Skip to main content
Log in

Environmental risk of combined emerging pollutants in terrestrial environments: chlorophyll a fluorescence analysis

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The risk assessment in terrestrial environments has been scarcely studied for mixtures of organic contaminants. To estimate toxicity due to these compounds, an ecotoxicological test may be done with the appropriate organism and biomarker. Photosynthesis is principally performed at photosystem II, and its efficiency is affected by any environmental stress. Consequently, the measure of this efficiency may be a good indicator of toxicity if different parameters are employed, e.g., the quantum efficiency of photosystem II and the photochemical quenching coefficient. We did a series of assays to determine the toxicity of two organic contaminants, ibuprofen and perfluorooctanoic acid, using a higher plant (Sorghum bicolor). The results showed more toxicity for the perfluorinated compound and greater sensibility for the quantum efficiency of photosystem II. Regarding the binary combination, three methods were applied to calculate EC50: combination index, concentration addition, and independent action. Synergistic behavior is the principal toxicological profile for this mix. Therefore, the combination index, which considers interactions among chemicals, gave the best estimation to determine risk indices. We conclude that the inhibition of photosynthesis efficiency can be a useful tool to determine the toxicity of the mixtures of organic pollutants and to estimate ecological risks in terrestrial environments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Altenburger R, Walter H, Grote M (2004) What contributes to the combined effect of a complex mixture? Environ Sci Technol 38:6353–6362

    Article  CAS  Google Scholar 

  • Arrhenius A, Grönvall F, Scholze M, Backhaus T, Blanck H (2004) Predictability of the mixture of 12 similarly acting congeneric inhibitors of photosystem II in marine periphyton and epipsammon communities. Aquat Toxicol 68:351–367

    Article  CAS  Google Scholar 

  • Aznar R, Sánchez-Brunete C, Albero B, Rodríguez JA, Tadea JL (2013) Occurrence and analysis of selected pharmaceutical compounds in soil from Spanish agricultural fields. Environ Sci Pollut Res. doi:10.1007/s11356-013-2438-7

    Google Scholar 

  • Bi YF, Miao SS, Lu YC, Qiu CB, Zhou Y, Yang H (2012) Phytotoxicity, bioaccumulation and degradation of isoproturon in green algae. J Hazard Mater 243:242–249

    Article  CAS  Google Scholar 

  • Buonasera K, Lambreva M, Rea G, Touloupakis E, Giardi MT (2011) Technological applications of chlorophyll a fluorescence for the assessment of environmental pollutants. Anal Bioanal Chem 401:1139–1151

    Article  CAS  Google Scholar 

  • Cambrollé J, Mancilla-Leytón JM, Muñoz-Vallés S, Figueroa-Luque E, Luque T, Figueroa ME (2013) Evaluation of zinc tolerance and accumulation potential of the coastal shrub Limoniastrum monopetalum (L.) Boiss. Environ Exp Bot 85:50–57

    Article  Google Scholar 

  • Chou TC (2006) Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 58:621–681

    Article  CAS  Google Scholar 

  • Chou TC, Martin N (2005) CompuSyn for drug combinations: PC software and user’s guide: a computer program for quantification of synergism and antagonism in drug combinations and the determination of IC50 and ED50 and LD50 values. ComboSyn, Inc., Paramus

    Google Scholar 

  • Chou TC, Talalay P (1984) Quantitative analysis of dose–effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzym Regul 22:27–55

    Article  CAS  Google Scholar 

  • Dordio A, Ferro R, Teixera D, Palace AJ, Pinto AP, Dias CMB (2011) Study on the use of Typha spp. for the phytotreatment of water contaminated with ibuprofen. Int J Environ Anal Chem 91:654–667

    Article  CAS  Google Scholar 

  • Duan Y, Dai C, Zhang Y, Chen L (2013) Selective trace enrichment of acidic pharmaceuticals in real water and sediment samples based on solid-phase extraction using multi-templates molecularly imprinted polymers. Anal Chim Acta 758:93–100

    Article  CAS  Google Scholar 

  • EMEA (2006) European Chemical Agency. Guideline on the environmental risk assessment of medicinal products for human use, doc ref. EMEA/CHMP/SWP/4447/00

  • Faraloni C, Cutino I, Petruccelli R, Leva AR, Lazzeri S, Torzillo G (2011) Chlorophyll fluorescence techniques as a rapid tool for in vitro screening of olive cultivars (Olea europaea L.) tolerant to drought stress. Environ Exp Bot 73:49–56

    Article  CAS  Google Scholar 

  • Faust M, Altenburger R, Backhaus T, Blanck H, Boedeker W, Gramatica P, Hamer V, Scholze M, Vighi M, Grimme LH (2001) Predicting the joint algal toxicity of multi-component s-triazine mixtures at low-effect concentrations of individual toxicants. Aquat Toxicol 56:13–32

    Article  CAS  Google Scholar 

  • Furtula V, Stephenson GL, Olaveson KM, Chambers PA (2012) Effects of the veterinary pharmaceutical salinomycin and its formulation on the plant Brassica rapa. Arch Environ Contam Toxicol 63:513–522

    Article  CAS  Google Scholar 

  • González-Naranjo V, Boltes K (2013) Toxicity of ibuprofen and perfluorooctanoic acid for risk assessment of mixtures in aquatic and terrestrial environments. Int J Environ Sci Technol. doi:10.1007/s13762-013-0379-9

    Google Scholar 

  • González-Naranjo V, Boltes K, Biel M (2013) Mobility of ibuprofen, a persistent active drug, in soils irrigated with reclaimed water. Plant Soil Environ 59:68–73

    Google Scholar 

  • González-Pleiter M, Gonzalo S, Rodea-Palomares I, Leganés F, Rosal R, Boltes K, Marco E, Fernández-Piñas F (2013) Toxicity of five antibiotics and their mixtures towards photosynthetic aquatic organisms: implications for environmental risk assessment. Water Res 47:2050–2064

    Article  Google Scholar 

  • Gottschall N, Topp E, Metcalfe C, Edwards M, Payne M, Kleywegt S, Russel P, Lapen DR (2012) Pharmaceutical and personal care products in groundwater, subsurface drainage, soil, and wheat grain, following a high single application of municipal biosolids to a field. Chemosphere 87:194–203

    Article  CAS  Google Scholar 

  • Grung M, Källqvist T, Sakshaug S, Skurtveit S, Thomas KV (2008) Environmental assessment of Norwegian priority pharmaceuticals based on the EMEA guideline. Ecotoxicol Environ Saf 71:328–340

    Article  CAS  Google Scholar 

  • Higgins CP, Luthy RG (2006) Sorption of perfluorinated surfactants on sediment. Environ Sci Technol 40:7251–7256

    Article  CAS  Google Scholar 

  • Hussain MI, Reigosa MJ (2011) A chlorophyll fluorescence analysis of photosynthetic efficiency, quantum yield and photon energy dissipation in PSII antennae of Lactuca sativa L. leaves exposed to cinnamic acid. Plant Physiol Biochem 49:1290–1298

    Article  CAS  Google Scholar 

  • Ibáñez H, Ballester A, Muñoz R, Quiles MJ (2010) Chlororespiration and tolerance to drought, heat and high illumination. J Plant Physiol 167:732–738

    Article  Google Scholar 

  • Iori V, Zacchini M, Pietrini F (2013) Growth, physiological response and phytoremoval capability of two willow clones exposed to ibuprofen under hydroponic culture. J Hazard Mater 262:796–804

    Article  CAS  Google Scholar 

  • Iriel A, Novo JM, Cordon GB, Lagorio MG (2014) Atrazine and methyl viologen effects on chlorophyll-a fluorescence revisited—implications in photosystems emission and ecotoxicity assessment. Photochem Photobiol 90:107–112

    Article  CAS  Google Scholar 

  • Karnjanapiboonwong A, Suski J, Shah A, Cai Q, Morse A, Anderson T (2011) Occurrence of PPCPs at a wastewater treatment plant and in soil and groundwater at a land application site. Water Air Soil Pollut 216:257–273

    Article  CAS  Google Scholar 

  • Katayama A, Bhula R, Burns GR, Carazo E, Felsot A, Hamilton D, Harris C, Kim YH, Kleter G, Koerdel W, Linders J, Peijnenburg JGMW, Sabljic A, Stephenson RG, Racke DK, Rubin B, Tanaka K, Unsworth J, Wauchope RD (2010) Bioavailability of xenobiotics in the soil environment. Rev Environ Contam Toxicol 203:1–86

    CAS  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    Article  CAS  Google Scholar 

  • Kumar KS, Han T (2011) Toxicity of single and combined herbicides on PSII maximum efficiency of an aquatic higher plant, Lemna sp. Toxicol Environ Heal Sci 3:97–105

    Article  Google Scholar 

  • Laviale M, Morin S, Créach A (2011) Short term recovery of periphyton photosynthesis after pulse exposition to the photosystem II inhibitors atrazine and isoproturon. Chemosphere 84:731–734

    Article  CAS  Google Scholar 

  • Li F, Zhang C, Qu Y, Chen J, Chen L, Liu Y, Zhou Q (2010) Quantitative characterization of short- and long-chain perfluorinated acids in solid matrices in Shanghai, China. Sci Total Environ 408:617–623

    Article  CAS  Google Scholar 

  • Liu W, Chen S, Quan X, Jin YH (2008) Toxic effect of serial perfluorosulfonic and perfluorocarboxylic acids on the membrane system of a freshwater alga measured by flow cytometry. Environ Toxicol Chem 27:1597–1604

    Article  CAS  Google Scholar 

  • Magnusson M, Heimann K, Quayle P, Negri A (2010) Additive toxicity of herbicide mixtures and comparative sensitivity of tropical benthic microalgae. Mar Pollut Bull 60:1978–1987

    Article  CAS  Google Scholar 

  • Martín J, Camacho-Muñoz D, Santos JL, Aparicio I, Alonso E (2012) Occurrence of pharmaceutical compounds in wastewater and sludge from wastewater treatment plants: removal and ecotoxicological impact of wastewater discharges and sludge disposal. J Hazard Mater 239–240:40–47

    Article  Google Scholar 

  • Martínez-Bueno MJ, Gómez MJ, Herrera S, Hernando MD, Agüera A, Fernández-Alba AR (2012) Occurrence and persistence of organic emerging contaminants and priority pollutants in five sewage treatment plants of Spain: two years pilot survey monitoring. Environ Pollut 164:267–273

    Article  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  CAS  Google Scholar 

  • Meng J, Wang TY, Wang P, Giesy JP, Lu YL (2013) Perfluorinated compounds and organochlorine pesticides in soils around Huaihe River: a heavily contaminated waatershed in Central China. Environ Sci Pollut Res 20:3965–3974

    Article  CAS  Google Scholar 

  • Millaleo R, Reyes-Díaz M, Alberdi M, Ivanov AG, Krol M, Hüner NPA (2012) Excess manganese differentially inhibits photosystem I versus II in Arabidopsis thaliana. J Exp Bot 64(1):343–354. doi:10.1093/jxb/ers339, Advance access publication 26 November 2012

    Article  Google Scholar 

  • Naumann JC, Anderson JE, Young DR (2010) Remote detection of plant physiological responses to TNT soil contamination. Plant Soil 329:239–248

    Article  CAS  Google Scholar 

  • OECD (2003) Guidelines for the testing of chemicals. Proposal for updating guideline 208. Terrestrial plant test: 208. Seedling emergence and seedling growth test; 2003. Draft document

  • OECD (2008) Guidelines for the testing of chemicals, no. 23: guidance document on aquatic toxicity testing of difficult substances and mixtures, PDF edition (ISSN 1607-310X), 2008, 18th addendum

  • Othman HB, Leboulanger C, Le Floc’h E, Mabrouk HH, Hlaili AS (2012) Toxicity of benz(a)anthracene and fluoranthene to marine phytoplankton in culture: does cell size really matter? J Hazard Mater 243:204–211

    Article  CAS  Google Scholar 

  • Oukarroum A, Perreault F, Popovic R (2012) Interactive effects of temperature and copper on photosystem II photochemistry in Chlorella vulgaris. J Photochem Photobiol B 110:9–14

    Article  CAS  Google Scholar 

  • Perkola N, Sainio P (2013) Survey of perfluorinated alkyl acids in Finnish effluents, storm water, landfill leachate and sludge. Environ Sci Pollut Res 20:7979–7987

    Article  CAS  Google Scholar 

  • Pico Y, Blasco C, Farré M, Barceló D (2012) Occurrence of perfluorinated compounds in water and sediment of L’Albufera Natural Park (València, Spain). Environ Sci Pollut Res 19:946–957

    Article  CAS  Google Scholar 

  • Qiu Z, Wang L, Zhou Q (2013) Effects of bisphenol A on growth, photosynthesis and chlorophyll fluorescence in above-ground organs of soybean seedlings. Chemosphere 90:1274–1280

    Article  CAS  Google Scholar 

  • Ralph PJ, Smith RA, Macinnis-Ng CMO, Seery CR (2007) Use of fluorescence-based ecotoxicological bioassays in monitoring toxicants and pollution in aquatic systems: review. Toxicol Environ Chem 89:589–607

    Article  CAS  Google Scholar 

  • Redondo-Gómez S, Mateos-Naranjo E, Andrades-Moreno L (2010) Accumulation and tolerance characteristics of cadmium in a halophytic Cd-hyperaccumulator, Arthrocnemum macrostachyum. J Hazard Mater 184:299–307

    Article  Google Scholar 

  • Redondo-Gómez S, Mateos-Naranjo E, Vecino-Bueno I, Feldman SR (2011) Accumulation and tolerance characteristics of chromium in a cordgrass Cr-hyperaccumulator, Spartina argentinensis. J Hazard Mater 185:862–869

    Article  Google Scholar 

  • Regulation EC No. 1272/2008 on classification, labelling and packaging of substances and mixtures, category I, EC50<1

  • Riddell J, Padget PE, Nash TH (2012) Physiological responses of lichens to factorial fumigations with nitric acid and ozone. Environ Pollut 170:202–210

    Article  CAS  Google Scholar 

  • Rodea-Palomares I, Petre AL, Boltes K, Leganés F, Perdigón-Melón JA, Rosal R, Fernández-Piñas F (2010) Application of the combination index (CI)–isobologram equation to study the toxicological interactions of lipid regulators in two aquatic bioluminescent organisms. Water Res 44:427–438

    Article  CAS  Google Scholar 

  • Rosal R, Rodea-Palomares I, Boltes K, Fernández-Piñas F, Leganés F, Petre A (2010) Ecotoxicological assessment of surfactants in the aquatic environment: combined toxicity of docusate sodium with chlorinated pollutants. Chemosphere 81:288–293

    Article  CAS  Google Scholar 

  • Sanderson H, Johnson DJ, Wilson CJ, Brain RA, Solomon KR (2003) Probabilistic hazard assessment of environmentally occurring pharmaceuticals toxicity to fish, daphnids and algae by ECOSAR screening. Toxicol Lett 144:383–395

    Article  CAS  Google Scholar 

  • Schnell S, Bols NC, Barata C, Porte C (2009) Single and combined toxicity of pharmaceuticals and personal care products (PPCPs) on the rainbow trout liver cell line RTL-W1. Aquat Toxicol 93:244–252

    Article  CAS  Google Scholar 

  • Shan C, Liang Z (2010) Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyrum cristatum leaves under water stress. Plant Sci 178:130–139

    Article  CAS  Google Scholar 

  • Skutlarek D, Exner M, Färber H (2006) Perfluorinated surfactants in surface and drinking waters. Environ Sci Pollut Res 13:299–307

    Article  CAS  Google Scholar 

  • Stahl T, Heyn J, Thiele H, Hüther J, Failing K, Georgii S, Brunn H (2009) Carryover of perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) from soil to plant. Arch Environ Contam Toxicol 57:289–298

    Article  CAS  Google Scholar 

  • Stasinakis AS, Memigka S, Samaras VG, Farmaki E, Thomaidis NS (2012) Occurrence of endocrine disrupters and selected pharmaceuticals in Aisonas River (Greece) and environmental risk assessment using hazard indexes. Environ Sci Pollut Res 19:1574–1583

    Article  CAS  Google Scholar 

  • Strasser RJ (1978) The grouping model of plant photosynthesis. In: Akoyunoglou G (ed) Chloroplast development. Elsevier, North Holland, pp 513–524

    Google Scholar 

  • Thakkar M, Randhawa V, Wei L (2013) Comparative responses of two species of marine phytoplankton to metolachlor exposure. Aquat Toxicol 126:198–206

    Article  CAS  Google Scholar 

  • USEPA (2002) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms, 5th edn. US Environmental Protection Agency, Washington, DC EPA-812-R02-012

  • Vantová I, Bačkor M, Klejdus B, Bačkorová M, Kováčik J (2013) Copper uptake and copper-induced physiological changes in the epiphytic lichen Evernia prunastri. Plant Growth Regul 69:1–9

    Article  Google Scholar 

  • Vázquez-Roig P, Andreu V, Onghena M, Blasco C, Picó Y (2011) Assessment of the occurrence and distribution of pharmaceuticals in a Mediterranean wetland (L’Albufera, Valencia, Spain) by LC-MS/MS. Anal Bioanal Chem 40:1287–1301

    Article  Google Scholar 

  • Von der Ohe PC, Dulio V, Slobodnik J, De Deckere E, Kühne R, Ebert RU, Ginebreda A, De Cooman W, Schürmann G, Brack W (2011) A new risk assessment approach for the prioritization of 500 classical and emerging organic microcontaminants as potential river basin specific pollutants under the European Water Framework Directive. Sci Total Environ 409:2064–2077

    Article  Google Scholar 

  • Wen B, Li L, Liu Y, Zhang H, Hu X, Shan X-q, Zhan, S (2013) Mechanistic studies of perfluorooctane sulfonate, perfluorooctanoic acid uptake by maize (Zea mays L. cv. TY2). Plant Soil 370:345–354

  • Wu X, Zhu Z, Li X, Zha D (2012) Effects of cytokinin on photosynthetic gas exchange, chlorophyll fluorescence parameters and antioxidative system in seedlings of eggplant (Solanum melongena L.) under salinity stress. Acta Physiol Plant 34:2105–2114

    Article  CAS  Google Scholar 

  • Xu QS, Hu JZ, Xie KB, Yang HY, Du KH, Shi GX (2010) Accumulation and acute toxicity of silver in Potamogeton crispus L. J Hazard Mater 173:186–193

    Article  CAS  Google Scholar 

  • Xu Q, Min H, Cai S, Fu Y, Sha S, Xie K, Du K (2012) Subcellular distribution and toxicity of cadmium in Potamogeton crispus L. Chemosphere 89:114–120

    Article  CAS  Google Scholar 

  • Xu D, Li C, Chen H, Shao B (2013) Cellular response of freshwater green algae to perfluorooctanoic acid toxicity. Ecotoxicol Environ Saf 88:103–107

    Article  CAS  Google Scholar 

  • Zarco-Tejada PJ, Berni JAJ, Súarez L, Sepulcre-Cantó G, Morales F, Miller JR (2009) Imaging chlorophyll fluorescence with an airborne narrow-band multispectral camera for vegetation stress detection. Remote Sens Environ 113:1262–1275

    Article  Google Scholar 

  • Zezulka S, Kummerová M, Babula P, Váňová L (2013) Lemna minor exposed to fluoranthene: Growth, biochemical, physiological and histochemical changes. Aquat Toxicol 140–141:37–47

  • Zhao H, Chen C, Zhang X, Chen J, Quan X (2011) Phytotoxicity of PFOS and PFOA to Brassica chinensis in different Chinese soils. Ecotoxicol Environ Saf 74:1343–1347

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was funded by the next research projects: CSD2006-00044, MICINN-CGL2009-13168-C03-01, CGL2012-39520-C03-01, and P2009/AMB-1588.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Víctor González-Naranjo.

Additional information

Responsible editor: Leif Kronberg

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 311 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

González-Naranjo, V., Boltes, K., de Bustamante, I. et al. Environmental risk of combined emerging pollutants in terrestrial environments: chlorophyll a fluorescence analysis. Environ Sci Pollut Res 22, 6920–6931 (2015). https://doi.org/10.1007/s11356-014-3899-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3899-z

Keywords

Navigation