Extending standard testing period in honeybees to predict lifespan impacts of pesticides and heavy metals using dynamic energy budget modelling

Abstract

Concern over reported honeybee (Apis mellifera spp.) losses has highlighted chemical exposure as a risk. Current laboratory oral toxicity tests in A. mellifera spp. use short-term, maximum 96 hour, exposures which may not necessarily account for chronic and cumulative toxicity. Here, we use extended 240 hour (10 day) exposures to examine seven agrochemicals and trace environmental pollutant toxicities for adult honeybees. Data were used to parameterise a dynamic energy budget model (DEBtox) to further examine potential survival effects up to 30 day and 90 day summer and winter worker lifespans. Honeybees were most sensitive to insecticides (clothianidin > dimethoate ≫ tau-fluvalinate), then trace metals/metalloids (cadmium, arsenic), followed by the fungicide propiconazole and herbicide 2,4-dichlorophenoxyacetic acid (2,4-D). LC50s calculated from DEBtox parameters indicated a 27 fold change comparing exposure from 48 to 720 hours (summer worker lifespan) for cadmium, as the most time-dependent chemical as driven by slow toxicokinetics. Clothianidin and dimethoate exhibited more rapid toxicokinetics with 48 to 720 hour LC50s changes of <4 fold. As effects from long-term exposure may exceed those measured in short-term tests, future regulatory tests should extend to 96 hours as standard, with extension to 240 hour exposures further improving realism.

Comparing bee species responses to chemical mixtures: Common response patterns?

“…[20, 21]) showed one or both chemicals to have an effect on survival at the tested concentrations. Controls containing only 50% w/v sucrose were included in all experiments.…”

An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: impacts on organisms and ecosystems

“…Improvement of research methods (sampling and measuring exposure) is also addressed by Benuszak et al (2017). Hesketh et al (2016) provide arguments for an increased exposure time (> 240 h) to better identify sublethal effects in honeybee toxicity test, the current standard being 96 h of exposure.…”

Time-Cumulative Toxicity of Neonicotinoids: Experimental Evidence and Implications for Environmental Risk Assessments

“…The data collected refers to 14 species of insects belonging to seven different taxonomic orders; among them is the brown planthopper (Nilaparvata lugens), a pest of rice crops and Frankiniella occidentalis, a pest of many flowers. In addition to the above, two tests using clothianidin showed that this compound followed Haber's rule when tested on honeybees (Apis mellifera) [44,45], whereas the same compound tested on bumblebees (Bombus terrestris) and mason bees (Osmia bicornis) appeared to show mainly dose-dependent toxicity [45]. One additional data set included acetamiprid, but this compound did not show time-dependent toxicity when tested on honeybees [46] (Table S2), perhaps because it is quickly metabolised [47].…”

“…The decrease in LC50 values (LC50) between the initial and final exposure times varies in the range 3 to 52 for all compounds, with notable exceptions for imidacloprid tested on female fruit flies (Drosophila melanogaster) and termites, which showed differences of 172 times over 8 days and 1167-3126 times over 21 days, respectively [44,46]. The result for imidacloprid on the fruit flies contrasts with previous tests that showed no time-dependent toxicity of this compound to the same species and equal 8-day testing period [47].…”

“…Nevertheless, given the good fit of the model to the dataset (r 2 = 0.85) this result cannot be excluded. Examples of time-cumulative toxicity for three chemicals are shown in Figure 3a,b. clothianidin on the predatory bug Cyrtorhinus lividipennis and the brown hopper pest species indicate values of n = 3.7 and 4.5, respectively [42]; imidacloprid on the ant Linepithema humile (n = 3.5) [43], on the termite Reticulitermes flavipes (n = 4.0) [44] and on the honeybee (n = 5.8) [45]. The latter value of n is unusually high, suggesting that the bees tested may have died by an interaction of the insecticide with other factors such as pathogenic infections or others.…”