Pollution and ecosystem adaptation to changes in the environment.

Does exposure to diffuse chemical pollution impair the ability of an ecosystem to respond to environmental fluctuations. In lakes, microscopic algae sustain the food web providing energy that support the life of superior organisms. Climate change is expected to increase intensity and frequency of fluctuations in environmental conditions. For example, stability of water column structure in lakes is key for the development of microalgae. Extreme weather mixes the water column and prevents the community to follow its natural progression. Algae naturally evolved to respond rapidly to these environmental variations. The diffuse burden of water chemical pollutants can however favour species of algae that are more tolerant to chemical pollution to the detriment of more adaptive ones. It is unlikely that pollution tolerant species are also those more able to efficiently respond to environmental changes. We have conducted experiments in lakes with different levels of nutrients and dissolved organic matter (from low production of algae (oligotrophic) to mid- (mesotrophic) and high productivity (Eutrophic). We grew natural microalgae communities confined in permeable microcosms directly in their lakes of origin and simulated eater column mixing. We treated the algae with chemical pollutants, and we observed their responses. In lakes that have low concentration of dissolved organic matter and low water acidity, chemical pollutants hindered biomass production and photosynthesis while favouring small-sized cells. These effects persisted for long time after stress was released. We investigated the fundamental mechanisms driving these community responses. We found that a recent ecological theory could predict observations. We developed a mathematical model of the phytoplankton community that assimilates this theory and used it to draw prediction on algae responses to contaminants. This is the first time such a theory was confirmed experimentally. Unlike in the mesotrophic and eutrophic lakes, contaminant exposure in the oligotrophic lake did not affect microalgae. We hypothesized that this was due to the peculiar water chemistry of this lake, and in particular the type of dissolved organic matter originating from the surrounding forest soils, in combination with the higher water acidity. Through laboratory tests we confirmed this hypothesis. These water conditions also prevented algae to evolve resistance to the chemical stress, because of the lack of a strong selection process. Our results represent an example of how the interaction of organisms, contaminants and environmental conditions determine responses and evolution of ecosystems. Next, we focused on assessing whether the observed community responses in the meso- and eutrophic lakes held the potential to affect resilience of freshwater ecosystems. Resilience can be seen as the ability of an ecosystem to revert to its typical state (e.g. biomass production, and biodiversity conditions) after being pushed by a stressor to a different one. We assessed resilience by looking at changes in the relative abundance of organisms of different size. Size is a fundamental trait of organisms relating to the way they utilize resources in the environment. We found that despite hindering biomass production and photosynthetic activity, contaminants were unlikely to affect microalgae resilience at the concentrations typical in European lakes. Finally, we focused on assessing whether historical exposure to chemical pollution results in adaptations of microalgae to grow in contaminated waters. We focused on a lake in a heavily impacted agricultural catchment in Sweden, historically exposed to herbicides. We collected sediments from this lake and a series of control lakes in the same region that were never exposed to herbicides. We germinated microalgae spores and resting stages from the sediments and grew them in the laboratory, obtaining communities that reflected the biodiversity of their native environments. We then exposed them to the same herbicide. We observed that present-day toxic responses were indeed affected by previous exposure history of the lakes. The community from the historically polluted lake grew equally well as the community from pristine areas in absence of the stressor. However, when the chemical stressor is applied, communities from historically contaminated lakes can express tolerant organisms. We linked this result to the concept of ecological memory and argue that chemical pollution has historically affected evolution of microalgae and development of water ecosystems.

We showed that pollutants at realistic concentrations can affect the ability of phytoplankton to recover from climate disturbance. Ecosystems historically impacted by chemical pollutants express microalgae that are more tolerant to these stressors, indicating their evolution has been historically influenced by contaminants. We invented new approaches to conduct studies on natural microalgae community directly in their environment. We developed a new model assimilating a novel ecological theory. This can be used to mechanistically predict ecosystem responses to pollution. Despite affecting microalgae productivity and community structure, pollution did not impact their resilience. This will help to better position exposure safety thresholds in environmental management. We found that dissolved organic matter from forest soils can prevent toxic effect in microalgae and development of tolerance. These results and outcomes reduce the gap between ecology and environmental toxicology.

Does exposure to diffuse chemical pollution impair the ability of an ecosystem to recover structures and functions following a disturbance event? The proposed research explores trade-offs between adaptation of phytoplankton communities to pollution and their adaptive capacity to recover after abrupt changes in environmental conditions. We define here adaptive capacity of a community its ability to restructure by ecological processes as a consequence of changing environment in order to maintain efficient use of resources, production and diversity. Through more frequent occurrence of extreme weather, climate change will result in increased disturbance on lake water column stability, affecting processes at the base of freshwater ecosystem functions and services, such as phytoplankton metacommunity structuring. We will conduct experiments in lakes using natural phytoplankton communities incubated in situ in innovative enclosures and simulate disturbance by mixing metacommunities from different depths of structured water columns. We will concomitantly treat the enclosures with realistic levels of contaminants and track the recovery process during post-disturbance by analyzing a complex set of eco/physiological traits over time. The rate of trait change, a proxy of adaptive capacity, will be compared between treatments and controls to assess the hypothesis that pollution hinders the capacity of the community to re-structure. We will investigate if such a response depends on lake contamination history by repeating the experiment in several lakes along a gradient of contamination. The occurrence of a negative relationship can suggest that communities from historically impacted lakes are better suited to cope with combined pollution and generic environmental stress as a result of ecological adaptation or evolution. Such a result can represent a direct evidence of the ongoing subtle impacts of diffuse sub-lethal pollution on freshwater ecosystem functioning.