Abstract
Seaweeds are good bio-monitors of heavy metal pollution and have been included in European coastal monitoring programs. However, data for seaweed species in China are scarce or missing. In this study, we explored the potential of seaweeds as bio-monitor by screening the natural occurring seaweeds in the “Kingdom of seaweed and shellfish” at Dongtou Islands, the East China Sea. Totally, 12 seaweed species were collected from six sites, with richness following the sequence of Rhodophyta > Phaeophyta > Chlorophyta. The concentration of heavy metals (Cu, Cr, Ni, Zn, Pb, Cd, As) in the seaweeds was determined, and the bioaccumulation coefficient was calculated. A combination of four seaweeds, Pachydictyon coriaceum, Gelidium divaricatum, Sargassum thunbergii, and Pterocladiella capillacea, were proposed as bio-monitors due to their high bioaccumulation capabilities of specific heavy metals in the East China Sea and hence hinted the importance of using seaweed community for monitoring of pollution rather than single species. Our results provide first-hand data for the selection of bio-monitor species for heavy metals in the East China Sea and contribute to selection of cosmopolitan bio-monitor communities over geographical large area, which will benefit the establishment of monitoring programs for coastal heavy metal contamination.
Similar content being viewed by others
References
Ajjabi LC, Chouba L (2009) Biosorption of Cu2+ and Zn2+ from aqueous solutions by dried marine green macroalga Chaetomorpha linum. J Environ Manag 90:3485–3489
Akcali I, Kucuksezgin F (2011) A biomonitoring study: heavy metals in macroalgae from eastern Aegean coastal areas. Mar Pollut Bull 62:637–645
Alhomaidan AA (2008) Accumulation of nickel by marine macroalgae from the Saudi coast of the Arabian Gulf. J Food Agric Environ 6:148–151
Areco MM, Dos SAM (2010) Copper, zinc, cadmium and lead biosorption by Gymnogongrus torulosus. Thermodynamics and kinetics studies. Colloids Surf B Biointerfaces 81:620–628
Aydın-Önen S, Öztürk M (2017) Investigation of heavy metal pollution in eastern Aegean Sea coastal waters by using Cystoseira barbata, Patella caerulea, and Liza aurata as biological indicators. Environ Sci Pollut Res 24:1–25
Ballesteros E, Torras X, Pinedo S, García M, Mangialajo L, De Torres M (2007) A new methodology based on littoral community cartography dominated by macroalgae for the implementation of the European Water Framework Directive. Mar Pollut Bull 55:172–180
Brito GB, De Souza TCL, Bressy FC, Moura CWDN, Korn MGA (2012) Levels and spatial distribution of trace elements in macroalgae species from the Todos os Santos Bay, Bahia, Brazil. Mar Pollut Bull 64:2238–2244
Caixue Z, Fujin B, Xingli S, Chun-Liang C (2010) Trace elements of spring and winter macroalgae in Liusha Bay. Oceanol Limnol Sin 41:154–160 (in Chinese)
Cazon JP, Bernardelli C, Viera M, Donati ER, Guibal E (2012) Zinc and cadmium biosorption by untreated and calcium-treated Macrocystis pyrifera in a batch system. Bioresour Technol 116:195–203
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 100:61–68
Chaudhuri A, Mitra M, Havrilla C, Waguespack Y, Schwarz J (2007) Heavy metal biomonitoring by seaweeds on the Delmarva Peninsula, east coast of the USA. Bot Mar 50:151–158
Costa GB, de Felix MRL, 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 (2016) Effects of copper and lead exposure on the ecophysiology of the brown seaweed Sargassum cymosum. Protoplasma 253:111–125
Davis TA, Volesky B, Mucci A (2003) A review of the biochemistry of heavy metal biosorption by brown algae. Water Res 37:4311–4330
Diez I, Santolaria A, Secilla A, Gorostiaga JM (2009) Recovery stages over long-term monitoring of the intertidal vegetation in the ‘Abra de Bilbao’ area and on the adjacent coast (N. Spain). Eur J Phycol 44:1–14
Ding L, Huang B, Xie Y (2011) Advances and problems with the study of marine macroalgae of China seas. Biodivers Sci 19:798–804 (in Chinese)
Duan YH, Ning JS, Zhai YX, Shang DR, Zhao YF (2015) Effect of different digestion methods on the determination of inorganic elements in aquatic products by inductively coupled plasma mass spectrometry. J Food Saf Qual
Elsikaily A, Nemr AE, Khaled A (2011) Copper sorption onto dried red alga Pterocladia capillacea and its activated carbon. Chem Eng J 168:707–714
FAO (2017) FAO yearbook fishery and aquaculture statistics. 2015 (Food and Agriculture Organizarion of the United Nations)
Figueira P, Henriques B, Teixeira A, Lopes CB, Reis AT, Monteiro RJR, Duarte AC, Pardal MA, Pereira E (2016) Comparative study on metal biosorption by two macroalgae in saline waters: single and ternary systems. Environ Sci Pollut Res 23:11985–11997
Fu FF, Akagi T, Yabuki S, Iwaki M, Ogura N (2000) Distribution of rare earth elements in seaweed: implication of two different sources of rare earth elements and silicon in seaweed. J Phycol 36:62–70
Gao X, Chen CT (2012) Heavy metal pollution status in surface sediments of the coastal Bohai Bay. Water Res 46:1901–1911
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 26:275–286
Gutierrez C, Hansen HK, Hernandez P, Pinilla C (2015) Biosorption of cadmium with brown macroalgae. Chemosphere 138:164–169
Hansen HK, Ribeiro AB, Mateus EP (2006) Biosorption of arsenic(V) with Lessonia nigrescens. Miner Eng 19:486–490
He J, Chen JP (2014) A comprehensive review on biosorption of heavy metals by algal biomass: materials, performances, chemistry, and modeling simulation tools. Bioresour Technol 160:67–78
Hoek CVD, Mann DG, Jahns HM (1995) Algae: an introduction to phycology. Cambridge University Press, UK
Ibrahim WM (2011) Biosorption of heavy metal ions from aqueous solution by red macroalgae. J Hazard Mater 192:1827–1835
Jayakumar R, Rajasimman M, Karthikeyan C (2015) Optimization, equilibrium, kinetic, thermodynamic and desorption studies on the sorption of Cu(II) from an aqueous solution using marine green algae: Halimeda gracilis. Ecotoxicol Environ Saf 121:199–210
Jiang XJ, Gan WE, Han SP, Zi HJ, He YZ (2009) Design and application of a novel integrated electrochemical hydride generation cell for the determination of arsenic in seaweeds by atomic fluorescence spectrometry. Talanta 79:314–318
Juanes J, Guinda X, Puente A, Revilla J (2008) Macroalgae, a suitable indicator of the ecological status of coastal rocky communities in the NE Atlantic. Ecol Indic 8:351–359
Kamalakannan S, Batvari BPD, Lee KJ, Kannan N, Krishnamoorthy R, Shanthi K, Jayaprakash M (2008) Assessment of heavy metals (Cd, Cr and Pb) in water, sediment and seaweed (Ulva lactuca) in the Pulicat Lake, South East India. Chemosphere 71:1233–1240
Khristoforova NK, Kozhenkova SI (2002) The use of the brown algae Sargassum spp. in heavy metal monitoring of the marine environment near Vladivostok, Russia. Ocean Polar Res 24:325–329
Kravtsova A, Milchakova NA, Frontasyeva MV (2015) Levels, spatial variation and compartmentalization of trace elements in brown algae Cystoseira from marine protected areas of Crimea (Black Sea). Mar Pollut Bull 97:548–554
Kumar JIN, Oommen C, Kumar RN (2009) Biosorption of heavy metals from aqueous solution by green marine macroalgae from Okha Port, Gulf of Kutch, India. Am Eurasian J Agric Environ Sci:317–323
La Rocha SRD, Sanchezmuniz FJ, Gomezjuaristi M, Marin MTL (2009) Trace elements determination in edible seaweeds by an optimized and validated ICP-MS method. J Food Compos Anal 22:330–336
Li X, Titlyanov EA, Zhang J, Titlyanova TV, Zhang G, Huang H (2016) Macroalgal assemblage changes on coral reefs along a natural gradient from fish farms in southern Hainan Island. Aquat Ecosyst Health Manag 19:74–82
Luna AS, Costa ALH, Costa ACAD, Henriques CA (2010) Competitive biosorption of cadmium(II) and zinc(II) ions from binary systems by Sargassum filipendula. Bioresour Technol 101:5104–5111
Malea P, Kevrekidis T (2014) Trace element patterns in marine macroalgae. Sci Total Environ 494-495:144–157
Mata YN, Blazquez ML, Ballester A, Gonzalez F, Munoz JA (2009) Biosorption of cadmium, lead and copper with calcium alginate xerogels and immobilized Fucus vesiculosus. J Hazard Mater 163:555–562
MEP (2008) Specification for offshore environmental monitoring. HJ442-2008. (Ministry of Environmental Protection of the People's Republic of China)
MEP (2015) Bulletin of environment quality for coastal waters of China (Ministry of Environmental Protection of the People's Republic of China)
Murphy V, Hughes H, Mcloughlin P (2007) Cu(II) binding by dried biomass of red, green and brown macroalgae. Water Res 41:731–740
Paraskevi M, Anastasia C, Theodoros K (2015) Trace element seasonality in marine macroalgae of different functional-form groups. Mar Environ Res 103:18–26
Pavasant P, Apiratikul R, Sungkhum V, Suthiparinyanont P, Wattanachira S, Marhaba TF (2006) Biosorption of Cu2+, Cd2+, Pb2+, and Zn2+ using dried marine green macroalga Caulerpa lentillifera. Bioresour Technol 97:2321–2329
Pinedo S, García M, Satta MP, De TM, Ballesteros E (2007) Rocky-shore communities as indicators of water quality: a case study in the Northwestern Mediterranean. Mar Pollut Bull 55:126–135
Rainbow PS (1995) Biomonitoring of heavy metal availability in the marine environment. Mar Pollut Bull 31:183–192
Reis PA, Salgado MA, Vasconcelos V (2011) Barnacles as biomonitors of metal contamination in coastal waters. Estuar Coast Shelf Sci 93:269–278
Reis PA, Cassiano J, Veiga P, Rubal M, Sousa-Pinto I (2014) Fucus spiralis as monitoring tool of metal contamination in the northwest coast of Portugal under the European Water Framework Directives. Environ Monit Assess 186:5447–5460
Reis PA, Gonçalves J, Abreu H, Pereira R, Benoit M, O’Mahony F, Connellan I, Maguire J, Ozório R (2016) Seaweed Alaria esculenta as a biomonitor species of metal contamination in Aughinish Bay (Ireland). Ecol Indic 69:19–25
Ryan S, McLoughlin P, O'Donovan O (2012) A comprehensive study of metal distribution in three main classes of seaweed. Environ Pollut 167:171–177
Sawidis T, Brown MT, Zachariadis GA, Sratis I (2001) Trace metal concentrations in marine macroalgae from different biotopes in the Aegean Sea. Environ Int 27:43–47
Scherner F, Horta PA, de Oliveira EC, Simonassi JC, Hall-Spencer JM, Chow F, Nunes JMC, Pereira SMB (2013) Coastal urbanization leads to remarkable seaweed species loss and community shifts along the SW Atlantic. Mar Pollut Bull 76:106–115
Schintu M, Marras B, Durante L, Meloni P, Contu A (2010) Macroalgae and DGT as indicators of available trace metals in marine coastal waters near a lead–zinc smelter. Environ Monit Assess 167:653–661
Sheng PX, Ting Y, Chen JP, Hong L (2004) Sorption of lead, copper, cadmium, zinc, and nickel by marine algal biomass: characterization of biosorptive capacity and investigation of mechanisms. J Colloid Interface Sci 275:131–141
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 Pollut Bull 48:902–909
Tamilselvan N, Hemachandran J, Thirumalai T, Sharma CV, Kannabiran K, David E (2013) Biosorption of heavy metals from aqueous solution by Gracilaria corticata varcartecala and Grateloupia lithophila. J Coast Life Med 1:102–107
Tseng CK, Chang CF (1959) On the economic marine algal flora of the Yellow Sea and the East China Sea. Oceanol Limnol Sin 1:43–52
Varma R, Turner A, Brown MT (2011) Bioaccumulation of metals by Fucus ceranoides in estuaries of South West England. Mar Pollut Bull 62:2557–2562
Viana I, Aboal J, Fernández J, Real C, Villares R, Carballeira A (2010) Use of macroalgae stored in an Environmental Specimen Bank for application of some European Framework Directives. Water Res 44:1713–1724
Vijayaraghavan K, Jegan J, Palanivelu K, Velan M (2005) Biosorption of copper, cobalt and nickel by marine green alga Ulva reticulata in a packed column. Chemosphere 60:419–426
Wang Z, Wang X, Ke C (2014) Bioaccumulation of trace metals by the live macroalga Gracilaria lemaneiformis. J Appl Phycol 26:1889–1897. https://doi.org/10.1007/s10811-013-0222-1
Xiao X et al. (2017) Nutrient removal from Chinese coastal waters by large-scale seaweed aquaculture. Sci Rep 7
Yipmantin A, Maldonado H, Ly M, Taulemesse JM, Guibal E (2011) Pb(II) and Cd(II) biosorption on Chondracanthus chamissoi (a red alga). J Hazard Mater 185:922–929
Zhang Y, Li Y, Shi F, Sun X, Lin G (2014) Seasonal and spatial variation in species diversity, abundance, and element accumulation capacities of macroalgae in mangrove forests of Zhanjiang, China. Acta Oceanol Sin 33:73–82
Acknowledgements
This study was supported by the National Key R and D Program of China (2016YFC1402104), the National Natural Science Foundation of China (21677122), and the International Science and Technology Cooperation Program of China (2015DFA01410). We acknowledge Mr. Junyu He, Ph.D., candidate in Zhejiang University for his assistance in drawing Fig. 4.
Author information
Authors and Affiliations
Contributions
Conceived and designed the analysis: X.X., T.W., and Y.P. Sampled and identified the seaweed: T.W., T.D., X.X., Y.P., K.L., F.L., J.W., and Y.Y. Wrote the paper: Y.P., X.X., M.H., and T.W. All authors analyzed, interpreted the results, and edited the manuscript.
Corresponding author
Additional information
Responsible editor: Elena Maestri
Rights and permissions
About this article
Cite this article
Pan, Y., Wernberg, T., de Bettignies, T. et al. Screening of seaweeds in the East China Sea as potential bio-monitors of heavy metals. Environ Sci Pollut Res 25, 16640–16651 (2018). https://doi.org/10.1007/s11356-018-1612-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-018-1612-3