Abstract
Genetically modified organisms are used extensively in agriculture. To assess potential side effects of genetically modified (GM) plant material on aquatic ecosystems, only a very small number of higher-tier studies have been performed. At the same time, these studies are particularly important for comprehensive risk assessment covering complex ecological relationships. Here we evaluate the methods of experimental higher-tier effect studies with GM plant material (or Bt toxin) in comparison to those well-established for pesticides. A major difference is that nominal test concentrations and thus dose-response relationships cannot easily be produced with GM plant material. Another important difference, particularly to non-systemic pesticides, is that aquatic organisms are exposed to GM plant material primarily through their feed. These and further differences in test requirements, compared with pesticides, call for a standardisation for GM-specific higher-tier study designs to assess their potentially complex effects in the aquatic ecosystems comprehensively.
Similar content being viewed by others
References
Anderson JA, Staley J, Challender M, Heuton J (2018) Safety of Pseudomonas chlororaphis as a gene source for genetically modified crops. Transgenic Res 27(1):103–113. https://doi.org/10.1007/s11248-018-0061-6
Armbrust KL, Peeler HB (2002) Effects of formulation on the run-off of imidacloprid from turf. Pest Manag Sci 58(7):702–706. https://doi.org/10.1002/ps.518
Axelsson E, Petter; Hjältén J, LeRoy CJ, Julkunen-Tiitto R, Wennström A, Pilate G (2010) Can Leaf Litter from genetically modified Trees affect aquatic ecosystems? Ecosystems 13(7):1049–1059. https://doi.org/10.1007/s10021-010-9373-y
Axelsson E, Petter; Hjältén J, LeRoy CJ, Whitham TG, Julkunen-Tiitto R, Wennström A (2011) Leaf litter from insect-resistant transgenic trees causes changes in aquatic insect community composition. J Appl Ecol 48(6):1472–1479. https://doi.org/10.1111/j.1365-2664.2011.02046.x
Beuter L-K, Dören L, Hommen U, Kotthoff M, Schäfers C, Ebke KP (2019) Testing effects of pesticides on macroinvertebrate communities in outdoor stream mesocosms using carbaryl as example test item. Environ Sci Eur 31(1):3290. https://doi.org/10.1186/s12302-019-0185-1
Boeckman CJ, Huang E, Sturtz K, Walker C, Woods R, Zhang J (2019) Characterization of the Spectrum of Insecticidal Activity for IPD072Aa: A protein derived from Pseudomonas chlororaphis with activity against Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae). J Econ Entomol 112(3):1190–1196. https://doi.org/10.1093/jee/toz029
Bøhn T, Traavik T, Primicerio R (2010) Demographic responses of Daphnia magna fed transgenic Bt-maize. Ecotoxicology 19(2):419–430. https://doi.org/10.1007/s10646-009-0427-x
Böttger R, Schaller J, Lintow S, Gert Dudel E (2015) Aquatic degradation of Cry1Ab protein and decomposition dynamics of transgenic corn leaves under controlled conditions. Ecotoxicol Environ Saf 113:454–459. https://doi.org/10.1016/j.ecoenv.2014.12.034
Brandão-Dias PFP, Rosi EJ, Shogren AJ, Tank JL, Fischer DT, Egan SP (2021) Fate of environmental proteins (eProteins) from genetically Engineered crops in Streams is controlled by Water pH and ecosystem metabolism. Environ Sci Technol 55(8):4688–4697. https://doi.org/10.1021/acs.est.0c05731
Brock TCM, Alix A, Brown CD, Capri E, Gottesbüren, Bernhard FF, Heimbach, Fred et al (eds) (2010) Linking aquatic exposure and effects. Risk assessment of pesticides. Boca Raton. CRC Press, Taylor & Francis Group (Society of environmental toxicology and chemistry (SETAC)), London, New York
Brown CD, Bellamy PH, Dubus IG (2002) Prediction of pesticide concentrations found in rivers in the UK. Pest Manag Sci 58(4):363–373. https://doi.org/10.1002/ps.466
Brühl CA, Després L, Frör O, Patil CD, Poulin B, Tetreau G, Allgeier S (2020) Environmental and socioeconomic effects of mosquito control in Europe using the biocide Bacillus thuringiensis subsp. israelensis (bti). Sci Total Environ 724:137800. https://doi.org/10.1016/j.scitotenv.2020.137800
Bundschuh M, Hahn T, Gessner MO, Schulz R (2009) Antibiotics as a chemical stressor affecting an aquatic decomposer-detritivore system. Environ Toxicol Chem 28(1):197–203. https://doi.org/10.1897/08-075.1
Bundschuh R, Bundschuh M, Otto M, Schulz R (2019) Food-related exposure to systemic pesticides and pesticides from transgenic plants: evaluation of aquatic test strategies. Environ Sci Eur 31(1):3290. https://doi.org/10.1186/s12302-019-0266-1
Bundschuh R, Kuhn U, Bundschuh M, Naegele C, Elsaesser D, Schlechtriemen U et al (2016) Prioritizing stream types according to their potential risk to receive crop plant material - A GIS-based procedure to assist in the risk assessment of genetically modified crops and systemic insecticide residues. Sci Total Environ 547:226–233. https://doi.org/10.1016/j.scitotenv.2015.12.124
Cañedo-Argüelles M, Bundschuh M, Gutiérrez-Cánovas C, Kefford BJ, Prat N, Trobajo R, Schäfer RB (2014) Effects of repeated salt pulses on ecosystem structure and functions in a stream mesocosm. Sci Total Environ 476–477. https://doi.org/10.1016/j.scitotenv.2013.12.067
Carstens K, Anderson J, Bachman P, De Schrijver A, Dively G, Federici B et al (2012) Genetically modified crops and aquatic ecosystems: considerations for environmental risk assessment and non-target organism testing. Transgenic Res 21(4):813–842. https://doi.org/10.1007/s11248-011-9569-8
Chambers CP, Whiles MR, Rosi-Marshall EJ, Tank JL, Royer TV, Griffiths NA et al (2010) Responses of stream macroinvertebrates to Bt maize leaf detritus. Ecol Appl 20(7):1949–1960. https://doi.org/10.1890/09-0598.1
De Schrijver A, Devos Y, De Clercq P, Gathmann A, Romeis J (2016) Quality of laboratory studies assessing effects of Bt-proteins on non-target organisms: minimal criteria for acceptability. Transgenic Res 25(4):395–411. https://doi.org/10.1007/s11248-016-9950-8
DIN EN ISO 21569:2013-08, Lebensmittel - Verfahren zum Nachweis von gentechnisch modifizierten Organismen und ihren Produkten - Qualitative auf Nukleinsäuren basierende Verfahren
DIN EN ISO 21570 :2013-08, Lebensmittel- Verfahren zum Nachweis von gentechnisch modifizierten Organismen und ihren Produkten- Quantitative auf Nukleinsäuren basierende Verfahren
DIN EN ISO 24276: 2013-10, Lebensmittel - Verfahren zum Nachweis von gentechnisch modifizierten Organismen und ihren Produkten- Allgemeine Anforderungen und Definitionen
Douville M, Gagn F, Masson L, McKay J, Blaise C (2005) Tracking the source of Bacillus thuringiensis Cry1Ab endotoxin in the environment. Biochem Syst Ecol 33(3):219–232. https://doi.org/10.1016/j.bse.2004.08.001
EFSA (2010a) : Guidance on the environmental risk assessment of genetically modified plants. In: EFS2 8 (11), S. 1879. https://doi.org/10.2903/j.efsa.2010.1879
EFSA (2010b) : Scientific Opinion on the assessment of potential impacts of genetically modified plants on non-target organisms. In: EFS2 8 (11), S. 1877. https://doi.org/10.2903/j.efsa.2010.1877
EFSA (2013) : Guidance on tiered risk assessment for plant protection products for aquatic organisms in edge-of‐field surface waters. In: EFS2 11 (7). https://doi.org/10.2903/j.efsa.2013.3290
Englert D, Bakanov N, Zubrod JP, Schulz R, Bundschuh M (2017a) Modeling remobilization of Neonicotinoid residues from Tree Foliage in Streams - a relevant exposure pathway in Risk Assessment? Environ Sci Technol 51(3):1785–1794. https://doi.org/10.1021/acs.est.6b05213
Englert D, Zubrod JP, Link M, Mertins S, Schulz R, Bundschuh M (2017b) Does Waterborne exposure explain Effects caused by neonicotinoid-contaminated plant material in aquatic Systems? Environ Sci Technol 51(10):5793–5802. https://doi.org/10.1021/acs.est.7b00827
Englert D, Zubrod JP, Pietz S, Stefani S, Krauss M, Schulz R, Bundschuh M (2017c) Relative importance of dietary uptake and waterborne exposure for a leaf-shredding amphipod exposed to thiacloprid-contaminated leaves. Sci Rep 7(1):16182. https://doi.org/10.1038/s41598-017-16452-9
Fausti SW, McDonald TM, Lundgren JG, Li J, Keating AR, Catangui M (2012) Insecticide use and crop selection in regions with high GM adoption rates. Renew Agric Food Syst 27(4):295–304. https://doi.org/10.1017/s1742170511000561
Flury M (1996) Experimental evidence of transport of Pesticides through Field Soils—A review. J environ qual 25(1):25–45. https://doi.org/10.2134/jeq1996.00472425002500010005x
Gill SS, Cowles EA, Pietrantonio PV (1992) The mode of action of Bacillus thuringiensis endotoxins. Ann Rev Entomol 37:615–636. https://doi.org/10.1146/annurev.en.37.010192.003151
Griffiths NA, Tank JL, Royer TV, Rosi EJ, Shogren AJ, Frauendorf TC, Whiles MR (2017) Occurrence, leaching, and degradation of Cry1Ab protein from transgenic maize detritus in agricultural streams. Sci Total Environ 592:97–105. https://doi.org/10.1016/j.scitotenv.2017.03.065
Griffiths NA, Tank JL, Royer TV, Rosi-Marshall EJ, Whiles MR, Chambers CP et al (2009) Rapid decomposition of maize detritus in agricultural headwater streams. Ecol Appl 19(1):133–142. https://doi.org/10.1890/07-1876.1
Hand LH, Oliver RG (2010) The behavior of isopyrazam in aquatic ecosystems: implementation of a tiered investigation. Environ Toxicol Chem 29(12):2702–2712. https://doi.org/10.1002/etc.337
Hanson ML, Graham DW, Babin E, Azam D, Coutellec M-A, Knapp CW et al (2007) Influence of isolation on the recovery of pond mesocosms from the application of an insecticide. I. Study design and planktonic community responses. Environ Toxicol Chem 26(6):1265–1279. https://doi.org/10.1897/06-248R.1
Hilbeck A, Bundschuh R, Bundschuh M, Hofmann F, Oehen B, Otto M et al (2017) Procedure to select test organisms for environmental risk assessment of genetically modified crops in aquatic systems. Integr Environ Assess Manag 13(6):974–979. https://doi.org/10.1002/ieam.1965
James C (2019) Global Status of Commercialized Biotech/GM crops: 2019. International Service for the Acquisition of Agri-biotech Applications (ISAAA)
Jensen PD, Dively GP, Swan CM, Lamp WO (2010) Exposure and nontarget effects of transgenic bt corn debris in streams. Environ Entomol 39(2):707–714. https://doi.org/10.1603/EN09037
Konschak M, Zubrod JP, Baudy P, Englert D, Herrmann B, Schulz R, Bundschuh M(2019) : Waterborne and diet-related effects of inorganic and organic fungicides on the insect leaf shredder Chaetopteryx villosa (Trichoptera). In: Aquatic toxicology (Amsterdam, Netherlands) 206, S. 33–42. https://doi.org/10.1016/j.aquatox.2018.10.021
Kreutzweiser DP, Good KP, Chartrand DT, Scarr TA, Thompson DG (2008) Are leaves that fall from imidacloprid-treated maple trees to control asian longhorned beetles toxic to non-target decomposer organisms? J Environ Qual 37(2):639–646. https://doi.org/10.2134/jeq2007.0278
Lamers M, Anyusheva M, La N, van Nguyen V, Streck T (2011) Pesticide Pollution in Surface- and Groundwater by Paddy Rice Cultivation: a Case Study from Northern Vietnam. Clean Soil Air Water 39(4):356–361. https://doi.org/10.1002/clen.201000268
Latham JR, Love M, Hilbeck A (2017) The distinct properties of natural and GM cry insecticidal proteins. Biotechnol Genet Eng Rev 33(1):62–96. https://doi.org/10.1080/02648725.2017.1357295
Li G, Wang Y, Liu B, Zhang G (2014) Transgenic Bacillus thuringiensis (bt) rice is safer to aquatic ecosystems than its non-transgenic counterpart. PLoS ONE 9(8):e104270. https://doi.org/10.1371/journal.pone.0104270
Li Y, Wu K, Zhang Y, Yuan G (2007) Degradation of Cry1Ac protein within transgenic Bacillus thuringiensis Rice Tissues under Field and Laboratory Conditions. Environ Entomol 36(5):1275–1282. https://doi.org/10.1093/ee/36.5.1275
Liu Y, Jiang W, Liang Y, Zhao C, Li J (2017) No effect of Bt-transgenic rice litter on the meiobenthos community in field ditches. Pest Manag Sci 73(6):1213–1219. https://doi.org/10.1002/ps.4446
Liu Y, Li J, Luo Z, Wang H, Liu F (2016) The fate of fusion Cry1Ab/1Ac proteins from Bt-transgenic rice in soil and water. Ecotoxicol Environ Saf 124:455–459. https://doi.org/10.1016/j.ecoenv.2015.11.025
Morrissey CA, Mineau P, Devries JH, Sanchez-Bayo F, Liess M, Cavallaro MC, Liber K (2015) Neonicotinoid contamination of global surface waters and associated risk to aquatic invertebrates: a review. Environ Int 74:291–303. https://doi.org/10.1016/j.envint.2014.10.024
Newton K, Zubrod JP, Englert D, Lüderwald S, Schell T, Baudy P et al(2018) : The evil within? Systemic fungicide application in trees enhances litter quality for an aquatic decomposer-detritivore system. In: Environmental pollution (Barking, Essex: 1987) 241, S. 549–556. https://doi.org/10.1016/j.envpol.2018.05.069
Parisi C, Tillie P, Rodríguez-Cerezo E (2016) The global pipeline of GM crops out to 2020. Nat Biotechnol 34(1):31–36. https://doi.org/10.1038/nbt.3449
Pott A, Bundschuh M, Bundschuh R, Otto M, Schulz R (2020) Effect of Bt toxin Cry1Ab on two freshwater caddisfly shredders - an attempt to establish dose-effect relationships through food-spiking. Sci Rep 10(1):5262. https://doi.org/10.1038/s41598-020-62055-2
Pott A, Otto M, Schulz R (2018) Impact of genetically modified organisms on aquatic environments: review of available data for the risk assessment. Sci Total Environ 635:687–698. https://doi.org/10.1016/j.scitotenv.2018.04.013
Preston BL (2002) Indirect effects in aquatic ecotoxicology: implications for ecological risk assessment. Environ Manage 29(3):311–323. https://doi.org/10.1007/s00267-001-0023-1
Prihoda KR, Coats JR (2008) Aquatic fate and effects of Bacillus thuringiensis Cry3Bb1 protein: toward risk assessment. Environ Toxicol Chem 27(4):793–798. https://doi.org/10.1897/07-300.1
Rosi-Marshall EJ, Tank JL, Royer TV, Whiles MR, Evans-White M, Chambers C et al (2007) Toxins in transgenic crop byproducts may affect headwater stream ecosystems. Proc Natl Acad Sci USA 104(41):16204–16208. https://doi.org/10.1073/pnas.0707177104
Sanderson H (2002) Pesticide studies: replicability of micro/mesocosms. Environ Sci Pollut Res Int 9(6):429–435. https://doi.org/10.1007/BF02987597
Saxena D, Stotzky G (2001) Bt corn has a higher lignin content than non-bt corn. Am J Bot 88(9):1704–1706. https://doi.org/10.2307/3558416
Schellenberger U, Oral J, Rosen BA, Wei J-Z, Zhu G, Xie W et al(2016) : A selective insecticidal protein from Pseudomonas for controlling corn rootworms. In: Science (New York, N.Y.) 354 (6312), S. 634–637. https://doi.org/10.1126/science.aaf6056
Schnepf E, Crickmore N, van Rie J, Lereclus D, Baum J, Feitelson J et al (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol biology reviews: MMBR 62(3):775–806. https://doi.org/10.1128/MMBR.62.3.775-806.1998
Schulz R, Bub S, Petschick LL, Stehle S, Wolfram J (2021) Applied pesticide toxicity shifts toward plants and invertebrates, even in GM crops. Sci (New York N Y) 372(6537):81–84. https://doi.org/10.1126/science.abe1148
Schulz R, Liess M (1995) Chronic effects of low insecticide concentrations on freshwater caddisfly larvae. Hydrobiologia 299(2):103–113. https://doi.org/10.1007/BF00017562
Schulz R, Peall SK, Dabrowski JM, Reinecke AJ (2001) Spray deposition of two insecticides into surface waters in a south african orchard area. J environ qual 30(3):814–822. https://doi.org/10.2134/jeq2001.303814x
Sharma HC, Sharma KK, Crouch JH (2004) Genetic Transformation of crops for Insect Resistance: potential and Limitations. CRC Crit Rev Plant Sci 23(1):47–72. https://doi.org/10.1080/07352680490273400
Stang C, Elsaesser D, Bundschuh M, Ternes TA, Schulz R (2013) Mitigation of biocide and fungicide concentrations in flow-through vegetated stream mesocosms. J environ qual 42(6):1889–1895. https://doi.org/10.2134/jeq2013.05.0186
Stang C, Wieczorek MV, Noss C, Lorke A, Scherr F, Goerlitz G, Schulz R (2014) Role of submerged vegetation in the retention processes of three plant protection products in flow-through stream mesocosms. Chemosphere 107:13–22. https://doi.org/10.1016/j.chemosphere.2014.02.055
Starner K, Goh KS (2012) Detections of the neonicotinoid insecticide imidacloprid in surface waters of three agricultural regions of California, USA, 2010–2011. Bull Environ Contam Toxicol 88(3):316–321. https://doi.org/10.1007/s00128-011-0515-5
Stehle S, Knäbel A, Schulz R (2013) Probabilistic risk assessment of insecticide concentrations in agricultural surface waters: a critical appraisal. Environ Monit Assess 185(8):6295–6310. https://doi.org/10.1007/s10661-012-3026-x
Strain KE, Lydy MJ (2015) The fate and transport of the Cry1Ab protein in an agricultural field and laboratory aquatic microcosms. Chemosphere 132:94–100. https://doi.org/10.1016/j.chemosphere.2015.03.005
Strain KE, Whiting SA, Lydy MJ (2014) Laboratory and field validation of a Cry1Ab protein quantitation method for water. Talanta 128:109–116. https://doi.org/10.1016/j.talanta.2014.04.036
Swan CM, Jensen PD, Dively GP, Lamp WO (2009) Processing of transgenic crop residues in stream ecosystems. J Appl Ecol 14:711. https://doi.org/10.1111/j.1365-2664.2009.01728.x
Tank JL, Rosi-Marshall EJ, Royer TV, Whiles MR, Griffiths NA, Frauendorf TC, Treering DJ (2010) Occurrence of maize detritus and a transgenic insecticidal protein (Cry1Ab) within the stream network of an agricultural landscape. Proc Natl Acad Sci USA 107(41):17645–17650. https://doi.org/10.1073/pnas.1006925107
van Wijngaarden RPA, Cuppen JGM, Arts GHP, Crum SJH, van den Hoorn, Martin W, van den Brink PJ, Brock TCM (2004) Aquatic risk assessment of a realistic exposure to pesticides used in bulb crops: a microcosm study. Environ Toxicol Chem 23(6):1479–1498. https://doi.org/10.1897/03-80
Venter HJ, Bøhn T (2016) Interactions between Bt crops and aquatic ecosystems: a review. Environ Toxicol Chem 35(12):2891–2902. https://doi.org/10.1002/etc.3583
Wang J, Chen X, Li Y, Zhu H, Ding J, Peng Y (2014) Effect of straw leachates from Cry1Ca-expressing transgenic rice on the growth of Chlorella pyrenoidosa. Environ Toxicol Chem 33(5):1156–1162. https://doi.org/10.1002/etc.2535
Wang Y, Huang J, Hu H, Li J, Liu B, Zhang G (2013) Field and laboratory studies on the impact of two Bt rice lines expressing a fusion protein Cry1Ab/1Ac on aquatic organisms. Ecotoxicol Environ Saf 92:87–93. https://doi.org/10.1016/j.ecoenv.2013.02.018
Wauchope RD (1978) The Pesticide content of Surface Water draining from Agricultural Fields - A Review. J environ qual 7(4):459–472. https://doi.org/10.2134/jeq1978.00472425000700040001x
Wieczorek MV, Bakanov N, Bilancia D, Szöcs E, Stehle S, Bundschuh M, Schulz R (2018) Structural and functional effects of a short-term pyrethroid pulse exposure on invertebrates in outdoor stream mesocosms. Sci Total Environ 610–611. https://doi.org/10.1016/j.scitotenv.2017.08.048
Wieczorek MV, Bakanov N, Lagadic L, Bruns E, Schulz R (2017) Response and recovery of the macrophytes Elodea canadensis and Myriophyllum spicatum following a pulse exposure to the herbicide iofensulfuron-sodium in outdoor stream mesocosms. Environ Toxicol Chem 36(4):1090–1100. https://doi.org/10.1002/etc.3636
Wieczorek MV, Bakanov N, Stang C, Bilancia D, Lagadic L, Bruns E, Schulz R (2016) Reference scenarios for exposure to plant protection products and invertebrate communities in stream mesocosms. Sci Total Environ 545–546. https://doi.org/10.1016/j.scitotenv.2015.12.048
Wieczorek MV, Kötter D, Gergs R, Schulz R (2015) Using stable isotope analysis in stream mesocosms to study potential effects of environmental chemicals on aquatic-terrestrial subsidies. Environ Sci Pollut Res Int 22(17):12892–12901. https://doi.org/10.1007/s11356-015-4071-0
Wolt JD, Keese P, Raybould A, Fitzpatrick JW, Burachik M, Gray A et al (2010) Problem formulation in the environmental risk assessment for genetically modified plants. Transgenic Res 19(3):425–436. https://doi.org/10.1007/s11248-009-9321-9
Zubrod JP, Baudy P, Schulz R, Bundschuh M(2014) : Effects of current-use fungicides and their mixtures on the feeding and survival of the key shredder Gammarus fossarum. In: Aquatic toxicology (Amsterdam, Netherlands) 150, S. 133–143. https://doi.org/10.1016/j.aquatox.2014.03.002
Zubrod JP, Bundschuh M, Arts G, Brühl CA, Imfeld G, Knäbel A et al (2019) Fungicides: an overlooked Pesticide Class? Environ Sci Technol 53(7):3347–3365. https://doi.org/10.1021/acs.est.8b04392
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Pott, A., Bundschuh, M., Otto, M. et al. Assessing Effects of Genetically Modified Plant Material on the Aquatic Environment Using higher-tier Studies. Bull Environ Contam Toxicol 110, 35 (2023). https://doi.org/10.1007/s00128-022-03678-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00128-022-03678-1