Reduced Fitness of Daphnia magna Fed a Bt-Transgenic Maize Variety

  • Thomas Bøhn
  • Raul Primicerio
  • Dag O. Hessen
  • Terje Traavik
Article

Abstract

Genetically modified (GM) maize expressing the Bt-toxin Cry1Ab (Bt-maize) was tested for effects on survival, growth, and reproduction of the water flea Daphnia magna, a crustacean arthropod commonly used as a model organism in ecotoxicological studies. In three repeated experiments, D. magna were fed 100% ground maize in suspension, using either GM or isogenic unmodified (UM) maize. D. magna fed GM-maize showed a significantly reduced fitness performance: The mortality was higher, a lower proportion of females reached sexual maturation, and the overall egg production was lower compared to D. magna fed UM isogenic maize. We conclude that the tested variety of Bt-maize and its UM counterpart do not have the same quality as food sources for this widely used model organism. The combination of a reduced fitness performance combined with earlier onset of reproduction of D. magna fed Bt-maize indicates a toxic effect rather than a lower nutritional value of the GM-maize.

References

  1. Aeschbacher K, Messikommer R, Meile L, Wenk C (2005) Bt176 corn in poultry nutrition: physiological characteristics and fate of recombinant plant DNA in chickens. Poult Sci 84(3):385–394Google Scholar
  2. Andow D, Hilbeck A (2004) Science-based risk assessment for nontarget effects of transgenic crops. Bioscience 54(7):637–649CrossRefGoogle Scholar
  3. Atienzar FA, Cheung VV, Vadesh NJ, Epledge MH (2001) Fitness parameters and DNA effects are sensitive indicators of copper-induced toxicity in Daphnia magna. Toxicol Sci 59:241–250CrossRefGoogle Scholar
  4. Barry MJ (1996) Effects of an organochlorine pesticide on different levels of organization in Daphnia. Ecotoxicology and environmental safety. Environ Safety 34:239–251CrossRefGoogle Scholar
  5. Brake J, Vlachos D (1998) Evaluation of transgenic event 176 “Bt” corn in broiler chickens. Poult Sci 77(5):648-653Google Scholar
  6. Brandt SL, Coudron TA, Habibi J et al (2004) Interaction of two Bacillus thuringiensis delta-endotoxins with the digestive system of lygus hesperus. Curr Microbiol 48(1):1–9CrossRefGoogle Scholar
  7. Bravo A, Gill SS, Soberon M (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49:423–435CrossRefGoogle Scholar
  8. Brett MT (1993) Resource quality effects on Daphnia-Longispina offspring fitness. J Plankton Res 15(4):403–412CrossRefGoogle Scholar
  9. Campbell AK, Wann KT, Matthews SB (2004) Lactose causes heart arrhythmia in the water flea Daphnia pulex. Comp Biochem Physiol B: Biochem Mol Biol 139(2):225–234CrossRefGoogle Scholar
  10. Clark BW, Prihoda KR, Coats JR (2006) Subacute effects of transgenic Cry1Ab Bacillus thuringiensis corn litter on the isopods Trachelipus rathkii and Armadillidium nasatum. Environ Toxicol Chem 25(10):2653–2661CrossRefGoogle Scholar
  11. Clark JH, Ipharraguerre IR (2001) Biotech crops as feeds for livestock. Abstr Papers Am Chem Soc 222:U67Google Scholar
  12. Crickmore N (2005) Using worms to better understand how Bacillus thuringiensis kills insects. Trends Microbioly 13(8):347–350CrossRefGoogle Scholar
  13. Domingo JL (2007) Toxicity studies of genetically modified plants: a review of the published literature. Crit Rev Food Sci Nutr 47:721–733CrossRefGoogle Scholar
  14. Douville M, Gagne F, Blaise C, Andre C (2007) Occurence and persistence of Bacillus thuringiensis (Bt) and transgenic Bt corn cry1Ab gene from an aquatic environment. Ecotoxicol Environ Safety 66:195–203CrossRefGoogle Scholar
  15. Dutton A, Romeis J, Bigler F (2003) Assessing the risks of insect resistant transgenic plants on entomophagous arthropods: Bt-maize expressing Cry1Ab as a case study. Biocontrol 48(6):611–636CrossRefGoogle Scholar
  16. Dutton A, Romeis J, Bigler F (2005) Effects of Bt maize expressing Cry1Ab and Bt spray on Spodoptera littoralis. Entomol Exp Applic 114(3):161–169CrossRefGoogle Scholar
  17. Enserink EL, Kerkhofs MJJ, Baltus CAM, Koeman JH (1995) Influence of food quantity and lead-exposure on maturation in Daphnia-Magna: evidence for a trade-off mechanism. Funct Ecol 9(2):175–185CrossRefGoogle Scholar
  18. Ewen SWB, Pusztai A (1999) Effect of diets containing genetically modified potatoes expressing Galanthus nivalis lectin on rat small intestine. Lancet 354(9187):1353–1354CrossRefGoogle Scholar
  19. Groot AT, Dicke M (2002) Insect-resistant transgenic plants in a multi-trophic context. Plant J 31(4):387–406CrossRefGoogle Scholar
  20. Hammond BG, Dudek R, Lemen JK, Nemeth MA (2006) Results of a 90-day safety assurance study with rats fed grain from corn borer-protected corn. Food Chem Toxicol 44(7):1092–1099CrossRefGoogle Scholar
  21. Hansen FT, Forbes VE, Forbes TL (1999) Effects of 4-n-nonylphenol on life-history traits and population dynamics of a polychaete. Ecol Appl 9(2):482–495CrossRefGoogle Scholar
  22. Hilbeck A (2001) Implications of transgenic, insecticidal plants for insect and plant biodiversity. Perspect Plant Ecol Evol Syst 4(1):43–61CrossRefGoogle Scholar
  23. Hilbeck A, Schmidt JEU (2006) Another view on Bt proteins: how specific are they and what else might they do? Biopestic Int 2(1):1–50Google Scholar
  24. Hill R, Sendashonga C (2006) Conservation biology, genetically modified organisms and the biosafety protocol. Conserv Biol 20(6):1620–1625CrossRefGoogle Scholar
  25. James C (2006) Global status of commercialized biotech/GM crops. ISAAA Brief No. 35. 2006. ISAAA, Ithaca, NYGoogle Scholar
  26. Kluttgen B, Dulmer U, Engels M, Ratte HT (1994) Adam, an artificial fresh-water for the culture of zooplankton. Water Res 28(3):743–746CrossRefGoogle Scholar
  27. Knudsen I, Poulsen M (2007) Comparative safety testing of genetically modified foods in a 90-day rat feeding study design allowing the distinction between primary and secondary effects of the new genetic event. Regul Toxicol Pharmacol 49(1):53–62CrossRefGoogle Scholar
  28. Kowalchuk GA, Bruinsma M, van Veen JA (2003) Assessing responses of soil microorganisms to GM plants. Trends Ecol Evol 18(8):403–410CrossRefGoogle Scholar
  29. Kramer KJM, Jak RG, van Hattum B, Hooftman RN, Zwolsman JJG (2004) Copper toxicity in relation to surface water-dissolved organic matter: biological effects to Daphnia magna. Environ Toxicol Chemistry 23(12):2971–2980CrossRefGoogle Scholar
  30. Lövei GL, Arpaia S (2005) The impact of transgenic plants on natural enemies: a critical review of laboratory studies. Entomol Exp Applic 114:1–14CrossRefGoogle Scholar
  31. Mauri M, Baraldi E, Simonini R (2003) Effects of zinc exposure on the polychaete Dinophilus gyrociliatus: a life-table response experiment. Aquat Toxicol 65(1):93–100CrossRefGoogle Scholar
  32. Mendelson M, Kough J, Vaituzis Z, Matthews K (2003) Are Bt crops safe? Nature Biotechnol 21(9):1003–1009CrossRefGoogle Scholar
  33. Nogueira ICG, Saker ML, Pflugmacher S, Wiegand C, Vasconcelos VM (2004) Toxicity of the cyanobacterium Cylindrospermopsis raciborskii to Daphnia magna. Environ Toxicol 19:453–459CrossRefGoogle Scholar
  34. O’Callaghan M, Glare TR, Burgess EPJ, Malone LA (2005) Effects of plants genetically modified for insect resistance on nontarget organisms. Annu Rev Entomol 50:271–292CrossRefGoogle Scholar
  35. Palm CJ, Schaller DL, Donegan KK, Seidler RJ (1996) Persistence in soil of transgenic plant produced Bacillus thuringiensis var kurstaki delta-endotoxin. Can J Microbiol 42(12):1258–1262CrossRefGoogle Scholar
  36. Pusztai A (2002) Can science give us the tools for recognizing possible health risks of GM food? Nutr Health 16:73–84Google Scholar
  37. Reuter T, Aulrich K, Berk A, Flachowsky G (2002) Investigations on genetically modified maize (Bt-maize) in pig nutrition: chemical composition and nutritional evaluation. Arch Anim Nutr 56(1):23–31CrossRefGoogle Scholar
  38. Roff DA (2002) Life history evolution. Sinauer Associates, Sunderland, MAGoogle Scholar
  39. Rosi-Marshall EJ, Tank JL, Royer TV et al (2007) Toxins in transgenic crop byproducts may affect headwater stream ecosystems. Proc Natl Acad Sci USA 104(41):16,204–16,208Google Scholar
  40. Sidhu RS, Hammond BG, Fuchs RL et al (2000) Glyphosate-tolerant corn: the composition and feeding value of grain from glyphosate-tolerant corn is equivalent to that of conventional corn (Zea mays L.). J Agric Food Chem 48(6):2305–2312CrossRefGoogle Scholar
  41. Sims IR, Watson S, Holmes D (1993) Toward a standard Daphnia juvenile production test. Environ Toxicol Chem 12(11):2053–2058CrossRefGoogle Scholar
  42. Stark JD, Banks JE (2003) Population-level effects of pesticides and other toxicants on arthropods. Annu Rev Entomol 48:505–519CrossRefGoogle Scholar
  43. Stearns SC, Koella JC (1986) The evolution of phenotypic plasticity in life-history traits: predictions of reaction norms for age and size at maturity. Evolution 40(5):893–913CrossRefGoogle Scholar
  44. Tapp H, Stotzky G (1995) Insecticidal activity of the toxins from Bacillus-Thuringiensis subspecies kurstaki and tenebrionis adsorbed and bound on pure and soil clays. Appl Environl Microbiol 61(5):1786–1790Google Scholar
  45. Teshima R, Watanabe T, Okunuki H et al (2002) Effect of subchronic feeding of genetically modified corn (CBH351) on immune system in BN rats and B10A mice. J Food Hyg Soc Japan 43(5):273–279CrossRefGoogle Scholar
  46. Twombly S, Clancy N, Burns CW (1998) Life history consequences of food quality in the freshwater copepod Boeckella triarticulata. Ecology 79(5):1711–1724Google Scholar
  47. Vanni MJ, Lampert W (1992) Food quality effects on life-history traits and fitness in the generalist herbivore Daphnia. Oecologia 92(1):48–57CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Thomas Bøhn
    • 1
  • Raul Primicerio
    • 2
  • Dag O. Hessen
    • 3
  • Terje Traavik
    • 1
    • 4
  1. 1.Genøk—Centre for BiosafetyTromsoNorway
  2. 2.Norwegian College of Fishery ScienceUniversity of TromsøTromsoNorway
  3. 3.Department of BiologyUniversity of OsloOsloNorway
  4. 4.Department of Microbiology and VirologySchool of Medicine, University of TromsøTromsoNorway

Personalised recommendations