Cadmium accumulation by halimione portulacoides (L.) aellen. A seasonal study

Marine Environmental Research 33 (1992) 17-29

Cadmium Accumulation by Halimione portulacoides (L.) Aellen. A Seasonal Study F. R e b o r e d o New University of Lisbon, Vegetal Biology Unit, 2825 Monte da Caparica, Portugal (Received 16 November 1990; revised version received 3 June 1991; accepted 23 June 1991)

ABSTRACT The analysis of Cadmium in soils and vegetation samples collected in several sampling sites in north and south banks of the River Sado estuary was carried out over the course of a year. The results confirm that Cd is easily taken up by H. portulacoides roots and translocated to the leaves. In 75% of the cases the Cd content of leaves was higher than the root content, enhancing the great mobility of this element. A well defined Cd accumulation pattern was observed, the maximum values being obtained in July and October for roots and leaves, respectively. The accumulation of Cd in soil-marshes varies according to the nature of the matrix. The levels in sandy soils are lower than those observed in silty-loam soils; however, neither the organic matter nor the finest fraction of the soil ( < 63 #m ) constituted important binding sites, since r values were not significant at the 0"05 significance level. The highest Cd levels in soils were generally found in two distinct sampling sites, one located in the south bank,far from the major pollution sources, and the other in the north bank, next to several industrial plants and very close to a densely populated area, indicating that the sources of contamination are d(fferent.

INTRODUCTION The increased concentration of heavy metals in salt marshes raises the question of identifying the metal levels that individual species can tolerate without affecting the whole ecosystem. Although metal uptake by marsh plants has been studied (Newell et al., 1982; Reboredo, 1985, 1988a, 1988b), 17 Marine Environ. Res. 0141-1136/92/$05.00© 1992ElsevierSciencePublishers Ltd, England. Printed in Great Britain

1g

t'~ Rehore~b~

the consequences io the structure and funclioning of the ecosystem had never been evaluated Grazing species living in salt marshes may be continuously exposed, particularly if leaves of contaminated plants are the main food source and the main organ for metal accumulation, e.g. Zn in H a l i m i o n e plants collected in the natural habitat (Reboredo, 1988a). Decomposing plant debris can also support numerous feeders and grazers, with implications for contamination of food chains. Although some heavy metals such as cadmium (Cd), mercury (Hg} and lead (Pb) are non-essential for life, they may be absorbed and cause damage. For example, Cd has deleterious effects on crop plants (Greger & Lindberg, 1986), diatoms (Rachlin et al., 1982; Jones et ell., 1987), or even man (Nogawa et al.. 1985), which is related with its great mobility in biological systems, its strong affinity for thiol-containing compounds and the possibility of competing with zinc (Zn) (an essential metal) in biochemical reactions, clue to the similar electronic configuration. The studied area (River Sado basin) receives untreated domestic sewage from Setfibal (Fig. 1), a densely populated area with approximately 70 000 inhabitants receiving industrial discharges from various pollution sources, e.g. shipbuilding; fertilizer, cement and metallurgy plants; pulp and paper mills; olive oil and canned food processing; and agricultural wastes from rice fields. An important mining activity (pyrite extraction) located upstream must also be taken into account, since Cd is one of the major elements entering the Sado basin. The aim of the present study was to investigate the levels of Cd in the soilmarsh and in the halophyte H a l i m i o n e p o r t u l a c o i d e s (L.) Aellen, a common

Fig. !.

Localization of the sampling points.

Cadmium accumulation by Halimione portulacoides

19

and representative species colonizing the substrate. The work was carried out during the course of a year at seven sampling sites.

MATERIAL AND METHODS Plant and soil samples were collected in April, July and October 1987 and January 1988, from seven sites shown in Fig. 1. Plant material was rinsed with dionized water in order to remove fine particles and ephyphytes, especially in the stems, and dried at 70°C to constant weight (yellow-green leaves, young leaflets, lignified stems and dead roots were not considered for metal determination). Cores were hand-collected during low tide and divided into three sections (0-5 cm, 5-10 cm and 10-15 cm depth). Soil characterization was done for each core according to the methodology described by Rivi6re (1977). In order to remove organic debris, soils were immersed in double-distilled water in a borosilicate beaker for 5 days and were passed through a nylon sieve (mesh < 63 #m). The residual fraction consisted mainly of decomposing detritus and live plant material (especially roots) plus sand. Sand was separated from the organic material and added to the rest of the soil. After sieving, the remaining sample was allowed to settle and the supernatant was carefully removed. The sample was then dried at 70°C to constant weight, crushed in an agate mortar, and dried again to constant weight. For digestion each gram of dry soil and vegetation samples was placed in a 100 ml borosilicate beaker with 10 ml HNO a and evaporated until dry. The samples were digested again with 10ml of HNO3 and 5ml of HC10 4 and evaporated until dry. The residue was dissolved in a 2% aqueous solution of HC1, filtered and diluted to a final volume of 10 ml (Agemian & Chau, 1976). Cadmium was determined by atomic absorption spectrometry using a Perkin-Elmer Model 5000 with deuterium background corrector. When necessary, the graphite atomizer furnace was used. The operating conditions were those recommended by the manufacturer. Pro-analysis grade reagents (Merck) were used in every case. Standards were prepared by serial dilution of commercially available stock solutions. Each analysis was carried out in triplicate, taking as the final result the arithmetic mean of the three analyses. Three-way analysis of variance and the Scheff6 multiple comparison method were used to examine the differences of metal levels between compartments (biota and substratum), sampling sites and sampling months. A value of P < 0.05 was considered to be significant.

2(!

~ Reboredo

"FABLE I Cadmium Levels in the Leaves, Stems and Roots of Hal±re±one portulacoides and in the Sol Salt-Marshes. Expressed as/~g g- ' Dry Weight Mean Value + Standard Deviation A. April 1987 Organ

Station Froia

Leaf Stem Root Soil depth (cm) 0-5 5-10 10--15

I:tar

Batalha 3

Setenat c IE ) 4,4

Setenave

Mourisca

Gambia

5

6

iVY')

l

2

4B

1.2±0.2 0.7-+0.2 0.9±0.4

1.0-+0-1 0.6 ±0.2 0.4±0.1

11 ±0.3 0.7+0.2 1.6±0.1

t.4-+0.1 0.4-+0.1 2.24-0.3

1.1-+0.2 0.5_+0-3 0.5±0.1

1.3 ±0.4 0.8 ±0.2 0.6±0-2

I2±0.2 0.5_+0.1 0.4_+0.1

1"3_+0-3 1-1±0-3 0-5±0-2

1'1±0.3 0.8±0-3 0"6±0"2

2"0±0"4 2"2±0-6 1'9±0"2

1"8-+0"3 1'8±0"1 2"24-0"3

1'9±0"6 1"2±0'4 1.2±0"3

1"5±0-2 0-9_+0-3 0-9±0.2

l'5-+~5 1"5±0"8 1.4±0.4

Mour~ca

Gambia

B. July 1987 O~an

Station ~oia

Etar

Bata~a

~tenave

1

2

3

4A

~tenave IW) 4B

3.5±0-7 0.44-0.1 3.2±0.5

3.3±0.9 2.7±0.6 3.8±1-6

3.4±0.6 22±0"5 2.8±0-8

4.9±0-8 0.8±0.2 4-9±0.6

4,0±0.4 2.3±0.6 2.9±0.8

3.64-0.6 16±0.3 2.8±0-9

38±1-0 2.2±0.3 3.4±1.2

0.8___0.2 0-5+0.2 0.4-+0.1

2"1_+0-2 1.9_+0-4 1-6_+0-3 1.8+0.6 1.2-+0-2 2-1 4-0.1

2.1_+0.5 2.1 +0-4 1.34-0.7

1.6___0-4 1-5__+0.2 1.3_+0-4

0.9 ±0.2 0-5 ± 0.2 0.4+_0.2

1.94-0.4 1.2_+0-3 1.3-+0-2

Setenat,e (E) 4A

Setenave (W) 4B

Mourisca

Gambia

5

6

(E)

Leaf Stem Root Soil depth (cm) 0-5 5-10 10--15

5

C. October 1987 Organ

Leaf Stem Root Soil depth (cm) 0-5 5 10 10-15

Stathm Troia

Etar

Batalha

1

2

3

3.0±0.4 1-4_+0.6 1.9±0.5

1-7± 0.8 1.4±0.4 2.5+0.8

4-0± 1-3 1.7+0.4 3.9-+0-4

4.8± 1.0 16±0'6 3.9±0-2

4.6+ 1.0 2.4±0.6 2.9±0.8

4.6+0.7 1.8±0-3 2.3+0.4

0-7±0"3 0"2±0"1 0'2&0'l

2 " 2 ±0 " 3 1'8±0-7 1"6±0"3

t'9±0"1 1"8±0'7 1"9±0"2

2"2±~5 1"4±0"1 1"5±0.2

1"4±ff4 2'3±0"5 1.4±0.2

0 " 5 ± 0 " 3 2-0±0"6 0"4±0.3 1'1±0'3 0'2±0-1 1"3±0.2

4.7-+1.0 22+0.5 1.9+0.4

Cadmium accumulation by Halimione portulacoides

21

TABLE l----contd. D. January 1988 Organ

Leaf Stem Root Soildepth Icml ~5 5-10 1~15

Station Troia

Etar

I

2

2.8±0.3 1.0±0.1 1.9±0.3

Batalha 3

1.9±0.2 1.6±0.2 1 . 2 ± 0 - 1 0.8±0.1 1.0±0.1 3.6±0.7

0-8±0'2 1'0±0'1 0.7±0.1 0'6±0"1 0"5±0"1 0 . 6 ± 0 - 1

1'9±0-1 1"7±0"2 1.7±0.3

Setenave (E) 4A

Setenave (W) 4B

Mourisca Gambia

2.4±0-2 0.8±0.1 1.0±0.1

1-8±0-1 1.0±0.1 1.1±0.1

1.9±0.3 2.5±0.3 1 ' 2 ± 0 " 1 1'1±0'1 0'9±0.1 I-0±0-1

1"5±0"2 2"4±0'4 1.5±0.3

2"2±0"3 2"2±0"2 1"8±0"4

1.4±0.1 0.5±0.1 0.7±0.1

5

6

1.4±0.2 1.4±0.1 1"6±0"3

RESULTS A N D DISCUSSION The results showed that Cd was easily accumulated by H. portulacoides roots, even when the metal was present in small amounts in the soil marsh (Table 1). The rank order of accumulation of Cd in the different organs in the majority of the cases followed the pattern: L e a f > Root > Stem(P < 0.05; see Table 2) The analysis of the leaf/root concentration ratios indicated that these values were >1 in 75%, =1 in 7.1% and <1 in 17.9% of the cases. In those situations where the ratio was > 1 the variation was between 1.1 and 3.0. TABLE 2 Mean Cd Concentration Values for Sampling Sites and Compartments Compartment

Sampling site 1

2

3

4A

4B

5

6

Mean

Leaf Stem Root Mean

2'6 0.9 2.0 1.8c

2'0 1.5 1.9 1.8c

2"5 1.4 3.0 2.3a

3'4 0.9 3.0 2.4a

2.9 1.6 1-9 2.1b

2'9 1.4 1.7 2.0b

3' 1 1.5 1.7 2.1b

2.8a 1.3c 2.1b

Soil depth (cm) 0-5 5-10 10-15 Mean

0"9 0.6 0.4 0.6e

1.6 1.2 1-0 1.3d

1.9 1.9 1'9 l'9a

1.9 1.9 1.6 1.8ab

1-8 1.8 1.4 1.7b

1-1 0-6 0.5 0-7e

1-7 1.3 1.4 1.5c

1.6a 1.3b 1-2b

Means not followed by a common letter differ at 0.05 significance level.

22

F. Rehoredo

[ h i s observation was consistent with the high mobility of Cd and agreed with previous studies with Azolla (Sela et aL, 1988), in which the mobility of Cd was relatively high in comparison with the low mobility of copper (Cut. Cd levels in roots increased from April to July 1987, then declined. The maximum leaf values were detected in October 1987, decreasing during the winter (Fig. 2). This contrasts with tile results of ,loshi el (//. (1987), who Roots 6 5

Station 1 8

Station 2 Station 3 Station 4A

8

Ap

•

Station 4B

a,

Station 5 Station 6

uary 88

1 =

2

=

4B

•

6

I

2

~

="

1t 0

I

I

April 87

July 87

,

I

'

4A

I

October 87 January 88

Leaves 6 5 A

E

~

~

1

4 ¸

--

8

2

A

3 4A 4B 5 6

1

0

Fig. 2.

!

i

April 87

July 87

i

-

I

October 87 January 88

Variation of the Cd levels in the different organs of H. portulacoides.

Cadmium accumulation by Halimione portulacoides

23

TABLE 3 Mean Cd Concentration Values for Sampling Months and Compartments

Compartment

Sampling month April/87

July/87

0ct./87

Jan./88

Mean

Leaf Stem Root Mean

1.2 0.6 0"9 0"9b

3.8 1.7 3-4 3.0a

3.9 1.8 2.7 2-8a

2.1 1.0 1.5 1.5b

2.8a 1.3c 2-1b

Soil depth (cm) 0-5 5-10 10-15 Mean

1.6 1.4 1.2 1.4a

1.6 !-3 !.1 1.3a

1.5 1.3 1.2 1.3a

1.5 1.4 1-2 1.4a

1.6a 1.3b 1.2b

Means not followed by a common letter differ at 0.05 significance level.

observed an increase in the iron (Fe 3 ÷), manganese (Mn 2 ÷), zinc (Zn 2÷ ) and nickel (Ni 2 ÷) content of the leaves of the succulent halophytes Salicornia brachiata and Suaeda nudiflora during winter. The fluctuation of Cd levels associated with the stems of H.portulacoides did not allow the establishment of a well defined accumulation pattern for that organ (Fig. 2). The analysis of variance clearly indicated that Cd mean values detected in the different organs in July and October 1987 were not significant at the 0.05 significance level (Table 3). The concentration of Mn, Cu and Zn in the shoots of Spartina alterniflora decreased over the growing season, especially from April to July. From July to September a slight increase was detected, while the Cu levels remained approximately constant (Gleason et al., 1979). Groenendijk (1984) detected the maximum above-ground biomass values (living material) of H. portulacoides in July-August. However, the author does not give any evidence indicating whether this peak is associated with the mobilization/utilization of essential elements. Reboredo et al. (1988b) reported that the minimum Cu values in H. portulacoides leaves were detected in July and the maximum values detected in October. Cd showed a similar pattern, therefore the accumulation pattern varies according to the species, the organ of the plant and even with the element considered. Cd levels in H. portulacoides leaves ranged from 1.0 to 4.9/ag g- 1 and in the stems from 0.4 to 2.7/zg g-1, being higher than those measured in the shoots of the same species by Beeftink et al. (1982), which ranged from 0.1 to 0-6, 0.2 to 2.9 and 0.2 to 2.4#gg-~, for individuals collected in the low, middle and high marsh, respectively.

24

F. Reboredo

F r o m the 10 submerged aquatic species studied it was observed that, apart t'rom one higher value (3.64 l~g g- ~ in Vallism'ria americana), Cd levels range l¥om 0.16 Itg g i in Mvriophyllum ,spicatum to 1"29 Izg g I in Potamogetotl peJJbliatus (Di Giulio & Scanlon. 19851. Cd levels from the other seven species ranged within these values. F r o m our results it seems that H. portulacoides has a high capacity for Cd, accumulating it in the leaves, especially if one takes into account the reduced levels found in the soils. Beeftink et al. (19821 indicated that this species is able to accumulate high concentrations of Cd compared with other saltmarsh plants. The interactions between the different t;actors (sampling site, sampling m o n t h and compartments) were highly significant (P < 0.001), indicating a very strong interdependence (Table 4). Concerning the accumulation of Cd in soil-marshes, we considered separately the Cd levels from Stations 1, 2 and 5 (sandy soils) and those from Stations 3, 4A, 4B and 6 (silty-loam soilsl. The variation of Cd in sandy soils (0.2-2.2 ~ugg- t) contrasted with that observed in silty-loam soils (1.1-2.4#gg- ~J. According to Page (1981), Cd concentrations in natural soils range from about 0.05 to 1.0 mg Cd kgexcept in cases where unusual situations occur, such as land applications of municipal sewage sludges. In sandy soils the highest Cd values were generally observed in the top layer (0-5 cmL decreasing considerably with depth (Table 1A-D). This fact is probably related to the superficial enrichment in fine particles deposited by the transport of the freshwater body, although a very weak correlation was observed between the concentration of Cd and the percentage of silt-clay in the top layer of the soil (see Fig. 3B). Characterization of the soil clearly indicated that this layer contained the highest content of carbonate and siltTABLE

4

Statistical lnterations Between Sampling Factors Factors and interactions

Compartment" Sampling site Compartment × sampling site Sampling month Compartment × sampling month Sampling site × sampling month

F test

164"291"** 46"138"** 8'309*** 155"023"** 5"501"** 3"478***

a Compartment = exact place in plant or soil where the sample was taken. *** ( P < 0.001 ~.

25

Cadmium accumulation by Halimione portulacoides TABLE 5

Characterization of Soil Marsh Stations

Station 1 (Tr6ia) Station 2 (ETAR) Station 3 (Batalha) Station 4A (Setenave E)

Depth (cm)

Carbonate content (%)

Organic matter content (O/o~

Silt-clay content (%)

Sand content (%)

pH

0--5 5-10 10-15 0-5 5-10 10-15 0-5 5-10 10-15 0-5 5-10

7.1 5.0 1.2 4.9 4.4 4.6 21.9 15-2 20'4 19.6 18.2 15.2 18-3 18'8 19.5 3.4 2.0

0'5 0.5 0'3 1.6 1.6 1-3 9.5 "7.0 9'4 9-1 8.3 15.9 5-6 4.8 4.2 1.7 1.1

30.4 18.1 7-5 6.0 3.0 3'8 68.6 77-8 70-2 70-8 73'5 68.8 76'0 76-4 76.3 19.3 9.8

62.0 76-4 91.0 87-5 91.0 90.3 ---0.5 -----75.6 87.1 86-1 9.3 6'3 5.7

7.6 7.4 7.4 7. I 7.1 7.2 6.9 6.9 6"5 6.5 6-9 7.0 7-3 7.2 7-2 7.3 7.1

10-15

Station 4B (Setenave W) Station 5 (Mourisca) Station 6 (G~mbia)

0-5 5-10 10-15 0-5 5-10 10-15

2.2

1.0

10.7

0-5 5-10 10-15

17.8 17.2 16.5

4.9 6"0 6.5

68.0 70.5 71.3

7.0

6.1 6.2 6.7

clay (Table 5). In silty-loam soils Cd levels were in some cases practically equal in the different layers. When Cd concentrations decreased with depth, the changes were generally not pronounced (Table 1A-D). Statistical analysis (ANOVA) confirmed that the top layer of the soil had the higher mean values. Those in the second and third layers were not significantly different from each other (P < 0.05) (Table 2). The highest Cd levels in the soil marsh were mainly found in Stations 3, 4A and 4B. The mean values in Stations 4A and 4B were not significantly different from each other (P < 0.05). In spite of the distance between Station 3 and 4A, mean values for these stations were also not significantly different from each other ( P < 0.05) (Table 2). Station 3 is located near Alc~cer do Sal (see Fig. 1), far from the major pollution sources, indicating that the source o f Cd contamination is further upstream, probably related to pyrite mining (Aljustrel mines). Fernandes & Henriques (1989) found elevated metal levels in the leaves o f holm-oak trees (Quercus rotundifolia Lam.) growing at the outskirts o f this mining area.

26

F. Reboredo

These levels were 50 x. 20 x, 10 x and 2 x higher than those observed in the control plants for Cu, Pb-Zn, Fe and Mn, respectively. However, the same authors stress that Cd was usually below the detection limit (0-1 #g g ~1 which means that the Cd uptake by that species does not occur or is insignificant. At what level the agricultural wastes from rice fields contributed to the Cd enrichment of soils from Station 3, is not yet known. Concerning the Cd accumulation in soils surrounding Stations 4A and 4B, it must be stressed that in this area are located important pollution sources such as shipbuilding, metallurgy, pulp, fertilizer and chemical industries, which may contribute to important inputs of Cd to the environment. From the linear regression analysis (Fig. 3) it is seen that neither the organic matter nor the finest fraction of the top layer of the soil ( < 63/~m) constituted important binding sites, since r values, although positive, were not significant at the 0"05 level. Beeftink et al. (1982) also observed that the correlations between clay and metals were highly significant for Ni, Cu and Pb, and weak for Cd. Nevertheless, Di Giulio & Scanlon (1985) verified that the concentrations of Cd in sediments, as well as the concentrations for other metals, were highly correlated to organic matter content, contradicting the above findings. Page (1981) states that the redox potential in soil is a relatively unimportant factor in terms of Cd uptake, since food crops (except rice) do not grow under reducing conditions, as was the case with our tested species. On the contrary, it appears that Cd concentration of the soil and its pH are the two most important factors (Page, 1981). Thus, the bioavailability of Cd is probably not controlled by the organic matter content and soil texture. Additionally, the concentration of Cd rather than the pH of the soil is probably the main factor determining its mobility. In conclusion, H. portulacoides absorbs and translocates to the leaves considerable amounts of Cd without apparent damage. It was observed in situ that green leaves are eaten, probably by insects, and mature yellow leaves fall abundantly to the ground and constitute the main organic debris. Beeftink et al. (1982) states that 'Plants growing on these litter-enriched high marsh areas, especially Artemisia maritima, Atriplex hastata, Elytrigia pungens and Halirnione portulacoides, run therefore the higher risk of translocating metals than those growing on localities where plant debris is removed'. If this assumption is true, the above-mentioned species must be examined for their degree of accumulation of Cd, or even Hg and Pb, although, as we stressed previously (Reboredo & Henriques, 1991), field research must be focused on the search for a ratio or index that allows to detection of the moment at which lethal or sub-lethal effects are expressed.

Cadmium accumulation by Halimione portulacoides y

=

7.731x--7.339,

R-squared:

27

.72

10.

]1

9, 8, 7,

v

6 t~

5

o

4

II

II

3

O

2 1 0

111

•8

.

.

1

..

1:2

1:4

1:6

1:8

Cd (ppm) (a)

80,,

y

= 49.546x

-- 28.708,

R-squared:

70.

.468 X It

60, 50,

401 "~

N

30. 20. 10. ,

0

•8

X

;

1:2

1:4

Cd (ppm)

1:6

1:8

(b) Fig. 3.

Linear regression analysis: Cd level in the soil (0-5 cm) plotted (a) against organic matter (0-5 cm) and (b) against silt-clay (0-5 cm).

Experimental work must be conducted in order to support field research. Studies are now in progress concerning the accumulation of Cd by Halimione spp. cultivated in vitro, in which particular attention is focused on isolation of chlorophylline pigments and on carbon and phosphorus nuclear magnetic resonance spectra.

ACKNOWLEDGEMENTS The author thanks Professor M. Telles Antunes and all the staff of the Geological Section (Universidade Nova de Lisboa) for their unconditional

28

b: Reboredo

support, to Engineer T. Miranda (Servi¢os Geologicos) for useful discussions and support during Cd determination and Professor T. Mexia ( U N L ) and Engineer M. J. Silva llnstituto Investigagfio Culturas Tropicais) for performing the analysis of variance and providing helpful indications about it. This work was done under contract No. 866.86.121 flom Junta Nacional de lnvestigaqfio Cientitica e Tecnol6gica.

REFERENCES Agemian, H. & Chau, A. S. Y. (1976). Evaluation of extraction techniques for the determination of metals in aquatic sediments. Analyst, 101, 761-7. Beeftink, W. G., Nieuwenhuize, J., Stoeppler, M. & Mohl, C. (1982). Heavy metal accumulation in salt marshes from the Western and Eastern Scheldt. Sci. Total Ent~iron., 25, 199-223. Di Giulio, R. T. & Scanlon, P. F. (1985). Heavy metals in aquatic plants, clams and sediments from the Chesapeake bay, USA. Implications for waterfowl. Sci. Total Environ., 41,259-74. Fernandes, J. C. & Henriques, F. S. (1989). Metal contamination in leaves and fruits of holm-oak (Quercus rotundifolio Lam.) trees growing in a pyrites mining area at Aljustrel, Portugal. Water Air Soil Potlut, 48, 409--15. Gleason, M. L., Drifmeyer, J. E. & Zieman, J. C. (1979). Seasonal and environmental variation in Mn, Fe, Cu and Zn content of Spartina alterniflora. Aquat. Bot., 7, 385-92. Greger, M. & Lindberg, S. (1986). Effects of Cd 2+ and EDTA on young sugar beets (Beta vulgaris). I. C d 2+ uptake and sugar accumulation. Physiol. Plant., 66, 69- 74. Groenendijk, A. M. (1984). Primary production of four dominant salt-marsh angiosperms in the SW Netherlands. Vegetatio, 57, 143-52. Jones, G. J., Nichols, P. D., Johns, R. B. & Smith, J. D. (1987). The effect of mercury and cadmium on the fatty acid and sterol composition of the marine diatom Asterionella glacialis. Phytoehemistry, 26, 1343--8. Joshi, A. J., Engenhart, M., Wickern, M. & Breckle, S. W. (1987). Seasonal changes in the trace metals in salt marsh angiosperms, J. Plant Physiol., 128, 173 7. Newell, S. Y., Hicks, R. E. & Nicora, M. (1982). Content of mercury in leaves of Spartina alterniflora Loisel in Georgia, USA. Estuar., Coastal Shelf Sci., 14, 465-9. Nogawa, K., Tsuritani, I., Yamada, Y., Kido, T., Honda, R., Ishizaki, M. & Yamaya, H. (1985). Is, 25(OH)2D in serum of humans with cadmium-induced renal damage. Proceedings o f the Fifth International Conference of Heavy Metals in the Environment, Vol. II. CEP Consultants Ltd., Edinburgh, pp. 64-6. Page, A. L. (1981). Cadmium in soils and its accumulation by food crops. Proceedings oJ" the Third International Conference of Heavy Metals in the Environment. CEP Consultants Ltd., Edinburgh, pp. 206-q3. Rachlin, J. W., Warkentine, B. & Jensen, T. E. (1982). The growth responses of Chlorella saccharophila, Navicula incerta and Nitzschia closterium to selected concentrations of cadmium. Bull. Torrey Bot. Club, 109, 129--35.

Cadmium accumulation by Halimione portulacoides

29

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