In our Insights columns, we discover the story behind a recent publication in Functional Ecology. This week, Dr Alexandre Budria, of French Agency for Biodiversity, Brest, discusses his new Review, Beyond troubled waters: the influence of eutrophication on host–parasite interactions
Can you briefly explain your field of expertise and why it is important?
My primary field of expertise is parasite ecology, meaning that I am interested in the role of parasites in ecosystems and what they can tell us about human impact on the environment. This research is important to society in a number of regards. Most immediately, it can help managing wildlife and public health. This is especially relevant considering global change and the current crisis of emerging infectious diseases. As eutrophication is a leading cause of water impairment worldwide, exploring its influence on parasites seems relevant to societal needs, while also addressing fundamental questions.
Can you explain your research in layman’s terms or with one conceptual graph?
In layman’s terms, I am interested in how parasites can reflect human impact on the environment and can be used in environmental management. To this end, I studied how a major source of water pollution – artificial nutrient enrichment – can impact epidemics in wildlife.
How did your ideas for your review evolve during the project? Did you run into difficulties, and if so, how did you solve these?
During my PhD, I studied on the influence of eutrophication on sticklebacks and their parasites in the Baltic Sea. Monitoring of epidemics led to complex patterns that did not always fit the results we would expect based on previous studies available in the literature. Actually, this area of research is still new, in the sense that little is known regarding the influence of eutrophication on parasites. This led me to hypothesize a number of mechanisms that could explain our findings, some of which remain widely unexplored so far. As such, I decided to write a synthesis on the topic in 2016.

The main difficulty was first presenting the various mechanisms through which eutrophication can impact host-parasite interactions in a structured and comprehensive text (the few colleagues who read the first version of the manuscript clearly agreed on this point). Once the structure had been improved, the manuscript was still too long for the standards of the journal, but the editorial team did a very good job in spotting parts of the manuscript that could be shortened. This also dramatically improved the readability of the manuscript.
In your review, you mentioned a few knowledge gaps. Which of these would you hope to see bridged earliest?
There are quite a few open questions mentioned in the review indeed. I believe that recent research is doing a great job in providing insightful answers to how nutrient enrichment can influence host-parasite interactions, especially thanks to the inputs from ecological stoichiometry. In my opinion, very difficult question still remaining to answer is how eutrophication affects patterns of parasite diversity, notably because our knowledge on the topic is limited to a very few examples only and necessitates large monitoring campaigns. Another related question mentioned at the very end of the review still remains widely unexplored: the role of parasites on the eutrophication process. Recently, Brunner et al. (2017, PNAS) published a very interesting study on the matter which, I hope, will generate further research on the fundamental importance of parasites on ecosystem functioning. Some insightful results are also expected from studies on chytrid fungi and viruses infecting cyanobacteria.
Your study discusses the effect of direct and indirect responses of nutrient enrichment on parasite transmission in lakes. How did you initially make the difference in which responses are direct and which are indirect?
The notion of direct and indirect responses to nutrient enrichment is fundamental to our current understanding of the eutrophication process and is particularly well presented in the classic review by Cloern (2001, Mar.Ecol.Progr.S.). Direct responses include the most immediate changes observed in impacted waters (e.g. increased primary production), while the consequences of these changes cause secondary symptoms of eutrophication (e.g. oxygen depletion). I think that this fundamental view of eutrophication deserves further attention when studying host-parasite systems in eutrophied ecosystems, because it shows that a great number of mechanisms have the potential to deeply affect epidemics in impacted waters.
Your analysis highlights that change in just one condition in an ecosystem can cascade through the food web, with large consequences on the nature of the whole system. Calling on critical shift theory, would your analysis be able to indicate threshold levels of eutrophication? Perhaps more importantly, is there an easy way of restoring natural conditions once things have gone wrong?
Yes, things can indeed go very wrong, but not necessarily, as this depends on a number of factors (e.g. sources, strength and frequency of the disturbance, capacity of resilience of the considered ecosystem). Current research in environmental parasitology notably shows how parasites can be early state indicators of human impact in ecosystems and might help defining or refining such thresholds for some systems. The use of parasites as bioindicators was notably considered during the early development of the Foodweb indicators required by the EU Marine Strategy Framework Directive, but not enough data is currently available to develop reliable indicators based on parasites (G. Safi, pers. com.). Indeed, we are just starting to explore the use of parasites in environmental management. In other words, there is currently a wide range of questions to be answered, some quite applied, others very fundamental, which is, I feel, very exciting.
What would be your message be for conservationists and policy makers based on your results? You call for mesocosms approaches and a more collaborative effort in monitoring, but could you go even further in your advice?
I think conservationists and policy makers are well aware of the importance of predators such as wolves or bears in ecosystems, but they should also consider that parasites might be just as important as predators in the environment. To this end, it is necessary to expand our knowledge on parasite ecology, through experimental and monitoring approaches, and especially consider the point of view of a parasite.
One final question- when you’re not at work, what do you like to do in your free time?
When I am not working, I love to fish, especially for trout and pike. Thanks to my grand-father, I have pursued this passion since my childhood, and I find the feeling of releasing a nice fish in a beautiful river priceless.
Click here for the article Beyond troubled waters: the influence of eutrophication on host–parasite interactions or the free plain language summary here (no subscription needed).
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