Neonicotinoid Insecticides from a Marine Perspective: Acute and Chronic Copepod Testing and Derivation of Environmental Quality Standards

Abstract

Neonicotinoid insecticides have become of global concern for the aquatic environment. Harpacticoid copepods are amongst the most sensitive organisms to neonicotinoids. Here, we exposed the brackish copepod Nitocra spinipes to four neonicotinoid insecticides, i.e. clothianidin (CLO), imidacloprid (IMI), thiacloprid (TCP) and thiamethoxam (TMX) to investigate acute toxicity on adults (96-h exposure) and effects on larval development (7-d exposure). We used these results in combination with publicly available ecotoxicity data to derive Environmental Quality Standards (EQS). These EQS were ultimately used in a single-substance and mixture risk assessment for the Belgian part of the North Sea. Acute toxicity testing revealed that immobilization is a more sensitive endpoint than mortality, with 96h-EC 50 values of 6.9, 7.2, 25 and 120 µg L-1 for CLO, TCP, IMI and TMX, respectively. In addition, the larval development tests resulted in 7d-NOECs of 2.5, 2.7, 4.2 and >99 µg L-1 for CLO, TCP, IMI and TMX, This article is protected by copyright. All rights reserved. Accepted Article respectively. The derived saltwater Annual Average (AA-)EQS were 0.05, 0.0048, 0.002 and 0.016 µg L-1 for CLO, TCP, IMI and TMX, respectively. Finally, the risk characterization revealed some exceedances of the AA-EQS in Belgian harbors for IMI (number of exceedances, n = 2/4), TCP (n = 1/4), TMX (n = 1/4) and the mixture of the four neonicotinoids (n = 4/4), but not at the open sea. At the open sea site, the toxic unit sum relative to the AA-EQS was 0.72 and 0.22, suggesting no mixture risk, albeit with a relatively small margin of safety. Including short-term EC 10 (96h) values of N. spinipes for the AA-EQS derivation led to a refinement of the AA-EQS for CLO and TMX, suggesting their use for the AA-EQS derivation since one of the overarching goals of the definition of EQS is to protect species at the population level.

Inhibition of Larval Development of Marine Copepods Acartia tonsa by Neonicotinoids

“…Literature data on the effects of NEOs toward saltwater copepods are available only for the benthic, brackish species N. spinipes. Acute effects on adult survival and mobility were observed at a concentration higher than the effective concentration calculated for A. tonsa, with 96h-EC 50 s in the range 6.9-120 µg L −1 [21]. The larval development test with N. spinipes was more sensitive than the acute test and produced 7d-NOECs in the range of 2.5-4.2 µg L −1 for THI, IMI and CLO and above 99 µg L −1 for TMX [21].…”

“…US Environmental Protection Agency (USEPA) Office of Pesticide Programs (OPP) aquatic life benchmarks were retrieved from https://www.epa.gov/pesticide-science-and-assessing-pesticiderisks/aquatic-life-benchmarks-and-ecological-risk, accessed on 2 June 2021. Environmental quality standards for saltwater were retrieved from Moeris et al [21]. The effect-concentration curves differed considerably among pesticides (Figure 1).…”

“…The effect-concentration data obtained with A. tonsa evidenced a different sensitivity toward the different NEOs, with ACE (EC 50 = 0.73 µg L −1 ) characterized by a higher inhibitory potential than the other NEOs. A different tolerance towards NEO compounds is a typical output for several species, sensitive freshwater insects (C. dilutus, N. triangulifer), oligochaetes (Lumbriculus variegatus) and both freshwater (Hyalella azteca, Gammarus pulex) and marine crustaceans (A. bahia, P. japonicus and N. spinipes) [5,10,15,21].…”

“…For this reason, toxic effects on copepods may generate disruption of food webs and detrimental effects on higher trophic levels. Many species of copepods are used as bioindicators to assess the adverse effects of chemicals and effluents in surface waters, including Acartia tonsa, Centropages sp., Eurytemora affinis and Nitocra spinipes [19][20][21]. In particular, planktonic copepods such as Acartia tonsa are very sensitive to pesticides and other organic chemicals acting as endocrine and nervous transmission disruptors [22][23][24][25].…”

A rapid evidence assessment of the potential risk to the environment presented by active ingredients in the UK’s most commonly sold companion animal parasiticides

“…Reproductive toxicity, such as reproductive cycle disruption and decreased sperm motility, occurred at 14-day oral exposure to 3 mg/kg bw in female and male rats respectively (de Barros et al 2017 ; 2016 ). Toxicity in birds occurred at similar levels, with behavioural changes and oxidative damage in the heart and lungs of Japanese quail at long term exposure to 2.26 mg/kg bw (Khalil et al 2017 ; 2019 ).…”