Water Air Soil Pollut (2011) 221:137–144 DOI 10.1007/s11270-011-0776-y Biosorption Capacity for Cadmium of Brown Seaweed Sargassum sinicola and Sargassum lapazeanum in the Gulf of California Mónica Patrón-Prado & Margarita Casas-Valdez & Elisa Serviere-Zaragoza & Tania Zenteno-Savín & Daniel B. Lluch-Cota & Lía Méndez-Rodríguez Received: 13 September 2010 / Accepted: 16 February 2011 / Published online: 4 March 2011 # Springer Science+Business Media B.V. 2011 Abstract Brown algae Sargassum sinicola and Sargassum lapazeanum were tested as cadmium biosorbents in coastal environments close to natural and enriched areas of phosphorite ore. Differences in the concentration of cadmium in these brown algae were found, reflecting the bioavailability of the metal ion in seawater at several sites. In the laboratory, maximum biosorption capacity (qmax) of cadmium by these nonliving algae was determined according to the Langmuir adsorption isotherm as 62.42±0.44 mg g−1 with the affinity constant (b) of 0.09 and 71.20±0.80 with b of 0.03 for S. sinicola and S. lapazeanum, respectively. Alginate yield was 19.16±1.52% and 12.7±1.31%, respectively. Although S. sinicola had far lower biosorption capacity than S. lapazeanum, the affinity for cadmium for S. sinicola makes this alga more suitable as a bio- M. Patrón-Prado : E. Serviere-Zaragoza : T. Zenteno-Savín : D. B. Lluch-Cota : L. Méndez-Rodríguez (*) Centro de Investigaciones Biológicas del Noroeste (CIBNOR), Mar Bermejo 195, Col. Playa Palo de Santa Rita, La Paz, Baja California Sur 23090, Mexico e-mail: lmendez04@cibnor.mx M. Casas-Valdez Centro Interdisciplinario de Ciencias Marinas-IPN (CICIMAR-IPN), Av. Instituto Politécnico Nacional S/N. Col., La Paz, Baja California Sur 23096, Mexico sorbent because of its high qmax and large biomass on the eastern coast of the Baja California Peninsula. Sargassum biomass was estimated at 180,000 t, with S. sinicola contributing to over 70%. Keywords Alginate . Biosorption . Cadmium . Gulf of California . Sargassum 1 Introduction Cadmium in the environment has being increasing because of its use in industrial and agricultural activities (Rule et al. 2006). High solubility in water enhances wide distribution in aquatic systems (Lockwood 1976). One of the most important sources of cadmium in aquatic ecosystems is mineral deposits, including phosphorite, in which this element is a common impurity (Mann and Ritchie 1995). One of the largest phosphorite deposits in the world is located in the Baja California Peninsula of Mexico (Riley 1989). A phosphorite mine is located close to the coast, about 50 km northwest of the city of La Paz (COREMI 2000). Previous reports regarding marine sediments and clams sampled near this area showed high cadmium levels at some sites that results upwelling currents, runoff, municipal wastewater and mining (Méndez et al. 1998; 2006). Efficient and affordable technologies to remove cadmium from water effluents include physicochemical and biological methods. Among the biological technologies, biosorp- 138 tion processes are useful because they are efficient and relatively inexpensive (Vieira and Volesky 2000). Biosorption processes use the ability of organisms to absorb heavy metals from water. Bacteria, fungi, yeast, and algae biomass, among other organisms, have high removal capacities for cadmium (Vieira and Volesky 2000). Brown algae Sargassum spp. are recognized as an effective biosorbent when their nonliving biomass binds heavy metals from contaminated effluents (Schiewer and Volesky 1999; Davis et al. 2003a, b; Lodeiro et al. 2004). Along the central coast of the Baja California Peninsula, Sargassum has the highest biomass in relation to other macroalgae (Pacheco-Ruiz et al. 1998; Casas-Valdez 2009); Huerta-Díaz et al. (2007) determined that Sargassum accumulates large amounts of divalent metals, which suggests that Sargassum could be used for bioremediation in polluted environments. However, no reports of cadmium levels in macroalgae along the shore of Bahía de la Paz are known. The algal cell wall plays an important role in metal binding because it contains high concentrations of polysaccharides (Davis et al. 2003b). The main polysaccharide responsible for absorption of metals in brown macroalgae is alginate (Chapman and Chapman 1980; Davis et al. 2003a, b; Mata et al. 2009). This study measured biosorption capacity of two species of brown seaweeds: Sargassum sinicola and Sargassum lapazeanum for cadmium in batch processing. Additionally, we measured cadmium concentration in both species close to natural and enriched areas of phosphorite and the concentration of alginate in the two species. Those values were compared with cadmium biosorption capacity. 2 Materials and Methods 2.1 Collection Sites Sargassum was collected along the rocky shoreline bordering Bahía de La Paz at Califin in the State of Baja California Sur, Mexico in March 2009 (Fig. 1). Large biomasses of both target species were found at this location. Beds of Sargassum spp. contained 70% S. sinicola and 30% S. lapazeanum (Casas-Valdez 2009). The two species were assayed for cadmium biosorption capacity, concentration of alginate, and concentration of cadmium. Water Air Soil Pollut (2011) 221:137–144 2.2 Cadmium Biosorption Capacity and Concentration of Alginate To analyze cadmium biosorption, the algae were rinsed with fresh water to remove external salt and sand. To remove divalent ions present in the algae and replace them with sodium ions, the biomass was treated by the method described in Hernández-Carmona et al. (1999a) and Patrón-Prado et al. (2010). The algae were washed with 0.1 M nitric acid solution at pH 4 for 15 min under constant agitation. The algal biomass was then filtered and washed with distilled water with slow stirring, while pH 7 was obtained with a solution of 0.1 M NaOH. The algae were filtered and dried until constant weight was reached, then chopped (0.2–0.5-mm fragments), and then stored in polyethylene bags until used. Solutions of cadmium were prepared at concentrations ranging from 5 to 900 mg L−1 by dissolving chloride salts (analytical grade) in distilled water. A 50-mL metallic solution (initial pH=4.5) was placed in a propylene tube containing 0.5-g pretreated macroalgae. The mixtures were stirred in an orbital shaker at 100 rpm for 24 h. The metallic solution was then passed through a 400μm nylon mesh filter. Concentration of cadmium ions in the filtrates was determinate by atomic absorption (AVANTA; GBC Scientific Equipment, Melbourne, Australia) with an air-acetylene flame. All experiments were performed in triplicate. Metal uptake (q) was determined as:  q ¼ V Ci Cf
 =S ð1Þ where q (in milligrams per gram) is the amount of metal ions adsorbed on the sorbent, V (in liters) is the volume of metal-containing solution in contact with the sorbent, Ci and Cf (in milligrams per liter) are the initial and final equilibrium (residual) concentrations of metal ions in the solution, and S (in grams) is the amount of added sorbent on a dry weight basis. The Langmuir adsorption isotherm estimates the maximum metal adsorption by the biosorbent:
 
q ¼ ðqmax ÞðbÞ Cf = 1 þ b  Cf ð2Þ where qmax is the maximum biosorption with complete saturation of the surface, b is a constant related to adsorption/desorption energy, which is a measure of the affinity of the biosorbent for a particular metal ion, and Cf is the final equilibrium concentration, as defined in the previous paragraph. Water Air Soil Pollut (2011) 221:137–144 139 Fig. 1 Study area and sampling sites near La Paz, BCS, Mexico. 1 Tarabillas, 2 San Juan de la Costa, 3 Califin The maximum biosorption capacity (qmax) is not the only parameter that needs to be considered in the screening of different biosorbents. The performance of a specific biosorbent is determined by both qmax and b; therefore, a better comparison among biosorbents is the following equation (Hashim and Chu 2004). S ¼ Ci Cf
 
 
1 þ b  Cf = ½qmax Š½bŠ Cf ð3Þ that combines Eqs. 1 and 2 to estimate the sorbent quantity (S) required to achieve a specified level of metal removal in a batch system. To assay the concentration of alginate, samples of S. sinicola and S. lapazeanum were hand-picked and sun-dried (ambient temperature 35–45°C), pulverized to 0.5 mm in a manual mill, and stored in polyethylene bags in a shaded and ventilated location until used. Alginate contents were estimated in the laboratory of a pilot plant for production of alginate at CICIMAR-IPN, using the following method. Dried and milled algae (10 g) were hydrated with 90 mL 0.1% formaldehyde solution for 12 h. The residual formaldehyde solution was drained, and the algae were washed three times with 150 mL of water, adjusting the pH to 4 with an HCl solution with constant stirring for 15 min during each washing. Alkaline extraction was carried out by placing the algae in 250 mL, adjusting the pH to 10 with 10% Na2SO3 solution. The algae were heated in a water bath at 80°C with constant stirring at 800 rpm for 2 h. The paste obtained was diluted with hot water and vacuum-filtered with diatomaceous earth and Whatman filter paper No. 4 (Hernández-Carmona et al. 1999a, b). The alginic acid fibers were precipitated in ethanol water solution (1:1 v/v) without conversion to calcium alginate (Haug 1965). The concentration of sodium alginate was calculated on a dry weight basis and was used to compare alginate content of the two species. Results are expressed as mean±standard error. 140 Water Air Soil Pollut (2011) 221:137–144 2.3 Concentration of Cadmium Concentrations in Sargassum were measured from samples collected close to the shore of Bahía de La Paz in March 2009 at three sites: Tarabillas, San Juan de La Costa, and Califin, which are north, at, and south of the waste discharged from the phosphorite mine (Fig. 1). Specimens were collected at low tides, rinsed in seawater collected at their respective locations, and placed in labeled polyethylene bags. In the laboratory, the samples were cleaned of sediments, epiphytes, and animals. The algae were dried at 60°C for 24 h and crushed in a mortar to obtain homogeneous material. Individual samples were then digested in acid-washed Teflon tubes with concentrated nitric acid in a microwave oven (CEM Mars 5 microwave oven, Matthews, NC). Samples were analyzed by atomic absorption (AVANTA, GBC Scientific Equipment, Melbourne, Australia) using an air-acetylene flame. Certified standard reference material (IAEA-392, International Atomic Energy Agency, Vienna, Austria) was used for calibration. Analytical values were within the range of certified values; level of recovery of cadmium was 95% of the detection limit (0.0390 mg kg−1). 3 Results and Discussion 3.1 Cadmium Biosorption Capacity and Concentration of Alginate The Langmuir adsorption isotherm model is the most widely used to express quantitatively the relationship between the extent of sorption and the residual solute concentration. Although the assumptions of the model are not fulfilled in the case of biosorption processes, the Langmuir model is a valuable tool for describing and comparing data between different biosorbents (Davis et al. 2003a, b). For S. sinicola, the maximum biosorption capacity (qmax) of cadmium was 62.42± 0.44 mg g−1 with an affinity constant (b) of 0.09. For S. lapazeanum, qmax was 71.2±0.80 mg g−1, b=0.03 (Fig. 2). This difference in affinity for cadmium is attributed to the number and chemical nature of the metal-binding sites, such as carboxyl, ether, alcohol, and amino groups of the biosorbent structure (Williams et al. 1998; Sheng et al. 2004). Sulfonate groups do not play an important role in binding of bivalent ions (Sheng et al. 2004). Both species had lower qmax Fig. 2 Sorption isotherm for cadmium (Cd2+). Line shows results calculated using the Langmuir model (Eq. 2); S. sinicola (solid line) and S. lapazeanum (dotted line) values than other brown algae, such as Fucus spiralis, but higher than some green algae, such as Chaetomorpha linum and Ulva sp., and red algae, such as Asparagopsis armata (Table 1). The qmax values were lower than values reported for other species of Sargassum, such as Sargassum baccularia, Sargassum filipendula, and Sargassum fluitans (Davis et al. 2000, 2004; Hashim and Chu 2004). Applying the data from the Langmuir model (Eq. 2) for S. sinicola and S. lapazeanum, the biosorbent quantity required to produce a final concentration (Cf) of 1 mg L−1 for each alga can be calculated from Eq. 3 as a function of the initial cadmium concentration (Ci). Although S. lapazeanum had a higher qmax than S. sinicola, S. sinicola outperforms S. lapazeanum because it has a higher b value (Fig. 3). S. sinicola has lower biosorption capacity than S. lapazeanum, but its affinity for cadmium makes S. sinicola more suitable. This is not apparent if both algae are compared only on the basis of the qmax parameter. Also, in the Gulf of California, S. sinicola is a potential biosorbent because it has a high qmax and large biomass. On the east coast of the Baja California Peninsula, Sargassum biomass is estimated at 180,000 t (wet), of which S. sinicola contributes >70%. The technology to harvest, dry, and mill this seaweed is available (Casas-Valdez 2009). Paul-Chávez (2005) suggests harvesting during late May and early June, when most of the thalli have released gametes and are still healthy. This ensures acceptable quality. After this period, the biomass begins to deteriorate and fragment. Water Air Soil Pollut (2011) 221:137–144 Table 1 Maximum capacity of biosorption (qmax) reported for several macroalgae 141 Species Green algae Brown algae qmax (mg g−1) Codium vermilara 21.8 Romera et al. (2007) Hashim and Chu (2004) Chaetomorpha linum 53.9 Spirogyra insignis 22.9 Romera et al. (2007) Ulva sp. 65.1 Sheng et al. (2004) Fucus spiralis 114.9 Romera et al. (2007) Padina sp. 84.3 Sheng et al. (2004) Sargassum baccularia 83.1 Hashim and Chu (2004) Sargassum filipendula 74.1 Davis et al. (2000) Sargassum fluitans Red algae Reference 106.7 Davis et al. (2004) Sargassum lapazeanum 71.2 This work Sargassum sinicola 62.4 This work Sargassum vulgare 88.7 Davis et al. (2000) Sargassum sp. 85.4 Sheng et al. (2004) Asparagopsis armata 32.3 Romera et al. (2007) Chondrus crispus 75.2 Romera et al. (2007) Gracilaria edulis 26.9 Hashim and Chu (2004) Gracilaria sp. 33.7 Sheng et al. (2004) Capacity of cadmium sequestration by nonliving algal biomass is largely dependent on availability of metals in solution and composition of the algae, mostly the concentration and composition of alginic acid in brown algae (Davis et al. 2003b; Mata et al. 2009). The concentration of alginate in S. sinicola was 19.2± 1.52%; in S. lapazeanum, it was 12.7±1.31%. The yield of alginate from S. sinicola was higher than that reported by Pérez-Reyes (1997) and Yabur et al. (2007), 16.8% and 15%, respectively, but it was lower than the 26% reported by Hernández-Carmona (1985) and similar to the 20.5% for Sargassum oligocystum reported by Davis et al. (2004). Differences in concen- Fig. 3 Algal biomass required to reduce the final concentration to 1 mg L−1 as a function of initial concentration of cadmium trations of alginate among species may be explained by seasonal and yearly fluctuations, local conditions, or characteristics of the species (Hernández-Carmona 1985; Pérez-Reyes 1997). Alginate is the salt of alginic acid, which is present as a gel inside the cell walls and mucilage or intracellular material (Chapman and Chapman 1980). It is a linear polysaccharide composed of two monomer β-D-mannuronic acid (M) and α-L-guluronic acid (G). These monomers are grouped into sequences MM and MG with glycosidic bonds β (1–4) and blocks GG and GM by glycosidic bonds α (1–4) (Haug et al. 1966). In S. vulgaris, Sheng et al. (2004) found that carboxyl groups of alginates are the dominant functional groups for heavy metal biosorption. According to their observations, the lower concentration of alginate in S. lapazeanum should mean a lower capacity to remove cadmium than S. sinicola; however, the opposite condition was observed in our study. This may relate to the presence of other compounds, particularly fucoidan, which contribute to metal sequestration or to different chemical composition of alginates (Figueira et al. 1999; Davis et al. 2003b; Sheng et al. 2004). Smidsrod and Haug (1968) report that affinity of alginate for divalent cations increased with increasing content of guluronic acid residues. No reports related to alginate composition of S. 142 Water Air Soil Pollut (2011) 221:137–144 lapazeanum has been found, but studies of S. sinicola show that this alga contains a greater proportion of guluronic acid residues than other brown algae species and similar to quantities found in S. fluitans (Davis et al. 2004; Murillo-Álvarez and Hernández-Carmona 2007). However, S. fluitans has higher biosorption capacity than S. sinicola (Table 1), but Davis et al. (2003a) did not find a direct relationship between high guluronic acid content in alginate and cadmium biosorption. Therefore, identification of other functional groups related to biosorption capacity of brown algae is required to explain the mechanisms involved in sorption of metals. 3.2 Concentration of Cadmium The highest concentration of cadmium in S. sinicola was recorded at San Juan de la Costa adjacent to the discharge site of waste from the phosphorite mine. Specimens collected north and south of San Juan had lower concentrations and were not significantly different from each other. In contrast, S. lapazeanum did not show significant differences in concentrations between San Juan and Califin. Also, this species was no found at Tarabillas (Table 2). Differences in concentration of cadmium between the two species could result from differences in metabolic rates or, more likely, to the affinity of each species for cadmium. Our results (Table 2) were above the average values reported for macroalgae (0.92±1.32 mg kg−1) from five regions throughout the world (Baoli and Congquiang 2004). However, these values, with the exception of results for S. sinicola from San Juan, are within the range reported in macroalgae in upwelling areas, such as Bahía Magdalena (24.5°N, 112°W) on the Pacific side of the peninsula (Riosmena-Rodríguez et al. 2010) where the range was from not detectable to 4.8 mg kg−1 and Playa El Monteón in the State of Nayarit (21°0′18′′N, 105°19′10″W) on the eastern side Table 2 Concentrations of cadmium (milligram per kilogram) in Sargassum species in the vicinity of San Juan de la Costa, BCS, Mexico Tarabillas S. lapazeanum –a S. sinicola 4.67±0.21 a Species not found San Juan of the gulf (Páez-Osuna et al. 2000), where the concentration averaged 5.6 mg kg−1. Concentrations of this metal in S. sinicola from San Juan de La Costa are similar to the brown alga Padina durvillaei from Santa Rosalía, ranging from 1.45 to 9.1 mg kg−1 (Rodríguez-Figueroa et al. 2009), which is contaminated by waste from copper mining. However, this value is lower than in brown and red macroalgae along the coast of Chile that is also contaminated by waste from copper mining, where Andrade et al. (2006) reports 17.8 mg kg−1 in Ahnfeltiopsis sp. Differences in the ability to absorb or adsorb cadmium by living and nonliving algae are affected by a variety of factors, such as temperature, salinity, light, pH, availability of nitrogen, seasonal differences, age, metabolic processes, and affinity of the organism for each element (Sánchez-Rodríguez et al. 2001; Davis et al. 2003b). Uptake of heavy metals in living algae occurs in two phases: (1) Ions bind to the inert ligands occurring on the cell surface, which is a fast, reversible process and does not require energy; and (2) Ions are bound, often irreversibly, to the cell wall or are actively taken up and bound within the cells (Wilde and Benemann 1993; Knauer et al. 1997). In nonliving algal biomass, only the first phase is involved, and environmental factors do not appear to participate (Stirk and Van Staden 2000). This ability also depends on two other main factors, the bioavailability of the metals in the water and the uptake capacity of live algae (Malea and Haritonidis 1999). Capacity to accumulate metals in living and nonliving algae is strongly influenced by the ionic form of the metal in the solution. In marine environments, accumulation of cadmium is influenced by the presence of other divalent metals, which compete with cadmium ions at the active sites in the algae. Previous work showed that the capacity of biosorption in S. sinicola is remarkably reduced by increasing salinity, apparently from complexing of cadmium ions with chloride ions in seawater (Patrón-Prado et al. 2010). Such interferences are avoided in laboratory tests, where cadmium biosorption by nonliving algae can be greater than the accumulation by living algae. Califin 2.75±0.20 2.75±0.22 10.96±0.15 4.15±0.19 4 Conclusions The capacity for biosorption of cadmium by nonliving S. sinicola and S. lapazeanum was determined as Water Air Soil Pollut (2011) 221:137–144 62.42±0.44 mg g−1 and 71.20±0.80 mg g−1, respectively; their corresponding alginate concentration was 19.2 ±1.52% and 12.7± 1.31% w/w. Although S. sinicola had lower biosorption capacity than S. lapazeanum, the affinity of S. sinicola for cadmium makes this alga more suitable as a biosorbent. Concentration of cadmium in S. sinicola varied at three coastal sites that reflected variations in cadmium bioavailability in seawater. Biosorption capacity of S. sinicola, coupled with the large algal biomass available, may be economically effective in bioremediation efforts at cadmium-impacted localities. Acknowledgments We thank to Dora L. Arvizu Higuera and Sonia Rodriguez Astudillo of the laboratory of CICIMAR-IPN and Baudilio Acosta, Alejandra Mazariegos, and Orlando Lugo of CIBNOR. Ira Fogel of CIBNOR provided editorial improvements. Funding was provided by Centro de Investigaciones Biológicas del Noroeste (grants EP 3.3, PC 2.0, and PC 2.1). M. P.P. is a recipient of a CONACYT doctoral fellowship. References Andrade, S., Medina, M. H., Moffett, J. W., & Correa, J. A. (2006). Cadmium-Copper antagonism in seaweeds inhabiting coastal areas affected by copper mine waste disposals. Environmental Science & Technology, 40, 4382–4387. Baoli, W., & Congquiang, L. (2004). Factors controlling the distribution of trace metals in macroalgae. Chinese Journal of Geochemistry, 23, 366–372. Casas-Valdez, M. (2009). El alga marina Sargassum (Sargassaceae) en el desarrollo regional. In: Urciaga-García, J. Lluch-Belda, D., Beltrán-Morales, L. F. (Eds.), Recursos marinos y servicios ambientales en el desarrollo regional (pp. 139– 156). La Paz, B.C.S., Mexico: CIBNOR Chapman, V. J., & Chapman, D. J. (1980). Seaweeds and their uses (3rd ed.). London: Chapman & Hall. COREMI (2000). Geological-mining monograph of the State of Baja California Sur. Consejo de Recursos Minerales, Publication M-24e, Mexico Davis, T. A., Volesky, B., & Vieira, R. H. S. F. (2000). Sargassum seaweed as biosorbent for heavy metals. Water Research, 34, 4270–4278. Davis, T. A., Llanes, F., Volesky, B., & Mucci, A. (2003a). Metal selectivity of Sargassum spp. and their alginate in relation to their a-L-guluronic acid content and conformation. Environmental Science & Technology, 37, 261–267. Davis, T. A., Volesky, B., & Mucci, A. (2003b). A review of the biochemistry of heavy metal biosorption by brown algae. Water Research, 37, 431–4330. Davis, T. A., Ali, F. C., Giannitti, E., Volesky, B., & Mucci, A. (2004). Cadmium biosorption by S. fluitans: treatment, resilience and uptake relative to other Sargassum spp. and brown algae. Water Quality Research Journal of Canada, 39, 183–189. 143 Figueira, M. M., Volesky, B., & Mathieu, H. J. (1999). Instrumental analysis study of iron species biosorption by Sargassum biomass. Environmental Science & Technology, 33, 1840–1846. Hashim, M. A., & Chu, K. H. (2004). Biosorption of cadmium by brown, green and red seaweeds. Chemical Engineering Journal, 97, 249–255. Haug, A. (1965). Alginic acid. In R. L. Whistler & L. M. Wofrom (Eds.), Methods in carbohydrate chemistry, analysis and preparation of sugars (Vol. 5, pp. 69–73). New York: Academic. Haug, A., Larsen, B., & Smidsrod, O. (1966). A study of the constitution of alginic acid by partial acid hydrolysis. Acta Chemica Scandinavica, 20, 183–190. Hernández-Carmona, G. (1985). Variación estacional del contenido de alginatos en tres especies de feofitas de Baja California Sur, México. Investigaciones Marinas CICIMAR, 2, 30–45. Hernández-Carmona, G., McHugh, D. J., Arvizu-Higuera, D. L., & Rodríguez-Montesinos, Y. E. (1999a). Pilot plant scale extraction of alginate from Macrocystis pyrifera. 1. Effect of pre-extraction treatments on yield and quality of alginate. Journal of Applied Phycology, 10, 507–513. Hernández-Carmona, G., McHugh, D. J., & López-Gutierrez, F. (1999b). Pilot plant scale extraction of alginate from Macrocystis pyrifera. 2. Studies on extraction conditions and methods of separating the alkaline-insoluble residue. Journal of Applied Phycology, 11, 493–502. Huerta-Díaz, M. A., De León-Chavira, F., Lares, M. L., Chee-Barragán, A., & Siqueiros-Valencia, A. (2007). Iron, manganese and trace metal concentrations in seaweeds from the central west coast of the Gulf of California. Applied Geochemistry, 22, 1380–1392. Knauer, K., Ahner, B., Xue, H. B., & Sigg, L. (1997). Metal and phytochelatin content in phytoplankton from freshwater lakes with different metal concentrations. Environmental Toxicology and Chemistry, 17, 2444–2452. Lockwood, M. P. (1976). Effects of pollutants on aquatic organisms. New York: Cambridge University Press. Lodeiro, P., Cordero, B., Grille, Z., Herrero, R., & Sastre de Vicente, M. E. (2004). Physicochemical studies of cadmium (II) biosorption by the invasive alga in Europe, Sargassum muticum. Biotechnology and Bioengineering, 88, 237–247. Malea, P., & Haritonidis, S. (1999). Seasonal accumulation of metals by red alga Gracilaria verrucosa (Huds.) Papens, from Thermaikos Gulf, Greece. Journal of Applied Phycology, 11, 503–509. Mann, S. S., & Ritchie, G. S. P. (1995). Forms of cadmium in sandy soils after amendment with soils of higher fixing capacity. Environmental Pollution, 87, 23–29. Mata, Y. N., Blázquez, M. L., Ballester, A., González, F., & Muñoz, J. A. (2009). Biosorption of cadmium, lead and copper with calcium alginate xerogels and immobilized Fucus vesiculus. Journal of Hazardous Materials, 163, 555–562. Méndez, L., Acosta, B., Álvarez-Castañeda, S. T., & LechugaDevéze, C. H. (1998). Trace metal distribution along the southern coast of Bahía de La Paz (Gulf of California), Mexico. Bulletin of Environmental Contamination and Toxicology, 61, 616–622. 144 Méndez, L., Palacios, E., Acosta, B., Monsalvo-Spencer, P., & Alvarez-Castañeda, T. (2006). Heavy metals in the clam Megapitaria squalida collected from wild and phosphorite mine-impacted sites in Baja California, Mexico. Biological Trace Element Research, 110, 275–287. Murillo-Álvarez, I., & Hernández-Carmona, G. (2007). Monomer composition and sequence of sodium alginate extracted at pilot plant scale from three commercially important seaweeds from Mexico. Journal of Applied Phycology, 19, 545–548. Pacheco-Ruíz, I., Zertuche-González, J. A., Chee-Barragán, A., & Blanco-Betancourt, R. (1998). Distribution and quantification of Sargassum beds along the west coast of the Gulf of California, Mexico. Botanica Marina, 14, 203–208. Páez-Osuna, F., Ochoa-Izaguirre, M. J., Bojórquez-Leyva, H., & Michel-Reynoso, I. L. (2000). Macroalgae as biomonitors of heavy metal availability in coastal lagoons from the subtropical Pacific of Mexico. Bulletin of Environmental Contamination and Toxicology, 64, 846–851. Patrón-Prado, M., Acosta-Vargas, B., Serviere-Zaragoza, E., & Méndez-Rodríguez, L. C. (2010). Copper and cadmium biosorption by dried seaweed Sargassum sinicola in saline wastewater. Water, Air, and Soil Pollution, 2010, 197–202. Paul-Chávez, L. (2005). Taxonomía y dinámica poblacional del complejo sinicola (Fucales: Phaeophyta) para el suroeste del Golfo de California. Tesis Doctoral. La Paz, Baja California Sur, México: CICIMAR. 194 pp. Pérez-Reyes, C. (1997). Composición química de Sargassum spp. Colectado en la Bahía de La Paz, B.C.S., y la factibilidad de su aprovechamiento en forma directa o como fuente de alginato. Masters’Thesis. La Paz, B.C.S., Mexico: CICIMAR. Riley, J. P. (1989). Los elementos más abundantes y menores en el agua de mar. In J. P. Riley & R. Chester (Eds.), Introducción a la química marina. Mexico City: AGT SA. Riosmena-Rodríguez, R., Talavera-Sáenz, A., Acosta-Vargas, B., & Gardner, S. C. (2010). Heavy metals dynamics in seaweeds and seagrasses in Bahía Magdalena, B.C.S., Mexico. Journal of Applied Phycology, 22, 283–291. Rodríguez-Figueroa, G. M., Shumilin, E., & Sánchez-Rodríguez, I. (2009). Heavy metal pollution monitoring using the brown seaweed Padina durviallaei in the coastal zone of the Santa Rosalía mining region, Baja California Peninsula, Mexico. Journal of Applied Phycology, 21, 19–26. Water Air Soil Pollut (2011) 221:137–144 Romera, E., González, F., Ballester, A., Blázquez, M. L., & Muñoz, J. A. (2007). Comparative study of biosoption of heavy metals using different types of algae. Bioresource Technology, 98, 3344–3353. Rule, K. L., Comber, S. D., Ross, D., Thornton, A., Makropoulos, C. K., & Rautiu, R. (2006). Diffuse sources of heavy metals entering an urban wastewater catchment. Chemosphere, 63, 64–72. Sánchez-Rodríguez, I., Huerta-Diaz, M. A., Choumiline, E., Holguín-Quiñones, O., & Zertuche-González, J. A. (2001). Elemental concentrations in different species of seaweed from Loreto Bay (Baja California del Sur). Mexico. Implications for the geochemical control of metals in algal tissues. Environmental Pollution, 114, 145–160. Schiewer, S., & Volesky, B. (1999). Advances in biosorption of heavy metals. In M. C. Flickinger & S. W. Drew (Eds.), Encyclopedia of bioprocess engineering. New York: Wiley. Sheng, P. S., Ting, Y. P., Chen, J. P., & Hong, L. (2004). Sorption of lead, copper, cadmium, zinc, and nickel by marine algal biomass: characterization of biosorptive capacity and investigation of mechanisms. Journal of Colloid and Interface Science, 275, 131–141. Smidsrod, O., & Haug, A. (1968). Dependence upon uronic acid and composition of some ion-exchange properties of alginates. Acta Chemica Scandinavica, 22, 1989–1997. Stirk, W. A., & Van Staden, J. (2000). Removal of heavy metals from solution using dried brown seaweed material. Botanica Marina, 43, 467–473. Vieira, R., & Volesky, B. (2000). Biosorption: a solution to pollution? International Microbiology, 3, 17–24. Wilde, E. W., & Benemann, J. R. (1993). Bioremoval of heavy metals by the use of microalgae. Biotechnology Advances, 11, 781–812. Williams, C. J., Aderhold, D., & Edyvean, G. J. (1998). Comparison between biosorbents for the removal of metal ions from aqueous solutions. Water Research, 32, 216– 224. Yabur, R., Basham, Y., & Hernández-Carmona, G. (2007). Alginate from the macroalgae Sargassum sinicola as a novel source for microbial immobilization material in wastewater treatment and plant growth promotion. Journal of Applied Phycology, 19, 43–53.