Journal of Applied Phycology

, Volume 29, Issue 2, pp 741–749 | Cite as

Investigating essential and toxic elements in Antarctic macroalgae using a green analytical method

  • Rochele S. Picoloto
  • Rodrigo M. Pereira
  • Vanize C. Costa
  • Carla A. Hartwig
  • Claudio M. P. Pereira
  • Pio Colepicolo
  • Fabio A. Duarte
  • Marcia F. Mesko
V REDEALGAS WORKSHOP (RIO DE JANEIRO, BRAZIL)
First Online:
Received:
Revised:
Accepted:

Abstract

A systematic study for the determination of essential and toxic elements (such as As, Cd, Cu, Mn, Ni, Pb, V and Zn) in Antarctic macroalgae species (Desmarestia anceps, Iridaea cordata, Palmaria decipiens and Pyropia endiviifolia) was performed. For this purpose, a green sample preparation method combined with a high-sensitivity detection technique (inductively coupled plasma mass spectrometry) was used. By using the microwave-assisted digestion combined with ultraviolet radiation (MW-UV) method, 700 mg of macroalgae were digested using a diluted HNO3 solution (2 mol L−1). The accuracy was evaluated by analysis of certified reference materials of aquatic plant (BCR 060) and apple leaves (NIST 1515). Agreement with reference or informed values for all analytes ranged from 94 to 106%, except for As and Mo in BCR 060. The results were also compared with those obtained by the reference method, which did not present a significant difference (t test, 95% confidence level). Based on the results, analysed samples showed considerable variations in regards to the concentrations of Zn, Ni and Mn. Moreover, a relatively high concentration of As in Desmarestia anceps and Pyropia endiviifolia was observed. The results for most of the analytes in Antarctic macroalgae were in agreement with other studies that have been published in literature. In addition, the proposed method was suitable for determining toxic and essential elements in Antarctic macroalgae reducing reagent consumption and waste generation, which is in agreement with the green chemistry recommendation.

Keywords

Metal and non-metal Seaweed Diluted acids Microwave-assisted digestion UV-digestion ICP-MS 
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Notes

Acknowledgements

The authors are grateful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS) for supporting this study. We are also grateful to Programa Antártico Brasileiro (PROANTAR) for supplying the macroalgae samples and also supporting this study.

References

  1. Akcali I, Kucuksezgin F (2011) A biomonitoring study: heavy metals in macroalgae from eastern Aegean coastal areas. Mar Pollut Bull 62:637–645CrossRefPubMedGoogle Scholar
  2. Andrade S, Medina MH, Moffett JW, Correa JA (2006) Cadmium–Copper antagonism in seaweeds inhabiting coastal areas affected by copper mine waste disposals. Environ Sci Technol 40:4382–4387CrossRefPubMedGoogle Scholar
  3. Astorga-España MS, Rodríguez Galdón B, Rodríguez Rodríguez EM, Díaz Romero C (2015) Mineral and trace element concentrations in seaweeds from the sub-Antarctic ecoregion of Magallanes (Chile). J Food Compos Anal 39:69–76CrossRefGoogle Scholar
  4. Balbinot L, Smichowski P, Farias S, Arruda MAZ, Vodopivez C, Poppi RJ (2005) Classification of Antarctic algae by applying Kohonen neural network with 14 elements determined by inductively coupled plasma optical emission spectrometry. Spectrochim Acta B 60:725–730CrossRefGoogle Scholar
  5. Barin JS, Mello PA, Mesko MF, Duarte FA, Flores EMM (2016) Determination of elemental impurities in pharmaceutical products and related matrices by ICP-based methods: a review. Anal Bioanal Chem 408:4547–4566CrossRefPubMedGoogle Scholar
  6. Barkacs K, Varga A, Gal-Solymos K, Zaray G (1999) Direct determination of metal concentrations in freshwater algae by total reflection X-ray fluorescence spectrometry. J Anal Atom Spectrom 14:577–581CrossRefGoogle Scholar
  7. Birkenmajer K (1983) Late Cenozoic phases of block-faulting on King George Island (South Shetland Islands, West Antarctica). Bull Pol Acad Sci Earth Sci 46:147–155Google Scholar
  8. Bizzi CA, Flores EMM, Picoloto RS, Barin JS, Nobrega JA (2010) Microwave-assisted digestion in closed vessels: effect of pressurization with oxygen on digestion process with diluted nitric acid. Anal Methods 2:734–738CrossRefGoogle Scholar
  9. Bizzi CA, Barin JS, Garcia EE, Nobrega JA, Dressler VL, Flores EMM (2011a) Improvement of microwave-assisted digestion of milk powder with diluted nitric acid using oxygen as auxiliary reagent. Spectrochim Acta B 66:394–398CrossRefGoogle Scholar
  10. Bizzi CA, Flores EMM, Barin JS, Garcia EE, Nobrega JA (2011b) Understanding the process of microwave-assisted digestion combining diluted nitric acid and oxygen as auxiliary reagent. Microchem J 99:193–196CrossRefGoogle Scholar
  11. Bizzi CA, Flores ELM, Nobrega JA, Oliveira JSS, Schmidt L, Mortari SR (2014a) Evaluation of a digestion procedure based on the use of diluted nitric acid solutions and H2O2 for the multielement determination of whole milk powder and bovine liver by ICP-based techniques. J Anal Atom Spectrom 29:332–338CrossRefGoogle Scholar
  12. Bizzi CA, Nobrega JA, Barin JS, Oliveira JSS, Schmidt L, Mello PA, Flores EMM (2014b) Effect of simultaneous cooling on microwave-assisted wet digestion of biological samples with diluted nitric acid and O2 pressure. Anal Chim Acta 837:16–22CrossRefPubMedGoogle Scholar
  13. Brito GB, de Souza TL, Bressy FC, Moura CWN, Korn MGA (2012) Levels and spatial distribution of trace elements in macroalgae species from the Todos os Santos Bay, Bahia, Brazil. Mar Pollut Bull 64:2238–2244CrossRefPubMedGoogle Scholar
  14. Brouwer PEM (1996) Decomposition in situ of the sublittoral Antarctic macroalga Desmarestia anceps Montagne. Polar Biol 16:129–137CrossRefGoogle Scholar
  15. Cabrita ARJ, Maia MRG, Oliveira HM, Sousa-Pinto I, Almeida AA, Pinto E, Fonseca AJM (2016) Tracing seaweeds as mineral sources for farm-animals. J Appl Phycol 28:3135–3150CrossRefGoogle Scholar
  16. Conti ME, Cecchetti G (2003) A biomonitoring study: trace metals in algae and molluscs from Tyrrhenian coastal areas. Environ Res 93:99–112CrossRefPubMedGoogle Scholar
  17. Díaz O, Tapia Y, Muñoz O, Montoro R, Velez D, Almela C (2012) Total and inorganic arsenic concentrations in different species of economically important algae harvested from coastal zones of Chile. Food Chem Toxicol 50:744–749CrossRefPubMedGoogle Scholar
  18. Domínguez-González R, Moreda-Piñeiro A, Bermejo-Barrera A, Bermejo-Barrera P (2005) Application of ultrasound-assisted acid leaching procedures for major and trace elements determination in edible seaweed by inductively coupled plasma-optical emission spectrometry. Talanta 66:937–942CrossRefPubMedGoogle Scholar
  19. Domínguez-González R, Romarís-Hortas V, García-Sartal C, Moreda-Piñeiro A, Barciela-Alonso MC, Bermejo-Barrera P (2010) Evaluation of an in vitro method to estimate trace elements bioavailability in edible seaweeds. Talanta 82:1668–1673CrossRefPubMedGoogle Scholar
  20. Duarte FA, Pereira JSF, Mesko MF, Goldschmidt F, Flores EMM, Dressler VL (2007) Evaluation of liquid chromatography inductively coupled plasma mass spectrometry for arsenic speciation in water from industrial treatment of shale. Spectrochim Acta B 62:978–984CrossRefGoogle Scholar
  21. Eisler R (2010) Algae and macrophytes. In: Eisler R (ed) Compendium of trace metals and marine biota. Elsevier, Amsterdam, pp. 7–97Google Scholar
  22. Farías S, Arisnabarreta SP, Vodopivez C, Smichowski P (2002) Levels of essential and potentially toxic trace metals in Antarctic macro algae. Spectrochim Acta B 57:2133–2140CrossRefGoogle Scholar
  23. Farías S, Smichowski P, Vélez D, Montoro R, Curtosi A, Vodopívez C (2007) Total and inorganic arsenic in Antarctic macroalgae. Chemosphere 69:1017–1024CrossRefPubMedGoogle Scholar
  24. Flores EMM, Barin JS, Mesko MF, Knapp G (2007) Sample preparation techniques based on combustion reactions in closed vessels—a brief overview and recent applications. Spectrochim Acta B 62:1051–1064CrossRefGoogle Scholar
  25. Fujii MT, Yoneshigue-Valentin Y, Yokoya NS, Pupo D, Guimaraes SMPB, Silva IB, Dalto AG, Martins AP, Pereira DC, Souza JMC, Pereira CMP, Mansilla A, Pellizzari FM, Colepicolo P (2014) Macroalgas marinhas da Antártica, 1st edn. Editora Cubo, São CarlosGoogle Scholar
  26. Grindlay G, Mora J, Loos-Vollebregt M, Vanhaecke F (2013) A systematic study on the influence of carbon on the behavior of hard-to-ionize elements in inductively coupled plasma-mass spectrometry. Spectrochim Acta B 86:42–49CrossRefGoogle Scholar
  27. Grotti M, Soggia F, Lagomarsino C, Riva SD, Goessler W, Francesconi KA (2008) Natural variability and distribution of trace elements in marine organisms from Antarctic coastal environments. Antarct Sci 20:39–52CrossRefGoogle Scholar
  28. Guiry MD, Guiry GM (2015) AlgaeBase. World-wide electronic publication. National University of Ireland. Galway. http://www.algaebase.org. Accessed 14 Oct 2016
  29. Hartwig CA, Pereira RM, Rondan FS, Cruz SM, Duarte FA, Flores EMM, Mesko MF (2016) The synergic effect of microwave and ultraviolet radiation for chocolate digestion and further determination of As, Cd, Ni and Pb by ICP-MS. J Anal Atom Spectrom 31:523–530CrossRefGoogle Scholar
  30. Himmelman JH, Carefoot TH (1975) Seasonal changes in calorific value of three pacific coast seaweeds, and their significance to some marine invertebrate herbivores. J Exp Mar Biol Ecol 18:139–151CrossRefGoogle Scholar
  31. Horwitz W, Latimer GW (2011) Official methods of analysis of AOAC International, 18 edn. AOAC International, GaithersburgGoogle Scholar
  32. Javed M, Usmani N (2014) Impact of heavy metal toxicity on hematology and glycogen status of fish: a review. Proc Natl Acad Sci India B 85:889–900Google Scholar
  33. Machado AAS, Spencer K, Kloas W, Toffolon M, Zarfl C (2016) Metal fate and effects in estuaries: a review and conceptual model for better understanding of toxicity. Sci Total Environ 541:268–281CrossRefGoogle Scholar
  34. Maciel JV, Knorr CL, Flores EMM, Müller EI, Mesko MF, Primel EG, Duarte FA (2014) Feasibility of microwave-induced combustion for trace element determination in Engraulis anchoita by ICP-MS. Food Chem 145:927–931CrossRefPubMedGoogle Scholar
  35. Majer AP, Petti MAV, Corbisier TN, Ribeiro AP, Theophilo CYS, Ferreira PAL, Figueira RCL (2014) Bioaccumulation of potentially toxic trace elements in benthic organisms of Admiralty Bay (King George Island, Antarctica). Mar Pollut Bull 79:321–325CrossRefPubMedGoogle Scholar
  36. Marzocchi M, Badocco D, Piovan A, Pastore P, Di Marco V, Filippini R, Caniato R (2016) Metals in Undaria pinnatifida (Harvey) Suringar and Sargassum muticum (Yendo) Fensholt edible seaweeds growing around Venice (Italy). J Appl Phycol 28:2605–2613CrossRefGoogle Scholar
  37. Mesko MF, Toralles IG, Crizel MG, Costa VC, Pires NRX, Pereira CMP, Picoloto RS, Mello PA (2014) Bromine and iodine determination in edible seaweed by ICP-MS after digestion by microwave-induced combustion. Quim Nov. 6:964–968Google Scholar
  38. Mesko MF, Picoloto RS, Ferreira LR, Costa VC, Pereira CMP, Colepicolo P, Muller EI, Flores EMM (2015) Ultraviolet radiation combined with microwave-assisted wet digestion of Antarctic seaweeds for further determination of toxic elements by ICP-MS. J Anal Atom Spectrom 30:260–266CrossRefGoogle Scholar
  39. Moreda-Piñeiro J, Moreda-Piñeiro A, Romarís-Hortas V, Domínguez-González R, Alonso-Rodríguez E, López-Mahía P, Muniategui-Lorenzo S, Prada-Rodríguez D, Bermejo-Barrera P (2012) Trace metals in marine foodstuff: bioavailability estimation and effect of major food constituents. Food Chem 134:339–345.5CrossRefGoogle Scholar
  40. Moreno AJE, Gerpe SM, Moreno JV, Vodopivez C (1997) Heavy metals in Antarctic organisms. Polar Biol 17:131–140CrossRefGoogle Scholar
  41. Muller ALH, Muller CC, Lyra F, Mello PA, Mesko MF, Muller EI, Flores EMM (2013) Determination of toxic elements in nuts by inductively coupled plasma mass spectrometry after microwave-induced combustion. Food Anal Meth 6:258–264CrossRefGoogle Scholar
  42. Muller ALH, Muller EI, Barin JS, Flores EMM (2015) Microwave-assisted digestion using diluted acids for toxic element determination in medicinal plants by ICP-MS in compliance with United States pharmacopeia requirements. Anal Methods 7:5218–5225CrossRefGoogle Scholar
  43. Oliveira JS, Picoloto RS, Bizzi CA, Mello PA, Barin JS, Flores EMM (2015) Microwave-assisted ultraviolet digestion of petroleum coke for the simultaneous determination of nickel, vanadium and sulfur by ICP-OES. Talanta 144:1052–1058CrossRefPubMedGoogle Scholar
  44. Pereira CMP, Hobuss CB, Maciel JV, Ferreira LR, Del Pino FB, Mesko MF, Jacob-Lopes E, Colepicolo P (2012) Biodiesel derived from microalgae: advances and perspectives. Quim Nov. 35:2013–2018Google Scholar
  45. Pereira JS, Picoloto RS, Pereira LS, Guimaraes RC, Guarnieri RA, Flores EMM (2013) High-efficiency microwave-assisted digestion combined to in situ ultraviolet radiation for the determination of rare earth elements by ultrasonic nebulization ICPMS in crude oils. Anal Chem 85:11034–11040CrossRefPubMedGoogle Scholar
  46. Peters KJ, Amsler CD, Amsler MO, McClintock JB, Dunbar RB, Baker BJ (2005) A comparative analysis of the nutritional and elemental composition of macroalgae from the western Antarctic Peninsula. Phycologia 44:453–463CrossRefGoogle Scholar
  47. Rajfur M, Kłos A, Wacławek M (2010) Sorption properties of algae Spirogyra sp. and their use for determination of heavy metal ions concentrations in surface water. Bioelectrochemistry 80:81–86CrossRefPubMedGoogle Scholar
  48. Robert T (2008) Practical guide to ICP-MS. CRC Press, Boca RatonGoogle Scholar
  49. Runcie JW, Riddle MJ (2004) Metal concentrations in macroalgae from East Antarctica. Mar Pollut Bull 49:1114–1119CrossRefPubMedGoogle Scholar
  50. Ryan S, McLoughlin P, O'Donovan O (2012) A comprehensive study of metal distribution in three main classes of seaweed. Environ Pollut 167:171–177CrossRefPubMedGoogle Scholar
  51. Smichowski P, Farias S, Valiente L, Iribarren ML, Vodopivez C (2004) Total arsenic content of nine species of Antarctic macro algae as determined by electrothermal atomic absorption spectrometry. Anal Bioanal Chem 378:465–469CrossRefPubMedGoogle Scholar
  52. Smith BD, Foreman RE (1984) An assessment of seaweed decomposition within a southern Strait of Georgia seaweed community. Mar Biol 84:197–205CrossRefGoogle Scholar
  53. Soares BM, Vieira AA, Lemões JS, Santos CMM, Mesko MF, Primel EG, Montes D’Oca MG, Duarte FA (2012) Investigation of major and trace element distribution in the extraction–transesterification process of fatty acid methyl esters from microalgae Chlorella sp. Bioresource Technol 110:730–734CrossRefGoogle Scholar
  54. Souza PO, Ferreira LR, Pires NRX, Filho PJS, Duarte FA, Pereira CMP, Mesko MF (2012) Algae of economic importance that accumulate cadmium and lead: a review. Rev Bras Farmacogn 22:825–837CrossRefGoogle Scholar
  55. Sunda WG, Huntsman SA (1998) Processes regulating cellular metal accumulation and physiological effects: phytoplankton as model systems. Sci Total Environ 219:165–181CrossRefGoogle Scholar
  56. Tabarsa M, Rezaei M, Ramezanpour Z, Waaland JR (2012) Chemical compositions of the marine algae Gracilaria salicornia (Rhodophyta) and Ulva lactuca (Chlorophyta) as a potential food source. J Sci Food Agric 92:2500–2506CrossRefPubMedGoogle Scholar
  57. Wang Z, Wang X, Ke C (2014) Bioaccumulation of trace metals by the live macroalga Gracilaria lemaneiformis. J Appl Phycol 26:1889–1897CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Rochele S. Picoloto
    • 1
  • Rodrigo M. Pereira
    • 2
  • Vanize C. Costa
    • 2
  • Carla A. Hartwig
    • 2
  • Claudio M. P. Pereira
    • 2
  • Pio Colepicolo
    • 3
  • Fabio A. Duarte
    • 1
  • Marcia F. Mesko
    • 2
  1. 1.Departamento de QuímicaUniversidade Federal de Santa MariaSanta MariaBrazil
  2. 2.Centro de Ciências Químicas, Farmacêuticas e de AlimentosUniversidade Federal de PelotasPelotasBrazil
  3. 3.Instituto de Química, Departamento de BioquímicaUniversidade de São PauloSão PauloBrazil

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