Parasites and host movement behaviour

A few weeks ago, we talked about the three parasite-themed organized oral sessions at ESA 2018. When I attended the “Uniting Predator-Prey and Parasite-Host Theory” session, I saw Dr. Dave Daversa from the University of Liverpool give a talk for the first time. He was mostly talking about a neat meta-analysis regarding the effects of predators versus parasites on prey/hosts, but he mentioned some of his work about “behavioural fever” in amphibians infected by the chytrid fungus. I made a note to look up the paper he mentioned, but then I didn’t need to, because he made a trip to Virginia Tech a week later to give a talk focused on that work. So convenient! His dissertation work tells a great story about disease ecology and research conundrums and successes. I thought y’all might be as interested as I was, and Dave kindly agreed to write a guest post about that work for us. So, without further ado, here’s the story of Dave’s dissertation and more:

Many wildlife species can be observed moving across the landscape when spending time outdoors.  Observing the movements of their parasites is less straightforward. My head began to ache as I gazed at my field data.  I had been tracking the movements of alpine newts (Ichthyosaura alpestris) among a network of ponds in Central Spain in hopes of clarifying the spread of the pathogenic fungus parasite, Batrachochytrium dendrobatidis (Bd), known also as “chytrid” for the disease chytridiomycosis that it causes. Chytrid had reached global distributions and was decimating populations of its amphibian hosts.  How this microscopic fungus managed to spread across the landscape remained a mystery.

Alpine newts were ideal candidates for being chytrid vectors.  Newts were susceptible hosts of chytrid, but chytrid infections were not highly lethal to newts. Furthermore, newts routinely moved to different ponds during the breeding season, in contrast to most amphibians that tend to pick a pond and stay put.  Together, these traits screamed “superspreader”. By characterizing newt movements, I therefore expected to characterize the spread of chytrid as well. That is not what the data were indicating though.  Rather, the hundreds of newts that I followed exhibited only weak chytrid infections, if any, leaving no signature of infection spread among the ponds. What was going on?

For newts, even localized movements to neighbouring ponds mark a significant change in habitat from fully aquatic ponds to dryer, terrestrial habitat like the mossy grasslands that surrounded the montane ponds in Spain. Perhaps switching habitats affects chytrid in ways that inhibited its spread from pond to pond? Movement of hosts onto land reduces how frequently newts contact (i.e., are exposed to) infective chytrid spores because the spores rely on moist environments to survive. Given these moisture requirements, terrestrial activity may also compromise the ability of chytrid to grow on newts after infecting them.  Since seasonal terrestrial migrations of common toads (Bufo spinosus) at these same sites allowed them to recover from chytrid infections (read more here), these potential terrestrial effects did not seem so far-fetched.

My colleagues and I decided to bring newts into the lab to take a closer look at their movement and infections. Doing so uncovered convincing evidence that terrestrial activity was detrimental to chytrid. Firstly, frequent exposures that came with prolonged time in water were an important condition for infections to develop; infrequent exposures to even high concentrations of spores did not pose a high risk of infection.  Secondly, when we kept newts in terrariums, they contracted fewer infections than when we kept them in aquariums.  Any infections that did pop up in terrestrial newts were weak and didn’t last long, while those in aquatic newts were stronger and more robust.  Terrestrial activity therefore hindered chytrid in two ways: by reducing frequency of contact between newts and spores and by inhibiting survival and reproduction of chytrid on newts.

We then put newts in tanks with both land and water containing chytrid spores, allowing them to move freely between the two habitats, and we videotaped their activity for a week. Upon reviewing the videos we noticed an interesting pattern.  After about four days, just about the time it takes for chytrid to fully establish an infection, newts that contracted infections spent increasingly more time in the terrestrial habitats, particularly newts that developed severe infections.  Yet, newts that remained uninfected didn’t change their activity much. Chytrid infections appeared to cause newts to head for land, a behaviour that, as we showed previously, can kill off those infections.

The effects of terrestrial habitat, combined newt behavioural responses to infection, may be a reason why newts are not superspreaders of chytrid. To definitively determine that will, as always, require more research.  However, what is clear from this work is that behaviours exhibited during routine activities can play a big role in shaping parasitism risk, especially when those activities span multiple habitats.  Parasites in turn, may influence day-to-day behaviours more than one might expect.  So, the next time you are commuting to work, whether by car, bike or train, note the different environments you are traversing.  Consider how the commute might affect your encounters with parasites, and how those parasites could be actually influencing the route that you take.

Many thanks to Dave for sharing his work! He offered to give us a newt photo as a visual, but it’s been awhile since I tortured people with puns, so instead, ponder this: