Ecohydrological and Metacommunity Studies of Proliferative Kidney Disease Spread in Freshwater Salmonid Fish

Proliferative kidney disease (PKD) is a high-mortality pathology affecting freshwater salmonid populations in Europe and North America. Its causative agent, the myxozoan Tetracapsuloides bryosalmonae, has a complex life-cycle exploiting freshwater bryozoans (mainly Fredericella sultana) and salmonids as hosts. PKD has recently increased in incidence and severity, causing remarkable declines in fish catches. In addition, environmental change is feared to cause PKD outbreaks in regions at higher latitude and altitude, as warmer water temperatures exacerbate disease development and fish mortality. In this perspective, this Thesis develops an integrated approach, involving field and modelling work, for the prediction of the incidence of PKD in river basins.

In particular, the Thesis develops a novel spatially-explicit model of PKD epidemiology in riverine host metacommunities. The model, summarizing the current knowledge on disease transmission modes and parasite's life-cycle, accounts for both local population and disease dynamics of bryozoans and fish, as well as hydrodynamic dispersion of parasite spores and hosts along the river network. Model validation was attained through an integrated study of PKD in a prealpine Swiss river, where data on fish abundance, disease prevalence, concentration of primary hosts' and parasite's DNA in environmental samples (eDNA) and water temperatures were gathered at multiple locations within the catchment. In this context, a new method for predicting the spatial distribution of bryozoan density based on eDNA samples was developed. As water temperature is crucial to PKD severity, a deterministic, spatially-explicit water temperature model was formulated and tested on the case-study basin. The model, based on water and energy budgets at the reach scale, considers the effects of the spatial heterogeneity in environmental drivers, allowing the evaluation of gradients of daily mean water temperature along the river network.

Stability and sensitivity analyses performed on the local epidemiological model proved that the introduction of T. bryosalmonae in a disease-free community is very likely to trigger a PKD outbreak. Simulation experiments conducted on synthetic river network replicas showed that network connectivity engenders high PKD prevalence at downstream sites, while the speed of invasion fronts in disease-free environments is amplified by climate change. Moreover, patchily located bryozoan hotspots proved able to sustain the infection at the whole river scale. Validation on the case study confirmed the reliability of the epidemiological model, and identified the prediction of bryozoan distribution as a key direction for future research. In this regard, the developed eDNA transport model possibly opens avenues for the modeling of species distributions in freshwater ecosystems, also beyond the case of PKD. The spatially-explicit temperature model was shown to outperform traditional models based on local heat budgets. Such a tool is instrumental to several ecohydrological applications, from the identification of river reaches at highest PKD-related risk, to the assessment of habitat suitability of fish or other freshwater species. Overall, this Thesis bridges the fields of ecology, epidemiology, hydrology and mathematical modelling in order to produce an integrated study of PKD, in the perspective of grasping the factors allowing disease persistence and devising mitigation strategies.

SESTET: A spatially explicit stream temperature model based on equilibrium temperature

Enrico Bertuzzo, Luca Carraro, Andrea Rinaldo, Marco Toffolon

Stream-water temperature is a key variable controlling chemical, biological, and ecological processes in freshwater environments. Most models focus on a single river cross-section; however, temperature gradients along stretches and tributaries of a river network are crucial to assess ecohydrological features such as aquatic species suitability, growth and feeding rates, or disease transmission. We propose SESTET, a deterministic, spatially explicit stream temperature model for a whole river network, based on water and energy budgets at a reach scale and requiring only commonly available spatially distributed datasets, such as morphology and air temperature, as input. Heat exchange processes at the air-water interface are modelled via the widely used equilibrium temperature concept, whereas the effects of network structure are accounted for through advective heat fluxes. A case study was conducted on the prealpine Wigger river (Switzerland), where water temperatures have been measured in the period 2014-2018 at 11 spatially distributed locations. The results show the advantages of accounting for water and energy budgets at the reach scale for the entire river network, compared with simpler, lumped formulations. Because our approach fundamentally relies on spatially distributed air temperature fields, adequate spatial interpolation techniques that account for the effects of both elevation and thermal inversion in air temperature are key to a successful application of the model. SESTET allows the assessment of the magnitude of the various components of the heat budget at the reach scale and the derivation of reliable estimates of spatial gradients of mean daily stream temperatures for the whole catchment based on a limited number of conveniently located (viz., spanning the largest possible elevation range) measuring stations. Moreover, accounting for mixing processes and advective fluxes through the river network allows one to trust regionalized values of the parameters controlling the relationship between equilibrium and air temperature, a key feature to generalize the model to data-scarce catchments.

2019

Long-term impacts of nutrient control, climate change, and invasive clams on phytoplankton and cyanobacteria biomass in a large temperate river

Camille Roland Marie Minaudo

Recent studies suggest that climate change, with warmer water temperatures and lower and longer low flows, may enhance harmful planktic cyanobacterial growth in lakes and large rivers. Concomitantly, controlling nutrient loadings has proven effective in reducing phytoplankton biomass especially in North America and Western Europe. In addition, the impact of invasive benthic filter-feeder species such as Corbicula on phytoplankton has largely been overlooked in large rivers, leading to even more uncertainty in predicting future trajectories in river water quality. To investigate how nutrient control, climate change and invasion of benthic filter-feeders may affect phytoplankton biomass and composition, we assembled a large database on the entire water course of the River Loire (France) over three decades (1991–2019). We focus on cyanobacteria to provide an in-depth analysis of the 30-year trend and insights on future possible trajectories. Since 1991, total phytoplankton and cyanobacteria biomasses have decreased 10-fold despite warmer water temperature (+0.23 °C·decade−1) and lower summer flow (−0.25 L·s−1·km−2·decade−1). In the long-term, the contribution of planktic cyanobacteria to total biomass was on average 2.8%. The main factors driving total phytoplankton and cyanobacteria biomasses were total phosphorus (4-fold decrease), the abundance of Corbicula clams (from absence before 1998 to 250–1250 individuals·m−2 after 2010), the duration of summer low flows and the intensity of summer heatwaves. The River Loire constitutes an example in Europe of how nutrient control can be an efficient mitigation strategy, counteracting already visible effects of climate change on the thermal regime and flow pattern of the river. This may hold true under future conditions, but further work is needed to account for the climate trajectory, land and water use scenarios, the risk of enhanced benthic biofilm and macrophyte proliferation, together with the spread of invasive filter-feeding bivalves.

2020

Characterization of bacterial communities in Lake Geneva by comparing genetic and physiological methods

Coralie Chappelier

Over the last century, the level of atmospheric CO2 has increased to the highest concentrations on Earth within the past 800'000 years. Current predictions anticipate that the effects of greenhouse gases will lead to a rise in air temperature ranging between 1.4 and 5.8°C. Oceans and freshwater ecosystems absorb large quantities of CO2, but are sensitive to global climate change that directly influences water temperature and pH. Specifically, phytoplankton accounts for approximately 50% of the total photosynthesis on Earth, and contributes to the mobilization of CO2 through sinking or transferring fixed carbon to deeper water layers and sediments. Bacteria are among the most abundant entities in plankton and play a major role on the biological pump for the cycling of carbon and other elements. In order to understand and anticipate the response of aquatic ecosystems to climate change, we need to characterize how planktonic organisms respond and adapt to environmental change. In this project, we will merge microbial ecology and genomics with the ultimate goals of (i) characterizing current ecological niches of the operational taxonomic units highlighted in bacteria populations of Lake Geneva, (ii) identifying candidate adaptive genes responsible for adaptation of freshwater bacterial communities to contrasting freshwater habitats, (iii) projecting current bacteria distributions as a function of the expected change and (iv) identifying possible alterations in ecosystem functioning and services as a function of climate change. By doing this, we expect to contribute expanding our ability to characterize ecological niches using genetic data and sensitizing society about the importance of protecting freshwater ecosystems.

2020

Long-term impacts of nutrient control, climate change, and invasive clams on phytoplankton and cyanobacteria biomass in a large temperate river

Camille Roland Marie Minaudo

2020

SESTET: A spatially explicit stream temperature model based on equilibrium temperature

Enrico Bertuzzo, Luca Carraro, Andrea Rinaldo, Marco Toffolon

2019