Abstract
Concentrations of glyphosate observed in the environment are generally lower than those found to exert toxicity on aquatic organisms in the laboratory. Toxicity is often tested in the absence of other expected co-occurring contaminants. By examining changes in the phytoplankton and zooplankton communities of shallow, partitioned wetlands over a 5 month period, we assessed the potential for direct and indirect effects of the glyphosate-based herbicide, Roundup WeatherMax© applied at the maximum label rate, both in isolation and in a mixture with nutrients (from fertilizers). The co-application of herbicide and nutrients resulted in an immediate but transient decline in dietary quality of phytoplankton (8.3 % decline in edible carbon content/L) and zooplankton community similarity (27 % decline in similarity and loss of three taxa), whereas these effects were not evident in wetlands treated only with the herbicide. Thus, even at a worst-case exposure, this herbicide in isolation, did not produce the acutely toxic effects on plankton communities suggested by laboratory or mesocosm studies. Indirect effects of the herbicide-nutrient mixture were evident in mid-summer, when glyphosate residues were no longer detectable in surface water. Zooplankton abundance tripled, and zooplankton taxa richness increased by an average of four taxa in the herbicide and nutrient treated wetlands. The lack of significant toxicity of Roundup WeatherMax alone, as well as the observation of delayed interactive or indirect effects of the mixture of herbicide and nutrients attest to the value of manipulative field experiments as part of a comprehensive, tiered approach to risk assessments in ecotoxicology.
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References
Baker LF, Mudge JF, Houlahan JE, Thompson DG, Kidd KA (2014) The direct and indirect effects of a glyphosate-based herbicide and nutrients on Chrionomidae (Diptera) emerging from small wetlands. Environ Toxicol Chem 33:2076–2085. doi:10.1002/etc.2657
Bartell SM, Gardner RH, O’Neill RV (1992) Ecological risk estimation. Lewis Publishers Inc., Chelsea
Battaglin WA, Kolpin DW, Scribner EA, Kuivila KM, Sandstrom MW (2005) Glyphosate, other herbicides, and transformation products in Midwestern streams, 2002. J Am Water Resour Assoc 41:323–332
Battaglin W, Meyer M, Kuivila K, Dietze J (2014) Glyphosate and its degradation product AMPA occur frequently and widely in US soils, surface water, groundwater, and precipitation. JAWRA J Am Water Resour Assoc 50:275–290
Bengtsson G, Hansson LA, Montenegro K (2004) Reduced grazing rates in Daphnia pulex caused by contaminants: implications for trophic cascades. Environ Toxicol Chem 23:2641–2648
Bollens SM, Frost BW, Thoreson DS, Watts SJ (1992) Diel vertical migration in zooplankton: field evidence in support of the predator avoidance hypothesis. Hydrobiologia 234:33–39
Boone MD, Bridges CM, Fairchild JF, Little EE (2005) Multiple sublethal chemicals negatively affect tadpoles of the green frog, Rana clamitans. Environ Toxicol Chem 24:1267–1272
Bray JR, Curtis JT (1957) An ordination of the upland forest communities of Southern Wisconsin. Ecol Monogr 27:326–349
Byer JD, Struger J, Klawunn P, Todd A, Sverko E (2008) Low cost monitoring of glyphosate in surface waters using the ELISA method: an evaluation. Environ Sci Technol 42:6052–6057. doi:10.1021/es8005207
Cairns J (1988) Putting the eco in ecotoxicology. Regul Toxicol Pharmacol 8:226–238
Cazzanelli M, Warming TP, Christoffersen KS (2008) Emergent and floating-leaved macrophytes as refuge for zooplankton in a eutrophic temperate lake without submerged vegetation. Hydrobiologia 605:113–122. doi:10.1007/s10750-008-9324-1
CCME (2012) Canadian water quality guidelines for the protection of aquatic life: glyphosate. Canadian Council of Ministers of the Environment, Winnipeg
Chen CY, Hathaway KM, Folt CL (2004) Multiple stress effects of Vision® herbicide, pH, and food on zooplankton and larval amphibian species from forest wetlands. Environ Toxicol Chem 23:823–831
Cottenie K, Michels E, Nuytten N, De Meester L (2003) Zooplankton metacommunity structure: regional vs. local processes in highly interconnected ponds. Ecology 84:991–1000. doi:10.1890/0012-9658(2003)084[0991:zmsrvl]2.0.co;2
Cottingham KL, Knight SE, Carpenter SR, Cole JJ, Pace ML, Wagner AE (1997) Response of phytoplankton and bacteria to nutrients and zooplankton: a mesocosm experiment. J Plankton Res 19:995–1010
Cuppen JGM, Gylstra R, Vanbeusekom S, Budde BJ, Brock TCM (1995) Effects of nutrient loading and insecticide application on the ecology of Elodea-dominated freshwater microcosms: 3. Responses of macroinvertebrate detritivores, breakdown of plant litter, and final conclusions. Arch Hydrobiol 134:157–177
Degenhardt D et al (2012) Dissipation of glyphosate and aminomethylphosphonic acid in water and sediment of two Canadian prairie wetlands. J Environ Sci Health B 47:631–639
Draggan S, Giddings JM (1978) Testing toxic substances for protection of the environment. Sci Total Environ 9:63–74
Edge C, Thompson D, Hao CY, Houlahan J (2014) The response of amphibian larvae to exposure to a glyphosate-based herbicide (Roundup WeatherMax) and nutrient enrichment in an ecosystem experiment. Ecotox Environ Safe 109:124–132. doi:10.1016/j.ecoenv.2014.07.040
Flinn MB, Whiles MR, Adams SR, Garvey JE (2005) Macroinvertebrate and zooplankton responses to emergent plant production in upper Mississippi River floodplain wetlands. Arch Hydrobiol 162:187–210. doi:10.1127/0003-9136/2005/0162-0187
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
Forlani G, Pavan M, Gramek M, Kafarski P, Lipok J (2008) Biochemical bases for a widespread tolerance of cyanobacteria to the phosphonate herbicide glyphosate. Plant Cell Physiol 49:443–456. doi:10.1093/pcp/pcn021
Ghadouani A, Pinel-Alloul B, Prepas EE (2006) Could increased cyanobacterial biomass following forest harvesting cause a reduction in zooplankton body size structure? Can J Fish Aquat Sci 63:2308–2317. doi:10.1139/f06-117
Giesy JP, Dobson S, Solomon KR (2000) Ecotoxicological risk assessment for Roundup® herbicide. Rev Environ Contam Toxicol 167:35–120
Glass RL (1987) Adsorption of glyphosate by soils and clay minerals. J Agric Food Chem 35:497–500. doi:10.1021/jf00076a013
Goldsborough LG, Beck AE (1989) Rapid dissipation of glyphosate in small forest ponds. Arch Environ Contam Toxicol 18:537–544
Goldsborough LG, Brown DJ (1993) Dissipation of glyphosate and aminomethylphosphonic acid in water and sediments of boreal forest ponds. Environ Toxicol Chem 12:1139–1147
Henry CJ, Higgins KF, Buhl KJ (1994) Acute toxicity and hazard assessment of Rodeo®, X-77 Spreader®, and Chem-Trol® to aquatic invertebrates. Arch Environ Contam Toxicol 27:392–399
Hunt BPV, Gurney LJ, Pakhomov EA (2008) Time-series analysis of hydrological and biological variability on the Prince Edward Island (Southern Ocean) shelf. Polar Biol 31:893–904. doi:10.1007/s00300-008-0427-y
Kerfoot WC, Deangelis DL (1989) Scale-dependent dynamics: zooplankton and the stability of fresh water food webs. Trends Ecol Evol 4:167–171
Kirchman D (1994) The uptake of inorganic nutrients by heterotrophic bacteria. Microb Ecol 28:255–271
Maillard E, Payraudeau S, Faivre E, Gregoire C, Gangloff S, Imfeld G (2011) Removal of pesticide mixtures in a stormwater wetland collecting runoff from a vineyard catchment. Sci Total Environ 409:2317–2324. doi:10.1016/j.scitotenv.2011.01.057
Mikó Z, Ujszegi J, Gál Z, Imrei Z, Hettyey A (2015) Choice of experimental venue matters in ecotoxicology studies: comparison of a laboratory-based and an outdoor mesocosm experiment. Aquat Toxicol 167:20–30
Monsanto Company (2009) Material safety data sheet roundup herbicide. Nufarm Australia http://search.nufarm.com.au/msds/nufarm/ROUNDUP%20HERBICIDE_24107668.pdf. Accessed 2 Jan 2013
Mudge JF, Baker LF, Edge CB, Houlahan JE (2012) Setting an optimal α that minimizes errors in null hypothesis significance tests. Public Libr Sci One 7:e32734. doi:10.1371/journal.pone.0032734
Munkittrick KR, Arens CJ, Lowell RB, Kaminski GP (2009) A review of potential methods of determining critical effect size for designing environmental monitoring programs. Environ Toxicol Chem 28:1361–1371
Oksanen J et al. (2015) Package ‘vegan’: Community Ecology Package. 2.2-1 version
Development Core Team R (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Ollsen C, Knopper L (2006) Task 2A: the history and science of herbicide use at CFB Gagetown from 1952 to present (Peer reviewed). Jacques Whitford Ltd., Ottawa
Perez GL et al (2007) Effects of the herbicide roundup on freshwater microbial communities: a mesocosm study. Ecol Appl 17:2310–2322
Powell HA, Kerby NW, Rowell P (1991) Natural tolerance of cyanobacteria to the herbicide glyphosate. New Phytol 119:421–426. doi:10.1111/j.1469-8137.1991.tb00042.x
Rasband WS (1997-2012) Image J. National Institutes of Health, Bethesda, MD, USA. http://imagej.nih.gov/ij/
Relyea RA (2005a) The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecol Appl 15:618–627
Relyea RA (2005b) The lethal impact of roundup on aquatic and terrestrial amphibians. Ecol Appl 15(4):1118–1124
Relyea RA (2009) A cocktail of contaminants: how mixtures of pesticides at low concentrations affect aquatic communities. Oecologia 159:363–376. doi:10.1007/s00442-008-1213-9
Rocha O, Duncan A (1985) The relationship between cell carbon and cell volume in fresh water algal species used in zooplanktonic studies. J Plankton Res 7:279–294. doi:10.1093/plankt/7.2.279
Sagrario G, De LosÁngeles M, Balseiro E, Ituarte R, Spivak E (2009) Macrophytes as refuge or risky area for zooplankton: a balance set by littoral predacious macroinvertebrates. Freshw Biol 54:1042–1053
Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E (1993) Alternative equilibria in shallow lakes. Trends Ecol Evol 8:275–279
Schindler DW (1974) Eutrophication and recovery in experimental lakes: implications for lake management. Science 184:897–899
Schindler DW (2001) The cumulative effects of climate warming and other human stresses on Canadian freshwaters in the new millennium. Can J Fish Aquat Sci 58:18–29
Scribner EA, Battaglin WA, 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 Scientific Investigations Report 2007-5122. Reston, Virginia
Simenstad CA, Cordell JR, Tear L, Weitkamp LA, Paveglio FL, Kilbride KM, Fresh KL, Grue CE (1996) Use of Rodeo® and X-77® spreader to control smooth cordgrass (Spartina alterniflora) in a southwestern Washington estuary. 2. Effects on benthic microflora and invertebrates. Environ Toxicol Chem 15:969–978
Solomon KR, Thompson DG (2003) Ecological risk assessment for aquatic organisms from over-water uses of glyphosate. J Toxicol Environ Health B 6:289–324
Struger J, Thompson D, Staznik B, Martin P, McDaniel T, Marvin C (2008) Occurrence of glyphosate in surface waters of Southern Ontario. Bull Environ Contam Toxicol 80:378–384
Thompson DG (2004) Potential effects of herbicides on native amphibians: a hierarchical approach to ecotoxicology research and risk assessment. Environ Toxicol Chem 23:813–814
Thorp JH, Covich AP (2001) Ecology and classification of North American freshwater invertebrates. Academic Press, San Diego, CA, p 1056
Timms RM, Moss B (1984) Prevention of growth of potentially dense phytoplankton populations by zooplankton grazing, in the presence of zooplanktivorous fish, in a shallow wetland ecosystem. Limnol Oceanogr 29:472–486
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
Tsui MTK, Chu LM (2004) Comparative toxicity of glyphosate-based herbicides: aqueous and sediment porewater exposures. Arch Environ Contam Toxicol 46:316–323
van den Brink PJ, ter Braak CJF (1999) Principal response curves: analysis of time-dependent multivariate responses of biological community to stress. Environ Toxicol Chem 18:138–148
Vandonk E, Grimm MP, Gulati RD, Breteler J (1990) Whole lake food wed manipulation as a means to study community interactions in a small ecosystem. Hydrobiologia 200:275–289
Vendrell E, de Barreda Gómez, Ferraz D, Sabater C, Carrasco JM (2009) Effect of glyphosate on growth of four freshwater species of phytoplankton: a microplate bioassay. Bull Environ Contam Toxicol 82:538–542. doi:10.1007/s00128-009-9674-z
Ward HB, Whipple GC (1945) Fresh-water biology. John Wiley and Sons, Inc., New York, NY, p 1111
Wetzel R (2001) Chapter 13: The phosphorus cycle. Limnology: lake and river ecosystems, 3rd edn. Academic Press, Orlando, FL, pp 239–331
Zaranyika MF, Nyandoro MG (1993) Degradation of glyphosate in the aquatic environment: an enzymic 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
Zrum L, Hann BJ (2002) Invertebrates associated with submersed macrophytes in a prairie wetland: effects of organophosphorus insecticide and inorganic nutrients. Arch Hydrobiol 154:413–445
Acknowledgments
Funding for the present study was provided by National Sciences and Engineering Research Council of Canada (NSERC) Strategic and Discovery grants, the Canada Research Chairs program, Natural Resources Canada, the National Department of Defence, and the University of New Brunswick Saint John. We thank V. Trudeau, B. Pauli, M. Gahl, L. Navarro, C. Edge, S. Melvin, C. Carpenter, S. Sadeghi, J. Stewart, B. Reinhart, M. Houle, B. Salmon, A. Carpenter, D. Harvey, and L. Perry for their assistance in the lab and field. We also thank P. Chambers for assistance with experimental design.
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Baker, L.F., Mudge, J.F., Thompson, D.G. et al. The combined influence of two agricultural contaminants on natural communities of phytoplankton and zooplankton. Ecotoxicology 25, 1021–1032 (2016). https://doi.org/10.1007/s10646-016-1659-1
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DOI: https://doi.org/10.1007/s10646-016-1659-1