Abstract
Multiple anthropogenic stressors act simultaneously on the environment, with consequences different from those caused by single-stressor exposure. We investigated how the combination of the invasive mussel Limnoperna fortunei and a widely applied herbicide, Roundup Max®, affected freshwater microscopic communities and water quality. Further, we compared these results with those induced by the combination of the mussel and technical-grade glyphosate. We carried out a 34-day experiment in outdoor mesocosms, applying the following six treatments: 6 mg L−1 of technical-grade glyphosate (G), the equivalent concentration of glyphosate in Roundup Max® (R), 100 mussels (M), the combination of mussels and herbicide either in the technical-grade or formulated form (MG and MR, respectively), and control (C). Herbicides significantly increased total phosphorus in water; R and MR showed greater initial total nitrogen and ammonium. R increased picoplankton abundance and caused an eightfold increase in phytoplankton, with high turbidity values; G had a lower effect on these variables. Herbicide-mussel combination induced an accelerated dissipation of glyphosate in water (MG 6.36 ± 0.83 mg G g DW−1 day−1 and MR 5.16 ± 1.26 mg G g DW−1 day−1). A synergistic effect on ammonium was observed in MR but not in MG. MR and MG had an antagonistic effect on phytoplankton, which showed a drastic reduction due to grazing, as revealed by M. We provide evidence of differential effects of Roundup Max® and technical-grade glyphosate over water quality and microscopic communities, and in combination with mussels. However, in the combination of mussels and herbicides, mussels seem to play a leading role. In the presence of L. fortunei, the effects of higher nutrient availability provided by herbicides addition were counteracted by the filtration activity of mussels, which released nutrients, grazed on picoplankton and phytoplankton, and boosted the development of other primary producers, periphyton and metaphyton.
Similar content being viewed by others
References
Austin AP, Harris GE, Lucey WP (1991) Impact of an organophosphate herbicide (glyphosate) on periphyton communities developed in experimental streams. Bull Environ Contam Toxicol 47:29–35
Avigliano L, Fassiano AV, Medesani DA, Ríos de Molina MC, Rodríguez EM (2014) Effects of glyphosate on growth rate, metabolic rate and energy reserves of early juvenile crayfish, Cherax quadricarinatus. Bull Environ Contam Toxicol 92:631–635. doi:10.1007/s00128-014-1240-7
Bengtsson G, Hansson LA, Montenegro K (2004) Reduced grazing rates in Daphnia pulex caused by contaminants: implications for trophic cascades. Environ Toxicol Chem 23(11):2641–2648
Boltovskoy D, Correa N, Cataldo D, Sylvester F (2006) Dispersion and ecological impact of the invasive freshwater bivalve Limnoperna fortunei in the Río de la Plata watershed and beyond. Biol Invasions 8:947–963. doi:10.1007/s10530-005-5107-z
Boltovskoy D, Karatayev A, Burlakova L, Cataldo D, Karatayev V, Sylvester F, Mariñelarena A (2009) Significant ecosystem-wide effects of the swiftly spreading invasive freshwater bivalve Limnoperna fortunei. Hydrobiologia 636:271–284. doi:10.1007/s10750-009-9956-9
Boltovskoy D, Correa N, Sylvester F, Cataldo D (2015) Nutrient recycling, phytoplankton grazing, and associated impacts of Limnoperna fortunei. In: Boltovskoy D (ed) Limnoperna fortunei: the ecology, distribution and control of a swiftly spreading invasive fouling mussel. Springer International Publishing, Cham, pp 153–176
Caquet T, Lagadic L, Sheffield S (2000) Mesocosms in ecotoxicology (1): outdoor aquatic systems. In: Ware GW et al. (eds) Rev environ Contam T 165. Springer-Verlag, New York, pp. 1–38
CASAFE (2014) Estudio de Mercado de Fitosanitarios 2013. Cámara de Sanidad Agropecuaria y Fertilizantes, Buenos Aires
Cataldo D, Boltovskoy D, Hermosa JL, Canzi C (2005) Temperature-dependent rates of larval development in Limnoperna fortunei (Bivalvia: Mytilidae). J Molluscan Stud 71:41–46. doi:10.1093/mollus/eyi005
Cataldo D, O’Farrell I, Paolucci E, Sylvester F, Boltovskoy D (2012a) Impact of the invasive golden mussel (Limnoperna fortunei) on phytoplankton and nutrient cycling. Aquat Invasions 7:91–100. doi:10.3391/ai.2012.7.1.010
Cataldo D, Vinocur A, O´ Farrell I, Paolucci E, Leites V, Boltovskoy D (2012b) The introduced bivalve Limnoperna fortunei boosts Microcystis growth in Salto Grande reservoir (Argentina): evidence from mesocosm experiments. Hydrobiologia 680:25–38. doi:10.1007/s10750-011-0897-8
Cataldo D (2015) Trophic relationships of Limnoperna fortunei with adult fishes. In: Boltovskoy D (ed) Limnoperna fortunei: the ecology, distribution and control of a swiftly spreading invasive fouling mussel. Springer International Publishing, Cham, pp 231–248
Christensen M, Graham M, Vinebrooke R, Findlay D, Paterson M, Turner M (2006) Multiple anthropogenic stressors cause ecological surprises in boreal lakes. Glob Chang Biol 12:2316–2322. doi:10.1111/j.1365-2486.2006.01257.x
Darrigran G, Damborenea C (2011) Ecosystem engineering impact of Limnoperna fortunei in South America. Zool Sci 28:1–7. doi:10.2108/zsj.28.1
Di Fiori E, Pizarro H, dos Santos AM, Cataldo D (2012) Impact of the invasive mussel Limnoperna fortunei on glyphosate concentration in water. Ecotoxicol Environ Saf 81:106–113. doi:10.1016/j.ecoenv.2012.04.024
Edwards WM, Triplett GB Jr, Kramer RM (1980) A watershed study of glyphosate transport in runoff. J Environ Qual 9:661–665
Feng JC, Thompson DG, Reynolds P (1990) Fate of glyphosate in a Canadian forest watershed. 1. Aquatic residues and off-target deposit assessment. J Agric Food Chem 38:1110–1118. doi:10.1021/jf00094a045
Folmar LC, Sanders HO, Julin AM (1979) Toxicity of the herbicide glyphosate and several of its formulations to fish and aquatic invertebrates. Arch Environ Contam Toxicol 8:269–278
Frau D, Rojas Molina F, Devercelli M, Paggi SJ (2012) The effect of an invading filter-feeding bivalve on a phytoplankton assemblage from the Paraná system: a mesocosm experiment. Mar Freshw Behav Physiol. doi:10.1080/10236244.2012.735419
Fuentes L, Moore LJ, Rodgers JH, Bowerman WW, Yarrow GK, Chao WY (2011) Comparative toxicity of two glyphosate formulations (original formulation of Roundup® and Roundup WeatherMAX®) to six North American larval anurans. Environ Toxicol Chem 30:2756–2761. doi:10.1002/etc.670
Gazulha V, Mansur MCD, Cybis LF, Azevedo SMFO (2012) Grazing impacts of the invasive bivalve Limnoperna fortunei (Dunker, 1857) on single-celled, colonial and filamentous cyanobacteria. Braz J Biol 72:33–39
Giesy JP, Dobson S, Solomon KR (2000) Ecotoxicological risk assessment for Roundup® herbicide. Rev Environ Contam Toxicol 167:35–120
Gimsing AL, Borggaard OK (2002) Competitive adsorption of glyphosate and phosphate on clay minerals and oxides. Clay Miner 37:509–515
Goldsborough LG, Beck AE (1989) Rapid dissipation of glyphosate in small forest ponds. Arch Environ Contam Toxicol 18:537–544
Hillebrand H (1983) Development and dynamics of floating clusters of filamentous algae. In: Wetzel RG (ed) Periphyton of freshwater ecosystems. Springer, The Hage, pp 31–39. doi:10.1007/978-94-009-7293-3_7
Horgan MJ, Mills EL (1997) Clearance rates and filtering activity of zebra mussel (Dreissena polymorpha): implications for freshwater lakes. Can J Fish Aquat Sci 54:249–255
Huang JL, Su ZC, Xu Y (2005) The evolution of microbial phosphonate degradative pathways. J Mol Evol 61:682–690. doi:10.1007/s00239-004-0349-4
Ilikchyan IN, McKay RLM, Zehr JP, Dyhrman ST, Bullerjahn GS (2009) Detection and expression of the phosphonate transporter gene phnD in marine and freshwater picocyanobacteria. Environ Microbiol 11(5):1314–1324. doi:10.1111/j.1462-2920.2009.01869.x
Iummato MM, Di Fiori E, Sabatini SE, Cacciatore LC, Cochón AC, Ríos de Molina MC, Juárez AB (2013) Evaluation of biochemical markers in the golden mussel Limnoperna fortunei exposed to glyphosate acid in outdoor microcosms. Ecotoxicol Environ Saf 95:123–129
Karatayev A, Boltovskoy D, Padilla D, Burlakova E (2007) The invasive bivalves Dreissena polymorpha and Limnoperna fortunei: parallels, contrasts, potential spread and invasion impacts. J Shellfish Res 26(1):205–213. doi:10.2983/0730-8000(2007)26[205:TIBDPA]2.0.CO;2
Lipok J, Studnik H, Gruyaert S (2010) The toxicity of Roundup® 360 SL formulation and its main constituents: glyphosate and isopropylamine towards non-target water photoautotrophs. Ecotoxicol Environ Saf 73:1681–1688. doi:10.1016/j.ecoenv.2010.08.017
Magbanua F, Townsend C, Hageman K, Piggot J, Matthaei C (2015) Individual and combined effects of fine sediment and glyphosate herbicide on invertebrate drift and insect emergence: a stream mesocosm experiment. Freshw Sci. doi:10.1086/684363
Mariazzi A, Donadelli JL, Arenas P, Di Siervi MA, Bonetto C (1992) Impact of a nuclear power plant on water quality of Embalse del Río Tercero Reservoir, (Cordoba, Argentina). Hydrobiologia 246:129–140
Mariazzi A, Romero M, Conzonno V, Mariñelarena A (1989) Results of a limnological study in a reservoir previous to the functioning of a nuclear power plant (Embalse Río III, Argentina). Rev Asoc Cs Nat Litoral 20:57–68
Mariñelarena A (2003) Estudio limnológico del Embalse del Río III, Córdoba. Nucleoeléctrica Argentina Technical Report, 103 pp
Marker AFH, Crowther CA, Gunn RJM (1980) Methanol and acetone as solvents for estimating chlorophyll a and phaeopigments by spectrophotometry. Archiv Hydrobiol Beiheft Ergebn Limnol 14:52–69
Meyer MT, Loftin KA, Lee EA, Hinshaw GH, Dietze JE, Scribner EA (2009) Determination of glyphosate, its degradation product aminomethylphosphonic acid, and glufosinate, in water by isotope dilution and online solid phase extraction and liquid chromatography/tandem mass spectrometry. U.S. Geological Survey Techniques and Methods. book 5, chap A10, 32p
Millenium Ecosystem Assessment (2005) Ecosystems and human well-being: biodiversity synthesis. World Resources Institute, Washington DC
Moore LJ, Fuentes L, Rodgers JH Jr, Bowerman WW, Yarrow GK, Chao WY, Bridges WC Jr (2012) Relative toxicity of the components of the original formulation of Roundup® to five North American anurans. Ecotoxicol Environ Saf 78:128–133. doi:10.1016/j.ecoenv.2011.11.025
Morton B (1977) The population dynamics of Limnoperna fortunei (Dunker 1857) (Bivalvia: Mytilacea) in Plover Cove reservoir, Hong Kong. Malacologia 16:165–182
Ormerod SJ, Dobson M, Hildrew AG, Townsend CR (2010) Multiple stressors in freshwater ecosystems. Freshw Biol 55:1–4
Paolucci E, Cataldo D, Fuentes C, Boltovskoy D (2007) Larvae of the invasive species, Limnoperna fortunei (Bivalvia), in the diet of fish larvae in the Paraná River. Hydrobiologia 589:219–233. doi:10.1007/s10750-007-0734-2
Paolucci E, Cataldo D, Boltovskoy D (2010a) Prey selection by larvae of Prochilodus lineatus (Pisces: Curimatidae): indigenous zooplankton versus veligers of the introduced bivalve Limnoperna fortunei (Bivalvia: Mitilidae). Aquat Ecol 44:255–267
Paolucci E, Thuesen E, Cataldo D, Boltovskoy D (2010b) Veligers of an introduced bivalve, Limnoperna fortunei, are a new food resource that enhances growth of larval fish in the Paraná River (South America). Freshw Biol 55:1831–1184
Pastorino G, Darrigran G, Martin S, Lunaschi L (1993) Limnoperna fortunei (Dunker, 1957) (Mytilidae) nuevo bivalvo invasor en aguas del Río de la Plata. Neotropica 39:101–102
Pérez GL, Torremorell A, Mugni H, Rodríguez P, Vera MS, Do Nascimento M, Allende L, Bustingorry J, Escaray R, Ferraro M, Izaguirre I, Pizarro H, Bonetto C, Morris DP, Zagarese H (2007) Effects of the herbicide Roundup on freshwater microbial communities: a mesocosm study. Ecol Appl 17:2310–2322. doi:10.1890/07-0499.1
Peruzzo PJ, Porta AA, Ronco AE (2008) Levels of glyphosate in surface waters, sediments and soils associated with direct sowing soybean cultivation in North Pampasic region of Argentina. Environ Pollut 156(1):61–66
Pizarro H, Di Fiori E, Sinistro R, Rodríguez M, Rodríguez P, Vinocur A, Cataldo D (2015a) Impact of multiple anthropogenic stressors on freshwater: how do glyphosate and the invasive mussel Limnoperna fortunei affect microbial communities and water quality? Ecotoxicology. doi:10.1007/s10646-015-1566-x
Pizarro H, Vera MS, Vinocur A, Pérez G, Ferraro M, Menéndez Helman R, dos Santos Afonso M (2015b) Glyphosate input modifies microbial community structure in clear and turbid freshwater systems. Environ Sci Pollut Res. doi:10.1007/s11356-015-5748-0
Porter KC, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948
Quayle DB (1948) Biology of Venerupis pallastra (Montagu). PhD Thesis, University of Glasgow, Scotland, pp 1–72
Relyea RA (2005) The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecol Appl 15(2):618–627
Relyea RA, Jones DK (2009) The toxicity of Roundup Original Max® to 13 species of larval amphibians. Environ Toxicol Chem 28(9):2004–2008
Relyea RA, Schoeppner NM, Hoverman JT (2005) Pesticides and amphibians: the importance of community context. Ecol Appl 5:1125–1134
Rojas Molina F, Paggi JC, Devercelli M (2010) Zooplanktophagy in the natural diet and selectivity of the invasive mollusk Limnoperna fortunei. Biol Invasions 12:1647–1659. doi:10.1007/s10530-009-9578-1
Rojas Molina F, Paggi S, Boltovskoy D (2011) Vulnerability of microcrustaceans to predation by the invasive filter-feeding mussel Limnoperna fortunei (Dunker). Mar Freshw Behav Physiol 44(6):329–338
Ronco AE, Carriquiriborde P, Natale GS, Martin ML, Mugni H, Bonetto C (2008) Integrated approach for the assessment of biotech soybean pesticides impact on low order stream ecosystems of the Pampasic Region. In: Chen J, Guo C (Eds) Ecosystem Ecology Research Trends, pp 209–239
Sáenz ME, Di Marzio WD, Alberdi JL, Tortorelli MC (1997) Effects of technical grade and a commercial formulation of glyphosate on algal population growth. Bull Environ Contam Toxicol 59:638–644
Sáenz ME, Di Marzio WD (2009) Ecotoxicity of herbicide glyphosate to four chlorophyceaen freshwater algae. Limnetica 28(1):149–158
Sancho JV, Hernandez F, Lopez FJ, Hogendoorn EA, Dijkman E (1996) Rapid determination of glufosinate, glyphosate and aminomethylphosphonic acid in environmental water samples using precolumn fluorogenic labeling and coupled-column liquid chromatography. J Chromatogr A 737(1):75–83
Saxton M, Morrow E, Bourbonniere R, Wilhelm S (2011) Glyphosate influence on phytoplankton community structure in Lake Erie. J Great Lakes Res 37:683–690
Schönbrunn E, Eschenburg S, Shuttleworth WA, Schloss JV, Amrhein N, Evans JNS, Kabsch W (2001) Interaction of the herbicide glyphosate with its target enzyme 5- enolpyruvylshikimate 3-phosphate synthase in atomic detail. Proc Natl Acad Sci U S A 98:1376–1380
Solomon K, Thompson D (2003) Ecological risk assessment for aquatic organisms from over-water uses of glyphosate. J Toxicol Environ Health B Crit Rev 6:289–324. doi:10.1080/15287390390155571
Stalikas CD, Konidari CN (2001) Analytical methods to determine phosphonic and amino acid group-containing pesticides. J Chromatogr A 907(1):1–19
Strayer D (2010) Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshw Biol 55(1):152–174. doi:10.1111/j.1365-2427.2009.02380.x
Sylvester F, Boltovskoy D, Cataldo D (2007) The invasive bivalve Limnoperna fortunei enhances benthic invertebrate densities in south American floodplain rivers. Hydrobiologia 589:15–27. doi:10.1007/s10750-007-0708-4
Sylvester F, Dorado J, Boltovskoy D, Juárez A, Cataldo D (2005) Filtration rates of the invasive pest bivalve Limnoperna fortunei as a function of size and temperature. Hydrobiologia 534:71–80. doi:10.1007/s10750-004-1322-3
Tilman D, Fargione J, Wolff B, D’Antonio C, Dobson A, Howarth R, Schindler D, Schlesinger WH, Simberloff D, Swackhamer D (2001) Forecasting agriculturally driven global environmental change. Science 292(5515):281–284
Tokumon R, Cataldo D, Boltovskoy D (2015) Effects of suspended inorganic matter on filtration and grazing rates of the invasive mussel Limnoperna fortunei (Bivalvia: Mytiloidea). J Molluscan Stud:1–4. doi:10.1093/mollus/eyv024
Townsend C, Uhlmann S, Matthaei C (2008) Individual and combined responses of stream ecosystems to multiple stressors. J Appl Ecol 45:1810–1819. doi:10.1111/j.1365-2664.2008.01548.x
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
Utermöhl H (1958) Zur vervollkommnung der quantitativen Phytoplankton Methodik. Mitt Int Ver Limnol 9:1–38
Valderrama JC (1981) The simultaneous analysis of total nitrogen and total phosphorus in natural waters. Mar Chem 10:109–122
Venrick EL (1978) How many cells to count? In: Sournia A (ed) Phytoplankton manual. UNESCO Press, Paris, pp. 167–180
Vera MS, Di Fiori E, Lagomarsino L, Sinistro R, Escaray R, Iummato M, Juárez A, Ríos de Molina M, Tell G, Pizarro H (2012) Direct and indirect effects of the glyphosate formulation Glifosato Atanor® on freshwater microbial communities. Ecotoxicology 21(7):1805–1816. doi:10.1007/s10646-012-0915-2
Vera MS, Lagomarsino L, Sylvester M, Pérez G, Rodríguez P, Mugni H, Sinistro R, Ferraro M, Bonetto C, Zagarese H, Pizarro H (2010) New evidences of Roundup® (glyphosate formulation) impact on the periphyton and the water quality of freshwater ecosystems. Ecotoxicology 19:710–772. doi:10.1007/s10646-009-0446-7
Waiman CV, Avena MJ, Garrido M, Band BF, Zanini GP (2012) A simple and rapid spectrophotometric method to quantify the herbicide glyphosate in aqueous media. Appl Adsorpt Isotherms Soils Goethite Geoderma 170:154–158
Acknowledgments
This work was supported by the Agencia Nacional de Promoción Científica y Tecnológica (PICT 2010 0908 and 2014 1586) and Universidad de Buenos Aires (UBACyT 20020100100550). We thank Leidy Velandia for field assistance.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Thomas Braunbeck
Rights and permissions
About this article
Cite this article
Gattás, F., Vinocur, A., Graziano, M. et al. Differential impact of Limnoperna fortunei-herbicide interaction between Roundup Max® and glyphosate on freshwater microscopic communities. Environ Sci Pollut Res 23, 18869–18882 (2016). https://doi.org/10.1007/s11356-016-7005-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-016-7005-6