THE ROLE OF HALOPHYTES IN THE TAGUS ESTUARY ENVIRONMENTAL QUALITY

THE ROLE OF HALOPHYTES IN THE TAGUS ESTUARY ENVIRONMENTAL QUALITY

I. Caçador & C. Vale*

ABSTRACT

Concentrations of zinc, lead, copper and cadmium in the root, stem and leaf of Spartina maritima, Halimione portulacoides and Arthrocnemum fruticosum, as well as in the sediment between roots, were surveyed in three salt marshes of the Tagus estuary. The highest metal concentrations both in sediments and in plants were found in the marshes near the industrial and urban areas. Among the analysed tissues, roots presented the higher metal concentrations and only a fraction was translocated to the earial parts. The results show that plants participate in the metal cycling basically though their subterranean components acting as temporary sinks for metals.

Instituto de Ocenografia, Departamento de.Biologia Vegetal, Faculdade de Ciências da Universidade de Lisboa, Bloco C2, Campo Grande, 1700 Lisboa Portugal

* IPIMAR, Instituto de Investigação das Pescas e do Mar, Av. Brasília, 1400 Lisboa, Portugal

INTRODUCTION

Salt marshes are important natural filter systems, removing nutrients and heavy metals from flooding water in estuaries (Oenema et al, 1988; Orson et al., 1992; Caçador et al., 1993). As a rule, salt marshes are covered with dense vegetation which acts as a trap for estuarine sediments and their associated pollutants (ADAM, 1990). The halophytic vegetation may interact with the metals, namely by changing the environmental conditions (Tinker & Barraclough, 1988; Otte, 1991) and accelerating metals recycling inside the sediments (Bourg, 1987). The amount of metals uptaken by the plants depends on their availability, which is a function of several factors, namely organic matter, pH, redox potencial, metal speciation and root-sediment interactions (Alloway, 1990). In this paper we report the levels of zinc, lead, copper and cadmium in Spartina maritima (Poales: Poaceae), Halimione portulacoides (Caryophyllales: Chenopodiaceae) and Arthrocnemum fruticosum (Caryophyllales: Chenopodiaceae) from the Tagus salt marshes and in the sediment between roots, and the metal partitioning in this system.

The Tagus Estuary

The Tagus estuary is one of the largest estuaries on the Atlantic coast of Europe, covering an area of 300 km2 at low tide and 340 km2 at extreme high tide (Fig. 1). The southern and eastern parts of the estuary contain extensive intertidal mud-flat areas with the presence of Spartina maritima, Halimione portulacoides and Arthrocnemum fruticosum. Due to the highly branched system of channels all the salt marsh area is inundated daily by the tide. The salt marsh sediments are mainly silt and clay. Contrary to many cases in Europe, where pollutants from industrial regions are discharged into rivers and brought to the estuaries via the rivers, in the Tagus most pollutants are discharged directly into the estuary. The estuary receives effluents from about 2.5 million inhabitants living in the Greater Lisbon area, together with the discharges from industries (chemicals, steelmaking, and shipbuilding). Previous studies showed that Tagus salt marshes receive large quantities of anthropogenic metals and incorporate them into the sediments (Vale, 1990; Caçador et al., 1993). However, different sink capacities for metals were observed in these salt marshes: Pb >> Zn > Cu > Cd (Caçador et al., 1996).

Fig. 1. The Tagus estuary showing the location of the sampling sites.

SAMPLING AND METHODS

Sediments between roots (5-15 cm) were sampled in September 1989 from three sites (S, H, A) of three Tagus salt marshes (Pancas, Rosário e Corroios) with different degrees of metal contamination. Each site corresponds to a different plant colonization: Spartina maritima (S); Halimione portulacoides (H); Arthrocnemum fruticosum (A). In the laboratory, sediment samples were dried, roots removed and homogenized. After homogeneizing, sediments were extracted with the following solutions: H2O; ammonium acetate solution (1M, pH 7) ; 0.005M DTPA in CaCl2; 0.1M triethanolamine at pH 7.3; and HNO3/HCl. For the water, NHO4Ac extractants and DTPA, 10 ml of solution were added to 2g dry sediment in polypropylene bottles and shaken on a rotating shaker for two hours at room temperature. The suspension was then filtered (Piccolo, 1989). For the HNO3/HCl extraction 10 ml of HNO3/HCl (3:1v/v) was added to 2g of dry soil twice at 130oC (Otte, 1991). The extractions were done independently and, thus, are not sequential extractions. Metal concentrations in the solutions were determined by atomic absorption spectrometry. Eight plants of Spartina maritima; Halimione portulacoides; Arthrocnemum fruticosum were collected and transported to the laboratory in plastic bags. The plants were washed with demineralized water, separated in roots, stems and leaves dried and homogenized. For the analysis of Zn, Pb, Cu and Cd, 10 ml HNO3/HClO4 were added to 100 mg of each plant material according to the methodology described in Otte (1991). Standard additions and sludge plus vegetal reference materials were used for sediment and plant analysis, respectively.

RESULTS

Roots, stems and leaves of the analysed plants contained distinct levels of Zn, Pb, Cu and Cd (Fig. 2). Zinc was the most abundant metal in all analysed parts of the plants. The highest metal concentrations were recorded in the root system, and only small fractions were found in the above ground parts of the plant. The accumulation partition was more prononced for Pb and Cd, since these metals were more efficiency stored in the roots, than for Zn and Cu that are translocated to the upper parts. The metal concentrations varied with the plant species and with the salt marsh. The differences were more stricking between Pancas and the other two marshes (Rosário and Corroios). Metal concentrations in sediments between roots were not uniformly high in salt marshes (Fig. 3). Sediments collected at different plant roots showed different metal concentrations, but a pattern for the three salt marshes was not found. Levels of Pb and Cu were lower in Pancas than in the other two studied marshes. These differences are statistically valid (p<0.01). Concentrations of Zn, Pb, Cu and Cd were determined in different chemical extractions of the same sediment samples: water, ammonium acetate and DTPA (Table 1). The metals removed by these procedures are assumed to simulate the metal uptake by plants (PICCOLO, 1989; Rozema et al., 1990). The quantities of metals extracted by water and NHO4Ac solution were small fractions of the total concentration. The DTPA extracted higher quantities particularly of Cd. To compare the ability of each plant to uptake metals from the sediment, the ratios [metal]root/[metal]sediment, were calculated for each metal in the three different salt marshes (Table 2). The highest ratios were determined for Cd (2.7-4.1), however for other elements values were close to one, meaning that concentrations in sediments and roots are the not very different.

Fig. 2. Zinc, lead, copper and cadmium concentrations (µg g-1, dry weight)), in roots (), stems () and leaves () of Spartina maritima (S), Halimione portulacoides (H) and Arthrocnemum fruticosum (A) in three salt marshes (Pancas, Rosário and Corroios) of the Tagus estuary.

Fig. 3. Mean of zinc, lead, cooper and cadmium concentrations, in the sediments between roots of Spartina maritima (), Halimione portulacoides (), and Arthrocnemum fruticosum (), (µg g-1 dry weight) collected at Pancas, Rosário and Corroios salt marshes in the Tagus estuary.

Table 1. Percentagens of Zn, Pb, Cu and Cd recovered with water, ammonium acetate and DTPA in relation to total concentrations in sediment between roots of Spartina maritima, Halimione portulacoides and Arthrocnemum fruticosum from the three Tagus salt marshes: Pancas (P), Rosário (R) and Corroios (C).

Specie/Metal	P	H2O R	C	P	NH4OAc R	C	P	DTPA R	C
Zn S. maritima H. portulacoides A. fruticosum Pb S. maritima H. portulacoides A. fruticosum Cu S. maritima H. portulacoides A. fruticosum Cd S. maritima H. portulacoides A. fruticosum	0.4 0.1 0.5 <0.1 <0.1 <0.1 0.8 <0.1 <0.1 0.7 <0.1 <0.1	0.1 0.2 0.3 <0.1 <0.1 <0.1 <0.1 0.6 0.2 <0.1 <0.1 <0.1	0.1 0.3 0.5 0.2 <0.1 <0.1 0.2 <0.1 <0.1 0.4 1.5 1.0	1 0.6 0.3 <0.1 0.7 <0.1 2.1 0.7 1.0 0.6 15.4 <0.1	0.3 2.6 2.2 <0.1 <0.1 0.6 0.8 0.4 <0.1 0.5 9.1 7.0	0.7 1.7 0.2 <0.1 <0.1 <0.1 0.8 0.9 <0.1 7.7 7.7 15.0	12.6 21.5 10.6 6.7 8.2 13.1 4.7 8.4 5.5 6.6 15.4 13.3	3.7 3.7 8.2 1.5 3.4 2.0 5.3 4.7 1.7 26.6 11.0 10.0	3.8 5.7 4.4 6.3 4.0 5.3 2.7 3.5 3.5 15.4 15.4 10.0

Tabela 2. Mean ratios of root/sediment concentrations for Zinc, Lead, Copper and Cadmium (µg µg-1) in areas colonised by Spartina maritima, Halimione portulacoides e Arthrocnemum fruticosum collected at Pancas, Rosário and Corroios (Tagus estuary salt marshes).

Species/Local	Zn	Pb	Cu	Cd
S. maritima Pancas Corroios Rosário	0.8 1.0 0.5	0.3 0.6 1.0	0.6 0.7 1.1	2.8 3.3 3.9
H. portulacoides Pancas Corroios Rosário	1.1 1.3 1.1	0.4 1.5 1.4	0.5 1.5 2.2	3.7 3.5 3.0
A. fruticosum Pancas Corroios Rosário	2.4 2.0 1.3	1.6 1.1 1.4	1.7 0.7 0.8	4.1 2.7 3.9

DISCUSSION

The halophytes play an important role on metal recycling in salt marshes, and this function appears to be an important vector helping to reduce the effects of metal contamination in estuarine areas. It is well documented that transition elements are acumulated in salt marsh plants during the growth season (Alberts et al., 1990) and the incorporation is mostly in the root system, only a small portion being translocated to the above ground parts (Rozema et al.,1990). The metal uptake by the roots involves complex processes due to the nature of the root-sediment interactions (Tinker & Barraclough, 1988; Otte, 1991). The chemistry of the rizosphere is very different from the surrounding sediment environment (Ernst, 1990). As plants colonise the sediment, oxygen is delivered by the roots, sulphide forms are oxidised and the micro-environment around the roots becomes more oxidative and acid (Madureira et al.1994; Caçador et al., 1996). In certain parts of the roots it may be formed iron plaques (Crowder et al., 1987; otte et al., 1989), that in the Tagus are degenerated in thick iron concretions, called rhizoconcretions (Vale et al., 1990). With such a variety of heterogeneous processes, metal uptake by salt marsh plants has a still limited understanding. Although the transfer of metal from sediment to root is not well clarified, the Tagus salt marsh plants accumulate considerable quantities of metals. For example, cadmium concentration in roots of Spartina maritima, Halimione portulacoides and Arthrocnemum fruticosum is 2-4 times the levels existing in the bulk sediment. The accumulation becomes particularly relevant in this ecosystem because the root biomass is high, the root:sediment proportion reaching a maximum of 1:4 (weight:weight) at the end of growth season (Caçador et al., submited). The roots are, thus, an important component of the salt marsh sediments interfering actively with the metal cycling.

As plants die roots are incorporated in the sediment as organic debris and metals return to the sediment. However, only a small fraction of the metals in the sediment between roots is available to the plants. Apparently this fracion barely exceeds 20% and this limit does not vary a great deal with the degree of metal contamination (except for Zn). Previous work has show that the residual fraction of metals in the sediment increases with depth presenting a sub-surface maximum root density is higher (Caçador et al., 1996a). Metals appear thus to be immobilised as a consequence of root activity and that may prevent the toxic action of these elements in the estuarine ecosystem.

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