Responses of freshwater phytoplankton exposed to chemical contaminants : Tolerance acquisition, physiological trade-offs and environmental controls

Rizzuto, Simone and Jones, Kevin and Zhang, Hao and Nizzetto, Luca and Leu, Eva (2022) Responses of freshwater phytoplankton exposed to chemical contaminants : Tolerance acquisition, physiological trade-offs and environmental controls. PhD thesis, Lancaster University.

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Abstract

Chemical pollution of freshwaters represents a large-scale environmental problem which needs to be reduced to avoid global or regional change. Integrating ecological theory in ecotoxicological approaches is instrumental to understand how the widespread presence of contaminants influence biota in complex natural systems. In this thesis, the concept of ecosystems as complex adaptive systems (CAS) is integrated as a guiding framework into ecotoxicological approaches, to unravel the implications arising from adaptation of freshwater phytoplankton to waterborne chemical contamination under realistic environmental conditions. The first experimental study examined the influence of two key environmental factors (dissolved organic matter – DOM and pH) on the responses, tolerance acquisition and associated trade-offs in a population of phytoplankton exposed to sub-lethal concentrations of a mix of twelve organic micropollutants (pharmaceuticals and personal care products - PPCPs) over multiple generations. DOM reduced the toxic effect of the mix of PPCPs at environmentally relevant concentrations and modulated tolerance acquisition and associated trade-offs in the microalgal population, possibly by complexing micropollutants. The concept of ecological memory (EM) recognizes the importance of previous stress encounters in promoting community tolerance and thereby enhances ecosystem stability, provided that gained tolerances are preserved during non-stress periods. It was hypothesized that the recruitment of tolerant species can be facilitated by imposing an initial sorting process (conditioning) during the early stages of community assembly, which should result in higher production (biomass development and photosynthetic efficiency) and stable community composition. To test this, phytoplankton resting stages were germinated from lake sediments originating from two catchments that differed in contamination history: one impacted by longterm herbicide and pesticide exposures historically contaminated lake) from an agricultural catchment, compared to a low-impacted one (near-pristine lake) from a forested catchment. Conditioning was achieved by adding an herbicide (Isoproturon, which was commonly used in the catchment of the historically contaminated lake) during germination. Afterwards, the communities obtained from germination were exposed to an increasing gradient of Isoproturon. As hypothesized, upon conditioning, the phytoplankton assemblages from the historically contaminated lake were able to rapidly restore photosynthetic efficiency (p > 0.01) and became structurally (community composition) more resistant to Isoproturon. The communities of the near-pristine lake did not yield these positive effects regardless of conditioning. Moreover, assemblages that displayed higher structural resistance concurrently yielded lower biomass, indicating that benefits of EM in increasing structural stability may trade-off with production. The results indicate that EM can foster ecosystem stability to a recurring stressor. The third study investigated how EM influences the functions (growth) and structure (diversity) of early-stage assemblages of phytoplankton by using a trait-based approach. Phytoplankton assemblages were germinated from the sediments of two lakes which differed in contamination history: a historically contaminated lake and a forested, near-pristine one, in presence/absence of Isoproturon. Results showed that the functions and responses of the two communities were dependent on the previous history of contamination, confirming the study’s expectations. The EM of previous contamination allowed the community originating from the sediments of the historically contaminated lake to maintain growth and diversity when germinated in presence of the herbicide. In contrast, sub-lethal concentrations of the herbicide caused negative effects on the growth and diversity of the community from the near-pristine lake. The last two studies arose from the need to explain the results observed in the first study, where the DOM appeared to decrease the toxicity/bioavailability of some PPCPs on microalgae. The main hypothesis was complexation mediated by the DOM lowering toxic effect or bioavailability, however the experimental design used in the firsts study did not allow the verification of this hypothesis. Hence, the binding of DOM with contaminants was examined in detail in two different studies, using an improved dialysis equilibrium-method. The method’s performance was critically evaluated through a series of rigorous QA/QC criteria, across a range of DOM concentrations and pH conditions, using the herbicide Isoproturon as model compound. Good measurement reproducibility, mass balance closure, and successful transmembrane equilibrium of ISU were obtained. The improved equilibrium-method was therefore applied to examine the interactions between DOM and a selection of compounds from the mix of PPCPs used in the first study, under the same conditions of DOM and pH. Association with DOM was confirmed for the more hydrophobic PPCPs at high pH. The results suggest the binding was driven by i) the presence of carboxylic groups of PPCPs, ii) high pH shifting the structural configuration of DOM, making it more suited to bind some of the PPCPs. A nonlinear change of binding capacity with increasing DOM concentration was also observed among the tested PPCPs. The thesis demonstrates that the concept of ecosystems as complex adaptive system can be an important addition in moving ecotoxicological approaches towards “chemical stress ecology”. Recommendations are made in support of future research to further support this transition.