Skip to main content
SpringerLink
Log in

Combining biomarker and community approaches using benthic macroinvertebrates can improve the assessment of the ecological status of rivers

  • Review Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Indices based on community structure provide a global ecological status of the biological communities but they are of limited value as early-warning indicators of contamination. Almost two decades after the Water Framework Directive (2000/60/EC) was adopted, we reviewed publications that measured biomarkers in benthic macroinvertebrates in biomonitoring programmes of fluvial systems. The focus was on studies that attempted to incorporate both biomarkers and community-based approaches in the evaluation of the ecological status of rivers and streams. Overall, the data showed that biomarker measurements in benthic macroinvertebrate species can offer complementary information on the factors threatening these communities. This information is particularly useful for water authorities, in order to take actions before a system collapses into a state from which recovery is difficult or impossible. Gaps in need to be addressed for rapid and efficient implementation of biomarkers in benthic macroinvertebrates in routine wide-scale monitoring are discussed. In particular, site-specific baselines have to be defined, taking into account the influence of biotic and abiotic factors on these biochemical responses. Further studies, including different biomarkers, environmental stressors, macroinvertebrate taxa and river types, will provide crucial information on how to establish adequate biomarker strategies to indicate future ecological damage.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

(adapted from Conti, 2008)

Fig. 2
Fig. 3
Fig. 4

(adapted from Allan et al., 2006)

Similar content being viewed by others

References

  • Adler, R. W., 2003. The two lost books in the water quality trilogy: the elusive objectives of physical and biological integrity. Environmental Law 33: 29–77.

    Google Scholar 

  • Aebi, H., 1984. Catalase in vitro. Methods in Enzymology 105: 121–126.

    Article  CAS  PubMed  Google Scholar 

  • Aguiar, F. C., P. Segurado, G. Urbanic, J. Cambra, C. Chauvin, S. Ciadamidaro, G. Dörflinger, J. Ferreira, M. Germ, P. Manolaki, M. R. Minciardi, A. Munné, E. Papastergiadou & M. T. Ferreira, 2014. Comparability of river quality assessment using macrophytes: a multi-step procedure to overcome biogeographical differences. Science of the Total Environment 476: 757–767.

    Article  CAS  PubMed  Google Scholar 

  • Ahmad, S., 1992. Biochemical defenses of pro-oxidant plant allelochemicals by herbivorous insects. Biochemical Systematics and Ecology 20: 269–296.

    Article  CAS  Google Scholar 

  • Allan, I. J., B. Vrana, R. Greenwood, G. A. Mills, B. Roig & C. Gonzalez, 2006. A “toolbox” for biological and chemical monitoring requirements for the European Union’s Water Framework Directive. Talanta 69: 302–322.

    Article  CAS  PubMed  Google Scholar 

  • Almeida, J. R., C. Oliveira, C. Gravato & L. Guilhermino, 2010. Linking behavioural alterations with biomarkers responses in the European seabass Dicentrarchus labrax L. exposed to the organophosphate pesticide fenitrothion. Ecotoxicology 19: 1369–1381.

    Article  CAS  PubMed  Google Scholar 

  • Almeida, S. F., C. Elias, J. Ferreira, E. Tornés, C. Puccinelli, F. Delmas, G. Dörflinge, G. Urbanič, S. Marcheggiani, J. Rosebery, L. Mancini & S. Sabater, 2014. Water quality assessment of rivers using diatom metrics across Mediterranean Europe: a methods intercalibration exercise. Science of the Total Environment 476–477: 768–776.

    Article  CAS  PubMed  Google Scholar 

  • Amiard-Triquet, C., J. C. Amiard & P. S. Rainbow, 2012. Ecological Biomarkers: Indicators of Ecotoxicological Effects. CRC Press, Boca Raton.

    Google Scholar 

  • Baird, D. J. & G. A. Burton, 2001. Ecological Variability: Separating Natural from Anthropogenic Causes of Ecosystem Impairment. SETAC, Brussels.

    Google Scholar 

  • Barata, C., A. Solayan & C. Porte, 2004. Role of B-esterases in assessing toxicity of organophosphorus (chlorpyrifos, malathion) and carbamate (carbofuran) pesticides to Daphnia magna. Aquatic Toxicology 66: 125–139.

    Article  CAS  PubMed  Google Scholar 

  • Barata, C., I. Lekumberri, M. Vila-Escale, N. Prat & C. Porte, 2005. Trace metal concentration, antioxidant enzyme activities and susceptibility to oxidative stress in the tricoptera larvae Hydropsyche exocellata from the Llobregat river basin (NE Spain). Aquatic Toxicology 74: 3–19.

    Article  CAS  PubMed  Google Scholar 

  • Barata, C., J. Damásio, M. A. Lopez, M. Kuster, M. L. de Alda, D. Barcelo, M. C. Riva & D. Raldua, 2007. Combined use of biomarkers and in situ bioassays in Daphnia magna to monitor environmental hazards of pesticides in the field. Environmental Toxicology and Chemistry 26: 370–379.

    Article  CAS  PubMed  Google Scholar 

  • Berra, E., M. Forcella, R. Giacchini, L. Marziali, B. Rossaro & P. Parenti, 2004. Evaluation of enzyme biomarkers in freshwater invertebrates from Taro and Ticino river, Italy. Annales de Limnologie – International Journal of Limnology 40: 169–180.

    Article  Google Scholar 

  • Berra, E., M. Forcella, R. Giacchini, B. Rossaro & P. Parenti, 2006. Biomarkers in caddisfly larvae of the species Hydropsyche pellucidula (Curtis, 1834) (Trichoptera: Hydropsychidae) measured in natural populations and after short term exposure to fenitrothion. Bulletin of Environmental Contamination and Toxicology 76: 863–870.

    Article  CAS  PubMed  Google Scholar 

  • Binelli, A., F. Ricciardi, C. Rica & A. Provini, 2006. New evidences for old biomarkers: effects of several xenobiotics on EROD and AChE activities in zebra mussel (Dreissena polymorpha). Chemosphere 62: 510–519.

    Article  CAS  PubMed  Google Scholar 

  • Birk, S., W. Bonne, A. Borja, S. Brucet, A. Courrat, S. Poikane & W. van de Bund, 2012. Three hundred ways to assess Europe’s surface waters: an almost complete overview of biological methods to implement the Water Framework Directive. Ecological Indicators 18: 31–41.

    Article  Google Scholar 

  • Birk, S., N. J. Willby, M. G. Kelly, W. Bonne, A. Borja, S. Poikane & W. Van de Bund, 2013. Intercalibrating classifications of ecological status: Europe’s quest for common management objectives for aquatic ecosystems. Science of the Total Environment 454: 490–499.

    Article  CAS  PubMed  Google Scholar 

  • Bocchetti, R., D. Fattorini, B. Pisanelli, S. Macchia, L. Oliviero, F. Pilato, D. Pellegrini & F. Regoli, 2008. Contaminant accumulation and biomarker responses in caged mussels, Mytilus galloprovincialis, to evaluate bioavailability and toxicological effects of remobilized chemicals during dredging and disposal operations in harbour areas. Aquatic Toxicology 89: 257–266.

    Article  CAS  PubMed  Google Scholar 

  • Bonada, N., C. Zamora-Muñoz, M. Rieradevall & N. Prat, 2004. Ecological profiles of caddisfly larvae in Mediterranean streams: implications for bioassessment methods. Environmental Pollution 132: 509–521.

    Article  CAS  PubMed  Google Scholar 

  • Bonada, N., N. Prat, V. H. Resh & B. Statzner, 2006. Developments in aquatic insect biomonitoring: a comparative analysis of recent approaches. Annual Review of Entomology 51: 495–523.

    Article  CAS  PubMed  Google Scholar 

  • Bonzini, S., A. Finizio, E. Berra, M. Forcella, P. Parenti & M. Vighi, 2008. Effects of river pollution on the colonisation of artificial substrates by macrozoobenthos. Aquatic Toxicolology 89: 1–10.

    Article  CAS  Google Scholar 

  • Brack, W., V. Dulio, M. Ågerstrand, I. Allan, R. Altenburger, M. Brinkmann, et al., 2017. Towards the review of the European Union Water Framework Directive: recommendations for more efficient assessment and management of chemical contamination in European surface water resources. Science of the Total Environment 576: 720–737.

    Article  CAS  PubMed  Google Scholar 

  • Bundschuh, M. & R. Schulz, 2011. Population response to ozone application in wastewater: an on-site microcosm study with Gammarus fossarum (Crustacea: Amphipoda). Ecotoxicology 20: 466–473.

    Article  CAS  PubMed  Google Scholar 

  • Callaghan, A., G. Hirthe, T. Fisher & A. Crane, 2001. Effect of short-term exposure to chlorpyrifos on developmental parameters and biochemical biomarkers in Chironomus riparius Meigen. Ecotoxicology and Environmental Safety 50: 19–24.

    Article  CAS  PubMed  Google Scholar 

  • Carew, M. E., V. J. Pettigrove, L. Metzeling & A. A. Hoffmann, 2013. Environmental monitoring using next generation sequencing: rapid identification of macroinvertebrate bioindicator species. Frontiers in Zoology 10: 45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapman, P. M., F. Wang & S. S. Caeiro, 2013. Assessing and managing sediment contamination in transitional waters. Environment International 55: 71–91.

    Article  CAS  PubMed  Google Scholar 

  • Choi, J. H., H. Roche & T. Caquet, 2001. Hypoxia, hyperoxia and exposure to potassium dichromate or fenitrothion alter the energy metabolism in Chironomus riparius Mg. (Diptera: Chironomidae) larvae. Comparative Biochemistry & Physiology C130: 11–17.

    Google Scholar 

  • Clark, A. G., 1989. The comparative enzymology of the glutathione S-transferases from non-vertebrate organisms. Comparative Biochemistry & Physiology B 92: 419–446.

    Article  CAS  Google Scholar 

  • Clements, W. H., 2000. Integrating effects of contaminants across levels of biological organization: an overview. Journal of Aquatic Ecosystem Stress and Recovery 7: 113–116.

    Article  Google Scholar 

  • Colin, N., C. Porte, D. Fernandes, C. Barata, F. Padrós, M. Carrassón, M. Monroy, O. Cano-Rocabayera, A. de Sostoa, B. Piña & A. Maceda-Veiga, 2016. Ecological relevance of biomarkers in monitoring studies of macro-invertebrates and fish in Mediterranean rivers. Science of the Total Environment 540: 307–323.

    Article  CAS  PubMed  Google Scholar 

  • Conti, M. E. (ed.), 2008. Biological Monitoring: Theory & Application – Bioindicators and Biomarkers for Environmental Quality and Human Exposure Assessment. WIT Press, Southampton.

    Google Scholar 

  • Cook, B. D., T. J. Page & J. M. Hughes, 2008. Importance of cryptic species for identifying ‘representative’ units of biodiversity for freshwater conservation. Biological Conservation 141: 2821–2831.

    Article  Google Scholar 

  • Cossu, C., A. Doyotte, M. Babut, A. Exinger & P. Vasseur, 2000. Antioxidant biomarkers in freshwater bivalves, Unio tumidus, in response to different contamination profiles of aquatic sediments. Ecotoxicology and Environmental Safety 45: 106–121.

    Article  CAS  PubMed  Google Scholar 

  • Coulaud, R., O. Geffard, A. Vigneron, H. Queau, A. Francois & A. Chaumot, 2015. Linking feeding inhibition with reproductive impairment in gammarus confirms the ecological relevance of feeding assays in environmental monitoring. Environmental Toxicology and Chemistry 34: 1031–1038.

    Article  CAS  PubMed  Google Scholar 

  • Crane, M., W. Sildanchandra, R. Kheir & A. Callaghan, 2002. Relationship between biomarker activity and developmental endpoints in Chironomus riparius Meigen exposed to an organophosphate insecticide. Ecotoxicology and Environmental Safety 53: 361–369.

    Article  CAS  PubMed  Google Scholar 

  • Damásio, J. B., C. Barata, A. Munne, A. Ginebreda, H. Guasch, S. Sabater, J. Caixach & C. Porte, 2007. Comparing the response of biochemical indicators (biomarkers) and biological indices to diagnose the ecological impact of an oil spillage in a Mediterranean river (NE Catalunya, Spain). Chemosphere 66: 1206–1216.

    Article  CAS  PubMed  Google Scholar 

  • Damásio, J., R. Tauler, E. Teixido, M. Rieradevall, N. Prat, M. C. Riva, A. Soares & C. Barata, 2008. Combined use of Daphnia magna in situ bioassays, biomarkers and biological indices to diagnose and identify environmental pressures on invertebrate communities in two Mediterranean urbanized and industrialized rivers (NE Spain). Aquatic Toxicology 87: 310–320.

    Article  CAS  PubMed  Google Scholar 

  • Damásio, J., A. Navarro, R. Tauler, S. Lacorte, D. Barceló, A. M. V. M. Soares, M. A. López, M. C. Riva & C. Barata, 2010. Identifying major pesticides affecting bivalve species exposed to agricultural pollution using multi-biomarker and multivariate methods. Ecotoxicology 19: 1084–1094.

    Article  CAS  PubMed  Google Scholar 

  • Damásio, J., M. Fernandez-Sanjuan, J. Sanchez-Avila, S. Lacorte, N. Prat, M. Rieradevall, A. Soares & C. Barata, 2011. Multi-biochemical responses of benthic macroinvertebrate species as a complementary tool to diagnose the cause of community impairment in polluted rivers. Water Research 45: 3599–3613.

    Article  CAS  PubMed  Google Scholar 

  • de Castro-Catala, N., I. Munoz, L. Armendariz, B. Campos, D. Barcelo, J. Lopez-Doval, S. Perez, M. Petrovic, Y. Pico & J. L. Riera, 2015. Invertebrate community responses to emerging water pollutants in Iberian river basins. Science of the Total Environment 503: 142–150.

    Article  CAS  PubMed  Google Scholar 

  • de Coen, W. M., C. R. Janssen & H. Segner, 2001. The use of biomarkers in Daphnia magna toxicity testing V. In vivo alteration in the carbohydrate metabolism of Daphnia magna exposed to sublethal concentrations of mercury and lindane. Ecotoxicology and Environmental Safety 48: 223–234.

    Article  CAS  PubMed  Google Scholar 

  • de Wit, H. A., M. J. Kainz & M. Lindholm, 2012. Methylmercury bioaccumulation in invertebrates of boreal streams in Norway: effects of aqueous methylmercury and diet retention. Environmental Pollution 164: 235–241.

    Article  CAS  PubMed  Google Scholar 

  • Depledge, M. H. & M. C. Fossi, 1994. The role of biomarkers in environmental assessment. 2. Invertebrates. Ecotoxicology 3: 161–172.

    Article  CAS  PubMed  Google Scholar 

  • Diamantino, T. C., E. Almeida, A. Soares & L. Guilhermino, 2001. Lactate dehydrogenase activity as an effect criterion in toxicity tests with Daphnia magna straus. Chemosphere 45: 553–560.

    Article  CAS  PubMed  Google Scholar 

  • Dietze, U., T. Braunbeck, W. Honnen, H. R. Koehler, J. Schwaiger, H. Segner, R. Triebskorn & G. Schueuermann, 2001. Chemometric discrimination between streams based on chemical, limnological and biological data taken from freshwater fishes and their interrelationships. Journal of Aquatic Ecosystem Stress and Recovery 8: 319–336.

    Article  CAS  Google Scholar 

  • Domingues, I., A. R. Agra, K. Monaghan, A. Soares & A. J. A. Nogueira, 2010. Cholinesterase and glutathione-S-transferase activities in freshwater invertebrates as biomarkers to assess pesticide contamination. Environmental Toxicology and Chemistry 29: 5–18.

    Article  CAS  PubMed  Google Scholar 

  • Duarte, I. A., P. Reis-Santos, S. Franca, H. Cabral & V. F. Fonseca, 2017. Biomarker responses to environmental contamination in estuaries: a comparative multi-taxa approach. Aquatic Toxicology 189: 31–41.

    Article  CAS  PubMed  Google Scholar 

  • Dudgeon, D., A. H. Arthington, M. O. Gessner, Z. I. Kawabata, D. J. Knowler, C. Leveque, R. J. Naiman, A. H. Prieur-Richard, D. Soto, M. L. J. Stiassny & C. A. Sullivan, 2006. Freshwater biodiversity: importance, threats, status and conservation challenges. Biological Reviews of the Cambridge Philosophical Society 81: 163–182.

    Article  PubMed  Google Scholar 

  • EC (European Commission), 2000. Directive 2000/60/EC of the European Parliament and of the Council of 23rd October 2000 establishing a framework for community action in the field of water policy. Official Journal of the European Communities L327/1.

  • EC (European Commission), 2008a. Directive 2008/56/EC of the European Parliament and the Council of 17 June 2008 establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). Official Journal of the European Union L164/19.

  • EC (European Commission), 2008b. Commission decision of 30 October 2008 establishing, pursuant to Directive 2000/60/EC of the European Parliament and the Council, the values of the Member State monitoring system classifications as a result of the intercalibration exercise 2008/915/EC. Official Journal of the European Union L332/20.

  • EC (European Commission), 2011. Common Implementation Strategy for the Water Framework Directive (2000/60/EC). Guidance Document 14 – Guidance on the Intercalibration Process 2008–2011. Office for Official Publications of the European Communities, Luxembourg.

  • EC (European Commission), 2013. Commission Decision of 20 September 2013 establishing, pursuant to Directive 2000/60/EC of the European Parliament and of the Council, the values of the Member State monitoring system classifications as a result of the intercalibration exercise and repealing Decision 2008/915/EC. Official Journal of European Union L266/1.

  • Echeverria-Saenz, S., F. Mena, M. Pinnock, C. Ruepert, K. Solano, E. de la Cruz, B. Campos, J. Sanchez-Avila, S. Lacorte & C. Barata, 2012. Environmental hazards of pesticides from pineapple crop production in the Rio Jimenez watershed (Caribbean Coast, Costa Rica). Science of the Total Environment 440: 106–114.

    Article  CAS  PubMed  Google Scholar 

  • Elbrecht, V., E. E. Vamos, K. Meissner, J. Aroviita & F. Leese, 2017. Assessing strengths and weaknesses of DNA metabarcoding-based macroinvertebrate identification for routine stream monitoring. Methods in Ecology and Evolution 8: 1265–1275.

    Article  Google Scholar 

  • Espinosa-Diez, C., V. Miguel, D. Mennerich, T. Kietzmann, P. Sánchez-Pérez, S. Cadenas & S. Lamas, 2015. Antioxidant responses and cellular adjustments to oxidative stress. Redox Biology 6: 183–197.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • EU (European Union), 2013. Directive 2013/39/EU of the European Parliament and of the Council of 12 August 2013 amending Directives 2000/60/EC and 2008/105/EC as regards priority substances in the field of water policy 2013/39/EU. Official Journal of European Union L226/1.

  • EU (European Union), 2015. Commission Implementing Decision (EU) 2015/495 of 20 March 2015 establishing a watch list of substances for Union-wide monitoring in the field of water policy pursuant to Directive 2008/105/EC of the European Parliament and of the Council. Official Journal of the European Union L78/40.

  • Faria, M., L. Carrasco, S. Diez, M. C. Riva, J. M. Bayona & C. Barata, 2009. Multi-biomarker responses in the freshwater mussel Dreissena polymorpha exposed to polychlorobiphenyls and metals. Comparative Biochemistry & Physiology C 149: 281–288.

    Google Scholar 

  • Faria, M., D. Huertas, D. X. Soto, J. O. Grimalt, J. Catalan, M. C. Riva & C. Barata, 2010a. Contaminant accumulation and multi-biomarker responses in field collected zebra mussels (Dreissena polymorpha) and crayfish (Procambarus clarkii), to evaluate toxicological effects of industrial hazardous dumps in the Ebro River (NE Spain). Chemosphere 78: 232–240.

    Article  CAS  PubMed  Google Scholar 

  • Faria, M., M. A. López, S. Díez & C. Barata, 2010b. Are native naiads more tolerant to pollution than exotic freshwater bivalve species? An hypothesis tested using physiological responses of three species transplanted to mercury contaminated sites in the Ebro River (NE, Spain). Chemosphere 81: 1218–1226.

    Article  CAS  PubMed  Google Scholar 

  • Feio, M. J., F. C. Aguiar, S. F. Almeida, J. Ferreira, M. T. Ferreira, C. Elias, S. R. Serra, A. Buffagni, J. Cambra, C. Chauvin, F. Delmas, G. Dörflinger, S. Erba, N. Flor, M. Ferréol, M. Germ, L. Mancini, P. Manolaki, S. Marcheggiani, M. R. Minciardi, A. Munné, E. Papastergiadou, N. Prat, C. Puccinelli, J. Rosebery, S. Sabater, S. Ciadamidaro, E. Tornés, I. Tziortzis, G. Urbanič & C. Vieira, 2014a. Least disturbed conditions for European Mediterranean rivers. Science of the Total Environment 476–477: 745–756.

    Article  CAS  PubMed  Google Scholar 

  • Feio, M. J., J. Ferreira, A. Buffagni, S. Erba, G. Dorflinger, M. Ferreol, A. Munné, N. Prat, I. Tziortzis & G. Urbanič, 2014b. Comparability of ecological quality boundaries in the Mediterranean basin using freshwater benthic invertebrates. Statistical options and implications. Science of the Total Environment 476–477: 777–784.

    Article  CAS  PubMed  Google Scholar 

  • Frasco, M. F. & L. Guilhermino, 2002. Effects of dimethoate and beta-naphthoflavone on selected biomarkers of Poecilia reticulata. Fish Physiology and Biochemistry 26: 149–156.

    Article  CAS  Google Scholar 

  • Friberg, N., T. H. Andersen, H. O. Hansen, T. M. Iversen, D. Jacobsen, L. Krojgaard & S. E. Larsen, 1994. The effect of brown trout (Salmo trutta L.) on stream invertebrate drift, with special reference to Gammarus pulex L. Hydrobiologia 294: 105–110.

    Article  Google Scholar 

  • Fulton, M. H. & P. B. Key, 2001. Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environmental Toxicology and Chemistry 20: 37–45.

    Article  CAS  PubMed  Google Scholar 

  • Garcia, L. M., B. Castro & L. Guilhermino, 2000. Characterization of cholinesterase from guppy (Poecilia reticulata) muscle and it’s in vitro inhibition by environmental contaminants. Biomarkers 5: 274–284.

    Article  CAS  PubMed  Google Scholar 

  • Geist, J., 2011. Integrative freshwater ecology and biodiversity conservation. Ecological Indicators 11: 1507–1516.

    Article  Google Scholar 

  • Grant, D. F. & F. Matsumura, 1989. Glutathione S-transferase 1 and 2 in susceptible and insecticide resistant Aedes aegypti. Pesticide Biochemistry and Physiology 33: 132–143.

    Article  CAS  Google Scholar 

  • Haberhauer-Troyer, C., M. Delic, B. Gasser, D. Mattanovich, S. Hann & G. Koellensperger, 2013. Accurate quantification of the redox-sensitive GSH/GSSG ratios in the yeast Pichia pastoris by HILIC-MS/MS. Analytical and Bioanalytical Chemistry 405: 2031–2039.

    Article  CAS  PubMed  Google Scholar 

  • Hagger, J. A., M. B. Jones, D. R. P. Leonard, R. Owen & T. S. Galloway, 2006. Biomarkers and integrated environmental risk assessment: are there more questions than answers? Integrated Environmental Assessment and Management 2: 312–329.

    Article  CAS  PubMed  Google Scholar 

  • Halliwell, B. & J. M. C. Gutteridge, 1999. Free Radicals in Biology and Medicine. Oxford University Press, Oxford.

    Google Scholar 

  • Hare, L., 1992. Aquatic insects and trace metals: bioavailability, bioaccumulation and toxicology. Critical Reviews in Toxicology 22: 327–369.

    Article  CAS  PubMed  Google Scholar 

  • Hassal, K. A., 1990. Biochemistry and Use of Pesticides. Macmillan Press Ltd, Hound mills, Basingstoke.

    Book  Google Scholar 

  • Hayaoka, T. & W. C. Dauterman, 1982. Induction of Glutathione S-transferase by phenobarbital and pesticides in various housefly strains and its effect on toxicity. Pesticide Biochemistry and Physiology 17: 113–119.

    Article  CAS  Google Scholar 

  • Hering, D., A. Borja, J. Carstensen, L. Carvalho, M. Elliott, C. K. Feld, A. S. Heiskanen, R. K. Johnson, J. Moe, D. Pont, A. L. Solheim & W. van de Bund, 2010. The European Water Framework Directive at the age of 10: a critical review of the achievements with recommendations for the future. Science of the Total Environment 408: 4007–4019.

    Article  CAS  PubMed  Google Scholar 

  • Hering, D., R. K. Johnson, S. Kramm, S. Schmutz, K. Szoszkiewicz & P. F. M. Verdonschot, 2006. Assessment of European streams with diatoms, macrophytes, macroinvertebrates and fish: a comparative metric-based analysis of organism response to stress. Freshwater Biology 51: 1757–1785.

    Article  Google Scholar 

  • Hirthe, G., T. C. Fisher, M. Crane & A. Callaghan, 2001. Short-term exposure to sub-lethal doses of lindane affects developmental parameters in Chironomus riparius Meigen, but has no effect on larval glutathione-S-transferase activity. Chemosphere 44: 583–589.

    Article  CAS  PubMed  Google Scholar 

  • Hyne, R. V. & W. A. Maher, 2003. Invertebrate biomarkers: links to toxicosis that predict population decline. Ecotoxicology and Environmental Safety 54: 366–374.

    Article  CAS  PubMed  Google Scholar 

  • INAG, 2009. Critérios para a classificação do estado das massas de água superficiais − rios e albufeiras. Ministério do ambiente, do ordenamento do território e do desenvolvimento regional. Instituto da Água, I.P., Lisboa (Portuguese).

  • Jha, A. N., 2008. Ecotoxicological applications and significance of the comet assay. Mutagenesis 23: 207–221.

    Article  CAS  PubMed  Google Scholar 

  • Jo, S. H., M. K. Son, H. J. Koh, S. M. Lee, I. H. Song, Y. O. Kim, Y. S. Lee, K. S. Jeong, W. B. Kim, J. W. Park, B. J. Song & T. L. Huhe, 2001. Control of mitochondrial redox balance and cellular defence against oxidative damage by mitochondrial NADP(+)-dependent isocitrate dehydrogenase. Journal of Biological Chemistry 276: 16168–16176.

    Article  CAS  PubMed  Google Scholar 

  • Jones, C., 2008. Taxonomic sufficiency: the influence of taxonomic resolution on freshwater bioassessments using benthic macroinvertebrates. Environmental Reviews 16: 45–69.

    Article  Google Scholar 

  • Jones, H. P. & O. J. Schmitz, 2009. Rapid recovery of damaged ecosystems. PLoS ONE 4: e5653.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kavitha, P. & J. V. Rao, 2009. Sub-lethal effects of profenophos on tissue-specific antioxidant responses in a euryhyaline fish Oreochromis mossambicus. Ecotoxicology and Environmental Safety 72: 1727–1733.

    Article  CAS  PubMed  Google Scholar 

  • Kaya, H., M. Akbulut, K. Selvi, B. Ileri & M. Duysak, 2014. Heavy metal accumulation, biomarker responses and sensitivity to oxidative stress in Isopoda Asellus aquaticus from Saricay Creek (Canakkale-Turkey). Ekoloji 23: 8–15.

    Article  CAS  Google Scholar 

  • Kheir, R., H. Ibrahim, J. Lewis, A. Callaghan & M. Crane, 2001. Comparison of acetylcholinesterase and glutathione S-transferase activity in Chironomus riparius Meigen exposed to chemical-spiked sediments. Bulletin of Environmental Contamination and Toxicology 66: 603–610.

    CAS  PubMed  Google Scholar 

  • Kostaropoulos, I., A. I. Papadopoulos, A. Metaxakis, E. Boukouvala & E. Papadopoulou-Mourkidou, 2001. Glutathione S-transferase in the defence against pyrethroids in insects. Insect Biochemistry and Molecular Biology 31: 313–319.

    Article  CAS  PubMed  Google Scholar 

  • Kristoff, G., N. R. V. Guerrero & A. C. Cochon, 2008. Effects of azinphos-methyl exposure on enzymatic and non-enzymatic antioxidant defenses in Biomphalaria glabrata and Lumbriculus variegatus. Chemosphere 72: 1333–1339.

    Article  CAS  PubMed  Google Scholar 

  • Kristoff, G., N. R. V. Guerrero & A. C. Cochon, 2010. Inhibition of cholinesterases and carboxylesterases of two invertebrate species, Biomphalaria glabrata and Lumbriculus variegatus, by the carbamate pesticide carbaryl. Aquatic Toxicology 96: 115–123.

    Article  CAS  PubMed  Google Scholar 

  • Lacaze, E., A. Devaux, G. Jubeaux, R. Mons, M. Gardette, S. Bony, J. Garric & O. Geffard, 2011. DNA damage in Gammarus fossarum sperm as a biomarker of genotoxic pressure: intrinsic variability and reference level. Science of the Total Environment 409: 3230–3236.

    Article  CAS  PubMed  Google Scholar 

  • Lagadic, L., A. Cuany, J. B. Bergé & M. Echaubard, 1993. Purification and partial characterization of glutathione S-transferases from insecticide-resistant and lindane-induced susceptible Spodoptera littoralis (Boisd.) larvae. Insect Biochemistry and Molecular Biology 23: 467–474.

    Article  CAS  Google Scholar 

  • Lam, P. K. S., 2009. Use of biomarkers in environmental monitoring. Ocean & Coastal Management 52: 348–354.

    Article  Google Scholar 

  • Lee, S. M., H. J. Koh, D. C. Park, B. J. Song, T. L. Huh & J. W. Park, 2002. Cytosolic NADP(+)-dependent isocitrate dehydrogenase status modulates oxidative damage to cells. Free Radical Biology and Medicine 32: 1185–1196.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H. P., R. Hershler & K. Clift, 2003. Mitochondrial DNA sequences reveal extensive cryptic diversity within a western American springsnail. Molecular Ecology 12(10): 2771–2782.

    Article  CAS  PubMed  Google Scholar 

  • Livingstone, D. R., 1991. Organic xenobiotic metabolism in marine invertebrates. In Gilles, R. (ed.), Advances in Comparative and Environmental Physiology. Springer, Berlin: 46–185.

    Google Scholar 

  • MacNeil, C., J. T. A. Dick, E. Bigsby, R. W. Elwood, W. I. Montgomery, C. N. Gibbins & D. W. Kelly, 2002. The validity of the Gammarus asellus ratio as an index of organic pollution: abiotic and biotic influences. Water Research 36: 75–84.

    Article  CAS  PubMed  Google Scholar 

  • Maher, W., G. E. Batley & I. Lawrence, 1999. Assessing the health of sediment ecosystems: use of chemical measurements. Freshwater Biology 41: 361–372.

    Article  Google Scholar 

  • Maltby, L. & L. Hills, 2008. Spray drift of pesticides and stream macroinvertebrates: experimental evidence of impacts and effectiveness of mitigation measures. Environmental Pollution 156: 1112–1120.

    Article  CAS  PubMed  Google Scholar 

  • Maltby, L., S. A. Clayton, R. M. Wood & N. McLoughlin, 2002. Evaluation of the Gammarus pulex in situ feeding assay as a biomonitor of water quality: robustness, responsiveness, and relevance. Environmental Toxicology and Chemistry 21: 361–368.

    Article  CAS  PubMed  Google Scholar 

  • Marshall, J. C., A. L. Steward & B. D. Harch, 2006. Taxonomic resolution and quantification of freshwater macroinvertebrate samples from an Australian dryland river: the benefits and costs of using species abundance data. Hydrobiologia 572: 171–194.

    Article  Google Scholar 

  • Martinez-Haro, M., R. Beiras, J. Bellas, R. Capela, J. P. Coelho, I. Lopes, M. Moreira-Santos, A. M. Reis-Henriques, R. Ribeiro, M. M. Santos & J. C. Marques, 2015. A review on the ecological quality status assessment in aquatic systems using community based indicators and ecotoxicological tools: what might be the added value of their combination? Ecological Indicators 48: 8–16.

    Article  CAS  Google Scholar 

  • Massoulie, J., L. Pezzementi, S. Bon, E. Krejci & F. M. Vallette, 1993. Molecular and cellular biology of cholinesterases. Progress in Neurobiology 41: 31–91.

    Article  CAS  PubMed  Google Scholar 

  • Mayon, N., A. Bertrand, D. Leroy, C. Malbrouck, S. N. M. Mandiki, F. Silvestre, A. Goffart, J. P. Thome & P. Kestemont, 2006. Multiscale approach of fish responses to different types of environmental contaminations: A case study. Science of the Total Environment 367: 715–731.

    Article  CAS  PubMed  Google Scholar 

  • McCord, J. M. & I. Fridovich, 1969. Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). Journal of Biological Chemistry 244: 6049–6055.

    CAS  PubMed  Google Scholar 

  • Metcalfe-Smith, J. L., 1994. Biological water quality assessment of rivers: use of macroinvertebrate communities. In Callow, P. & G. E. Petts (eds), The Rivers Handbook, Hydrological and Ecological Principles. Blackwell Science, Oxford: 144–170.

    Google Scholar 

  • Minutoli, R., A. Granata & L. Guglielmo, 2013. Potential use of ecotoxicological biomarkers in Serratella ignita (Ephemeroptera) larvae for Alcantara river (Sicily, Italy) water quality assessment. Journal of Limnology 72: 394–399.

    Article  Google Scholar 

  • Mishra, R. & S. P. Shukla, 1997. Impact of endosulfan on lactate dehydrogenase from the freshwater catfish Clarias batrachus. Pesticide Biochemistry and Physiology 57: 220–234.

    Article  CAS  Google Scholar 

  • Morrissey, C. A., A. Boldt, A. Mapstone, J. Newton & S. J. Ormerod, 2013. Stable isotopes as indicators of wastewater effects on the macroinvertebrates of urban rivers. Hydrobiologia 700: 231–244.

    Article  CAS  Google Scholar 

  • Mouneyrac, C., P. T. Y. Leung & K. M. Y. Leung, 2011. Costs of tolerance. In Amiard-Triquet, C., P. S. Rainbow & M. Roméo (eds), Tolerance to Environmental Contaminants. Environmental and Ecological Risk Assessment Series. CRC Press, Boca Raton: 265–297.

    Google Scholar 

  • Nørum, U., N. Friberg, M. R. Jensen, J. M. Pedersen & P. Bjerregaard, 2010. Behavioural changes in three species of freshwater macroinvertebrates exposed to the pyrethroid lamda-cyhalothrin: laboratory and stream microcosm studies. Aquatic Toxicology 98: 328–335.

    Article  CAS  PubMed  Google Scholar 

  • Oakes, K. D. & G. J. van der Kraak, 2003. Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquatic Toxicology 63: 447–463.

    Article  CAS  PubMed  Google Scholar 

  • Oliveira, M., V. L. Maria, I. Ahmad, A. Serafim, M. J. Bebianno, M. Pacheco & M. A. Santos, 2009. Contamination assessment of a coastal lagoon (Ria de Aveiro, Portugal) using defence and damage biochemical indicators in gill of Liza aurata − an integrated biomarker approach. Environmental Pollution 157: 959–967.

    Article  CAS  PubMed  Google Scholar 

  • Oliveira, C., J. Almeida, L. Guilhermino, A. M. V. M. Soares & C. Gravato, 2012. Acute effects of deltamethrin on swimming velocity and biomarkers of the common prawn Palaemon serratus. Aquatic Toxicology 124: 209–216.

    Article  CAS  PubMed  Google Scholar 

  • Olsen, T., L. Ellerbeck, T. Fisher, A. Callaghan & M. Crane, 2001. Variability in acetylcholinesterase and glutathione S-transferase activities in Chironomus riparius Meigen deployed in situ at uncontaminated field sites. Environmental Toxicology and Chemistry 20: 1725–1732.

    Article  CAS  PubMed  Google Scholar 

  • Orbea, A., M. Ortiz-Zarragoitia, M. Sole, C. Porte & M. P. Cajaraville, 2002. Antioxidant enzymes and peroxisome proliferation in relation to contaminant body burdens of PAHs and PCBs in bivalve molluscs, crabs and fish from the Urdaibai and Plentzia estuaries (Bay of Biscay). Aquatic Toxicology 58: 75–98.

    Article  CAS  PubMed  Google Scholar 

  • Peña-Llopis, S., M. D. Ferrando & J. B. Peña, 2003. Fish tolerance to organophosphate-induced oxidative stress is dependent on the glutathione metabolism and enhanced by N-acetylcysteine. Chemosphere 65: 337–360.

    Google Scholar 

  • Peschke, K., J. Geburzi, H. R. Köhler, K. Wurm & R. Triebskorn, 2014. Invertebrates as indicators for chemical stress in sewage-influenced stream systems: toxic and endocrine effects in gammarids and reactions at the community level in two tributaries of Lake Constance, Schussen and Argen. Ecotoxicology and Environmental Safety 106: 115–125.

    Article  CAS  PubMed  Google Scholar 

  • Pestana, J. L. T., S. Loureiro, D. J. Baird & A. Soares, 2009. Fear and loathing in the benthos: responses of aquatic insect larvae to the pesticide imidacloprid in the presence of chemical signals of predation risk. Aquatic Toxicology 93: 138–149.

    Article  CAS  PubMed  Google Scholar 

  • Pestana, J. L. T., S. C. Novais, M. F. L. Lemos & A. Soares, 2014. Cholinesterase activity in the caddisfly Sericostoma vittatum: biochemical enzyme characterization and in vitro effects of insecticides and psychiatric drugs. Ecotoxicology and Environmental Safety 104: 263–268.

    Article  CAS  PubMed  Google Scholar 

  • Poikane, S., N. Zampoukas, A. Borja, S. P. Davies, W. van de Bund & S. Birk, 2014. Intercalibration of aquatic ecological assessment methods in the European Union: lessons learned and way forward. Environmental Science & Policy 44: 237–246.

    Article  Google Scholar 

  • Prat, N., M. Rieradevall, C. Barata & A. Munné, 2013. The combined use of metrics of biological quality and biomarkers to detect the effects of reclaimed water on macroinvertebrate assemblages in the lower part of a polluted Mediterranean river (Llobregat River, NE Spain). Ecological Indicators 24: 167–176.

    Article  CAS  Google Scholar 

  • Puértolas, L., J. Damásio, C. Barata, A. Soares & N. Prat, 2010. Evaluation of side-effects of glyphosate mediated control of giant reed (Arundo donax) on the structure and function of a nearby Mediterranean river ecosystem. Environmental Research 110: 556–564.

    Article  CAS  PubMed  Google Scholar 

  • Regoli, F., S. Gorbi, G. Frenzilli, M. Nigro, I. Corsi, S. Focardi & G. W. Winston, 2002. Oxidative stress in ecotoxicology: from the analysis of individual antioxidants to a more integrated approach. Marine Environmental Research 54: 419–423.

    Article  CAS  PubMed  Google Scholar 

  • Regoli, F., G. W. Winston, S. Gorbi, G. Frenzilli, M. Nigro, I. Corsi & S. Focardi, 2003. Integrating enzymatic responses to organic chemical exposure with total oxyradical absorbing capacity and DNA damage in the European eel Anguilla anguilla. Environmental Toxicology and Chemistry 22: 2120–2129.

    Article  CAS  PubMed  Google Scholar 

  • Reidy, G. F., H. A. Rose, S. Visetson & M. Murray, 1990. Increased glutathione S-transferase activity and glutathione content in an insecticide-resistant strain of Tribolium castaneum (Herbst). Pesticide Biochemistry and Physiology 36: 269–276.

    Article  CAS  Google Scholar 

  • Rodrigues, A. P., C. Gravato & L. Guimaraes, 2013. Involvement of the antioxidant system in differential sensitivity of Carcinus maenas to fenitrothion exposure. Environmental Science-Processes & Impacts 15: 1938–1948.

    Article  CAS  Google Scholar 

  • Rusconi, M., R. Bettinetti, S. Polesello & F. Stefani, 2018. Evolutionary toxicology as a tool to assess the ecotoxicological risk in freshwater ecosystems. Water 10: 490.

    Article  CAS  Google Scholar 

  • Sáenz, L. A., E. L. Seibert, J. Zanette, H. D. Fiedler, A. J. Curtius, J. F. Ferreira, E. A. de Almeida, M. R. F. Marques & A. C. D. Bainy, 2010. Biochemical biomarkers and metals in Perna perna mussels from mariculture zones of Santa Catarina, Brazil. Ecotoxicology and Environmental Safety 73: 796–804.

    Article  CAS  PubMed  Google Scholar 

  • Sahan, A., E. B. Kurutas & T. Altun, 2010. The determination of biochemical indicators (biomarkers) in the common carp (Cyprinus carpio) to the physico-chemical parameters of the Ceyhan River (Adana-Turkey). Ekoloji 19: 8–14.

    Article  CAS  Google Scholar 

  • Sanchez, W. & J. M. Porcher, 2009. Fish biomarkers for environmental monitoring within the Water Framework Directive of the European Union. TrAC Trends in Analytical Chemistry 28: 150–158.

    Article  CAS  Google Scholar 

  • Sanchez, W., B. Piccini, J. M. Ditche & J. M. Porcher, 2008. Assessment of seasonal variability of biomarkers in three-spined stickleback (Gasterosteus aculeatus L.) from a low contaminated stream: implication for environmental biomonitoring. Environment International 34: 791–798.

    Article  PubMed  Google Scholar 

  • Santos, C. S. A., M. S. Monteiro, A. Soares & S. Loureiro, 2012. Characterization of cholinesterases in plasma of three Portuguese native bird species: application to biomonitoring. PLoS ONE 7: e33975.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scandalios, J. G., 1993. Oxygen stress and superoxide dismutases. Plant Physiology 101: 7–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schirling, M., D. Jungmann, V. Ladewig, R. Nagel, R. Triebskorn & H. R. Kohler, 2005. Endocrine effects in Gammarus fossarum (Amphipoda): influence of wastewater effluents, temporal variability, and spatial aspects on natural populations. Archives of Environmental Contamination and Toxicology 49: 53–61.

    Article  CAS  PubMed  Google Scholar 

  • Schneider, I., J. Oehlmann & M. Oetken, 2015. Impact of an estrogenic sewage treatment plant effluent on life-history traits of the freshwater amphipod Gammarus pulex. Journal of Environmental Science and Health A 50: 272–281.

    Article  CAS  Google Scholar 

  • Schulz, R. & M. Liess, 1999. A field study of the effects of agriculturally derived insecticide input on stream macroinvertebrate dynamics. Aquatic Toxicology 46: 155–176.

    Article  CAS  Google Scholar 

  • Schulz, R. & M. Liess, 2000. Toxicity of fenvalerate to caddisfly larvae: chronic effects of 1-vs 10-h pulse-exposure with constant doses. Chemosphere 41: 1511–1517.

    Article  CAS  PubMed  Google Scholar 

  • Szakács, G., A. Váradi, C. Özvegy-Laczka & B. Sarkadi, 2008. The role of ABC transporters in drug absorption, distribution, metabolism, excretion and toxicity (ADME–Tox). Drug Discovery Today 13: 379–393.

    Article  CAS  PubMed  Google Scholar 

  • Segurado, P., N. Caiola, D. Pont, J. M. Oliveira, O. Delaigue & M. T. Ferreira, 2014. Comparability of fish-based ecological quality assessments for geographically distinct Iberian regions. Science of the Total Environment 476: 785–794.

    Article  CAS  PubMed  Google Scholar 

  • Sheehan, D. & A. Power, 1999. Effects of seasonality on xenobiotic and antioxidant defence mechanisms of bivalve molluscs. Comparative Biochemistry & Physiology C123: 193–199.

    Google Scholar 

  • Shugart, L. R., J. Bickham, G. Jackim, G. McMahon, W. Ridley, J. Stein & S. Steinert, 1992. DNA alterations. In Huggett, R. J., R. A. Kimerly, P. M. Mehrle & H. L. Bergman (eds), Biomarkers: biochemical, physiological and histological markers of anthropogenic stress. Lewis Publishers, Chelsea, MI: 155–210.

    Google Scholar 

  • Siebel, A. M., E. P. Rico, K. M. Capiotti, A. L. Piato, C. T. Cusinato, T. M. A. Franco, M. R. Bogo & C. D. Bonan, 2010. In vitro effects of antiepileptic drugs on acetylcholinesterase and ectonucleotidase activities in zebrafish (Danio rerio) brain. Toxicology 24: 1279–1284.

    CAS  Google Scholar 

  • Simić, V., A. Petrović, B. Erg, D. Dimović, J. Makovinska, B. Karadžić & M. Paunović, 2012. Indicative status assessment, biodiversity conservation, and protected areas within the Sava River Basin. In Milačič, R., J. Ščančar & Paunovič M. (eds), The Sava River. The handbook of Environmental Chemistry, Springer, Berlin, Heidelberg: 453 − 500.

  • Stegeman, J. J., M. Brouwer, T. D. G. Richard, L. Förlin, B. A. Fowler, B. M. Sanders & P. A. van Veld, 1992. Molecular responses to environmental contamination: enzyme and protein systems as indicators of chemical exposure and effect. In Huggett, R. J., R. A. Kimerly, P. M. Mehrle & H. L. Jr Bergman (eds), Biomarkers: Biochemical, Physiological and Histological markers of Anthropogenic Stress. Lewis Publishers, Chelsea, MI: 235 − 335.

  • Stohs, S. J. & D. Bagchi, 1995. Oxidative mechanisms in the toxicity of metal-ions. Free Radical Biology & Medicine 18: 321–336.

    Article  CAS  Google Scholar 

  • Sushchik, N. N., M. I. Gladyshev, A. V. Moskvichova, O. N. Makhutova & G. S. Kalachova, 2003. Comparison of fatty acid composition in major lipid classes of the dominant benthic invertebrates of the Yenisei river. Comparative Biochemistry and Physiology Part B 134: 111–122.

    Article  CAS  Google Scholar 

  • Tachet, H., P. Richoux, M. Bournaud & P. Usseglio-Polatera, 2002. Invertébrés d’eau douce. CNRS edn, Paris.

    Google Scholar 

  • van der Oost, R., J. Beyer & N. P. E. Vermeulen, 2003. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology 13: 57–149.

    Article  PubMed  Google Scholar 

  • van de Bund, W. & A. G. Solimini, 2007. Ecological Quality Ratios for Ecological Quality Assessment in Inland and Marine Waters. Institute for Environment and Sustainability, Ispra.

    Google Scholar 

  • van der Oost, R., C. Porte & N. W. Van den Brink, 2005. Biomarkers in environmental risk assessment. In den Besten, P. J. & M. Munawar (eds), Ecotoxicological Testing of Marine and Freshwaters Ecosystems: Emerging Techniques, Trends and Strategies. Taylor & Francis, London: 83–133.

    Google Scholar 

  • Viarengo, A., D. Lowe, C. Bolognesi, E. Fabbri & A. Koehler, 2007. The use of biomarkers in biomonitoring: a 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comparative Biochemistry & Physiology C 146: 281–300.

    CAS  Google Scholar 

  • Vieira, L. R., C. Gravato, A. Soares, F. Morgado & L. Guilhermino, 2009. Acute effects of copper and mercury on the estuarine fish Pomatoschistus microps: linking biomarkers to behaviour. Chemosphere 76: 1416–1427.

    Article  CAS  PubMed  Google Scholar 

  • Voulvoulis, N., K. D. Arpon & T. Giakoumis, 2017. The EU Water Framework Directive: from great expectation to problems with implementation. Science of the Total Environment 575: 358–366.

    Article  CAS  PubMed  Google Scholar 

  • Wallace, J. B. & J. R. Webster, 1996. The role of macroinvertebrates in stream ecosystem function. Annual Review of Entomology 41: 115–139.

    Article  CAS  PubMed  Google Scholar 

  • Welton, J. S., 1979. Life-history and production of the amphipod Gammarus pulex in a Dorset chalk stream. Freshwater Biology 9: 263–275.

    Article  Google Scholar 

  • Weigand, H., M. Weiss, H. Cai, Y. Li, L. Yu, C. Zhang & F. Leese, 2018. Fishing in troubled waters: revealing genomic signatures of local adaptation in response to freshwater pollutants in two macroinvertebrates. Science of the Total Environment 633: 875–891.

    Article  CAS  PubMed  Google Scholar 

  • Weiss, M., J. N. Macher, M. A. Seefeldt & F. Leese, 2014. Molecular evidence for further overlooked species within the Gammarus fossarum complex (Crustacea: Amphipoda). Hydrobiologia 721: 165–184.

    Article  CAS  Google Scholar 

  • Wiklund, A. K. E. & B. Sundelin, 2004. Biomarker sensitivity to temperature and hypoxia – a seven year field study. Marine Ecology Progress Series 274: 209–214.

    Article  Google Scholar 

  • Winston, G. W. & R. T. Di Giulio, 1991. Prooxidant and antioxidant mechanisms in aquatic organisms. Aquatic Toxicology 19: 137–161.

    Article  CAS  Google Scholar 

  • Xuereb, B., P. Noury, V. Felten, J. Garric & O. Geffard, 2007. Cholinesterase activity in Gammarus pulex (Crustacea Amphipoda): characterization and effects of chlorpyrifos. Toxicology 236: 178–189.

    Article  CAS  PubMed  Google Scholar 

  • Xuereb, B., A. Chaumot, R. Mons, J. Garric & O. Geffard, 2009. Acetylcholinesterase activity in Gammarus fossarum (Crustacea Amphipoda): intrinsic variability, reference levels, and a reliable tool for field surveys. Aquatic Toxicology 93: 225–233.

    Article  CAS  PubMed  Google Scholar 

  • Yuan, J. & H. W. Chambers, 1996. Toxicology and biochemistry of two aliesterase inhibitors as synergists of four organophosphorus insecticides in Boll Weevils (Coleoptera: Curculionidae). Pesticide Biochemistry and Physiology 54: 210–219.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The present study was supported by Foundation for Science and Technology (FCT) through a PhD grant attributed to Rodrigues C. (SFRH/BD/87695/2012). We thank the associate editor and two anonymous reviewers, whose constructive comments and suggestions were very helpful to improve the manuscript.

Author information

Authors and Affiliations

  1. Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR/CIMAR), Universidade do Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos, s/n, 4450-208, Matosinhos, Portugal

    Carolina Rodrigues, Laura Guimarães & Natividade Vieira

  2. Departamento de Biologia da Faculdade de Ciências da Universidade do Porto, Rua do Campo Alegre, s/n, 4169-007, Porto, Portugal

    Carolina Rodrigues & Natividade Vieira

Authors
  1. Carolina Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laura Guimarães
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natividade Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carolina Rodrigues.

Additional information

Handling editor: Katya E. Kovalenko

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rodrigues, C., Guimarães, L. & Vieira, N. Combining biomarker and community approaches using benthic macroinvertebrates can improve the assessment of the ecological status of rivers. Hydrobiologia 839, 1–24 (2019). https://doi.org/10.1007/s10750-019-03991-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-019-03991-7

Keywords

Search

Navigation