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

Journal of Toxicology and Environmental Health - Part A: Current Issues

Volumn 78, Issue 15, 2015, Pages 993-1007

  Holderbaum, Daniel Ferreira ^a,b   Cuhra, Marek ^b,c   Wickson, Fern ^b   Orth, Afonso Inácio ^a   Nodari, Rubens Onofre ^a   Bøhn, Thomas ^b,c  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b Gen k Centre for Biosafety   (Norway)

^c UNIVERSITY OF TROMSØ   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CRY1AB TOXIN; BACTERIAL PROTEIN; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS; INSECTICIDE;

ARTICLE; BACILLUS THURINGIENSIS; BIOASSAY; BODY SIZE; CHRONIC TOXICITY; CONTROLLED STUDY; DAPHNIA MAGNA; DIETARY INTAKE; DRY MASS; EXPOSURE; FERTILITY; INSECT RESISTANCE; LONG TERM EXPOSURE; MAIZE; NONHUMAN; NONTARGET ORGANISM; NUTRIENT SUPPLY; NUTRITIONAL VALUE; PHOTOPERIODICITY; PLANT LEAF; PRIORITY JOURNAL; PROGENY; ADVERSE EFFECTS; ANIMAL; CHEMISTRY; DAPHNIA; DIET; DRUG EFFECTS; GENETICS; PHYSIOLOGY; TOXICITY; TRANSGENIC PLANT;

BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS); CLADOCERA; DAPHNIA; DAPHNIA MAGNA; HEXAPODA; ZEA MAYS;

ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; DAPHNIA; DIET; ENDOTOXINS; HEMOLYSIN PROTEINS; INSECTICIDES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; ZEA MAYS;

EID: 84939526200     PISSN: 15287394     EISSN: 10872620     Source Type: Journal    
DOI: 10.1080/15287394.2015.1037877     Document Type: Article

References (60)

1. 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.
2. 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.
3. 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.
4. 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.
5. 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.
6. 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.
7. 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.
8. Bøhn, T., Traavik, T., and Primicerio, R. 2010. Demographic responses of Daphnia magna fed transgenic Bt-maize. Ecotoxicology 19: 419-430.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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
14. 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.
15. 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.
16. 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.
17. Crickmore, N. 2005. Using worms to better understand how Bacillus thuringiensis kills insects. Trends Microbiol. 13: 347-350.
18. 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.
19. Elendt, B. 1990. Selenium deficiency in Crustacea: An ultrastructural approach to antennal damage in Daphnia magna Straus. Protoplasma 154: 25-33.
20. 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.
21. 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.
22. 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.
23. 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.
24. 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.
25. Hebert, D. N. 1978. The population biology of Daphnia (Crustacea, Daphnidae). Biol. Res. 53: 387-426.
26. 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.
27. Hougaard, P. 2000. Analysis of multivariate survival data. New York, NY: Springer.
28. James, C. 2014. Executive Summary of Global Status of Commercialized Biotech/GM Crops: 2014. ISAAA Brief 49. ISAAA, Ithaca, NY.
29. 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.
30. 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.
31. Lampert, W. 2006. Daphnia: Model herbivore, predator and prey. Polish J. Ecol. 54: 607-620.
32. Latshaw, W. L. 1924. Elemental composition of the corn plant. J. Agric. Res. 27: 845-860.
33. Lemaux, P. G. 2008. Genetically engineered plants and foods: A scientists analysis of the issues (Part I). Annu. Rev. Plant Biol. 59: 771-812.
34. 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.
35. Müller-Navarra, D. C. 1995. Biochemical versus mineral limitation in Daphnia. Limnol. Oceanogr. 40: 1209-1214.
36. 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.
37. 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.
38. Organization for Economic Cooperation and Development. 2008. OECD guideline for testing of chemicals 211: Daphnia magna reproduction test. Paris, France: OECD.
39. 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.
40. 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).
41. 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.
42. Ricroch, A., Bergé, J. B., and Kuntz, M. 2010. Is the German suspension of MON810 maize cultivation scientifically justified? Transgenic Res. 19: 1-12.
43. 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.
44. 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.
45. 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.
46. Schwarz, G. 1978. Estimating the dimension of a model. Ann. Stat. 6: 461-464.
47. 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.
48. Székács, A., Lauber, É., Juracsek, J., and Darvas, B. 2010a. Cry1Ab toxin production of MON810 transgenic maize. Environ. Toxicol. Chem. 29: 182-190.
49. 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.
50. 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.
51. 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.
52. Then, C. 2010. Risk assessment of toxins derived from Bacillus thuringiensis-Synergism, efficacy, and selectivity. Environ. Sci. Pollut. Res. 17: 791-797.
53. 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
54. 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.
55. Vollmer, C. 1960. Wasserflöhe, 3rd ed. Lutherstadt Wittenberg, Germany: Ziemsen Verlag.
56. Waltz, E. 2009. GM crops: Battlefield. Nature 461: 27-32.
57. 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.
58. 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.
59. 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.
60. 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.