Can warming accelerate the decline of Odonata species in experimental paddies due to insecticide fipronil exposure?

Systemic insecticides are one of the causes of Odonata declines in paddy fields. Since rising temperatures associated with global warming can contribute to strengthen pesticide toxicity, insecticide exposures under increasing temperatures may accelerate the decline of Odonata species in the future. However, the combined effects of multiple stressors on Odonata diversity and abundance within ecosystems under various environmental conditions and species interactions are little known. Here, we evaluate the combined effects of the insecticide fipronil and warming on the abundance of Odonata nymphs in experimental paddies. We show that the stand-alone effect of the insecticide exposure caused a significant decrease in abundance of the Odonata community, while nymphs decreased synergistically in the combined treatments with temperature rise in paddy water. However, impacts of each stressor alone were different among species. This study provides experimental evidence that warming could accelerate a reduction in abundance of the Odonata community exposed to insecticides (synergistic effect), although the strength of that effect might vary with the community composition in targeted habitats, due mainly to different susceptibilities among species to each stressor. Community-based monitoring in actual fields is deemed necessary for a realistic evaluation of the combined effects of multiple stressors on biodiversity.

Global warming intensifies the interference competition by a poleward-expanding invader on a native dragonfly species.

Rapid climate warming has boosted biological invasions and the distribution or expansion polewards of many species: this can cause serious impacts on local ecosystems within the invaded areas. Subsequently, native species may be exposed to threats of both interspecific competition with invaders and temperature rises. However, effects of warming on interspecific interactions, especially competition between invader and native species remains unclear. To better understand the combined threats of biological invasions and warming, the effect of temperature on competitive interactions between two dragonfly species, the expanding Trithemis aurora from Southeast Asia and the Japanese native Orthetrum albistylum speciosum were assessed based on their foraging capacity. Although the stand-alone effect of temperature on foraging intake of the native dragonfly was not apparent, its intake significantly decreased with increasing temperatures when the invader T. aurora was present. Such reductions in foraging might lead to displacement of the native species through competition for food resources. This suggests that impacts of invader species against native species are expected to be more severe when interspecific competition is exacerbated by temperature rises.

Indirect Effect of Pesticides on Insects and Other Arthropods.

Pesticides released to the environment can indirectly affect target and non-target species in ways that are often contrary to their intended use. Such indirect effects are mediated through direct impacts on other species or the physical environment and depend on ecological mechanisms and species interactions. Typical mechanisms are the release of herbivores from predation and release from competition among species with similar niches. Application of insecticides to agriculture often results in subsequent pest outbreaks due to the elimination of natural enemies. The loss of floristic diversity and food resources that result from herbicide applications can reduce populations of pollinators and natural enemies of crop pests. In aquatic ecosystems, insecticides and fungicides often induce algae blooms as the chemicals reduce grazing by zooplankton and benthic herbivores. Increases in periphyton biomass typically result in the replacement of arthropods with more tolerant species such as snails, worms and tadpoles. Fungicides and systemic insecticides also reduce nutrient recycling by impairing the ability of detritivorous arthropods. Residues of herbicides can reduce the biomass of macrophytes in ponds and wetlands, indirectly affecting the protection and breeding of predatory insects in that environment. The direct impacts of pesticides in the environment are therefore either amplified or compensated by their indirect effects.

An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 1: new molecules, metabolism, fate, and transport.

With the exponential number of published data on neonicotinoids and fipronil during the last decade, an updated review of literature has been conducted in three parts. The present part focuses on gaps of knowledge that have been addressed after publication of the Worldwide Integrated Assessment (WIA) on systemic insecticides in 2015. More specifically, new data on the mode of action and metabolism of neonicotinoids and fipronil, and their toxicity to invertebrates and vertebrates, were obtained. We included the newly detected synergistic effects and/or interactions of these systemic insecticides with other insecticides, fungicides, herbicides, adjuvants, honeybee viruses, and parasites of honeybees. New studies have also investigated the contamination of all environmental compartments (air and dust, soil, water, sediments, and plants) as well as bees and apicultural products, food and beverages, and the exposure of invertebrates and vertebrates to such contaminants. Finally, we review new publications on remediation of neonicotinoids and fipronil, especially in water systems. Conclusions of the previous WIA in 2015 are reinforced; neonicotinoids and fipronil represent a major threat worldwide for biodiversity, ecosystems, and all the services the latter provide.

An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: impacts on organisms and ecosystems.

New information on the lethal and sublethal effects of neonicotinoids and fipronil on organisms is presented in this review, complementing the previous Worldwide Integrated Assessment (WIA) in 2015. The high toxicity of these systemic insecticides to invertebrates has been confirmed and expanded to include more species and compounds. Most of the recent research has focused on bees and the sublethal and ecological impacts these insecticides have on pollinators. Toxic effects on other invertebrate taxa also covered predatory and parasitoid natural enemies and aquatic arthropods. Little new information has been gathered on soil organisms. The impact on marine and coastal ecosystems is still largely uncharted. The chronic lethality of neonicotinoids to insects and crustaceans, and the strengthened evidence that these chemicals also impair the immune system and reproduction, highlights the dangers of this particular insecticidal class (neonicotinoids and fipronil), with the potential to greatly decrease populations of arthropods in both terrestrial and aquatic environments. Sublethal effects on fish, reptiles, frogs, birds, and mammals are also reported, showing a better understanding of the mechanisms of toxicity of these insecticides in vertebrates and their deleterious impacts on growth, reproduction, and neurobehaviour of most of the species tested. This review concludes with a summary of impacts on the ecosystem services and functioning, particularly on pollination, soil biota, and aquatic invertebrate communities, thus reinforcing the previous WIA conclusions (van der Sluijs et al. 2015).

An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 3: alternatives to systemic insecticides.

Over-reliance on pesticides for pest control is inflicting serious damage to the environmental services that underpin agricultural productivity. The widespread use of systemic insecticides, neonicotinoids, and the phenylpyrazole fipronil in particular is assessed here in terms of their actual use in pest management, effects on crop yields, and the development of pest resistance to these compounds in many crops after two decades of usage. Resistance can only be overcome in the longterm by implementing methods that are not exclusively based on synthetic pesticides. A diverse range of pest management tactics is already available, all of which can achieve efficient pest control below the economic injury level while maintaining the productivity of the crops. A novel insurance method against crop failure is shown here as an example of alternative methods that can protect farmer's crops and their livelihoods without having to use insecticides. Finally, some concluding remarks about the need for a new framework for a truly sustainable agriculture that relies mainly on natural ecosystem services instead of chemicals are included; this reinforcing the previous WIA conclusions (van der Sluijs et al. Environ Sci Pollut Res 22:148-154, 2015).

Residues of neonicotinoids in soil, water and people's hair: A case study from three agricultural regions of the Philippines.

Synthetic pesticides such as neonicotinoids are commonly used to treat crops in tropical regions, where data on environmental and human contamination are patchy and make it difficult to assess to what extent pesticides may harm human health, especially in less developed countries. To assess the degree of environmental and human contamination with neonicotinoids we collected soil, water and people's hair in three agricultural regions of the Philippines and analysed them by ultra-high performance liquid chromatography coupled to tandem mass spectrometry (UHPLC-MS-MS). Five neonicotinoids, namely acetamiprid, clothianidin, imidacloprid, thiacloprid and thiamethoxam were targeted. Residues of neonicotinoids were found in 78% of 67 soil samples from the three provinces. Total neonicotinoid loads ranged on average between 0.017 and 0.89 µg/kg in soils of rice, banana and vegetable crops, and were 130 times higher (113.5 µg/kg) in soils of a citrus grove. Imidacloprid was the most prevalent compound at an average of 0.56 µg/kg in soil while thiacloprid was below the limit of detection. Half of the eight water samples from a rice field and nearby creek contained residues of imidacloprid (mean 1.29 ng/L) and one contained thiamethoxam (0.15 ng/L). Residues of neonicotinoids were found in 81% of 99 samples of people's hair from the surveyed regions (average total concentrations 0.14 to 1.18 ng/g, maximum 350 ng/g). Hair residue levels correlated well with the concentrations of thiamethoxam and total residues in soils from the same locality (r = 0.98). The presence of thiacloprid in 15% of the hair samples but not in soil samples suggests an additional route of exposure among people, which is most likely to be through ingestion of agricultural food and drinks available in the market.

Resolving the twin human and environmental health hazards of a plant-based diet.

Food can be health-giving. A global transition towards plant-based diets may equally help curb carbon emissions, slow land-system change and conserve finite resources. Yet, projected benefits of such 'planetary health' diets imperfectly capture the environmental or societal health outcomes tied to food production. Here, we examine pesticide-related hazards of fruit and vegetable consumption, and list proven management alternatives per commodity, geography and chemical compound. Across countries, pesticide use in these alleged healthful foods is extensive with up to 97% food items containing residues and up to 42% posing dietary risks to consumers. Multiple residues are present in 70-92% of US- and China-grown stone fruit while 58% US cauliflower is tainted with neonicotinoid insecticides. Science-based alternatives and decision-support frameworks can help food producers reduce risks and potential harm by deliberately abstaining from pesticide use. As such, opportunities abound to advance 'win-win' diets that simultaneously nurture human health and conserve global biodiversity.

Time-Cumulative Toxicity of Neonicotinoids: Experimental Evidence and Implications for Environmental Risk Assessments.

Our mechanistic understanding of the toxicity of chemicals that target biochemical and/or physiological pathways, such as pesticides and medical drugs is that they do so by binding to specific molecules. The nature of the latter molecules (e.g., enzymes, receptors, DNA, proteins, etc.) and the strength of the binding to such chemicals elicit a toxic effect in organisms, which magnitude depends on the doses exposed in a given timeframe. While dose and time of exposure are critical factors determining the toxicity of pesticides, different types of chemicals behave differently. Experimental evidence demonstrates that the toxicity of neonicotinoids increases with exposure time as much as with the dose, and therefore it has been described as time-cumulative toxicity. Examples for aquatic and terrestrial organisms are shown here. This pattern of toxicity, also found among carcinogenic compounds and other toxicants, has been ignored in ecotoxicology and risk assessments for a long time. The implications of the time-cumulative toxicity of neonicotinoids on non-target organisms of aquatic and terrestrial environments are far reaching. Firstly, neonicotinoids are incompatible with integrated pest management (IPM) approaches and secondly regulatory assessments for this class of compounds cannot be based solely on exposure doses but need also to take into consideration the time factor.

Effects of a herbicide on paddy predatory insects depend on their microhabitat use and an insecticide application.

Indirect effects of agrochemicals on organisms via biotic interactions are less studied than direct chemical toxicity despite their potential relevance in agricultural landscapes. In particular, the role of species traits in characterizing indirect effects of pesticides has been largely overlooked. Moreover, it is still unclear whether such indirect effects on organisms are prevalent even when the organisms are exposed to direct toxicity. We conducted a mesocosm experiment to examine indirect effects of a herbicide (pentoxazone) on aquatic predatory insects of rice paddies. Because the herbicide selectively controls photosynthetic organisms, we assumed that the effects of the herbicide on predatory insects would be indirect. We hypothesized that phytophilous predators such as some Odonata larvae, which cling to aquatic macrophytes, would be more subject to negative indirect effects of the herbicide through a decrease in abundance of aquatic macrophytes than benthic, nektonic, and neustonic predators. Also, we crossed-applied an insecticide (fipronil) with herbicide application to examine whether the indirect effects of the herbicide on the assembling predators act additively with direct adverse effects of the insecticide. The herbicide application did not decrease the abundance of phytoplankton constitutively, and there were no clear negative impacts of the herbicide on zooplankton and prey insects (detritivores and herbivores). However, the abundance of aquatic macrophytes was significantly decreased by the herbicide application. Although indirect effects of the herbicide were not so strong on most predators, their magnitude and sign differed markedly among predator species. In particular, the abundance of phytophilous predators was more likely to decrease than that of benthic, nektonic, and neustonic predators when the herbicide was applied. However, these indirect effects of the herbicide could not be detected when the insecticide was also applied, seemingly due to fipronil's high lethal toxicity. Our study highlights the importance of species traits such as microhabitat use, which characterize biotic interactions, for predicting indirect effects of agrochemicals. Given that indirect effects of the chemicals vary in response to species traits and direct toxicity of other chemicals, efforts to explain this variation are needed to predict the realistic risks of indirect effects of agrochemicals in nature.

A survey and risk assessment of neonicotinoids in water, soil and sediments of Belize.

Usage of neonicotinoids is common in all agricultural regions of the world but data on environmental contamination in tropical regions is scarce. We conducted a survey of five neonicotinoids in soil, water and sediment samples along gradients from crops fields to protected lowland tropical forest, mangroves and wetlands in northern Belize, a region of high biodiversity value. Neonicotinoid frequency of detection and concentrations were highest in soil (68%) and lowest in water (12%). Imidacloprid was the most common residue reaching a maximum of 17.1 ng/g in soil samples. Concentrations in soils differed among crop types, being highest in melon fields and lowest in banana and sugarcane fields. Residues in soil declined with distance to the planted fields, with clothianidin being detected at 100 m and imidacloprid at more than 10 km from the nearest applied field. About half (47%) of the sediments collected contained residues of at least one compound up to 10 km from the source. Total neonicotinoid concentrations in sediments (range 0.014-0.348 ng/g d. w.) were about 10 times lower than in soils from the fields, with imidacloprid being the highest (0.175 ng/g). A probabilistic risk assessment of the residues in the aquatic environment indicates that 31% of sediment samples pose a risk to invertebrate aquatic and benthic organisms by chronic exposure, whereas less than 5% of sediment samples may incur a risk by acute exposure. Current residue levels in water samples do not appear to pose risks to the aquatic fauna. Fugacity modeling of the four main compounds detected suggest that most of the dissipation from the agricultural fields occurs via runoff and leaching through the porous soils of this region. We call for better monitoring of pesticide contamination and invertebrate inventories and finding alternatives to the use of neonicotinoids in agriculture.

Host-Tree Selection by the Invasive Argentine Ant (Hymenoptera: Formicidae) in Relation to Honeydew-Producing Insects.

The Argentine ant, Linepithema humile (Mayr; Hymenoptera: Formicidae), is one of the world's most hazardous invasive species, and thus its eradication from Japan is important. Physical and chemical controls can be expensive and cause strong adverse effects on local terrestrial ecosystems regardless of their high efficacy. Here, presence/absence of host-tree selection by Argentine ants was investigated to understand the ant-honeydew-producing insects interactions in order to develop new cultural controls compatible with biodiversity conservation. Abundance of Argentine ants and their tree utilization ratio was measured among dominant roadside trees (Cinnamomum camphora, Myrica rubra, Nerium indicum, Rhaphiolepis indica var. umbellata, Juniperus chinensis var. kaizuka) in two areas around Kobe, Japan. Almost all ants collected were Argentine ants suggesting that native ants would have been competitively excluded. Tree utilization of Argentine ants clearly differed among host trees. Abundance of both Argentine ants and honeydew-producing insects and tree utilization rate of the ants were significantly lower in especially C. camphora and J. chinensis. Few Argentine ants were observed trailing on C. camphora, J. Chinensis, and N. indicum, most probably due to low abundance of honeydew-producing insects on these trees with the toxic and repellent chemical components. On the other hand, high abundance of both Argentine ants and homopterans were found in M. rubra and especially R. indica. We suggest that reductions of R. indica and M. rubra would lead to a decrease in abundance of honeydew-producing insects, and thus effectively control populations of Argentine ants. At the same time, planting of C. camphora, J. Chinensis, and N. indicum may also play a role in restraint efficacy against invasion of the invasive ants.

Lethal and sublethal effects, and incomplete clearance of ingested imidacloprid in honey bees (Apis mellifera).

A previous study claimed a differential behavioural resilience between spring or summer honey bees (Apis mellifera) and bumble bees (Bombus terrestris) after exposure to syrup contaminated with 125 µg L-1 imidacloprid for 8 days. The authors of that study based their assertion on the lack of body residues and toxic effects in honey bees, whereas bumble bees showed body residues of imidacloprid and impaired locomotion during the exposure. We have reproduced their experiment using winter honey bees subject to the same protocol. After exposure to syrup contaminated with 125 µg L-1 imidacloprid, honey bees experienced high mortality rates (up to 45%), had body residues of imidacloprid in the range 2.7-5.7 ng g-1 and exhibited abnormal behaviours (restless, apathetic, trembling and falling over) that were significantly different from the controls. There was incomplete clearance of the insecticide during the 10-day exposure period. Our results contrast with the findings reported in the previous study for spring or summer honey bees, but are consistent with the results reported for the other bee species.

Dose-response analysis indicating time-dependent neurotoxicity caused by organic and inorganic mercury-Implications for toxic effects in the developing brain.

A latency period preceding neurotoxicity is a common characteristic in the dose-response relationship induced by organic mercury. Latency periods have typically been observed with genotoxicants in carcinogenesis, with cancer being manifested a long time after the initiating event. These observations indicate that even a very small dose may cause extensive adverse effects later in life, so the toxicity of the genotoxic compound is dose and time-dependent. In children, methylmercury exposure during pregnancy (in utero) has been associated with delays in reaching developmental milestones (e.g., age at first walking) and decreases in intelligence, increasing in severity with increasing exposure. Ethylmercury exposure from thimerosal in some vaccines has been associated, in some studies, with autism and other neurological disorders in children. In this paper, we have examined whether dose-response data from in vitro and in vivo organic mercury toxicity studies fit the Druckrey-Küpfmüller equation c·t(n)=constant (c=exposure concentration, t=latency period), first established for genotoxic carcinogens, and whether or not irreversible effects are enhanced by time of exposure (n≥1), or else toxic effects are dose-dependent while time has only minor influence on the adverse outcome (n<1). The mode of action underlying time-dependent toxicity is irreversible binding to critical receptors causing adverse and cumulative effects. The results indicate that the Druckrey-Küpfmüller equation describes well the dose-response characteristics of organic mercury induced neurotoxic effects. This amounts to a paradigm shift in chemical risk assessment of mercurial compounds and highlights that it is vital to perform toxicity testing geared to investigate time-dependent effects.

Are bee diseases linked to pesticides? - A brief review.

The negative impacts of pesticides, in particular insecticides, on bees and other pollinators have never been disputed. Insecticides can directly kill these vital insects, whereas herbicides reduce the diversity of their food resources, thus indirectly affecting their survival and reproduction. At sub-lethal level (

Different acute toxicity of fipronil baits on invasive Linepithema humile supercolonies and some non-target ground arthropods.

Fipronil is one of the most effective insecticides to control the invasive ant Linepithema humile, but its effectiveness has been assessed without considering the genetic differences among L. humile supercolonies. We hypothesized that the susceptibility of the ant to fipronil might differ among supercolonies. If so, dosage and concentration of fipronil may need to be adjusted for effective eradication of each supercolony. The relative sensitivities of four L. humile supercolonies established in Hyogo (Japan) to fipronil baits were examined based on their acute toxicity (48-h LC(50)). Toxicities of fipronil to seven ground arthropods, including four native ant species, one native isopoda, and two cockroaches were also determined and compared to that of L. humile supercolonies using species sensitivity distributions. Marked differences in susceptibility of fipronil were apparent among the supercolonies (P < 0.008), with the 'Japanese main supercolony' (271 µg L(-1)) being five to ten times more sensitive to fipronil than other colonies (1183-2782 µg L(-1)). Toxicities to non-target species (330-2327 µg L(-1)) were in the same range as that of L. humile, and SSDs between the two species groups were not significantly different (t = -1.389, P = 0.180), suggesting that fipronil's insecticidal activity is practically the same for L. humile as for non-target arthropods. Therefore, if the invasive ant is to be controlled using fipronil, this would also affect the local arthropod biodiversity. Only the 'Japanese main supercolony' can be controlled with appropriate bait dosages of fipronil that would have little impact on the other species.

Neonicotinoid contamination of global surface waters and associated risk to aquatic invertebrates: a review.

Neonicotinoids, broad-spectrum systemic insecticides, are the fastest growing class of insecticides worldwide and are now registered for use on hundreds of field crops in over 120 different countries. The environmental profile of this class of pesticides indicate that they are persistent, have high leaching and runoff potential, and are highly toxic to a wide range of invertebrates. Therefore, neonicotinoids represent a significant risk to surface waters and the diverse aquatic and terrestrial fauna that these ecosystems support. This review synthesizes the current state of knowledge on the reported concentrations of neonicotinoids in surface waters from 29 studies in 9 countries world-wide in tandem with published data on their acute and chronic toxicity to 49 species of aquatic insects and crustaceans spanning 12 invertebrate orders. Strong evidence exists that water-borne neonicotinoid exposures are frequent, long-term and at levels (geometric means=0.13µg/L (averages) and 0.63µg/L (maxima)) which commonly exceed several existing water quality guidelines. Imidacloprid is by far the most widely studied neonicotinoid (66% of the 214 toxicity tests reviewed) with differences in sensitivity among aquatic invertebrate species ranging several orders of magnitude; other neonicotinoids display analogous modes of action and similar toxicities, although comparative data are limited. Of the species evaluated, insects belonging to the orders Ephemeroptera, Trichoptera and Diptera appear to be the most sensitive, while those of Crustacea (although not universally so) are less sensitive. In particular, the standard test species Daphnia magna appears to be very tolerant, with 24-96hour LC50 values exceeding 100,000µg/L (geometric mean>44,000µg/L), which is at least 2-3 orders of magnitude higher than the geometric mean of all other invertebrate species tested. Overall, neonicotinoids can exert adverse effects on survival, growth, emergence, mobility, and behavior of many sensitive aquatic invertebrate taxa at concentrations at or below 1µg/L under acute exposure and 0.1µg/L for chronic exposure. Using probabilistic approaches (species sensitivity distributions), we recommend here that ecological thresholds for neonicotinoid water concentrations need to be below 0.2µg/L (short-term acute) or 0.035µg/L (long-term chronic) to avoid lasting effects on aquatic invertebrate communities. The application of safety factors may still be warranted considering potential issues of slow recovery, additive or synergistic effects and multiple stressors that can occur in the field. Our analysis revealed that 81% (22/27) and 74% (14/19) of global surface water studies reporting maximum and average individual neonicotinoid concentrations respectively, exceeded these thresholds of 0.2 and 0.035µg/L. Therefore, it appears that environmentally relevant concentrations of neonicotinoids in surface waters worldwide are well within the range where both short- and long-term impacts on aquatic invertebrate species are possible over broad spatial scales.