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In situ relationships between spatial–temporal variations in potential ecological risk indexes for metals and the short-term effects on periphyton in a macrophyte-dominated lake: a comparison of structural and functional metrics

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Abstract

Heavy metals may adversely affect the structure and function of the periphyton community in lake ecosystems. We carried out samplings of three habitats at eight sites located in the Lake Baiyangdian that is strongly influenced by wastewater discharge (Sites 1 and 2), aquaculture and densely populated villages (Sites 3, 6, and 8), and the least disturbed (Sites 4, 5, and 7). Cu, Ni, Pb, Zn, Hg, Cd, and Cr were determined in these samples, and the periphyton community was simultaneously studied. The contamination factor (C i f ) was estimated for every metal as the ratio between pre-industrial records from sediments (C i n ) and present concentration values (C i), and the individual potential risk (E i r ) was calculated by multiply the toxic response factor (Tr i) and C i f for a given substance were based on Hakanson’s methodology. The RI was obtained for each sampling site by summing the values of E i r first and the average was calculated across the sampling sites. The results showed that the RI for all three habitats was lower than 94, and they are in decreasing order: wastewater discharge, aquaculture and densely populated villages, and the least anthropogenic impacted. When the three sampling seasons were compared, August appeared to show the highest risk, followed by April and November. The RI values showed negative correlations (r = −0.444 to −0.851, p < 0.05) with the structural and functional metrics. The best correlation was detected between chlorophyll c/chlorophyll a (Chl c/a) ratio and E i r Hg (r = −0.851, p < 0.01). Our results suggest the periphyton community can be used in bio-monitoring.

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References

  • Admiraal W, Blank H, Buckert-de Jong M, Guasch H, Ivorra N, Lehmann V, Nystrom BAH, Paulsson M, Sabater S (1999) Short-term toxicity of zinc to microbenthic algae and bacteria in a metal polluted stream. Water Res 33:1989–1996

    Article  CAS  Google Scholar 

  • Ali MB, Tripathi RD, Rai UN, Pal A, Singh SP (1999) Physico-chemical characteristics and pollution level of lake Nainital (U.P., India): role of macrophytes and phytoplankton in biomonitoring and phytoremediation of toxic metal ions. Chemosphere 39(12):2171–2182

    Article  CAS  Google Scholar 

  • An KG, Park SS, Shin JY (2002) An evaluation of a river health using the index of biological integrity along with relations to chemical and habitat conditions. Environ Int 28:411–420

    Article  CAS  Google Scholar 

  • Ancion PY, Lear G, Lewis GD (2010) Three common metal contaminants of urban runoff (Zn, Cu & Pb) accumulate in freshwater biofilm and modify embedded bacterial communities. Environ Pollut 158:2738–2745

    Article  CAS  Google Scholar 

  • Beck MW, Hatch LK, Vondracek B, Valley RD (2010) Development of a macrophyte-based index of biotoc integrity for Minnesota Lakes. Ecol Indic 10:968–979

    Article  CAS  Google Scholar 

  • Behra R, Landwehrjohann R, Vogel K, Wagner B, Sigg L (2002) Copper and zinc content of periphyton from two rivers as a function of dissolved metal concentration. Aquat Sci 64:300–306

    Article  CAS  Google Scholar 

  • Blanco S, Bécares E (2010) Are biotic indices sensitive to river toxicants? A comparison of metrics based on diatoms and macro-invertebrates. Chemosphere 79:18–25

    Article  CAS  Google Scholar 

  • Blasco P, Picó Y (2009) Prospects for combining chemical and biological methods for integrated environmental assessment. Trac-Trend Anal Chem 28(6):745–757

    Article  CAS  Google Scholar 

  • Brack W, Schmitt-Jansen M, Machala M, Brix R, Barcelo D, Schymanski E, Streck G, Schulze T (2008) How to confirm identified toxicants in effect-directed analysis. Anal Bioanal Chem 390:1959-1973

    Google Scholar 

  • Burton GA (2002) Sediment quality criteria in use around the world. Limnology 3:65–75

    Article  CAS  Google Scholar 

  • China Bureau of Environmental Protection (CBEP) (2002) Methods for monitoring and analysis of water and wastewater, 4th edn. China Environmental Science Press, Beijing (in Chinese)

    Google Scholar 

  • Clearwater SJ, Farag AM, Meyer JS (2002) Bioavailability and toxicity of dietborne copper and zinc to fish. Comp Biochem Physiol C 132:269–313

    Article  Google Scholar 

  • Constanza R, dArge R, deGroot R (1997) The values of the world’s ecosystem services and natural capital. Nature 387:253–260

    Article  Google Scholar 

  • De Jonge M, Van de Vijver B, Blust R, Bervoets L (2008) Response of aquatic organisms to metal pollution in a lowland river in Flanders: a comparsion of diatoms and macroinvertebrates. Sci Total Environ 407:615–629

    Article  Google Scholar 

  • De Schamphelaere KAC, Canll M, Van Lierde V, Forrez I, Vanhaecke F, Janssen CR (2004) Reproductive toxicity of dietary zinc to Daphnia magna. Aquat Toxicol 70:233–244

    Article  Google Scholar 

  • Duong TT, Morin S, Coste M, Herlory O, Feurtet-Mazel A, Boudou A (2010) Experimental toxicity and bioaccumulation of cadmium in freshwater periphytic diatoms in relation with biofilm maturity. Sci Total Environ 408:552–562

    Article  CAS  Google Scholar 

  • Fano EA, Mistri M, Rossi R (2003) The ecofunctional quality index (EQI): a new tool for assessing lagoonal ecosystem impairment. Estuar Coast Shelf Sci 56:709–716

    Article  Google Scholar 

  • Farag AM, Nimick DA, Kimball BA, Church SE, Harper DD, Brumbaugh WG (2007) Concentrations of metals in water, sediment, biofilm, benthic macroinvertebrates, and fish in the Boulder River watershed, Montana, and the role of colloids in metal uptake. Arch Environ Conam Toxicol 52:397–409

    Article  CAS  Google Scholar 

  • Fechner LC, Gourlay-Francé C, Uher E, Tusseau-Vuillemin MH (2010) Adapting an enzymatic toxicity test to allow comparative evaluation of natural freshwater biofilms’ tolerance to metals. Ecotoxicology 19(7):1302–1311

    Article  CAS  Google Scholar 

  • Feio MJ, Alves T, Boavida M, Medeiros A, Graca MAS (2010) Functional indicators of stream health: a river-basin approach. Freshw Biol 55:1050–1065

    Article  Google Scholar 

  • Fernandez MP, Noguerol TN, Lacorte S, Buchanan I, Piña B (2009) Toxicity identification fractionation of environmental estrogens in waste water and sludge using gas and liquid chromatography coupled to mass spectrometry and recombinant yeast assay. Anal Bioanal Chem 394:957–968

    Article  Google Scholar 

  • Gabriels W, Lock K, DePauw N, Goethals PLM (2010) Multimetric Macroinvertebrate Index Flanders (MMIF) for biological assessment of rivers and lakes in Flanders (Belgium). Limnologica 40:199–207

    Article  Google Scholar 

  • Ginebreda A, Muñoz I, López de Alda M, Brix R, López-Doval J, Barceló D (2010) Environmental risk assessment of pharmaceuticals in rivers: Relationships between hazard indexes and aquatic macroinvertebrate diversity indexes in the Llobregat River (NE Spain). Environ Int 36:153–162

    Article  CAS  Google Scholar 

  • Gold C, Feurtet-Mazel A, Coste M, Boudou A (2002) Field transfer of periphytic diatom communities to assess short-term structural effects of metals (Cd, Zn) in rivers. Water Res 36(14):3654–3664

    Article  CAS  Google Scholar 

  • Gold C, Feurtet-Mazel A, Coste M, Boudou A (2003) Effects of cadmium stress on periphytic diatom communities in indoor artificial streams. Freshw Biol 48:316–328

    Article  CAS  Google Scholar 

  • Gonzalez-Martinez MA, Puchades R, Maquieira A (2007) Optical immunosensors for environmental monitoring: How far have we come? Anal Bioanal Chem 387:205–218

    Article  CAS  Google Scholar 

  • Griffith MB, Hill BH, McCormick FH, Kaufmann PR, Herlihy AT, Selle AR (2005) Comparative application of indices of biotic integrity based on periphyton, macroinvertebrates, and fish to southern Rocky Mountain streams. Ecol Indic 5:117–136

    Article  Google Scholar 

  • Hakanson L (1980) An ecological risk index for aquatic pollution control. A sedimentological approach. Water Res 14(8):975–1001

    Article  Google Scholar 

  • Holding KL, Gill RA, Carter J (2003) The relationship between epilithic periphyton (biofilm) bound metals and metals bound to sediments in freshwater systems. Environ Geochem Health 25:87–93

    Article  CAS  Google Scholar 

  • Institute of Soil Science, Chinese Academy of Sciences, (1978). Physical and chemical analysis of soil. Shanghai Science and Technology Press, Shanghai, pp 132–136 (In Chinese)

  • Ivorra N (2000). Metal induced succession in benthic diatom Consortia. PhD Thesis. University of Amsterdam, Amsterdam

  • Ivorra N, Hettelaar J, Tubbing GMJ, Kraak MHS, Sabater S, Admiraal W (1999) Translocation of microbenthic assemblages used for in situ analysis of metal pollution in rivers. Arch Environ Contam Toxicol 37:19–28

    Article  CAS  Google Scholar 

  • Ivorra N, Hettelaar J, Kraak MHS, Sabater S, Admiraal W (2002) Responses pf biofilms to combined nutrient and metal exposure. Environ Toxicol Chem 21(3):626–632

    Article  CAS  Google Scholar 

  • Karr JR (1981) Assessment of biotic integrity using fish communities. Fisheries 6:21–27

    Article  Google Scholar 

  • Kireta AR, Reavie ED, Sgro GV, Angradi TR, Bolgrien DW, Hill BH, Jicha TM (2012) Planktonic and periphytic diatoms as indicators of stress on great rivers of the United States: Testing water quality and disturbance models. Ecol Indic 13:222–231

    Article  Google Scholar 

  • Kröncke I, Reiss H (2010) Influence of macrofauna long-term natural variability on benthic indices used in ecological quality assessment. Mar Pollut Bull 60:58–68

    Article  Google Scholar 

  • Liu GS (1996) Soil physical and chemical analyses and soil profile description. Chinese Standards Publisher, Beijing

    Google Scholar 

  • Liu JL, Li YL, Zhang B, Cao JL, Cao ZG, Domagalski J (2009) Ecological risk of heavy metals in sediments of the Luan River source water. Ecotoxicology 18(6):748–758

    Article  CAS  Google Scholar 

  • Liu ZJ, Li PY, Zhang XL, Li P, Zhu LH (2012) Regional distribution and ecological risk evaluation of heavy metals in surface sediments from coastal wetlands of the Yellow River Delta. Environ Sci 33(4):1182–1188 (in Chinese)

    Google Scholar 

  • Long ER, MacDonald DD, Smith SL, Calder FD (1995) Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments. Environ Manage 19:81–97

    Article  Google Scholar 

  • Lu RK (2000) Methods for soil agricultural chemistry analysis. Chinese Agricultural Science and Technology Press, Beijing

    Google Scholar 

  • Ma MY, Liu JL, Wang XM (2011) Biofilms as potential indicators of macrophyte-dominated lake health. Ecotoxicology 20:982–992

    Article  CAS  Google Scholar 

  • Mahmoud HMA, Goulder R, Carvalho GR (2005) The response of epilithic bacteria to different metals regime in two upland streams: assessed by conventional microbiological methods and PCR-DGGE. Arch Hydrobiol 163:405–427

    Article  CAS  Google Scholar 

  • Medley CN, Clements WH (1998) Responses of diatom communities to heavy metals in streams: the influence of longitudinal variation. Ecol Appl 8:631–644

    Article  Google Scholar 

  • Meylan S, Behra R, Sigg L (2003) Accumulation of copper and zinc in periphyton in response to dynamic variations of metal speciation in freshwater. Environ Sci Technol 37:5204–5212

    Article  CAS  Google Scholar 

  • Moore MJC, Langrehr HA, Angradi TR (2012) A submersed macrophyte index of condition for the Upper Mississippi River. Ecol Indic 13:196–205

    Article  Google Scholar 

  • Morin S, Duong TT, Dabrin A, Coynel A, Herlory O, Baudrimont M, Delmas F, Durrieu G, Schäfer J, Winterton P, Blanc G, Coste M (2008) Long-term survey of heavy-metal pollution, biofilm contamination and diatom community structure in the Riou Mort watershed, South-West France. Environ Pollut 151(3):532–542

    Article  CAS  Google Scholar 

  • Pesce S, Margoum C, Montuelle B (2010) In situ relationship between spatio-temporal variations in diuron concentrations and phototrophic biofilm tolerance in a contaminated river. Water Res 44:1941–1949

    Article  CAS  Google Scholar 

  • Rodriguez-Mozaz S, Lopez de Alda MJ, Barceló D (2006) Biosensors as useful tools for environmental analysis and monitoring. Anal Bioanal Chemosphere 386:1025–1041

    Article  CAS  Google Scholar 

  • Rothrock PE, Simon TP, Stewart PM (2008) Development, calibration, and validation of a littoral zone plant index of biotic integrity (PIBI) for lacustrine wetlands. Ecol Indic 8:79–88

    Article  Google Scholar 

  • Rushforth SR, Brotherson JD, Fungladda N, Evenson WE (1981) The effect of dissolved heavy metals on attached diatoms in the Uintah Basin of Utah, USA. Hydrobiologia 83:313–323

    Article  CAS  Google Scholar 

  • Seele J, Mayr M, Staab F, Raeder U (2000) Combination of two indication systems in pre-alpine lakes-diatom index and macrophyte index. Ecol Model 130:145–149

    Article  Google Scholar 

  • Serra A, Corcoll N, Guasch H (2009) Copper accumulation and toxicity in fluvial periphyton: the influence of exposure history. Chemosphere 74:633–641

    Article  CAS  Google Scholar 

  • Serra A, Guasch H, Admiraal W, Van der Geest HG, Van Beusekom SAM (2010) Influence of phosphorus on copper sensitivity of fluvial periphyton: the role of chemical, physiological and community-related factors. Ecotoxicology 19(4):770–780

    Article  CAS  Google Scholar 

  • Sorace A, Formichetti P, Boano A, Andreani P, Gramegna C, Mancini L (2002) The presence of a river bird, the dipper, in relation to water quality and biotic indices in central Italy. Environ Pollut 118:89–96

    Article  CAS  Google Scholar 

  • Steinberg C, Schiefele S (1988) Biological indication of trophy and pollution of running waters. Z Wasser Abwasser Forsch 21:227–234

    CAS  Google Scholar 

  • Su LY, Liu JL, Christensen P (2011) Spatial distribution and ecological risk assessment of metals in sediments of Baiyangdian wetland ecosystem. Ecotoxicology 20:1107–1116

    Article  CAS  Google Scholar 

  • ter Braak C, Smiauer P (1998). CANOCO reference manual and user’s guide to Canoco for Windows: software for canonical community ordination (version 4). Ithaca, NY

  • Tesgaye T, Sheppard D, Islam K, Tadesse W, Atalay A, Marzen L (2006) Development of chemical index as a measure of instream water quality in response to land-use and land cover changes. Water Air Soil Pollut 174:161–179

    Article  Google Scholar 

  • Tlili A, Corcoll N, Bonet B, Morin S, Montuelle B, Bérard A, Guasch H (2011) In situ spatio-temporal changes in pollution-induced community tolerance to zinc in autotrophic and heterotrophic biofilm communities. Ecotoxicology 20(8):1823–1839

    Article  CAS  Google Scholar 

  • van Dam H, Mertens A, Sinkeldam J (1994) A coded checklist and ecological indicator values of freshwater diatoms from the Netherlands. Netherlands J Aquatic Ecol 28:117–133

    Article  Google Scholar 

  • Wefering FM, Danielson LE, White NM (2000) Using the AMOEBA approach to measure progress toward ecosystem sustainability within a shellfish restoration project in North Carolina. Ecol Model 130:157–166

    Article  Google Scholar 

  • Xu FL, Tao S, Dawson RW, Li PG, Cao J (2001) Lake ecosystem health assessment: indicators and methods. Water Res 35(13):3157–3167

    Article  CAS  Google Scholar 

  • Zhou HD, Zhao J, Lu J, Wang YC, Yuan H, Wan XH (2008) Distribution, sources and ecological risk assessment of polycyclic aromatic hydrocarbons in sediments from BaiYangDian Wetland. Asian J Ecotoxicol 3:291–299 (in Chinese)

    Google Scholar 

  • Zhu JG, Chai ZY, Mao ZC (2002) Using reduction gasification-AFS method quickly measure of arsenic and mercury in the soil of organic food base. Anal Testing Technol Instrum 8(2):103–106

    Google Scholar 

  • Žižek S, Milačič R, Kovač N, Jaćimović R, Toman MJ, Horvat M (2011) Periphyton as a bioindicator of mercury pollution in a temperate torrential river ecosystem. Chemosphere 85:883–891

    Article  Google Scholar 

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Acknowledgments

This study was supported by the National Water Pollution Control Major Project of China (2008ZX07209-009, 2012ZX07203-006). We want to thank B.B. Wang for field sampling, We also want to thank Q.Y. Chen for providing critical feedback during preparation of the manuscript. Finally, we want to thank M.Y. Ma and X.M. Wang for providing some periphyton data.

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The authors declare that they have no conflict of interest.

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Correspondence to Jingling Liu.

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Zhang, L., Liu, J. In situ relationships between spatial–temporal variations in potential ecological risk indexes for metals and the short-term effects on periphyton in a macrophyte-dominated lake: a comparison of structural and functional metrics. Ecotoxicology 23, 553–566 (2014). https://doi.org/10.1007/s10646-014-1175-0

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