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Effects of the herbicide Roundup® on the metabolic activity of Gammarus fossarum Koch, 1836 (Crustacea; Amphipoda)

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Abstract

Pesticides can easily reach surface waters via runoff and their potential to have detrimental impacts on freshwater organisms is high. Not much is known about how macroinvertebrates react to glyphosate contamination. In this study we investigated lethal and sublethal effects of the exposure of Gammarus fossarum to Roundup®, a glyphosate-based herbicide. The LC10 and LC50 values after 96 h were determined to be 0.65 ml/L Roundup® (230 mg/L glyphosate) and 0.96 ml/L Roundup® (340 mg/L glyphosate), respectively. As a sublethal measure of toxicity we conducted eight experiments with the feeding activity and the respiratory electron transport system (ETS) activity as endpoints. All experiments lasted seven days. Although the LC10 concentration of Roundup® was used for the feeding activity tests, 49% of the gammarids died before the end of the experiments, which is inconsistent with the calculated LC10-values. The feeding activity was significantly higher in Roundup®-enriched water (mean = 0.18 mg/mg x d) in comparison to pure spring water (mean = 0.079 mg/mg x d). No significant difference was observed between the ETS activity, which was determined after 24, 48 or 96 h after the start of the experiment, of the gammarids in Roundup® solution and in the control. The LC-values determined here are rather high, and exceed background glyphosate concentrations in most anthropogenically influenced surface waters. The increased feeding activity when exposed to Roundup® in combination with an unchanged ETS activity suggests effects on the metabolic efficiency of G. fossarum. We argue that Roundup® enhances the anabolic activity (feeding activity) in order to maintain the catabolic activity (ETS activity).

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References

  • Alonso A, De Lange HJ, Peeters ETHM (2010) Contrasting sensitivities to toxicants of the freshwater amphipods Gammarus pulex and G. fossarum. Ecotoxicol 19:133–140

    Article  CAS  Google Scholar 

  • Altermatt F, Alther R, Fišer C, Jokela J, Konec M, Küry D, Mächler E, Stucki P, Westram AM (2014) Diversity and distribution of freshwater amphipod species in Switzerland (Crustacea: Amphipoda). PLoS One 9:e110328

    Article  Google Scholar 

  • Aparicio VC, De Gerónimo E, Marino D, Primost J, Carriquiriborde P, Costa JL (2013) Environmental fate of glyphosate and aminomethylphosphonic acid in surface waters and soil of agricultural basins. Chemosphere 93:1866–1873. https://doi.org/10.1016/j.chemosphere.2013.06.041

    Article  CAS  Google Scholar 

  • Baylis AD (2000) Why glyphosate is a global herbicide: strengths, weaknesses and prospects. Pest Manag Sci 56:299–308

    Article  CAS  Google Scholar 

  • Baudrot V, Charles S, Delignette-Muller ML, Duchemin W, Kon-Kam-King G, Lopes C, Ruiz P, Veber P (2018) Morse: modelling tools for reproduction and survival data in ecotoxicology. R package version 3.1.1, University of Lyon

  • Becker J, Ortmann C, Wetzel MA, Koop JHE (2016) Metabolic activity and behavior of the invasive amphipod Dikerogammarus villosus and two common central European gammarid species (Gammarus fossarum, Gammarus roeselii): low metabolic rates may favor the invader. Comp Biochem Phys A 191:119–126. https://doi.org/10.1016/j.cbpa.2015.10.015

    Article  CAS  Google Scholar 

  • Beggel S, Brandner J, Cerwenka AF, Geist J (2016) Synergistic impacts by an invasive amphipod and an invasive fish explain native gammarid extinction. BMC Ecol 16:32. https://doi.org/10.1186/s12898-016-0088-6

    Article  CAS  Google Scholar 

  • Benbrook CM (2016) Trends in glyphosate herbicide use in the United States and globally. Env Sci Eur 28(3). https://doi.org/10.1186/s12302-016-0070-0

  • Besse J-P, Coquery M, Lopes C, Chaumot A, Budzinski H, Labadie P, Geffard O (2013) Caged Gammarus fossarum (Crustacea) as a robust tool for the characterization of bioavailable contamination levels in continental waters: towards the determination of threshold values. Water Res 47:650–660. https://doi.org/10.1016/j.watres.2012.10.024

    Article  CAS  Google Scholar 

  • Bloor MC (2010) Animal standardisation for mixed species ecotoxicological studies: establishing a laboratory breeding programme for Gammarus pulex and Asellus aquaticus. Zool Baetica 21:179–190

    Google Scholar 

  • Bloor MC, Banks CJ (2006) An evaluation of mixed species in situ and ex situ feeding assays: the altered response of Asellus aquaticus and Gammarus pulex. Environ Int 32:22–27

    Article  CAS  Google Scholar 

  • Bonansea RI, Filippi I, Wunderlin DA, Marino DJG, Amé MV (2018) The fate of glyphosate and AMPA in a freshwater endorheic basin: an ecotoxicological risk assessment. Toxics 6:3. https://doi.org/10.3390/toxics6010003

    Article  Google Scholar 

  • Brausch JM, Smith PN (2007) Toxicity of three polyethoxylated tallowamine surfactant formulations to laboratory and field collected fairy shrimp, Thamnocephalus platyurus. Arch Environ Contam Toxicol 52:217–221. https://doi.org/10.1007/s00244-006-0151-y

    Article  CAS  Google Scholar 

  • Bundschuh M, Mckie BG (2016) An ecological and ecotoxicological perspective on fine particulate organic matter in streams. Freshw Biol 61:2063–2074. https://doi.org/10.1111/fwb.12608

    Article  CAS  Google Scholar 

  • Bundschuh M, Hahn T, Gessner MO, Schulz R (2017) Antibiotic mixture effects on growth of the leaf-shredding stream detritivore Gammarus fossarum. Ecotoxicology 26:547–554. https://doi.org/10.1007/s10646-017-1787-2

    Article  CAS  Google Scholar 

  • Carlisle SM, Trevors JT (1988) Glyphosate in the environment. Water, Air, Soil Pollut 39:409–420

    CAS  Google Scholar 

  • Chen W, Bierbach D, Plath M, Streit B, Klaus S (2012) Distribution of amphipod communities in the middle to upper rhine and five of its tributaries. Bioinvasions Rec 1:263–271. https://doi.org/10.3391/bir.2012.1.4.04

    Article  Google Scholar 

  • Cohen J (1988) Statistical power analysis for the behavioral sciences. Hoboken: Taylor and Francis, New York, USA

    Google Scholar 

  • Coulaud R, Geffard O, Xuereb B, Lacaze E, Quéau H, Garric J, Charles S, Chaumot A (2011) In situ feeding assay with Gammarus fosssarum (Crustacea): modelling the influence of confounding factors to improve water quality biomonitoring. Water Res 45:6417–6429

    Article  CAS  Google Scholar 

  • Coupe RH, Kalkhoff SJ, Capel PD, Gregoire C (2012) Fate and transport of glyphosate and aminomethylphosphonic acid in surface waters of agricultural basins. Pest Manag Sci 68:16–30

    Article  CAS  Google Scholar 

  • Cuhra M, Traavik T, Bøhn T (2013) Clone- and age-dependent toxicity of a glyphosate commercial formulation and its active ingredient in Daphnia magna. Ecotoxicology 22:251–262. https://doi.org/10.1007/s10646-012-1021-1

    Article  CAS  Google Scholar 

  • Daouk S, Copin P-J, Rossi L, Chèvre N, Pfeifer H-R (2013) Dynamics and environmental risk assessment of the herbicide glyphosate and its metabolite AMPA in a small vineyard river of the Lake Geneva catchment. Environ Toxicol Chem 32:2035–2044. https://doi.org/10.1002/etc.2276

    Article  CAS  Google Scholar 

  • de Campos Oliveira R, Boas LKV, Branco CCZ (2016) Assessment of the potential toxicity of glyphosate-based herbicides on the photosynthesis of Nitella microcarpa var. wrightii (Charophyceae). Phycologia 55:577–584. https://doi.org/10.2216/16-12.1

    Article  CAS  Google Scholar 

  • 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 77:1569–1576

    Article  CAS  Google Scholar 

  • Devin S, Piscart C, Beisel JN, Moreteau JC (2003) Ecological traits of the amphiopod invader Dikerogammarus villosus on a mesohabitat scale. Arch Hydrobiol 158:43–56

    Article  Google Scholar 

  • Edginton AN, Sheridan PM, Stephenson GR, Thompson DG, Boermans HJ (2004) Comparative effects of pH and vision herbicide on two life stages of four anuran amphibian species. Environ Toxicol Chem 23:815–822. https://doi.org/10.1897/03-115

    Article  CAS  Google Scholar 

  • Edwards WM, Triplett GB, Kramer RM (1980) A watershed study of glyphosate transport in runoff. J Environ Qual 9:661–665

    Article  CAS  Google Scholar 

  • Fleeger JW, Carman KR, Nisbet RM (2003) Indirect effects of contaminants in aquatic ecosystems. Sci Total Environ 317:207–233. https://doi.org/10.1016/S0048-9697(03)00141-4

    Article  CAS  Google Scholar 

  • Folmar LC, Sanders HO, Julin AM (1979) Toxicity of the herbicide glyphosate and several of its formulations to fish and aquatic invertebrates. Arch Environm Contain Toxicol 8:269–278

    Article  CAS  Google Scholar 

  • Forfait-Dubuc C, Charles S, Billoir E, Delignette-Muller ML (2012) Survival data analyses in ecotoxicology: critical effect concentrations, methods and models. What should we Use? Ecotoxicol 21:1072–1083. https://doi.org/10.1007/s10646-012-0860-0

    Article  CAS  Google Scholar 

  • Fulda B, Aldrich A, Kasteel R, Balmer M, Poiger T, Concentration PE (2015) Pflanzenschutzmittel in fliessgewässern. Aqua & Gas 9:80–91

    Google Scholar 

  • Glusczak L, Miron Ddos S, Moraes BS, Simões RR, Schetinger MR, Morsch VM, Loro VL (2007) Acute effects of glyphosate herbicide on metabolic and enzymatic parameters of silver catfish (Rhamdia quelen). Comp Biochem Physiol C Toxicol Pharmacol 146:519–524. https://doi.org/10.1016/j.cbpc.2007.06.004

    Article  CAS  Google Scholar 

  • Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818. https://doi.org/10.1126/science.1185383

    Article  CAS  Google Scholar 

  • Gonçalves AL, Lírio AV, Pratas J, Canhoto C (2011) Uranium contaminated water does not affect microbial activity but decreases feeding by the shredder Sericostoma vittatum. Fund Appl Limnol 179:17–25. https://doi.org/10.1127/1863-9135/2011/0179-0017

    Article  CAS  Google Scholar 

  • Guilherme S, Gaivão I, Santos MA, Pacheco M (2012) DNA damage in fish (Anguilla anguilla) exposed to a glyphosate-based herbicide – elucidation of organ-specificity and the role of oxidative stress. Mutat Res – Gen Tox En 743:1–9. https://doi.org/10.1016/j.mrgentox.2011.10.017

    Article  CAS  Google Scholar 

  • Haeckel J-W, Meijering MPD, Rusetzki H (1973) Gammarus fossarum als Falllaubzersetzer in Waldbächen. Freshw Biol 3:241–249

    Article  Google Scholar 

  • Hanazato T (2001) Pesticide effects on freshwater zooplankton: an ecological perspective. Environ Pollut 112:1–10

    Article  CAS  Google Scholar 

  • Hanke I, Singer H, Hollender J (2008) Ultratrace-level determination of glyphosate, aminomethylphosphonic acid and glufosinate in natural waters by solid-phase extraction followed by liquid chromatography–tandem mass spectrometry: performance tuning of derivatization, enrichment and detection. Anal Bioanal Chem 391:2265–2276. https://doi.org/10.1007/s00216-008-2134-5

    Article  CAS  Google Scholar 

  • Hieber M, Gessner MO (2002) Contributions of stream detritivores, fungi, and bacteria to leaf breakdown based on biomass estimates. Ecology 83:1026–1038. https://doi.org/10.2307/3071911

    Article  Google Scholar 

  • Howe CM, Berrill M, Pauli BD, Helbing CC, Werry K, Veldhoen N (2004) Toxicity of glyphosate-based pesticides to four North American frog species. Environ Toxicol Chem 23:1928–1938. https://doi.org/10.1897/03-71

    Article  CAS  Google Scholar 

  • Hua J, Relyea R (2014) Chemical cocktails in aquatic systems: pesticide effects on the response and recovery of >20 animal taxa. Environ Poll 189:18–26. https://doi.org/10.1016/j.envpol.2014.02.007

    Article  CAS  Google Scholar 

  • James C (2008) Global status of commercialized biotech/GM crops: 2008. the first thirteen years, 1996 to 2008. ISAAA Brief No. 39, Ithaca, New York, NY, USA

    Google Scholar 

  • Jonsson M, Malmqvist B (2000) Ecosystem process rate increases with animal species richness: evidence from leaf-eating, aquatic insects. OIKOS 89:519–523

    Article  Google Scholar 

  • Kaiser Dutra B, Amorim Fernandes F, Motta Failace D, Turcato Oliveira G (2011) Effect of Roundup (glyphosate formulation) in the energy metabolism and reproductive traits of Hyalella castroi. Ecotoxicology 20:255–263. https://doi.org/10.1007/s10646-010-0577-x

    Article  CAS  Google Scholar 

  • Kenner RA, Ahmed SI (1975) Measurements of electron transport activities in marine phytoplankton. Mar Biol 33:119–127. https://doi.org/10.1007/BF00390716

    Article  CAS  Google Scholar 

  • Koop JHE, Winkelmann C, Becker J, Hellmann C, Ortmann C (2011) Physiological indicators of fitness in benthic invertebrates: a useful measure for ecological health assessment and experimental ecology. Aquat Ecol 45:547–559. https://doi.org/10.1007/s10452-011-9375-7

    Article  Google Scholar 

  • Kreutzweiser D, Gooda K, Chartranda D, Scarrb T, Thompson D (2007) Non-target effects on aquatic decomposer organisms of imidacloprid as a systemic insecticide to control emerald ash borer in riparian trees. Ecotoxicol Environ Saf 68:315–325. https://doi.org/10.1016/j.ecoenv.2007.04.011

    Article  CAS  Google Scholar 

  • Kunz PY, Kienle C, Gerhardt A (2010) Gammarus spp. in aquatic ecotoxicology and water quality assessment: toward integrated multilevel tests. In: Whitcare DM (Ed.) Reviews of Environmental Contamination and Toxicology, vol 205.Springer, New York, NY, pp 1–76. 10.1007/978-1-4419-5623-1

    Chapter  Google Scholar 

  • Lawrence JA, Poulter C (1998) Development of a sub-lethal pollution bioassay using the estuarine amphipod Gammarus duebeni. Water Res 32:569–578. https://doi.org/10.1016/S0043-1354(97)00306-0

    Article  CAS  Google Scholar 

  • Levine SL, von Mérey G, Minderhout T, Manson P, Sutton P (2015) Aminomethylphosphonic acid has low chronic toxicity to Daphnia magna and Pimephales promelas. Environ Toxicol Chem 34:1382–1389. https://doi.org/10.1002/etc.2940

    Article  CAS  Google Scholar 

  • Lukančič S, Žibrat U, Mezek T, Jerebic A, Simčič T, Brancelj A (2009) Effects of exposing two non-target crustacean species, Asellus aquaticus L., and Gammarus fossarum Koch., to Atrazine and Imidacloprid. Bull Environ Contam Toxicol 84:85–90. https://doi.org/10.1007/s00128-009-9854-x

    Article  CAS  Google Scholar 

  • Maltby L (1999) Studying stress: the importance of organism-level responses. Ecol Appl 9:431–440

    Article  Google Scholar 

  • Maltby L, Naylor C, Calow P (1990) Effect of stress on a freshwater benthic detritivore: scope for growth in gammarus pulex. Ecotoxicol Environ Saf 19:285–291. https://doi.org/10.1016/0147-6513(90)90030-9

    Article  CAS  Google Scholar 

  • Maltby L, Clayton SA, Wood RM, McLoughlin N (2002) Evaluation of the Gammarus pulex in situ feeding assay as a biomonitor of water quality: robustness, responsiveness and relevance. Env Sci Eur 21:361–368

    CAS  Google Scholar 

  • Mann RM, Bidwell JR (1999) The toxicity of glyphosate and several glyphosate formulations to four species of southwestern australian frogs. Arch Environ Contam Toxicol 36:193–199

    Article  CAS  Google Scholar 

  • Mbanaso FU, Coupe SJ, Charlesworth SM, Nnadi EO, Ifelebuegu AO (2014) Potential microbial toxicity and non-target impact of different concentrations of glyphosate-containing herbicide (GCH) in a model pervious paving system. Chemosphere 100:34–41. https://doi.org/10.1016/j.chemosphere.2013.12.091

    Article  CAS  Google Scholar 

  • Monsanto Europe S.A./N.V. (2016) Sicherheitsdatenblatt Roundup LB Plus

  • Mottier A, Kientz-Bouchart V, Serpentini A, Lebel JM, Jha AN, Costil K (2013) Effects of glyphosate-based herbicides on embryo-larval development and metamorphosis in the Pacific oyster, Crassostrea gigas. Aquat Toxicol 128–129:67–78. https://doi.org/10.1016/j.aquatox.2012.12.002

    Article  CAS  Google Scholar 

  • Mugni H, Paracampo A, Solis M, Fanelli S, Bonetto C (2015) Acute toxicity of roundup to the nontarget organism Hyalella curvispina. Laboratory and field study. Toxicol Environ Chem 96:1054–1063. https://doi.org/10.1080/02772248.2014.993641

    Article  CAS  Google Scholar 

  • Navarro CDC, Martinez CBR (2014) Effects of the surfactant polyoxyethylene amine (POEA) on genotoxic, biochemical and physiological parameters of the freshwater teleost Prochilodus lineatus. Comp Biochem Physiol C Toxicol Pharmacol 165:83–90. https://doi.org/10.1016/j.cbpc.2014.06.003

    Article  CAS  Google Scholar 

  • Naylor C, Maltby L, Calow P (1990) Scope for growth in Gammarus pulex, a freshwater benthic detritivore. Hydrobiologia 188/189:517–523

    Article  Google Scholar 

  • Newton M, Horner LH, Cowell JE, White DE, Cole EC (1994) Dissipation of glyphosate and aminomethylphos- phonic acid in North American forests. J Agric Food Chem 42:1795–1802

    Article  CAS  Google Scholar 

  • Nyman A, Hintermeister A, Schirmer K, Ashauer R (2013) The Insecticide Imidacloprid causes mortality of the freshwater amphipod Gammarus pulex by interfering with feeding behavior. PLoS One, 8(5). https://doi.org/10.1371/journal.pone.0062472

    Article  CAS  Google Scholar 

  • Packard TT, Christensen JP (2004) Respiration and vertical carbon flux in the gulf of Maine water column. J Mar Res 62:93–115

    Article  Google Scholar 

  • Packard TT, Williams B (1981) Rates of respiratory oxygen consumption and electron transport in surface seawater from the northwest Atlantic. Oceanol Acta 4:351–358

    CAS  Google Scholar 

  • Pantani C, Pannunzio G, de Cristofaro M, Novelli AA, Salvatori M (1997) Comparative acute toxicity of some pesticides, metals, and surfactants to Gammarus italicus Goedm.and Echinogammarus tibaldii pink. and stock (Crustacea: Amphipoda). Bull Environ Contam Toxic 59:963–967

    Article  CAS  Google Scholar 

  • Partearroyo MA, Pilling SJ, Jones MN (1991) The lysis of isolated fish (Oncorhynchus mykiss) gill epithelial cells by surfactants. Comp Biochem Physiol C Comp Pharmacol 100:381–388. https://doi.org/10.1016/0742-8413(91)90012-I

    Article  Google Scholar 

  • Pérez GL, Vera MS, Miranda LA (2011) Effects of herbicide glyphosate and glyphosate-based formulations on aquatic ecosystems. In: Kortekamp A (ed) Herbicides and environment. InTech, Europe, Rijeka, pp 343–368

    Google Scholar 

  • Pestana JLT, Re A, Nogueira AJA, Soares AMVM (2007) Effects of cadmium and zinc on the feeding behaviour of two freshwater crustaceans: Atyaephyra desmarestii (Decapoda) and Echinogammarus meridionalis (Amphipoda). Chemosphere 68:1556–1562

    Article  CAS  Google Scholar 

  • Pöckl M (1993) Reproductive potential and lifetime potential fecundity of the freshwater amphipods Gammarus fossarum and G. roeseli in Austrian streams and rivers. Freshw Biol 30:73–91. https://doi.org/10.1111/j.1365-2427.1993.tb00790.x

    Article  Google Scholar 

  • Relyea RA (2005) The lethal impact of roundup on aquatic and terrestrial amphibians. Ecol Appl 15:1118–1124

    Article  Google Scholar 

  • Relyea RA (2009) A cocktail of contaminants: how mixtures of pesticides at low concentrations affect aquatic communities. Oecologia 159:363–376. https://doi.org/10.1007/s00442-008-1213-9

    Article  Google Scholar 

  • Relyea RA, Hoverman J (2006) Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecol Lett 9:1157–1171. https://doi.org/10.1111/j.1461-0248.2006.00966.x

    Article  Google Scholar 

  • Rinderhagen M, Ritterhof J, Zauke G (2000) Crustaceans as bioindicators. In: Gerhardt A (ed) Biomonitoring of polluted water—reviews on actual topics, vol 9. Environmental Research ForumTrans Tech Publications - ScitechPublications, Uetikon- Zuerich, p 161–194

    Google Scholar 

  • Schmidlin L, von Fumetti S, Nagel P (2015a) Effects of increased temperatures on Gammarus fossarum under the influence of copper sulphate. Ecotoxicology 24:433–444

    Article  CAS  Google Scholar 

  • Schmidlin L, von Fumetti S, Nagel P (2015b) Temperature effects on the feeding and electron transport system (ETS) activity of Gammarus fossarum. Aquat Ecol 49:71–80

    Article  Google Scholar 

  • Schmidlin L, von Fumetti S, Nagel P (2015c) Copper sulphate reduces the metabolic activity of Gammarus fossarum in laboratory and field experiments. Aquat Toxicol 161:138–145. https://doi.org/10.1016/j.aquatox.2015.02.005

    Article  CAS  Google Scholar 

  • Scribner E, Battaglin W, Gilliom RJ, Meyer MT (2007) Concentrations of glyphosate, its degradation product, aminomethylphosphonic acid, and glufosinate in ground- and surface-water, rainfall, and soil samples collected in the United States, 2001–06. U.S. Geological Survey Investigations Report 2007

  • Shiogiri NS, Paulino MG, Carraschi SP, Baraldi FG, da Cruz C, Narciso Fernandes M (2012) Acute exposure of a glyphosate-based herbicide affects the gills and liver of the Neotropical fish, Piaractus mesopotamicus. Environ Toxicol Pharmacol 34:388–396. https://doi.org/10.1016/j.etap.2012.05.007

    Article  CAS  Google Scholar 

  • Simčič T, Brancelj A (2006) Effects of pH on electron transport system (ETS) activity and oxygen consumption in Gammarus fossarum, Asellus aquaticus and Niphargus sphagnicolus. Freshw Biol 51:686–694. https://doi.org/10.1111/j.1365-2427.2006.01522.x

    Article  CAS  Google Scholar 

  • Simčič T, Lukančič S, Brancelj A (2005) Comparative study of electron transport system activity and oxygen consumption of amphipods from caves and surface habitats. Freshw Biol 50:494–501

    Article  Google Scholar 

  • Toth GL (1999) Aktivität des Elektronentransportsystems. In: von Tümpling W, Friedrich G (eds) Biologische Gewässeruntersuchung. Methoden der Biologischen Wasseruntersuchung 2.. Gustav Fischer Verl., Jena, Stuttgart, Lübeck, Ulm, pp 465–473

    Google Scholar 

  • Tsui CKM, Hyde KD, Hodgkiss IJ (2001) Effects of glyphosate on lignicolous freshwater fungi of Hong Kong. Sydowia 53:167–174

    Google Scholar 

  • Tsui MTK, Chu LM (2003) Aquatic toxicity of glyphosate-based formulations: comparison between different organisms and the effects of environmental factors. Chemosphere 52:1189–1197. https://doi.org/10.1016/S0045-6535(03)00306-0

    Article  CAS  Google Scholar 

  • Tsui MTK, Wang WX, Chu LM (2005) Influence of glyphosate and its formulation (Roundup®) on the toxicity and bioavailability of metals to Ceriodaphnia dubia. Environ Poll 138:59–68. https://doi.org/10.1016/j.envpol.2005.02.018

    Article  CAS  Google Scholar 

  • Von Fumetti S, Nagel P (2012) Discharge variability and its effect on faunistic assemblages in springs. Freshw Sci 31:647–656. https://doi.org/10.1899/10-159.1

    Article  Google Scholar 

  • Wallace JB, Webster JR (1996) The role of macroinvertebrates in stream ecosystem function Annu Rev Entomol 41:115–139

    Article  CAS  Google Scholar 

  • Weiss M, Macher JN, Seefeldt MA, Leese F (2014) Molecular evidence for further overlooked species within the Gammarus fossarum complex (Crustacea:Amphipoda). Hydrobiologia 721:165–184. https://doi.org/10.1007/s10750-013-1658-7

    Article  CAS  Google Scholar 

  • Westram AM, Jokela J, Baumgartner C, Keller I (2011) Spatial distribution of cryptic species diversity in european freshwater amphipods (Gammarus fossarum) as revealed by pyrosequencing. PLoS One 6:1–6. https://doi.org/10.1371/journal.pone.0023879

    Article  CAS  Google Scholar 

  • Widenfalk A, Bertilsson S, Sundh I, Goedkoop W (2008) Effects of pesticides on community composition and activity of sediment microbes e responses at various levels of microbial community organization. Env Poll 152:576–584. https://doi.org/10.1016/j.envpol.2007.07.003

    Article  CAS  Google Scholar 

  • Xuereb B, Bezin L, Chaumot A, Budzinski H, Augagneur S, Tutundjian R, Garric J, Geffard O (2011) Vitellogenin-like gene expression in freshwater amphipod Gammarus fossarum (Koch, 1835): functional characterization in females and potential for use as an endocrine disruption biomarker in males. Ecotoxicology 20:1286–1299. https://doi.org/10.1007/s10646-011-0685-2

    Article  CAS  Google Scholar 

  • Xuereb B, Lefèvre E, Garric J, Geffard O (2009) Acetylcholinesterase activity in Gammarus fossarum (Crustacea Amphipoda): Linking AChE inhibition and behavioural alteration. Aquat Toxicol 94:114–122. https://doi.org/10.1016/j.aquatox.2009.06.010

    Article  CAS  Google Scholar 

  • Zaranyika MF, Nyandoro MG (1993) Degradation of glyphosate in the aquatic environment: an enzymatic kinetic model that takes into account microbial degradation of both free and colloidal (or sediment) particle adsorbed glyphosate. J Agric Food Chem 41:838–842

    Article  CAS  Google Scholar 

  • Zomer Sandrini J, Coimbra Rola R, Moreira Lopes F, Buffon HF, Freitas MM, de Martinez Gaspar Martins C, da Rosa CE (2013) Effects of glyphosate on cholinesterase activity of the mussel Perna perna and the fish Danio rerio and Jenynsia multidentata: in vitro studies. Aquat Toxicol 130–131:171–173. https://doi.org/10.1016/j.aquatox.2013.01.006

    Article  CAS  Google Scholar 

  • Zubrod JP, Englert D, Wolfram J, Wallace D, Schnetzer N, Baudy P, Konschak M, Schulz R, Bundschuh M (2015) Waterborne toxicity and diet-related effects of fungicides in the keyleaf shredder Gammarus fossarum (Crustacea: Amphipoda). Aquat Toxicol 169:105–112. https://doi.org/10.1016/j.aquatox.2015.10.008

    Article  CAS  Google Scholar 

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Acknowledgements

Thanks are owing to those, who helped collecting specimens. We thank L. Schmidlin for her support in conducting the ETS test and for valuable discussions. M. Lehmann gave helpful comments on drafts of the manuscript. Thanks are owing to two anonymous reviewers, who made valuable comments on the manuscript.

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Authors and Affiliations

  1. Department of Environmental Sciences, Biogeography Research Group, University of Basel, Basel, Switzerland

    Stefanie von Fumetti

  2. Department of Hydrology, Faculty for Biology, Chemistry, and Earth Sciences, University of Bayreuth, Bayreuth, Germany

    Katharina Blaurock

Authors
  1. Stefanie von Fumetti
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  2. Katharina Blaurock
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Correspondence to Stefanie von Fumetti.

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von Fumetti, S., Blaurock, K. Effects of the herbicide Roundup® on the metabolic activity of Gammarus fossarum Koch, 1836 (Crustacea; Amphipoda). Ecotoxicology 27, 1249–1260 (2018). https://doi.org/10.1007/s10646-018-1978-5

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  • DOI: https://doi.org/10.1007/s10646-018-1978-5

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