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      Were the sharp declines of dragonfly populations in the 1990s in Japan caused by fipronil and imidacloprid? An analysis of Hill’s causality for the case of Sympetrum frequens

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          Abstract

          Neonicotinoids and fipronil are the most widely used insecticides in the world. Previous studies showed that these compounds have high toxicity to a wide taxonomic range of non-target invertebrates. In rice cultivation, they are frequently used for nursery-box treatment of rice seedlings. The use of fipronil and neonicotinoid imidacloprid is suspected to be the main cause of population declines of red dragonflies, in particular Sympetrum frequens, because they have high lethal toxicity to dragonfly nymphs and the timing of the insecticides’ introduction in Japan (i.e., the late 1990s) overlapped with the sharp population declines. However, a causal link between application of these insecticides and population declines of the dragonflies remains unclear. Therefore, we estimated the amount of the insecticides applied for nursery-box treatment of rice seedlings and analyzed currently available information to evaluate the causality between fipronil and imidacloprid usage and population decline of S. frequens using Hill’s causality criteria. Based on our scoring of Hill’s nine criteria, the strongest lines of evidence were strength, plausibility, and coherence, whereas the weakest were temporality and biological gradient. We conclude that the use of these insecticides, particularly fipronil, was a major cause of the declines of S. frequens in Japan in the 1990s, with a high degree of certainty. The existing information and our analyses, however, do not allow us to exclude the possibility that some agronomic practices (e.g., midsummer drainage or crop rotation) that can severely limit the survival of aquatic nymphs also played a role in the dragonfly’s decline.

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

          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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            Causation and causal inference in epidemiology.

            Concepts of cause and causal inference are largely self-taught from early learning experiences. A model of causation that describes causes in terms of sufficient causes and their component causes illuminates important principles such as multi-causality, the dependence of the strength of component causes on the prevalence of complementary component causes, and interaction between component causes. Philosophers agree that causal propositions cannot be proved, and find flaws or practical limitations in all philosophies of causal inference. Hence, the role of logic, belief, and observation in evaluating causal propositions is not settled. Causal inference in epidemiology is better viewed as an exercise in measurement of an effect rather than as a criterion-guided process for deciding whether an effect is present or not.
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              Effects of neonicotinoids and fipronil on non-target invertebrates

              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
                +81-29-850-2144 , nakanishi.kosuke@nies.go.jp
                Journal
                Environ Sci Pollut Res Int
                Environ Sci Pollut Res Int
                Environmental Science and Pollution Research International
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                0944-1344
                1614-7499
                20 October 2018
                20 October 2018
                2018
                : 25
                : 35
                : 35352-35364
                Affiliations
                ISNI 0000 0001 0746 5933, GRID grid.140139.e, National Institute for Environmental Studies, ; Onogawa 16-2, Tsukuba, Ibaraki, 305-8506 Japan
                Author notes

                Responsible editor: Philippe Garrigues

                Author information
                http://orcid.org/0000-0002-7530-7141
                Article
                3440
                10.1007/s11356-018-3440-x
                6280840
                30343370
                49fccc16-d417-46ea-958b-6ad0943273af
                © The Author(s) 2018

                Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 23 May 2018
                : 10 October 2018
                Funding
                Funded by: Environment Research and Technology Development Fund
                Award ID: 4-1701
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2018

                General environmental science
                agrochemicals,neonicotinoid,nursery box,paddy fields,pesticides,phenylpyrazole,rice fields,odonata

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