Thiamethoxam Differentially Impacts the Survival of the Generalist Predators,  Orius insidiosus  (Hemiptera: Anthocoridae) and  Hippodamia convergens  (Coleoptera: Coccinellidae), When Exposed via the Food Chain

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Abstract

Insect predators are seldom considered during toxicological trophic assessments for insecticide product development. As a result, the ecological impact of novel insecticides on predators is not well understood, especially via the food chain, i.e., when their prey is exposed to insecticides. Neonicotinoids are systemic insecticides widely used in agriculture to control herbivorous insects, but their effects on predatory insects via the food chain have not been well characterized. In this study, we documented the time-course effects of the neonicotinoid thiamethoxam on the survival of two predators, the insidiosus flower bug Orius insidiosus (Say) and the convergent lady beetle Hippodamia convergens Guérin-Méneville, when preying upon the aphids Aphis glycines Matsumura (Hemiptera: Aphididae), Aphis gossypii Glover (Hemiptera: Aphididae), and Myzus persicae (Sulzer) (Hemiptera: Aphididae). Aphids were exposed to thiamethoxam-treated or untreated plants every week over the course of 5 wk. After transferring aphids to Petri dishes, predators were allowed to feed on aphids. We found that the survival of the insidiosus flower bug, but not the convergent lady beetle, was reduced after consuming aphids reared on thiamethoxam-treated plants compared to untreated plants. Survival reduction of the insidiosus flower bug was observed only during the first weeks after thiamethoxam application; no reduction occurred 28 d after treatment or beyond. These results demonstrate that a systemic application of thiamethoxam could be compatible with convergent lady beetles and insidiosus flower bugs, if the time of predator release does not coincide with thiamethoxam activity. These findings are critical for the development of future pest control programs that integrate biological and chemical control.

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Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites

N. Simon-Delso, V. Amaral-Rogers, L P Belzunces … (2014)

Since their discovery in the late 1980s, neonicotinoid pesticides have become the most widely used class of insecticides worldwide, with large-scale applications ranging from plant protection (crops, vegetables, fruits), veterinary products, and biocides to invertebrate pest control in fish farming. In this review, we address the phenyl-pyrazole fipronil together with neonicotinoids because of similarities in their toxicity, physicochemical profiles, and presence in the environment. Neonicotinoids and fipronil currently account for approximately one third of the world insecticide market; the annual world production of the archetype neonicotinoid, imidacloprid, was estimated to be ca. 20,000 tonnes active substance in 2010. There were several reasons for the initial success of neonicotinoids and fipronil: (1) there was no known pesticide resistance in target pests, mainly because of their recent development, (2) their physicochemical properties included many advantages over previous generations of insecticides (i.e., organophosphates, carbamates, pyrethroids, etc.), and (3) they shared an assumed reduced operator and consumer risk. Due to their systemic nature, they are taken up by the roots or leaves and translocated to all parts of the plant, which, in turn, makes them effectively toxic to herbivorous insects. The toxicity persists for a variable period of time—depending on the plant, its growth stage, and the amount of pesticide applied. A wide variety of applications are available, including the most common prophylactic non-Good Agricultural Practices (GAP) application by seed coating. As a result of their extensive use and physicochemical properties, these substances can be found in all environmental compartments including soil, water, and air. Neonicotinoids and fipronil operate by disrupting neural transmission in the central nervous system of invertebrates. Neonicotinoids mimic the action of neurotransmitters, while fipronil inhibits neuronal receptors. In doing so, they continuously stimulate neurons leading ultimately to death of target invertebrates. Like virtually all insecticides, they can also have lethal and sublethal impacts on non-target organisms, including insect predators and vertebrates. Furthermore, a range of synergistic effects with other stressors have been documented. Here, we review extensively their metabolic pathways, showing how they form both compound-specific and common metabolites which can themselves be toxic. These may result in prolonged toxicity. Considering their wide commercial expansion, mode of action, the systemic properties in plants, persistence and environmental fate, coupled with limited information about the toxicity profiles of these compounds and their metabolites, neonicotinoids and fipronil may entail significant risks to the environment. A global evaluation of the potential collateral effects of their use is therefore timely. The present paper and subsequent chapters in this review of the global literature explore these risks and show a growing body of evidence that persistent, low concentrations of these insecticides pose serious risks of undesirable environmental impacts.

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Environmental fate and exposure; neonicotinoids and fipronil

J-M. Bonmatin, C. Giorio, V. Girolami … (2014)

Systemic insecticides are applied to plants using a wide variety of methods, ranging from foliar sprays to seed treatments and soil drenches. Neonicotinoids and fipronil are among the most widely used pesticides in the world. Their popularity is largely due to their high toxicity to invertebrates, the ease and flexibility with which they can be applied, their long persistence, and their systemic nature, which ensures that they spread to all parts of the target crop. However, these properties also increase the probability of environmental contamination and exposure of nontarget organisms. Environmental contamination occurs via a number of routes including dust generated during drilling of dressed seeds, contamination and accumulation in arable soils and soil water, runoff into waterways, and uptake of pesticides by nontarget plants via their roots or dust deposition on leaves. Persistence in soils, waterways, and nontarget plants is variable but can be prolonged; for example, the half-lives of neonicotinoids in soils can exceed 1,000 days, so they can accumulate when used repeatedly. Similarly, they can persist in woody plants for periods exceeding 1 year. Breakdown results in toxic metabolites, though concentrations of these in the environment are rarely measured. Overall, there is strong evidence that soils, waterways, and plants in agricultural environments and neighboring areas are contaminated with variable levels of neonicotinoids or fipronil mixtures and their metabolites (soil, parts per billion (ppb)-parts per million (ppm) range; water, parts per trillion (ppt)-ppb range; and plants, ppb-ppm range). This provides multiple routes for chronic (and acute in some cases) exposure of nontarget animals. For example, pollinators are exposed through direct contact with dust during drilling; consumption of pollen, nectar, or guttation drops from seed-treated crops, water, and consumption of contaminated pollen and nectar from wild flowers and trees growing near-treated crops. Studies of food stores in honeybee colonies from across the globe demonstrate that colonies are routinely and chronically exposed to neonicotinoids, fipronil, and their metabolites (generally in the 1–100 ppb range), mixed with other pesticides some of which are known to act synergistically with neonicotinoids. Other nontarget organisms, particularly those inhabiting soils, aquatic habitats, or herbivorous insects feeding on noncrop plants in farmland, will also inevitably receive exposure, although data are generally lacking for these groups. We summarize the current state of knowledge regarding the environmental fate of these compounds by outlining what is known about the chemical properties of these compounds, and placing these properties in the context of modern agricultural practices.

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Effects of neonicotinoids and fipronil on non-target invertebrates

L. Pisa, V. Amaral-Rogers, L P Belzunces … (2014)

We assessed the state of knowledge regarding the effects of large-scale pollution with neonicotinoid insecticides and fipronil on non-target invertebrate species of terrestrial, freshwater and marine environments. A large section of the assessment is dedicated to the state of knowledge on sublethal effects on honeybees (Apis mellifera) because this important pollinator is the most studied non-target invertebrate species. Lepidoptera (butterflies and moths), Lumbricidae (earthworms), Apoidae sensu lato (bumblebees, solitary bees) and the section “other invertebrates” review available studies on the other terrestrial species. The sections on freshwater and marine species are rather short as little is known so far about the impact of neonicotinoid insecticides and fipronil on the diverse invertebrate fauna of these widely exposed habitats. For terrestrial and aquatic invertebrate species, the known effects of neonicotinoid pesticides and fipronil are described ranging from organismal toxicology and behavioural effects to population-level effects. For earthworms, freshwater and marine species, the relation of findings to regulatory risk assessment is described. Neonicotinoid insecticides exhibit very high toxicity to a wide range of invertebrates, particularly insects, and field-realistic exposure is likely to result in both lethal and a broad range of important sublethal impacts. There is a major knowledge gap regarding impacts on the grand majority of invertebrates, many of which perform essential roles enabling healthy ecosystem functioning. The data on the few non-target species on which field tests have been performed are limited by major flaws in the outdated test protocols. Despite large knowledge gaps and uncertainties, enough knowledge exists to conclude that existing levels of pollution with neonicotinoids and fipronil resulting from presently authorized uses frequently exceed the lowest observed adverse effect concentrations and are thus likely to have large-scale and wide ranging negative biological and ecological impacts on a wide range of non-target invertebrates in terrestrial, aquatic, marine and benthic habitats.

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Author and article information

Contributors

Junwei (Jerry) Zhu: Role: Subject Editor

Journal

Journal ID (nlm-ta): J Insect Sci

Journal ID (iso-abbrev): J. Insect Sci

Journal ID (publisher-id): jis

Title: Journal of Insect Science

Publisher: Oxford University Press (US )

ISSN (Electronic): 1536-2442

Publication date Collection: July 2020

Publication date (Electronic): 08 August 2020

Publication date PMC-release: 08 August 2020

Volume: 20

Issue: 4

Electronic Location Identifier: 13

Affiliations

[1 ] Department of Entomology, Ohio Agricultural Research and Development Center, The Ohio State University , Wooster, OH

[2 ] Escuela Agrícola Panamericana, El Zamorano , Valle del Yeguare, Francisco Morazán, Honduras

[3 ] USDA-Agricultural Research Service, Horticultural Insects Research Lab , Wooster, OH

[4 ] Center of Applied Plant Sciences, The Ohio State University , Wooster, OH

Author notes

Corresponding author, e-mail: canas.4@ 123456osu.edu

Author information

Christopher M Ranger http://orcid.org/0000-0002-2012-6984

Andrew Michel http://orcid.org/0000-0002-2953-9187

Article

Publisher ID: ieaa070

DOI: 10.1093/jisesa/ieaa070

PMC ID: 7414795

PubMed ID: 32770249

SO-VID: 6245a504-e6ae-4e24-aea6-f9762c692ffe

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

History

Date received : 30 March 2020

Date: 16 June 2020

Page count

Pages: 10

Funding

Funded by: Ohio Agricultural Research and Development Center;

Funded by: Ohio State University, DOI 10.13039/100006928;

Funded by: Escuela Agrícola Panamericana, El Zamorano;

Funded by: U.S. Department of Agriculture, DOI 10.13039/100000199;

Funded by: National Institute of Food and Agriculture, DOI 10.13039/100005825;

Funded by: Agricultural Research Service, DOI 10.13039/100007917;

Award ID: 58-5082-8-018

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Thiamethoxam Differentially Impacts the Survival of the Generalist Predators, Orius insidiosus (Hemiptera: Anthocoridae) and Hippodamia convergens (Coleoptera: Coccinellidae), When Exposed via the Food Chain

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Coleoptera

Most cited references 63

Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites

Environmental fate and exposure; neonicotinoids and fipronil

Effects of neonicotinoids and fipronil on non-target invertebrates

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