Engineered nanoparticles interact with nutrients to intensify eutrophication in a wetland ecosystem experiment

Abstract

Despite the rapid rise in diversity and quantities of engineered nanomaterials produced, the impacts of these emerging contaminants on the structure and function of ecosystems have received little attention from ecologists. Moreover, little is known about how manufactured nanomaterials may interact with nutrient pollution in altering ecosystem productivity, despite the recognition that eutrophication is the primary water quality issue in freshwater ecosystems worldwide. In this study, we asked two main questions: (1) To what extent do manufactured nanoparticles affect the biomass and productivity of primary producers in wetland ecosystems? (2) How are these impacts mediated by nutrient pollution? To address these questions, we examined the impacts of a citrate-coated gold nanoparticle (AuNPs) and of a commercial pesticide containing Cu(OH)₂ nanoparticles (CuNPs) on aquatic primary producers under both ambient and enriched nutrient conditions. Wetland mesocosms were exposed repeatedly with low concentrations of nanoparticles and nutrients over the course of a 9-month experiment in an effort to replicate realistic field exposure scenarios. In the absence of nutrient enrichment, there were no persistent effects of AuNPs or CuNPs on primary producers or ecosystem productivity. However, when combined with nutrient enrichment, both NPs intensified eutrophication. When either of these NPs were added in combination with nutrients, algal blooms persisted for >50 d longer than in the nutrient-only treatment. In the AuNP treatment, this shift from clear waters to turbid waters led to large declines in both macrophyte growth and rates of ecosystem gross primary productivity (average reduction of 52% ± 6% and 92% ± 5%, respectively) during the summer. Our results suggest that nutrient status greatly influences the ecosystem-scale impact of two emerging contaminants and that synthetic chemicals may be playing an under-appreciated role in the global trends of increasing eutrophication. We provide evidence here that chronic exposure to Au and Cu(OH)₂ nanoparticles at low concentrations can intensify eutrophication of wetlands and promote the occurrence of algal blooms.

Keywords: Egeria; algae; algal bloom; aquatic ecosystems; copper nanoparticles; eutrophication; gold nanoparticles; macrophytes; multiple stressors; nanomaterial; nutrients.

Fig. 1.

Total nitrogen (a, b), dissolved organic carbon (c, d), total phosphorus (e, f) in the water column in the nutrient enriched treatments only. The AuNP (a, c, e) and CuNP (b, d, f) nutrient enriched treatments are displayed in different panels along with their respective control treatment means and 95% confidence intervals are presented and significant effects are indicated by asterisks.

Fig. 2.

Chlorophyll a concentration on a log-scale in the surface water over the 9 months of the experiment. The different treatments are displayed in different panels along with their respective control treatment: (a) AuNP-Ambient Nutrient, (b) AuNP-Nutrient Enriched, (c) CuNP-Ambient Nutrient, (d) CuNP-Nutrient Enriched. Significant effects are indicated by an asterisk. The horizontal line represents the threshold at which a major algal bloom event was observed.

Fig. 3.

a) Cumulative number of algal bloom days in each treatment. Asterisks denote significant (P ≤ 0.001) difference between each NP treatment and the control at the same nutrient level. b) Photographs of the aquatic zone of three representative mesocosms in the Nutrient Enriched Control, AuNP and CuNP treatments at six time points during the experiment. Photographs of mesocosms experiencing a major algal bloom are indicated with the letters “AB”. The small white forms that we can observe on Day 76, 117 and 138 in the control mesocosm are Egeria densa flowers.

Fig. 4.

Dissolved oxygen saturation at the surface water before dawn over the 9 months of the experiment. The different treatments are displayed in different panels along with their respective control treatment: (a) in AuNP-Ambient Nutrient, (b) AuNP-Nutrient Enriched, (c) CuNP-Ambient Nutrient, (d) CuNP-Nutrient Enriched. Asterisks denote significant (P ≤ 0.05) difference between NP treatment and control of each sampling date.

Fig. 5.

Ecosystem metabolism: Gross Primary Productivity (GPP, top) and Ecosystem Respiration (ER, bottom) in the AuNP and Control-Nutrient Enriched treatments measured at discrete times between Day 86 and the end of the experiment. Asterisks denote significant (* P ≤ 0.05, ** P ≤ 0.01) difference between NP treatment and control of each sampling date.

Fig. 6.

Egeria densa stem photosynthesis (top) and respiration (bottom) rates in the Ambient Nutrient treatments (right) and in the Nutrient Enriched treatments (left). Asterisks denote significant (* P ≤ 0.05, *** P ≤ 0.001) difference between NP treatment and control at the same nutrient level of each sampling date.

Fig. 7.

Egeria densa growth rates in the Ambient Nutrient treatments (right) and in the Nutrient Enriched treatments (left). Asterisk denotes significant (P ≤ 0.05) difference between NP treatment and control at the same nutrient level of each sampling date.

Fig. 8.

Gold (a) and copper (b) concentrations (mg of metal per kg of plant, dry weight) in Egeria densa stems. Note that the y axis scales are different between the two graphs. Different letters indicate significantly different dates in the same treatment. Within each nutrient level, treatment means of the three sampling dates annotated by the same letters are not discernible at α = 0.05.

Fig. 9.

Conceptual diagram representing our hypothesis of how nutrient availability in the water column and the competitive interactions between macrophytes and algae are modified under (A) nutrient enrichment alone compared to (B) nutrient enrichment combined with NPs additions.