipal sewage (Samecka-Cymerman et al. 2004; Bragato et al. 2006; Lesage et al. 2007a; Lesage et al. 2007b; Liu et al. 2007; Bragato et al. 2009; Du Laing et al. 2009; Vymazal et al. 2009; Liu et al. 2010; Galletti et al.
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commonly computed by multiplying nutrient concentrations in the plant tissue by biomass per unit area and are expressed as mass per unit area (usually g m2 or kg ha1) ( Johnston ). Therefore, both biomass amount and heavy metal concentration are important for standing stock determination. In temperate and cold climates, the maximum standing stock for nutrients (nitrogen and phosphorus) usually occurs at the time of maximum biomass which, indeed, does not occur during the time of maximum concentration (early in the growing season). The standing stock for heavy metals, however, varies between metals and also between plants (Vymazal & Kröpfelová ) and therefore, there is no clear time pattern. Standing stock, and therefore accumulation of heavy metals, is usually higher in the belowground biomass as compared to aboveground biomass due to high concentrations in roots (Vymazal et al. , ). However, due to lower production of roots in heavily loaded CWs, the high concentrations of heavy metals in roots may not result in higher standing stock as compared to aboveground biomass. Data presented in Figure 1 clearly reveal how misleading it could be to estimate the accumulation of heavy metals in plants according to the concentration only. The results from CW Morǐ na in the Czech Republic (horizontal subsurface flow, in operation since 2001, municipal sewage, surface area 3,500 m2, 700 PE, filtration material: gravel 4/8 mm, planted with a mixture of Phalaris arundinacea and P. australis) show that, despite substantially higher zinc concentration in the roots and the belowground biomass as compared to concentrations in the aboveground parts, the standing stock is about four times higher in the aboveground biomass. The major factor is the low biomass of roots and rhizomes as compared to leaves and stems. The results in Figure 1 also indicate a high level of translocation from belowground to aboveground parts of P. arundinacea. The data were obtained using the same method described in the previous section on concentration.
SEASONALITY OF HEAVY METALS IN PLANT BIOMASS Heavy metal concentrations in the plant biomass of wetland plants vary considerably during the season but unfortunately, they do not follow the well-known pattern for nutrients (Figure 2). The concentrations of nutrients in aboveground biomass are highest during the early growing season and then steadily decrease as the concentration is ‘diluted’ by an increase in dry mass. However, for heavy metals, the seasonal
Figure 1
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Zinc concentration in various parts of Phalaris arundinacea (top), Phalaris biomass (middle) and zinc standing stock (bottom) at constructed wetland Morǐ na, Czech Republic.
pattern is very variable (Figure 2). Data in Figure 2 show three seasonal patterns for copper, zinc and lead in a sedge meadow in Sweden (Tyler ). The concentrations of copper followed the seasonality of nitrogen, zinc concentrations decreased in June but then remained more or less stable, while lead concentration decreased sharply between May and July and remained stable until September following a sharp increase up to the level measured in May. Bragato et al. () observed steady concentrations of Cr and Ni in P. australis during the period June–October followed by an
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shoots in the fall and winter, while concentrations of zinc steadily decreased from spring to winter. Moreover, seasonal patterns for one species may vary among various stands within one water body. This situation was, for example, reported by Baldantoni et al. () for P. australis in south Italy.
HEAVY METAL COMPARTMENTALIZATION WITHIN LEAVES AND STEMS It is generally accepted that concentrations of nutrients and heavy metals differ in the leaves and stems of wetland plants in relation to position on the shoot, but there is limited information available in the literature on this topic (e.g., Schierup & Larsen ). However, should this point be taken into account when measuring heavy metal concentration and calculating standing stocks in plants? For example, to evaluate heavy metal (and nutrient) concentrations and consequently standing stocks in the aboveground biomass, some authors analyzed ‘mature leaves picked randomly from the culm’ or ‘the upper leaves and the whole stem’ or ‘five leaves from the top of the shoot’. In 2014, an experiment was carried out at CW Morǐ na. Fifteen P. australis shoots were clipped at ground level and split into three sub-samples. The shoots were divided into thirds and divided into leaves, including the sheaths, (L) and stems (S). The lower parts were labelled S1/3 and L1/3, middle parts S2/3 and L2/3, and the upper parts of the shoots were labelled S3/3 and L3/3. The samples were dried in the oven at 60 C to a constant weight and analyzed for heavy metal according to the method described in the Concentration section of this paper. In Figure 3, the results of the study aimed at lead compartmentalization in the aboveground shoots of P. australis are shown. The highest concentration of lead was found in the leaves (mostly sheaths only) on the bottom part of the shoot, and lead concentrations in leaves sharply decreased towards the top of the shoot. The concentration of lead in stems followed the opposite distribution, with the highest concentrations in the top parts of the shoot. To calculate the average leaf and stem Pb concentration (CPb), it is necessary to include the biomass dry matter (DM) of individual compartments W
Figure 2
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Nitrogen, copper, zinc and lead concentrations in aboveground biomass of Triglochin maritimum (N) and Juncus gerardi (Cu, Zn, Pb) from sea-shore meadow in Sweden. Data elaborated from Tyler (1971).
extremely sharp increase in December. On the other hand, zinc and copper concentrations fluctuated only a little during the period June–December. Duman et al. () reported a sharp increase of lead concentration in P. australis
CPbleaf ¼ [(CPbleaf 1=3 × DMleaf 1=3 ) þ (CPbleaf 2=3 × DMleaf 2=3 ) þ (CPbleaf 3=3 × DMleaf 3=3 )]=(DMleaf 1=3 þ DMleaf 2=3 þ DMleaf 3=3 )
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in the lower stems resulted in the highest standing stock due to the high biomass of lower stems. Again, this is a clear example of how misleading the estimation of metal accumulation based on concentration only could be. Indeed, it is not possible for every measurement estimation to split shoots into more parts; however, to minimize potential error, for an appropriate estimation of heavy metal standing stock in the plant biomass it is necessary to (a) measure concentration separately in leaves and stems, (b) determine the biomass of stems and leaves separately, and (c) include all leaf and stem biomass in analyses rather than selecting only certain parts of the shoot.
CONCLUSIONS 1. Concentrations of heavy metal in plant biomass are similar in constructed and natural wetlands. 2. Concentrations usually decrease in the order of roots > rhizomes leaves > stems, with the possible exception of zinc, which usually exhibits higher concentrations in stems than in leaves. 3. The information about heavy metal concentrations does not provide any information about translocation and accumulation without knowing the amount of biomass. 4. Seasonal fluctuations of heavy metal concentrations in wetland plants vary between elements and also between stands. 5. Heavy metal standing stock depends both on metal concentration and plant biomass, but biomass is the more important factor. 6. Concentrations of heavy metal in leaves and stems vary in relation to the position within the shoot. 7. For appropriate evaluation of the aboveground standing stock, it is necessary to analyze leaves and stems separately and to use the whole shoot for analysis. Figure 3
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Average concentrations of lead, plant biomass and lead standing stock in leaves and stems in three different parts of Phragmites australis shoots at CW Morǐ na, Czech Republic.
The average lead concentration in the stem was calculated using the concentration and biomass of individual stem parts. The results shown in Figure 3 indicate that the value of the average lead concentration in leaves is more than five times lower than the lead concentration in the lower leaves. The data also revealed that biomass is a more important factor than concentration when calculating standing stocks. The extremely high lead concentration in the lower leaves resulted in a very low standing stock because of the low biomass of lower leaves. On the other hand, very low lead concentration
ACKNOWLEDGEMENT The study was supported by grant TA03030400 ‘Development of technologies for road and other paved areas stormwater runoff cleaning’ from the Technology Agency of the Czech Republic.
REFERENCES Aksoy, A., Demirezen, D. & Duman, F. Bioaccumulation, detection and analyses of heavy metal pollution in Sultan
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First received 27 August 2014; accepted in revised form 28 November 2014. Available online 11 December 2014
