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Heavy metal contamination in the seaweeds of the Venice lagoon
Chemosphere 47 (2002) 443–454 www.elsevier.com/locate/chemosphere
Heavy metal contamination in the seaweeds of the Venice lagoon M. Caliceti, E. Argese, A. Sfriso, B. Pavoni
*
Dipartimento Scienze Ambientali, Facolt a di Scienze MM. FF. NN., Centro di Studio sulla Chimica e Tecnologia per l’Ambiente, Universit a Ca’ Foscari di Venezia, Calle Large Santa Marta 2137, 30123 Venezia, Italy Received 20 December 2000; received in revised form 23 October 2001; accepted 26 October 2001
Abstract The concentrations of heavy metals (Fe, Zn, Cu, Cd, Ni, Pb, Cr, As) were determined in seven seaweeds of environmental and commercial relevance (Ulva rigida C. Ag., Gracilaria gracilis (Stackhouse) Steentoft, L. Irvine and Farnham, Porphyra leucosticta Thuret, Grateloupia doryphora (Montagne) Howe., Undaria pinnatifida (Harv.) Suringar, Fucus virsoides J. Agardh, Cystoseira barbata (Good. et Wood.) Ag.) collected in four sampling sites in the lagoon of Venice, in spring and autumn 1999. Metals were extracted using hot concentrated acids in a Microwave Digestion Rotor and analysed by absorption spectrophotometry using a flame mode for Fe and Zn and a graphite furnace for Pb, Cr, Cd, Cu, Ni and As. High contamination levels, especially for Pb, were detected in Ulva and to a lesser extent in Gracilaria. Brown seaweeds, especially Cystoseira was highly contaminated by As. The least contaminated genera with all metals except As were Porphyra and Undaria. A concentration decrease for Zn and Cd was observed from the inner parts of the central lagoon, close to the industrial district, towards the lagoon openings to the sea. Ó 2002 Elsevier Science Ltd. All rights reserved. Keywords: Seaweeds; Heavy metals; Biomonitors; Venice lagoon
1. Introduction The use of seaweeds as animal and human food, soil manure, salt extractions (soda, iodine, etc.), colloid production (agar, alginates, carrageenan, furcellaran, etc.), cosmetics, pharmaceuticals, energy production is a very old and widespread practice (Chapman and Chapman, 1980; Bird and Benson, 1987; Bressan and De Luca, 1987; COST 48, 1989 and references therein, Bradford and Bradford, 1996). Seaweeds represent an important economical resource mostly in the Indian and Pacific countries where they are not only largely harvested but also intensively and largely employed in the human nutrition.
*
Corresponding author. Tel.: +39-041-257-85-22; fax: +39041-257-85-82. E-mail address: [email protected] (B. Pavoni).
In Europe the collection and utilization of seaweeds have a lower diffusion than in the Indian and Pacific areas. Except for the extraction of iodine and soda from fucoids, which has been practiced since the 17th century, and the use of fresh seaweeds as fodder for sheep, cattle and horses, which browse on the shore in some northern countries (Scotland, Norway, Iceland, etc.), the attention to seaweeds has been drawn mostly after the Second World War. The excessive growth of some species (especially Ulva, Enteromorpha, Chaetomorpha, Cladophora, Gracilaria, etc.), which colonized many lagoons and shallow coastal areas, created serious problems for the environment quality, the local populations and economies (Casabianca-Chassany, 1984, 1989; Sfriso et al., 1987, 1992; Schramm, 1991; Schramm and Nienhuis, 1996 and references therein; Briand, 1991; CEVA, 1993; Menesguen and Piriou, 1995; Morand and Briand, 1996; Sfriso and Marcomini, 1996; Viaroli et al., 1992,
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1994; etc.). In these areas seaweeds are mainly harvested to prevent or mitigate the effects of an abnormal biomass proliferation and possible anoxic events. However, in European countries the collected biomass is more a problem than a profit. As a consequence, many seaweed studies and projects have been addressed to the biomass conversion and digestion (COST 48, 1987 and references therein; Croatto, 1982; Morand et al., 1990, 1991; Cuomo et al., 1993, 1995; Orlandini, 1994; Morand and Briand, 1996). Another actual European application of seaweeds deals with the environmental monitoring and restoration. Some seaweeds are used or indicated as appropriate biomonitors to study the environment contamination (Munda, 1982; COST 48, 1987; Munda and Hundnik, 1991 and references therein; Marcomini et al., 1993; Haritonidis and Malea, 1995, 1999; Sfriso et al., 1995; Malea and Haritonidis, 1999a,b, 2000). Seaweed crop is also used for nutrient and contaminant abatement (Croatto, 1982; COST 48, 1987 and references therein; Morand and Briand, 1996). The lagoon of Venice, is the widest shallow area populated by macrophytes, in Italy. Starting from the 60s, the lagoon has been affected by an abnormal production of nitrophilic species, especially Ulva rigida C. Ag., which caused a change in the benthic-flora structure (Sfriso, 1987), the alteration of the nutrient cycles and the occurrence of dystrophic crises (Sfriso et al., 1992). In the 1970’s and 1980’s, in the central basin, about a third of the entire lagoon, a gross seaweed production of ten million tonnes was estimated (Sfriso and Marcomini, 1994). Since the late 1980’s, to prevent the effects of this abnormal biomass proliferation and decomposition, the local administration provided for the seaweed biomass to be harvested (up to 55.000 m3 yr1 ). Many projects explored the use of seaweed crops in agriculture, in the production of compost and biogas without obtaining economically satisfactory results (Croatto, 1982; Cuomo et al., 1993, 1995). Finally, a method for converting the biomass in paper pulp, after a suitable pre-treatment, to produce the ‘‘Ulva carta’’ has been developed from a local paper company, thus solving the problem of the macrophyte crops in an economically convenient way. Since 1990 a new trend emerged: a strong reduction of Ulva distribution and production was coupled with a re-population of native seagrass and seaweed species. At the same time new seaweeds of eastern origin entered the lagoon of Venice through fishing and commercial traffic. Among these the hard-bottom species: Sargassum muticum (Yendo) Fensholt, Undaria pinnatifida (Harvey) Suringar and Grateloupia doryphora (Montagne) Howe spread over the whole lagoon, while Cystoseira barbata (Good. et Woodw.), a species very common before the Ulva proliferation, re-colonized some areas. At present, the Venice lagoon is populated by over 250 seaweed taxa differently spread and distributed in
the inner and outer littorals. Many of these have a possible economic relevance or can be used as biomonitors for waters (Levine, 1984; Phillips, 1995; Moy and Walday, 1996 and references therein; Haritonidis and Malea, 1995, 1999; Malea and Haritonidis, 1999a,b, 2000), especially for dissolved heavy metal contamination (R€ onnberg et al., 1990; Ganesan et al., 1991; Kureishy, 1991; Rajendran et al., 1993; Rainbow and Phillips, 1993; Tariq et al., 1993; Karez et al., 1994; €ksezgin and Balci, 1994; Rainbow, 1995; Riget K€ ußcu et al., 1995; Leal et al., 1997). The objective of this paper is to investigate on the contamination level and the capacity of some highly widespread seaweeds growing in the Venice lagoon (viz. Ulva rigida C. Ag., Gracolaria gracilis, Grateloupia doryphora (Montagne) Howe, Porphyra leucosticta Thuret, Fucus virsoides J. Ag., Undaria pinnatifida (Harvey) Suringar, Cystoseira barbata (Good, et Woodw.) Ag.) to selectively accumulate inorganic contaminants: Fe, Zn, Cu, Cd, Ni, Pb, Cr, As. These species were selected for their abundance, biomonitoring capacity and actual (paper pulp making, gas production, soil amendment) and potential uses (as nutrient and contaminant traps, for the extraction of phycocolloids, agar and alginate, and use in cosmetics, pharmacology and animal or human nutrition (Bressan and De Luca, 1987; Penso, 1987; Keiji and Kanji, 1989).
2. Materials and methods 2.1. Study area The lagoon of Venice is a shallow water body with a mean depth of 1 m and a total surface of 549 km2 (Fig. 1). It is subdivided into three main sections, named the southern, the northern and the central basins. The city of Venice is located in the central basin. The mean tidal excursion is 62 cm and the water change is guaranteed by three inlets, which enable the renewal of 60% of the lagoon water every 12 h. The industrial district of Porto Marghera has severely affected the lagoon environmental conditions: in the past the main impact derived from the production of phosphorus–nitrogen fertilizers and non-ferrous metals, such as Al and Zn, at present the petrochemical activity is probably prevailing. The inland urban settlements, especially the towns of Marghera and Mestre and the island of Lido, which have been connected to sewage treatment plants only recently, as well as Venice historical centre, and the islands of Murano, Burano and Pellestrina, which have a marked tourist-vocation and lack of an advanced sewage system, have also contributed to the lagoon contamination (Lee et al., 1990).
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2.2. Sampling sites Seaweeds were collected in the hard substrates of four stations (Fig. 1) placed in a transect from the mainland towards the Lido lagoon inlet: Ponte della Liberta (St. 1), Tronchetto (St. 2), Celestia (St. 3), Lido inlet (St. 4), in two sampling sessions: In spring 1999 during their highest biomass production and in autumn of the same year when the perennial species showed a secondary biomass peak. Some seasonal species such as Porphyra leucosticta and Undaria pinnatifida, were found only in spring. Other species such as Undaria pinnatifida, Cystoseira barbata, Fucus virsoides and Gracilaria gracilis were not found in all the sampling sites which are located in different areas of the lagoon with peculiar hydrodynamics and human impacts (Fig. 1). St. 1: Ponte della Liberta. This station is located at north-west of Venice close to the mainland. It is influenced both by the urban effluents of Mestre and its hinterland and by the industrial area of Porto Marghera. Therefore, this area was assumed to be the most contaminated. Moreover the site is close to the heavy traffic translagoonar bridge connecting Venice to the city of Mestre. Water renewal is rather low and micropollutant contamination in sediments is high (Sfriso, 2000). In this station only Ulva and Gracilaria were found. St. 2: Tronchetto. This station is placed in the western district of Venice historical centre, 3 km far from station 1. It is placed close to the parking area of Tronchetto and characterized by an intense maritime traffic. Water exchange is guaranteed by the adjacent
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Vittorio Emanuele canal leading to the Lido inlet. In this area Cystoseira was missing. St. 3: Celestia. It is located at north–east of Venice close to a highly populated area, where household activities and maritime traffic are the main pollution sources. In this area the ebb tide conveys all the nontreated sewage of the historical centre. Furthermore the island of Murano, with its numerous glass factories, is very close to this sampling site. In this station were found all the studied species. St. 4: Lido inlet. This station is located 10 km far from St. 1 near the lagoon inlet of Lido, through which waters from the Adriatic Sea flood the northern and the central basins. Among the four stations this one is the farthest away from contamination sources. For these reasons it was assumed to be the least contaminated. In this area Cystoseira was not found. 2.3. Seaweed selection Among 250 macroalgal taxa living in the Venice lagoon, seven species have been selected because of their abundance, actual use and potential relevance. (1) Ulva rigida C. Ag., is the most abundant species in the Venice lagoon even though its standing crop and production have significantly decreased during the 1990’s (Sfriso and Marcomini, 1996; Sfriso, 2000). In the past this species was harvested to prevent anoxic crises and used for paper manufacturing. This widespread seaweed is reported as a valid indicator species, especially of Pb (Malea and Haritonidis, 2000).
Fig. 1. Distribution of sampling sites in the central basin of the lagoon of Venice.
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(2) Gracilaria gracilis (Stackhouse) Steentoft, L. Irvine and Farnham in terms of biomass production until the end of the 1980’s was the second macroalgal species growing in the Venice lagoon. This species was harvested for agar extraction since the 1940s (12 t, dry wt., per year). The highest biomass was collected in 1985 (1700 t, dry wt. per year), then the biomass began to decrease and in the 1990’s its harvesting was considered no more profitable. (Orlandini and Favretto, 1987; Sfriso et al., 1994). Gracilaria gracilis is suggested as a good bioindicator especially for Cd (Malea and Haritonidis, 1999b). (3) Porphyra leucosticta Thuret, shows an important biomass in spring, although this species has never been harvested in the Venice lagoon. Because of its high production and use as human nourishment, ‘‘Nori’’ in the eastern countries (Chapman and Chapman, 1980; COST 48, 1989; Bradford and Bradford, 1996) and its natural availability and abundance, Porphyra can be an interesting species in the view of a possible future utilization. (4) Fucus virsoides J. Ag., is an endemic species very interesting for algin production and its cosmetic implications. In the past a national company investigated its availability for salt-bath production. However this species, very sensitive to eutrophication and anoxic crises, was not available with an adequate biomass. At present, as the nitrophilic species, like Ulva rigida, are markedly reduced and no anoxia events occur, this species has spread over the hard substrates close to the lagoon inlets, where waters are less eutrophicated and well renewed. (5) Cystoseira barbata (Good. et Woodw.), a seaweed very abundant in the hard substrates of the Venice lagoon might become a source of raw material for alginate production. (6) Grateloupia doryphora (Montagne) Howe, is a new species for the Venice lagoon. This seaweed is cultivated in Japan and China for the production of Funoran a seaweed glue called ‘‘Funori’’ which is used as an adhesive and for sizing paper, fibre or cloth. This species lives on the hard substrates, especially in the winter and the spring seasons. (7) Undaria pinnatifida (Harvey) Suringar, is also an invasive seaweed species which has populated the hard Venice lagoon substrates only recently, during the 1990’s. This species has a big size and a fast growth. In late spring Undaria reaches biomasses of many kg m2 (5–10 kg m2 , wet wt.). Undaria is a species very cultivated and harvested in the eastern seas where is used mainly as human food (in soups, with rice, sauces etc.) and it is known as ‘‘Wakame’’ (Chapman and Chapman, 1980; Bradford and Bradford, 1996). 2.4. Seaweed collection and preparation Many entire thalli of each seaweed species were hand-picked or collected with a hand net taking into
account the different age and depth in order to obtain homogeneous samples representative of the entire algal population living in the study area. All the collected samples were attached to the substrate in order to avoid to collect samples moving from different areas. The obtained seaweed samples (0.5–1 kg for the small size species and 2–3 kg for Undaria and Cystoseira) were carefully washed with sea-water in order to remove the trapped sediment, epiphytic organisms and the hidden fauna. Stored at 20 °C in PET-LD bags, after freezedrying, seaweed samples were crashed and homogenized in a porcelain mortar. The residual water content of the obtained seaweed samples processed for the metal determination was determined by dessication at 80 °C for a night, in order to correct the final values. 2.5. Materials The used reagents were: Hydrogen peroxide ‘‘ARISTAR’’ 30% w/v (BDH), Nitric acid ‘‘ARISTAR’’ acidimetric titer 68.5–69.5% (BDH). The reference material CRM 062 (Olive leaves) was donated by the EU Joint Research Centre of Ispra (Varese, Italy). 2.6. Extraction Metals were extracted using a Microwave Digestion Rotor, MDR, Ethos 1600 Milestone (wave length: 12.25 cm, frequency 2450 MHz). The following procedure was experimented as the most suitable for handling seaweed samples to obtain extracts free from undissolved residues. Freeze-dried samples (300 mg) were digested with 3 mL milli-Q water, 5 mL nitric acid and 1 mL hydrogen peroxide. The heating program was: 2 min at 250 W, 2 min at 0 W, 5 min at 250 W, 5 min at 400 W. Two replicates of each sample were analysed. Blank assays were carried out. The extracts were stored at þ4 °C in PET-HD flasks previously cleaned with nitric acid. 2.7. Instrumental analysis Metals were determined by means of a SpectrAA-250 Plus VARIAN spectrometer (flame mode for Fe and Zn, graphite furnace of Pb, Cr, Cd, Cu, Ni and As), using the standard addition procedure. The precision of the methodology expressed as standard deviation percentage was less than 15% for all metals except for Ni (23%) and Cr (26%). The methodology was tested using a reference sample, certified for Cd, Cu, Pb and Zn. Metal concentrations were determined in triplicate; the results are reported in Table 1. The results of Zn resulted significantly different from the certified ones. For this metal a probable contamination of the standard sample has occurred before the
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Table 1 Results of the reference material analyses (Olea europea) Dry wt. (lg g1 )
Sub-sample I
Sub-sample II
Sub-sample III
Mean
CRM 062
Cd Cu Pb Zn
0.10 52 28 24
0.09 46 23 37
0.11 55 23 31
0.10 0.01 51 4 25 3 31 8
0:10 0:02 46:6 1:8 25:0 1:5 16:0 0:7
analysis. This problem was not considered critical as the analytical procedure tested on certified sediments gave variations with respect to the certified results of the same order as for the other metals. Except Fe (17 mg L1 ) and Zn (12 lg L1 ), the blank values of the considered metals were 6 the detection limits: i.e. 0.7 lg L1 (Cu), 1.0 lg L1 (Pb), 0.1 lg L1 (Cd), 1.0 lg L1 (Ni), 1.2 lg L1 (As) and 1.0 lg L1 (Cr).
The concentration values of the metals are summarized in Table 3. They are the mean of the values obtained in the four sampling sites during the sampling period calculated in order to obtain synthetic information per species. The standard deviations presented in Table 3 are therefore a time and space variability index of the detected concentrations. 3.1. Bio-essential elements
3. Results and discussion In Table 2 the collected seaweed genera are listed as per sampling station and per session. The seaweeds sampled at Ponte della Liberta were only Ulva and Gracilaria, which are known to be the most pollutiontolerant species among the collected ones. Porphyra, Undaria, are seasonal genera, which were collected in spring only. The contamination level of these genera will be discussed as an indication of spatial variability. Fucus, the species more sensible to eutrophication, was found in the Lido inlet station only.
Table 2 Period, site and genera sampled Spring 1999
Autumn 1999
Ponte della Libert a
Ulva Gracilaria
Ulva Gracilaria
Tronchetto
Ulva Gracilaria Grateloupia Porphyra Undaria
Ulva Gracilaria Grateloupia
Celestia
Ulva Gracilaria Grateloupia Porphyra Undaria Cystoseira
Ulva Gracilaria Grateloupia Cystoseira
Lido inlet
Ulva Porphyra Fucus Cystoseira
Ulva Gracilaria Fucus Cystoseira
The relative abundance of the bio-essential elements was always the following Fe > Zn > Cu. An analogous sequence is reported in other paper concerning metal distribution in seaweeds (Ganesan et al., 1991; Rajendran et al., 1993; Malea and Haritonidis, 1999b, 2000). Iron: As for Fe the highest mean concentrations were detected in Ulva (1033 564 lg g1 dry wt.). The overall variability ranged from 134 to 1630 lg g1 dry wt. The mean value is approximately three times higher than the values found in the same species collected in the Thermaikos Gulf, Greece (Malea and Haritonidis, 2000) which is considered a polluted area. The range is analogous to that reported for some seaweeds living in sites of the Bay of Bengal which are also considered to be polluted (Ganesan et al., 1991, and references therein). Assuming that the metal uptake in temperate region is generally low because shorter day-length and lower light intensity affect photosynthesis rate, the values detected for Fe in the seaweeds of the Venice lagoon are relatively high. Zinc: Zinc ranged from 15 to 300 lg g1 dry wt.; the genera with the highest values were Grateloupia and Gracilaria (Fig. 2). Gracilaria showed a Zn mean value (163 64 lg g1 dry wt.) approximately twice higher than in the same species collected in the Thermaikos Gulf, Greece (Malea and Haritonidis, 1999b). Moore and Ramamoorthy (1984) reported that in the absence of metal mines/smelters, i.e. main Zn-contamination sources, levels in seawater plants are generally <100 lg g1 dry wt.; however, examples of heavy Zncontaminated sites are characterized by values as high as 104 lg g1 dry wt. The Zn values reported by other authors (Riget et al., 1995) for Fucus vesiculosus in unpolluted areas are one order of magnitude lower than those obtained in the Venice lagoon (110 61 lg g1 dry wt.). It should be noticed that the samples of Fucus virsoides were picked
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Table 3 Maximum, minimum and mean values obtained as average of the two sampling periods and four sampling sites for each genus Dry wt. (lg g1 )
Fe
Zn
Cu
Cd
Pb
Ni
Cr
As
Ulva
Max. Mean Min.
1630 100 1033 564 173 13
179 70 64 55 25 1
29 1 13 7 40
0:7 0:1 0:2 0:0 <0.1
17:6 0:2 7:3 6:4 0:7 0:1
5:0 3:0 2:6 0:9 2:2 0:1
8:6 2:0 4:6 2:3 0:7 0:3
12 2 73 20
Gracilaria
Max. Mean Min.
1080 90 471 278 224 21
240 80 163 64 36 6
12 1 83 40
0:6 0:0 0:4 0:2 0:1 0:0
20:6 1 6:9 6:2 2:8 0:0
1:9 0:1 1:1 0:5 0:4 0:1
1:7 0:1 0:7 0:5 0:3 0:0
32 1 15 10 <1
Grateloupia
Max. Mean Min.
448 33 295 123 190 9
300 100 248 61 163 8
14 1 11 4 60
0:3 0:0 0:2 0:0 <0.1
5:6 0:5 3:0 2:7 0:6 0:0
4:3 5 1:9 2:1 0:6 0:0
7:9 10 3:0 4:2 0:3 0:1
56 13 31 28 20
Porphyra
Max. Mean Min.
710 100 590 125 460 20
60 5 48 18 27 3
11 1 92 81
0:2 0:0 0:1 0:0 <0.1
3:9 0:2 2:7 1:0 2:1 0:9
1:5 0:3 1:1 0:4 0:7 0:2
1:0 0:3 0:8 0:3 0:5 0:0
27 1 13 13 <1
Undaria
Max. Mean Min.
190 2 171 27 152 3
163 4 97 94 30 1
30 21 10
0:1 0:0 0:1 0:0 <0.1
4:0 0:1 2:2 2:5 0:5 0:1
1:3 0:1 1:2 0:1 1:1 0:1
0:5 0:0 0:5 0:0 0:5 0:0
93 11 70 33 47 6
Fucus
Max. Mean Min.
328 11 231 137 134 3
154 6 110 61 67 8
10 0 84 50
0:8 0:1 0:6 0:3 0:4 0:0
2:0 0:2 1:6 0:6 1:2 0:2
4:7 0:1 4:6 0:2 4:4 0:7
0:7 0:1 0:5 0:2 0:4 0:1
73 13 40 45 82
Cystoseira
Max. Mean Min.
609 100 444 198 199 7
88 11 38 33 15 4
21 0 79 20
0:2 0:0 0:1 0:0 <0.1
5:6 0:7 3:2 2:0 1:4 0:0
2:7 0:6 1:8 0:6 1:4 0:1
1:5 0:1 1:1 0:3 0:7 0:3
360 50 242 104 148 21
up in the station assumed to be the least contaminated (Lido inlet). They exceeded the highest permissible limits for seafood in India (50 ppm), and the values detected by Rajendran et al. (1993) in some Indian seaweeds collected in an area polluted by domestic and industrial wastes and harbor activities. Copper: The concentrations detected for Cu were from 1 to 29 lg g1 dry wt. The peak value was recorded in Ulva (29 161 lg g1 dry wt.) and resulted approximately six times higher than in Ulva of the Thermaikos Gulf (Malea and Haritonidis, 2000). Moore and Ramamoorthy (1984) reported the range 10–100 lg g1 dry wt. as typical of attached species inhabiting polluted waters. The concentrations of Cu in Porphyra in the Venice lagoon are comparable to those reported by Leal et al. (1997) for Porphyra spp. in the Oporto Coast which was described as a polluted and industrialized coastal area. The values found in Fucus virsoides (from 5 up to 10 lg g1 dry wt.) are slightly higher than those reported for Fucus vesiculosus in an unpolluted area (2.2 lg g1 dry wt., Riget et al., 1995). 3.2. Non-essential or inactive elements Concerning the non-essential or inactive elements no general trend was evident for concentrations of metals in
the different genera. However, Cd levels were constantly <0.1 lg g1 dry wt. in Ulva, Grateloupia, Porphyra, Undaria, Cystoseira and 6 0.8 lg g1 dry wt. in Fucus. In Fig. 2 are reported the mean values obtained considering the two sampling periods for each genus in the considered sampling sites. The standard deviations can be considered an index of temporal variability. Cadmium: This element ranged from 0.1 to 0.6 lg g1 dry wt. Fucus and Gracilaria were characterized by Cd tissue concentrations slightly higher than those found in the other seaweeds, whereas the lowest values where found in Porphyra, Undaria and Cystoseira. The highest concentration variability was evident for Ulva and Fucus. For these genera a marked Cd seasonal pattern had already been observed (Riget et al., 1995). Moore and Ramamoorthy (1984) reported several ranges of concentrations for Cd. In three brown seaweeds (not specified) sampled in a non-polluted area of the United Kingdom, Cd concentrations ranged from 0.15 to 0.43 lg g1 dry wt. Highly contaminated sites by industrial activities, e.g. a smelting plant are reported bearing mean values of 4.9 lg g1 dry wt. (Fucus vesiculosus). The Cd values found in Ulva and Gracilaria were similar to those found by Malea and Haritonidis (1999b, 2000) in the Thermaikos Gulf. Leal et al. (1997) detected Cd values comparable to those reported in the present work in Porphyra spp. samples from the Oporto Coast
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449
Fig. 2. Mean values of As, Zn, Pb, Cr, Ni, Cd (lg g1 , dry wt.) calculated for the two sampling periods for the seven genera of seaweeds in the four sampling sites. (P ¼ Ponte della Liberta, T ¼ Tronchetto, C ¼ Celestia, L ¼ Lido inlet; Ul ¼ Ulva, Gr ¼ Gracilaria, Gt ¼ Grateloupia, Po ¼ Porphyra, Un ¼ Undaria, Fu ¼ Fucus, Cy ¼ Cystoseira).
which had been presented as a polluted and industrialized coastal area. Nickel: Nickel values ranged between 0.4 lg g1 dry wt. in Gracilaria, and 4.7 lg g1 dry wt. in Fucus. The highest mean concentrations were found in Fucus and Ulva. The mean value found in the last species (2:6 0:9 lg g1 dry wt.) was similar to that found by Malea and Haritonidis (2000). Concentrations of Ni in aquatic plants are reported to be rather low. For nine species from the Indian coastal waters a range of 0.5–39.1 lg g1 dry wt. is reported. For Fucus vesiculosus collected along the Welsh coasts, a range of 4.5–8.9 lg g1 dry wt. was detected (Moore and Ramamoorthy, 1984). The values reported
in this paper are slightly lower than those quoted above and are in accordance with those reported by Kureishy (1991) for seaweeds collected around an industrialpetrochemical area. Lead: Lead values ranged from 0.5 up to 20.6 lg g1 dry wt. The highest mean concentrations and seasonal variability were detected in Ulva (7.3 2.6 g1 dry wt.) and Gracilaria (6:9 6:2 g1 dry wt.) at the Celestia and Lido inlet stations. The Pb ranges quoted by Moore and Ramamoorthy (1984) for estuarine and coastal marine species show, for heavily polluted areas, values up to 170 lg g1 dry wt. Malea and Haritonidis (2000) report for Ulva Pb concentrations up to 3213 g1 dry wt., with mean values
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of 748 206 g1 dry wt. The same authors found in Gracilaria Pb values only twice higher than in the Venice samples. In contrast, the concentrations reported by Riget et al. (1995) with reference to Fucus vesiculosus picked up in an unpolluted area were one–two orders of magnitude lower than those detected in this work (0.05–0.70 lg g1 dry wt.). Concentrations determined in Porphyra spp. sampled in industrialized European coastal areas (Leal et al., 1997) are similar to those found in this work. Chromium: The concentrations of this element ranged between 0.3 and 8.6 lg g1 dry wt.; the highest mean concentrations were determined in Ulva, which was the seaweed showing the highest seasonal variability. Orders of 10 lg g1 were detected in seaweeds collected in unpolluted areas; values of 103 lg g1 wet wt. were recorded in high Cr-contaminated areas (Dahab et al., 1990). The values found in Ulva were similar to those found by Malea and Haritonidis (2000). Arsenic: The concentrations of As refer to the total element content. The range was rather wide, 0–360 lg g1 dry wt. The highest values were detected in Cystoseira barbata, a brown seaweed whose seasonal variability (50%) was considerably higher than its spatial difference (6–13%). It is possible to individualize a pollution gradient among the seaweed taxa: brown seaweeds > red seaweeds > green seaweeds. Generally, seaweeds shown high As content and especially brown seaweeds are known to accumulate As hundred times as much as land plants (Keiji and Kanji, 1989). Residues detected in Fucus serratus in highly contaminated waters reached 54 lg g1 dry wt. This value is in accordance with the one detected in Fucus virsoides
(8–73 lg g1 dry wt.) in the present work. The values of five attached species in estuarine waters along the SW coast of England were around 59–189 lg g1 dry wt. (Moore and Ramamoorthy, 1984). Heavy metal concentrations in some seaweeds of the Venice lagoon had previously been determined by Sfriso et al. (1994, 1995) and Sfriso (2000) in two stations (Alberoni and San Giuliano) very similar to the Lido inlet and Ponte della Libert a, respectively. An analysis of the considered species is possible by comparing the data reported in this work with those reported by Sfriso et al. (1995), as Sfriso, 2000 values refer only to Ulva. Ulva and Gracilaria were considered to be the most representative (Fig. 3). As arsenic had not been detected in 1994 and 1995, it was not included in the comparison. The only values relative to As in Ulva are those detected by Sfriso (2000). They ranged from 4 to 65 lg g1 , with a mean of 30 lg g1 and a great deal of variability (83%) among samples collected in different sites and periods. The As concentration was three times as high as the one detected in the present work. With reference to the considered species, metal concentrations are comparable to those detected by Sfriso et al. (1994). At San Giuliano and Ponte della Libert a the seaweed contamination was higher than at Alberoni and Lido inlet, except for Pb, Ni and Cr. However, from data obtained in 1994 and 2000, it is possible to point out a generalized decrease in metal concentrations, with the exception of Pb which was recorded to increase. The generalized depletion of metals linked to industrial activities suggests a reduced contamination impact of Porto Marghera industrial district. On the contrary, the increased lead concentration increase reveals the
Fig. 3. Comparison between values (lg g1 , dry wt.) found in Ulva and Gracilaria detected at Lido inlet and Ponte della Liberta and values found by Sfriso (2000) in two analogous stations: Alberoni and San Giuliano.
8 9 n.d. 32 12 6 18 15 10 5 12 21 5 2 1 6 17.6 6.3 n.d. 3.6 16 0.7 21 7 2.3 1.1 6 3 6 8 5.7 3.4 2.3 5 n.d. 1.0 2.5 3 1.9 2 3.2 2.7 1.3 0.7 2.5 2.2 0.5 0.8 0 0.1 n.d. 0.1 0.1 0.2 0.4 0.6 0.1 0.3 0.4 0.5 0.2 0.7 0.2 0.4 11 8 n.d. 4 4 10 12 10 9 13 5 8 11 29 6 11 30 25 n.d. 36 43 28 240 166 32 33 200 162 104 179 140 198 Gracilaria
Ulva
I II I II
P
1340 1630 1400 1170 1334 217 173 1460 400 380 1080 n.d. 430 224 357 424
As Pb Ni Cd Cu Zn Fe
dry wt.
T
C
L
P
T
C
L
P
T
C
L
P
T
C
L
P
T
C
L
P
T
C
L
P
T
C
L
451
lg g1
Ulva and Gracilaria comparison among the four sampling sites (P ¼ Ponte della Liberta, T ¼ Tronchetto, C ¼ Celestia, L ¼ Lido inlet). I ¼ first sampling period; II ¼ second sampling period; n.d: ¼ not determined
importance of gasoline combustion as a source of this contamination (leaded gasoline will be available in Italy till Dec. 31, 2001). The concentrations of heavy metals in Ulva and Gracilaria can be used to investigate possible spatial trends in the lagoon of Venice, since Gracilaria and Ulva are the only species available in all the sampling stations (Table 4) of the present work. Zinc, Cu and Cd concentrations showed, in fact, a decreasing trend in samples taken in stations from the inner lagoon towards the sea Lido inlet. For Zn this depletion was almost of one order of magnitude. For Cu and Cd the same trend resulted evident during the autumn sampling session. On the contrary, Pb concentrations at the Celestia and the Lido inlet stations resulted to be higher than in the other stations. As for As, it seems possible to exclude that the industrial area could be a contamination source since the highest values were found at the Celestia and Tronchetto stations. It is known that As has been employed as a colorant agent by the glass-factories located on the island of Murano, which is rather close to the Celestia sampling station. Existing correlations between elements were also investigated (Table 5). The highest correlation indices refers to Fe–Cr. The results (r ¼ 54, p < 0:05, N ¼ 29) were similar to those found by Sfriso et al. (1995). The use of metallurgical grade chromite in the production of iron-alloys is reported (Moore and Ramamoorthy, 1984) as a source of these two contaminants; thus a common industrial origin could be a probable reason for this correlation. Iron and Pb concentrations were also significantly correlated. Moore and Ramamoorthy (1984) reported that the main discharges of Pb are linked to oil and gasoline combustion, secondarily to non-ferrous metal production and iron steel production. The same relationship (r ¼ 90, p < 0:05, N ¼ 29) was also observed by Sfriso et al. (1995). This paper also reports the sediment concentrations in the sampling areas. The correlation found for the concentrations of these elements in the sediment was significant but negative (r ¼ 0:92, p < 0:05, N ¼ 24). Such an evidence seems to exclude a common origin of the contamination, on the contrary it suggests a common dispersion mechanism in solution and/or an analogous uptake strategy by seaweeds. Correlations Cd–Zn and Cd–Cu were also significant, as well. By analyzing the values reported in literature, similar correlations were found by Kureishy (1991) (r ¼ 1:00 and 0.92, respectively, for p < 0:05 and N ¼ 35) and Karez et al. (1994) (r ¼ 0:92, p < 0:05, N ¼ 14). Sfriso et al. (1995) found significant Cd–Zn and Cd– Cu correlations in the surface sediment of the Venice lagoon. The probable reasons for these results are to be found in the relative position of these elements in the periodic table of the elements which implies a similar chemical behavior and the common origin from
Table 4
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Table 5 Correlation matrix relative to concentration values detected for 30 observations Variable Fe Zn Cu Cd Pb Ni Cr As a
Correlations Fe
Zn
Cu
Cd
Pb
Ni
Cr
As
1.00 0.19 0.33 0.08 0.59a 0.34 0.72a 0.23
1.00 0.31 0.44a 0.15 0.23 0.00 0.30
1.00 0.46a 0.22 0.21 0.51a 0.28
1.00 0.06 0.28 0.07 0.26
1.00 0.09 0.35 0.18
1.00 0.52a 0.06
1.00 0.17
1.00
Values significative for p > 0:05 and N ¼ 30.
sphalerite processing. The correlations and trends of Cd and Cu, as reported by Malea and Haritonidis (2000), but also of Zn could also reflect the seaweed growth dynamics showing lower concentrations in spring when the growth rate is faster and higher values in autumn when seaweed populations are older and the growth rate is reduced. Whereas a significant correlation is reported in the literature for Ni–Cr (r ¼ 0:96, p < 0:05, N ¼ 4; Tariq et al., 1993), for the pair Cu–Cr no analogous relevant relationships were found. A probable common origin for Ni and Cr could be the production and use of Ni–Cr stainless steel. Moore and Ramamoorthy (1984) attributed these correlations to the large use of Ni–Cr alloys in the heating elements of domestic stoves and industrial furnaces.
As contamination because the mean concentration ratio with the other considered species ranged from 35 (Ulva) to 3.5 (Undaria). 5. By considering Ulva and Gracilaria, the only seaweeds collected in all sampling sites, Zn and Cd were significantly correlated and showed a decreasing trend from the inside of the lagoon to the outside. Such a behavior suggests a common industrial source. 6. The generalized decrease in metal concentrations, except for Pb, in seaweed tissues during the last five years is in accordance with the trend observed for nutrients and other pollutants in the surface sediments. Conversely, the Pb increase suggests the relevance of leaded gasoline combustion as the main source of contamination for this element.
Acknowledgements 4. Conclusions By these results it is possible to conclude that: 1. The heavy metal contamination of the considered seaweed species was in ranges comparable to those reported in the literature for industrialized coastal areas. 2. Porphyra and Undaria show the lowest heavy metal contamination. As these seaweeds are seasonal, it is evident that time exposure is a key factor in the metal uptake. 3. Ulva exhibited the highest contamination for many of the considered metals, i.e. Fe, Cu, Pb and Cr, and together with Fucus the highest values of Cd and Ni. Ulva, a species abundantly spread in the whole lagoon and not used for the animal and human nutrition, could be employed as environmental biomonitor. 4. Cystoseira displayed the highest values for As. This species could be used as an excellent indicator for
This work was partly supported by the Consorzio Ricerche Lagunari, (CORILA, Consortium for the coordination of the scientific research on the Lagoon of Venice). The authors are grateful to Mrs. Sonia Ceoldo for technical assistance and to Dr. Orietta Zucchetta for reviewing the English text.
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Heavy metal contamination in the seaweeds of the Venice lagoon M. Caliceti, E. Argese, A. Sfriso, B. Pavoni
*
Dipartimento Scienze Ambientali, Facolt a di Scienze MM. FF. NN., Centro di Studio sulla Chimica e Tecnologia per l’Ambiente, Universit a Ca’ Foscari di Venezia, Calle Large Santa Marta 2137, 30123 Venezia, Italy Received 20 December 2000; received in revised form 23 October 2001; accepted 26 October 2001
Abstract The concentrations of heavy metals (Fe, Zn, Cu, Cd, Ni, Pb, Cr, As) were determined in seven seaweeds of environmental and commercial relevance (Ulva rigida C. Ag., Gracilaria gracilis (Stackhouse) Steentoft, L. Irvine and Farnham, Porphyra leucosticta Thuret, Grateloupia doryphora (Montagne) Howe., Undaria pinnatifida (Harv.) Suringar, Fucus virsoides J. Agardh, Cystoseira barbata (Good. et Wood.) Ag.) collected in four sampling sites in the lagoon of Venice, in spring and autumn 1999. Metals were extracted using hot concentrated acids in a Microwave Digestion Rotor and analysed by absorption spectrophotometry using a flame mode for Fe and Zn and a graphite furnace for Pb, Cr, Cd, Cu, Ni and As. High contamination levels, especially for Pb, were detected in Ulva and to a lesser extent in Gracilaria. Brown seaweeds, especially Cystoseira was highly contaminated by As. The least contaminated genera with all metals except As were Porphyra and Undaria. A concentration decrease for Zn and Cd was observed from the inner parts of the central lagoon, close to the industrial district, towards the lagoon openings to the sea. Ó 2002 Elsevier Science Ltd. All rights reserved. Keywords: Seaweeds; Heavy metals; Biomonitors; Venice lagoon
1. Introduction The use of seaweeds as animal and human food, soil manure, salt extractions (soda, iodine, etc.), colloid production (agar, alginates, carrageenan, furcellaran, etc.), cosmetics, pharmaceuticals, energy production is a very old and widespread practice (Chapman and Chapman, 1980; Bird and Benson, 1987; Bressan and De Luca, 1987; COST 48, 1989 and references therein, Bradford and Bradford, 1996). Seaweeds represent an important economical resource mostly in the Indian and Pacific countries where they are not only largely harvested but also intensively and largely employed in the human nutrition.
*
Corresponding author. Tel.: +39-041-257-85-22; fax: +39041-257-85-82. E-mail address: [email protected] (B. Pavoni).
In Europe the collection and utilization of seaweeds have a lower diffusion than in the Indian and Pacific areas. Except for the extraction of iodine and soda from fucoids, which has been practiced since the 17th century, and the use of fresh seaweeds as fodder for sheep, cattle and horses, which browse on the shore in some northern countries (Scotland, Norway, Iceland, etc.), the attention to seaweeds has been drawn mostly after the Second World War. The excessive growth of some species (especially Ulva, Enteromorpha, Chaetomorpha, Cladophora, Gracilaria, etc.), which colonized many lagoons and shallow coastal areas, created serious problems for the environment quality, the local populations and economies (Casabianca-Chassany, 1984, 1989; Sfriso et al., 1987, 1992; Schramm, 1991; Schramm and Nienhuis, 1996 and references therein; Briand, 1991; CEVA, 1993; Menesguen and Piriou, 1995; Morand and Briand, 1996; Sfriso and Marcomini, 1996; Viaroli et al., 1992,
0045-6535/02/$ - see front matter Ó 2002 Elsevier Science Ltd. All rights reserved. PII: S 0 0 4 5 - 6 5 3 5 ( 0 1 ) 0 0 2 9 2 - 2
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1994; etc.). In these areas seaweeds are mainly harvested to prevent or mitigate the effects of an abnormal biomass proliferation and possible anoxic events. However, in European countries the collected biomass is more a problem than a profit. As a consequence, many seaweed studies and projects have been addressed to the biomass conversion and digestion (COST 48, 1987 and references therein; Croatto, 1982; Morand et al., 1990, 1991; Cuomo et al., 1993, 1995; Orlandini, 1994; Morand and Briand, 1996). Another actual European application of seaweeds deals with the environmental monitoring and restoration. Some seaweeds are used or indicated as appropriate biomonitors to study the environment contamination (Munda, 1982; COST 48, 1987; Munda and Hundnik, 1991 and references therein; Marcomini et al., 1993; Haritonidis and Malea, 1995, 1999; Sfriso et al., 1995; Malea and Haritonidis, 1999a,b, 2000). Seaweed crop is also used for nutrient and contaminant abatement (Croatto, 1982; COST 48, 1987 and references therein; Morand and Briand, 1996). The lagoon of Venice, is the widest shallow area populated by macrophytes, in Italy. Starting from the 60s, the lagoon has been affected by an abnormal production of nitrophilic species, especially Ulva rigida C. Ag., which caused a change in the benthic-flora structure (Sfriso, 1987), the alteration of the nutrient cycles and the occurrence of dystrophic crises (Sfriso et al., 1992). In the 1970’s and 1980’s, in the central basin, about a third of the entire lagoon, a gross seaweed production of ten million tonnes was estimated (Sfriso and Marcomini, 1994). Since the late 1980’s, to prevent the effects of this abnormal biomass proliferation and decomposition, the local administration provided for the seaweed biomass to be harvested (up to 55.000 m3 yr1 ). Many projects explored the use of seaweed crops in agriculture, in the production of compost and biogas without obtaining economically satisfactory results (Croatto, 1982; Cuomo et al., 1993, 1995). Finally, a method for converting the biomass in paper pulp, after a suitable pre-treatment, to produce the ‘‘Ulva carta’’ has been developed from a local paper company, thus solving the problem of the macrophyte crops in an economically convenient way. Since 1990 a new trend emerged: a strong reduction of Ulva distribution and production was coupled with a re-population of native seagrass and seaweed species. At the same time new seaweeds of eastern origin entered the lagoon of Venice through fishing and commercial traffic. Among these the hard-bottom species: Sargassum muticum (Yendo) Fensholt, Undaria pinnatifida (Harvey) Suringar and Grateloupia doryphora (Montagne) Howe spread over the whole lagoon, while Cystoseira barbata (Good. et Woodw.), a species very common before the Ulva proliferation, re-colonized some areas. At present, the Venice lagoon is populated by over 250 seaweed taxa differently spread and distributed in
the inner and outer littorals. Many of these have a possible economic relevance or can be used as biomonitors for waters (Levine, 1984; Phillips, 1995; Moy and Walday, 1996 and references therein; Haritonidis and Malea, 1995, 1999; Malea and Haritonidis, 1999a,b, 2000), especially for dissolved heavy metal contamination (R€ onnberg et al., 1990; Ganesan et al., 1991; Kureishy, 1991; Rajendran et al., 1993; Rainbow and Phillips, 1993; Tariq et al., 1993; Karez et al., 1994; €ksezgin and Balci, 1994; Rainbow, 1995; Riget K€ ußcu et al., 1995; Leal et al., 1997). The objective of this paper is to investigate on the contamination level and the capacity of some highly widespread seaweeds growing in the Venice lagoon (viz. Ulva rigida C. Ag., Gracolaria gracilis, Grateloupia doryphora (Montagne) Howe, Porphyra leucosticta Thuret, Fucus virsoides J. Ag., Undaria pinnatifida (Harvey) Suringar, Cystoseira barbata (Good, et Woodw.) Ag.) to selectively accumulate inorganic contaminants: Fe, Zn, Cu, Cd, Ni, Pb, Cr, As. These species were selected for their abundance, biomonitoring capacity and actual (paper pulp making, gas production, soil amendment) and potential uses (as nutrient and contaminant traps, for the extraction of phycocolloids, agar and alginate, and use in cosmetics, pharmacology and animal or human nutrition (Bressan and De Luca, 1987; Penso, 1987; Keiji and Kanji, 1989).
2. Materials and methods 2.1. Study area The lagoon of Venice is a shallow water body with a mean depth of 1 m and a total surface of 549 km2 (Fig. 1). It is subdivided into three main sections, named the southern, the northern and the central basins. The city of Venice is located in the central basin. The mean tidal excursion is 62 cm and the water change is guaranteed by three inlets, which enable the renewal of 60% of the lagoon water every 12 h. The industrial district of Porto Marghera has severely affected the lagoon environmental conditions: in the past the main impact derived from the production of phosphorus–nitrogen fertilizers and non-ferrous metals, such as Al and Zn, at present the petrochemical activity is probably prevailing. The inland urban settlements, especially the towns of Marghera and Mestre and the island of Lido, which have been connected to sewage treatment plants only recently, as well as Venice historical centre, and the islands of Murano, Burano and Pellestrina, which have a marked tourist-vocation and lack of an advanced sewage system, have also contributed to the lagoon contamination (Lee et al., 1990).
M. Caliceti et al. / Chemosphere 47 (2002) 443–454
2.2. Sampling sites Seaweeds were collected in the hard substrates of four stations (Fig. 1) placed in a transect from the mainland towards the Lido lagoon inlet: Ponte della Liberta (St. 1), Tronchetto (St. 2), Celestia (St. 3), Lido inlet (St. 4), in two sampling sessions: In spring 1999 during their highest biomass production and in autumn of the same year when the perennial species showed a secondary biomass peak. Some seasonal species such as Porphyra leucosticta and Undaria pinnatifida, were found only in spring. Other species such as Undaria pinnatifida, Cystoseira barbata, Fucus virsoides and Gracilaria gracilis were not found in all the sampling sites which are located in different areas of the lagoon with peculiar hydrodynamics and human impacts (Fig. 1). St. 1: Ponte della Liberta. This station is located at north-west of Venice close to the mainland. It is influenced both by the urban effluents of Mestre and its hinterland and by the industrial area of Porto Marghera. Therefore, this area was assumed to be the most contaminated. Moreover the site is close to the heavy traffic translagoonar bridge connecting Venice to the city of Mestre. Water renewal is rather low and micropollutant contamination in sediments is high (Sfriso, 2000). In this station only Ulva and Gracilaria were found. St. 2: Tronchetto. This station is placed in the western district of Venice historical centre, 3 km far from station 1. It is placed close to the parking area of Tronchetto and characterized by an intense maritime traffic. Water exchange is guaranteed by the adjacent
445
Vittorio Emanuele canal leading to the Lido inlet. In this area Cystoseira was missing. St. 3: Celestia. It is located at north–east of Venice close to a highly populated area, where household activities and maritime traffic are the main pollution sources. In this area the ebb tide conveys all the nontreated sewage of the historical centre. Furthermore the island of Murano, with its numerous glass factories, is very close to this sampling site. In this station were found all the studied species. St. 4: Lido inlet. This station is located 10 km far from St. 1 near the lagoon inlet of Lido, through which waters from the Adriatic Sea flood the northern and the central basins. Among the four stations this one is the farthest away from contamination sources. For these reasons it was assumed to be the least contaminated. In this area Cystoseira was not found. 2.3. Seaweed selection Among 250 macroalgal taxa living in the Venice lagoon, seven species have been selected because of their abundance, actual use and potential relevance. (1) Ulva rigida C. Ag., is the most abundant species in the Venice lagoon even though its standing crop and production have significantly decreased during the 1990’s (Sfriso and Marcomini, 1996; Sfriso, 2000). In the past this species was harvested to prevent anoxic crises and used for paper manufacturing. This widespread seaweed is reported as a valid indicator species, especially of Pb (Malea and Haritonidis, 2000).
Fig. 1. Distribution of sampling sites in the central basin of the lagoon of Venice.
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(2) Gracilaria gracilis (Stackhouse) Steentoft, L. Irvine and Farnham in terms of biomass production until the end of the 1980’s was the second macroalgal species growing in the Venice lagoon. This species was harvested for agar extraction since the 1940s (12 t, dry wt., per year). The highest biomass was collected in 1985 (1700 t, dry wt. per year), then the biomass began to decrease and in the 1990’s its harvesting was considered no more profitable. (Orlandini and Favretto, 1987; Sfriso et al., 1994). Gracilaria gracilis is suggested as a good bioindicator especially for Cd (Malea and Haritonidis, 1999b). (3) Porphyra leucosticta Thuret, shows an important biomass in spring, although this species has never been harvested in the Venice lagoon. Because of its high production and use as human nourishment, ‘‘Nori’’ in the eastern countries (Chapman and Chapman, 1980; COST 48, 1989; Bradford and Bradford, 1996) and its natural availability and abundance, Porphyra can be an interesting species in the view of a possible future utilization. (4) Fucus virsoides J. Ag., is an endemic species very interesting for algin production and its cosmetic implications. In the past a national company investigated its availability for salt-bath production. However this species, very sensitive to eutrophication and anoxic crises, was not available with an adequate biomass. At present, as the nitrophilic species, like Ulva rigida, are markedly reduced and no anoxia events occur, this species has spread over the hard substrates close to the lagoon inlets, where waters are less eutrophicated and well renewed. (5) Cystoseira barbata (Good. et Woodw.), a seaweed very abundant in the hard substrates of the Venice lagoon might become a source of raw material for alginate production. (6) Grateloupia doryphora (Montagne) Howe, is a new species for the Venice lagoon. This seaweed is cultivated in Japan and China for the production of Funoran a seaweed glue called ‘‘Funori’’ which is used as an adhesive and for sizing paper, fibre or cloth. This species lives on the hard substrates, especially in the winter and the spring seasons. (7) Undaria pinnatifida (Harvey) Suringar, is also an invasive seaweed species which has populated the hard Venice lagoon substrates only recently, during the 1990’s. This species has a big size and a fast growth. In late spring Undaria reaches biomasses of many kg m2 (5–10 kg m2 , wet wt.). Undaria is a species very cultivated and harvested in the eastern seas where is used mainly as human food (in soups, with rice, sauces etc.) and it is known as ‘‘Wakame’’ (Chapman and Chapman, 1980; Bradford and Bradford, 1996). 2.4. Seaweed collection and preparation Many entire thalli of each seaweed species were hand-picked or collected with a hand net taking into
account the different age and depth in order to obtain homogeneous samples representative of the entire algal population living in the study area. All the collected samples were attached to the substrate in order to avoid to collect samples moving from different areas. The obtained seaweed samples (0.5–1 kg for the small size species and 2–3 kg for Undaria and Cystoseira) were carefully washed with sea-water in order to remove the trapped sediment, epiphytic organisms and the hidden fauna. Stored at 20 °C in PET-LD bags, after freezedrying, seaweed samples were crashed and homogenized in a porcelain mortar. The residual water content of the obtained seaweed samples processed for the metal determination was determined by dessication at 80 °C for a night, in order to correct the final values. 2.5. Materials The used reagents were: Hydrogen peroxide ‘‘ARISTAR’’ 30% w/v (BDH), Nitric acid ‘‘ARISTAR’’ acidimetric titer 68.5–69.5% (BDH). The reference material CRM 062 (Olive leaves) was donated by the EU Joint Research Centre of Ispra (Varese, Italy). 2.6. Extraction Metals were extracted using a Microwave Digestion Rotor, MDR, Ethos 1600 Milestone (wave length: 12.25 cm, frequency 2450 MHz). The following procedure was experimented as the most suitable for handling seaweed samples to obtain extracts free from undissolved residues. Freeze-dried samples (300 mg) were digested with 3 mL milli-Q water, 5 mL nitric acid and 1 mL hydrogen peroxide. The heating program was: 2 min at 250 W, 2 min at 0 W, 5 min at 250 W, 5 min at 400 W. Two replicates of each sample were analysed. Blank assays were carried out. The extracts were stored at þ4 °C in PET-HD flasks previously cleaned with nitric acid. 2.7. Instrumental analysis Metals were determined by means of a SpectrAA-250 Plus VARIAN spectrometer (flame mode for Fe and Zn, graphite furnace of Pb, Cr, Cd, Cu, Ni and As), using the standard addition procedure. The precision of the methodology expressed as standard deviation percentage was less than 15% for all metals except for Ni (23%) and Cr (26%). The methodology was tested using a reference sample, certified for Cd, Cu, Pb and Zn. Metal concentrations were determined in triplicate; the results are reported in Table 1. The results of Zn resulted significantly different from the certified ones. For this metal a probable contamination of the standard sample has occurred before the
M. Caliceti et al. / Chemosphere 47 (2002) 443–454
447
Table 1 Results of the reference material analyses (Olea europea) Dry wt. (lg g1 )
Sub-sample I
Sub-sample II
Sub-sample III
Mean
CRM 062
Cd Cu Pb Zn
0.10 52 28 24
0.09 46 23 37
0.11 55 23 31
0.10 0.01 51 4 25 3 31 8
0:10 0:02 46:6 1:8 25:0 1:5 16:0 0:7
analysis. This problem was not considered critical as the analytical procedure tested on certified sediments gave variations with respect to the certified results of the same order as for the other metals. Except Fe (17 mg L1 ) and Zn (12 lg L1 ), the blank values of the considered metals were 6 the detection limits: i.e. 0.7 lg L1 (Cu), 1.0 lg L1 (Pb), 0.1 lg L1 (Cd), 1.0 lg L1 (Ni), 1.2 lg L1 (As) and 1.0 lg L1 (Cr).
The concentration values of the metals are summarized in Table 3. They are the mean of the values obtained in the four sampling sites during the sampling period calculated in order to obtain synthetic information per species. The standard deviations presented in Table 3 are therefore a time and space variability index of the detected concentrations. 3.1. Bio-essential elements
3. Results and discussion In Table 2 the collected seaweed genera are listed as per sampling station and per session. The seaweeds sampled at Ponte della Liberta were only Ulva and Gracilaria, which are known to be the most pollutiontolerant species among the collected ones. Porphyra, Undaria, are seasonal genera, which were collected in spring only. The contamination level of these genera will be discussed as an indication of spatial variability. Fucus, the species more sensible to eutrophication, was found in the Lido inlet station only.
Table 2 Period, site and genera sampled Spring 1999
Autumn 1999
Ponte della Libert a
Ulva Gracilaria
Ulva Gracilaria
Tronchetto
Ulva Gracilaria Grateloupia Porphyra Undaria
Ulva Gracilaria Grateloupia
Celestia
Ulva Gracilaria Grateloupia Porphyra Undaria Cystoseira
Ulva Gracilaria Grateloupia Cystoseira
Lido inlet
Ulva Porphyra Fucus Cystoseira
Ulva Gracilaria Fucus Cystoseira
The relative abundance of the bio-essential elements was always the following Fe > Zn > Cu. An analogous sequence is reported in other paper concerning metal distribution in seaweeds (Ganesan et al., 1991; Rajendran et al., 1993; Malea and Haritonidis, 1999b, 2000). Iron: As for Fe the highest mean concentrations were detected in Ulva (1033 564 lg g1 dry wt.). The overall variability ranged from 134 to 1630 lg g1 dry wt. The mean value is approximately three times higher than the values found in the same species collected in the Thermaikos Gulf, Greece (Malea and Haritonidis, 2000) which is considered a polluted area. The range is analogous to that reported for some seaweeds living in sites of the Bay of Bengal which are also considered to be polluted (Ganesan et al., 1991, and references therein). Assuming that the metal uptake in temperate region is generally low because shorter day-length and lower light intensity affect photosynthesis rate, the values detected for Fe in the seaweeds of the Venice lagoon are relatively high. Zinc: Zinc ranged from 15 to 300 lg g1 dry wt.; the genera with the highest values were Grateloupia and Gracilaria (Fig. 2). Gracilaria showed a Zn mean value (163 64 lg g1 dry wt.) approximately twice higher than in the same species collected in the Thermaikos Gulf, Greece (Malea and Haritonidis, 1999b). Moore and Ramamoorthy (1984) reported that in the absence of metal mines/smelters, i.e. main Zn-contamination sources, levels in seawater plants are generally <100 lg g1 dry wt.; however, examples of heavy Zncontaminated sites are characterized by values as high as 104 lg g1 dry wt. The Zn values reported by other authors (Riget et al., 1995) for Fucus vesiculosus in unpolluted areas are one order of magnitude lower than those obtained in the Venice lagoon (110 61 lg g1 dry wt.). It should be noticed that the samples of Fucus virsoides were picked
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Table 3 Maximum, minimum and mean values obtained as average of the two sampling periods and four sampling sites for each genus Dry wt. (lg g1 )
Fe
Zn
Cu
Cd
Pb
Ni
Cr
As
Ulva
Max. Mean Min.
1630 100 1033 564 173 13
179 70 64 55 25 1
29 1 13 7 40
0:7 0:1 0:2 0:0 <0.1
17:6 0:2 7:3 6:4 0:7 0:1
5:0 3:0 2:6 0:9 2:2 0:1
8:6 2:0 4:6 2:3 0:7 0:3
12 2 73 20
Gracilaria
Max. Mean Min.
1080 90 471 278 224 21
240 80 163 64 36 6
12 1 83 40
0:6 0:0 0:4 0:2 0:1 0:0
20:6 1 6:9 6:2 2:8 0:0
1:9 0:1 1:1 0:5 0:4 0:1
1:7 0:1 0:7 0:5 0:3 0:0
32 1 15 10 <1
Grateloupia
Max. Mean Min.
448 33 295 123 190 9
300 100 248 61 163 8
14 1 11 4 60
0:3 0:0 0:2 0:0 <0.1
5:6 0:5 3:0 2:7 0:6 0:0
4:3 5 1:9 2:1 0:6 0:0
7:9 10 3:0 4:2 0:3 0:1
56 13 31 28 20
Porphyra
Max. Mean Min.
710 100 590 125 460 20
60 5 48 18 27 3
11 1 92 81
0:2 0:0 0:1 0:0 <0.1
3:9 0:2 2:7 1:0 2:1 0:9
1:5 0:3 1:1 0:4 0:7 0:2
1:0 0:3 0:8 0:3 0:5 0:0
27 1 13 13 <1
Undaria
Max. Mean Min.
190 2 171 27 152 3
163 4 97 94 30 1
30 21 10
0:1 0:0 0:1 0:0 <0.1
4:0 0:1 2:2 2:5 0:5 0:1
1:3 0:1 1:2 0:1 1:1 0:1
0:5 0:0 0:5 0:0 0:5 0:0
93 11 70 33 47 6
Fucus
Max. Mean Min.
328 11 231 137 134 3
154 6 110 61 67 8
10 0 84 50
0:8 0:1 0:6 0:3 0:4 0:0
2:0 0:2 1:6 0:6 1:2 0:2
4:7 0:1 4:6 0:2 4:4 0:7
0:7 0:1 0:5 0:2 0:4 0:1
73 13 40 45 82
Cystoseira
Max. Mean Min.
609 100 444 198 199 7
88 11 38 33 15 4
21 0 79 20
0:2 0:0 0:1 0:0 <0.1
5:6 0:7 3:2 2:0 1:4 0:0
2:7 0:6 1:8 0:6 1:4 0:1
1:5 0:1 1:1 0:3 0:7 0:3
360 50 242 104 148 21
up in the station assumed to be the least contaminated (Lido inlet). They exceeded the highest permissible limits for seafood in India (50 ppm), and the values detected by Rajendran et al. (1993) in some Indian seaweeds collected in an area polluted by domestic and industrial wastes and harbor activities. Copper: The concentrations detected for Cu were from 1 to 29 lg g1 dry wt. The peak value was recorded in Ulva (29 161 lg g1 dry wt.) and resulted approximately six times higher than in Ulva of the Thermaikos Gulf (Malea and Haritonidis, 2000). Moore and Ramamoorthy (1984) reported the range 10–100 lg g1 dry wt. as typical of attached species inhabiting polluted waters. The concentrations of Cu in Porphyra in the Venice lagoon are comparable to those reported by Leal et al. (1997) for Porphyra spp. in the Oporto Coast which was described as a polluted and industrialized coastal area. The values found in Fucus virsoides (from 5 up to 10 lg g1 dry wt.) are slightly higher than those reported for Fucus vesiculosus in an unpolluted area (2.2 lg g1 dry wt., Riget et al., 1995). 3.2. Non-essential or inactive elements Concerning the non-essential or inactive elements no general trend was evident for concentrations of metals in
the different genera. However, Cd levels were constantly <0.1 lg g1 dry wt. in Ulva, Grateloupia, Porphyra, Undaria, Cystoseira and 6 0.8 lg g1 dry wt. in Fucus. In Fig. 2 are reported the mean values obtained considering the two sampling periods for each genus in the considered sampling sites. The standard deviations can be considered an index of temporal variability. Cadmium: This element ranged from 0.1 to 0.6 lg g1 dry wt. Fucus and Gracilaria were characterized by Cd tissue concentrations slightly higher than those found in the other seaweeds, whereas the lowest values where found in Porphyra, Undaria and Cystoseira. The highest concentration variability was evident for Ulva and Fucus. For these genera a marked Cd seasonal pattern had already been observed (Riget et al., 1995). Moore and Ramamoorthy (1984) reported several ranges of concentrations for Cd. In three brown seaweeds (not specified) sampled in a non-polluted area of the United Kingdom, Cd concentrations ranged from 0.15 to 0.43 lg g1 dry wt. Highly contaminated sites by industrial activities, e.g. a smelting plant are reported bearing mean values of 4.9 lg g1 dry wt. (Fucus vesiculosus). The Cd values found in Ulva and Gracilaria were similar to those found by Malea and Haritonidis (1999b, 2000) in the Thermaikos Gulf. Leal et al. (1997) detected Cd values comparable to those reported in the present work in Porphyra spp. samples from the Oporto Coast
M. Caliceti et al. / Chemosphere 47 (2002) 443–454
449
Fig. 2. Mean values of As, Zn, Pb, Cr, Ni, Cd (lg g1 , dry wt.) calculated for the two sampling periods for the seven genera of seaweeds in the four sampling sites. (P ¼ Ponte della Liberta, T ¼ Tronchetto, C ¼ Celestia, L ¼ Lido inlet; Ul ¼ Ulva, Gr ¼ Gracilaria, Gt ¼ Grateloupia, Po ¼ Porphyra, Un ¼ Undaria, Fu ¼ Fucus, Cy ¼ Cystoseira).
which had been presented as a polluted and industrialized coastal area. Nickel: Nickel values ranged between 0.4 lg g1 dry wt. in Gracilaria, and 4.7 lg g1 dry wt. in Fucus. The highest mean concentrations were found in Fucus and Ulva. The mean value found in the last species (2:6 0:9 lg g1 dry wt.) was similar to that found by Malea and Haritonidis (2000). Concentrations of Ni in aquatic plants are reported to be rather low. For nine species from the Indian coastal waters a range of 0.5–39.1 lg g1 dry wt. is reported. For Fucus vesiculosus collected along the Welsh coasts, a range of 4.5–8.9 lg g1 dry wt. was detected (Moore and Ramamoorthy, 1984). The values reported
in this paper are slightly lower than those quoted above and are in accordance with those reported by Kureishy (1991) for seaweeds collected around an industrialpetrochemical area. Lead: Lead values ranged from 0.5 up to 20.6 lg g1 dry wt. The highest mean concentrations and seasonal variability were detected in Ulva (7.3 2.6 g1 dry wt.) and Gracilaria (6:9 6:2 g1 dry wt.) at the Celestia and Lido inlet stations. The Pb ranges quoted by Moore and Ramamoorthy (1984) for estuarine and coastal marine species show, for heavily polluted areas, values up to 170 lg g1 dry wt. Malea and Haritonidis (2000) report for Ulva Pb concentrations up to 3213 g1 dry wt., with mean values
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M. Caliceti et al. / Chemosphere 47 (2002) 443–454
of 748 206 g1 dry wt. The same authors found in Gracilaria Pb values only twice higher than in the Venice samples. In contrast, the concentrations reported by Riget et al. (1995) with reference to Fucus vesiculosus picked up in an unpolluted area were one–two orders of magnitude lower than those detected in this work (0.05–0.70 lg g1 dry wt.). Concentrations determined in Porphyra spp. sampled in industrialized European coastal areas (Leal et al., 1997) are similar to those found in this work. Chromium: The concentrations of this element ranged between 0.3 and 8.6 lg g1 dry wt.; the highest mean concentrations were determined in Ulva, which was the seaweed showing the highest seasonal variability. Orders of 10 lg g1 were detected in seaweeds collected in unpolluted areas; values of 103 lg g1 wet wt. were recorded in high Cr-contaminated areas (Dahab et al., 1990). The values found in Ulva were similar to those found by Malea and Haritonidis (2000). Arsenic: The concentrations of As refer to the total element content. The range was rather wide, 0–360 lg g1 dry wt. The highest values were detected in Cystoseira barbata, a brown seaweed whose seasonal variability (50%) was considerably higher than its spatial difference (6–13%). It is possible to individualize a pollution gradient among the seaweed taxa: brown seaweeds > red seaweeds > green seaweeds. Generally, seaweeds shown high As content and especially brown seaweeds are known to accumulate As hundred times as much as land plants (Keiji and Kanji, 1989). Residues detected in Fucus serratus in highly contaminated waters reached 54 lg g1 dry wt. This value is in accordance with the one detected in Fucus virsoides
(8–73 lg g1 dry wt.) in the present work. The values of five attached species in estuarine waters along the SW coast of England were around 59–189 lg g1 dry wt. (Moore and Ramamoorthy, 1984). Heavy metal concentrations in some seaweeds of the Venice lagoon had previously been determined by Sfriso et al. (1994, 1995) and Sfriso (2000) in two stations (Alberoni and San Giuliano) very similar to the Lido inlet and Ponte della Libert a, respectively. An analysis of the considered species is possible by comparing the data reported in this work with those reported by Sfriso et al. (1995), as Sfriso, 2000 values refer only to Ulva. Ulva and Gracilaria were considered to be the most representative (Fig. 3). As arsenic had not been detected in 1994 and 1995, it was not included in the comparison. The only values relative to As in Ulva are those detected by Sfriso (2000). They ranged from 4 to 65 lg g1 , with a mean of 30 lg g1 and a great deal of variability (83%) among samples collected in different sites and periods. The As concentration was three times as high as the one detected in the present work. With reference to the considered species, metal concentrations are comparable to those detected by Sfriso et al. (1994). At San Giuliano and Ponte della Libert a the seaweed contamination was higher than at Alberoni and Lido inlet, except for Pb, Ni and Cr. However, from data obtained in 1994 and 2000, it is possible to point out a generalized decrease in metal concentrations, with the exception of Pb which was recorded to increase. The generalized depletion of metals linked to industrial activities suggests a reduced contamination impact of Porto Marghera industrial district. On the contrary, the increased lead concentration increase reveals the
Fig. 3. Comparison between values (lg g1 , dry wt.) found in Ulva and Gracilaria detected at Lido inlet and Ponte della Liberta and values found by Sfriso (2000) in two analogous stations: Alberoni and San Giuliano.
8 9 n.d. 32 12 6 18 15 10 5 12 21 5 2 1 6 17.6 6.3 n.d. 3.6 16 0.7 21 7 2.3 1.1 6 3 6 8 5.7 3.4 2.3 5 n.d. 1.0 2.5 3 1.9 2 3.2 2.7 1.3 0.7 2.5 2.2 0.5 0.8 0 0.1 n.d. 0.1 0.1 0.2 0.4 0.6 0.1 0.3 0.4 0.5 0.2 0.7 0.2 0.4 11 8 n.d. 4 4 10 12 10 9 13 5 8 11 29 6 11 30 25 n.d. 36 43 28 240 166 32 33 200 162 104 179 140 198 Gracilaria
Ulva
I II I II
P
1340 1630 1400 1170 1334 217 173 1460 400 380 1080 n.d. 430 224 357 424
As Pb Ni Cd Cu Zn Fe
dry wt.
T
C
L
P
T
C
L
P
T
C
L
P
T
C
L
P
T
C
L
P
T
C
L
P
T
C
L
451
lg g1
Ulva and Gracilaria comparison among the four sampling sites (P ¼ Ponte della Liberta, T ¼ Tronchetto, C ¼ Celestia, L ¼ Lido inlet). I ¼ first sampling period; II ¼ second sampling period; n.d: ¼ not determined
importance of gasoline combustion as a source of this contamination (leaded gasoline will be available in Italy till Dec. 31, 2001). The concentrations of heavy metals in Ulva and Gracilaria can be used to investigate possible spatial trends in the lagoon of Venice, since Gracilaria and Ulva are the only species available in all the sampling stations (Table 4) of the present work. Zinc, Cu and Cd concentrations showed, in fact, a decreasing trend in samples taken in stations from the inner lagoon towards the sea Lido inlet. For Zn this depletion was almost of one order of magnitude. For Cu and Cd the same trend resulted evident during the autumn sampling session. On the contrary, Pb concentrations at the Celestia and the Lido inlet stations resulted to be higher than in the other stations. As for As, it seems possible to exclude that the industrial area could be a contamination source since the highest values were found at the Celestia and Tronchetto stations. It is known that As has been employed as a colorant agent by the glass-factories located on the island of Murano, which is rather close to the Celestia sampling station. Existing correlations between elements were also investigated (Table 5). The highest correlation indices refers to Fe–Cr. The results (r ¼ 54, p < 0:05, N ¼ 29) were similar to those found by Sfriso et al. (1995). The use of metallurgical grade chromite in the production of iron-alloys is reported (Moore and Ramamoorthy, 1984) as a source of these two contaminants; thus a common industrial origin could be a probable reason for this correlation. Iron and Pb concentrations were also significantly correlated. Moore and Ramamoorthy (1984) reported that the main discharges of Pb are linked to oil and gasoline combustion, secondarily to non-ferrous metal production and iron steel production. The same relationship (r ¼ 90, p < 0:05, N ¼ 29) was also observed by Sfriso et al. (1995). This paper also reports the sediment concentrations in the sampling areas. The correlation found for the concentrations of these elements in the sediment was significant but negative (r ¼ 0:92, p < 0:05, N ¼ 24). Such an evidence seems to exclude a common origin of the contamination, on the contrary it suggests a common dispersion mechanism in solution and/or an analogous uptake strategy by seaweeds. Correlations Cd–Zn and Cd–Cu were also significant, as well. By analyzing the values reported in literature, similar correlations were found by Kureishy (1991) (r ¼ 1:00 and 0.92, respectively, for p < 0:05 and N ¼ 35) and Karez et al. (1994) (r ¼ 0:92, p < 0:05, N ¼ 14). Sfriso et al. (1995) found significant Cd–Zn and Cd– Cu correlations in the surface sediment of the Venice lagoon. The probable reasons for these results are to be found in the relative position of these elements in the periodic table of the elements which implies a similar chemical behavior and the common origin from
Table 4
M. Caliceti et al. / Chemosphere 47 (2002) 443–454
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Table 5 Correlation matrix relative to concentration values detected for 30 observations Variable Fe Zn Cu Cd Pb Ni Cr As a
Correlations Fe
Zn
Cu
Cd
Pb
Ni
Cr
As
1.00 0.19 0.33 0.08 0.59a 0.34 0.72a 0.23
1.00 0.31 0.44a 0.15 0.23 0.00 0.30
1.00 0.46a 0.22 0.21 0.51a 0.28
1.00 0.06 0.28 0.07 0.26
1.00 0.09 0.35 0.18
1.00 0.52a 0.06
1.00 0.17
1.00
Values significative for p > 0:05 and N ¼ 30.
sphalerite processing. The correlations and trends of Cd and Cu, as reported by Malea and Haritonidis (2000), but also of Zn could also reflect the seaweed growth dynamics showing lower concentrations in spring when the growth rate is faster and higher values in autumn when seaweed populations are older and the growth rate is reduced. Whereas a significant correlation is reported in the literature for Ni–Cr (r ¼ 0:96, p < 0:05, N ¼ 4; Tariq et al., 1993), for the pair Cu–Cr no analogous relevant relationships were found. A probable common origin for Ni and Cr could be the production and use of Ni–Cr stainless steel. Moore and Ramamoorthy (1984) attributed these correlations to the large use of Ni–Cr alloys in the heating elements of domestic stoves and industrial furnaces.
As contamination because the mean concentration ratio with the other considered species ranged from 35 (Ulva) to 3.5 (Undaria). 5. By considering Ulva and Gracilaria, the only seaweeds collected in all sampling sites, Zn and Cd were significantly correlated and showed a decreasing trend from the inside of the lagoon to the outside. Such a behavior suggests a common industrial source. 6. The generalized decrease in metal concentrations, except for Pb, in seaweed tissues during the last five years is in accordance with the trend observed for nutrients and other pollutants in the surface sediments. Conversely, the Pb increase suggests the relevance of leaded gasoline combustion as the main source of contamination for this element.
Acknowledgements 4. Conclusions By these results it is possible to conclude that: 1. The heavy metal contamination of the considered seaweed species was in ranges comparable to those reported in the literature for industrialized coastal areas. 2. Porphyra and Undaria show the lowest heavy metal contamination. As these seaweeds are seasonal, it is evident that time exposure is a key factor in the metal uptake. 3. Ulva exhibited the highest contamination for many of the considered metals, i.e. Fe, Cu, Pb and Cr, and together with Fucus the highest values of Cd and Ni. Ulva, a species abundantly spread in the whole lagoon and not used for the animal and human nutrition, could be employed as environmental biomonitor. 4. Cystoseira displayed the highest values for As. This species could be used as an excellent indicator for
This work was partly supported by the Consorzio Ricerche Lagunari, (CORILA, Consortium for the coordination of the scientific research on the Lagoon of Venice). The authors are grateful to Mrs. Sonia Ceoldo for technical assistance and to Dr. Orietta Zucchetta for reviewing the English text.
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