Heavy metals in benthic organisms from Todos os Santos Bay, Brazil/Metais pesados em organismos bentonicos da Baia de Todos os Santos, Brasil.
In contaminated environments, more important than the total load of contaminants, is the bioavailability. According to Phillips and Rainbow (1993), bioavailability can only be measured appropriately by what is found in the tissues of a target organism. Moreover, despite the importance of the chemical species of the contaminant or the abiotic conditions of the environment, bioaccumulation is a biological property and relates directly to the target organism (Beeby, 2001). Thus, it is imperative to use several organisms to evaluate environmental contamination, assessing different uptake capabilities of diverse chemical species and reservoirs.
In marine coastal zones, seagrasses and seaweeds are more exposed to the dissolved fraction of contaminants, and bivalve mollusks to the suspended particles (Rainbow, 1995). For tropical Western Atlantic coastal areas previous studies have shown three benthic organisms as good bioaccumulators of metals: the oyster Crassostrea rhizophorae (Guilding, 1828) exhibits high filtration rates of suspended particles and a high metal bioaccumulation capability (Lima et al., 1986; Wallner-Kersanach et al., 2000; Rebelo et al., 2003), the brown seaweeds, specially Padina gymnospora (Kuetzing) Sonder, 1871 exhibit high capability of accumulating metals from the dissolved fraction of water column (Amado Filho et al., 1999) and the seagrass Halodule wrightii Ascherson, 1868, which is an important contributor to primary production (Klumpp and Van der Valk, 1984), take up metals from both water, through leaf surfaces, and from sediment and interstitial water, by way of their roots (Pulich, 1980; Amado Filho et al., 2004).
Todos os Santos Bay--TSB (13[degrees] S and 38[degrees] W) is the largest tropical bay in Brazil with an area of about 1,000 [km.sup.2] (Figure 1) situated in the state of Bahia (BA). This bay is impacted by the presence of a large metropolitan area (the city of Salvador with 2,600,000 habitants) and industrial activity that includes chemical and petrochemical plants as well as an oil refinery and harbor activities located in the North and Northeastern area of the bay. It also receives discharges from Subae River (Figure 1), which drains an industrial area containing a lead smelter plant, a paper mill and alcohol distilleries. Water circulation is mainly controlled by tide (Lessa et al., 2001). TBS is also an important center of tourism and shell-fishing activities that take place throughout the whole bay. The most important ecosystems are the mangroves situated in the northern part of the bay. There are also reefs in several regions of the bay. Although it's considered ecologically important, there is little data available concerning metal contamination in organisms from TSB. The mollusks Anomalocardia brasiliana (Gmelin, 1791), Brachidontes exustus (Linnaeus, 1758) and Crassostrea rhizophorae were analyzed for their metal content in TSB (Tavares, 1983, Wallner-Kersanach et al., 1994; 2000) and it was shown that differences between TSB area and control sites were detected only for C. rhizophorae.
[FIGURE 1 OMITTED]
Our aim was to assess the heavy metals contamination in the north and northeastern areas of TSB these being the main areas affected by industrial activities. This was done by analysis of metal concentrations in marine benthic organisms: Crassostrea rhizophorae which is a typical sentinel organism (Lima et al., 1986; Wallner-Kersanach et al., 2000; Rebelo et al., 2003) abundant in the mangroves and reefs along the coast, the seagrass Halodule wrightii, which forms extensive beds on the shallow sea bottom (Amado Filho et al., 2004) and Padina gymnospora and Sargassum sp., two abundant seaweed species in Brazilian tropical areas (Karez et al., 1994a; Amado Filho et al. 1999).
2. Material and Methods
Organism samples were collected in 3 sites, Botelho, Paramana and Tapera located near industrial areas in the north and the northeastern regions of the Bay (Figure 1). Oyster samples were analyzed only for Botelho and Tapera because populations of this species were not found in Paramana. Samples were collected at the end of rainy season in August of 2000. In order to verify a seasonal effect in organism metal concentrations, samples of C. rhizophorae and P. gymnospora were re-collected in Botelho at the end of the dry season in February of 2001.
Macrophyte Halodule wrightii samples were collected at 2 m depth, washed and cleaned in seawater accordingly to Amado Filho et al. (2004). Roots, rhizomes and leaves were separated manually. About 3 g (wet weight) of each plant compartment were washed in seawater and in distilled water and dried at 60 [degrees]C to constant weight. The seaweeds Padina gymnospora and Sargassum sp. were cleaned of epiphytes, washed in seawater, then in distilled water, dried at 60[degrees]C to constant weight (at least 1 g) and then homogenized in porcelain mortar. Around 20 specimens of Crassostrea rhizophorae with similar shell lengths (3.5 cm) and at the same tidal height (low tide) were collected at each station. Soft tissues were removed from the shells and entirely homogenized and dried at 60[degrees]C to constant weighed and ashed (48 hours at 400[degrees]C). The samples were digested accordingly Lacerda et al. (1987) with concentrated HNO3 (Merck, 65%) and HCl (Merck, 37%) until complete dissolution of the organic tissues. The resulting solution was evaporated and re-dissolved in 0.1 N HCl.
The concentrations of Al, Cd, Cr, Cu, Fe, Mn, Ni, Pb and Zn were determined by Atomic Absorption Spectrophometry (Varian AA-1475) in triplicate samples and the results expressed in [micro]g.[g.sup.-1] (dry weight). Standard samples from IAEA-140 (Sea plant homogenate, Fucus) and NIST 296 (Mussel) were analyzed and retrieval corresponded to a minimal of 90% of the reference values.
One-Way Analysis of Variance (ANOVA) was used to compare metal concentrations between parts of Halodule wrightii and among sampling sites. Differences were considered significant when p < 0.05 (STATISCA 4.2). Comparisons between obtained data of metal concentrations of TSB organisms and previous published works were done taking in account uniformity in body size, stage of the life cycle, and season of the year.
3. Results and Discussion
Average metal concentrations in biological samples are presented in Table 1. Among the organisms sampled in TSB, C. rhizophorae exhibited the highest concentrations for Cu (526.1 [+ or -] 153.8 [micro]g.[g.sup.-1]), Cd (8.29 [+ or -] 2.43 [micro]g.[g.sup.-1]), Ni (1990.9 ??91.4 [micro]g.[g.sup.-1]) and Zn (4733 [+ or -] 1291 [micro]g.[g.sup.-1]); while H. wrightii exhibited the highest concentrations for Cr (12.2 [+ or -] 4.9 [micro]g.[g.sup.-1]), Fe (5664 [+ or -] 460 [micro]g.[g.sup.-1]), Mn (803.5 [+ or -] 47.8 [micro]g.[g.sup.-1]) and Pb (13.6 [+ or -] 2.0 [micro]g.[g.sup.-1]); and P. gymnospora exhibited significantly higher values for Al (4412 [+ or -] 133 [micro]g.[g.sup.-1]).
The concentrations for the nine metals analyzed in H. wrightii population from TSB exhibited differences among plant compartments (roots, rhizomes and shoots) and sampling sites (ANOVA, p < 0.05). In relation to plant compartments, considerably higher concentrations were observed in the roots for eight metals (except for Mn) when compared to the rhizomes. Concentrations were also notably higher in roots for six metals (except Cd, Cu and Pb) when compared to shoots. Concentrations were significantly higher in the rhizomes compared to shoots for Cr, Fe, Mn and Pb.
The observed trend of higher metal concentrations in roots than rhizomes and shoots, suggests that H. wrightii roots are the main compartment for metal accumulation, reflecting the metal concentration and availability in the sediment pore waters. On the other hand, Mn which presented an elevated concentration in the shoots, has been noted in other seagrass species as a metal that tends to be accumulated in a higher degree in shoots, as was pointed out by Malea (1994), Sanchiz et al. (1999) and Prange and Dennison (2000).
In the comparison of the sample sites, it was found that samples from Botelho exhibited significantly higher concentrations than Paramana or Tapera for Al (root), Cd (root), Cu (root, rhizome and shoot), Fe (root, rhizome and shoot), Mn (rhizome and shoot) and Zn (root and shoot); Tapera presents higher concentrations than Paramana of Al (root) and Mn (shoots). No differences were detected in Cr, Ni and Pb concentrations among the three sample sites.
In relation to the metal concentrations in seaweeds, the same trend observed in the seagrass of highest metal concentrations in Botelho was seen. P. gymnospora presented significantly higher concentrations of Al, Cu, Fe, Mn and Zn in Botelho and Cd in Tapera. Sargassum spp. presented higher concentrations of Cr in Botelho, Cd in Tapera and Cu and Mn in Paramana.
In oyster samples, differences between sites were seen in the following metals, Cd, Cr, Cu, Fe, Ni, Zn. Higher concentrations of Cr, Cu, Ni and Zn were observed in Botelho and higher concentrations of Cd and Fe were observed in Tapera.
The observed trend of higher metal concentrations in samples from Botelho can be related to the localization of this site in front of Cotegipe Channel. This channel connected the Aratu Bay (Figure 1) to TSB. Most industries are situated in the northern part of the Aratu Bay. Direct anthropogenic contributions from the Cotegipe Channel originate from an ore terminal, harbor activities of naval vessels and offshore oil rig repairs, and transport of organic products (Wallner-Kersanach et al., 2000).
Even though there was a general trend of higher metal concentration in both P. gymnospora and C. rhizophorae observed in the rainy season (2000) when compared to the dry season (2001) (Table 1), no significant difference (p < 0.05) was detected between both seasons, and the levels of all analyzed metals were maintained in the same range. The available data about salinity of TSB indicates that the main portion of the Bay is dominated by typical marine conditions (range of 33.0 and 36.7 PSU) that don't change seasonally (Wolgemuth et al., 1981; Lessa et al., 2001). In this way, the levels of metal accumulated by benthic organisms of the studied sites should be more related to the load of metals to the Bay system by the anthropogenic inputs than natural seasonal changes of abiotic parameters.
A comparison between the obtained data with other results of contaminated Brazilian coastal areas by using the same studied species shows that the metals Cd, Cu and Ni from TSB were in the similar range of concentrations (Amado Filho et al., 1999; Rebelo et al., 2003). The higher Cd concentrations of 1.56 [micro]g.[g.sup.-1] in seagrass, 1.64 [micro]g.[g.sup.-1] in seaweed and 8.29 [micro]g.[g.sup.-1] in oyster are similar to that concentrations found in Sepetiba Bay (H. wrightii = 0.4-1.5 [micro]g.[g.sup.-1], Amado Filho et al., 2004; P. gymnospora 1.0-2.7 [micro]g.[g.sup.-1], Amado Filho et al., 1999; C. rhizophorae = 1.3-29.8 [micro]g.[g.sup.-1], Rebelo et al., 2003), which have been studied due to the impact of a Cd and Zn smelting plant. Cadmium concentrations found in TSB samples are higher than that found in non contaminated Brazilian coastal areas (H. wrightii = 0.2-0.3 [micro]g.[g.sup.-1], Amado Filho et al., 2004; P. gymnospora = 0.30-0.42 [micro]g.[g.sup.-1], Karez et al., 1994a; C. rhizophorae = 0.8-2.3 [micro]g.[g.sup.-1], Rebelo et al., 2003). The Cu concentrations of 32.2 [micro]g.[g.sup.-1] in seagrass, 32.4 [micro]g.[g.sup.-1] in seaweed and 526.1 [micro]g.[g.sup.-1] in oysters were higher than those observed in Cu contaminated areas, like Guanabara Bay (P. gymnospora = 13.6 ??0.9 [micro]g.[g.sup.-1], Karez et al., 1994b; C. rhizophorae = 148 [micro]g.[g.sup.-1], Carvalho and Lacerda, 1992) and the Potengi River Estuary (C. rhizophorae = 234 ??55 [micro]g.[g.sup.-1], Silva et al., 2001) and other less contaminated areas (H. wrightii = 4.0-14.1 [micro]g.[g.sup.-1], Amado Filho et al., 2004). Among the three considered organisms only the oysters exhibited higher Ni concentrations. In relation to other Brazilian coastal areas, Ni concentrations in oyster found at TSB (531.8-1990.1 [micro]g.[g.sup.-1]) were two order of magnitude higher than previously reported values (15-20 [micro]g.[g.sup.-1], Carvalho et al., 1991 and Pfeiffer et al., 1985). Wallner-Kersanach et al. (2000) who carried out transplant experiments with C. rhizophorae populations of TSB during the year of 1991, analyzed Cd, Cu, Pb and Zn in oysters from Cotegipe Channel (Figure 1). Comparison of data between 1991 and 2000 showed similar concentrations of Cu and Zn and an increase of Cd and Pb concentrations in 2000.
When wet weight is considered, the concentrations of Cu and Ni in oysters from TSB exceeded the limits recommended for human consumption according to the Brazilian Health Agency (Cu and Ni < 2.0 [micro]g.[g.sup.-1] wet weight). As oysters and other mollusks are used as food sources by the local population, the contaminated oysters of TSB may constitute a health risk for this population.
In addition to previous results of metal concentrations in oysters (Wallner-Kersanach et al. 2000), the obtained data from TSB indicates that Cd and Cu concentrations were in range of contaminated coastal areas. This conclusion is supported by levels of Cd and Cu in seaweeds, seagrass and oysters. Cadmium and Cu are available to organisms through suspended particles, dissolved fraction in the water column and bottom sediment interstitial water. Although the observed result of Ni in oysters indicates elevated concentration, they were not supported by results in other organisms, suggesting that more evidence is needed to confirm this element as a contaminant in TSB. In summary, our results show the usefulness of analyzing different organisms that can take up metals from different ecosystem compartments and that a heavy metals biomonitoring program has to be implemented in the marine biota of TSB.
Acknowledgments--This study was financially supported by the Brazilian Program PRONEX/MCT and by research grants from the Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq-Brazil) to GM Amado Filho (521688/96-5) and CE Rezende (420110/97-6).
Received April 10, 2006--Accepted July 17, 2006--Distributed February 29, 2008 (With 1 figure)
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Amado-Filho, GM. (a) *, Salgado, LT. (a), Rebelo, MF. (b), Rezende, CE. (c), Karez, CS. (d), and Pfeiffer, WC. (b)
(a) Programa Zona Costeira, Instituto de Pesquisas Jardim Botanico do Rio de Janeiro, Rua Pacheco Leao, 915, CEP 22460-030, Rio de Janeiro, RJ, Brazil
(b) Laboratorio de Radioisotopos, Instituto de Biofisica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, CEP 22949-900, Rio de Janeiro, RJ, Brazil
(c) Laboratorio de Ciencias Ambientais, Centro de Biociencias e Biotecnologia, Universidade Estadual do Norte Fluminense, Av. Alberto Lamego 2000, CEP 28023-602, Campos dos Goytacazes, RJ, Brazil
(d) Programa de Ciencias Ecologicas y de la Tierra, Oficina Regional de Ciencia para America Latina y el Caribe, UNESCO, Calle Luis Piera 1992, 2. Piso, 11000 Montevideo, Uruguay
* e-mail: email@example.com
Table 1. Mean ([+ or -] standard deviation) metal concentrations ([micro]g.[g.sup.-1] dry weight) in seagrass (H. wrightii) seaweeds (P. gymnospora, and Sargassum sp.) and bivalve mollusk (Crassostrea rhizophorae) from the collected sites of Todos os Santas Bay. Species Sites Tissue Al Halodule Botelho Root 4236 [+ or -] 153 wrigthii Rhizome 1432 [+ or -] 28 Leave 1266 [+ or -] 239 Paramana Root 2846 [+ or -] 258 Rhizome 1160 [+ or -] 85 Leave 747 [+ or -] 282 Tapera Root 4435 [+ or -] 458 Rhizome 1487 [+ or -] 280 Leave 933 [+ or -] 113 Padina Botelho Entire 4412 [+ or -] 133 gymnospora Paramana Entire 2744 [+ or -] 305 Tapera Entire 2774 [+ or -] 258 Sargassum sp. Botelho Entire 2688 [+ or -] 601 Paramana Entire 2454 [+ or -] 226 Tapera Entire 2844 [+ or -] 479 Crassostrea Botelho Entire 4.3 [+ or -] 2.9 rhizophorae Tapera Entire 5.3 [+ or -] 1.6 Padina Botelho Entire 2744 [+ or -] 305 gymnospora * Crassostrea Botelho Entire 3.6 [+ or -] 0.8 rhizophorae * Species Sites Tissue Cd Halodule Botelho Root 1.56 [+ or -] 0.18 wrigthii Rhizome 0.70 [+ or -] 0.55 Leave 0.79 [+ or -] 0.05 Paramana Root 1.01 [+ or -] 0.05 Rhizome 0.78 [+ or -] 0.08 Leave 1.21 [+ or -] 0.15 Tapera Root 0.90 [+ or -] 0.28 Rhizome 0.80 [+ or -] 0.14 Leave 0.60 [+ or -] 0.10 Padina Botelho Entire 1.03 [+ or -] 0.18 gymnospora Paramana Entire 1.01 [+ or -] 0.11 Tapera Entire 1.64 [+ or -] 0.19 Sargassum sp. Botelho Entire 1.29 [+ or -] 0.28 Paramana Entire 0.40 [+ or -] 0.06 Tapera Entire 1.45 [+ or -] 0.26 Crassostrea Botelho Entire 8.29 [+ or -] 2.43 rhizophorae Tapera Entire 2.71 [+ or -] 0.58 Padina Botelho Entire 1.10 [+ or -] 0.13 gymnospora * Crassostrea Botelho Entire 6.98 [+ or -] 0.75 rhizophorae * Species Sites Tissue Cr Halodule Botelho Root 12.2 [+ or -] 4.9 wrigthii Rhizome 6.1 [+ or -] 0.4 Leave 5.0 [+ or -] 0.8 Paramana Root 10.3 [+ or -] 0.4 Rhizome 2.4 [+ or -] 0.2 Leave 1.0 [+ or -] 0.0 Tapera Root 8.8 [+ or -] 0.7 Rhizome 8.6 [+ or -] 1.4 Leave 2.2 [+ or -] 0.3 Padina Botelho Entire 5.5 [+ or -] 0.3 gymnospora Paramana Entire 7.2 [+ or -] 1.9 Tapera Entire 6.0 [+ or -] 1.5 Sargassum sp. Botelho Entire 9.0 [+ or -] 0.5 Paramana Entire 7.3 [+ or -] 0.7 Tapera Entire 1.5 [+ or -] 0.3 Crassostrea Botelho Entire 2.5 [+ or -] 0.7 rhizophorae Tapera Entire 4.5 [+ or -] 0.6 Padina Botelho Entire 5.9 [+ or -] 1.0 gymnospora * Crassostrea Botelho Entire 2.2 [+ or -] 0.6 rhizophorae * Species Sites Tissue Cu Halodule Botelho Root 32.2 [+ or -] 2.5 wrigthii Rhizome 15.5 [+ or -] 0.4 Leave 26.3 [+ or -] 1.0 Paramana Root 9.1 [+ or -] 0.3 Rhizome 5.5 [+ or -] 0.6 Leave 10.9 [+ or -] 0.2 Tapera Root 9.2 [+ or -] 1.2 Rhizome 7.1 [+ or -] 0.5 Leave 7.2 [+ or -] 0.1 Padina Botelho Entire 32.4 [+ or -] 1.3 gymnospora Paramana Entire 8.8 [+ or -] 1.2 Tapera Entire 6.6 [+ or -] 0.4 Sargassum sp. Botelho Entire 6.5 [+ or -] 0.9 Paramana Entire 16.8 [+ or -] 0.5 Tapera Entire 6.0 [+ or -] 0.4 Crassostrea Botelho Entire 276.1 [+ or -] 129.7 rhizophorae Tapera Entire 526.1 [+ or -] 153.8 Padina Botelho Entire 28.8 [+ or -] 1.2 gymnospora * Crassostrea Botelho Entire 224.6 [+ or -] 44.5 rhizophorae * Species Sites Tissue Fe Halodule Botelho Root 5664 [+ or -] 460 wrigthii Rhizome 2800 [+ or -] 234 Leave 661 [+ or -] 140 Paramana Root 2826 [+ or -] 84 Rhizome 955 [+ or -] 87 Leave 331 [+ or -] 132 Tapera Root 4160 [+ or -] 355 Rhizome 1737 [+ or -] 137 Leave 447 [+ or -] 61 Padina Botelho Entire 1967 [+ or -] 15 gymnospora Paramana Entire 1304 [+ or -] 109 Tapera Entire 1248 [+ or -] 153 Sargassum sp. Botelho Entire 1234 [+ or -] 236 Paramana Entire 1100 [+ or -] 115 Tapera Entire 1502 [+ or -] 326 Crassostrea Botelho Entire 330 [+ or -] 48 rhizophorae Tapera Entire 924 [+ or -] 133 Padina Botelho Entire 1807 [+ or -] 109 gymnospora * Crassostrea Botelho Entire 260 [+ or -] 22 rhizophorae * Species Sites Tissue Mn Halodule Botelho Root 16.1 [+ or -] 3.0 wrigthii Rhizome 102.5 [+ or -] 7.4 Leave 803.5 [+ or -] 47.8 Paramana Root 23.9 [+ or -] 2.0 Rhizome 17.6 [+ or -] 0.1 Leave 115.0 [+ or -] 4.2 Tapera Root 42.7 [+ or -] 1.5 Rhizome 29.5 [+ or -] 4.5 Leave 149.0 [+ or -] 13.9 Padina Botelho Entire 630.4 [+ or -] 43.1 gymnospora Paramana Entire 350.1 [+ or -] 24.0 Tapera Entire 584.6 [+ or -] 17.4 Sargassum sp. Botelho Entire 93.7 [+ or -] 5.9 Paramana Entire 334.9 [+ or -] 21.2 Tapera Entire 126.7 [+ or -] 8.2 Crassostrea Botelho Entire 16.4 [+ or -] 1.6 rhizophorae Tapera Entire 17.1 [+ or -] 1.8 Padina Botelho Entire 709.1 [+ or -] 62.0 gymnospora * Crassostrea Botelho Entire 16.1 [+ or -] 1.2 rhizophorae * Species Sites Tissue Ni Halodule Botelho Root 8.2 [+ or -] 2.7 wrigthii Rhizome 5.3 [+ or -] 0.3 Leave 5.6 [+ or -] 0.1 Paramana Root 8.0 [+ or -] 1.7 Rhizome 4.5 [+ or -] 0.5 Leave 4.4 [+ or -] 1.6 Tapera Root 6.8 [+ or -] 1.2 Rhizome 6.2 [+ or -] 1.6 Leave 6.3 [+ or -] 0.3 Padina Botelho Entire 11.7 [+ or -] 0.7 gymnospora Paramana Entire 7.8 [+ or -] 2.9 Tapera Entire 9.8 [+ or -] 1.5 Sargassum sp. Botelho Entire 9.1 [+ or -] 1.0 Paramana Entire 8.5 [+ or -] 0.7 Tapera Entire 9.7 [+ or -] 1.4 Crassostrea Botelho Entire 531.8 [+ or -] 92.2 rhizophorae Tapera Entire 1990.9 [+ or -] 91.4 Padina Botelho Entire 11.4 [+ or -] 1.2 gymnospora * Crassostrea Botelho Entire 499.2 [+ or -] 28.4 rhizophorae * Species Sites Tissue Pb Halodule Botelho Root 13.6 [+ or -] 2.0 wrigthii Rhizome 6.7 [+ or -] 1.6 Leave 12.8 [+ or -] 0.7 Paramana Root 13.2 [+ or -] 1.5 Rhizome 5.1 [+ or -] 0.8 Leave 11.0 [+ or -] 1.5 Tapera Root 12.0 [+ or -] 3.2 Rhizome 10.8 [+ or -] 1.4 Leave 7.8 [+ or -] 0.9 Padina Botelho Entire 9.0 [+ or -] 0.5 gymnospora Paramana Entire 6.1 [+ or -] 0.7 Tapera Entire 8.7 [+ or -] 1.4 Sargassum sp. Botelho Entire 8.5 [+ or -] 1.5 Paramana Entire 11.1 [+ or -] 2.5 Tapera Entire 6.2 [+ or -] 0.7 Crassostrea Botelho Entire 6.6 [+ or -] 2.0 rhizophorae Tapera Entire 4.5 [+ or -] 1.3 Padina Botelho Entire 11.4 [+ or -] 1.2 gymnospora * Crassostrea Botelho Entire 6.2 [+ or -] 1.1 rhizophorae * Species Sites Tissue Zn Halodule Botelho Root 23.0 [+ or -] 3.1 wrigthii Rhizome 30.1 [+ or -] 3.5 Leave 37.2 [+ or -] 1.4 Paramana Root 13.0 [+ or -] 0.1 Rhizome 21.1 [+ or -] 2.4 Leave 23.2 [+ or -] 4.2 Tapera Root 16.3 [+ or -] 7.5 Rhizome 26.1 [+ or -] 7.3 Leave 17.7 [+ or -] 3.2 Padina Botelho Entire 42.6 [+ or -] 7.4 gymnospora Paramana Entire 24.4 [+ or -] 14.3 Tapera Entire 18.4 [+ or -] 1.7 Sargassum sp. Botelho Entire 13.5 [+ or -] 0.8 Paramana Entire 27.1 [+ or -] 6.7 Tapera Entire 13.7 [+ or -] 6.7 Crassostrea Botelho Entire 2099 [+ or -] 501 rhizophorae Tapera Entire 4733 [+ or -] 1291 Padina Botelho Entire 54.3 [+ or -] 5.5 gymnospora * Crassostrea Botelho Entire 1890 [+ or -] 160 rhizophorae * * Results obtained in February 2001.