Salt marsh macrophyte Phragmites australis strategies assessment for its dominance in mercury-contaminated coastal lagoon (Ria de Aveiro, Portugal) Naser A. Anjum, Iqbal Ahmad, Mónica Válega, Mário Pacheco, Etelvina Figueira, Armando C. Duarte & Eduarda Pereira Environmental Science and Pollution Research ISSN 0944-1344 Volume 19 Number 7 Environ Sci Pollut Res (2012) 19:2879-2888 DOI 10.1007/s11356-012-0794-3
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Author's personal copy Environ Sci Pollut Res (2012) 19:2879–2888 DOI 10.1007/s11356-012-0794-3
RESEARCH ARTICLE
Salt marsh macrophyte Phragmites australis strategies assessment for its dominance in mercury-contaminated coastal lagoon (Ria de Aveiro, Portugal) Naser A. Anjum & Iqbal Ahmad & Mónica Válega & Mário Pacheco & Etelvina Figueira & Armando C. Duarte & Eduarda Pereira
Received: 15 November 2011 / Accepted: 25 January 2012 / Published online: 8 February 2012 # Springer-Verlag 2012
Abstract Introduction and aims The dominance of a plant species in highly metal-contaminated areas reflects its tolerance or adaptability potential to these scenarios. Hence, plants with high adaptability and/or tolerance to exceptionally high metal-contaminated scenarios may help protect environmental degradation. The present study aimed to assess the strategies adopted by common reed, Phragmites australis for its dominance in highly mercury-contaminated Ria de Aveiro coastal lagoon (Portugal). Materials and methods Both plant samples and the sediments vegetated by monospecific stand of Phragmites australis were collected in five replicates from mercury-free (reference) and contaminated sites during low tide between March 2006 and January 2007. The sediments’ physico-chemical traits, plant dry mass, uptake, partitioning, and transfer of mercury were evaluated during growing season (spring, summer, autumn, and winter) of P. australis. Redox potential and pH of the Responsible editor: Stuart Simpson N. A. Anjum : I. Ahmad : M. Válega : A. C. Duarte : E. Pereira Centre for Environmental and Marine Studies (CESAM) and Department of Chemistry, University of Aveiro, 3810-193 Aveiro, Portugal I. Ahmad (*) : M. Pacheco Centre for Environmental and Marine Studies (CESAM) and Department of Biology, University of Aveiro, 3810-193 Aveiro, Portugal e-mail:
[email protected] E. Figueira Department of Biology, Centre for Cell Biology, University of Aveiro, 3810-193 Aveiro, Portugal
sediment around roots were measured in situ using a WTWpH 330i meter. Dried sediments were incinerated for 4 h at 500°C for the estimation of organic matter whereas plant samples were oven-dried at 60°C till constant weight for plant dry mass determination. Mercury concentrations in sediments and plant parts were determined by atomic absorption spectrometry with thermal decomposition, using an advanced mercury analyzer (LECO 254) and maintaining the accuracy and precision of the analytical methodologies. In addition, mercury bioaccumulation and translocation factors were also determined to differentiate the accumulation of mercury and its subsequent translocation to plant parts in P. australis. Results and conclusions P. australis root exhibited the highest mercury accumulation followed by rhizome and leaves during the reproductive phase (autumn). During the same phase, P. australis exhibited ≈5 times less mercurytranslocation factor (0.03 in leaf) when compared with the highest mercury bioaccumulation factor for root (0.14). Moreover, seasonal variations differentially impacted the studied parameters. P. australis’ extraordinary ability to (a) pool the maximum mercury in its roots and rhizomes, (b) protect its leaf against mercury toxicity by adopting the mercury exclusion, and (c) adjust the rhizosphere-sediment environment during the seasonal changes significantly helps to withstand the highly mercury-contaminated Ria de Aveiro lagoon. The current study implies that P. australis has enough potential to be used for mercury stabilization and restoration of sediments/soils rich in mercury as well. Keywords Phragmites australis . Abundance . Mercury . Sediments . Remediation . Exclusion . Tolerance
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1 Introduction Among major toxic metals, mercury is a global priority and widespread pollutant being introduced into the aquatic environments in coastal and estuarine areas including salt marshes by several pathways (Pereira et al. 2009). Mercury pollution has been shown to originate mainly from nonpoint and point anthropogenic sources such as agriculture, industry (e.g., chlor-alkali/coal-fired plants), and mining activities, through diffuse sources, or domestic/municipal wastes and waters (Pereira et al. 2009). Moreover, majority of these mercury sources have been regarded as the major responsible factors for the highest local environmental impacts (Pereira et al. 2009). Sediments are considered as a natural reservoir of mercury in aquatic environments including salt marshes and despite the cessation of the release of mercury-laden discharges into these areas sediments have been shown to constitute a historical record of this metal released over a period of time through exhibiting high mercury levels. Therefore, mercury-contaminated sediments are still a cause for concerns due to potential release of mercury into other environmental matrices including overlying water column and biota (Pereira et al. 2009). Moreover, like other toxic metals mercury cannot be degraded into less toxic components but rather only be immobilized in less available forms or physically removed, thus, majority of the metals, once released to the environment, remain as persistent contaminants in ecosystems (Weis and Weis 2004; Pereira et al. 2009). Plants have many natural properties such as (a) metal extraction: where they accumulate and extract metals from metal-polluted soil/sediment or water and (b) metal stabilization: where metal-tolerant plants reduce the mobility of metals, thereby reducing risks of further environmental degradation at varied extents (Pilon-Smits 2005; Prasad 2006). However, out of the two previous processes, the former may be negative to environment to a great extent since the above-ground organs laden with toxic metals may pave the way for their entry into food-chain after decomposition (Mertens et al. 2004). Therefore, based on the plants’ natural traits for metals, the selection of appropriate plants for a particular environment contaminated with specific toxic metals decides the effectiveness of a phytoremediation system. Additionally, the knowledge about the toxic metal accumulation, partitioning, or retention properties of aquatic plant species can be useful in choosing appropriate plants for successful phytoremediation systems in salt marshes or wetlands. In this perspective, salt marsh plants play significant role in the chemical speciation of trace metals and thus, control their bioavailability and toxicity to itself and to other biotic community through differential accumulation and partition or allocation of majority of sediment-associated metals in plant parts (Weis and Weis 2004; Válega et al.
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2008). As the majority of salt marsh plants have been shown to differentially accumulate, retain, partition, or allocate various toxic metals in below- and above-ground plants’ organs (Castro et al. 2009; Anjum et al. 2011a), it would be imperative to explore the metal-phytostabilizer and/or metal-excluder potential plant species in order to remediate toxic metals from the contaminated areas and hence to minimize the toxic metals-accrued degradation of varied environments. The salt marsh macrophyte Phragmites australis (Cav.) Trin. ex Steud is a rhizomatous plant with wide geographical distribution. Reports are available on the differential remediation ability of P. australis for considerable amounts of both nutrients, metals, and many other organic compounds from water, soil, and sediments (Windham et al. 2003; Weis and Weis 2004; Aksoy et al. 2005; Duman et al. 2007; Bragato et al. 2009; Černe et al. 2011) and also on its tolerance to varied environmental conditions. However, to the authors’ knowledge, no report is available which interprets the mercury accumulation, partitioning, and its subsequent transfer ability of P. australis within the plant system in relation to the significance of these processes for its dominance in areas with high mercury levels. Thus, assuming the fact that biota of trace metalcontaminated areas may exhibit their extraordinary ability or adaptability to withstand in and tolerance to elevated levels of toxic metals, the current study was carried out to evaluate the strategies adopted by P. australis for its dominance at the mercury-point source (exhibiting 64% coverage) (Válega et al. 2008) in mercury-contaminated Laranjo basin, in the Ria de Aveiro coastal lagoon (Northwestern Portugal) through evaluating the uptake, partitioning, and transfer of mercury into P. australis plant parts during its growing season (spring, summer, autumn, and winter). A well-defined mercury gradient was identified in Laranjo basin due to chlor-alkali plant discharges, and since no other important sources of contaminants other than mercury have been reported in this area, Laranjo basin has been regarded as “field laboratory” for assessing mercury toxicity under realistic environmental conditions (Pereira et al. 2009). Additionally, such a situation may also provide an in situ model in context with the current study for the assessment of strategies adopted by P. australis for its dominance in highly mercury-polluted Ria de Aveiro coastal lagoon.
2 Materials and methods 2.1 Study area The Ria de Aveiro is a temperate shallow coastal lagoon (45 km length; 10 km wide) located along the Atlantic Ocean on the northwest coast of Portugal (40′38′N, 8′44′W). Within
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Ria de Aveiro, there is a confined area called Laranjo basin which is one of the most mercury-contaminated coastal areas in Portugal, where several tons of mercury has been deposited mainly in the sediments due to discharges from a chlor-alkali industry over the last 50 years (Pereira et al. 1998). Although the mercury discharge diminished considerably in the last two decades, mercury concentration in the surface sediments of Laranjo basin is still much higher than pre-industrial levels (Pereira 1997). One sampling site (contaminated, C) was selected at main mercury point source in the Laranjo basin whereas samples were also collected from a mercury-free site (reference, R at Chegado Quay) as detailed also in our earlier reports (Válega et al. 2008; Anjum et al. 2011a) (Fig. 1).
showed its capacity for varied elements bioaccumulation (Duman et al. 2007; Bragato et al. 2009). 2.3 Samplings Both plant samples and the sediments vegetated by monospecific stand of P. australis were collected from R (reference) and C (contaminated) sites during low tide between March 2006 and January 2007. Plants were collected in five replicates at each sampling location, and a composite sample was used for determination of total mercury concentration. Sediments of the rhizosphere of each plant (10–15 cm depth) were also collected with a stainless steel shovel. All samples were transported to the laboratory under refrigerated conditions.
2.2 Plant material P. australis (Cav.) Trin. ex Steud. is a C3 monocot, large, perennial grass (hemicryptophyte/geophytes), belonging to Poaceae family and forms wide stands known as reed beds, hence also called common reed, prefers lakes and rivers or brackish wetlands such as marshes, across temperate and tropical regions all over the world (Pignatti 1982), is the most common species of the Phragmites genus, and is one of the most distributed macrophytes in aquatic ecosystems. This species has been reported to prefer eutrophic and stagnating waters and tolerate a moderate salinity (Cooper et al. 1996). Moreover, numerous studies
2.4 Sediment physico-chemical analysis and determination of plant dry mass Redox potential (Eh) and pH of the sediment around roots were measured in situ using a WTW-pH 330i meter. After sampling, sediment sub-samples were analyzed for organic matter content (OMC) as a percentage of loss on ignition (% LOI). Dried sediments were incinerated for 4 h at 500°C (Pereira 1997). Organic matter content was calculated as the weight lost during incineration and expressed as percentage of dry weight. Plant samples were oven-dried at 60°C till constant weight and the plant dry mass were determined.
N Industrial effluent discharge Portugal
Estarreja Aveiro
C
Chegado Quay
Laranjo Bay
R 0 Fig. 1 Location of the Laranjo basin with the sampling stations
0.5 1 km
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2.5 Determinations of mercury concentrations in sediments and plant biomass Mercury concentrations in sediments and plant parts (viz., roots, rhizomes, and leaves) were determined by atomic absorption spectrometry (AAS) with thermal decomposition, using an advanced mercury analyzer LECO 254. This methodology is simple and based on a thermal decomposition of the sample and collection of the mercury vapor on a gold amalgamator (Costley et al. 2000). The equipment includes a Ni boat in a quartz combustion tube, containing a catalyst, where the sample (between 50 and 500 mg) is initially dried at 120°C prior the combustion at 680–700°C (150 s) in an oxygen atmosphere. The mercury vapor is collected in a gold amalgamator and, after a pre-defined time (45 s), the amalgamator is heated at 900°C. The released mercury is transported to a heated cuvette (120°C) and then analyzed by AAS using a silicon UV diode detector. The accuracy and precision of the analytical methodology for mercury determinations was assessed by replicate analysis of certified materials, BCR-060 (trace elements in an aquatic plant) and NRC PACS 2 (trace elements in marine sediment). Certified and measured values were in general agreement, varying the recovery efficiency between 91% and 102% for BCR-060 and between 60% and 105% for PACS 2. 2.6 Mercury bioaccumulation and translocation factors To differentiate the accumulation of mercury and its subsequent translocation to plant parts in P. australis, mercury bioaccumulation factors (sediment-to-root; sediment-torhizome; sediment-to-below ground parts, roots+rhizome; and sediment-to-leaf) and mercury-translocation factor (root-to-leaf and below-ground parts-to-above ground parts) were determined. Mercury bioaccumulation factor was calculated as mercury concentration ratio of plant-tosediment, whereas mercury translocation factor was described as ratio of mercury in leaf to that in plant root/rhizome. 2.7 Data analysis The data are expressed as mean±SD. Data were evaluated using analysis of variance (two-way factor without replication) and Student’s t test for determining the significant change over control values. The significance level was set at P
