Environmental Science and Pollution Research

, Volume 25, Issue 12, pp 11281–11294 | Cite as

Metal release from contaminated leaf litter and leachate toxicity for the freshwater crustacean Gammarus fossarum

  • Florence Maunoury-Danger
  • Vincent Felten
  • Clément Bojic
  • Fabrice Fraysse
  • Mar Cosin Ponce
  • Odile Dedourge-Geffard
  • Alain Geffard
  • François Guérold
  • Michael DangerEmail author
Aquatic organisms and biological responses to assess water contamination and ecotoxicity


Industrialization has left large surfaces of contaminated soils, which may act as a source of pollution for contiguous ecosystems, either terrestrial or aquatic. When polluted sites are recolonized by plants, dispersion of leaf litter might represent a non-negligible source of contaminants, especially metals. To evaluate the risks associated to contaminated leaf litter dispersion in aquatic ecosystems, we first measured the dynamics of metal loss from leaf litter during a 48-h experimental leaching. We used aspen (Populus tremula L.), a common tree species on these polluted sites, and collected leaf litter on three polluted sites (settling pond of a former steel mill) and three control sites situated in the same geographic area. Then, toxicity tests were carried out on individuals of a key detritivore species widely used in ecotoxicology tests, Gammarus fossarum (Crustacea, Amphipoda), with uncontaminated and contaminated leaf litter leachates, using a battery of biomarkers selected for their sensitivity to metallic stress. Leaf litters collected on polluted sites exhibited not only significantly higher cadmium and zinc concentrations but also lower lignin contents. All leaf litters released high amounts of chemical elements during the leaching process, especially potassium and magnesium, and, in a lesser extent, phosphorus, calcium, and trace metals (copper, cadmium, and zinc but not lead). Toxicity tests revealed that the most important toxic effects measured on G. fossarum were due to leaf litter leachates by themselves, whatever the origin of litter (from polluted or control sites), confirming the toxicity of such substances, probably due to their high content in phenolic compounds. Small additional toxic effects of leachates from contaminated leaf litters were only evidenced on gammarid lipid peroxidation, indicating that contaminated leaf litter leachates might be slightly more toxic than uncontaminated ones, but in a very reduced manner. Further studies will be required to verify if these patterns are generalizable to other species and to investigate the effects of contaminated leaf litter ingestion by consumers on aquatic food webs. Nevertheless, our results do not permit to exclude potential chronic effects of an exposure to contaminated leaf litter leachates in aquatic ecosystems.


Contaminated brownfield Metals Leaf litter leaching Toxicity test Aquatic ecosystems 



This study was supported by the TransMet EC2CO program to F. Fraysse, by the « Agence De l’Environnement et de la Maitrise de l’Energie » (ADEME—grant number 1172C0040), and the « Observatoire Terre Environnement Lorrain » (OteLo—grant number L01648/PROJET). We also thank C. Fouque for technical help for preliminary tests and two anonymous reviewers for their helpful suggestions.


  1. Arab K, Steghens JP (2004) Plasma lipid hydroperoxides measurement by an automated xylenol orange method. Anal Biochem 325:158–163CrossRefGoogle Scholar
  2. Arce Funck J (2014) Modulation d’un stress chimique par la contrainte alimentaire: approche intégrée de l’individu au fonctionnement de l’écosystème. University of Lorraine, France 271pp Google Scholar
  3. Arce Funck J, Danger M, Gismondi E, Cossu-Leguille C, Guérold F, Felten V (2013) Behavioural and physiological responses of Gammarus fossarum (Crustacea Amphipoda) exposed to silver. Aquat Toxicol 142:73–84CrossRefGoogle Scholar
  4. Arce Funck J, Crenier C, Danger M, Cossu-Leguille C, Guérold F, Felten V (2016) Stoichiometric constraints modulate impacts of silver contamination on stream detritivores: an experimental test with Gammarus fossarum. Freshw Biol 61(12):2075–2089CrossRefGoogle Scholar
  5. Bährs H, Putschew A, Steinberg CEW (2012) Toxicity of hydroquinone to different freshwater phototrophs is influenced by time of exposure and pH. Environ Sci Pollut Res 20:146–154CrossRefGoogle Scholar
  6. Bärlocher F (2005) Leaching. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study leaf litter decomposition, pp33–36.Google Scholar
  7. Bernfeld P (1955) Amylases, a and b. In: KN CSP (ed) Methods in Enzymology. Academic Press, New York, pp 149–158Google Scholar
  8. Berti WR, Cunningham SD (2000) Phytostabilization of metals. In: Raskin I, Ensley BD (eds) Phytoremediation of Toxic Metals: Using Plants to Clean up the Environment. Wiley, New York, pp 71–88Google Scholar
  9. Besser JM, Rabeni CF (1987) Bioavailability and toxicity of metals leached from lead-mine tailings to aquatic invertebrates. Environ Toxicol Chem 6:879–890CrossRefGoogle Scholar
  10. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  11. Bray JR, Gorham E (1964) Litter production in forests of the world. Adv Ecol Res 2:101–157CrossRefGoogle Scholar
  12. Calabrese EJ, Baldwin LA (1998) Hormesis as a biological hypothesis. Environ Health Perspect 106:357CrossRefGoogle Scholar
  13. Cameron GN, LaPoint TW (1978) Effects of tannins on the decomposition of Chinese tallow leaves by terrestrial and aquatic invertebrates. Oecologia 32:349–366CrossRefGoogle Scholar
  14. Canhoto C, Laranjeira C (2007) Leachates of Eucalyptus globulus in intermittent streams affect water parameters and invertebrates. Int Rev Hydrobiol 92(2):173–182CrossRefGoogle Scholar
  15. Canhoto C, Calapez R, Gonçalves AL, Moreira-Santos M (2013) Effects of Eucalyptus leachates and oxygen on leaf-litter processing by fungi and stream invertebrates. Freshwater Science 32:411–424CrossRefGoogle Scholar
  16. Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899CrossRefGoogle Scholar
  17. da Silva ST, Christofoletti CA, Bozzatto V, Fontanetti CS (2014) The use of diplopods in soil ecotoxicology—a review. Ecotoxicol Environ Saf 103:68–73CrossRefGoogle Scholar
  18. Dedourge-Geffard O, Palais F, Biagianti-Risbourg S, Geffard O, Geffard A (2009) Effects of metals on feeding rate and digestive enzymes in Gammarus fossarum: an in situ experiment. Chemosphere 77(11):1569–1576CrossRefGoogle Scholar
  19. Dudka S, Ponce-Hernandez R, Tate G, Hutchinson TC (1996) Forms of Cu, Ni and Zn in soils of Sudbury, Ontario and the metal concentrations in plants. Water Air Soil Pollut 90:531–542CrossRefGoogle Scholar
  20. Felten V, Charmentier G, Mons R, Geffard A, Rousselle P, Coquery M, Garric J, Geffard O (2008) Physiological and behavioural responses of Gammarus pulex (Crustacea: Amphipoda) exposed to cadmium. Aquat Toxicol 86(3):413–425CrossRefGoogle Scholar
  21. Fisher SG, Likens GE (1973) Energy flow in bear brook, New Hampshire: an integrative approach to stream ecosystem metabolism. Ecological Monographs 43:421–43e9CrossRefGoogle Scholar
  22. Fraysse F, Pokrovsky OS, Meunier JD (2010) Experimental study of terrestrial plant litter interaction with aqueous solutions. Geochimica Cosmochimica Acta 74:70–84CrossRefGoogle Scholar
  23. Gallagher FJ, Pechmann I, Bogden JD, Grabosky J, Weis P (2008) Soil metal concentrations and vegetative assemblage structure in an urban brownfield. Environ Pollut 153:351–361CrossRefGoogle Scholar
  24. Gama M, Guilhermino L, Canhoto C (2014) Comparison of three shredders response to acute stress induced by eucalyptus leaf leachates and copper: single and combined exposure at two distinct temperatures. Ann Limnol Int J Limnol 50:97–107CrossRefGoogle Scholar
  25. Garaud M, Auffan M, Devin S, Felten V, Pagnout C, Pain-Devin S, Proux O, Rodius F, Sohm B, Giambérini L (2015) Fate and integrated assessment of ceria nanoparticle impacts on the freshwater bivalve Dreissena polymorpha: a mesocosm approach. Nanotoxicology 10:935–944CrossRefGoogle Scholar
  26. Geffard O, Xuereb B, Chaumot A, Geffard A, Biagianti S, Noel C, Abbaci K, Garric J, Charmentier G, Charmantier-Daures M (2010) Ovarian cycle and embryonic development in Gammarus fossarum: application for reproductive toxicity assessment. Environ Toxicol Chem 29(10):2249–2259CrossRefGoogle Scholar
  27. Gessner MO, Chauvet E, Dobson M (1999) A perspective on leaf litter breakdown in streams. Oikos 85:377–384CrossRefGoogle Scholar
  28. Herms DA, Mattson WJ (1992) The dilemma of plants—to grow or defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  29. Hervant F, Mathieu J, Barré H, Simon K, Pinon C (1997) Comparative study on the behavioural, ventilatory and respiratory responses of hypogean and epigean crustacean to long-term starvation and subsequent feeding. Comp Biochem Physiol 118A:1277–1283CrossRefGoogle Scholar
  30. Huot H, Simonnot MO, Marion P, Yvon J, De Donato P, Morel JL (2013) Characteristicsc and potential pedogenetic processes of a Technosol developing on iron industry deposits. J Soils Sediments 13:555–568CrossRefGoogle Scholar
  31. Huot H, Simonnot MO, Watteau F, Marion P, Yvon J, De Donato P, Morel JL (2014) Early transformation and transfer processes in a Technosol developing on iron industry deposits. Eur J Soil Sci 65(4):470–484CrossRefGoogle Scholar
  32. Issartel J, Hervant F, Voituron Y, Renault D, Vernon P (2005) Behavioural, ventilatory and respiratory responses of epigean and hypogean crustaceans to different temperatures. Comp Biochem Physiol 141A:1–7CrossRefGoogle Scholar
  33. Kieffer P, Dommes J, Hoffmann L, Hausman JF, Renaut J (2008) Quantitative changes in protein expression of cadmium-exposed poplar plants. Proteomics 8:2514–2530CrossRefGoogle Scholar
  34. Krpata D, Peintner U, Langer I, Fitz WJ, Schweiger P (2008) Ectomycorrhizal communities associated with Populus tremula growing on a heavy metal contaminated site. Mycol Res 112(9):1069–1079CrossRefGoogle Scholar
  35. Kumar PBAN, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1232–1238CrossRefGoogle Scholar
  36. Kunz PY, Kienle C, Gerhardt A (2010) Gammarus spp. in aquatic ecotoxicology and water quality assessment: toward integrated multilevel tests. Rev Environ Contam Toxicol 205:1–76Google Scholar
  37. Laureysens I, Bogaert J, Blust R, Ceulemans R (2004) Biomass production of 17 poplar clones in a short-rotation coppice culture on a waste disposal site and its relation to soil characteristics. For Ecol Manag 187:295–309CrossRefGoogle Scholar
  38. Leroux SJ, Loreau M (2008) Subsidy hypothesis and strength of trophic cascades across ecosystems. Ecol Lett 11:1147–1156CrossRefGoogle Scholar
  39. Linacre NA, Whiting SN, Angle JS (2005) The impact of uncertainty on phytoremediation project costs. Int J Phytoremediation 7:259–269CrossRefGoogle Scholar
  40. Lucisine P, Lecerf A, Danger M, Felten V, Aran D, Auclerc A, Gross EM, Huot H, Morel JL, Muller S, Nahmani J, Maunoury-Danger F (2015) Litter chemistry prevails over litter consumers in mediating effects of past steel industry activities on leaf litter decomposition. Sci Total Environ 537:213–224CrossRefGoogle Scholar
  41. Markiewicz-Patkowska J, Hursthouse A, Przybyla-Kij H (2005) The interaction of heavy metals with urban soils: sorption behavior of Cd, Cu, Cr, Pb and Zn with a typical mixed brownfield deposit. Environ Int 31:513–521CrossRefGoogle Scholar
  42. Mehennaoui K, Georgantzopoulou A, Felten V, Andreï J, Garaud M, Cambier S, Serchi T, Pain-Devin S, Guérold F, Audinot J-N, Giambérini L, Gutleb AC (2016) Gammarus fossarum (Crustacea, Amphipoda) as a model organism to study the effects of silver nanoparticles. Sci Total Environ 566:1649–1659CrossRefGoogle Scholar
  43. Miller JK, Brzezinska-Lebodzinska E, Madsen FC (1993) Oxidative stress, antioxidants, and animal function. J Dairy Sci 76:2812–2823CrossRefGoogle Scholar
  44. Palais F, Jubeaux G, Dedourge-Geffard O, Giambérini L, Biagianti-Risbourg S et al (2010) Amylolytic and cellulolytic activities in the cristalline style and the digestive diverticulae of the freshwater bivalve Dreissena polymorpha (Pallas,1771). Molluscan Res 30:29–36Google Scholar
  45. Parsons WFJ, Taylor BR, Parkinson D (1990) Decomposition of aspen (Populus tremuloides) leaf litter modified by leaching. Can J For Res 20:943–951CrossRefGoogle Scholar
  46. Perronnet K, Schwartz C, Gérard E, Morel JL (2000) Availability of cadmium and zinc accumulated in the leaves of Thlaspi caerulescens incorporated into soil. Plant Soil 227:257–263CrossRefGoogle Scholar
  47. Petersen RC, Cummins KW (1974) Leaf processing in a woodland stream. Freshw Biol 4:343–368CrossRefGoogle Scholar
  48. Pulford ID, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees—a review. Environ Int 29(4):529–540CrossRefGoogle Scholar
  49. Qian Y, Gallagher FJ, Feng H, Wu M (2012) A geochemical study of toxic metal translocation in an urban brownfield wetland. Environ Pollut 166:23–30CrossRefGoogle Scholar
  50. Rey D, David JP, Martins D, Pautou MP, Long A, Marigo G, Meyran JC (2000) Role of vegetable tannins in habitat selection among mosquito communities from the Alpine hydrosystems. C R Acad Sci III 323:391–398CrossRefGoogle Scholar
  51. Rosas C, Sanchez A, Escohar E, Soto L, Bolongaro-Crevenna A (1992) Daily variations of oxygen consumption and glucose hemolymph level related to morphophysiological and ecological adaptations of crustacea. Comp Biochem Physiol 101A:323–328CrossRefGoogle Scholar
  52. Roy S, Labelle S, Mehta P, Mihoc A, Fortin N, Masson C, Leblanc R, Guy Chateauneuf G, Sura C, Gallipeau C, Olsen C, Delisle S, Labrecque M, Greer CW (2005) Phytoremediation of heavy metal and PAH-contaminated brownfield sites. Plant Soil 272:277–290CrossRefGoogle Scholar
  53. Schofield JA, Hagerman AE, Harold A (1998) Loss of tannins and other phenolics from willow leaf litter. J Chem Ecol 24:1409–1421CrossRefGoogle Scholar
  54. Schwartz C, Florentin L, Charpentier D, Muzika S, Morel JL (2001) Le pédologue en milieux industriels et urbains. I Sols d’une friche industrielle Etude et Gestion des Sols 8:135–148Google Scholar
  55. Sroda S, Cossu-Leguille C (2011) Effects of sublethal copper exposure on two gammarid species: which is the best competitor? Ecotoxicology 20:264–273CrossRefGoogle Scholar
  56. Suberkropp K, Godshalk GL, Klug MJ (1976) Changes in the chemical composition of leaves during processing in a woodland stream. Ecology 57:720–727CrossRefGoogle Scholar
  57. Taylor BR, Bärlocher F (1996) Variable effects of air-drying on leaching losses from tree leaf litter. Hydrobiologia 325(3):173–182CrossRefGoogle Scholar
  58. Taylor BR, Carmichael NB (2003) Toxicity and chemistry of aspen wood leachate to aquatic life: field study. Environ Toxicol Chem 22:2048–2056CrossRefGoogle Scholar
  59. Tessier A, Turner DR (eds) (1995) Metal speciation and bioavailability in aquatic systems. Wiley, ChichesterGoogle Scholar
  60. Thornton G, Franz M, Edwards D, Pahlen G, Nathanail P (2007) The challenge of sustainability: incentives for brownfield regeneration in Europe. Environ Sci Policy 10:116–134CrossRefGoogle Scholar
  61. Tremolieres M (1988) Deoxygenating effect and toxicity of ground-up dried coniferous needles and deciduous leaves of Canadian trees in water: a preliminary study in comparison with litter of European trees. Water Res 22:21–28CrossRefGoogle Scholar
  62. Tsuda K, Takamura N, Matsuyama M, Fujii Y (2005) Assessment method for leaf litters allelopathic effect on cyanobacteria. J Aquat Plant Manag 43:43–46Google Scholar
  63. Unterbrunner R, Puschenreiter M, Sommer P, Wieshammer G, Tlustos P, Zupan M, Wenzel WW (2006) Heavy metal accumulation in trees growing on contaminated sites in Central Europe. Environ Pollut 148:107–114CrossRefGoogle Scholar
  64. van Nevel L, Mertens J, Oorts K, Verheyen K (2007) Phytoextraction of metals from soils: how far from practice? Environ Pollut 150(1):34–40CrossRefGoogle Scholar
  65. van Nevel L, Mertens J, Demey A, De Schrijver A, De Neve S, Tack FM, Verheyen K (2014) Metal and nutrient dynamics in decomposing tree litter on ametal contaminated site. Environ Pollut 189:54–62CrossRefGoogle Scholar
  66. Vangronsveld J, van Assche F, Clijsters H (1995) Reclamation of a bare industrial area contaminated by non-ferrous metals: in situ metal immobilization and revegetation. Environ Pollut 87:51–59CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Florence Maunoury-Danger
    • 1
    • 2
  • Vincent Felten
    • 1
    • 2
  • Clément Bojic
    • 1
  • Fabrice Fraysse
    • 1
    • 2
  • Mar Cosin Ponce
    • 3
  • Odile Dedourge-Geffard
    • 3
  • Alain Geffard
    • 3
  • François Guérold
    • 1
    • 2
  • Michael Danger
    • 1
    • 2
    • 4
    Email author
  1. 1.UMR 7360, Laboratoire Interdisciplinaire des Environnements Continentaux (LIEC)Université de LorraineMetzFrance
  2. 2.CNRS, UMR 7360, LIEC, UMR 7360MetzFrance
  3. 3.UMR-I 02 Stress Environnementaux et BIOsurveillance des milieux aquatiques (SEBIO), INERIS-URCA-ULHUniversité de Reims Champagne-ArdenneMetzFrance
  4. 4.LTER-“Zone Atelier Moselle”, LIEC, UMR7360MetzFrance

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