Macro-Invertebrate Decline in Surface Water Polluted with Imidacloprid

Citation: Van Dijk TC, Van Staalduinen MA, Van der Sluijs JP ( Macro-Invertebrate Decline in Surface Water Polluted with Imidacloprid Tessa C. Van Dijk 0 Marja A. Van Staalduinen 0 Jeroen P. Van der Sluijs 0 Nicolas Desneux, French National Institute for Agricultural Research (INRA), France 0 Environmental Sciences, Utrecht University , Utrecht , The Netherlands Imidacloprid is one of the most widely used insecticides in the world. Its concentration in surface water exceeds the water quality norms in many parts of the Netherlands. Several studies have demonstrated harmful effects of this neonicotinoid to a wide range of non-target species. Therefore we expected that surface water pollution with imidacloprid would negatively impact aquatic ecosystems. Availability of extensive monitoring data on the abundance of aquatic macro-invertebrate species, and on imidacloprid concentrations in surface water in the Netherlands enabled us to test this hypothesis. Our regression analysis showed a significant negative relationship (P,0.001) between macro-invertebrate abundance and imidacloprid concentration for all species pooled. A significant negative relationship was also found for the orders Amphipoda, Basommatophora, Diptera, Ephemeroptera and Isopoda, and for several species separately. The order Odonata had a negative relationship very close to the significance threshold of 0.05 (P = 0.051). However, in accordance with previous research, a positive relationship was found for the order Actinedida. We used the monitoring field data to test whether the existing three water quality norms for imidacloprid in the Netherlands are protective in real conditions. Our data show that macrofauna abundance drops sharply between 13 and 67 ng l21. For aquatic ecosystem protection, two of the norms are not protective at all while the strictest norm of 13 ng l21 (MTR) seems somewhat protective. In addition to the existing experimental evidence on the negative effects of imidacloprid on invertebrate life, our study, based on data from large-scale field monitoring during multiple years, shows that serious concern about the far-reaching consequences of the abundant use of imidacloprid for aquatic ecosystems is justified. - Funding: Financial support was given to TVD and MVS by the Triodos Foundations Support Fund for Independent Research on Bee Decline and Systemic Pesticides. This Support Fund has been created from donations by Adessium Foundation (The Netherlands), Act Beyond Trust (Japan), Universiteit Utrecht (Netherlands), Stichting Triodos Foundation (The Netherlands), Gesellschaft fu r Schmetterlingsschutz (Germany), M.A.O.C. Gravin van Bylandt Stichting (The Netherlands), Zukunft Stiftung Landwirtschaft (Germany), Beekeepers Union ABTB (Netherlands), Study Association Storm (Student Association Environmental Sciences Utrecht University) and citizens. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. When neonicotinoids were introduced as new, systemic, insecticides in the 1990s, they were supposed to be much more efficient than the older generation of insecticides [1]. As a seed treatment they could be used in much lower quantities and they promised to be less polluting to the environment. Seed dressing makes spraying crops with insecticides unnecessary because the active substances are spread to all plant tissues when the plant grows. However, soon after the introduction of this new type of insecticides, concern rose that neonicotinoid residues in pollen and nectar might be harmful to honey bees [1,2], and several studies have provided supporting evidence for this [3]. Neonicotinoids are neuro-active insecticides which derive their toxicity to target species from acting mainly agonistically on nicotinic acetylcholine receptors (nAChRs) on the post-synaptic membrane [46]. This means that normal nerve impulses become impaired [7]. Some authors [8] have also indicated some antagonistic action. The binding sites in mammal nAChRs are different from those in insect nAChRs, and the neonicotinoid imidacloprid shows selective toxicity for insects over vertebrates. This partly attributable to a higher affinity of imidacloprid for insect nAChRs compared with their vertebrate counterparts [5]. In short-term (10-day) tests on the effects of imidacloprid [9] on the aquatic worm Lumbriculus variegatus a high mortality was observed at the highest concentrations of imidacloprid in the sediments (1 to 5 mg/kg). At lower concentrations (0.05 to 0.5 mg/kg) effects were observed on growth and behaviour of L. variegatus. In another test [10] the aquatic invertebrates Chironomus tentans and Hyallella Azteca were able to recover from a short-term pulse exposure, but a chronic low-level exposure (.1.14 mg l21 for C. tentans) to imidacloprid reduced the species survival and growth. Different effects of imidacloprid exposure in an aquatic microcosm experiment were found for two species of stream insects [11]; while the survival of the stonefly, Pteronarcys dorsata, was significantly reduced at 48 and 96 mg l21, no significant mortality was found for the cranefly, Tipula sp., although a change in behaviour was observed. In acute toxicity bioassays [12] of imidacloprid to zooplankton crustaceans, the imidacloprid 48-h LC50-s for cladocerans (65133 mg l21) were two orders of magnitude higher than for ostracods (301715 mg l21). In an acute toxicity test on an amphibian [13] the 48-h LC50-s for imidacloprid were found to be 165 mg l21 for tadpoles of Rana limnocharis and 219 mg l21 for tadpoles of Rana nivalis. The variation in susceptibility among different animal taxa indicates that certain biochemical traits particular to a group of organisms are responsible for a specific level of sensitivity [14]. Long-term alterations in aquatic invertebrate community structure occurred after single pulse contamination of a stream ecosystem with the neonicotinoid insecticide thiacloprid [15]. In other community studies, the caddisfly Neureclipsis sp. reacted very sensitively to a single pulse of imidacloprid, and Diptera and Ephemeroptera larvae were affected after repeated pulses [16]. In field mesocosms, zooplankton, benthic, nekton as well as neuston communities exposed to imidacloprid were significantly less abundant than non-treated controls [17]. At low concentrations of neonicotinoid insecticides sub-lethal effects can occur in invertebrates. Given the many limitations of acute toxicity as an indicator for impacts of agrochemicals on aquatic invertebrate communities, the sublethal effects must be considered for a complete and realistic assessment of the long term impact [18]. In a study [19] on the effect of imidacloprid exposure on the mayfly Epeorus lingimanus and the aquatic oligochaete, Lumbriculus variegatus a reduction of feeding and egestion was fo (...truncated)