Interactive Effects of Pesticides and Nutrients on Microbial Communities Responsible of Litter Decomposition in Streams

Abstract

Global contamination of streams by a large variety of compounds, such as nutrients and pesticides, may exert a high pressure on aquatic organisms, including microbial communities and their activity of organic matter decomposition. In this study, we assessed the potential interaction between nutrients and a fungicide and herbicide [tebuconazole (TBZ) and S-metolachlor (S-Met), respectively] at realistic environmental concentrations on the structure (biomass, diversity) and decomposition activity of fungal and bacterial communities (leaf decay rates, extracellular enzymatic activities) associated with Alnus glutinosa (Alnus) leaves. A 40-day microcosm experiment was used to combine two nutrient conditions (mesotrophic and eutrophic) with four pesticide treatments at a nominal concentrations of 15 μg L-1 (control, TBZ and S-Met, alone or mixed) following a 2 × 4 full factorial design. We also investigated resulting indirect effects on Gammarus fossarum feeding rates using leaves previously exposed to each of the treatments described above. Results showed interactive effects between nutrients and pesticides, only when nutrient (i.e., nitrogen and phosphorus) concentrations were the highest (eutrophic condition). Specifically, slight decreases in Alnus leaf decomposition rates were observed in channels exposed to TBZ (0.01119 days-1) and S-Met (0.01139 days-1) than in control ones (0.01334 days-1) that can partially be explained by changes in the structure of leaf-associated microbial communities. However, exposition to both TBZ and S-Met in mixture (MIX) led to comparable decay rates to those exposed to the pesticides alone (0.01048 days-1), suggesting no interaction between these two compounds on microbial decomposition. Moreover, stimulation in ligninolytic activities (laccase and phenol oxidase) was observed in presence of the fungicide, possibly highlighting detoxification mechanisms employed by microbes. Such stimulation was not observed for laccase activity exposed to the MIX, suggesting antagonistic interaction of these two compounds on the ability of microbial communities to cope with stress by xenobiotics. Besides, no effects of the treatments were observed on leaf palatability for macroinvertebrates. Overall, the present study highlights that complex interactions between nutrients and xenobiotics in streams and resulting from global change can negatively affect microbial communities associated with leaf litter, although effects on higher trophic-level organisms remains unclear.

A common fungicide impairs stream ecosystem functioning through effects on aquatic hyphomycetes and detritivorous caddisflies

“…We found a decrease of microbial decomposition in pre-treated litter, but the waterborne fungicide effects were more complex: decomposition was higher at the low concentration, suggesting a subsidy effect of the fungicide (sensu Odum et al, 1979), as previously observed for other toxic compounds (Swift et al, 1988), or a shift in the relative contribution of fungi and bacteria to microbial decomposition (Gulis and Suberkropp, 2003). Previous studies have shown a variety of responses of microbial decomposition to fungicides, from severe reductions after waterborne exposition (Zubrod et al, 2015a;Rossi et al, 2018) to non-significant effects with pre-treated litter (Dimitrov et al, 2014) or waterborne fungicides (Zubrod et al, 2015a). Furthermore, Zubrod et al (2017) failed to find effects on microbial decomposition when combining five different fungicides with different exposure modes.…”

“…The use of different fungicides and different exposure modes can also explain differences among experiments (Maltby et al, 2009). For example, we found the greatest invertebrate mortality in the litter pre-treatment with fungicide, while others have found no mortality in G. fossarum fed litter that had been conditioned in water with a fungicide (Rossi et al, 2018), or litter from trees which had been treated with systemic fungicides for 6 weeks (Newton et al, 2018). In these cases, fungicide treatments were more indirect than in our experiment, in which the fungicide was sprayed on the litter 2 days before the beginning of the experiment and/or added to the water in experimental microcosms.…”

“…The wide variety of fungicides and invertebrates used in experiments precludes any generalization currently. For example, our litter pre-treatment aimed to simulate the fungicide application mode (i.e., spraying fungicide on leaves), while other studies pre-treated litter by exposing it to fungicides in the water column during their initial conditioning, resulting in smaller effects than those observed here (Zubrod et al, 2011(Zubrod et al, , 2015b(Zubrod et al, , 2017Flores et al, 2014a;Rossi et al, 2018).…”

Agricultural pressures impair trophic link between aquatic microorganisms and invertebrates

“…It is The copyright holder for this preprint this version posted March 19, 2021. ; https://doi.org/10.1101/2021.03.18.435985 doi: bioRxiv preprint 4 on invertebrates relied predominantly on feeding preference experiments and singled-out chemicals that are often applied to the overlying water (e.g. Feckler et al, 2016;Rossi et al, 2018;Barmentlo et al, 2018Barmentlo et al, , 2019. This approach prevents the distinction between direct and indirect effects on microbially-mediated trophic linkages that are caused by chemical deposition and sorption of chemical to OM on temporal scales that are relevant to ecosystem processes.…”

“…To date, studies aimed at assessing effects of agricultural practices mostly focussed on direct effects (e.g., toxicity) to aquatic invertebrates, while studies focused on indirect effects of chemicals on invertebrates relied predominantly on feeding preference experiments and singled-out chemicals that are often applied to the overlying water (e.g. Feckler et al, 2016; Vijver et al, 2017; Rossi et al, 2018; Barmentlo et al, 2018, 2019). This approach prevents the distinction between direct and indirect effects on microbially-mediated trophic linkages that are caused by chemical deposition and sorption of chemical to OM on temporal scales that are relevant to ecosystem processes.…”