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Hydrobiologia

, Volume 773, Issue 1, pp 87–102 | Cite as

Litter breakdown for ecosystem integrity assessment also applies to streams affected by pesticides

  • Brosed MagaliEmail author
  • Lamothe Sylvain
  • Chauvet Eric
Primary Research Paper

Abstract

While the impact of various anthropogenic alterations, e.g. nutrient enrichment, has been documented on leaf litter breakdown—a key process for stream ecosystems—, our objective was to assess the response of this process to pesticides in agricultural streams. We hypothesized the impairment to be correlated with the pesticides contamination gradient, and the invertebrate decomposers to be more affected than microbial ones. Alder total breakdown rate was found to strongly decrease along the pesticide concentration in 12 French streams, only due to invertebrate-driven breakdown (as determined in coarse-mesh bags) since microbial-driven breakdown (fine-mesh bags) remained unchanged. Coherently, litter-associated shredder taxa richness and abundance together with SPEARpesticide (a specific indicator based on invertebrate traits) were greatly reduced, whereas pesticide toxicity did not affect litter-associated fungal biomass and taxa richness. Consequently, the presence of pesticides compromised leaf breakdown, as microbial decomposers did not compensate for the invertebrate decomposers decline. This occurred while pesticides concentrations even in the most contaminated stream were under the European Union’s Uniform Principles thresholds for targeted species. Our study showed that litter breakdown, particularly the ratio of total to microbial-driven breakdown rate, is a pertinent proxy to assess the functional integrity of pesticide-contaminated streams.

Keywords

Decomposition rate Fungi Shredders SPEARpesticide Toxic units 

Notes

Acknowledgments

We thank two anonymous reviewers for their helpful comments. We are very grateful to Didier Lambrigot and Robert Fernandez for ergosterol determination and field assistance and to Margaux Saüt and coworkers from the Adour-Garonne Water Agency for providing water chemistry data. This work was financially supported by the CIFRE PhD Plan of the French Association for Research and Technology, the Adour-Garonne Water Agency, Asconit Consultants and the Centre National de la Recherche Scientifique (CNRS).

Supplementary material

10750_2016_2681_MOESM1_ESM.docx (72 kb)
Supplementary material 1 (DOCX 71 kb)
10750_2016_2681_MOESM2_ESM.docx (57 kb)
Supplementary material 2 (DOCX 56 kb)
10750_2016_2681_MOESM3_ESM.docx (63 kb)
Supplementary material 3 (DOCX 63 kb)

References

  1. Alexander, A. C., J. M. Culp, K. Liber & A. J. Cessna, 2007. Effects of insecticide exposure on feeding inhibition in mayflies and oligochaetes. Environmental Toxicology and Chemistry 26: 1726–1732.CrossRefPubMedGoogle Scholar
  2. Artigas, J., J. Majerholc, A. Foulquier, C. Margoum, B. Volat, M. Neyra & S. Pesce, 2012. Effects of the fungicide tebuconazole on microbial capacities for litter breakdown in streams. Aquatic Toxicology 122–123: 197–205.CrossRefPubMedGoogle Scholar
  3. Backhaus, T. & M. Faust, 2012. Predictive environmental risk assessment of chemical mixtures: a conceptual framework. Environmental Science and Technology 46: 2564–2573.CrossRefPubMedGoogle Scholar
  4. Baldy, V., V. Gobert, F. Guérold, E. Chauvet, D. Lambrigot & J.-Y. Charcosset, 2007. Leaf litter breakdown budgets in streams of various trophic status: effects of dissolved inorganic nutrients on microorganisms and invertebrates. Freshwater Biology 52: 1322–1335.CrossRefGoogle Scholar
  5. Bärlocher, F., 1980. Leaf-eating invertebrates as competitors of aquatic hyphomycetes. Oecologia 47: 303–306.CrossRefGoogle Scholar
  6. Beketov, M. A., K. Foit, R. B. Schäfer, C. A. Schriever, A. Sacchi, E. Capri, J. Biggs, C. Wells & M. Liess, 2009. SPEAR indicates pesticide effects in streams – comparative use of species- and family-level biomonitoring data. Environmental Pollution 157: 1841–1848.CrossRefPubMedGoogle Scholar
  7. Beketov, M. A., B. J. Kefford, R. B. Schäfer & M. Liess, 2013. Pesticides reduce regional biodiversity of stream invertebrates. Proceedings of the National Academy of Sciences of the United States of America 110: 11039–11043.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bermingham, S., P. Fisher, A. Martin, M. Marriott & H. Lappin-Scott, 1998. The effect of the herbicide mecoprop on Heliscus lugdunensis and its influence on the preferential feeding of Gammarus pseudolimnaeus. Microbial Ecology 35: 199–204.CrossRefPubMedGoogle Scholar
  9. Brock, T. C., G. H. Arts, L. Maltby & P. J. Van den Brink, 2006. Aquatic risks of pesticides, ecological protection goals, and common aims in European Union legislation. Integrated Environmental Assessment and Management 2: 20–46.CrossRefGoogle Scholar
  10. Bundschuh, M., J. P. Zubrod, P. Klemm, D. Elsaesser, C. Stang & R. Schulz, 2013. Effects of peak exposure scenarios on Gammarus fossarum using field relevant pesticide mixtures. Ecotoxicology and Environmental Safety 95: 137–143.CrossRefPubMedGoogle Scholar
  11. Bunn, S. E. & P. M. Davies, 2000. Biological processes in running waters and their implications for the assessment of ecological integrity. Hydrobiologia 422(423): 61–70.CrossRefGoogle Scholar
  12. Bunzel, K., M. Kattwinkel & M. Liess, 2013. Effects of organic pollutants from wastewater treatment plants on aquatic invertebrate communities. Water Research 47: 597–606.CrossRefPubMedGoogle Scholar
  13. Campos, D., A. Alves, M. F. L. Lemos, A. Correia, A. M. V. M. Soares & J. L. T. Pestana, 2014. Effects of cadmium and resource quality on freshwater detritus processing chains: a microcosm approach with two insect species. Ecotoxicology 23: 830–839.CrossRefPubMedGoogle Scholar
  14. Carlisle, D. M. & W. H. Clements, 2005. Leaf litter breakdown, microbial respiration and shredder production in metal-polluted streams. Freshwater Biology 50: 380–390.CrossRefGoogle Scholar
  15. Chandrashekar, K. R. & K. M. Kaveriappa, 1989. Effect of pesticides on the growth of aquatic hyphomycetes. Toxicology Letters 48: 311–315.CrossRefPubMedGoogle Scholar
  16. Chauvet, E., 1990. Hyphomycètes aquatiques du sud-ouest de la France. Gaussenia 6: 3–31.Google Scholar
  17. Cheng, Z. L., P. Andre & C. Chiang, 1997. Hyphomycetes and macroinvertebrates colonizing leaf litter in two Belgian streams with contrasting water quality. Limnetica 13: 57–63.Google Scholar
  18. Dalton, S. A., M. Hodkinson & K. A. Smith, 1970. Interactions between DDT and river fungi. Applied Microbiology 20: 662–666.PubMedPubMedCentralGoogle Scholar
  19. Dijksterhuis, J., T. Van Doorn, R. Samson & J. Postma, 2011. Effects of seven fungicides on non-target aquatic fungi. Water, Air, and Soil Pollution 222: 421–425.CrossRefPubMedPubMedCentralGoogle Scholar
  20. ECOTOX Database. US Environmental Protection Agency [available on internet at http://cfpub.epa.gov/ecotox/ecotox_home.cfm].
  21. EEC, 1991. Council Directive of 15 July 1991 Concerning the Placing of Plant Protection Products on the Market (91/414/EEC).Google Scholar
  22. Elosegi, A. & S. Sabater, 2013. Effects of hydromorphological impacts on river ecosystem functioning: a review and suggestions for assessing ecological impacts. Hydrobiologia 712: 129–143.CrossRefGoogle Scholar
  23. Englert, D., J. P. Zubrod, R. Schulz & M. Bundschuh, 2015. Variability in ecosystem structure and functioning in a low order stream: implications of land use and season. Science of the Total Environment 538: 341–349.CrossRefPubMedGoogle Scholar
  24. Fernández, D., K. Voss, M. Bundschuh, J. P. Zubrod & R. B. Schäfer, 2015. Effects of fungicides on decomposer communities and litter decomposition in vineyard streams. Science of the Total Environment 533: 40–48.CrossRefPubMedGoogle Scholar
  25. Ferreira, V., V. Gulis & M. A. S. Graça, 2006. Whole-stream nitrate addition affects litter decomposition and associated fungi but not invertebrates. Oecologia 149: 718–729.CrossRefPubMedGoogle Scholar
  26. Ferreira, V., B. Castagneyrol, J. Koricheva, V. Gulis, E. Chauvet & M. A. S. Graça, 2015. A meta-analysis of the effects of nutrient enrichment on litter decomposition in streams. Biological Reviews 90: 669–688.CrossRefGoogle Scholar
  27. Flores, L., Z. Banjac, M. Farré, A. Larrañaga, E. Mas-Martí, I. Muñoz, D. Barceló & A. Elosegi, 2014. Effects of a fungicide (imazalil) and an insecticide (diazinon) on stream fungi and invertebrates associated with litter breakdown. Science of the Total Environment 476–477: 532–541.CrossRefPubMedGoogle Scholar
  28. Gessner, M. O., 2005. Ergosterol as a measure of fungal biomass. In Graça, M. A. S., F. Bärlocher & M. O. Gessner (eds), Methods to Study Litter Decomposition. Springer, Dordrecht: 189–195.CrossRefGoogle Scholar
  29. Gessner, M. O. & E. Chauvet, 1993. Ergosterol-to-biomass conversion factors for aquatic hyphomycetes. Applied and Environmental Microbiology 59: 502–507.PubMedPubMedCentralGoogle Scholar
  30. Gessner, M. O. & E. Chauvet, 2002. A case for using litter breakdown to assess functional stream integrity. Ecological Applications 12: 498–510.CrossRefGoogle Scholar
  31. Gessner, M. O., F. Bärlocher & E. Chauvet, 2003. Qualitative and quantitative analysis of aquatic hyphomycetes in streams. In Tsui, C. K. M. & K. D. Hyde (eds), Freshwater Mycology. Fungal Diversity Press, Hong Kong: 127–157.Google Scholar
  32. Gonçalves, A. L., E. Chauvet, F. Bärlocher, M. A. S. Graça & C. Canhoto, 2014. Top-down and bottom-up control of litter decomposers in streams. Freshwater Biology 59: 2172–2182.CrossRefGoogle Scholar
  33. Gulis, V., L. Marvanová & E. Descals, 2005. An illustrated key to the common temperate species of aquatic hyphomycetes. In Graça, M. A. S., F. Bärlocher & M. O. Gessner (eds), Methods to Study Litter Decomposition. Kluwer Academic, Dordrecht: 153–167.CrossRefGoogle Scholar
  34. Hagen, E. M., J. R. Webster & E. F. Benfield, 2006. Are leaf breakdown rates a useful measure of stream integrity along an agricultural landuse gradient? Journal of the North American Benthological Society 25: 330–343.CrossRefGoogle Scholar
  35. Hladyz, S., S. D. Tiegs, M. O. Gessner, P. S. Giller, G. Rîşnoveanu, E. Preda, M. Nistorescu, M. Schindler & G. Woodward, 2010. Leaf-litter breakdown in pasture and deciduous woodland streams: a comparison among three European regions. Freshwater Biology 55: 1916–1929.CrossRefGoogle Scholar
  36. Kominoski, J. S., L. B. Marczak & J. S. Richardson, 2011. Riparian forest composition affects stream litter decomposition despite similar microbial and invertebrate communities. Ecology 92: 151–159.CrossRefPubMedGoogle Scholar
  37. Kreutzweiser, D. P., D. G. Thompson & T. A. Scarr, 2009. Imidacloprid in leaves from systemically treated trees may inhibit litter breakdown by non-target invertebrates. Ecotoxicology and Environmental Safety 72: 1053–1057.CrossRefPubMedGoogle Scholar
  38. Lecerf, A. & E. Chauvet, 2008. Diversity and functions of leaf-decaying fungi in human-altered streams. Freshwater Biology 53: 1658–1672.CrossRefGoogle Scholar
  39. Lecerf, A., M. Dobson, C. K. Dang & E. Chauvet, 2005. Riparian plant species loss alters trophic dynamics in detritus-based stream ecosystems. Oecologia 146: 432–442.CrossRefPubMedGoogle Scholar
  40. Lecerf, A., P. Usseglio-Polatera, J.-Y. Charcosset, D. Lambrigot, B. Bracht & E. Chauvet, 2006. Assessment of functional integrity of eutrophic streams using litter breakdown and benthic macroinvertebrates. Archiv für Hydrobiologie 165: 105–126.CrossRefGoogle Scholar
  41. Liess, M. & P. C. Von der Ohe, 2005. Analyzing effects of pesticides on invertebrate communities in streams. Environmental Toxicology and Chemistry 24: 954–965.CrossRefPubMedGoogle Scholar
  42. Liess, M., R. B. Schäfer & C. A. Schriever, 2008. The footprint of pesticide stress in communities-species traits reveal community effects of toxicants. Science of the Total Environment 406: 484–490.CrossRefPubMedGoogle Scholar
  43. Maltby, L., T. C. M. Brock & P. J. Van Den Brink, 2009. Fungicide risk assessment for aquatic ecosystems: importance of interspecific variation, toxic mode of action, and exposure regime. Environmental Science and Technology 43: 7556–7563.CrossRefPubMedGoogle Scholar
  44. Morin, S., S. Pesce, A. Tlili, M. Coste & B. Montuelle, 2010. Recovery potential of periphytic communities in a river impacted by a vineyard watershed. Ecological Indicators 10: 419–426.CrossRefGoogle Scholar
  45. Palmer, M. A. & C. M. Febria, 2012. The heartbeat of ecosystems. Science 336: 1393–1394.CrossRefPubMedGoogle Scholar
  46. Pascoal, C., F. Cássio & P. Gomes, 2001. Leaf breakdown rates: a measure of water quality? International Review of Hydrobiology 86: 407–416.CrossRefGoogle Scholar
  47. Pestana, J. L. T., A. C. Alexander, J. M. Culp, D. J. Baird, A. J. Cessna & A. M. V. M. Soares, 2009. Structural and functional responses of benthic invertebrates to imidacloprid in outdoor stream mesocosms. Environmental Pollution 157: 2328–2334.CrossRefPubMedGoogle Scholar
  48. Peters, K., M. Bundschuh & R. B. Schäfer, 2013. Review on the effects of toxicants on freshwater ecosystem functions. Environmental Pollution 180: 324–329.CrossRefPubMedGoogle Scholar
  49. Piscart, C., S. Navel, C. Maazouzi, B. Montuelle, J. Cornut, F. Mermillod-Blondin, M. Creuze des Chatelliers, L. Simon & P. Marmonier, 2011. Leaf litter recycling in benthic and hyporheic layers in agricultural streams with different types of land use. Science of the Total Environment 409: 4373–4380.CrossRefPubMedGoogle Scholar
  50. Rasmussen, J. J., P. Wiberg-Larsen, A. Baattrup-Pedersen, R. J. Monberg & B. Kronvang, 2012a. Impacts of pesticides and natural stressors on leaf litter decomposition in agricultural streams. Science of the Total Environment 416: 148–155.CrossRefPubMedGoogle Scholar
  51. Rasmussen, J. J., P. Wiberg-Larsen, A. Baattrup-Pedersen, N. Friberg & B. Kronvang, 2012b. Stream habitat structure influences macroinvertebrate response to pesticides. Environmental Pollution 164: 142–149.CrossRefPubMedGoogle Scholar
  52. Rasmussen, J. J., R. J. Monberg, A. Baattrup-Pedersen, N. Cedergreen, P. Wiberg-Larsen, B. Strobel & B. Kronvang, 2012c. Effects of a triazole fungicide and a pyrethroid insecticide on the decomposition of leaves in the presence or absence of macroinvertebrate shredders. Aquatic Toxicology 118–119: 54–61.CrossRefPubMedGoogle Scholar
  53. Reyjol, Y., C. Argillier, W. Bonne, A. Borja, A. D. Buijse, A. C. Cardoso, M. Daufresne, M. Kernan, M. T. Ferreira, S. Poikane, N. Prat, A.-L. Solheim, S. Stroffek, P. Usseglio-Polatera, B. Villeneuve & W. van de Bund, 2014. Assessing the ecological status in the context of the European Water Framework Directive: where do we go now? Science of the Total Environment 497–498: 332–344.CrossRefPubMedGoogle Scholar
  54. Roussel, H., E. Chauvet & J.-M. Bonzom, 2008. Alteration of leaf decomposition in copper-contaminated freshwater mesocosms. Environmental Toxicology and Chemistry 27: 637–644.CrossRefPubMedGoogle Scholar
  55. Schäfer, R. B., T. Caquet, K. Siimes, R. Mueller, L. Lagadic & M. Liess, 2007. Effects of pesticides on community structure and ecosystem functions in agricultural streams of three biogeographical regions in Europe. Science of the Total Environment 382: 272–285.CrossRefPubMedGoogle Scholar
  56. Schäfer, R. B., M. Bundschuh, D. A. Rouch, E. Szöcs, P. C. Von der Ohe, V. Pettigrove, R. Schulz, D. Nugegoda & B. J. Kefford, 2012a. Effects of pesticide toxicity, salinity and other environmental variables on selected ecosystem functions in streams and the relevance for ecosystem services. Science of the Total Environment 415: 69–78.CrossRefPubMedGoogle Scholar
  57. Schäfer, R. B., P. C. Von der Ohe, J. Rasmussen, B. J. Kefford, M. A. Beketov, R. Schulz & M. Liess, 2012b. Thresholds for the effects of pesticides on invertebrate communities and leaf breakdown in stream ecosystems. Environmental Science and Technology 46: 5134–5142.CrossRefPubMedGoogle Scholar
  58. Schwarzenbach, R. P., B. I. Escher, K. Fenner, T. B. Hofstetter, C. A. Johnson, U. von Gunten & B. Wehrli, 2006. The challenge of micropollutants in aquatic systems. Science 313: 1072–1077.CrossRefPubMedGoogle Scholar
  59. Suberkropp, K. & J. B. Wallace, 1992. Aquatic hyphomycetes in insecticide-treated and untreated streams. Journal of the North American Benthological Society 11: 165–171.CrossRefGoogle Scholar
  60. Tachet, H., P. Richoux, M. Bournaud & P. Usseglio-Polatera, 2010. Invertébrés d’eau douce: systématique, biologie, écologie. CNRS Editions, Paris. 600 pp.Google Scholar
  61. Thompson, M. S. A., C. Bankier, T. Bell, A. J. Dumbrell, C. Gray, M. E. Ledger, K. Lehmann, B. A. McKew, C. D. Sayer, F. Shelley, M. Trimmer, S. L. Warren & G. Woodward, 2015. Gene-to-ecosystem impacts of a catastrophic pesticide spill: testing a multilevel bioassessment approach in a river ecosystem. Freshwater Biology. doi: 10.1111/fwb.12676.Google Scholar
  62. Tsui, C. K. M., K. D. Hyde & I. J. Hodgkiss, 2001. Effects of glyphosate on lignicolous freshwater fungi of Hong Kong. Sydowia 200: 167–174.Google Scholar
  63. University of Hertfordshire, 2013. The Pesticide Properties Database (PPDB). Agriculture and Environment Research Unit (AERU), University of Hertfordshire: 2006–2013.Google Scholar
  64. Von der Ohe, P. C. & W. Goedkoop, 2013. Distinguishing the effects of habitat degradation and pesticide stress on benthic invertebrates using stressor-specific metrics. Science of the Total Environment 444: 480–490.CrossRefPubMedGoogle Scholar
  65. Von der Ohe, P. C., E. De Deckere, A. Prüss, I. Muñoz, G. Wolfram, M. Villagrasa, A. Ginebreda, M. Hein & W. Brack, 2009. Toward an integrated assessment of the ecological and chemical status of European river basins. Integrated Environmental Assessment and Management 5: 50–61.CrossRefPubMedGoogle Scholar
  66. Wasson, J.-G., A. Chandesris, H. Pella & L. Blanc, 2002. Les hydro-écorégions de France métropolitaine approche régionale de la typologie des eaux courantes et éléments pour la définition des peuplements de référence d’invertébrés. Cemagref report, 190 pp.Google Scholar
  67. Webster, J. R. & E. F. Benfield, 1986. Vascular plant breakdown in fresh-water ecosystems. Annual Review of Ecology and Systematics 17: 567–594.CrossRefGoogle Scholar
  68. Wieder, R. K. & G. E. Lang, 1982. A critique of the analytical methods used in examining decomposition data obtained from litter bags. Ecology 63: 1636–1642.CrossRefGoogle Scholar
  69. Woodward, G., M. O. Gessner, P. S. Giller, V. Gulis, S. Hladyz, A. Lecerf, B. Malmqvist, B. G. McKie, S. D. Tiegs, H. Cariss, M. Dobson, A. Elosegi, V. Ferreira, M. A. S. Graça, T. Fleituch, J. O. Lacoursière, M. Nistorescu, J. Pozo, G. Risnoveanu, M. Schindler, A. Vadineanu, L. B.-M. Vought & E. Chauvet, 2012. Continental-scale effects of nutrient pollution on stream ecosystem functioning. Science 336: 1438–1440.CrossRefPubMedGoogle Scholar
  70. Zubrod, J. P., D. Englert, A. Feckler, N. Koksharova, M. Konschak, R. Bundschuh, N. Schnetzer, K. Englert, R. Schulz & M. Bundschuh, 2015. Does the current fungicide risk assessment provide sufficient protection for key drivers in aquatic ecosystem functioning? Environmental Science and Technology 49: 1173–1181.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.EcoLabUniversité de Toulouse, CNRS, INPT, UPSToulouseFrance
  2. 2.ASCONIT ConsultantsRamonville Saint-AgneFrance

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