There is an ongoing unprecedented loss in insects, both in terms of richness and biomass. The usage of pesticides, especially neonicotinoid insecticides, has been widely suggested to be a contributor to this decline. However, the risks of neonicotinoids to natural insect populations have remained largely unknown due to a lack of field-realistic experiments. Here, we used an outdoor experiment to determine effects of field-realistic concentrations of the commonly applied neonicotinoid thiacloprid on the emergence of naturally assembled aquatic insect populations. Following application, all major orders of emerging aquatic insects (Coleoptera, Diptera, Ephemeroptera, Odonata, and Trichoptera) declined strongly in both abundance and biomass. At the highest concentration (10 µg/L), emergence of most orders was nearly absent. Diversity of the most species-rich family, Chironomidae, decreased by 50% at more commonly observed concentrations (1 µg/L) and was generally reduced to a single species at the highest concentration. Our experimental findings thereby showcase a causal link of neonicotinoids and the ongoing insect decline. Given the urgency of the insect decline, our results highlight the need to reconsider the mass usage of neonicotinoids to preserve freshwater insects as well as the life and services depending on them.

Adviesbureau Haliplus 378 46 Roseč Czech Republic

Institute of Environmental Sciences Leiden University 2300 RA Leiden The Netherlands

Institute of Environmental Sciences Leiden University 2300 RA Leiden The Netherlands;

Netherlands Institute of Ecology 6700 AB Wageningen The Netherlands

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May R. M., How many species are there on Earth? Science 241, 1441–1449 (1988). PubMed

Vanbergen A. J., et al. ., Threats to an ecosystem service: Pressures on pollinators. Front. Ecol. Environ. 11, 251–259 (2013).

Bianchi F. J. J. A., Booij C. J. H., Tscharntke T., Sustainable pest regulation in agricultural landscapes: A review on landscape composition, biodiversity and natural pest control. Proc. Biol. Sci. 273, 1715–1727 (2006). PubMed PMC

Hallmann C. A., et al. ., More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS One 12, e0185809 (2017). PubMed PMC

Hallmann C. A., et al. ., Declining abundance of beetles, moths and caddisflies in the Netherlands. Insect Conserv. Divers. 13, 127–139 (2019).

Sánchez-Bayo F., Wyckhuys K. A., Worldwide decline of the entomofauna: A review of its drivers. Biol. Conserv. 232, 8–27 (2019).

Homburg K., et al. ., Where have all the beetles gone? Long-term study reveals carabid species decline in a nature reserve in Northern Germany. Insect Conserv. Divers. 12, 268–277 (2019).

Lister B. C., Garcia A., Climate-driven declines in arthropod abundance restructure a rainforest food web. Proc. Natl. Acad. Sci. U.S.A. 115, E10397–E10406 (2018). PubMed PMC

Powney G. D., et al. ., Widespread losses of pollinating insects in Britain. Nat. Commun. 10, 1018 (2019). PubMed PMC

van Klink R., et al. ., Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances. Science 368, 417–420 (2020). PubMed

Dirzo R., et al. ., Defaunation in the Anthropocene. Science 345, 401–406 (2014). PubMed

Wagner D. L., Insect declines in the Anthropocene. Annu. Rev. Entomol. 65, 457–480 (2020). PubMed

Harvey J. A., et al. ., International scientists formulate a roadmap for insect conservation and recovery. Nat. Ecol. Evol. 4, 174–176 (2020). PubMed

Wagner D. L., Grames E. M., Forister M. L., Berenbaum M. R., Stopak D., Insect decline in the Anthropocene: Death by a thousand cuts. Proc. Natl. Acad. Sci. U.S.A. 118, e2023989118 (2021). PubMed PMC

Musters C., et al. ., Partitioning the impact of environmental drivers and species interactions in dynamic aquatic communities. Ecosphere 10, e02910 (2019).

Thomas C. D., Jones T. H., Hartley S. E., “Insectageddon”: A call for more robust data and rigorous analyses. Glob. Change Biol. 25, 1891–1892 (2019). PubMed

Saunders M. E., Janes J. K., O’Hanlon J. C., Moving on from the insect apocalypse narrative: Engaging with evidence-based insect conservation. Bioscience 70, 80–89 (2020).

Forister M. L., Pelton E. M., Black S. H., Declines in insect abundance and diversity: We know enough to act now. Conserv. Sci. Pract. 1, e80 (2019).

Sgolastra F., et al. ., Bees and pesticide regulation: Lessons from the neonicotinoid experience. Biol. Conserv. 241, 108356 (2020).

Siviter H., Muth F., Do novel insecticides pose a threat to beneficial insects? Proc. Biol. Sci. 287, 20201265 (2020). PubMed PMC

Habel J. C., Trusch R., Schmitt T., Ochse M., Ulrich W., Long-term large-scale decline in relative abundances of butterfly and burnet moth species across south-western Germany. Sci. Rep. 9, 14921 (2019). PubMed PMC

Nakanishi K., Yokomizo H., Hayashi T. I., 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. Environ. Sci. Pollut. Res. Int. 25, 35352–35364 (2018). PubMed PMC

Jeschke P., Nauen R., Schindler M., Elbert A., Overview of the status and global strategy for neonicotinoids. J. Agric. Food Chem. 59, 2897–2908 (2011). PubMed

Sparks T. C., Insecticide discovery: An evaluation and analysis. Pestic. Biochem. Physiol. 107, 8–17 (2013). PubMed

Bonmatin J. M., et al. ., Environmental fate and exposure; Neonicotinoids and fipronil. Environ. Sci. Pollut. Res. Int. 22, 35–67 (2015). PubMed PMC

European Academies Science Advisory Council (EASAC), Ecosystem services, agriculture and neonicotinoids. https://easac.eu/fileadmin/PDF_s/reports_statements/Easac_15_ES_web_complete.pdf. Accessed 11 November 2019.

Jeschke P., Nauen R., Neonicotinoids-from zero to hero in insecticide chemistry. Pest Manag. Sci. 64, 1084–1098 (2008). PubMed

Goulson D., An overview of the environmental risks posed by neonicotinoid insecticides. J. Appl. Ecol. 50, 977–987 (2013).

Sánchez-Bayo F., Goka K., Hayasaka D., Contamination of the aquatic environment with neonicotinoids and its implication for ecosystems. Front. Environ. Sci. 4, 71 (2016).

Morrissey C. A., et al. ., Neonicotinoid contamination of global surface waters and associated risk to aquatic invertebrates: A review. Environ. Int. 74, 291–303 (2015). PubMed

Casado J., Brigden K., Santillo D., Johnston P., Screening of pesticides and veterinary drugs in small streams in the European Union by liquid chromatography high resolution mass spectrometry. Sci. Total Environ. 670, 1204–1225 (2019). PubMed

Hladik M. L., Kolpin D. W., Kuivila K. M., Widespread occurrence of neonicotinoid insecticides in streams in a high corn and soybean producing region, USA. Environ. Pollut. 193, 189–196 (2014). PubMed

Woodcock B. A., et al. ., Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science 356, 1393–1395 (2017). PubMed

Vijver M. G., et al. ., Postregistration monitoring of pesticides is urgently required to protect ecosystems. Environ. Toxicol. Chem. 36, 860–865 (2017). PubMed

Pisa L., et al. ., An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: Impacts on organisms and ecosystems. Environ. Sci. Pollut. Res. Int. 28, 11749–11797 (2021). PubMed PMC

Simon-Delso N., et al. ., Systemic insecticides (neonicotinoids and fipronil): Trends, uses, mode of action and metabolites. Environ. Sci. Pollut. Res. Int. 22, 5–34 (2015). PubMed PMC

Beketov M. A., Schäfer R. B., Marwitz A., Paschke A., Liess M., Long-term stream invertebrate community alterations induced by the insecticide thiacloprid: Effect concentrations and recovery dynamics. Sci. Total Environ. 405, 96–108 (2008). PubMed

Sánchez-Bayo F., Goka K., Ecological effects of the insecticide imidacloprid and a pollutant from antidandruff shampoo in experimental rice fields. Environ. Toxicol. Chem. 25, 1677–1687 (2006). PubMed

Brain R. A., Anderson J. C., The agro-enabled urban revolution, pesticides, politics, and popular culture: A case study of land use, birds, and insecticides in the USA. Environ. Sci. Pollut. Res. Int. 26, 21717–21735 (2019). PubMed PMC

Gilburn A. S., et al. ., Are neonicotinoid insecticides driving declines of widespread butterflies? PeerJ 3, e1402 (2015). PubMed PMC

Barmentlo S. H., Vriend L. M., van Grunsven R. H. A., Vijver M. G., Environmental levels of neonicotinoids reduce prey consumption, mobility and emergence of the damselfly Ischnura elegans. J. Appl. Ecol. 56, 2034–2044 (2019).

Jarvis B., “The insect apocalypse is here,” NY Times, 27 November 2018. https://www.nytimes.com/2018/11/27/magazine/insect-apocalypse.html. Accessed 22 January 2020.

Carrington D., “Plummeting insect numbers ‘threaten collapse of nature’,” The Guardian, 10 February 2019. https://www.theguardian.com/environment/2019/feb/10/plummeting-insect-numbers-threaten-collapse-of-nature. Accessed 22 January 2020.

Hayasaka D., Kobashi K., Hashimoto K., Community responses of aquatic insects in paddy mesocosms to repeated exposures of the neonicotinoids imidacloprid and dinotefuran. Ecotoxicol. Environ. Saf. 175, 272–281 (2019). PubMed

Van Dijk T. C., Van Staalduinen M. A., Van der Sluijs J. P., Macro-invertebrate decline in surface water polluted with imidacloprid. PLoS One 8, e62374 (2013). PubMed PMC

Roessink I., Merga L. B., Zweers H. J., Van den Brink P. J., The neonicotinoid imidacloprid shows high chronic toxicity to mayfly nymphs. Environ. Toxicol. Chem. 32, 1096–1100 (2013). PubMed

Beketov M. A., Liess M., Acute and delayed effects of the neonicotinoid insecticide thiacloprid on seven freshwater arthropods. Environ. Toxicol. Chem. 27, 461–470 (2008). PubMed

Barmentlo S. H., et al. ., Neonicotinoids and fertilizers jointly structure naturally assembled freshwater macroinvertebrate communities. Sci. Total Environ. 691, 36–44 (2019). PubMed

Sweeney B. W., Funk D. H., Camp A. A., Buchwalter D. B., Jackson J. K., Why adult mayflies of Cloeon dipterum (Ephemeroptera: Baetidae) become smaller as temperature warms. Freshw. Sci. 37, 64–81 (2018).

Danks H. V., Short life cycles in insects and mites. Can. Entomol. 138, 407–463 (2006).

Xing Z., et al. ., Influences of sampling methodologies on pesticide-residue detection in stream water. Arch. Environ. Contam. Toxicol. 64, 208–218 (2013). PubMed

Langer-Jaesrich M., Köhler H. R., Gerhardt A., Assessing toxicity of the insecticide thiacloprid on Chironomus riparius (Insecta: Diptera) using multiple end points. Arch. Environ. Contam. Toxicol. 58, 963–972 (2010). PubMed

Williams N., Sweetman J., Sweetman J., Effects of neonicotinoids on the emergence and composition of chironomids in the Prairie Pothole Region. Environ. Sci. Pollut. Res. Int. 26, 3862–3868 (2019). PubMed

Rico A., et al. ., Effects of imidacloprid and a neonicotinoid mixture on aquatic invertebrate communities under Mediterranean conditions. Aquat. Toxicol. 204, 130–143 (2018). PubMed

Barmentlo S. H., Parmentier E. M., de Snoo G. R., Vijver M. G., Thiacloprid-induced toxicity influenced by nutrients: Evidence from in situ bioassays in experimental ditches. Environ. Toxicol. Chem. 37, 1907–1915 (2018). PubMed

Sánchez-Bayo F., Goka K., Evaluation of suitable endpoints for assessing the impacts of toxicants at the community level. Ecotoxicology 21, 667–680 (2012). PubMed

Cavallaro M. C., Liber K., Headley J. V., Peru K. M., Morrissey C. A., Community-level and phenological responses of emerging aquatic insects exposed to 3 neonicotinoid insecticides: An in situ wetland limnocorral approach. Environ. Toxicol. Chem. 37, 2401–2412 (2018). PubMed

Pinder L. C. V., Biology of freshwater Chironomidae. Annu. Rev. Entomol. 31, 1–23 (1986).

Lencioni V., Marziali L., Rossaro B., Chironomids as bioindicators of environmental quality in mountain springs. Freshw. Sci. 31, 525–541 (2012).

Hallmann C. A., Foppen R. P. B., van Turnhout C. A. M., de Kroon H., Jongejans E., Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 511, 341–343 (2014). PubMed

Li Y., Miao R., Khanna M., Neonicotinoids and decline in bird biodiversity in the United States. Nat. Sustain. 3, 1027–1035 (2020).

Lennon R. J., et al. ., Using long-term datasets to assess the impacts of dietary exposure to neonicotinoids on farmland bird populations in England. PLoS One 14, e0223093 (2019). PubMed PMC

Nakano S., Murakami M., Reciprocal subsidies: Dynamic interdependence between terrestrial and aquatic food webs. Proc. Natl. Acad. Sci. U.S.A. 98, 166–170 (2001). PubMed PMC

Twining C. W., et al. ., Aquatic and terrestrial resources are not nutritionally reciprocal for consumers. Funct. Ecol. 33, 2042–2052 (2019).

Lack D., The breeding seasons of European birds. Ibis 92, 288–316 (1951).

Vijver M. G., van den Brink P. J., Macro-invertebrate decline in surface water polluted with imidacloprid: A rebuttal and some new analyses. PLoS One 9, e89837 (2014). PubMed PMC

Clements W. H., Hickey C. W., Kidd K. A., How do aquatic communities respond to contaminants? It depends on the ecological context. Environ. Toxicol. Chem. 31, 1932–1940 (2012). PubMed

Gessner M. O., Tlili A., Fostering integration of freshwater ecology with ecotoxicology. Freshw. Biol. 61, 1991–2001 (2016).

Mesnage R., Antoniou M. N., Ignoring adjuvant toxicity falsifies the safety profile of commercial pesticides. Front. Public Health 5, 361 (2018). PubMed PMC

Cadmus P., Pomeranz J. P., Kraus J. M., Low-cost floating emergence net and bottle trap: Comparison of two designs. J. Freshwat. Ecol. 31, 653–658 (2016).

Stehle S., Bub S., Schulz R., Compilation and analysis of global surface water concentrations for individual insecticide compounds. Sci. Total Environ. 639, 516–525 (2018). PubMed

Leiden University (CML), Rijkswaterstaat-WVL, Pesticide Atlas, version 2.0 (2018). https://www.bestrijdingsmiddelenatlas.nl. Accessed 22 November 2018.

Giorio C., et al. ., An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 1: New molecules, metabolism, fate, and transport. Environ. Sci. Pollut. Res. Int. 28, 11716–11748 (2021). PubMed PMC

Oosterbroek P., The European Families of the Diptera (KNNV Publishing, 2016).

Langton P. H., Pinder L. C. V., Keys to the Adult Male Chironomidae of Britain and Ireland (Freshw. Biol. Assoc., 2007), vols. 1 and 2.

Hirvenoja M., Hirvenoja E., Corynoneura brundini spec. nov. Ein Beitrag zur Systematik der Gattung Corynoneura (Diptera: Chironomidae). Spixiana 14 (suppl.), 213–238 (1988).

Sæther O. A., A review of the genus Limnophyes Eaton from the Holarctic and Afrotropical regions (Diptera: Chironomidae, Orthocladiinae). Entomol. Scand. 35 (suppl.), 1–139 (1990).

R Core Team, R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2019).

S. H. Barmentlo et al.., Data from: Experimental evidence for neonicotinoid driven decline in aquatic emerging insects. Dryad. 10.5061/dryad.dz08kprzg. Deposited 7 October 2021. PubMed DOI PMC

Experimental evidence for neonicotinoid driven decline in aquatic emerging insects