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Assessing Toxicity of the Insecticide Thiacloprid on Chironomus Riparius (Insecta: Diptera) Using Multiple End Points

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Assessing Toxicity of the Insecticide Thiacloprid on Chironomus Riparius (Insecta: Diptera) Using Multiple End Points Arch Environ Contam Toxicol DOI 10.1007/s00244-009-9420-x Assessing Toxicity of the Insecticide Thiacloprid on Chironomus riparius (Insecta: Diptera) Using Multiple End Points Miriam Langer-Jaesrich • Heinz-R. Ko¨hler • Almut Gerhardt Received: 22 July 2009 / Accepted: 3 November 2009 Ó Springer Science+Business Media, LLC 2009 Abstract Since data documentation on neonicotinic tox- aquatic organisms, a number of test systems have been icity to nontarget organisms should be enhanced, we developed. However, these methods focus primarily on investigate the effects of thiacloprid, a novel neonicotinoid pelagic organisms, such as fish and daphnids. Communities insecticide, on the sediment-dwelling nontarget insect of benthic organisms play a key role in energy, nutrient, Chironomus riparius. Further, we wanted to validate the and contaminant fluxes and they play a key role in trans- sensitivity of end points on different biological levels and ferring environmental contaminants to higher trophic levels obtain the greatest amount of information regarding the (Burton 1991; Reynoldson 1987). For this reason, the effects of this compound by using a battery of several end consequences of toxic substance exposure to benthic points such as larval mortality, behavior, body weight gain, communities should be studied more closely. emergence rate, time of development, gender ratio, Hsp70 Thiacloprid, a neurotoxic insecticide, belongs to the new stress protein level, and larval mouthpart deformities after and commercially very successful family of the neonicot- exposure at a concentration range of 0.1 to 1000 lg/L inoids. Both its structure and its mode of action are related thiacloprid. C. riparius was impacted starting at concen- to imidacloprid—one of the biggest-selling insecticides trations of 0.5 lg/L, a concentration that can be considered worldwide (Jeschke et al. 2001). In 2007 it was registered environmentally relevant. Larval mortality, behavior, in more than 50 countries (Bayer Crop Science 2008). emergence, and Hsp70 protein level were sensitive indica- Thiacloprid, as all neonicotinoids, acts on the insect ner- tors for the toxic effect of thiacloprid, whereas gender ratio vous system as an agonist of the nicotinic acetylcholine and mouthpart morphology were not affected. In our case receptor (nAChR) (Jeschke et al. 2001). It exhibits high life-cycle end points like survival rate (LC50: 1.57 lg/L) water solubility (184–186 mg/L) and a relatively low log- and emergence rate (EC50: 0.54 lg/L) proved to be more Kow (1.26) at 20°C. This insecticide has a half-life (DT50) sensitive than tested physiological end points for the neu- in water of 6–11 days and a DT50 in water sediment sys- rotoxic insecticide. tems lasting between 11 and 27 days (European Commis- sion 2004). Thiacloprid may therefore contaminate surface waters following rainstorm events (Beketov and Liess The use of pesticides can affect nontarget species of 2008b). The currently predicted worst-case environmental organisms, since they can be at risk from pesticide leach- concentration for thiacloprid via spray drift in surface ing, spray drift, or surface runoff into aquatic ecosystems water has been predicted to be 1.99 lg/L (ornamentals) and (Kreuger 1998; Palma et al. 2004). To evaluate this risk for 17.52 lg/L (orchards), respectively (Schmuck 2001). For runoff events this scenario is not yet available. Studies on M. Langer-Jaesrich (&) Á H.-R. Ko¨hler measured thiacloprid concentrations in the environment are Animal Physiological Ecology Department, University of rare due to its brief time of availability on the market. Tu¨bingen, Konrad-Adenauer-Str. 20, 72072 Tu¨bingen, Germany A single study conducted in apple orchards in the area e-mail: [email protected] surrounding Hamburg, Germany, detected thiacloprid A. Gerhardt concentrations of 4.5 lg/L in a nearby water system (Su¨ß LimCo International, Oststr. 24, 49477 Ibbenbu¨ren, Germany et al. 2006). 123 Arch Environ Contam Toxicol Information about the toxicity of thiacloprid to nontarget Preparation of Insecticide Stock Solutions freshwater invertebrates and about its potential effects on freshwater ecosystems is limited (Beketov and Liess At room temperature (RT) a 5 mg/L thiacloprid (Riedel-de 2008b). However, in previous experiments insects showed Hae¨n; CAS 111988499 analytical standard; Germany) stock a higher sensitivity to this insecticide than other freshwater solution was prepared every third day with declorinated tap arthropods (Beketov and Liess 2008a, b; Beketov et al. water (pH 7.8 ± 0.2) and stirred for 14 h in the dark. The 2008). This strongly suggests the inclusion of insects in following nominal test concentrations were directly pre- further additional ecotoxicological testing. pared before use with aerated declorinated tap water—0.1, The worldwide-distributed family of Chironomidae are 0.5, 1, 5, 10, and 1000 lg/L thiacloprid—as well as one suitable test species due to their aquatic and sediment- negative control containing only pure dechlorinated tap bound larval stages. Chironomids are frequently the most water. Concentrations of insecticide were chosen on the abundant group of insects in freshwater environments and basis of a preliminary range of tests with L3 larvae and also their function as prey for other species makes them envi- from measured environmental concentrations (Su¨ß et al. ronmentally relevant (Armitage et al. 1995; Pinder 1986). 2006). Each treatment was replicated four times. The nonbiting midge, Chironomus riparius, is widely used for toxicity testing (OECD 2004a, b; US EPA 2000) due to Spiking of Sediment its easy cultivation, short generation time, and relative sensitivity to pollutants. To simulate natural conditions we first spiked the sedi- Beketov and Liess (2008b) pointed out that the knowl- ments with an aqueous solution assuming that the parti- edge of sublethal effects of thiacloprid on life cycle traits tioning between sediments and the water phase takes 24 h of insect species is limited. The aim of this study was to to reach equilibrium. The day before being used in the evaluate the effects of thiacloprid on the insect C. riparius experiment 50 g of quartz sediment (particle size, using established end points such as emergence rate, time 0.1–0.3 mm; burned for 3 h at 500°C to remove organic needed for development, and larval body weight gain matter; Dehner, Germany) was filled into a 250-ml glass (OECD 2004a, b). In addition, these main parameters were beaker. For spiking, the sediment was covered with 200 ml complemented with other end points including hatching of the respective test solution and subsequently shaken for rate, behavior changes, larval mortality (L3 and L4), stress 24 h in the dark. Subsequently we removed the water phase protein response (70-kD heat shock protein family; Hsp70), and added fresh test solution representing the environ- mouthpart deformation, and gender ratio. mental conditions under which thiacloprid is repeatedly introduced. The aim of this was to stabilize the concen- tration of insecticide in both the water and the sediment. Materials and Methods Egg Preparation and Exposure Maintenance of Parent Animals Different egg clutches from the breeding stock were collected Stock cultures of Chironomus riparius, from different at 8 a.m., separated into smaller clusters of visually the same genetic sources, in order to avoid genetic impoverishment size, and mixed randomly. A preliminary experiment was (LimCo International, Germany; University of Joensuu, designed to test whether egg clutch disassembly with and Finland; and Universidade de Coimbra, Portugal), were kept without thiacloprid treatment had an effect on hatching rate. as larvae in fine quartz sand and dechlorinated tap water After counting the eggs, between 100 and 120 eggs per under constant aeration. Every day the chironomid larvae replicate were exposed to the appropriate thiacloprid con- were fed with finely ground fish flakes (50% Tetramin, 50% centration. The number of hatched larvae was counted Tetraphyll; Tetra, Germany). Declorinated tap water was under a stereomicroscope daily at the same time of day for exchanged one or two times per week. Before emergence a period of 6 days after oviposition. Since larvae exposed occurred, a breeding cage (55 9 65 9 120 cm) was instal- to the highest thiacloprid concentration of 1000 lg/L did led over the stock containers, in which the adults were not hatch, but died immediately after hatching (see results), allowed to fly, swarm, and breed. The egg masses which were only concentrations up to 10 lg/L thiacloprid were tested attached to the vessel wall were collected every morning and in the procedures that follow. used subsequently for experiments. Stock breeding and all experiments were conducted in a climatized chamber at Larval Exposure and Maintenance 21.0 ± 0.5°C, with a light–dark cycle of 16:8 h artificial daylight (Philips standard daylight 54765; 2500 lumen; After 3 days 33 first-instar larvae from each replicate were Germany). transferred with a glass pipette to glass beakers (providing a 123 Arch Environ Contam Toxicol density of 1.34 individuals/cm2). The beakers were covered in development time, for each concentration the develop- with parafilm to reduce evaporation (Parafilm ‘M;’ mental rate was calculated using the formula given in the American National Can, Chicago, IL, USA). Larvae were OECD Guideline (OECD 2004a, b). The gender ratio of fed daily with 12 ± 1 mg finely ground fish food (50% emerged chironomids was calculated in each replicate as Tetramin, 50% Tetraphyll; Tetra), corresponding to the number of male-to-female organisms. C0.36 mg/day/larva. From the second day after transfer the beakers were aerated through a glass Pasteur pipette. Water Mouthpart Deformities was exchanged every third day with new insecticide-spiked water. Temperature, pH, conductivity, dissolved oxygen The remaining head capsule exuviae of the emerged saturation, and nitrite content were regularly measured in the midges were collected and stored in 100% alcohol.
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