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      Extremely low neonicotinoid doses alter navigation of pest insects along pheromone plumes

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          Abstract

          The prevailing use of neonicotinoids in pest control has adverse effects on non-target organisms, like honeybees. However, relatively few studies have explored the effect of sublethal neonicotinoid levels on olfactory responses of pest insects, and thus their potential impact on semiochemical surveillance and control methods, such as monitoring or mating disruption. We recently reported that sublethal doses of the neonicotinoid thiacloprid (TIA) had dramatic effects on sex pheromone release in three tortricid moth species. We present now effects of TIA on pheromone detection and, for the first time, navigational responses of pest insects to pheromone sources. TIA delayed and reduced the percentage of males responding in the wind tunnel without analogous alteration of electrophysiological antennal responses. During navigation along an odor plume, treated males exhibited markedly slower flights and, in general, described narrower flight tracks, with an increased susceptibility to wind-induced drift. All these effects increased in a dose-dependent manner starting at LC 0.001 - which would kill just 10 out of 10 6 individuals - and revealed an especially pronounced sensitivity in one of the species, Grapholita molesta. Our results suggest that minimal neonicotinoid quantities alter chemical communication, and thus could affect the efficacy of semiochemical pest management methods.

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          Most cited references45

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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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            Sex pheromones and their impact on pest management.

            The idea of using species-specific behavior-modifying chemicals for the management of noxious insects in agriculture, horticulture, forestry, stored products, and for insect vectors of diseases has been a driving ambition through five decades of pheromone research. Hundreds of pheromones and other semiochemicals have been discovered that are used to monitor the presence and abundance of insects and to protect plants and animals against insects. The estimated annual production of lures for monitoring and mass trapping is on the order of tens of millions, covering at least 10 million hectares. Insect populations are controlled by air permeation and attract-and-kill techniques on at least 1 million hectares. Here, we review the most important and widespread practical applications. Pheromones are increasingly efficient at low population densities, they do not adversely affect natural enemies, and they can, therefore, bring about a long-term reduction in insect populations that cannot be accomplished with conventional insecticides. A changing climate with higher growing season temperatures and altered rainfall patterns makes control of native and invasive insects an increasingly urgent challenge. Intensified insecticide use will not provide a solution, but pheromones and other semiochemicals instead can be implemented for sustainable area-wide management and will thus improve food security for a growing population. Given the scale of the challenges we face to mitigate the impacts of climate change, the time is right to intensify goal-oriented interdisciplinary research on semiochemicals, involving chemists, entomologists, and plant protection experts, in order to provide the urgently needed, and cost-effective technical solutions for sustainable insect management worldwide.
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              Mechanisms of animal navigation in odor plumes.

              N Vickers (2000)
              Chemical signals mediate many of life's processes. For organisms that use these signals to orient and navigate in their environment, where and when these cues are encountered is crucial in determining behavioral responses. In air and water, fluid mechanics impinge directly upon the distribution of odorous molecules in time and space. Animals frequently employ behavioral mechanisms that allow them to take advantage of both chemical and fluid dynamic information in order to move toward the source. In turbulent plumes, where odor is patchily distributed, animals are exposed to a highly intermittent signal. The most detailed studies that have attempted to measure fluid dynamic conditions, odor plume structure, and resultant orientation behavior have involved moths, crabs, and lobsters. The behavioral mechanisms employed by these organisms are different but generally integrate some form of chemically modulated orientation (chemotaxis) with a visual or mechanical assessment of flow conditions in order to steer up-current or upwind (rheo- or anemo-taxis, respectively). Across-stream turns are another conspicuous feature of odor-modulated tracks of a variety of organisms in different fluid conditions. In some cases, turning is initiated by detection of the lateral edges of a well-defined plume (crabs), whereas in other animals turning appears to be steered according to an internally generated program modulated by odor contacts (moth counterturning). Other organisms such as birds and fish may use similar mechanisms, but the experimental data for these organisms is not yet as convincing. The behavioral strategies employed by a variety of animals result in orientation responses that are appropriate for the dispersed, intermittent plumes dictated by the fluid-mechanical conditions in the environments that these different macroscopic organisms inhabit.
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                Author and article information

                Contributors
                cesar.gemeno@pvcf.udl.cat
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                31 May 2019
                31 May 2019
                2019
                : 9
                : 8150
                Affiliations
                [1 ]ISNI 0000 0001 2163 1432, GRID grid.15043.33, Department of Crop and Forest Sciences, , University of Lleida (UdL), ; 25198 Lleida, Spain
                [2 ]GRID grid.440820.a, Department of Biosciences, , University of Vic – Central University of Catalonia, ; 08500 Vic, Spain
                Author information
                http://orcid.org/0000-0002-0371-2455
                http://orcid.org/0000-0002-9231-2356
                http://orcid.org/0000-0001-5543-6141
                Article
                44581
                10.1038/s41598-019-44581-w
                6544627
                31148562
                172adc98-588a-4238-8535-f11ac49f7fbc
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 17 January 2019
                : 15 May 2019
                Funding
                Funded by: Funder: MINECO (Ministerio de Economía y Competitividad Spain) Grant number: AGL2013-49164-C2-1
                Categories
                Article
                Custom metadata
                © The Author(s) 2019

                Uncategorized
                behavioural ecology,agroecology
                Uncategorized
                behavioural ecology, agroecology

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