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Atrazine and Amphibians: A Story of Profits, Controversy, and Animus

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Abstract

The herbicide atrazine is one of the most commonly used, well studied, and controversial pesticides on the planet. Much of the controversy surrounds the effects of atrazine on wildlife, particularly amphibians, and involves representatives from Syngenta Crop Protection, Inc., the company that produces atrazine, the US Environmental Protection Agency, and several academics with current, past, or no associations with Syngenta. Here, I briefly review the effects of atrazine on amphibians and provide a timeline of some of the most salient events in the history of the atrazine-amphibian controversy.
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Allran JWand Karasov WH(2000) Effects of atrazine andnitrate on northern leopard frog (Rana pipiens) l arvaeexposed in the laboratory from posthatch through metamorphosis.
Environmental Toxicology and Chemistry 19: 2850–2855.
Allran JWand Karasov WH(2001) Effects of atrazine on embryos, larvae, and adults of anuran amphibians. Environmental Toxicology and Chemistry 20: 769–775.
Aviv R (2014) A valuable r eputation. The New Yorker, http://www.newyorker.com/magazine/2014/2002/2010/a-valuable-reputation.
Baxter LR, Moore DL, Sibley PK, et al. (2011) Atrazine does not affect algal biomass or snail populations in microcosm communities at environmentally relevant concentrations.
Environmental Toxicology and Chemistry 30: 1689–1696.
Beyond_Pestici des (2015) Atr azine and glyphosate to be analyzed by EPA for i mpacts on 1,500 endangered species. Daily New Blog. Beyond Pestici des, http://beyondpesticides.org/
dailynewsblog/2015/06/atrazine-and-glypohsate-to-be-analyzed-by-epa-for-impacts-on-1500-endangered-species/.
Blackstone Band Drozdiak N(2016) SyngentaandChemChina miss EUdeadlinefor antitrust remedies. TheWall Street Journal, NewYork. http://www.wsj.com/articles/syngenta-and-
chemchina-miss-eu-antitrust-deadline-for-merger-1477304119.
Blumenstyk G (2003) The pri ce of research: a Berkeley sci entist says a corpor ate sponsor tri ed to bury hi s unwelcome findi ngs and then buy hi s silence. The Chroni cle of Higher
Education 50: A26. http://www.chronicle.com/article/The-Price-of-Research/21691/.
BooneMD and James SM (2003) Interactions of an insecticide, herbi cide, and natural stressors in amphibian community mesocosms. Ecological Applications 13: 829–841.
Boone MD and Rohr JR (2015) The trouble with risk assessment l ies at the foundation. Bi oscience 65: 227–228.
BooneMD, Bishop CA, Boswell LA, et al. (2014) Pesticide regulation amid the influenceof industry. Bioscience64: 917–922.
Civitell o DJ, Cohen J, Fatima H, et al. (2015) Biodi versity inhibi ts parasites: broad evidence for the dilution effect. Proceedings of the National Academy of Sciences of the United
States of Ameri ca 112: 8667–8671.
Clements WH and Rohr JR (2009) Community responses to contaminants: usi ng basic ecologi cal princi ples to predict ecotoxicol ogical effects. Environmental Toxicology and
Chemistry 28: 1789–1800.
Cohen JM, Civitello DJ, Brace AJ, et al. (2016) Spatial scale modulates thestrength of ecological processes driving diseasedistributions. Proceedings of the National Academy of
Sciences of theUnited States of America113: E3359–E3364.
Dalton R(2010) E-mail s spark ethics row. Nature 466: 913.
DeLaender F, Rohr JR, Ashauer R, et al. (2016) Re-introducing environmental changedrivers in biodiversity-ecosystem functi oning research. Trends in Ecology and Evoluti on
12: 905–915.
de Noyell es F, Kettl eWD, FrommCH, et al. ( 1989) Useof experimental ponds to assess theeffects of a pestici deon t heaquatic environment. In: Voshell JR(ed.) Using mesocosms t o
assess theaquatic ecological risk of pesticides: theory andpractice, pp. 41–56, Lanham, MD: Entomological Society of America.
DobsonA, Cattadori I, Holt RD, et al. (2006) Sacred cows and sympathetic squirrels: the importance of biological diversity to humanhealth. PLOSMedici ne 3: 714–718.
Douglas MR, Rohr JR, and Tooker JF (2015) Neonicotinoid insecticide travels through asoil food chain, disrupting biological control of non-target pest s and decr easing soya bean
yield. Journal of Applied Ecology 52: 250–260.
EhrsamM, Knutie SA, andRohr JR(2016) Theherbici deatrazine induces hyperactivity and compromises tadpole detection of predator chemical cues. Envir onmental Toxi cology and
Chemistry 35: 2239–2244.
Fan WQ, YanaseT, Morinaga H, et al. (2007) Atrazine-i nduced aromataseexpression is SF-1 dependent: i mplications for endocri nedi sruption in wildlife and reproducti vecancers in
humans. Environmental Health Perspectives 115: 720–727.
Farruggia FT, Rossmeisl CM, Hetrick JA, et al. (2016) Refined ecological risk assessment for atrazine. Washington, DC: USEnvironmental Protection Agency, Office of Pest icide
Programs.
Forson D and Storf er A (2006a) Effects of atrazine and iri dovirus i nfection on survival and lif e-hi story traits of t hel ong-toed salamander (Ambystomamacrodactylum). Environmental
Toxicology and Chemistry 25: 168–173.
Forson DD and Storfer A (2006b) Atrazine i ncreases ranavirus susceptibil ity i n the ti ger sal amander, Ambystoma tigr inum. Ecologi cal Appli cations 16: 2325–2332.
Gabor CR, Roznik EA, Knutie SA, et al. (2016) Does corticosteronemediatethenegative effects of atrazine andBatrachochytriumdendrobatidi son growth and survival? Integrative and
Comparative Biol ogy 56: E70.
Gendron AD, Bishop CA, Fortin R, et al. (1997) In vivo testing of the functi onal integrity of the corti costerone-producing axis in mudpuppy (amphibia) exposed to chlorinated
hydrocarbons in the wil d. Environmental Toxicology and Chemistry 16: 1694–1706.
Grube A, Donaldson D, Kiely T, et al. (2011) Pesticide industry sales andusage: 2006and 2007 market estimates. Washington, DC: U.S. Environmental Protection Agency.
Halstead NT, McMahon TA, Johnson SA, et al. (2014) Community ecology theory predicts the effects of agrochemical mixtures on aquatic biodiversity and ecosystem properti es.
Ecology Letters 17: 932–941.
HayesTB (2003) Alteration of the hormonal milieu following atrazine exposure: what do amphibian studies tell us about humans? Biol ogy of Reproduction 68: 103.
Hayes TB (2004) There is no denying this: defusing the confusion about atrazine. Bioscience 54: 1138–1149.
HayesT, Haston K, Tsui M, et al. (2002a) Herbicides: feminization of male frogs in the wild. Nature 419: 895–896.
HayesTB, Collins A, LeeM, et al. (2002b) Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologi call y relevant doses. Proceedings of theNational
Academy of Sciences of the United States of America 99: 5476–5480.
HayesT, Haston K, Tsui M, et al. (2003) Atrazine-induced hermaphroditism at 0.1 ppbin Americanleopard frogs (Ranapipiens): l aboratory andfield evidence. Environmental Health
Perspectives 111: 568–575.
Hayes TB, Case P, Chui S, et al. (2006) Pestici de mixt ures, endocrine di srupti on, and amphibi an decli nes: are we underestimating the i mpact? Environmental Heal th Perspecti ves
114: 40–50.
Hayes TB, Khoury V, Narayan A, et al. (2010) Atrazine induces complete femini zation and chemical castrati on in male African clawed frogs (Xenopus laevis). Proceedings of the
National Academy of Sciences of theUnited States of America107: 4612–4617.
Herman D, Kaushik NK, and Solomon KR(1986) Impact of atrazine on periphyton in fresh-water enclosures and some ecologi cal consequences. Canadian Journal of Fisheries and
Aquatic Sciences 43: 1917–1925.
Howard C (2013a) Pest control : Syngenta’s Secret Campaign to Discredit Atrazine’s Critics. https://100r.org/2013/2006/pest-control-syngentas-secret-campaign-to-
discredit-atrazines-critics/ in 100Reporters, editor.
Howard C (2013b) Til lery to represent Hayes against UC Berkeley in dispute over lab fees. https://100r.org/2013/2008/excessive-lab-fees-choking-research-scientist-says/ in
100Reporters, editor.
Ivory D (2009) EPA fails to inform public about weed-kill er in drinking water. The Huffington Post, http://www.huffingtonpost.com/2009/2008/2023/epa-fails-to-inform-publi_n_
266686.html.
Ivory D (2010) Is weed kil ler in drinking water dangerous? Govt. is letting the chemical industry comeup with the answer, in Alternet.org,editor.
Kerby JL and Storfer A (2009) Combined effects of atrazine and chlorpyrifos on susceptibi lity of the ti ger salamander to Ambystoma tigrinum virus. EcoHealth 6: 91–98.
Kiesecker JM (2002) Synergi smbetween trematodei nfecti on and pesti cide exposure: a li nk to amphibi an li mb deformiti es in nature? Proceedings of t heNational Academy of Sciences
of the UnitedStates of America 99: 9900–9904.
Knutson MG, Richardson WB, ReinekeDM, et al. (2004) Agricultural ponds support amphibian populations. Ecological Applications 14: 669–684.
Koprivnikar J (2010) Interactions of environmental stressors impact survival anddevelopment of parasitized larval amphibians. Ecological Applications 20: 2263–2272.
Landis WG, Rohr JR, Moe SJ, et al. (2014) Global climate change and contaminants, a call to arms not yet heard? Integrated Environmental Assessment and Management
10: 483–484.
Langerveld AJ, Celestine R, ZayaR, et al. (2009) Chronic exposure to high levels of atrazine alters expression of genes that regulate immune and growth-relatedfunctions in
developing Xenopus laevis tadpoles. Environmental Research 109: 379–389.
Larson DL, McDonald S, Fivizzani AJ, et al. (1998) Effects of the herbicide atrazineon Ambystomatigrinum metamorphosis: duration, larval growth, and hormonal response.
Physiological Zoology 71: 671–679.
Li Y, Cohen JM, and Rohr JR(2013) Reviewand synthesis of the effects of climatechangeon amphibians. Integrative Zoology 8: 145–161.
Liu X, Rohr JR, and Li YM (2013) Climate, vegetation, introduced hosts and tradeshapea global wildlifepandemic. Proceedings of the Royal Society B: Biological Sciences 280:
20122506. http://dx.doi.org/10.1098/rspb.2012.2506.
Lurling M and Scheffer M (2007) Info-di sruption: pollution and the transfer of chemical information between organisms. Trends in Ecology & Evolution 22: 374–379.
Madliger CL, CookeSJ, Crespi EJ, et al. (2016) Success stories and emerging themes in conservation physiology. Conservation Physiology 4.
Martin LB, Hopkins WA, Mydlarz LD, et al. (2010) The effects of anthropogenic global changes on immune functions and diseaseresistance. Year in Ecology and Conservation
Biology. Annals of the New York Academy of Sciences 1195: 129–148. http://dx.doi.org/10.1111/j.1749-6632.2010.05454.x.
McMahon TA, Halstead NT, Johnson S, et al. (2011) The fungicide chlorothalonil is nonlinearly associated with corticosterone levels, immunity, and mortalityin amphibians.
Environmental Health Perspectives 119: 1098–1103.
McMahon TA, Halstead NT, Johnson S, et al. (2012) Fungicide-induced decli nes of freshwater biodiversi ty modify ecosystemfuncti ons and services. Ecology Letters 15: 714–722.
McMahon TA, Romansic JM, and Rohr JR(2013) Nonmonotonic and monotonic effects of pesticides on the pathogenic fungus Batrachochytrium dendrobatidis incultureandon
tadpoles. Environmental Sci ence & Technology 47: 7958–7964.
McMahonTA, Sears BF, VeneskyMD, et al. (2014) Amphibians acquireresistance to live and dead fungus overcoming fungal immunosuppression. Nature 511: 224–227.
McMahon TA, Boughton RK, Marti n LB, et al. ( 2017) Exposure to the herbi cide atrazine nonlinearly affects t adpole corticosterone levels. Journal of Herpetology (in press).
Michaels D and Monforton C (2005) Manufacturing uncertainty: contested science and the protection of the public’s health and environment. American Journal of Publi c Health
95: S39–S48.
Moore A and Waring CP (1998) Mechanistic effects of a tri azine pesticide on reproductive endocrine function i n mature male Atlantic salmon (Salmo salar L.) parr. Pesticide
Biochemistry and Physiology 62: 41–50.
Polansek T(2016) Widely used U.S. farm chemical atrazine may threaten animals: EPA. http://www.reuters.com/articl e/us-usa-epa-atrazine-idUSKCN0YO2X9 Reuter s, http://www.
reuters.com/article/us-usa-epa-atrazine-idUSKCN0YO2X9.
Raffel TR, Sheingold JL, and Rohr JR(2009) Lack of pestici detoxicity to Echinostoma tri volvis eggs and miracidi a. Journal of Parasitol ogy 95: 1548–1551.
Raffel TR, Hoverman JT, Halstead NT, et al. (2010) Parasitism in acommunity context: trait-mediated interactions with competition and predation. Ecology 91: 1900–1907.
Raffel TR, Halstead NT, McMahon T, et al. (2013) Diseaseand thermal acclimation in a more variable and unpredictable climate. Nature Cli mateChange3: 146–151.
Rohr JR and Crumrine PW(2005) Effects of an herbicide and an insecticide on pond community structure and processes. Ecological Appli cations 15: 1135–1147.
Rohr JR and McCoyKA (2010a) Preserving environmental health and scientific credibility: a practical guide to reducing confl icts of interest. Conservation Letters 3: 143–150.
Rohr JR and McCoy KA (2010b) A qualitative meta-analysi s reveals consi stent effects of atrazine on freshwater fish and amphibi ans. Environmental Health Perspectives 18: 20–32.
Rohr JRand Palmer BD (2005) Aquatic herbicide exposureincreases salamander desiccation risk eight months later in a terrestrial environment. Environmental Toxicology and
Chemistry 24: 1253–1258.
Rohr JR and Palmer BD (2013) Cli mate change, mul tipl e stressors, and the decli ne of ectotherms. Conservation Biol ogy 27: 741–751.
Rohr JRandRaffel TR(2010) Linkingglobal climateandtemperaturevariabilityto widespreadamphibian declinesputatively caused bydisease. Proceedings of t heNational Academy
of Sci ences of the Unit ed States of America 107: 8269–8274.
Rohr JR, Elskus AA, Shepherd BS, et al. (2003) Lethal andsublethal effects of atrazine, carbaryl, endosulfan, and octylphenol on the streamside salamander, Ambystoma barbouri .
Environmental Toxicology and Chemistry 22: 2385–2392.
Rohr JR, Elskus AA, Shepherd BS, et al. (2004) Mul tipl est ressors and salamanders: effects of an herbi cide, food l imitati on, and hydroperiod. Ecologi cal Appl ications 14: 1028–1040.
Rohr JR, Kerby JL, and Sih A (2006a) Community ecology as aframework for predicti ng contaminant effects. Trends in Ecology & Evolution 21: 606–613.
Rohr JR, Sager T, Sesterhenn TM, et al. (2006b) Exposure, postexposure, and density-mediated effects of atrazine on amphibians: breaking down net effects into their parts.
Environmental Health Perspectives 114: 46–50.
Rohr JR, Raffel TR, Romansic JM, et al. (2008a) Evaluating thelinks betweencli mate, diseasespread, and amphibiandeclines. Proceedings of the National Academy of Sciences of the
United States of America 105: 17436–17441.
Rohr JR, Raffel TR, Sessions SK, et al. (2008b) Understanding thenet effects of pesticideson amphibian trematode infections. Ecological Applications 18: 1743–1753.
Rohr JR, Schotthoefer AM, Raffel TR, et al. (2008c) Agrochemicals increase trematode infections in adeclining amphibian species. Nature 455: 1235–1239.
Rohr JR, SwanA, Raffel TR, et al. (2009) Parasites, info-disruption, andtheecology of fear. Oecologia159: 447–454.
Rohr JR, Raffel TR, and Hall CA (2010) Developmental variation in resistanceand tolerance in a multi -host-parasite system. Functional Ecology 24: 1110–1121.
Rohr JR, Sesterhenn TM, and Stieha C(2011) Wil l climate change reducethe effects of a pesticide on amphibians?: Partitioning effects on exposure and susceptibilitytopollution.
Global Change Biol ogy 17: 657– 666.
Rohr JR, Halstead NT, and Raffel TR(2012) Theherbicide atrazine, algae, and snail populations. Environmental Toxicology and Chemistry 31: 973–974.
Rohr JR, Johnson P, Hickey CW, et al . (2013a) I mpli cations of gl obal cl imate change for natural r esource damage assessment, r estorati on, and rehabil itation. Environmental
Toxicology and Chemistry 32: 93–101.
Rohr JR, Raffel TR, Blaustein AR, et al. (2013b) Usi ng physiol ogy to understand cli mate-dr iven changes in diseaseand their i mpli cati ons for conservation. Conservation Physiology 1.
http://dx.doi.org/10.1093/conphys/cot1022.
Rohr JR, Raffel TR, HalsteadNT, et al. (2013c) Early-lifeexposure to aherbicide hasenduring effects on pathogen-i nduced mortality. Proceedings of the Royal Society B: Biologi cal
Sciences 280: 20131502.
Rohr JR, Civitello DJ, Crumrine PW, et al. (2015) Predator diversity, intraguild predation, and indirect effects drive parasitetransmission. Proceedings of the National Academy of
Sciences of t he United States of America 112: 3008–3013.
Rohr JR, Salice CJ, and Nisbet RM(2016) The pros and cons of ecological risk assessment based on data from different levels of biologi cal organization. Critical Reviews in
Toxicology 46: 756–784.
Sass JB and Colangelo A (2006) European Union bans atrazine, while the United States negotiates continued use. International Journal of Occupational and Environmental Health
12: 260–267.
Sass JB and Devine JP (2004) The center for regulatory effecti veness invokes the data quali ty act to reject published studies on atrazine toxicity. Environmental Health Perspecti ves
112: A18.
Schor E(2010) Enviro Groups Cheer as scientist bombards agribusiness with profanee-mails. TheNewYork Times, E&EPublishing, NewYork. http://www.nytimes.com/gwire/
2010/2008/2026/2026greenwire-enviro-groups-cheer-as-scientist-bombards-agri-18199.html?pagewanted¼all.
Schotthoefer AM, Rohr JR, Cole RA, et al. (2011) Effects of wetland vs. landscapevariableson parasite communities of Rana pipiens: links to anthropogenic factors. Ecologi cal
Applications 21: 1257–1271.
Sears BF, Snyder PW, and Rohr JR (2013) Infecti on deflection: hosts control parasite location with behaviour to improve tolerance. Proceedings of the Royal Soci ety B: Bi ologi cal
Sciences 280: 20130759. http://dx.doi.org/10.1098/rspb.2013.0759.
Sears BF, Snyder PW, and Rohr JR(2015) Host life history and host-parasite syntopy predict behavioural resistance and toleranceof parasites. Journal of Animal Ecology
84: 625–636.
Slater D(2012) Thefrog of war. Mother Jones ,http://www.motherjones.com/environment/2011/2011/tyrone-hayes-atrazine-syngenta-feud-frog-endangered.
Solomon KR, Carr JA, PreezLHDu, et al. (2008) Effects of atrazine on fish, amphibians, and aquatic reptiles: acritical review. Critical Reviewsin Toxicology 38: 721–772.
Spegele B, and Chu K ( 2016) ChemChina-Syngenta 43 billion deal approved by U.S. Security Panel. The Wall Street Journal, NewYork. http://www.wsj.com/articles/u-s-
security-watchdog-clears-43-bi llion-chemchina-syngenta-takeover-deal-1471844896.
Staley Z, Harwood VJ, and Rohr JR(2010) The effect of agrochemicals on i ndicator bacteria densities in outdoor mesocosms. Environmental Microbiology 12: 3150–3158.
Staley ZR, Rohr JR, and HarwoodVJ (2011) Test of direct andindirect effects of agrochemicals on the survival of fecal indicator bacteria. Applied and Environmental Microbiology
77: 8765–8774.
Staley ZR, Senkbeil JK, Rohr JR, et al. (2012) Lack of direct effects of agrochemicals on zoonotic pathogens and fecal indicator bacteria. Applied and Environmental Microbiology
78: 8146–8150.
Staley ZR, Rohr JR, Senkbeil JK, et al. (2014) Agrochemicals indirectly increasesurvival of E. coli O157:H7 and indicator bacteria byreducing ecosystem services. Ecologi cal
Applications 24: 1945–1953.
Staley ZR, Harwood VJ, and Rohr JR(2015) A synthesis of the effects of pesticides on microbial persistencein aquatic ecosystems. Critical Reviews in Toxicology 45: 813–836.
Storrs SI and Kiesecker JM (2004) Survivorship patterns of larval amphibians exposed to low concentrations of atrazine. Environmental Health Perspectives 112: 1054–1057.
Tierney KB, Singh CR, Ross PS, et al. (2007) Relating olfactory neurotoxi city to altered olfactory-mediated behaviors in rainbow trout exposed to three currentl y-used pestici des.
Aquatic Toxicology 81: 55–64.
USEPA( 2012) Meeting of the FIFRA Scienti fic Advisory Panel on the probl em formulati on for the environmental fateand ecologi cal risk assessment for atrazine. Washington, DC: US
Environmental Protection Agency.
Vandenberg LN, Colborn T, HayesTB, et al. (2012) Hormones and endocrine-disrupting chemicals: low-doseeffects andnonmonotonic doseresponses. Endocrine Reviews
33: 378–455.
VeneskyMD, Liu X, Sauer EL, et al. (2014a) Linking manipulative experiments to field data to test the dilution effect. Journal of Animal Ecology 83: 557–565.
VeneskyMD, Raffel TR, McMahonTA, et al. (2014b) Confronti nginconsistenciesin the amphibi an-chytridiomycosis system: impli cations for diseasemanagement. Biological Reviews
89: 477–483.
WakeDB and Vredenburg VT (2008) Are wein the midst of the sixth mass extincti on?A viewfrom the world of amphibi ans. Proceedings of the National Academy of Sciences of the
United States of America105: 11466–11473.
Welshons WV, Thayer KA, JudyBM, et al. (2003) Large effects from small exposures. I. Mechanisms for endocrine-disrupti ngchemicals with estrogenic activity. Environmental Health
Perspectives 111: 994–1006.
... Despite the USEPA concluding in 2016 that atrazine poses risks to aquatic plants, fish, amphibians, mammals, birds, and reptiles (Farruggia et al. 2016), and in 2018, that it poses reproductive and developmental risks to humans, particularly children (US Environmental Protection Agency 2018), in 2020, the USEPA renewed the registration of atrazine and relaxed regulations, allowing 50% more atrazine to enter water bodies (Erickson 2019; US Environmental Protection Agency 2020). Although the story of atrazine has been partially told (Rohr 2018), these recent regulatory events, the Trump administration's regular dismissal of science (Lin 2019), and the change in the United States presidency, underscore the importance of drawing new attention to this remarkable story in the history of toxicology that is unfamiliar to so many. Hence, I provide a more complete and updated account of the most salient moments in the history of the atrazine controversy, emphasizing bent science and how it might have impacted decision making with potential consequences for ecosystem and human health and public trust in science. ...
... I focus predominantly on the effects of atrazine on amphibians because most of the controversy surrounding atrazine has centered on amphibian studies. Atrazine is documented to affect amphibian growth and timing of metamorphosis, (Larson et al. 1998;Karasov 2000, 2001;Boone and James 2003;Rohr et al. 2004;Storfer 2006a, 2006b) behaviors crucial for foraging and avoiding predators, (Rohr et al. 2003(Rohr et al. , 2004 and desiccation (Rohr andPalmer 2005, 2013). Moreover, delayed or persistent effects of atrazine on behavior and physiology can increase mortality risk (Storrs and Kiesecker 2004;Rohr and McCoy 2010b;Rohr andPalmer 2005, 2013). ...
... Atrazine is documented to affect amphibian growth and timing of metamorphosis, (Larson et al. 1998;Karasov 2000, 2001;Boone and James 2003;Rohr et al. 2004;Storfer 2006a, 2006b) behaviors crucial for foraging and avoiding predators, (Rohr et al. 2003(Rohr et al. , 2004 and desiccation (Rohr andPalmer 2005, 2013). Moreover, delayed or persistent effects of atrazine on behavior and physiology can increase mortality risk (Storrs and Kiesecker 2004;Rohr and McCoy 2010b;Rohr andPalmer 2005, 2013). There have been numerous studies on the effects of atrazine on physiology because of the role of physiology to vertebrate survival and conservation (Martin et al. 2010;Rohr et al. 2013b;Madliger et al. 2016). ...
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The herbicide atrazine is one of the most commonly used, well studied, and controversial pesticides on the planet. Much of the controversy involves the effects of atrazine on wildlife, particularly amphibians, and the ethically questionable decision making of members of industry, government, the legal system, and institutions of higher education, in most cases in an effort to “bend science,” defined as manipulating research to advance economic, political, or ideological ends. In this Critical Perspective I provide a timeline of the most salient events in the history of the atrazine saga, which includes a multimillion‐dollar smear campaign, lawsuits, investigative reporting, accusation of impropriety against the US Environmental Protection Agency, and a multibillion‐dollar transaction. I argue that the atrazine controversy must be more than just a true story of cover‐ups, bias, and vengeance. It must be used as an example of how manufacturing uncertainty and bending science can be exploited to delay undesired regulatory decisions and how greed and conflicts of interest—situations where personal or organizational considerations have compromised or biased professional judgment and objectivity—can affect environmental and public health and erode trust in the discipline of toxicology, science in general, and the honorable functioning of societies. Most importantly, I offer several recommendations that should help to 1) prevent the history of atrazine from repeating itself, 2) enhance the credibility and integrity of science, and 3) enrich human and environmental health. Environ Toxicol Chem 2021;00:1–15.
... Atrazine acts by inhibiting electron transport in Photosystem II, which disrupts the plant's ability to photosynthesize and causes starvation in broad-leaf plants and eventual death (Giddings et al 2004). It has been shown to have diverse effects on organisms such as amphibians and fish that develop and live in freshwater (Rohr 2018). Low concentrations of atrazine (1 μg/l) have been found to alter olfactory-mediated endocrine function in male Atlantic salmon (Salmo salar) (Moore and Lower, 2001). ...
... Glyphosate (Nphosphonomethyl glycine) is a non-selective herbicide used to control a wide variety of annual and perennial grasses and broadleaved weeds in commercial farmlands and household gardens. Glyphosate, known as Roundup®, is next to atrazine (Rohr 2018). These three herbicides are highly soluble in water. ...
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Pesticides from agricultural run-off pose a severe threat to non-target organisms, such as fishes. This study was carried out to evaluate acute toxicity and histological and genotoxic effects (erythrocytic nuclear abnormalities) of lethal and sub-lethal concentrations of three commonly used pesticides: Atrazine, Butachlor and Glyphosate on the African mud catfish (Clarias gariepinus). Fishes were exposed to the pesticides for 96h periods to determine their LC50 and the sub-lethal effect at various concentrations (1/10th, 1/100th , 1/1000th 96h LC50) over 28 days. The 96h LC50 values were 7.63mg/l, 0.7mg/l and 15.97mg/l for atrazine, butachlor and glyphosate, respectively. Histological sections of the liver of C. gariepinus exposed to the three pesticides showed mild vascular congestion but no necrosis in the tissue. There was a significant (p<0.5) dose-dependent increase in micronuclei and nuclear abnormalities in the erythrocytes of exposed C. gariepinus compared to the control by 28 days. The study confirmed that C. gariepinus are at risk of adverse effects from exposure to pesticides. Discharge of agricultural run-off around water bodies should be prevented or prohibited to avoid adverse effects on aquatic life.
... Despite the plethora of controversies surrounding the toxicity of atrazine based herbicides on non-target organisms such as amphibians [26], they have been proven to have non-target effects on animals [15,27]. For example, atrazine based herbicides are known to alter reproductive processes and development in insects, amphibians, fish, reptiles, birds, rodents and goats [15,16,[28][29][30] Vogel et al. [15] reported that exposure to atrazine had significant effects on males of Drosophila melanogaster Meigen (Diptera: Drosophilidae) mating ability and the number of eggs his partner laid when he was successful at mating. ...
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Recent empirical evidence suggests that herbicides have damaging effects on non-target organisms in both natural and semi-natural ecosystems. The African mound building termite, Macrotermes bellicosus, is an important beneficial insect that functions as an ecosystem engineer due to its role in the breakdown of dead and decaying materials. Here, we examined the effects of 2,4-D amine salt (2,4-D) and atrazine based herbicides viz. Vestamine ® and Ultrazine® on the survival and locomotion response of M. bellicosus. Worker termites were treated with a range of concentrations of Vestamine® (the recommended concentration: 6.25 ml per 500 ml of water, 0.25- and 0.5-fold below the recommended concentration and distilled water as control) and Ultrazine® (the recommended concentration: 3.75 ml per 500 ml of water, 0.25-, 0.5-, 2.0- and 4-fold of the recommended concentration and distilled water as control) for 24 hours for the mortality test, and allowed to run for 15 seconds for the locomotion trial. All concentrations of both Vestamine® and ltrazine® were highly toxic to worker termites and mortality increased as the concentration and time after treatment increased. For both herbicides, concentrations far less than the recommended rates caused 100% mortality. The speed of termites was significantly influenced by both Vestamine® and Ultrazine® as termites exposed to all tested concentrations of the herbicides exhibited reduced running speed than the control. These findings suggest that beneficial insects, especially M. bellicosus may experience high mortality (up to 100%) and reduced mobility if they are sprayed upon or come in contact with plant materials that have been freshly sprayed with (less or more than) the recommended concentrations of Vestamine ® and Ultrazine®. The findings of our study calls for the reassessment of the usage of 2,4-D and atrazine based herbicides in weed control in termite and other beneficial insect populated habitats.
... Despite the plethora of controversies surrounding the toxicity of atrazine based herbicides on non-target organisms such as amphibians [26], they have been proven to have non-target effects on animals [15,27]. For example, atrazine based herbicides are known to alter reproductive processes and development in insects, amphibians, fish, reptiles, birds, rodents and goats [15,16,[28][29][30] Vogel et al. [15] reported that exposure to atrazine had significant effects on males of Drosophila melanogaster Meigen (Diptera: Drosophilidae) mating ability and the number of eggs his partner laid when he was successful at mating. ...
Article
Full-text available
Recent empirical evidence suggests that herbicides have damaging effects on non-target organisms in both natural and semi-natural ecosystems. The African mound building termite, Macrotermes bellicosus, is an important beneficial insect that functions as an ecosystem engineer due to its role in the breakdown of dead and decaying materials. Here, we examined the effects of 2,4-D amine salt (2,4-D) and atrazine based herbicides viz. Vestamine® and Ultrazine® on the survival and locomotion response of M. bellicosus. Worker termites were treated with a range of concentrations of Vestamine® (the recommended concentration: 6.25 ml per 500 ml of water, 0.25- and 0.5-fold below the recommended concentration and distilled water as control) and Ultrazine® (the recommended concentration: 3.75 ml per 500 ml of water, 0.25-, 0.5-, 2.0- and 4-fold of the recommended concentration and distilled water as control) for 24 hours for the mortality test, and allowed to run for 15 seconds for the locomotion trial. All concentrations of both Vestamine® and Ultrazine® were highly toxic to worker termites and mortality increased as the concentration and time after treatment increased. For both herbicides, concentrations far less than the recommended rates caused 100% mortality. The speed of termites was significantly influenced by both Vestamine® and Ultrazine® as termites exposed to all tested concentrations of the herbicides exhibited reduced running speed than the control. These findings suggest that beneficial insects, especially M. bellicosus may experience high mortality (up to 100%) and reduced mobility if they are sprayed upon or come in contact with plant materials that have been freshly sprayed with (less or more than) the recommended concentrations of Vestamine® and Ultrazine®. The findings of our study calls for the reassessment of the usage of 2,4-D and atrazine based herbicides in weed control in termite and other beneficial insect populated habitats.
... Atrazine has been reported to interfere with physiological and biochemical systems in the nontarget aquatic organisms, affecting functions such as development, reproduction, and survival of aquatic biota (Nwani et al., 2010;Rohr and McCoy, 2010). These effects corroborate the reports on extreme population declines in Piscean and amphibian communities (Hayes et al., 2006;Hayes et al., 2010;Rohr, 2013). Atrazine has also been reported to bio-accumulate in various organ tissues (Xing et al., 2012;Dornelles and Oliveira, 2014;Singh et al., 2017). ...
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The toxic effects of different atrazine concentrations on tadpoles and adult male African clawed frogs (Xenopus laevis) were assessed in a controlled laboratory environment following 90 days' exposure. The aim was to elucidate the danger of atrazine exposure on the cardiac tissue relative to its critical function of rhythmic contractility, fundamental for optimal blood circulation and homeostasis. Tadpoles and adult frogs were exposed to 0 μg/L (control), 0.01 μg L-1, 200 μg L-1 and 500 μg L-1 concentrations of atrazine for 90 days. Mortality was concenration-dependent and significantly increased in juvenile group (77%, 43%, 23% and 0 respectively for 500 μg L-1, 200 μg L-1, 0.01 μg L-1, and control group). While the mean juvenile heart area decreased concentration-dependently, adult frog mean heart area significantly increased in the 200 μg L-1 group only and mean heart weight change was variable across all exposure levels. Light microscopy of hematoxylin and eosin (H&E) and Mallory-Heidenhain rapid one-step staining techniques on cardiac tissue sections of the juvenile and adult frogs revealed shrinkage of cardiac muscle cells into thin wavy myocytes. Additionally, disorganized branching of muscle fibres with reduced striations were observed in 0.01 μg L-1 and 200 μg L-1 but hypertrophied myocytes, thickened intensely staining myofibrils in the 500 μg L-1 group in juvenile and adult frogs. Significant increase in the mean percentage area of connective tissue in all the treated groups (p < 0.036) were also recorded. Immunohistochemistry analysis showed decreased eNOS localization in cardiac tissue in 200 μg L-1 and 500 μg L-1 of both juvenile and adult group, suggestive of decreased cardiac contractility due to atrazine exposure. The results indicate that environmentally relevant atrazine concentrations cause significant mortality in tadpoles while concentrations ≥200 μg L-1 adversely affect cardiac muscle morphology and may induce functional perturbations in cardiac tissue contractility and consequent dysfunction which generally may have an adverse impact on their survival and longevity.
Chapter
The fourth edition of this compendium of information resources detailed the explosion of the literature regarding pesticide toxicology since publication of the third edition in 2000. Indeed a search using GOOGLE Scholar, an engine that gathers primarily papers from research journals (i.e., the primary research literature), on just the word “pesticide” today returns over two million “hits.” The fourth edition focused more on the mammalian toxicology of pesticide technology. Thus the information highlighted was primarily focused on human exposure and epidemiology of pesticides with minor attention to environmental chemistry and ecotoxicology.The focus of this updated chapter is greatly expanded to cover more conventional questions in the realm of environmental toxicology since 2009. In particular, key references regarding the major controversies about pesticides covers effects on frogs (amphibians) and bees (mainly the honey bee, Apis mellifera). Literature addressing human health hazards and risk assessment of organophosphorus and pyrethroid insecticides was updated with information about neonicotinoid insecticides and glyphosate herbicide. Additionally, the literature about transgenerational epigenetic effects was listed.
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Proc. R. Soc. B 280, 20131502. (7 December 2013; Published online 23 October 2013) (doi:10.1098/rspb.2013.1502). In the second paragraph of the ‘Material and methods’ section, the concentration of atrazine is incorrectly listed as 65.9 ± 3.48 mg l⁻¹, mean ± s.e. The concentration should be listed as 65.9 ± 3.48 µg l⁻¹, mean ± s.e. • © 2014 The Author(s) Published by the Royal Society. All rights reserved.
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To determine whether the herbicide, atrazine, affects the stress hormone corticosterone, we exposed Osteopilus septentrionalis (Cuban Treefrog) tadpoles to four concentrations of atrazine and two controls (water and acetone) for three time durations (4, 28, and 100 h). Atrazine concentration, but not exposure duration, had significant nonlinear effects on whole-body corticosterone. Relative to controls, intermediate concentrations of atrazine (10.2 and 50.6 μg/L) tended to lower corticosterone, whereas the lowest (0.1 μg/L) and highest atrazine concentrations (102 μg/L) elevated corticosterone. These results indicate that atrazine exposure might dysregulate corticosterone, a hormone integral to vertebrate immunity, neurogenesis, and health.
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Ecological risk assessment (ERA) is the process used to evaluate the safety of manufactured chemicals to the environment. Here we review the pros and cons of ERA across levels of biological organization, including suborganismal (e.g., biomarkers), individual, population, community, ecosystem and landscapes levels. Our review revealed that level of biological organization is often related negatively with ease at assessing cause-effect relationships, ease of high-throughput screening of large numbers of chemicals (it is especially easier for suborganismal endpoints), and uncertainty of the ERA because low levels of biological organization tend to have a large distance between their measurement (what is quantified) and assessment endpoints (what is to be protected). In contrast, level of biological organization is often related positively with sensitivity to important negative and positive feedbacks and context dependencies within biological systems, and ease at capturing recovery from adverse contaminant effects. Some endpoints did not show obvious trends across levels of biological organization, such as the use of vertebrate animals in chemical testing and ease at screening large numbers of species, and other factors lacked sufficient data across levels of biological organization, such as repeatability, variability, cost per study and cost per species of effects assessment, the latter of which might be a more defensible way to compare costs of ERAs than cost per study. To compensate for weaknesses of ERA at any particular level of biological organization, we also review mathematical modeling approaches commonly used to extrapolate effects across levels of organization. Finally, we provide recommendations for next generation ERA, submitting that if there is an ideal level of biological organization to conduct ERA, it will only emerge if ERA is approached simultaneously from the bottom of biological organization up as well as from the top down, all while employing mathematical modeling approaches where possible to enhance ERA. Because top-down ERA is unconventional, we also offer some suggestions for how it might be implemented efficaciously. We hope this review helps researchers in the field of ERA fill key information gaps and helps risk assessors identify the best levels of biological organization to conduct ERAs with differing goals.
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The ability to detect chemical cues is often critical for freshwater organisms to avoid predation and find food and mates. In particular, reduced activity and avoidance of chemical cues signaling predation risk are generally adaptive behaviors that reduce prey encounter rates with predators. Here, we examined the effects of the common herbicide atrazine on the ability of Cuban tree frog (Osteopilus septentrionalis) tadpoles to detect and respond to chemical cues from larval dragonfly (Libellulidae sp.) predators. Tadpoles exposed to an estimated environmental concentration of atrazine (calculated using US EPA software; measured concentration: 178 µg/L) were significantly hyperactive relative to those exposed to solvent control. Additionally, control tadpoles significantly avoided predator chemical cues, but tadpoles exposed to atrazine did not. These results are consistent with previous studies that have demonstrated that ecologically relevant concentrations of atrazine can induce hyperactivity and impair the olfactory abilities of other freshwater vertebrates. We call for additional studies examining the role of chemical contaminants in disrupting chemical communication and the quantification of subsequent impacts on the fitness and population dynamics of wildlife. This article is protected by copyright. All rights reserved.
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Significance Humans are altering biodiversity globally and infectious diseases are on the rise; thus, there is considerable interest in understanding how changes to biodiversity affect disease risk. We show that the diversity of predators that consume parasites was the best negative predictor of infections in frogs, suggesting that predation on parasites can be an important mechanism of disease reduction. Follow-up experiments, field data, and mathematical models revealed that intraguild predators, predators that consume both hosts and parasites, decrease macroparasite infections per host less than predators that only consume parasites, representing a general trait of predators that predicts their ability to reduce disease. Consequently, managing assemblages of non-intraguild and intraguild predators is an underutilized tool to minimize human and wildlife diseases.
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