Developing gene-to-ecosystem approaches to understanding pesticide impacts in natural ecosystems

Background/Question/Methods - Pesticides used in agriculture enter the freshwater system through run off, leeching or accidental spills, and cause deleterious effects on freshwater biotic communities. Research into these effects has been conducted mainly at the scale of laboratory trials and mesocosm experiments. Research into the effects of pesticides on the whole freshwater community spanning multiple organisational levels, from genes to ecosystems, is so far lacking.

We use an accidental spill of the pesticide Chlopyrifos, a widely used organophosphate pesticide, in the River Kennet, UK, in July 2013 as a case study in which to investigate the direct and indirect effects on a whole river community, from microbes to top-predators, as well as ecosystem functioning. We tested the following hypotheses: 1) macro-invertebrate mediated decomposition will be reduced in pesticide exposed sites, while microbial mediated decomposition will increase due to the release from top-down control, 2) microbial functional capacity will increase in pesticide exposed sites reflecting the increase in available substrates (both the pesticide itself and the carcasses of sensitive invertebrates and 3) food webs exposed to the pesticide will undergo re-structuring as sensitive taxa are lost from the system. We began large-scale biological sampling shortly after the spill, using a replicated experimental design comprising two upstream control and two downstream impacted reaches. Citizen science data provided an important before-after-control-impact (BACI) element to the study.

Results/Conclusions -  Citizen science data showed that the pre-impact invertebrate community composition in the three months prior to the spill was similar but following the spill there was a 99.5% reduction in total abundance. By the time of our sampling date, total abundance had increased slightly, but the community composition was altered. Within impacted sites microbial mediated decomposition was higher, whereas total decomposition was lower than control sites reflecting the decline of detritivores macro-invertebrates and partial compensation by microbial consumers, confirming our first hypothesis. Within the microbial community, populations of ammonia oxidisers increased in impacted sites as did organophosphate degraders, revealing direct (i.e. resource) and indirect effects (i.e. ammonia from decaying invertebrates) of chlorpyrifos on the microbial community, confirming our second hypothesis. Food web analysis showed that whole-network metrics were insensitive to the spill, while substructural analysis revealed marked changes caused by both the direct and indirect effects of the pesticide.

This study shows that pesticides act both directly and indirectly across multiple levels of organisation, and a more integrated approach is needed to fully reveal these effects in natural ecosystems.