THE HERBICIDE GLYPHOSATE: CROP TREE PRODUCTIVITY AND NON-TARGET IMPACTS A COMPENDIUM OF REFERENCES AND ABSTRACTS 6th EDITION 2000-2012 INFORMATION REPORT APPLIED MAMMAL RESEARCH INSTITUTE i RATIONALE AND BACKGROUND The original concept of a compendium of references and abstracts outlining the “non-target impacts of the herbicide glyphosate” arose from the apparent incomplete and scattered sources of information on this subject. A common complaint from both lay and professional people is: “What research has been done on non-target impacts of glyphosate and how do we access this information?” The digital literature search, resulting in this sixth edition of the compendium, involved several thousand references covering environmental impacts, toxicology, and human health. This edition represents the period 2000-2012. A new section on crop tree productivity was added in this edition and generally covers the period 1990- 2012. Thus, there is a considerable ongoing literature base for glyphosate and this compendium was updated to provide, in as complete a manner as possible, a collection of titles and abstracts of articles reporting on the non-target impacts of this herbicide. ORIGIN AND USE OF COMPENDIUM This edition of the compendium is designed as an Information Report to provide an objective assessment of the effects of glyphosate on non-target species and ecosystems, as well as crop tree productivity. References are from peer reviewed publications in scientific journals from 2000 to 2012 and were extracted from a computerized literature search via Google Scholar. Titles and abstracts have been reproduced exactly as they appear in the original article or as abstracted by the source system. In the case of a few journal articles without a formal abstract, a summary of the study has been abstracted by the compilers and this is clearly indicated by an asterisk (*). The compendium is composed of 11 sections: (1) Amphibians, Aquatic Invertebrates and Plants, and Algae, (2) Biodiversity, Conservation, and Habitat Restoration, (3) Birds, (4) Crop Tree Productivity, (5) Fish, (6) Human Health, (7) Mammals, (8) Microbiota and Fungi, (9) Plant and Soil Residues, (10) Terrestrial Invertebrates, and (11) Water Quality. All titles and abstracts of references with author(s) and publication outlet are listed alphabetically in each section. References are identified by country to assist the reader. References which pertain to more than one section are referred to in each section with the abstract appearing in the section deemed most relevant to the article. For complete accuracy, we recommend that users cite from the original references and not from the abstracts presented here. Druscilla S. Sullivan, M.Sc. Research Associate Thomas P. Sullivan, Ph.D. Director and Research Scientist Applied Mammal Research Institute Summerland, B.C., Canada September 2012 ii TABLE OF CONTENTS I. Amphibians, Aquatic Invertebrates and Plants, and Algae .............................. 1 II. Biodiversity, Conservation, and Habitat Restoration ...................................... 51 III. Birds ............................................................................................................... 81 IV. Crop Tree Productivity ……………………………………………………………88 V. Fish .............................................................................................................. 135 VI. Human Health .............................................................................................. 160 VII. Mammals ..................................................................................................... 187 VIII. Microbiota and Fungi ................................................................................... 195 IX. Plant and Soil Residues ............................................................................... 227 X. Terrestrial Invertebrates ............................................................................... 237 XI. Water Quality ............................................................................................... 261 iii SOURCE LISTING OF COUNTRIES Argentina 29 Malaysia 1 Australia 10 Mexico 3 Austria 2 N. Europe 1 Bangladesh 1 New Zealand 6 Belize 1 Nigeria 4 Brazil 34 Philippines 1 Canada 102 Poland 6 Chile 2 Portugal 5 China 10 Romania 1 Colombia 9 Russia 2 Costa Rica 1 Serbia 1 Croatia 2 Slovak Republic 2 Czech Republic 2 South Africa 9 Denmark 7 South Korea 1 Egypt 3 Spain 5 Ecuador 1 Sri Lanka 3 Finland 3 Sweden 4 France 17 Switzerland 2 Germany 3 Thailand 1 India 7 The Netherlands 4 Indonesia 1 Turkey 1 Iran 2 U.S.A. 159 Italy 2 Ukraine 1 Japan 5 United Kingdom 14 Kenya 1 iv Production for the 6th Compendium of the Herbicide Glyphosate: Crop Tree Productivity and Non-Target is thanks to the following sponsors: December, 2012 Valued Clients, Leadership is not a word that is taken likely at Monsanto Canada. We understand our Roundup brands are leaders in agriculture, lawn and garden, industrial vegetation management and forestry renewal. To maintain that leadership means supporting our markets with tools to keep our clients as leaders in their business. The 6th Edition of the Compendium continues to show our pledge to providing our clients the most update to date and factual information on our products to maintain that leadership. Supporting client education, providing stewardship on our brands and maintaining freedom to operate are important pledges from Monsanto to its clients. Glyphosate has become the most widely used active ingredient for vegetation management in the world. At Monsanto, providing important tools like the 6th Compendium will maintain our leadership for many years to come. Bill Sherk, Crop Protection Business Lead Monsanto Canada Inc. www.monsanto.ca December, 2012 Vegetation Management Professionals, Since 1995, Engage Agro Corporation has been developing, registering, marketing and servicing crop protection products for niche and smaller market segments in Canada. Our clientele are continuously looking for ways to access new pest control options as well as maintaining important active ingredients like glyphosate. This 6th Compendium marks an important milestone in the growth of Engage Agro Corporation. It is the first time we have partnered with one of our major suppliers on an important technical piece for one of our key markets. Our Forestry division provides leadership in the Canadian market. Our sponsorship of this document shows our commitment to our supply partner and our continued support for our clients. I am confident this new Compendium will meet your expectations, Best Wishes, Ray Chyc, President Engage Agro Corporation www.engageagro.ca Amphibians, Aquatic Invertebrates and Plants, and Algae 1 Amphibians, Aquatic Invertebrates and Plants, and Algae 1. Battaglin, W.A., K.C. Rice, M.J. Focazio, S. Salmons, and R.X. Barry. 2009. The occurrence of glyphosate, atrazine, and other pesticides in vernal pools and adjacent streams in Washington, DC, Maryland, Iowa, and Wyoming, 2005-2006. Environmental Monitoring and Assessment 155(1-4): 281-307. See Water Quality Section. 2. Battaglin, W.A., D.W. Kolpin, E.A. Scribner, K.M. Kuivila, and M.W. Sandstrom. 2005. Glyphosate, other herbicides, and transformation products in Midwestern streams, 2002. Journal of the American Water Resources Association 41(2): 323- 332. See Water Quality Section. 3. Beachy, J.R., R. Neville, and C. Arnott. 2011. Successful control of an incipient invasive amphibian: Eleutherodactylus coqui on O‘ahu, Hawai‘i. Pages 140-147 In: Veitch, C. R.; Clout, M. N. and Towns, D. R. (eds.). 2011. Island invasives: eradication and management. IUCN, Gland, Switzerland. See Biodiversity and Restoration Section. 4. Bernal, M.H., K.R. Solomon and G. Carrasquilla. 2009. Toxicity of formulated glyphosate (Glyphos) and Cosmo-Flux to larval Colombian frogs 1. laboratory acute toxicity. Journal of Toxicology and Environmental Health, Part A 72(15): 961-965. The spraying of coca (Erythroxylum coca) with glyphosate in Colombia has raised concerns about possible impacts on amphibians. There are few toxicity data for species other than those from temperate regions, and these have not been generated with the combination of formulated glyphosate (Glyphos) and the adjuvant, Cosmo-Flux (coca mix) as used in coca control in Colombia. In order to characterize toxicity of the spray mixture to frogs from Colombia, Gosner stage-25 tadpoles of Scinax ruber, Dendropophus microcephalus, Hypsiboas crepitans, Rhinella granulosa, Rhinella marina, Rhinella typhonius, Centrolene prosoblepon, and Engystomops pustulosus were exposed to the coca mix at concentrations of glyphosate ranging from 1 to 4.2 mg a.e./L diluted in dechlorinated tap water in glass containers. Cosmo-Flux was added to Glyphos in the proportion of 2.3% v/v, as used in aerial application for coca control. Exposures were for 96 h at 23 ± 1.5oC with 12:12-h light/dark cycle. Test solutions were renewed every 24 h. Concentrations, measured within the first hour and at 24 and 96 h using enzyme- linked immunosorbent assay (ELISA) (Abraxis, LLC), ranged from 70 to 130% of nominal values. LC50 values ranged from 1200 to 2780 mg glyphosate acid equivalents (a.e.)/L for the 8 species tested. Data suggest that sensitivity to Roundup-type formulations of glyphosate in these species is similar to that observed in other tropical and temperate species. In addition, sensitivity of larval amphibians to Roundup-type formulations spans a relatively narrow range. Finally, toxicity of the mixture as used to