instrumental neutron activation analysis in the brown alga, Fucus vesiculosus from Eckwarder H6rne, North Sea and from R~gen, Baltic Sea. Another brown ...
Environmental Geochemistry and Health (1996), 18, 63-68
Use of seaweeds for monitoring trace elements in coastal waters Ranjith Jayasekera 1. and Matthias Rossbach 2 1Department of Botany, University of Kelaniya, Sri Lanka 2Institute of Appfied Physical Chemistry, Research Centre Juefich, D-52425 Juelich, Germany
Concentrations of a wide range of trace elements: arsenic, cadmium, cobalt, chromium, hafnium, nickel, thorium, uranium, zinc and the rare earth elements, cerium, europium, samarium, terbium and ytterbium were determined by instrumental neutron activation analysis in the brown alga, Fucus vesiculosus from Eckwarder H6rne, North Sea and from R~gen, Baltic Sea. Another brown alga, Sargassum filipendula from Sri Lanka, Indian ocean (representing an unpolluted control station) was similarly investigated. Cobalt, chromium and nickel concentrations were highest in F. vesiculosus from the North Sea while zinc was highest in samples from the Baltic Sea, reflecting high levels of these elements in coastal waters of the North and the Baltic sea. Cadmium, cobalt, nickel and zinc levels were lowest in S. filipendula from Sri Lanka, probably demonstrating lower levels of those elements in coastal waters. Concentration levels of hafnium, thorium, uranium, and the rare earth elements were highest in S. filipendula. Two years later in 1994, S. filipendula along with Ulva sp. (green alga) was resampled from the same sampling site, and in addition to the above elements, six other trace elements (Ag, Ba, Br, Rb, Se and Sr) were determined. Sargassium filipendula showed a particular affinity for Ag, As, Br and Sr. For the other elements, marginal concentration differences were observed between S. filipendula and Ulva sp., probably reflecting the regional background levels. Substantially higher concentrations of Hf, Th, U, and the rare earths were found again in the 1994 Sargassum and Ulva samples, reflecting the effect of a substrate rich in rare earth elements. The brown algae used in this study may be used to monitor trace elements in coastal waters.
Keywords: Baltic Sea, brown algae, coastal water monitoring, trace elements, North Sea, seaweeds, Sri Lanka, Ulva
Introduction
During the last decade or so, interest in various aspects of the significance of trace elements in the environment has rapidly increased as human activities have altered the global cycles of trace elements (Adriano, 1986). There is, however, only fimited knowledge at present on the environmental impact of a majority of trace elements which are used at an increasing rate in modern technology and agriculture worldwide. It has therefore, become essential to obtain more detailed information on their natural baseline concentration levels as well as their environmental impact when present in excess. The use of seaweeds as continuous sampling monitors for pollutants to characterise coastal water quality has increased in recent years. Seaweeds have been used as bioaccumulators as trace metal concentrations in their tissues are magnified many times with respect to their concentrations in sea water (Fuge and James, 1973; Seeliger and Edwards, 1977). To this end, macrophytic brown algae have been widely employed for monitoring trace metal pollution in marine waters (Nickless et *To whom correspondence should be addressed. 0269-4042 9 1996 Chapman & Hall
al., 1972; Shubert, 1984; Stoeppler et al., 1986). Published information indicates that brown algae are unable to regulate their uptake of trace metals, so accumulation is mostly passive, resulting in extremely high tissue concentrations relative t o the surrounding sea water (Moris and Bale, 1975; Markham et al., 1980). For seaweeds to be used as biomonitors, two major criteria have to be fulfilled. Firstly, they must be sessile in order to be representative of the area where collected so that they reflect environmental conditions at one site over a long time. Secondly, the relationship between concentrations of metals in seaweeds and in seawater must be linear, resulting in a constant concentration factor for a particular element over a wide range of external concentrations (Levine, 1984). Green algae have received the least attention in marine pollution applications, because their greatest abundance is in fresh water environments (Levine, 1984).
Within the scope of the environmental monitoring programme of the German Environmental Specimen Bank at Jfilich, the marine brown alga, Fucus vesiculosus (division Phaeophyta) has been sampled at regular intervals from defined sampling areas along the German North Sea coast during the
64 past few years. The samples are taken according to the standard operating procedures (SOPs) and are stored at liquid nitrogen temperature for retrospective analysis. Large amounts of samples (5-10 kg per sampling) are taken, placed in stainless steel containers over the gaseous phase of liquid nitrogen and transported to the laboratory. A specially designed Cryo-mill (Cryo-Palla, Teflon, stainless steel or titanium rods and drum) is used to homogenise the material at -140 ~ A large number of 10 g samples of identical and homogeneous material is available for all kinds of analytical investigations. Our observations and the general lack of data on concentrations of trace elements in very remote and industrially unaffected tropical coastal environments prompted us to conduct a comparable survey on selected trace elements in two types of sea weeds growing on the western coast of Sri Lanka. To this end, another brown alga, Sargassum filipendula (division Phaeophyta) which inhabits tropical marine environments was sampled from the western coast of Sri Lanka for compar• Therefore, the main objective of this study was to assess the relative abundance and variations in seaweed concentrations of selected trace elements in the brown algae, F. vesiculosus and S. filipendula derived from different locations. The sessile green alga, Ulva sp. from the same sampling site in Sri Lanka was also analysed for comparison with S. filipendula. Methodology
This study was conducted as an extension of extensive regional work carried out by the German Environmental Specimen Bank in the coastal area of the North and Baltic Sea. To avoid changes induced by the age and plant part, whole mature plants of S. filipendula were sampled in February 1992 at a location distant from river inputs and major cities on the western coast of Sri Lanka which served as an unpolluted control station for this study. The alga grows at or near low water mark in the rocky intertidal area where it is subjected to tidal influences. Two years later, in February 1994, S.filipendula, along with the green alga Ulva sp,, was resampled from the same sampling site in Sri Lanka for comparison with earlier analyses in 1992. The samples were washed with seawater and then any of the epiphytes and epifauna attached were removed. They were then dried in a vacuum oven for 48 h at 60~ homogenised in an agate mill under contamination-free conditions. Homogenised material of F. vesiculosus originated from Eckwarder H6rne, North Sea and from Riigen, Baltic Sea, and stored in the German Environmental Specimen Bank and was analysed for comparison; these samples have been collected at 2-month intervals (six samplings per year), and thoroughly mixed to yield a composite sample (1992, homogenate) representing a particular year.
Jayasekera and Rossbach Table 1. Analytical values of constituent elements obtained by INAA for the NIES No. 9 Sargasso certified reference material. (values are in gg g-1 dry weight, unless otherwise indicated, figures in parentheses are reference values only) (NIES, 1988)
Element Ag As Au
Certified value
Found
0.31 4- 0.02 115 i 9 -
0.31 115 0.003 10 269
Ba
-
Br
(270)
Cd Ce Co Cr Cs
0.15 4- 0.02 0.12 4- 0.01 (0.2) (0.04)
0.197 0.11 0.223 0.041
Eu Fe Hf I Mo
187 4, 6 (520) -
Na% Ni Rb Sb Sc
1.70 + 0.08 24 + 2 (0.04) (0.09)
1.12 24 O.O4 0.088
Se
Sm Sr Tb Te
(0.05) 1000 4, 30 -
0.048 0.064 960 0.004 0.265
Th U Yb Zn Zr
(0.4) 15.6 4. 1.2 -
0.004 0.428 0.012 15.6 3.4
-
0.006 187 0.155 500 0.344
Multi-element analysis was performed by nondestructive instrumental neutron activation analysis (INAA) following established quality assuranceprocedures (Table 1). A Compton suppression spectrometer consisting of a 25% HPGe (1.8 keV resolution at 1.3 MeV) and a Bicron NaI(TI) well detector and plug was used to detect gamma radiation from neutron-irradiated samples (1.8 x 1018 N cm-2), and an Ortec multichannel analyzer (919a) with Ortec software (Omnigam) was used to evaluate the spectra (Rossbach et al., 1990). Results and Discussion
The concentration levels of selected trace elements in F. vesiculosus and S. filipendula derived from different locations are presented in Figure 1. First and foremost, it must be emphasised that these two species are not directly comparable although they belong to the same division (Phaeophyta). C o m -
Seaweeds for monitoring trace elements
65
Concentration (~g/g) 200
20
0.2
0.02
As
Cd
Co Cr Hf Ni Th [r-qNorth Sea iBaltic Sea I~Sri Lanka I
U
Zn
Figure 1 Concentration levels of selected trace elements (gg g-1 dry weight) in Fucus vesiculosus from the North Sea and the Baltic Sea, and in Sargassum filipendula sampled in 1992from Sri Lanka. paring trace element results from different locations (Europe versus Sri Lanka) may be difficult, particularly since the environmental parameters of the two locations are quite different; parameters
100
10
such as temperature, salinity or turbidity could affect metabolic rates of the algae, thus influencing the seaweed growth rate. Further, the temperate brown alga, F. vesiculosus shows a clear seasonal
Concentration (pg/g)
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i
12111111111111111111211111111111111111111111111111111 2111122211111L22111
................. 9........
0.1
0.01 Ce
Eu
Sm
Tb
Yb
Ir-]North Sea mBaltic Sea l~Sri Lanka I Figure 2 Comparison of the rare earth element concentrations (gg g-] dry weight) in Fucus vesiculosus from the North Sea and the Baltic Sea, and in Sargassum filipendula sampled in 1992from Sri Lanka.
66
Jayasekera and Rossbach
activity in growth linked with the metabolic activity and climatic factors. Keeping all these facts in mind, the main objective of this study was to obtain the trace element data on comparable seaweeds from a remote, uncontaminated location in the Southern hemisphere, in contrast to temperate F. vesiculosus. As Fucus is not available in tropical coastal environments, the easily available Sargassum was used in this study.
cannot be answered at present as no sea water values are available. Because of the great difficulties involved in determining the amount of 'available' elements in sea water, it was not possible to analyse the surrounding sea water. With respect to Ni levels, variations observed between locations seem marginal. The zinc content in F. vesiculosus was found to be higher by a factor of 15-19 than in S. filipendula.
Cobalt, chromium and nickel concentrations were highest in Fucus samples from the North Sea which is probably due to the high input of these elements to the sea by industrial and domestic waste disposal from both the British Isles and European continent (Weichart, 1973). In contrast, highest zinc and arsenic values were found in Fucus samples from Rtigen, Baltic Sea which has been exposed to severe environmental pollution during the last two decades or so. Sargassurn samples from Sri Lanka, on the other hand, possessed the lowest concentrations of cadmium, cobalt, nickel and zinc, probably reflecting the regional background (minimum) levels as the plants originated from an unpolluted control station. However, Cr content in 1992-Sargassum samples (Figure 1) is about five times higher than in the Baltic Sea Fucus samples. Even higher Cr concentrations were observed in 1994Sargassum samples (Figure 3). In a previous study (Jayasekera, 1994), the Cr content in S. filipendula was found to be higher (2.35 mg kg -1) by a factor of 11-12 than in NIES (National Institute of Environmental Studies in Japan) No. 9 Sargasso reference material (1988) (0.2 mg kg-1). Whether the elevated Cr levels in S. filipendula are due to its preferential bioaccumulation properties or to the high levels present in the sea water or substrate
Interestingly, the highest concentration levels of hafnium, thorium and uranium were found in Sargassum samples from Sri Lanka, reflecting the effect of the substrate rich in those elements; the results obtained on 1994 Sargassum samples also show high values for those elements (Figure 3). The concentration order of the nine elements in F. vesiculosus seems to remain more or less constant irrespective of the place of origin ( Z n > A s > Ni > Cr > Co > H f > U > Th for samples from the North Sea; Z n > A s > N i > C o > C d > C r > H f > U > Th for samples from the Baltic Sea). However, a totally different pattern As > H f > Ni > Zn > Th > Cr > U > Co > Cd can be observed in S. fiIipendula. Arsenic values showed little variation with respect to the sampling site (Figure 1) which is in good agreement with the previous studies (Stoeppler et al., 1986); 1994-Sargassum samples show a similar concentration level for arsenic (Figure 3). Figure 2 compares the seaweed concentration levels of five rare earth elements in F. vesiculosus from two different European locations and S. filipendula from Sri Lanka. The concentration levels of all five elements, Ce, Eu, Sm, Tb, and Yb were substantially higher in Sargassum samples
Concentration (pg/g)
1000
100 10
0.1 0.01 Ag As Ba
Br Ce Co Cr
Eu
Hf
Ni
Rb Se Sm Sr
Tb Th Yb Zn
[E3Sargassum m Ulva I Figure 3 Trace element concentrations (gg g-1 dry weight) in Sargassum filipendula and Ulva sp. sampled in 1994from Sri Lanka.
Seaweeds for monitoring trace elements
from Sri Lanka than in F. vesiculosus, probably due to the lanthanide-rich substrate on which they grew (Gschneidner and Eyring, 1990). However, the order of accumulation of these elements, Ce > Sm > Yb > Eu > Tb, in algae remained unchanged irrespective of the sampling site (Figure 2). Higher concentration levels of the rare earth elements were observed not only in the 1994 Sargassum samples but also in the green alga, Ulva (Figure 3) which can only be attributed to the influence of a monazite-like substrate rich in rare earth elements (Gschneidner and Eyring, 1990). Figure 3 compares the concentration levels of 18 trace elements in the green alga, Ulva and S. filipendula sampled from Sri Lanka in 1994. Published literature indicates that the brown algae preferentially bioaccumulate certain elements like arsenic, bromine and strontium which is further supported by the results shown in Figure 3. In addition, silver concentration in S. filipendula is substantially higher (about seven-fold) than in Ulva, indicating its bioaccumulation properties for silver. As a whole, somewhat similar concentration levels and distribution patterns can be observed both in 1992 and 1994-Sargassum samples. For a majority of elements, there were only marginal concentration differences between Sargassum and Utva, probably reflecting the regional background levels at an anthropogenically undisturbed location. In conclusion, concentration levels of a wide range of trace elements in seaweeds originated from two different locations, i.e. Europe versus Sri Lanka, have been established. From the present study and from previous studies (Stoeppler et aI., 1986; Jayasekera, 1994) it is apparent that trace element concentrations in brown seaweeds vary with environmental concentrations. The species used in this study may be suitable for deducing comparative environmental data on the differences in the dissolved trace element content of coastal marine waters. However, tissue concentrations are subject to several sources of variation compounded with errors associated with sampling techniques, sample preparation and analysis, and therefore the interpretation of such data needs careful consideration. Elevated concentration levels of Hf, Th, U, and the rare earth elements in Sargassum and Ulva samples from Sri Lanka could be attributed to the effect of substrate rich in rare earth elements. Compared with the green alga, Ulva, the brown alga, S. filipendula seems to accumulate Ag, As, Br and Sr preferentially. For the other trace elements (Figure 3), concentration differences between Sargassum and Ulva seem marginal, probably indicating low background levels of those elements in the environment. Further work is needed to confirm the results of this study. It is hoped that the results presented in this paper will provide useful reference
67
data for other researchers involved in environmental monitoring activities.
Acknowledgements M.R. gratefully acknowledges the finacial support of the 'Bundesminister ftir Umwelt, Reaktorsicherheit und Naturschutz', Bonn and the 'Bundesumweltamt', Berlin. R.J. would like to thank the European Union for providing travel costs enabling this paper to be presented at the Geotrop94 International Conference in Jamaica. We thank Mr Hany Amer for assistance in the analysis of the 1994 samples. Thanks are also due to two anonymous reviewers for their valuable comments on the manuscript.
References Adriano, D.C. 1986. Trace Elements in the Terrestrial Environment. Springer Verlag, New York, Heidelberg. Fuge, R. and James, K.H. 1973. Trace metal concentrations in brown seaweeds, Cardigan Bay, Wales. Marine Chemistry, 1, 281-293. Gschneidner Jr, K.A. and Eyring, L. (eds). 1990. Handbook on the Physics and Chemistry of Rare Earths, Volume 13. North-Holland, Amsterdam, New York. Jayasekera, R. 1994. Pattern of distribution of selected trace elements in the marine brown alga, Sargassum filipendula Ag. from Sri Lanka. Environmental Geochemistry and Health, 16, 70-75. Levine, H.G. 1984. The use of seaweeds for monitoring coastal waters. In: L.E. Shubert (ed.), Algae as Ecological Indicators, pp 188-210. Academic Press, London, New York. Markham, J.W., Kremer, B.P. and Sperling, K.R. 1980. Effects of cadmium on Laminaria saccharina in culture. Marine Ecology Progress Series, 3, 31-39. Moris, A.W. and Bale, A.J. 1975. The accumulation of cadmium, copper, manganese and zinc by Fucus vesiculosus in the Bristol Channel. Estuarine and Coastal Marine Science, 3, 153-163. Nickless, G., Stenner, R. and Terrille, N. 1972. Distribution of cadmium, lead and zinc in the Bristol Channel. Marine Pollution Bulletin, 3, 188-I90. NIES, 1988. No. 9 Sargasso. Certificate of analysis, National Institute of Environmental Studies, Japan. Rossbach, M., Zeisler, R. and Woittiez, J.R.W. 1990. The use of Compton suppression spectrometers for trace element studies in biological materials. In: R. Zeisler and V.P. Guinn (eds), Nuclear Analytical Methods in the Life Sciences, pp. 63-73. The Humana Press, Clifton, NJ. Seeliger, U. and Edwards, P. 1977. Correlation coefficients and concentration factors of copper and lead in seawater and benthic algae. Marine Pollution Bulletin, 8, 16-19. Shubert, L.L. (ed.) 1984. Algae as Ecological Indicators. Academic Press, London, New York. Stoeppler, M., Burow, M., Backhaus, F., Schramm, W. and Nfirnberg, H.W. 1986. Arsenic in seawater and brown algae of the Baltic and North Sea. Marine Chemistry, 18, 321- 334.
68 Weichart, G. 1973. Pollution of the North Sea. Ambio, 2, 99-106.
Jayasekera and Rossbach [Manuscript No. 383: received December 5, 1994 and accepted after revision, August 16, 1995.]
