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Journal of Applied Phycology

, Volume 31, Issue 1, pp 691–708 | Cite as

An introduction to copper and zinc pollution in macroalgae: for use in remediation and nutritional applications

  • Alexander W. GeddieEmail author
  • Steven G. Hall
Article

Abstract

Macroalgae are an economically significant and fast-growing global commodity. However, pollution significantly affects the production and quality of macroalgae. Various studies have shown copper and zinc concentrations above 20 ppb (Cu) and 30 ppb (Zn) generally inhibit macroalgae growth. However, accumulation of metals in macroalgae is affected by several different factors, substances, and processes. Currently, not all of these factors, such as salinity, are well-understood and require further research. This review provides some background information on the biology and uses of macroalgae, as well as the kinetics of metal accumulation, the role of copper and zinc as toxic substances in macroalgae, and defensive mechanisms that macroalgae use to protect against metal toxicity from those metals. Finally, it describes various ways in which copper and zinc accumulation in macroalgae could be used in multiple beneficial applications.

Keywords

Macroalgae Copper Zinc Aquatic pollution 

Notes

Funding information

The work is supported through funding from the North Carolina State University Department of Biological and Agricultural Engineering and the William White Endowment of the NC Agriculture Foundation and the North Carolina State University College of Agriculture and Life Sciences.

References

  1. Achary MS, Satpathy KK, Panigrahi S, Mohanty AK, Padhi RK, Biswas S, Prabhu RK, Vijayalakshmi S, Panigrahy RC (2017) Concentration of heavy metals in the food chain components of the nearshore coastal waters of Kalpakkam, southeast coast of India. Food Control 72(Part B):232–243Google Scholar
  2. Alam F, Mobin S, Chowdhury H (2015) Third generation biofuel from algae. Procedia Engineer 105:763–768Google Scholar
  3. Ali SS, Shaaban MT, Abomohra AE, El-Safity K (2016) Macroalgal activity against multiple drug resistant Aeromonas hydrophila: a novel treatment study towards enhancement of fish growth performance. Microb Pathogenesis 101:89–95Google Scholar
  4. Amado Filho GM, Karez CS, Andrade LR, Yoneshigue-Valentin Y, Pfeiffer WC (1997) Effects on growth and accumulation of zinc in six seaweed species. Ecotoxicol Environ Saf 37:223–228PubMedGoogle Scholar
  5. Andrade LR, Farina M, Amado Filho GM (2004) Effects of copper on Enteromorpha flexuosa (Chlorophyta) in vitro. Ecotoxicol Environ Saf 58:117–125PubMedGoogle Scholar
  6. Andrade S, Contreras L, Moffett JW, Correa JA (2006) Kinetics of copper accumulation in Lessonia nigrescens (Phaeophyceae) under conditions of environmental oxidative stress. Aquat Toxicol 78:398–401PubMedGoogle Scholar
  7. Aquaculture Stewardship Council (2012) Final salmon aquaculture dialogue standards for aquaculture stewardship, 35–37Google Scholar
  8. Arora N, Gulati K, Patel A, Pruthi PA, Poluri KM, Pruthi V (2017) A hybrid approach integrating arsenic detoxification with biodiesel production using oleaginous microalgae. Algal Res 24:29–39Google Scholar
  9. Babu MY, Palanikumar L, Nagarani N, Devi VJ, Kumar SR, Ramakritinan CM, Kumaraguru AK (2014) Cadmium and copper toxicity in three marine macroalgae: evaluation of the biochemical responses and DNA damage. Environ Sci Pollut Res 21:9604–9616Google Scholar
  10. Bădescu IS, Bulgariu D, Bulgariu L (2017) Alternative utilization of algal biomass (Ulva sp.) loaded with Zn(II) ions for improving of soil quality. J Appl Phycol 29:1069–1079Google Scholar
  11. Balina K, Romagnoli F, Blumberga D (2016) Chemical composition and potential use of Fucus vesiculosus from Gulf of Riga. Energy Procedia 95:43–49Google Scholar
  12. Bansemer MS, Qin JG, Harris JO, Duong DN, Currie K, Howarth GS, Stone DAJ (2016) Dietary inclusions of dried macroalgae meal in formulated diets improve the growth of greenlip abalone (Haliotis laevigata). J Appl Phycol 28:3645–3658Google Scholar
  13. Bao VWW, Lui GCS, Leung KMY (2014) Acute and chronic toxicities of zinc pyrithione alone and in combination with copper to the marine copepod Tigriopus japonicus. Aquat Toxicol 157:81–93PubMedGoogle Scholar
  14. Baumann HA, Morrison L, Stengel DB (2009) Metal accumulation and toxicity measured by PAM—chlorophyll fluorescence in seven species of marine macroalgae. Ecotoxicol Environ Saf 72:1063–1075PubMedGoogle Scholar
  15. Beg MU, Al-Muzaini S, Saeed T, Jacob PG, Beg KR, Al-Bahloul M, Al-Matrouk K, Al-Obaid T, Kurian A (2001) Chemical contamination and toxicity of sediment from a coastal area receiving industrial effluents in Kuwait. Arch Environ Contam Toxicol 41:289–297PubMedGoogle Scholar
  16. Beiras R, Bellas J, Fernández N, Lorenzo JI, Cobelo-Garcı́a A (2003) Assessment of coastal marine pollution in Galicia (NW Iberian Peninsula); metal concentrations in seawater, sediments and mussels (Mytilus galloprovincialis) versus embryo–larval bioassays using Paracentrotus lividus and Ciona intestinalis. Mar Environ Res 56:531–553PubMedGoogle Scholar
  17. Bertini I, Luchinat C (1994) The reaction pathways of zinc enzymes and related biological catalysts. In: Bertini I, Gray H, Lippard S, Valentine J (eds) Bioinorganic Chemistry. University Science Books, Mill Valley, pp 37–106Google Scholar
  18. Bielmyer GK, Bullington JB, DeCarlo CA, Chalk SJ, Smith K (2012) The effects of salinity on acute toxicity of zinc to two euryhaline species of fish, Fundulus heteroclitus and Kryptolebias marmoratus. Integr Comp Biol 52:753–760PubMedPubMedCentralGoogle Scholar
  19. Boxall ABA, Comber SD, Conrad AU, Howcroft J, Zaman N (2000) Inputs, monitoring and fate modelling of antifouling biocides in UK estuaries. Mar Pollut Bull 40:898–905Google Scholar
  20. Boyle J, Sayer C, Hoare D, Bennion H, Heppel K, Lambert S, Appleby P, Rose N, Davy A (2016) Toxic metal enrichment and boating intensity: sediment records of antifoulant copper in shallow lakes of eastern England. J Paleolimnol 55:195–208Google Scholar
  21. Braithwaite RA, McEvoy LA (2005) Marine biofouling on fish farms and its remediation. Adv Mar Biol 47:215–252PubMedGoogle Scholar
  22. Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F (2012) Functions of mineral nutrients: micronutrients. In: Marschner H (ed) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic Press, London, pp. 313–404Google Scholar
  23. Brown M, Newman J, Han T (2012) Inter-population comparisons of copper resistance and accumulation in the red seaweed, Gracilariopsis longissima. Ecotoxicology 21:591–600PubMedGoogle Scholar
  24. Cabral-Oliveira J, Coelho H, Pratas J, Mendes S, Pardal M (2016) Arsenic accumulation in intertidal macroalgae exposed to sewage discharges. J Appl Phycol 28:3697–3703Google Scholar
  25. 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 28:3135–3150Google Scholar
  26. Cabrita ARJ, Correia A, Rodrigues AR, Cortez PP, Vilanova M, Fonseca AJM (2017) Assessing in vivo digestibility and effects on immune system of sheep fed alfalfa hay supplemented with a fixed amount of Ulva rigida and Gracilaria vermiculophylla. J Appl Phycol 29:1057–1067Google Scholar
  27. Caesar J, Hiritius A, Schneider R (1962) Bellum Africanum. Weidmann, BerlinGoogle Scholar
  28. Callaway E (2015) Lab staple agar hit by seaweed shortage. Nature 528:171–172PubMedGoogle Scholar
  29. Cao D, Xie P, Deng J, Zhang H, Ma R, Liu C, Liu R, Liang Y, Li H, Shi X (2015) Effects of Cu2+ and Zn2+ on growth and physiological characteristics of green algae, Cladophora. Environ Sci Pollut Res 22:16535–16541Google Scholar
  30. Chae JS, Choi MS, Song YH, Um IK, Kim JG (2014) Source identification of heavy metal contamination using metal association and Pb isotopes in Ulsan Bay sediments, East Sea, Korea. Mar Poll Bull 88:373–382Google Scholar
  31. Chakraborty S, Bhattacharya T, Singh G, Maity JP (2014) Benthic macroalgae as biological indicators of heavy metal pollution in the marine environments: a biomonitoring approach for pollution assessment. Ecotoxicol Environ Saf 100:61–68PubMedGoogle Scholar
  32. Charney M (2012) USDA national nutrient database for standard reference, release 24 and dietary supplement ingredient database, release 2. J Agr Food Inform 13(4):358Google Scholar
  33. Charters FJ, Cochrane TA, O'Sullivan AD (2016) Untreated runoff quality from roof and road surfaces in a low intensity rainfall climate. Sci Total Environ 550:265–272PubMedGoogle Scholar
  34. Chaudhuri A, Mitra M, Havrillia C, Waguespack Y, Schwarz J (2007) Heavy metal biomonitoring by seaweeds on the Delmarva Peninsula, east coast of the USA. Bot Mar 50:151–158Google Scholar
  35. Choi Y, Kim K, Kim D, Nam T (2017) Evaluation of different Pyropia yezoensis extracts as feed additives for growth and immunity of japanese flounder Paralichthys olivaceus. Fisheries Sci 83:819–826Google Scholar
  36. Clabeaux BL, Navarro DA, Aga DS, Bisson MA (2013) Combined effects of cadmium and zinc on growth, tolerance, and metal accumulation in Chara australis and enhanced phytoextraction using EDTA. Ecotoxicol Environ Saf 98:236–243PubMedGoogle Scholar
  37. Collén J, Pinto E, Pedersén M, Colepicolo P (2003) Induction of oxidative stress in the red macroalga Gracilaria tenuistipitata by pollutant metals. Arch Environ Contam Toxicol 45:337–342PubMedGoogle Scholar
  38. Connan S, Stengel DB (2011) Impacts of ambient salinity and copper on brown algae: 1. Interactive effects on photosynthesis, growth, and copper accumulation. Aquat Toxicol 104:94–107PubMedGoogle Scholar
  39. Contreras L, Mella D, Moenne A, Correa JA (2009) Differential responses to copper-induced oxidative stress in the marine macroalgae Lessonia nigrescens and Scytosiphon lomentaria (Phaeophyceae). Aquat Toxicol 94:94–102PubMedGoogle Scholar
  40. Correa JA, Castilla JC, Ramírez M, Varas M, Lagos N, Vergara S, Moenne A, Román D, Brown MT (1999) Copper, copper mine tailings and their effect on marine algae in Northern Chile. J Appl Phycol 11:57–67Google Scholar
  41. Costa GB, Felix Marthiellen RL, de Simioni C, Ramlov F, Oliveira ER, Pereira DT, Maraschin M, Chow F, Horta PA, Lalau CM, da Costa CH, Matias WG, Bouzon ZL, Schmidt ÉC (2015) Effects of copper and lead exposure on the ecophysiology of the brown seaweed Sargassum cymosum. Protoplasma 253:111–125PubMedGoogle Scholar
  42. Cyrus MD, Bolton JJ, Scholtz R, Macey BM (2015) The advantages of Ulva (Chlorophyta) as an additive in sea urchin formulated feeds: effects on palatability, consumption and digestibility. Aquac Nutr 21:578–591Google Scholar
  43. Dai J, Song J, Li X, Yuan H, Li N, Zheng G (2007) Environmental changes reflected by sedimentary geochemistry in recent hundred years of Jiaozhou Bay, North China. Environ Pollut 145:656–667PubMedGoogle Scholar
  44. Damrongsiri S, Vassanadumrongdee S, Tanwattana P (2016) Heavy metal contamination characteristic of soil in WEEE (waste electrical and electronic equipment) dismantling community: a case study of Bangkok, Thailand. Environ Sci Pollut Res 23:17026–17034Google Scholar
  45. Daneshvar E, Vazirzadeh A, Niazi A, Sillanpää M, Bhatnagar A (2017) A comparative study of methylene blue biosorption using different modified brown, red and green macroalgae—effect of pretreatment. Chem Eng J 307:435–446Google Scholar
  46. Davis AP, Shokouhian M, Ni S (2001) Loading estimates of lead, copper, cadmium, and zinc in urban runoff from specific sources. Chemosphere 44:997–1009PubMedGoogle Scholar
  47. Day JW, Lane RR, D’Elia CF, Wiegman ARH, Rutherford JS, Shaffer GP, Brantley CG, Kemp GP (2016) Large infrequently operated river diversions for Mississippi Delta restoration. Estuar Coast Shelf Sci 183:292–303Google Scholar
  48. Desideri D, Cantaluppi C, Ceccotto F, Meli MA, Roselli C, Feduzi L (2016) Essential and toxic elements in seaweeds for human consumption. J Toxicol Environ Health A 79:112–122PubMedGoogle Scholar
  49. Dillehay TD, Ramírez C, Pino M, Collins MB, Rossen J, Pino-Navarro JD (2008) Monte Verde: seaweed, food, medicine, and the peopling of South America. Science 320:784–786PubMedGoogle Scholar
  50. Dittert I, Vilar V, da Silva E, de Souza S, de Souza A, Botelho C, Boaventura R (2013) Turning Laminaria digitata seaweed into a resource for sustainable and ecological removal of trivalent chromium ions from aqueous solutions. Clean Technol Environ 15:955–965Google Scholar
  51. Ebenezer V, Lim W, Ki J (2014) Effects of the algicides CuSO4 and NaOCl on various physiological parameters in the harmful dinoflagellate Cochlodinium polykrikoides. J Appl Phycol 26:2357–2365Google Scholar
  52. El Din NGS, El-Sherif ZM (2012) Nutritional value of some algae from the north-western Mediterranean coast of Egypt. J Appl Phycol 24:613–626Google Scholar
  53. El-Waziry A, Al-Haidary A, Okab A, Samara E, Abdoun K (2015) Effect of dietary seaweed (Ulva lactuca) supplementation on growth performance of sheep and on in vitro gas production kinetics. Turk J Vet Anim Sci 39:81–86Google Scholar
  54. Evans FD, Critchley AT (2014) Seaweeds for animal production use. J Appl Phycol 26:891–899Google Scholar
  55. FAO (2016) The state of world fisheries and aquaculture 2016. Contributing to food security and nutrition for all. FAO, Rome, p 200Google Scholar
  56. Fargašová A (1999) Toxicity of Cd2+ in mixture with Cu2+, Zn2+, Pb2+ and Fe2+ on growth and chlorophyll content of alga Scenedesmus quadricauda. Biologia 54:661–666Google Scholar
  57. Farias DR, Hurd CL, Eriksen RS, Simioni C, Schmidt E, Bouzon ZL, Macleod CK (2017) In situ assessment of Ulva australis as a monitoring and management tool for metal pollution. J Appl Phycol 29:2489–2502Google Scholar
  58. Farmer BD, Beck BH, Mitchell AJ, Rawles SD, Straus DL (2017) Dietary copper effects survival of channel catfish challenged with Flavobacterium columnare. Aquac Res 48:1751–1758Google Scholar
  59. Feng J, Chen J, Chen M, Su X, Shi Q (2017) Effects of biocide treatments on durability of wood and bamboo/high density polyethylene composites against algal and fungal decay. J Appl Polym Sci 134:1996–2003Google Scholar
  60. Fongmoon D, Pongnikorn S, Chaisena A, Iamsaard S (2014) Particulate matters collected from ceramic factories in Lampang Province affecting rat lungs. J Zhejiang Univ Sci B 15(1):75–83PubMedPubMedCentralGoogle Scholar
  61. Fostier AH, Costa FN, Korn MSGA (2016) Assessment of mercury contamination based on mercury distribution in sediment, macroalgae, and seagrass in the Todos os Santos Bay, Bahia, Brazil. Environ Sci Pollut Res 23:19686–19695Google Scholar
  62. Fourest E, Canal C, Roux J (1994) Improvement of heavy metal biosorption by mycelial dead biomasses (Rhizopus arrhizus, Mucor miehei and Penicillium chrysogenum): pH control and cationic activation. FEMS Microbiol Rev 14:325–332PubMedGoogle Scholar
  63. de França FP, Tavares APM, da Costa ACA (2002) Calcium interference with continuous biosorption of zinc by Sargassum sp. (Phaeophyceae) in tubular laboratory reactors. Bioresour Technol 83:159–163Google Scholar
  64. Gaete Olivares H, Moyano Lagos N, Jara Gutierrez C, Carrasco Kittelsen R, Lobos Valenzuela G, Hidalgo Lillo ME (2016) Assessment oxidative stress biomarkers and metal bioaccumulation in macroalgae from coastal areas with mining activities in Chile. Environ Monit Assess 188(25)Google Scholar
  65. Ganesan M, Mairh OP, Eswaran K, Subba Rao PV (1999) Effect of salinity, light intensity and nitrogen source on growth and composition of UIlva fasciata Delile (Chlorophyta, Ulvales). Indian J Mar Sci 28:70–73Google Scholar
  66. Gao G, Liu Y, Li X, Feng Z, Xu Z, Wu H, Xu J (2017a) Expected CO2-induced ocean acidification modulates copper toxicity in the green tide alga Ulva prolifera. Environ Exp Bot 135:63–72Google Scholar
  67. Gao L, Wang Z, Shan J, Chen J, Tang C, Yi M (2017b) Aquatic environmental changes and anthropogenic activities reflected by the sedimentary records of the Shima River, Southern China. Environ Pollut 224:70–81PubMedGoogle Scholar
  68. García-Casal MN, Pereira AC, Leets I, Ramírez J, Quiroga MF (2007) High iron content and bioavailability in humans from four species of marine algae. J Nutr 137:2691–2695PubMedGoogle Scholar
  69. Garcia-Rios V, Freile-Pelegrin Y, Robledo D, Mendoza-Cozatl D, Moreno-Sanchez R, Gold-Bouchot G (2007) Cell wall composition affects Cd2+ accumulation and intracellular thiol peptides in marine red algae. Aquat Toxicol 81:65–72PubMedGoogle Scholar
  70. Girling JA, Thomas KV, Brooks SJ, Smith DJ, Shahsavari E, Ball AS (2015) A macroalgal germling bioassay to assess biocide concentrations in marine waters. Mar Poll Bull 91:82–86Google Scholar
  71. Giusti L (2001) Heavy metal contamination of brown seaweed and sediments from the UK coastline between the Wear River and the Tees River. Environ Int 26:275–286PubMedGoogle Scholar
  72. Gledhill M, Nimmo M, Hill SJ, Brown MT (1997) The toxicity of copper(II) species to marine algae, with particular reference to macroalgae. J Phycol 33:2–11Google Scholar
  73. Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818PubMedGoogle Scholar
  74. Greger M, Malm T, Kautsky L (2007) Heavy metal transfer from composted macroalgae to crops. Eur J Agron 26:257–265Google Scholar
  75. Gubelit Y, Polyak Y, Dembska G, Pazikowska-Sapota G, Zegarowski L, Kochura D, Krivorotov D, Podgornaya E, Burova O, Maazouzi C (2016) Nutrient and metal pollution of the eastern Gulf of Finland coastline: sediments, macroalgae, microbiota. Sci Total Environ 550:806–819PubMedGoogle Scholar
  76. Guiry MD (2012) How many species of algae are there? J Phycol 48:1057–1063PubMedGoogle Scholar
  77. Gumgum B, Unlu E, Tez Z, Gulsun Z (1994) Heavy-metal pollution in water, sediment and fish from the Tigris River. Chemosphere 29:111–116PubMedGoogle Scholar
  78. Gunawardena J, Egodawatta P, Ayoko GA, Goonetilleke A (2013) Atmospheric deposition as a source of heavy metals in urban stormwater. Atmos Environ 68:235–242Google Scholar
  79. Hagemann M (2016) Coping with high and variable salinity: molecular aspects of compatible solute accumulation. In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer, Dordrecht, pp 359–372Google Scholar
  80. Hamed SM, Zinta G, Klöck G, Asard H, Selim S, AbdElgawad H (2017) Zinc-induced differential oxidative stress and antioxidant responses in Chlorella sorokiniana and Scenedesmus acuminatus. Ecotoxicol Environ Saf 140:256–263PubMedGoogle Scholar
  81. Hansen HR, Hector BL, Feldmann J (2003) A qualitative and quantitative evaluation of the seaweed diet of North Ronaldsay sheep. Anim Feed Sci Technol 105:21–28Google Scholar
  82. Harrison JA, Bouwman AF, Mayorga E, Seitzinger S (2010) Magnitudes and sources of dissolved inorganic phosphorus inputs to surface fresh waters and the coastal zone: a new global model. Glob Biogeochem Cycles 24:1–16Google Scholar
  83. Henriques B, Rocha LS, Lopes CB, Figueira P, Monteiro RJR, Duarte AC, Pardal MA, Pereira E (2015) Study on bioaccumulation and biosorption of mercury by living marine macroalgae: prospecting for a new remediation biotechnology applied to saline waters. Chem Eng J 281:759–770Google Scholar
  84. Henriques B, Lopes CB, Figueira P, Rocha LS, Duarte AC, Vale C, Pardal MA, Pereira E (2017a) Bioaccumulation of Hg, Cd and Pb by Fucus vesiculosus in single and multi-metal contamination scenarios and its effect on growth rate. Chemosphere 171:208–222PubMedGoogle Scholar
  85. Henriques B, Rocha LS, Lopes CB, Figueira P, Duarte AC, Vale C, Pardal MA, Pereira E (2017b) A macroalgae-based biotechnology for water remediation: simultaneous removal of Cd, Pb and Hg by living Ulva lactuca. J Environ Manag 191:275–289Google Scholar
  86. Herrero R, Lodeiro P, Rojo R, Ciorba A, Rodríguez P, Sastre de Vicente ME (2008) The efficiency of the red alga Mastocarpus stellatus for remediation of cadmium pollution. Bioresour Technol 99:4138–4146PubMedGoogle Scholar
  87. Howarth RW, Sharpley A, Walker D (2002) Sources of nutrient pollution to coastal waters in the United States: implications for achieving coastal water quality goals. Estuaries 25:656–676Google Scholar
  88. Huang H, Liang J, Wu X, Zhang H, Li Q, Zhang Q (2013) Comparison in copper accumulation and physiological responses of Gracilaria lemaneiformis and G. lichenoides (Rhodophyceae). Chin J Oceanol Limnol 31:803–812Google Scholar
  89. Hughes TP, Kerry JT, Álvarez-Noriega M, et al (2017). Global warming and recurrent mass bleaching of corals. Nature, 543 :373–377Google Scholar
  90. Hurd CL, Harrison PJ, Bischof K, Lobban CS (2014) Seaweed ecology and physiology, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  91. Jarvis TA, Bielmyer-Fraser GK (2015) Accumulation and effects of metals in two seaweed species. Comp Biochem Physiol C 171:28–33Google Scholar
  92. Jie X, Xiaohong Z, Chunlei G, Meijie J, Ruixiang L, Zongling W, Yan L, Shiliang F, Xuelei Z (2016) Effect of temperature, salinity and irradiance on growth and photosynthesis of Ulva prolifera. Acta Oceanol Sinica 35:114–121Google Scholar
  93. Jones BG, Chenhall BE, Debretsion F, Hutton AC (2003) Geochemical comparisons between estuaries with non-industrialised and industrialised catchments: the Huon and Derwent River estuaries, Tasmania. Aust J Earth Sci 50:653–667Google Scholar
  94. Jung SM, Kang SG, Son JS, Jeon JH, Lee HJ, Shin HW (2016) Temporal and spatial variations in the proximate composition, amino acid, and mineral content of Pyropia yezoensis. J Appl Phycol 28:3459–3467Google Scholar
  95. Kaduková J, Virčíková E (2005) Comparison of differences between copper bioaccumulation and biosorption. Environ Int 31:227–232PubMedGoogle Scholar
  96. Kemp A, Horton B, Donnelly J, Mann M, Vermeer M, Rahmstorf S (2011) Climate related sea-level variations over the past two millennia. Proc Nat Acad Sci U S A 108:11017–11022Google Scholar
  97. Kidgell JT, de Nys R, Paul NA, Roberts DA (2014) The sequential application of macroalgal biosorbents for the bioremediation of a complex industrial effluent. PLoS One 9(7):e101309PubMedPubMedCentralGoogle Scholar
  98. Koch KA, Pena MMO, Thiele DJ (1997) Copper-binding motifs in catalysis, transport, detoxification and signaling. Chem Biol 4:549–560PubMedGoogle Scholar
  99. Konda N, Singh S, Simmons BA, Klein-Marcuschamer D (2015) An investigation on the economic feasibility of macroalgae as a potential feedstock for biorefineries. Bioenerg Res 8:1046–1056Google Scholar
  100. Kumar V, Sinha AK, Makkar HPS, Becker K (2010) Dietary roles of phytate and phytase in human nutrition: a review. Food Chem 120:945–959Google Scholar
  101. Kumar SD, Santhanam P, Selvaraju A, Devi S, Kumar N, Prasath B, Selvakumaran J, Thillainayagam S, Ananthi P (2014) Effect of different dosages of zinc on the growth and biomass in five marine microalgae. Int J Fish Aquat 6:1–8Google Scholar
  102. Kupper H, Kupper FC, Spiller M (1996) Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants. J Exp Bot 47:259–266Google Scholar
  103. Lee W, Wang W (2001) Metal accumulation in the green macroalga Ulva fasciata: effects of nitrate, ammonium and phosphate. Sci Total Environ 278:11–22PubMedGoogle Scholar
  104. Leung A, Cai ZW, Wong MH (2006) Environmental contamination from electronic waste recycling at Guiyu, Southeast China. J Mater Cycles Waste 8:21–33Google Scholar
  105. Liu X, Yuan W, Meng X (2017) Extraction and quantification of phlorotannins from edible brown algae. Trans ASABE 60:265–271Google Scholar
  106. Luoma S (1983) Bioavailability of trace-metals to aquatic organisms - a review. Sci Total Environ 28:1–22PubMedGoogle Scholar
  107. Ma M, Zhu W, Wang Z, Witkamp GJ (2003) Accumulation, assimilation and growth inhibition of copper on freshwater alga (Scenedesmus subspicatus 86.81 SAG) in the presence of EDTA and fulvic acid. Aquat Toxicol 63:221–228PubMedGoogle Scholar
  108. Machado L, Kinley RD, Magnusson M, de Nys R, Tomkins NW (2015) The potential of macroalgae for beef production systems in Northern Australia. J Appl Phycol 27:2001–2005Google Scholar
  109. Machado L, Magnusson M, Paul NA, Kinley R, Nys RD, Tomkins N (2016) Identification of bioactives from the red seaweed Asparagopsis taxiformis that promote antimethanogenic activity in vitro. J Appl Phycol 28:3117–3126Google Scholar
  110. Madden M, Mitra M, Ruby D, Schwarz J (2012) Seasonality of selected nutritional constituents of edible Delmarva seaweeds. J Phycol 48:1289–1298PubMedGoogle Scholar
  111. Makkar HPS, Tran G, Heuzé V, Giger-Reverdin S, Lessire M, Lebas F, Ankers P (2016) Seaweeds for livestock diets: a review. Anim Feed Sci Technol 212:1–17Google Scholar
  112. Malasarn D, Kropat J, Hsieh SI, Finazzi G, Casero D, Loo JA, Pelligrini M, Wollman F-A, Merchant SS (2013) Zinc deficiency impacts CO2 assimilation and disrupts copper homeostasis in Chlamydomonas reinhardtii. J Biol Chem 288:10672–10683PubMedPubMedCentralGoogle Scholar
  113. Malea P, Haritonidis S (1999) Seasonal accumulation of metals by red alga Gracilaria verrucosa (Huds.) Papens. from Thermaikos Gulf, Greece. J Appl Phycol 11:503–509Google Scholar
  114. Mamboya F, Lyimo TJ, Landberg T, Björk M (2009) Influence of combined changes in salinity and copper modulation on growth and copper uptake in the tropical green macroalga Ulva reticulata. Estuar Coast Shelf Sci 84:326–330Google Scholar
  115. Mantri VA, Singh RP, Bijo AJ, Kumari P, Reddy CRK, Jha B (2011) Differential response of varying salinity and temperature on zoospore induction, regeneration and daily growth rate in Ulva fasciata (Chlorophyta, Ulvales). J Appl Phycol 23:243–250Google Scholar
  116. McHugh DJ (2003) A guide to the seaweed industry. FAO Fisheries Technical Paper 441, Rome. 105 ppGoogle Scholar
  117. Medina M, Andrade S, Faugeron S, Lagos N, Mella D, Correa JA (2005) Biodiversity of rocky intertidal benthic communities associated with copper mine tailing discharges in northern Chile. Mar Poll Bull 50:396–409Google Scholar
  118. Mendes LF, Zambotti-Villela L, Colepicolo P, Marinho-Soriano E, Stevani CV, Yokoya NS (2013) Metal cation toxicity in the alga Gracilaria domingensis as evaluated by the daily growth rates in synthetic seawater. J Appl Phycol 25:1939–1947Google Scholar
  119. Mendes L, Stevani C, Zambotti-Villela L, Yokoya N, Colepicolo P (2014) Toxic effect of metal cation binary mixtures to the seaweed Gracilaria domingensis (Gracilariales, Rhodophyta). Environ Sci Pollut Res 21:8216–8223Google Scholar
  120. Merrifield ME, Ngu T, Stillman MJ (2004) Arsenic binding to Fucus vesiculosus metallothionein. Biochem Biophys Res Commun 324:127–132PubMedGoogle Scholar
  121. Michalak I, Chojnacka K, Dobrzański Z, Górecki H, Zielińska A, Korczyński M, Opaliński S (2011) Effect of macroalgae enriched with microelements on egg quality parameters and mineral content of eggs, eggshell, blood, feathers and droppings. J Anim Physiol Anim Nutr 95:374–387Google Scholar
  122. Michalak I, Chojnacka K, Korniewicz D (2015) New feed supplement from macroalgae as the dietary source of microelements for pigs. Open Chem 13:1341–1352Google Scholar
  123. Millero FJ, Woosley R, Ditrolio B, Waters J (2009) Effect of ocean acidification on the speciation of metals in seawater. Oceanography 22:72–85Google Scholar
  124. Oliveira MN, Freitas ALP, Carvalho AFU, Sampaio TMT, Farias DF, Alves Teixeira DI, Gouveia ST, Pereira JG, Sena MMCC (2009) Nutritive and non-nutritive attributes of washed-up seaweeds from the coast of Ceará, Brazil. Food Chem 115:254–259Google Scholar
  125. Moenne A, González A, Sáez CA (2016) Mechanisms of metal tolerance in marine macroalgae, with emphasis on copper tolerance in Chlorophyta and Rhodophyta. Aquat Toxicol 176:30–37PubMedGoogle Scholar
  126. Morris CA, Nicolaus B, Sampson V, Harwood JL, Kille P (1999) Identification and characterization of a recombinant metallothionein protein from a marine alga, Fucus vesiculosus. Biochem J 338:553–560PubMedPubMedCentralGoogle Scholar
  127. Morrison L, Baumann HA, Stengel DB (2008) An assessment of metal contamination along the Irish coast using the seaweed Ascophyllum nodosum (Fucales, Phaeophyceae). Environ Pollut 152:293–303PubMedGoogle Scholar
  128. Morshedi V, Nafisi Bahabadi M, Sotoudeh E, Azodi M, Hafezieh M (2018) Nutritional evaluation of Gracilaria pulvinata as partial substitute with fish meal in practical diets of barramundi (Lates calcarifer). J Appl Phycol 30:619–628Google Scholar
  129. Moutinho S, Linares F, Rodríguez JL, Sousa V, Valente LMP (2018) Inclusion of 10% seaweed meal in diets for juvenile and on-growing life stages of Senegalese sole (Solea senegalensis). J Appl Phycol.  https://doi.org/10.1007/s10811-018-1482-6
  130. Munksgaard NC, Burchert S, Kaestli M, Nowland SJ, O’Connor W, Gibb KS (2017) Cadmium uptake and zinc-cadmium antagonism in Australian tropical rock oysters: potential solutions for oyster aquaculture enterprises. Mar Poll Bull 123:47–56Google Scholar
  131. Murphy V, Hughes H, McLoughlin P (2009) Enhancement strategies for Cu(II), Cr(III) and Cr(VI) remediation by a variety of seaweed species. J Hazard Mater 166:318–326PubMedGoogle Scholar
  132. Muse JO, Stripeikis JD, Fernandez FM, d'Huicque L, Tudino MB, Carducci CN, Troccoli OE (1999) Seaweeds in the assessment of heavy metal pollution in the Gulf San Jorge, Argentina. Environ Pollut 104:315–322Google Scholar
  133. Nagai T, De Schamphelaere KAC (2016) The effect of binary mixtures of zinc, copper, cadmium, and nickel on the growth of the freshwater diatom Navicula pelliculosa and comparison with mixture toxicity model predictions. Environ Toxicol Chem 35:2765–2773PubMedGoogle Scholar
  134. Nayar S, Bott K (2014) Current status of global cultivated seaweed production and markets. World Aquacult 45:32–37Google Scholar
  135. Nejrup LB, Pedersen MF (2012) The effect of temporal variability in salinity on the invasive red alga Gracilaria vermiculophylla. Eur J Phycol 47:254–263Google Scholar
  136. Nikolic D, Milosevic N, Zivkovic Z, Mihajlovic I, Kovacevic R, Petrovic N (2011) Multi-criteria analysis of soil pollution by heavy metals in the vicinity of the copper smelting plant in Bor (Serbia). J Serb Chem Soc 76(4):625–641Google Scholar
  137. Nkemka VN, Murto M (2012) Exploring strategies for seaweed hydrolysis: effect on methane potential and heavy metal mobilisation. Process Biochem 47:2523–2526Google Scholar
  138. Nonova T, Tosheva Z (2016) Sr-90, pb-210, po-210 and Ra isotopes in marine macroalgae and mussel Mytilus galloprovincialis from the Bulgarian Black Sea zone. J Radioanal Nucl Chem 307:1183–1194Google Scholar
  139. Oh J, Choi EM, Han YS, Yoon J, Park A, Jin K, Lee J-W, Choi H, Kim S, Brown MT, Han T (2012) Influence of salinity on metal toxicity to Ulva pertusa. Toxicol Environ Health Sci 4:9–13Google Scholar
  140. Okogbue CO, Oyesanya OU, Anyiam OA, Omonona VO (2017) Assessment of pollution from produced water discharges in seawater and sediments in offshore, Niger Delta. Environ Earth Sci 76(10):359Google Scholar
  141. O'Neill A, Gupta BS, Phillips DH (2014) Distribution of arsenic and risk assessment of activities on a golf course fertilised with arsenic-containing Ascophyllum nodosum seaweed. Sci Total Environ 482:252–259PubMedGoogle Scholar
  142. Ozyigit II, Uyanik OL, Sahin NR, Yalcin IE, Demir G (2017) Monitoring the pollution level in Istanbul coast of the Sea of Marmara using algal species Ulva lactuca L. Pol J Environ Stud 26(2):773–778Google Scholar
  143. Padhi RK, Biswas S, Mohanty AK, Prabhu RK, Satpathy KK, Nayak L (2013) Temporal distribution of dissolved trace metal in the coastal waters of southwestern Bay of Bengal, India. Water Environ Res 85:696–705PubMedGoogle Scholar
  144. Paiva L, Lima E, Neto AI, Marcone M, Baptista J (2017) Health-promoting ingredients from four selected Azorean macroalgae. Food Res Int 89(1):432–438Google Scholar
  145. Pallaoro MF, Vieira FN, Hayashi L (2016) Ulva lactuca (Chlorophyta Ulvales) as co-feed for pacific white shrimp. J Appl Phycol 28:3659–3665Google Scholar
  146. Palma H, Killoran E, Sheehan M, Berner F, Heimann K (2017) Assessment of microalga biofilms for simultaneous remediation and biofuel generation in mine tailings water. Bioresour Technol 234:327–335PubMedGoogle Scholar
  147. Patarra R, Paiva L, Neto A, Lima E, Baptista J (2011) Nutritional value of selected macroalgae. J Appl Phycol 23:205–208Google Scholar
  148. Peers G, Quesnel SA, Price NM (2005) Copper requirements for iron acquisition and growth of coastal and oceanic diatoms. Limnol Oceanogr 50:1149–1158Google Scholar
  149. Peixoto M, Svendsen J, Malte H, Pereira L, Carvalho P, Pereira R, Gonçalves J, Ozório R (2016) Diets supplemented with seaweed affect metabolic rate, innate immune, and antioxidant responses, but not individual growth rate in European seabass (Dicentrarchus labrax). J Appl Phycol 28:2061–2071Google Scholar
  150. Pellegrini M, Laugier A, Sergent M, Phan-Tan-Luu R, Valls R, Pellegrini L (1993) Interactions between the toxicity of the heavy metals cadmium, copper, zinc in combinations and the detoxifying role of calcium in the brown alga Cystoseira barbata. J Appl Phycol 5:351–336Google Scholar
  151. Pereira P, de Pablo H, Rosa-Santos F, Pacheco M, Vale C (2009) Metal accumulation and oxidative stress in Ulva sp. substantiated by response integration into a general stress index. Aquat Toxicol 91:336–345PubMedGoogle Scholar
  152. Perez AA, Farias SS, Strobl AM, Perez LB, Lopez CM, Pineiro A, Roses O, Fajardo MA (2007) Levels of essential and toxic elements in Porphyra columbina and Ulva sp from San Jorge Gulf, Patagonia Argentina. Sci Total Environ 376:51–59PubMedGoogle Scholar
  153. Porse H, Rudolph B (2017) The seaweed hydrocolloid industry: 2016 updates, requirements, and outlook. J Appl Phycol 29:2187–2200Google Scholar
  154. Qiu X, Neori A, Kim JK, Yarish C, Shpigel M, Guttman L, Ben Ezra D, Odintsov V, Davis DA (2018a) Evaluation of green seaweed Ulva sp. as a replacement of fish meal in plant-based practical diets for pacific white shrimp, Litopenaeus vannamei. J Appl Phycol 30:1305–1316Google Scholar
  155. Qiu X, Neori A, Kim JK, Yarish C, Shpigel M, Guttman L, Ben Ezra D, Odintsov V, Davis DA (2018b) Green seaweed Ulva sp. as an alternative ingredient in plant-based practical diets for Pacific white shrimp, Litopenaeus vannamei. J Appl Phycol 30:1317–1333Google Scholar
  156. Quigg A (2016) Micronutrients. In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer, Dordrecht, pp 359–372Google Scholar
  157. Racionero-Gomez B, Sproson AD, Selby D, Grocke DR, Redden H, Greenwell HC (2016) Rhenium uptake and distribution in Phaeophyceae macroalgae, Fucus vesiculosus. R Soc Open Sci 3(5):1–18Google Scholar
  158. Raize O, Argaman Y, Yannai S (2004) Mechanisms of biosorption of different heavy metals by brown marine macroalgae. Biotechnol Bioeng 87:451–458PubMedGoogle Scholar
  159. Rajfur M, Klos A (2014) Use of algae in active biomonitoring of surface waters. Ecol Chem Eng Sci 21:561–576Google Scholar
  160. Rangabhashiyam S, Suganya E, Lity AV, Selvaraju N (2016) Equilibrium and kinetics studies of hexavalent chromium biosorption on a novel green macroalgae Enteromorpha sp. Res Chem Intermed 42:1275–1294Google Scholar
  161. Ratcliff JJ, Wan AHL, Edwards MD, Soler-Vila A, Johnson MP, Abreu MH, Morrison L (2016) Metal content of kelp (Laminaria digitate) co-cultivated with Atlantic salmon in an integrated multi-trophic aquaculture system. Aquaculture 459:234–243Google Scholar
  162. Reed R, Moffat L (1983) Copper toxicity and copper tolerance in Enteromorpha compressa (L.) Grev. J Exp Mar Biol Ecol 69:85–103Google Scholar
  163. Ren T, Fu G, Liu T, Hu K, Li H, Fang W, Yang X (2017) Toxicity and accumulation of zinc pyrithione in the liver and kidneys of Carassius auratus Gibelio: association with P-glycoprotein expression. Fish Physiol Biochem 43:1–9PubMedGoogle Scholar
  164. Rey-Crespo F, Lopez-Alonso M, Miranda M (2014) The use of seaweed from the Galician coast as a mineral supplement in organic dairy cattle. Animal 8:580–586PubMedGoogle Scholar
  165. Riba I, Garcia-Luque E, Blasco J, Delvalls TA (2003) Bioavailability of heavy metals bound to estuarine sediments as a function of pH and salinity values. Chem Speciat Bioavailab 15(4):101–114Google Scholar
  166. Rink L, Gabriel P (2000) Zinc and the immune system. Proc Nutr Soc 59:541–552PubMedGoogle Scholar
  167. Rjiba-Ktita S, Chermiti A, Bodas R, France J, López S (2017) Aquatic plants and macroalgae as potential feed ingredients in ruminant diets. J Appl Phycol 29:449–458Google Scholar
  168. Roberts DA, Paul NA, Cole AJ, de Nys R (2015) From waste water treatment to land management: conversion of aquatic biomass to biochar for soil amelioration and the fortification of crops with essential trace elements. J Environ Manag 157:60–68Google Scholar
  169. Romera E, Gonzalez F, Ballester A, Blazquez ML, Munoz JA (2007) Comparative study of biosorption of heavy metals using different types of algae. Bioresour Technol 98:3344–3353PubMedGoogle Scholar
  170. Rowbotham JS, Dyer PW, Greenwell HC, Selby D, Theodorou MK (2013) Copper(II)-mediated thermolysis of alginates: a model kinetic study on the influence of metal ions in the thermochemical processing of macroalgae. Interface Focus 3:1–16Google Scholar
  171. Rubio C, Napoleone G, Luis-González G, Gutiérrez AJ, González-Weller D, Hardisson A, Revert C (2017) Metals in edible seaweed. Chemosphere 173:572–579PubMedGoogle Scholar
  172. Ruperez P (2002) Mineral content of edible marine seaweeds. Food Chem 79:23–26Google Scholar
  173. Ryan S, McLoughlin P, O'Donovan O (2012) A comprehensive study of metal distribution in three main classes of seaweed. Environ Pollut 167:171–177PubMedGoogle Scholar
  174. Sáez CA, Roncarati F, Moenne A, Moody AJ, Brown MT (2015) Copper-induced intra-specific oxidative damage and antioxidant responses in strains of the brown alga Ectocarpus siliculosus with different pollution histories. Aquat Toxicol 159:81–89PubMedGoogle Scholar
  175. Sağlam E, Akçay M (2016) Chemical and mineralogical changes of waste and tailings from the murgul Cu deposit (Artvin, NE Turkey): implications for occurrence of acid mine drainage. Environ Sci Pollut Res 23:6584–6607Google Scholar
  176. Sánchez-Thomas R, Moreno-Sánchez R, García-García JD (2016) Accumulation of zinc protects against cadmium stress in photosynthetic Euglena gracilis. Environ Exp Bot 131:19–31Google Scholar
  177. Santore RC, Di Toro DM, Paquin PR, Allen HE, Meyer JS (2001) Biotic ligand model of the acute toxicity of metals. 2. Application to acute copper toxicity in freshwater fish and Daphnia. Environ Toxicol Chem 20:2397–2402PubMedGoogle Scholar
  178. Santos R, Melo RA (2018) Global shortage of technical agars: back to basics (resource management). J Appl Phycol.  https://doi.org/10.1007/s10811-018-1425-2
  179. Senthilkumar R, Vijayaraghavan K, Thilakavathi M, Iyer PVR, Velan M (2006) Seaweeds for the remediation of wastewaters contaminated with zinc(II) ions. J Hazard Mater 136:791–799PubMedGoogle Scholar
  180. Silva DM, Valente LMP, Sousa-Pinto I, Pereira R, Pires MA, Seixas F, Rema P (2014) Evaluation of IMTA-produced seaweeds (Gracilaria, Porphyra, and Ulva) as dietary ingredients in Nile tilapia, Oreochromis niloticus L. juveniles. Effects on growth performance and gut histology. J Appl Phycol 27:1671–1680Google Scholar
  181. Sondak CFA, Ang PO, Beardall J, Bellgrove A, Boo SM, Gerung GS, Hepburn CD, Hong DD, Hu Z, Kawai H, Largo D, Lee JA, Lim P-E, Mayakun J, Nelson WA, Oak JH, Phang S-M, Sahoo D, Peerapornpis Y, Yang Y, Chung IK (2017) Carbon dioxide mitigation potential of seaweed aquaculture beds (SABs). J Appl Phycol 29:2363–2373Google Scholar
  182. Sotoudeh E, Mardani F (2017) Antioxidant-related parameters, digestive enzyme activity and intestinal morphology in rainbow trout (Oncorhynchus mykiss) fry fed graded levels of red seaweed, Gracilaria pygmaea. Aquac Nutr 24:777–785Google Scholar
  183. Srinivasa Gowd S, Govil P (2008) Distribution of heavy metals in surface water of Ranipet industrial area in Tamil Nadu. India Environ Monit Assess 136:197–207PubMedGoogle Scholar
  184. Stengel DB, Macken A, Morrison L, Morley N (2004) Zinc concentrations in marine macroalgae and a lichen from western Ireland in relation to phylogenetic grouping, habitat and morphology. Mar Poll Bull 48:902–909Google Scholar
  185. Suresh Kumar K, Ganesan K, Subba Rao PV (2008) Heavy metal chelation by non-living biomass of three color forms of Kappaphycus alvarezii (Doty) Doty. J Appl Phycol 20:63–66Google Scholar
  186. Suutari M, Leskinen E, Spilling K, Kostamo K, Seppälä J (2016) Nutrient removal by biomass accumulation on artificial substrata in the northern Baltic Sea. J Appl Phycol 29:1707–1720Google Scholar
  187. 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 Agr 92:2500–2506Google Scholar
  188. Tang X, Shen C, Shi D, Cheema SA, Khan MI, Zhang C, Chen Y (2010) Heavy metal and persistent organic compound contamination in soil from Wenling: an emerging e-waste recycling city in Taizhou area, China. J Hazard Mater 173:653–660PubMedGoogle Scholar
  189. Tayyab U, Novoa-Garrido M, Roleda MY, Lind V, Weisbjerg MR (2016) Ruminal and intestinal protein degradability of various seaweed species measured in situ in dairy cows. Anim Feed Sci Technol 213:44–54Google Scholar
  190. Tibbetts SM, Milley JE, Lall SP (2016) Nutritional quality of some wild and cultivated seaweeds: nutrient composition, total phenolic content and in vitro digestibility. J Appl Phycol 28:3575–3585Google Scholar
  191. Trumbo P, Yates AA, Schlicker S, Poos M (2001) Dietary reference intakes: vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. J Am Diet Assoc 101:294–301PubMedGoogle Scholar
  192. Tseng CK (2004) The past, present and future of phycology in China. Hydrobiologia 512:11–20Google Scholar
  193. Tuhy L, Samoraj M, Basladynska S, Chojnacka K (2015) New micronutrient fertilizer biocomponents based on seaweed biomass. Pol J Environ Stud 24:2213–2221Google Scholar
  194. Turner A, Rice L (2010) Toxicity of tire wear particle leachate to the marine macroalga, Ulva lactuca. Environ Pollut 158:3650–3654PubMedGoogle Scholar
  195. Turner A, Pedroso SS, Brown MT (2008) Influence of salinity and humic substances on the uptake of trace metals by the marine macroalga, Ulva lactuca: experimental observations and modelling using WHAM. Mar Chem 110:176–184Google Scholar
  196. Turner A, Pollock H, Brown MT (2009) Accumulation of Cu and Zn from antifouling paint particles by the marine macroalga, Ulva lactuca. Environ Pollut 157:2314–2319PubMedGoogle Scholar
  197. U.S. Environmental Protection Agency (USEPA) (2000) National Recommended Water Quality Criteria; 65 FR 31682. USEPA Office of Water, Washington, DC, USA, pp 31682–31719Google Scholar
  198. Valdés FA, Gabriela Lobos M, Díaz P, Sáez CA (2018) Metal assessment and cellular accumulation dynamics in the green macroalga Ulva lactuca. J Appl Phycol 30:663–671Google Scholar
  199. Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E, van der Lelie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794Google Scholar
  200. Varol M, Şen B (2012) Assessment of nutrient and heavy metal contamination in surface water and sediments of the upper Tigris River, Turkey. Catena 92:1–10Google Scholar
  201. Viriyatum R, Boyd CE (2016) Slow-release coated copper sulfate as an algicide for aquaculture. J World Aquacult Soc 47:667–675Google Scholar
  202. Wan L, Wang N, Li Q, Sun B, Zhou Z, Xue K, Ma Z, Tian J, Song L (2007) Distribution of dissolved metals in seawater of Jinzhou Bay, China. Environ Toxicol Chem 27:43–48Google Scholar
  203. Wan A, Soler-Vila A, O’Keeffe D, Casburn P, Fitzgerald R, Johnson M (2016) The inclusion of Palmaria palmata macroalgae in Atlantic salmon (Salmo salar) diets: effects on growth, haematology, immunity and liver function. J Appl Phycol 28:3091–3100Google Scholar
  204. Wang Z, Wang X, Ke C (2014) Bioaccumulation of trace metals by the live macroalga Gracilaria lemaneiformis. J Appl Phycol 26:1889–1897Google Scholar
  205. Wassef EA, El-Sayed A-FM, Sakr EM (2013) Pterocladia (Rhodophyta) and Ulva (Chlorophyta) as feed supplements for European seabass, Dicentrarchus labrax L. fry. J Appl Phycol 25:1369–1376Google Scholar
  206. Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Smith AG, Camire ME, Brawley SH (2017) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol 29:949–982PubMedGoogle Scholar
  207. Wendt I, Arrhenius Å, Backhaus T, Hilvarsson A, Holm K, Langford K, Tunovic T, Blanck H (2013) Effects of five antifouling biocides on settlement and growth of zoospores from the marine macroalga Ulva lactuca L. Bull Environ Contam Toxicol 91:426–432PubMedGoogle Scholar
  208. Wessells KR, Brown KH (2012) Estimating the global prevalence of zinc deficiency: results based on zinc availability in national food supplies and the prevalence of stunting. PLoS One 7(11):e50568PubMedPubMedCentralGoogle Scholar
  209. Wi SG, Kim HJ, Mahadevan SA, Yang D, Bae H (2009) The potential value of the seaweed Ceylon moss (Gelidium amansii) as an alternative bioenergy resource. Bioresour Technol 100:6658–6660PubMedGoogle Scholar
  210. Wu T, Hsu Y, Sung M, Hsu Y, Lee T (2009) Expression of genes involved in redox homeostasis and antioxidant defense in a marine macroalga Ulva fasciata by excess copper. Aquat Toxicol 94:275–285PubMedGoogle Scholar
  211. Wu X, Wang G, Fu X (2014) Variations in the chemical composition of Costaria costata during harvest. J Appl Phycol 26:2389–2396Google Scholar
  212. Xu L, Wang T, Ni K, Liu S, Wang P, Xie S, Meng J, Zheng X, Lu Y (2014) Ecological risk assessment of arsenic and metals in surface sediments from estuarine and coastal areas of the southern Bohai Sea, China. Human Ecol Risk Assess 20:388–401Google Scholar
  213. Yangthong M, Hutadilok-Towatana N, Thawonsuwan J, Phromkunthong W (2016) An aqueous extract from Sargassum sp enhances the immune response and resistance against Streptococcus iniae in the asian sea bass (Lates calcarifer bloch). J Appl Phycol 28(6):3587–3598Google Scholar
  214. Yi S, Heki K, Qian A (2017) Acceleration in the global mean sea level rise: 2005–2015. Geophys Res Lett 44:11905–11913Google Scholar
  215. Yong YS, Yong WTL, Ng SE, Anton A, Yassir S (2015) Chemical composition of farmed and micropropagated Kappaphycus alvarezii (Rhodophyta, Gigartinales), a commercially important seaweed in Malaysia. J Appl Phycol 27:1271–1275Google Scholar
  216. Ytreberg E, Karlsson J, Ndungu K, Hassellov M, Breitbarth E, Eklund B (2011) Influence of salinity and organic matter on the toxicity of Cu to a brackish water and marine clone of the red macroalga Ceramium tenuicorne. Ecotoxicol Environ Saf 74:636–642PubMedGoogle Scholar
  217. Yun YS, Park D, Park JM, Volesky B (2001) Biosorption of trivalent chromium on the brown seaweed biomass. Environ Sci Technol 35:4353–4358PubMedGoogle Scholar
  218. Yunus SM, Hamzah Z, Wood AK, Ahmad (2015) Assessment of heavy metals in seawater and fish tissues at Pulau Indah, Selangor, Malaysia. AIP Conference Proceedings, 1659 (1):050007Google Scholar
  219. Zhang C, Wang J, Tan L, Chen X (2016) Toxic effects of nano-ZnO on marine microalgae Skeletonema costatum: attention to the accumulation of intracellular Zn. Aquat Toxicol 178:158–164PubMedGoogle Scholar
  220. Zhou Y, Lang RH, Dinnat EP, Le Vine DM (2017) L-band model function of the dielectric constant of seawater. IEEE Trans Geosci Remote Sens 55:6964–6974Google Scholar
  221. Zhu D, Wen X, Xuan X, Li S, Li Y (2016) The green alga Ulva lactuca as a potential ingredient in diets for juvenile white spotted snapper Lutjanus stellatus Akazaki. J Appl Phycol 28:703–711Google Scholar

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© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.North Carolina State UniversityRaleighUSA

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