Widespread agrochemicals differentially affect zooplankton biomass and community structure

Abstract

Anthropogenic environmental change is causing habitat deterioration at unprecedented rates in freshwater ecosystems. Despite increasing more rapidly than other agents of global change, synthetic chemical pollution –including agrochemicals such as pesticides– has received relatively little attention in freshwater biotic assessments. Determining the effects of multiple agrochemicals on complex community and ecosystem properties remains a major challenge, requiring a cross-field integration of ecology and ecotoxicology. Using a large-scale array of experimental ponds, we investigated the response of zooplankton community properties (biomass, composition, diversity metrics) to the individual and joint presence of three widespread agrochemicals: the herbicide glyphosate, the neonicotinoid insecticide imidacloprid, and fertilisers. We tracked temporal variation in community biomass and structure (i.e., composition, diversity metrics) along single and combined pesticide gradients (each spanning eight levels), under low (mesotrophic) and high (eutrophic) nutrient-enriched conditions, and quantified (i) agrochemical interactions, (ii) response threshold concentrations, and (iii) community resistance and recovery. We found that major zooplankton groups differed in their sensitivity to pesticides: ≥3 µg/L imidacloprid impaired copepods, rotifers collapsed at glyphosate levels ≥0.3 mg/L, whereas some cladocerans were highly tolerant to pesticide contamination. Glyphosate was the most influential driver of community properties, with biomass and community structure responding rapidly but recovering unequally over time. Zooplankton biomass showed little resistance when first exposed to glyphosate, but rapidly recovered and even increased with glyphosate concentration; in contrast, richness declined in more contaminated ponds but failed to recover. Our results show that the biomass of tolerant taxa compensated for the loss of sensitive species, conferring greater resistance upon subsequent exposure; a rare example of pollution-induced community tolerance in freshwater metazoans. Overall, zooplankton biomass appears to be more resilient to agrochemical pollution than community structure, yet all community properties measured in this study were affected at glyphosate levels below common water quality guidelines in North America.

Resistance, resilience, and functional redundancy of freshwater bacterioplankton communities facing a gradient of agricultural stressors in a mesocosm experiment

“…The absence of a bacterioplankton response is also consistent with the weak or undetectable response of zooplankton biomass to imidacloprid pulses in the same experiment (Hébert et al, 2021). The invertebrate community in the experimental ponds was mainly composed of the zooplanktonic groups Cladocera, Copepoda and Rotifera, and only copepods declined over time after pulse 2, with no resulting effect in total zooplankton biomass (Hébert et al, 2021). Overall, these results indicate that the concentrations of imidacloprid applied in this experiment were not sufficient to strongly alter either zooplankton or bacterioplankton biomass or community structure.…”

“…Alternatively, the absence of a detectable response might be due in part to rapid degradation of imidacloprid in water, which fell below the limit of detection between pulses (Figure ). The absence of a bacterioplankton response is also consistent with the weak or undetectable response of zooplankton biomass to imidacloprid pulses in the same experiment (Hébert et al, 2021). The invertebrate community in the experimental ponds was mainly composed of the zooplanktonic groups Cladocera, Copepoda and Rotifera, and only copepods declined over time after pulse 2, with no resulting effect in total zooplankton biomass (Hébert et al, 2021).…”

“…Additional lake water was added on a biweekly basis (~10% of total volume) between May and August to ensure a continuous input of lake bacterioplankton, tracking seasonal changes in the source lake community, and to homogenize communities across ponds. The experiment reported here used 48 of these pond mesocosms from 17 August (day 1) to 28 September (day 43), and it is part of a collaborative experiment that also assessed responses of zooplankton in the same set of ponds (Hébert et al, 2021) and phytoplankton responses in a subset of these ponds for a longer period of time (Fugère et al, 2020).…”

Zooplankton assemblage structure and diversity since pre‐industrial times in relation to land use

“…This lack of correspondence between studies could be related to differences in taxonomic resolution, given that the positive correlation between FRic and agriculture across all 624 lakes was related to Daphnia pulicaria responses, a taxon that could not be identified to species level in this current subfossil study. Instead, we observed lower FRic values in highly impacted sites (Figure 5b), as would be expected given documented negative effects of intensive pesticide use on zooplankton diversity (Hébert et al, 2021; Relyea & Hoverman, 2008). Moreover, in contrast to all other α‐diversity indices, FRic did not decrease between time points (Table 2).…”

Environmental drivers of taxonomic and functional variation in zooplankton diversity and composition in freshwater lakes across Canadian continental watersheds

“…Meanwhile, in sites from the Hudson Bay basin (which includes the Canadian Prairies ecozone, where most of the extensive agriculture occurs in Canada), FRic was negatively related to agriculture as would be expected. Indeed, intensive pesticide use is of growing concern for freshwater ecosystems in agricultural regions with a variety of documented negative effects on zooplankton, including altered sex ratios, modified population dynamics, and reduced abundances or diversity (Hanazato 2001; Hasenbein et al 2016; Hébert et al 2021). However, a positive relation between diversity and agriculture‐related variables, as we report, has also been previously observed and ascribed to an increase in the relative biomass of small zooplankton species as the more efficient herbivores such as Daphnia are lost and energy transfer from phytoplankton to zooplankton is reduced (Havens and Hanazato 1993; Hanazato 1998).…”