Christy A. Morrissey

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 The data on the few non-target species on which field tests have been performed are limited by major flaws in the outdated test protocols.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.

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.

A review of the direct and indirect effects of neonicotinoids and fipronil on vertebrate wildlife

Concerns over the role of pesticides affecting vertebrate wildlife populations have recently focussed on systemic products which exert broad-spectrum toxicity. Given that the neonicotinoids have become the fastest-growing class of insecticides globally, we review here 150 studies of their direct (toxic) and indirect (e.g. food chain) effects on vertebrate wildlife—mammals, birds, fish, amphibians and reptiles. We focus on two neonicotinoids, imidacloprid and clothianidin, and a third insecticide, fipronil, which also acts in the same systemic manner. Imidacloprid and fipronil were found to be toxic to many birds and most fish, respectively. All three insecticides exert sub-lethal effects, ranging from genotoxic and cytotoxic effects, and impaired immune function, to reduced growth and reproductive success, often at concentrations well below those associated with mortality. Use of imidacloprid and clothianidin as seed treatments on some crops poses risks to small birds, and ingestion of even a few treated seeds could cause mortality or reproductive impairment to sensitive bird species. In contrast, environmental concentrations of imidacloprid and clothianidin appear to be at levels below those which will cause mortality to freshwater vertebrates, although sub-lethal effects may occur. Some recorded environmental concentrations of fipronil, however, may be sufficiently high to harm fish. Indirect effects are rarely considered in risk assessment processes and there is a paucity of data, despite the potential to exert population-level effects. Our research revealed two field case studies of indirect effects. In one, reductions in invertebrate prey from both imidacloprid and fipronil uses led to impaired growth in a fish species, and in another, reductions in populations in two lizard species were linked to effects of fipronil on termite prey. Evidence presented here suggests that the systemic insecticides, neonicotinoids and fipronil, are capable of exerting direct and indirect effects on terrestrial and aquatic vertebrate wildlife, thus warranting further review of their environmental safety.

Widespread Use and Frequent Detection of Neonicotinoid Insecticides in Wetlands of Canada's Prairie Pothole Region

Neonicotinoids currently dominate the insecticide market as seed treatments on Canadas major Prairie crops (e.g., canola). The potential impact to ecologically significant wetlands in this dominantly agro-environment has largely been overlooked while the distribution of use, incidence and level of contamination remains unreported. We modelled the spatial distribution of neonicotinoid use across the three Prairie Provinces in combination with temporal assessments of water and sediment concentrations in wetlands to measure four active ingredients (clothianidin, thiamethoxam, imidacloprid and acetamiprid). From 2009 to 2012, neonicotinoid use was increasing; by 2012, applications covered an estimated ∼11 million hectares (44% of Prairie cropland) with >216,000 kg of active ingredients. Thiamethoxam, followed by clothianidin, were the dominant seed treatments by mass and area. Areas of high neonicotinoid use were identified as high density canola or soybean production. Water sampled four times from 136 wetlands (spring, summer, fall 2012 and spring 2013) across four rural municipalities in Saskatchewan similarly revealed clothianidin and thiamethoxam in the majority of samples. In spring 2012 prior to seeding, 36% of wetlands contained at least one neonicotinoid. Detections increased to 62% in summer 2012, declined to 16% in fall, and increased to 91% the following spring 2013 after ice-off. Peak concentrations were recorded during summer 2012 for both thiamethoxam (range: <LOQ - 1490 ng/L, canola) and clothianidin (range: <LOQ – 3110 ng/L, canola). Sediment samples collected during the same period rarely (6%) contained neonicotinoid concentrations (which did not exceed 20 ng/L). Wetlands situated in barley, canola and oat fields consistently contained higher mean concentrations of neonicotinoids than in grasslands, but no individual crop singularly influenced overall detections or concentrations. Distribution maps indicate neonicotinoid use is increasing and becoming more widespread with concerns for environmental loading, while frequently detected neonicotinoid concentrations in Prairie wetlands suggest high persistence and transport into wetlands.

Risks of large-scale use of systemic insecticides to ecosystem functioning and services

Large-scale use of the persistent and potent neonicotinoid and fipronil insecticides has raised concerns about risks to ecosystem functions provided by a wide range of species and environments affected by these insecticides. The concept of ecosystem services is widely used in decision making in the context of valuing the service potentials, benefits, and use values that well-functioning ecosystems provide to humans and the biosphere and, as an endpoint (value to be protected), in ecological risk assessment of chemicals. Neonicotinoid insecticides are frequently detected in soil and water and are also found in air, as dust particles during sowing of crops and aerosols during spraying. These environmental media provide essential resources to support biodiversity, but are known to be threatened by long-term or repeated contamination by neonicotinoids and fipronil. We review the state of knowledge regarding the potential impacts of these insecticides on ecosystem functioning and services provided by terrestrial and aquatic ecosystems including soil and freshwater functions, fisheries, biological pest control, and pollination services. Empirical studies examining the specific impacts of neonicotinoids and fipronil to ecosystem services have focused largely on the negative impacts to beneficial insect species (honeybees) and the impact on pollination service of food crops. However, here we document broader evidence of the effects on ecosystem functions regulating soil and water quality, pest control, pollination, ecosystem resilience, and community diversity. In particular, microbes, invertebrates, and fish play critical roles as decomposers, pollinators, consumers, and predators, which collectively maintain healthy communities and ecosystem integrity. Several examples in this review demonstrate evidence of the negative impacts of systemic insecticides on decomposition, nutrient cycling, soil respiration, and invertebrate populations valued by humans. Invertebrates, particularly earthworms that are important for soil processes, wild and domestic insect pollinators which are important for plant and crop production, and several freshwater taxa which are involved in aquatic nutrient cycling, were all found to be highly susceptible to lethal and sublethal effects of neonicotinoids and/or fipronil at environmentally relevant concentrations. By contrast, most microbes and fish do not appear to be as sensitive under normal exposure scenarios, though the effects on fish may be important in certain realms such as combined fish-rice farming systems and through food chain effects. We highlight the economic and cultural concerns around agriculture and aquaculture production and the role these insecticides may have in threatening food security. Overall, we recommend improved sustainable agricultural practices that restrict systemic insecticide use to maintain and support several ecosystem services that humans fundamentally depend on.

Conclusions of the Worldwide Integrated Assessment on the risks of neonicotinoids and fipronil to biodiversity and ecosystem functioning

The side effects of the current global use of pesticides on wildlife, particularly at higher levels of biological organization: populations, communities and ecosystems, are poorly understood (Kohler and Triebskorn 2013). Here, we focus on one of the problematic groups of agrochemicals, the systemic insecticides fipronil and those of the neonicotinoid family. The increasing global reliance on the partly prophylactic use of these persistent and potent neurotoxic systemic insecticides has raised concerns about their impacts on biodiversity, ecosystem functioning and ecosystem services provided by a wide range of affected species and environments. The present scale of use, combined with the properties of these compounds, has resulted in widespread contamination of agricultural soils, freshwater resources, wetlands, non-target vegetation and estuarine and coastal marine systems, which means that many organisms inhabiting these habitats are being repeatedly and chronically expose...

Assessing trace‐metal exposure to American dippers in mountain streams of southwestern British Columbia, Canada

To develop a suitable biomonitor of metal pollution in watersheds, we examined trends in exposure to nine trace elements in the diet (benthic invertebrates and fish), feathers (n = 104), and feces (n = 14) of an aquatic passerine, the American dipper (Cinclus mexicanus), from the Chilliwack watershed in British Columbia, Canada. We hypothesized that key differences may exist in exposure to metals for resident dippers that occupy the main river year-round and altitudinal migrants that breed on higher elevation tributaries because of differences in prey metal levels between locations or possible differences in diet composition. Metals most commonly detected in dipper feather samples in decreasing order were Zn > Cu > Hg > Se > Pb > Mn > Cd > Al > As. Resident dipper feathers contained significantly higher mean concentrations of mercury (0.64 microg/g dry wt), cadmium (0.19 microg/g dry wt), and copper (10.8 microg/g dry wt) relative to migrants. Mass balance models used to predict daily metal exposure for dippers with different diets and breeding locations within a watershed showed that variation in metal levels primarily was attributed to differences in the proportion of fish and invertebrates in the diet of residents and migrants. In comparing predicted metal exposure values to tolerable daily intakes (TDI), we found that most metals were below or within the range of TDI, except selenium, aluminum, and zinc. Other metals, such as cadmium, copper, and arsenic, were only of concern for dippers mainly feeding on insects; mercury was only of concern for dippers consuming high fish diets. The models were useful tools to demonstrate how shifts in diet and breeding location within a single watershed can result in changes in exposure that may be of toxicological significance.

Stable isotopes as indicators of wastewater effects on the macroinvertebrates of urban rivers

Rivers in urban locations frequently receive contaminated wastewater and particulate waste either directly from storm overflows or from sewage treatment facilities. Although many urban streams are now recovering from wide-scale historic pollution, lower-level effects on water chemistry, nutrients and biotic composition are still widespread. We aimed to determine whether such effects could be detected using stable isotope ratios (δ15N, δ13C and δ34S) in macroinvertebrates alone or in conjunction with traditional biomonitoring. Macroinvertebrates were collected upstream and downstream of 11 different secondary wastewater treatment works (WwTW) in South Wales and the Welsh borders (United Kingdom). Overall, mean invertebrate δ15N signatures downstream of the WwTW were significantly enriched despite variation amongst sites. Moreover, changes between upstream and downstream macroinvertebrate δ15N values were highly correlated with patterns in macroinvertebrate community composition, increased total macroinvertebrate abundance, and reduced Shannon Diversity and other biomonitoring indices (% EPT, % shredders and ASPT scores). Changes in invertebrate δ15N values also paralleled the consented discharge volumes and population equivalents from each WwTW. In contrast, isotopic ratios of δ13C and δ34S were unable to distinguish or quantify wastewater input into the rivers but differences were apparent amongst study streams. Overall, these results suggest that macroinvertebrate δ15N signatures can detect and quantify the effects of secondary sewage treatment inputs to riverine ecosystems. Moreover, the method potentially provides a sensitive means for tracing sewage-derived nutrients into food webs while inferring effects on aquatic communities where sewage-loads are subtle or confounded by other stressors.

Diet shifts during egg laying: Implications for measuring contaminants in bird eggs.

We combined stable isotope tracers of blood plasma, blood cells and egg contents with faecal analysis during pre-breeding and egg laying phases in two dipper species Cinclus cinclus and Cinclus mexicanus to determine the occurrence of dietary shifts during egg production and to assess consequences for egg contaminant loads. In both species, changes in delta(13)C (C. cinclus) or delta(15)N (C. mexicanus) in female plasma relative to red blood cells indicated a dietary shift during laying that was not observed in males. Eurasian dippers increased prey consumption as breeding approached, shifting from primarily trichopteran insect larvae to ephemeropterans and plecopterans. In American dippers, egg-laying females switched to feeding at a higher trophic level by consuming more fish. Eggs derived from higher trophic level diets contained more mercury (American dipper), polychlorinated biphenyls and some organochlorines, especially DDT metabolites. The results demonstrate how dietary changes during egg laying accompany the demands for egg production with consequences for contaminant deposition in avian eggs.

Comparative chronic toxicity of imidacloprid, clothianidin, and thiamethoxam to Chironomus dilutus and estimation of toxic equivalency factors

Nontarget aquatic insects are susceptible to chronic neonicotinoid insecticide exposure during the early stages of development from repeated runoff events and prolonged persistence of these chemicals. Investigations on the chronic toxicity of neonicotinoids to aquatic invertebrates have been limited to a few species and under different laboratory conditions that often preclude direct comparisons of the relative toxicity of different compounds. In the present study, full life-cycle toxicity tests using Chironomus dilutus were performed to compare the toxicity of 3 commonly used neonicotinoids: imidacloprid, clothianidin, and thiamethoxam. Test conditions followed a static-renewal exposure protocol in which lethal and sublethal endpoints were assessed on days 14 and 40. Reduced emergence success, advanced emergence timing, and male-biased sex ratios were sensitive responses to low-level neonicotinoid exposure. The 14-d median lethal concentrations for imidacloprid, clothianidin, and thiamethoxam were 1.52 μg/L, 2.41 μg/L, and 23.60 μg/L, respectively. The 40-d median effect concentrations (emergence) for imidacloprid, clothianidin, and thiamethoxam were 0.39 μg/L, 0.28 μg/L, and 4.13 μg/L, respectively. Toxic equivalence relative to imidacloprid was estimated through a 3-point response average of equivalencies calculated at 20%, 50%, and 90% lethal and effect concentrations. Relative to imidacloprid (toxic equivalency factor [TEF] = 1.0), chronic (lethality) 14-d TEFs for clothianidin and thiamethoxam were 1.05 and 0.14, respectively, and chronic (emergence inhibition) 40-d TEFs were 1.62 and 0.11, respectively. These population-relevant endpoints and TEFs suggest that imidacloprid and clothianidin exert comparable chronic toxicity to C. dilutus, whereas thiamethoxam induced comparable effects only at concentrations an order of magnitude higher. However, the authors caution that under field conditions, thiamethoxam readily degrades to clothianidin, thereby likely enhancing toxicity. Environ Toxicol Chem 2017;36:372-382.