Chronic Responses of Daphnia magna Under Dietary Exposure to Leaves of a Transgenic (Event MON810) Bt–Maize Hybrid and its Conventional Near-Isoline

REFERENCES

• Agapito-Tenfen, S. Z., Guerra, M. P., Wikmark, O., and Nodari, R. O. 2013. Comparative proteomic analysis of genetically modified maize grown under different agroecosystems conditions in Brazil. Proteome Sci, 11: 46.
   PubMed Web of Science ®Google Scholar
• Alzate, O., Osorio, C., Florenz, A. M., and Dean, D. H. 2010. Participation of Valine 171 in a α-helix 5 of Bacillus thuringiensis Cry1Ab δ-endotoxin in translocation of toxin into Lymantria dispar midgut mambranes. Appl. Environ. Microbiol. 76: 7878–7880.
   PubMed Web of Science ®Google Scholar
• Axelsson, E. P., Hjältén, J., LeRoy, C. J., Whitham, T. J., Julkunen-Tiitto, R., and Wennström, A. 2011a. Leaf litter from insect-resistant transgenic trees causes changes in aquatic insect community composition. J. Appl. Ecol. 48: 1472–1479.
   Web of Science ®Google Scholar
• Axelsson, E. P., Hjältén, J., and Whitham, T. G. 2011b. Leaf ontogeny interacts with Bt modification to affect innate resistance in GM aspens. Chemoecology 21: 161–169.
   Web of Science ®Google Scholar
• Ban, S., Tenma, H., Mori, T., and Nishimura, K. 2009. Effects of physical interference on life history shifts in Daphnia pulex. J. Exp. Biol. 212: 3174–3183.
   Google Scholar
• Bøhn, T., Primicerio, R., and Traavik, T. 2008. Reduced fitness of Daphnia magna fed a Bt-transgenic maize variety. Arch. Environ. Contam. Toxicol. 55: 584–592.
   PubMed Web of Science ®Google Scholar
• Bøhn, T., Primicerio, R., and Traavik, T. 2012. The German ban on GM maize MON810: Scientifically justified or unjustified? Environ. Sci. Eur. 24: 1–7.
   Google Scholar
• Bøhn, T., Traavik, T., and Primicerio, R. 2010. Demographic responses of Daphnia magna fed transgenic Bt–maize. Ecotoxicology 19: 419–430.
   PubMed Web of Science ®Google Scholar
• Bolker, B. M., Brooks, M. E., Clark, C. J., Geange, S. W., Poulsen, J. R., Stevens, M. H. H., and White, J. S. S. 2009. Generalized linear mixed models: A practical guide for ecology and evolution. Trends Ecol. Evol. 24: 127–135.
   PubMed Web of Science ®Google Scholar
• Bouchnak, R., and Steinberg, C. E. W. 2010. Modulation of longevity in Daphnia magna by food quality and simultaneous exposure to dissolved humic substances. Limnologica 40: 86–91.
   Web of Science ®Google Scholar
• Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of dye binding. Anal. Biochem. 72: 248–254.
   PubMed Web of Science ®Google Scholar
• Bravo, A., Sarjeet, S. G., and Soberón, M. 2007. Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49: 423–435.
   PubMed Web of Science ®Google Scholar
• Center for Environmental Risk Assessment. 2015. GM Crop Database, MON-ØØ81Ø-6 (MON810). Center for Environmental Risk Assessment (CERA), ILSI Research Foundation, Washington, DC. http://cera-gmc.org/GmCropDatabaseEvent/MON810/short
   Google Scholar
• Chambers, C. P., Whiles, M. R., Rosi-Marshall, E. J., Tank, J. L., Royer, T. V., Griffiths, N. A., Evans-White, M. A., and Stojak, A. J. 2010. Responses of stream macroinvertebrates to Bt maize leaf detritus. Ecol. Appl. 20: 1949–1960.
   PubMed Web of Science ®Google Scholar
• Chandini, T. 1989. Survival, growth and reproduction of Daphnia carinata (Crustacea: Cladocera) exposed to chronic cadmium stress at different food (Chlorela) levels. Environ. Pollut. 60: 29–45.
   PubMed Web of Science ®Google Scholar
• Colbourne, J. K., Pfrender, M. E., Gilbert, D., Thomas, W. K., Tucker, A., Oakley, T. H., Tokishita, S., Aerts, A., Arnold, G. J., Basu, M. K., Bauer, D. J., Caceres, C. E., Carmel, L., Casola, C., Choi, J. H., Detter, J. C., Dong, Q. F., Dusheyko, S., Eads, B. D., Frohlich, T., Geiler-Samerotte, K. A., Gerlach, D., Hatcher, P., Jogdeo, S., Krijgsveld, J., Kriventseva, E. V., Kultz, D., Laforsch, C., Lindquist, E., Lopez, J., Manak, J. R., Muller, J., Pangilinan, J., Patwardhan, R. P., Pitluck, S., Pritham, E. J., Rechtsteiner, A., Rho, M., Rogozin, I. B., Sakarya, O., Salamov, A., Schaack, S., Shapiro, H., Shiga, Y., Skalitzky, C., Smith, Z., Souvorov, A., Sung, W., Tang, Z. J., Tsuchiya, D., Tu, H., Vos, H., Wang, M., Wolf, Y. I., Yamagata, H., Yamada, T., Ye, Y. Z., Shaw, J. R., Andrews, J., Crease, T. J., Tang, H. X., Lucas, S. M., Robertson, H. M., Bork, P., Koonin, E. V., Zdobnov, E. M., Grigoriev, I. V., Lynch, M., and Boore, J. L. 2011. The ecoresponsive genome of Daphnia pulex. Science 331: 555–561.
   Google Scholar
• Crickmore, N. 2005. Using worms to better understand how Bacillus thuringiensis kills insects. Trends Microbiol. 13: 347–350.
   Google Scholar
• Dao, T. S., Do-Hong, L., and Wiegand, C. 2010. Chronic effects of cyanobacterial toxins on Daphnia magna and their offspring. Toxicon 55: 1244–1254.
   PubMed Web of Science ®Google Scholar
• Elendt, B. 1990. Selenium deficiency in Crustacea: An ultrastructural approach to antennal damage in Daphnia magna Straus. Protoplasma 154: 25–33.
   Web of Science ®Google Scholar
• Franck-Oberaspach, S. L., and Keller, B. 1997. Consequences of classical and biotechnological resistance breeding for food toxicology and allergenicity. Plant Breed. 116: 1–17.
   Web of Science ®Google Scholar
• Grubber, H., Paul, V., Guertler, P., Spiekers, H., Tichopad, A., Meyer, H. H., and Muller, M. 2011. Fate of Cry1Ab protein in agricultural systems under slurry management of cows fed genetically modified maize (Zea mays L.) MON810: A quantitative assessment. J. Agric. Food Chem. 59: 7135–7144.
   PubMed Web of Science ®Google Scholar
• Gu, J., Krogdahl, Å., Sissener, N. H., Kortner, T. M., Gelencser, E., Hemre, G.-I., and Bakke, A. M. 2013. Effects of oral Bt–maize (MON810) exposure on growth and health parameters in normal and sensitised Atlantic salmon, Salmo salar L. Br. J. Nutr, 109: 1408–1423.
   PubMed Web of Science ®Google Scholar
• Gu, J., Bakke, A. M., Valen, E. C., Lein, I., and Krogdahl, Å. 2014. Bt–maize (MON810) and on-GM soybean meal in diets for Atlantic salmon (Salmo salar L.) juveniles—Impact on survival, growth performance, development, digestive function, and transcriptional expression of intestinal immune and stressr esponses. PLoS ONE 9: e99932.
   PubMed Web of Science ®Google Scholar
• Haider, M. Z., Knowles, B. H., and Ellar, D. J. 1986. Specificity of Bacillus thuringiensis var. colmeri insecticidal δ-endotoxin is determined by differential proteolytic processing of the protoxin by larval gut proteases. Eur. J. Biochem. 156: 531–540.
   PubMedGoogle Scholar
• Hebert, D. N. 1978. The population biology of Daphnia (Crustacea, Daphnidae). Biol. Res. 53: 387–426.
   Web of Science ®Google Scholar
• Heugens, E. H. W., Tokkie, L. T. B., Kraak, M. H. S., Hendriks, A. J. and Van Straalen, N. M. 2006. Population growth of Daphnia magna under multiple stress conditions: Joint effects of temperature, food, and cadmium. Environ. Toxicol. Chem. 25: 1399–1407.
   PubMed Web of Science ®Google Scholar
• Hougaard, P. 2000. Analysis of multivariate survival data. New York, NY: Springer.
   Google Scholar
• James, C. 2014. Executive Summary of Global Status of Commercialized Biotech/GM Crops: 2014. ISAAA Brief 49. ISAAA, Ithaca, NY.
   Google Scholar
• Kuhl, A., and Lorenzen, H. 1964. Handling and culturing of Chlorella. In Methods in cell physiology, ed. D. M. Prescott, 152–187. New York, NY: Academic Press.
   Google Scholar
• La Paz, J. L., Pla, M., Centeno, E., Vicient, C. M., and Puigdomènech, P. 2014. The use of massive sequencing to detect differences between immature embryos of MON810 and a comparable non-GM maize variety. PLoS ONE 9: e100895.
   PubMed Web of Science ®Google Scholar
• Lampert, W. 2006. Daphnia: Model herbivore, predator and prey. Polish J. Ecol. 54: 607–620.
   Web of Science ®Google Scholar
• Latshaw, W. L. 1924. Elemental composition of the corn plant. J. Agric. Res. 27: 845–860.
   Google Scholar
• Lemaux, P. G. 2008. Genetically engineered plants and foods: A scientist’s analysis of the issues (Part I). Annu. Rev. Plant Biol. 59: 771–812.
   PubMed Web of Science ®Google Scholar
• Marvier, M., McCreedy, C., Regetz, J., and Kareiva, P. 2007. A meta-analysis of effects of Bt cotton and maize on nontarget invertebrates. Science 316: 1475–1477.
   PubMed Web of Science ®Google Scholar
• Müller-Navarra, D. C. 1995. Biochemical versus mineral limitation in Daphnia. Limnol. Oceanogr. 40: 1209–1214.
   Web of Science ®Google Scholar
• Naranjo, S. E. 2009. Impacts of Bt crops on non-target organisms and insecticide use patterns. Perspect. Agric. Vet. Sci, Nutr. Nat. Resources 4: 1–23.
   Google Scholar
• Nguyen, H. T., and Jehle, J. A. 2007. Quantitative analysis of the seasonal and tissue-specific expression of Cry1Ab in transgenic maize MON810. J. Plant Dis. Protect. 114: 82–87.
   Web of Science ®Google Scholar
• Organization for Economic Cooperation and Development. 2008. OECD guideline for testing of chemicals 211: Daphnia magna reproduction test. Paris, France: OECD.
   Google Scholar
• Paul, V., Guertler, P., Wiedemann, S., and Meyer, H. H. D. 2010. Degradation of Cry1Ab protein from genetically modified maize (MON810) in relation to total dietary feed proteins in dairy cow digestion. Transgenic Res. 19: 683–689.
   PubMed Web of Science ®Google Scholar
• Rasband, W. S. 1997 –2008. Image J. U. S. National Institutes of Health, Bethesda, MD. http://rsb.info.nih.gov/ij (accessed December 18, 2012).
   Google Scholar
• Raybould, A., Kilby, P., and Graser, G. 2013. Characterizing microbial protein test substances and establishing their equivalence with plant-produced proteins for use in risk assessments of transgenic crops. Transgenic Res. 22: 445–460.
   PubMed Web of Science ®Google Scholar
• Ricroch, A., Bergé, J. B., and Kuntz, M. 2010. Is the German suspension of MON810 maize cultivation scientifically justified? Transgenic Res. 19: 1–12.
   Web of Science ®Google Scholar
• Rosati, A., Bogani, P., Santarlasci, A., and Buiatti, M. 2008. Characterization of 3′ transgene insertion site and derived mRNAs in MON810 Yieldgard maize. Plant Mol. Biol. 67: 271–281.
   PubMed Web of Science ®Google Scholar
• Romeis, J., Mclean, M. A., and Shelton, A. M. 2013. When bad science makes good headlines: Bt maize and regulatory bans. Nat. Biotechnol. 31: 386–387.
   PubMed Web of Science ®Google Scholar
• Rosi-Marshall, E. J., Tank, J. L., Royer, T. V., Whiles, M. R., Evans-White, M., Chambers, C., Griffiths, N. A., Pokelsek, J., and Stephen, M. L. 2007. Toxins in transgenic crop byproducts may affect headwater stream ecosystems. Proc. Natl. Acad. Sci. USA 104: 16204–16208.
   PubMed Web of Science ®Google Scholar
• Schwarz, G. 1978. Estimating the dimension of a model. Ann. Stat. 6: 461–464.
   Web of Science ®Google Scholar
• Stige, L. C., Hessen, D. O., and Vøllestad, L. A. 2004. Severe food stress has no detectable impact on developmental instability in Daphnia magna. OIKOS 107: 519–530.
   Web of Science ®Google Scholar
• Székács, A., Lauber, É., Juracsek, J., and Darvas, B. 2010a. Cry1Ab toxin production of MON810 transgenic maize. Environ. Toxicol. Chem. 29: 182–190.
   PubMed Web of Science ®Google Scholar
• Székács, A., Lauber, É., Takács, E., and Darvas, B. 2010b. Detection of Cry1Ab toxin in the leaves of MON810 transgenic maize. Anal. Bioanal. Chem. 396: 2203–2211.
   PubMed Web of Science ®Google Scholar
• Tank, J. L., Rosi-Marshall, E. J., Royer, T. V., Whiles, M. R., Griffiths, N. A., Frauendorf, T. C., and Treering, D. J. 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: 17645–17650.
   PubMed Web of Science ®Google Scholar
• Taverniers, I., Papazova, N., Bertheau, Y., De Loose, M., and Holst-Jensen, A. 2008. Gene stacking in transgenic plants: Towards compliance between definitions, terminology, and detection within the EU regulatory framework. Environ. Biosafety Res. 7:197–218.
   PubMedGoogle Scholar
• Then, C. 2010. Risk assessment of toxins derived from Bacillus thuringiensis—Synergism, efficacy, and selectivity. Environ. Sci. Pollut. Res. 17: 791–797.
   PubMed Web of Science ®Google Scholar
• U.S. Environmental Protection Agency. 2010. Cry1Ab and Cry1F Bacillus thuringiensis (Bt) Corn Plant-Incorporated Protectants. BRAD. U.S. EPA Office of Pesticide Programs, Biopesticides and Pollution Prevention Division. http://www.epa.gov/oppbppd1/biopesticides/pips/cry1f-cry1ab-brad.pdf
   Google Scholar
• Villarroel, M. J., Sancho, E., Ferrando, M. D., and Andreu, E. 2003. Acute, chronic and sublethal effects of the herbicide propanil on Daphnia magna. Chemosphere 53: 857–864.
   PubMed Web of Science ®Google Scholar
• Vollmer, C. 1960. Wasserflöhe, 3rd ed. Lutherstadt Wittenberg, Germany: Ziemsen Verlag.
   Google Scholar
• Waltz, E. 2009. GM crops: Battlefield. Nature 461: 27–32.
   PubMed Web of Science ®Google Scholar
• Ward, E. S., Ellar, D. J., and Chilcott, C. N. 1988. Single amino acid changes in the Bacillus thuringiensis var. israelensis δ-endotoxin affect the toxicity and expression of the protein. J. Mol. Biol. 202: 527–535.
   PubMed Web of Science ®Google Scholar
• Wickson, F., Bøhn, T., Wynne, B., Hilbeck, A., and Funtowicz, S. 2013. Science-based risk assessment requires careful evaluation of all studies. Nat. Biotechnol. 31: 1077–1078.
   PubMed Web of Science ®Google Scholar
• Zeven, A. C., and Waninge, J. 1986. The degree of phenotypic resemblance of the near-isogenic lines of the wheat cultivar Thatcher with their recurrent parent. Euphytica 35: 665–676.
   Web of Science ®Google Scholar
• Zolla, L., Rinalducci, S., Antonioli, P., and Righetti, P. G. 2008. Proteomics as a complementary tool for identifying unintended side effects occurring in transgenic maize seeds as a result of genetic modifications. J. Proteome Res. 7: 1850–1861.
   PubMed Web of Science ®Google Scholar