Impact of GM crops on biodiversity

The potential impact of GM crops on biodiversity has been a topic of interest both in general as well as specifically in the context of the Convention on Biological Diversity. Agricultural biodiversity has been defined at levels from genes to ecosystems that are involved or impacted by agricultural production (www.cbd.int/agro/whatis.shtml). After fifteen years of commercial cultivation, a substantial body of literature now exists addressing the potential impacts of GM crops on the environment. This review takes a biodiversity lens to this literature, considering the impacts at three levels: the crop, farm and landscape scales. Within that framework, this review covers potential impacts of the introduction of genetically engineered crops on: crop diversity, biodiversity of wild relatives, non-target soil organisms, weeds, land use, non-target above-ground organisms, and area-wide pest suppression.

[1]  Stuart E. Marsh,et al.  Farm-scale evaluation of the impacts of transgenic cotton on biodiversity, pesticide use, and yield , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Arata Katayama,et al.  Altered pesticide use on transgenic crops and the associated general impact from an environmental perspective. , 2007, Pest management science.

[3]  M. May.  Economic consequences for UK farmers of growing GM herbicide tolerant sugar beet , 2003 .

[4]  David A. Bohan,et al.  Invertebrate responses to the management of genetically modified herbicide-tolerant and conventional spring crops. II. Within-field epigeal and aerial arthropods. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[5]  X. Pons,et al.  Responsiveness of Arthropod Herbivores and Their Natural Enemies to Modified Weed Management in Corn , 2009, Environmental entomology.

[6]  Peter Kareiva,et al.  A Meta-Analysis of Effects of Bt Cotton and Maize on Nontarget Invertebrates , 2007, Science.

[7]  G. Stotzky,et al.  Fate and effects of insect-resistant Bt crops in soil ecosystems , 2008 .

[8]  A. Lewandowski,et al.  Effect of Transgenic Maize Mon 810 on Selected Non-Target Organisms: The Bird Cherry-Oat Aphid (Rhopalosiphum padi L.) and its Predator - Green Lacewing (Chrysoperla carnea Steph.) , 2008 .

[9]  F. Wan,et al.  Response of multiple generations of beet armyworm, Spodoptera exigua (Hübner), feeding on transgenic Bt cotton , 2009 .

[10]  R. Uaiene,et al.  The Economic Impacts of Introducing Bt Technology in Smallholder Cotton Production Systems of West Africa: A Case Study from Mali , 2007 .

[11]  B. Mullinix,et al.  Influence of herbicide tolerant soybean production systems on insect pest populations and pest-induced crop damage. , 2003, Journal of economic entomology.

[12]  David B Lobell,et al.  Greenhouse gas mitigation by agricultural intensification , 2010, Proceedings of the National Academy of Sciences.

[13]  F. Bigler,et al.  Biological Activity of Cry1Ab Toxin Expressed by Bt Maize Following Ingestion by Herbivorous Arthropods and Exposure of the Predator Chrysoperla carnea , 2006, BioControl.

[14]  E. Trigo,et al.  Ten years of genetically modified crops in Argentine agriculture , 2006 .

[15]  Division on Earth,et al.  The Impact of Genetically Engineered Crops on Farm Sustainability in the United States , 2010 .

[16]  H. Sharma,et al.  Effects of Bacillus thuringiensis δ-endotoxins Cry1Ab and Cry1Ac on the coccinellid beetle, Cheilomenes sexmaculatus (Coleoptera, Coccinellidae) under direct and indirect exposure conditions , 2009 .

[17]  G. Tylka,et al.  Effects of Weed Management Systems on Canopy Insects in Herbicide-Resistant Soybeans , 2000, Journal of economic entomology.

[18]  Kongming Wu,et al.  Suppression of Cotton Bollworm in Multiple Crops in China in Areas with Bt Toxin–Containing Cotton , 2008, Science.

[19]  Matin Qaim,et al.  Bt cotton and pesticide use in Argentina: economic and environmental effects , 2005, Environment and Development Economics.

[20]  David S. Bullock,et al.  Simulating a relative environmental effect of glyphosate-resistant soybeans , 2003 .

[21]  Philip J. Dale,et al.  Potential for the environmental impact of transgenic crops , 2002, Nature Biotechnology.

[22]  David Zilberman,et al.  The Role of Biotechnology in a Sustainable Biofuel Future , 2009 .

[23]  S. Bonny,et al.  Genetically modified glyphosate-tolerant soybean in the USA: adoption factors, impacts and prospects. A review , 2011, Agronomy for Sustainable Development.

[24]  Richard Bennett,et al.  The use of life-cycle assessment to evaluate the environmental impacts of growing genetically modified, nitrogen use-efficient canola. , 2008, Plant biotechnology journal.

[25]  L. Hothorn,et al.  Effects of Cultivation of Genetically Modified Bt Maize on Epigeic Arthropods (Araneae; Carabidae) , 2007, Environmental entomology.

[26]  J. Carpenter,et al.  Peer-reviewed surveys indicate positive impact of commercialized GM crops , 2010, Nature Biotechnology.

[27]  M. Smulders,et al.  GM-related sustainability: agro-ecological impacts, risk and opportunities of soy production in Argentina and Brazil , 2009 .

[28]  O. L. May,et al.  Genetic Uniformity of the U.S. Upland Cotton Crop since the Introduction of Transgenic Cottons , 2003, Crop Science.

[29]  J. Coats,et al.  Aquatic fate and effects of Bacillus thuringiensis Cry3Bb1 protein: Toward risk assessment , 2008, Environmental toxicology and chemistry.

[30]  J. Adamczyk,et al.  ARTHROPOD MANAGEMENT Changes in Populations of Heliothis virescens (F.) (Lepidoptera: Noctuidae) and Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) in the Mississippi Delta from 1986 to 2005 as Indicated by Adult Male Pheromone Traps , 2006 .

[31]  Greg Traxler,et al.  Roundup Ready soybeans in Argentina: farm level and aggregate welfare effects , 2004 .

[32]  Z. Huang,et al.  Field and Semifield Evaluation of Impacts of Transgenic Canola Pollen on Survival and Development of Worker Honey Bees , 2004, Journal of economic entomology.

[33]  Steven E. Naranjo,et al.  Impacts of Bt crops on non-target invertebrates and insecticide use patterns , 2009 .

[34]  Fiona Thorne,et al.  An Economic Cost-Benefit Analysis of GM Crop Cultivation: An Irish Case Study , 2004 .

[35]  Mark J. VanGessel,et al.  Glyphosate-resistant horseweed from Delaware , 2001, Weed Science.

[36]  J. Babcock,et al.  Three-Year Field Monitoring of Cry1F, Event DAS-Ø15Ø7-1, Maize Hybrids for Nontarget Arthropod Effects , 2009, Environmental entomology.

[37]  R. Herman,et al.  Landscape Effects of Insect-Resistant Genetically Modified Crops , 2008 .

[38]  D. Andow,et al.  Transgenic Insecticidal Crops and Natural Enemies: A Detailed Review of Laboratory Studies , 2009, Environmental entomology.

[39]  Wayne Parrott,et al.  Study of Bt impact on caddisflies overstates its conclusions: Response to Rosi-Marshall et al. , 2008, Proceedings of the National Academy of Sciences.

[40]  R. P. Freckleton,et al.  Deciding the Future of GM Crops in Europe , 2003, Science.

[41]  J. Cortet,et al.  Effects of Bt-maize material on the life cycle of the land snail Cantareus aspersus , 2009 .

[42]  Jikun Huang,et al.  Insect-Resistant GM Rice in Farmers' Fields: Assessing Productivity and Health Effects in China , 2005, Science.

[43]  S. Eber,et al.  Impact of Bt-corn MON88017 in comparison to three conventional lines on Trigonotylus caelestialium (Kirkaldy) (Heteroptera: Miridae) field densities , 2009, Transgenic Research.

[44]  D. Neher,et al.  Impact of coleopteran targeting toxin (Cry3Bb1) of Bt corn on microbially mediated decomposition , 2009 .

[45]  M. Brownbridge,et al.  Field trials to evaluate effects of Bt-transgenic silage corn expressing the Cry1Ab insecticidal toxin on non-target soil arthropods in northern New England, USA , 2009, Transgenic Research.

[46]  Aziz Elbehri,et al.  Estimating the Impact of Transgenic Bt Cotton on West and Central Africa: A General Equilibrium Approach , 2004 .

[47]  Graham Brookes,et al.  Global Impact of Biotech Crops: Socio-Economic & Environmental Effects 1996–2007 , 2009 .

[48]  Yanhui Lu,et al.  Mirid Bug Outbreaks in Multiple Crops Correlated with Wide-Scale Adoption of Bt Cotton in China , 2010, Science.

[49]  P. Rieder,et al.  Biodiversity, Biotechnology, and Institutions Among Crops:: Situation and Outlook , 1995 .

[50]  F. Wäckers,et al.  Indian Bt Cotton Varieties Do Not Affect the Performance of Cotton Aphids , 2009, PloS one.

[51]  K. Ammann.  Effects of biotechnology on biodiversity: herbicide-tolerant and insect-resistant GM crops. , 2005, Trends in biotechnology.

[52]  E. Natwick,et al.  Pink bollworm moth (Lepidoptera: Gelechiidae) catches in the Imperial Valley, California from 1989 to 2003 , 2006 .

[53]  D. Andow,et al.  Earthworm populations in a northern U.S. Cornbelt soil are not affected by long-term cultivation of Bt maize expressing Cry1Ab and Cry3Bb1 proteins , 2010 .

[54]  Steven E. Naranjo,et al.  Bt Crop Effects on Functional Guilds of Non-Target Arthropods: A Meta-Analysis , 2008, PloS one.

[55]  Stefan Rauschen.  A case of “pseudo science”? A study claiming effects of the Cry1Ab protein on larvae of the two-spotted ladybird is reminiscent of the case of the green lacewing , 2009, Transgenic Research.

[56]  Greg A. Constable,et al.  Environmental impact of conventional and Bt insecticidal cotton expressing one and two Cry genes in Australia , 2006 .

[57]  J. Romeis,et al.  Bt maize expressing Cry3Bb1 does not harm the spider mite, Tetranychus urticae, or its ladybird beetle predator, Stethorus punctillum , 2010 .

[58]  Jan-Peter Nap,et al.  The release of genetically modified crops into the environment. Part I. Overview of current status and regulations. , 2003, The Plant journal : for cell and molecular biology.

[59]  J. Romeis,et al.  Assessing the utilization of a carbohydrate food source and the impact of insecticidal proteins on larvae of the green lacewing, Chrysoperla carnea , 2008 .

[60]  James A. Larson,et al.  Simultaneous Adoption of Herbicide-Resistant and Conservation-Tillage Cotton Technologies , 2006, Journal of Agricultural and Applied Economics.

[61]  E. Trigo,et al.  The case of zero-tillage technology in Argentina. , 2009 .

[62]  G. A. Carlson,et al.  The net benefits, including convenience, of Roundup Ready® soybeans: results from a national survey. , 2004 .

[63]  Chen Hao,et al.  The Impact of Genetically Engineered Crops on Farm Sustainability in the United States , 2010 .

[64]  D. Quist,et al.  Transgenic DNA introgressed into traditional maize landraces in Oaxaca, Mexico , 2001, Nature.

[65]  D. Reheul,et al.  Environmental impact of herbicide regimes used with genetically modified herbicide-resistant maize , 2008, Transgenic Research.

[66]  Vijay K. Nandula,et al.  Glyphosate resistance in crops and weeds: history, development, and management. , 2010 .

[67]  N. Ferry,et al.  Environmental Impact of Genetically Modified Crops , 2009 .

[68]  Cathy Hawes,et al.  Effects on weed and invertebrate abundance and diversity of herbicide management in genetically modified herbicide-tolerant winter-sown oilseed rape , 2005, Proceedings of the Royal Society B: Biological Sciences.

[69]  C. Sneller.  Impact of Transgenic Genotypes and Subdivision on Diversity within Elite North American Soybean Germplasm , 2003 .

[70]  B. Tabashnik,et al.  Effects of transgenic Bt cotton on insecticide use and abundance of two generalist predators , 2007 .

[71]  W. Sutherland,et al.  Reaping the Benefits: Science and the sustainable intensification of global agriculture , 2009 .

[72]  Richard L. Hellmich,et al.  Impact of Bt corn pollen on monarch butterfly populations: A risk assessment , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[73]  N. Fedoroff,et al.  The burden of proof: A response to Rosi-Marshall et al. , 2008, Proceedings of the National Academy of Sciences.

[74]  J. Schiemann,et al.  A mathematical model of exposure of non-target Lepidoptera to Bt-maize pollen expressing Cry1Ab within Europe , 2010, Proceedings of the Royal Society B: Biological Sciences.

[75]  Kun Xue,et al.  Assessing effects of transgenic Cry1Ac cotton on the earthworm Eisenia fetida. , 2009 .

[76]  George B. Frisvold,et al.  Simultaneous Diffusion of Herbicide Resistant Cotton and Conservation Tillage , 2009 .

[77]  F. Ortego,et al.  Prey mediated effects of Bt maize on fitness and digestive physiology of the red spider mite predator Stethorus punctillum Weise (Coleoptera: Coccinellidae) , 2008, Transgenic Research.

[78]  A. Shelton,et al.  Setting the record straight: a rebuttal to an erroneous analysis on transgenic insecticidal crops and natural enemies , 2009, Transgenic Research.

[79]  Jörg Romeis,et al.  Transgenic crops expressing Bacillus thuringiensis toxins and biological control , 2006, Nature Biotechnology.

[80]  Leonard P. Gianessi,et al.  Herbicide tolerant soybeans: why growers are adopting Roundup Ready varieties , 1999 .

[81]  J. Kiss,et al.  Rove beetle (Coleoptera: Staphylinidae) communities in transgenic Bt (MON810) and near isogenic maize , 2010 .

[82]  I. Heap.  International survey of herbicide-resistant weeds , 1997 .

[83]  D. Zilberman,et al.  Transgenic technology adoption and on-farm varietal diversity , 2009 .

[84]  P. Christou.  No Credible Scientific Evidence is Presented to Support Claims that Transgenic DNA was Introgressed into Traditional Maize Landraces in Oaxaca, Mexico , 2002, Transgenic Research.

[85]  L. Lynd,et al.  How biotech can transform biofuels , 2008, Nature Biotechnology.

[86]  Olivier Sanvido,et al.  Ecological impacts of genetically modified crops: ten years of field research and commercial cultivation. , 2007, Advances in biochemical engineering/biotechnology.

[87]  T. V. van Hintum,et al.  Genetic diversity trends in twentieth century crop cultivars: a meta analysis , 2010, Theoretical and Applied Genetics.

[88]  Timothy J. Dennehy,et al.  Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[89]  F. Ortego,et al.  Bt maize fed-prey mediated effect on fitness and digestive physiology of the ground predator Poecilus cupreus L. (Coleoptera: Carabidae). , 2009, Journal of insect physiology.

[90]  C. Rempel,et al.  Field Efficacy Assessment of Transgenic Roundup Ready Wheat , 2003 .

[91]  Ada Wossink,et al.  Environmental and cost efficiency of pesticide use in transgenic and conventional cotton production , 2006 .

[92]  A. Shelton,et al.  UK field-scale evaluations answer wrong questions , 2003, Nature Biotechnology.

[93]  L G Firbank,et al.  Crop management and agronomic context of the Farm Scale Evaluations of genetically modified herbicide-tolerant crops. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[94]  The Impact of Biotech Corn Traits on Ethanol Production , 2008 .

[95]  Amani Elobeid,et al.  The Production and Price Impact of Biotech Corn, Canola, and Soybean Crops , 2010 .

[96]  G. Norton,et al.  The potential benefits of herbicide-resistant transgenic rice in Uruguay: Lessons for small developing countries , 2006 .

[97]  R. Blackshaw,et al.  Response of Ground Beetle (Coleoptera: Carabidae) Field Populations to Four Years of Lepidoptera-Specific Bt Corn Production , 2007, Environmental entomology.

[98]  Z. Huang,et al.  A Meta-Analysis of Effects of Bt Crops on Honey Bees (Hymenoptera: Apidae) , 2008, PloS one.

[99]  M. O’Callaghan,et al.  Effects of plants genetically modified for insect resistance on nontarget organisms. , 2005, Annual review of entomology.

[100]  L. Gianessi,et al.  Economic Impact of Glyphosate‐Resistant Weeds , 2010 .

[101]  P. Ehrlich,et al.  Biodiversity Studies: Science and Policy , 1991, Science.

[102]  M. Hill,et al.  Weeds in fields with contrasting conventional and genetically modified herbicide-tolerant crops. II. Effects on individual species. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[103]  J. Bennett,et al.  A two-year field study with transgenic Bacillus thuringiensis maize: effects on soil microorganisms. , 2008, The Science of the total environment.

[104]  David A. Bohan,et al.  Responses of plants and invertebrate trophic groups to contrasting herbicide regimes in the Farm Scale Evaluations of genetically modified herbicide-tolerant crops. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[105]  David A. Bohan,et al.  On the rationale and interpretation of the Farm Scale Evaluations of genetically modified herbicide-tolerant crops. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[106]  Micheal D. K. Owen,et al.  Survey of Tillage Trends Following The Adoption of Glyphosate-Resistant Crops , 2009, Weed Technology.

[107]  V. Krishna,et al.  Potential impacts of Bt eggplant on economic surplus and farmers' health in India , 2008 .

[108]  R. Bennett,et al.  Reductions in insecticide use from adoption of Bt cotton in South Africa: impacts on economic performance and toxic load to the environment , 2004, The Journal of Agricultural Science.

[109]  L. Pedigo,et al.  Effects of Transgenic Herbicide-Resistant Soybean Varieties and Systems on Surface-Active Springtails (Entognatha: Collembola) , 2002 .

[110]  An evaluation of methods for assessing the impacts of Bt‐maize MON810 cultivation and pyrethroid insecticide use on Auchenorrhyncha (planthoppers and leafhoppers) , 2008 .

[111]  S. Arpaia,et al.  The impact of transgenic plants on natural enemies: a critical review of laboratory studies , 2005 .

[112]  J. Gressel,et al.  Genetic Glass Ceilings: Transgenics for Crop Biodiversity , 2008 .

[113]  Scott Rozelle,et al.  Bt Cotton in China: Are Secondary Insect Infestations Offsetting the Benefits in Farmer Fields? , 2009 .

[114]  P. Motavalli,et al.  Assessing changes in soil microbial communities and carbon mineralization in Bt and non-Bt corn residue-amended soils , 2007 .

[115]  David A. Bohan,et al.  Invertebrate responses to the management of genetically modified herbicide-tolerant and conventional spring crops. I. Soil-surface-active invertebrates. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[116]  M. Hill,et al.  Weeds in fields with contrasting conventional and genetically modified herbicide-tolerant crops. I. Effects on abundance and diversity. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[117]  P. Kramarz,et al.  Studying the effect of exposure of the snail Helix aspersa to the purified Bt toxin, Cry1Ab , 2007 .

[118]  Rosalind J Wright,et al.  Areawide Suppression of European Corn Borer with Bt Maize Reaps Savings to Non-Bt Maize Growers , 2010, Science.

[119]  J. Pritchard,et al.  High Susceptibility of Bt Maize to Aphids Enhances the Performance of Parasitoids of Lepidopteran Pests , 2007, PloS one.

[120]  M. Van Lijsebettens,et al.  Molecular Improvement of Tropical Maize for Drought Stress Tolerance in Sub-Saharan Africa , 2009 .

[121]  F. Bigler,et al.  Uptake of Bt‐toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea , 2002 .

[122]  David A. Bohan,et al.  Invertebrates and vegetation of field margins adjacent to crops subject to contrasting herbicide regimes in the Farm Scale Evaluations of genetically modified herbicide-tolerant crops. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[123]  J. Losey,et al.  Transgenic pollen harms monarch larvae , 1999, Nature.

[124]  Hari C. Sharma,et al.  Influence of transgenic cottons with Bacillus thuringiensis cry1Ac gene on the natural enemies of Helicoverpa armigera , 2007, BioControl.

[125]  Aiming Qi,et al.  A novel approach to the use of genetically modified herbicide tolerant crops for environmental benefit , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[126]  W. Nentwig,et al.  Effects of Bt-corn decomposition on the composition of the soil meso- and macrofauna , 2008 .

[127]  Cho‐ying Huang,et al.  Landscape effects of transgenic cotton on non-target ants and beetles , 2009 .

[128]  J. Fernandez-Cornejo,et al.  Adoption of Bioengineered Crops , 2005 .

[129]  E. J. Rosi-Marshall,et al.  Toxins in transgenic crop byproducts may affect headwater stream ecosystems , 2007, Proceedings of the National Academy of Sciences.

[130]  C. Swan,et al.  Exposure and Nontarget Effects of Transgenic Bt Corn Debris in Streams , 2010, Environmental entomology.

[131]  W. G. Johnson,et al.  U.S. Grower Views on Problematic Weeds and Changes in Weed Pressure in Glyphosate-Resistant Corn, Cotton, and Soybean Cropping Systems , 2009, Weed Technology.

[132]  Paul E. Waggoner,et al.  How Much Land Can Ten Billion People Spare for Nature , 1995 .

[133]  Jeffrey D. Wolt,et al.  Genetically modified crops for the bioeconomy: meeting public and regulatory expectations , 2007, Transgenic Research.

[134]  S. Freeman,et al.  The effects of GMHT crops on bird abundance in arable fields in the UK , 2007 .

[136]  W. Nentwig,et al.  Are survival and reproduction of Enchytraeus albidus (Annelida: Enchytraeidae) at risk by feeding on Bt-maize litter? , 2009 .

[137]  X. Pons,et al.  Managing weeds in herbicide-tolerant GM maize for biological control enhancement. , 2010 .

[138]  L. Kaiser,et al.  Impact assessment of Bt-maize on a moth parasitoid, Cotesia marginiventris (Hymenoptera: Braconidae), via host exposure to purified Cry1Ab protein or Bt-plants , 2007 .

[139]  Angelika Hilbeck,et al.  Effects of Activated Bt Transgene Products (Cry1Ab, Cry3Bb) on Immature Stages of the Ladybird Adalia bipunctata in Laboratory Ecotoxicity Testing , 2009, Archives of environmental contamination and toxicology.

[140]  K. Yamaguchi-Shinozaki,et al.  Stress-inducible expression of At DREB1A in transgenic peanut (Arachis hypogaea L.) increases transpiration efficiency under water-limiting conditions , 2007, Plant Cell Reports.

[141]  G. Stephenson,et al.  Influence of herbicide-resistant canola on the environmental impact of weed management. , 2005, Pest management science.

[142]  H. Hamburg,et al.  Diversity and comparative phenology of Lepidoptera on Bt and non-Bt maize in South Africa , 2008 .

[143]  M. Pedersen,et al.  Weed and arthropod populations in conventional and genetically modified herbicide tolerant fodder beet fields , 2005 .

[144]  B. Dale,et al.  Corn Amylase: Improving the Efficiency and Environmental Footprint of Corn to Ethanol through Plant Biotechnology , 2009 .