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:

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Parasite Ecology at ESA 2018

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ESA 2018 in New Orleans was filled with opportunities to learn about some great parasite ecology research, meet new people, and catch up with existing colleagues. (Speaking of colleagues, Chelsea Wood won the Unofficial Parasite Ecology Cartoon Contest with her animated Haeckel parasite drawings!) ESA 2018 was especially great because there was not one, not two, but THREE organized oral sessions about parasites! Julia Buck and Grace DiRenzo (both of UCSB) kindly agreed to help me write this post summarizing the three organized oral sessions for those who couldn’t be at ESA (and for those who had to choose between sessions, since two were unfortunately scheduled concurrently).

OOS 25: Uniting Predator-Prey and Parasite-Host Theory Under a General Consumer-Resource Framework

Organizer: Dr. Julia Buck (author of this summary)

Co-organizers: Tara Stewart Merrill, Dr. Armand Kuris

A year ago, I watched jealously on twitter as everyone attending ESA 2017 posted about the amazing science being presented there. One tweet in particular described an invited talk by Andy Dobson, and upon reading his abstract, I realized that I needed to organize a session for ESA 2018. I decided that applying predator-prey theory to parasite-host dynamics would be a broad enough topic to attract a large audience, while still being narrow enough to have meaningful boundaries. My session was motivated by the need for more cross-talk between predator-prey and parasite-host ecologists.

I invited Armand Kuris to parasitize the first couple of minutes of my talk so that he could introduce the consumer framework in Lafferty and Kuris 2002 (TREE). Once we had distinguished the different types of consumers from one another, I delved into their direct and indirect effects. Like predators, parasites can cause DMIEs through their consumptive effects and TMIEs through their nonconsumptive effects, but unlike predators, they can also cause TMIEs through their consumptive effects. Next up, Dave Daversa presented the results of a meta-analysis on the nonlethal effects of predators vs. parasites. In general, predators elicit stronger avoidance responses than parasites, but their net effects may be similar in magnitude than those of predators because the response to parasites is integrated through time. Next up, Janet Koprivnikar presented the results of several studies that Dave included in his meta-analysis. Specifically, she found that tadpoles avoid parasites and predators, but when forced to choose between them, they prefer to forage in the presence of parasites – the less lethal threat. Although avoidance of trematode cercariae by tadpoles might be motivated by fear, Caroline Amoroso showed that parasite avoidance by lemurs might be more strongly motivated by disgust, an emotion previously thought to be unique to humans.

Next up, Kevin Lafferty presented our theoretical work on the functional and numerical responses of predators vs. parasites, showing that whether we detect the functional or numerical response depends, in part, on study scale. Mike Cortez also presented theoretical work showing that differences between predators and parasites whose victims compete for resources are due, in part, to the fact that predators are immediately lethal to prey but parasites are not immediately lethal to hosts. Next Cherie Briggs shook things up by asking where all the parasitoid talks have gone. Parasitoids are similar to predators in that they are lethal to their victims, but they attack a single host during a life stage and establish a durable relationship with it, so they are a type of infectious agent. Apparently, ecologists used to study (and publish on) parasitoids in ecology journals, but most parasitoid work is now found in entomology journals. Tom Raffel presented a fascinating comparison of the thermal biology of parasitism vs. predation – a topic I never would have considered if not for this session. Finally, Andy Dobson and John McLaughlin presented their work on parasites in food webs. Andy applied the Lafferty et al. 2015 general consumer-resource model to the Yellowstone food web, while John compared predators vs. parasites in terms of their diversity, biomass, and impact on network structure.

Overall, the attendance at and reception to the talks in this session was excellent. Despite the fact that several speakers panicked when they realized what they had agreed to (sorry!), I found these talks inspiring. Thanks to all who presented, and to Tara Stewart Merrill for moderating.

OOS 32: Novel Modeling Approaches in Disease Ecology

Organizer: Dr. Graziella DiRenzo (author of this summary)

Co-organizer: Dr. Cherie Briggs

In disease ecology, there are so many statistical and mathematical models that can be used to answer a number of ecological/evolutionary questions that it can be difficult to pick “the right one”. There likely isn’t a right model – because as George Box said, “all models are wrong, but some are useful”. When I started my post-doc with Dr. Cherie Briggs at UCSB, I started thinking about compiling an organized oral session at ESA where we could learn about a bunch of cool and emerging models in disease ecology.  

We kicked off the session with Monique Ambrose, a graduate student, talking to us about spillover events and R0 in monkeypox from Dr. Jamie Lloyd-Smith’s Lab at UCLA. She had very interesting methods on how to account for a number of parameters in her likelihood model – and this was one of the only wildlife applications we saw in the session along with Dr. Kim Pepin. Dr. Kim Pepin spoke to us about methods the USDA-APHIS is trying to treat the leading edge of rabies in the eastern United States with vaccines. When is the best time to vaccinate raccoons? Questions like this and others were answered during her talk.

The remainder of the talks fell into the category of vector-borne diseases. Dr. Miguel Acevedo began with a great anecdote from a class he taught, telling us that a set of students from a class did not like a host-predator model because it was too simple BUT they liked the simple output,  reminding us about the tradeoffs in complexity, realism, and interpretation. Dr. Michaela Martinez followed-up with the awesome data collection methods they are employing in their lab to understand polio outbreaks and other human diseases from medical records. And along those same lines, Dr. Felicia Magpantay explained the differences that vaccination methods can have on the number of infected hosts using simulated data.

Dr. Mercedes Pascual, Dr. Victoria Romeo, Dr. Nicole Mideo, and Dr. Leah Johnson discussed malaria and other vector-borne diseases. Who knew the interactions between mosquitoes and temperature could make models so complicated?

We ended the session with an amazing presentation on integral projection models by Dr. Jessica Metcalf followed by a discussion/Q&A with Dr. Hal Caswell. This name may sound familiar because of his work on population matrix models.  

In the end – it was a successful session with between 80 and 150 people in the room at any particular talk. The presenters were engaging, animated, and made the material they were discussing easily accessible to everyone in the audience, regardless of career stage. Thank you to everyone who came, participated, and tweeted!!!

OOS 33: Parasite Conservation in the Face of Global Change: Opportunities, Challenges, and Next Steps

Organizer: Dr. Skylar Hopkins (author of this summary)

Co-organizer: Dr. Colin Carlson

When I told people about our parasite conservation session, most had the same questions: “Conserving parasites? Aren’t they bad? Why would you want to do that?” I’m happy to admit that some parasites are “bad” for people, our domesticated species, and wildlife. For instance, I don’t want to be infected by Guinea worm and I don’t want my dog to be infected by heartworm. But I also don’t want to get eaten by a lion, and I still think that large carnivore conservation is important. Therefore, I think that the question that we need to answer is not, “Should we conserve parasites?”, but rather, “Which parasite species should we conserve, and how will we accomplish those conservation goals?” Though parasites have historically been neglected and even persecuted by conservation research and practice, scattered groups of people have begun to tackle the pressing parasite conservation questions in the past decade or so, and my co-organizer (Colin) and I thought it was finally time to get a bunch of us in one place to try to coalesce as a subfield. Thus, roughly one year ago, the plan for the Parasite Conservation OOS was hatched! On extremely short notice, we cobbled together an international group of people from diverse institutions and career stages, and we were so pleased with the outcome at ESA! Here’s a synopsis of the session:

Giovanni Strona opened our session with a rousing discussion of community structure, community disassembly, and (co)extinction rates: he previously found that the order in which host species become extinct determines parasite co-extinction rates, and more recently, he found that removing parasites from systems accelerates biodiversity loss via a positive feedback loop, whereas reintroducing parasite species slows total biodiversity loss. But we might lose fewer parasite species than we expect if parasites can switch host species instead of going down with the ship. For instance, Jorge Doña told us that even in groups that are thought to be highly specific, like the bird feather mites that he studies, ~5% of symbionts are found on unexpected host species, suggesting that (1) the bipartite networks that we base our co-extinction simulations on might contain many stragglers; and (2) host switching deserves further study, because even though major switches are rare, they are a means by which symbionts might escape co-extinction. Speaking of specificity and host range, Tad Dallas followed with a discussion of how well we can estimate host range from host–parasite co-occurrence data, concluding that 20-40% of parasite ranges are currently unknown. Despite these big gaps in our knowledge of parasite ecology (e.g., host specificity), we might be able to use general parasite biodiversity patterns to make parasite conservation decisions. For instance, Chelsea Wood reminded us that a general law in parasite ecology is that parasite biodiversity increases with host biodiversity, suggesting that parasite and host biodiversity hotspots will coincide. However, Chelsea also showed us how fishing can decouple this classic relationship; when complex life cycle parasites are lost with their fished hosts, parasite and fish diversity are no longer correlated! And Mark Torchin showed us that unlike the classic latitudinal gradients that we see in free-living species, parasite biodiversity and interaction intensity can be higher in temperate regions.

If we already know a lot about host and parasite distributions, we can specifically model how global change will affect primary and secondary parasite extinctions, which Colin Carlson told us would be better than just relying on predictions from simulations with bipartite networks. And then I argued that no matter which kinds of models we’re using, we’re going to want to test their predictions regarding parasite extinction patterns on long-term, high-resolution host–parasite datasets; I used Chesapeake Bay fish parasites to illustrate how museum specimens might let us build those long-term datasets retrospectively. Kayce Bell followed my talk with a much broader discussion of all of the parasite museum collections available for parasite ecology and conservation research. And then Roger Jovani reminded us that not all symbionts are parasites, like feather mites that clean bird feathers (!!), and we should really embrace all symbionts for conservation purposes. And finally, Kelly Speer reminded us that symbionts even have their own hyper-symbionts, like microbes living in bat flies, and environmental changes that alter symbiont microbiomes might be important conservation considerations.

Overall, it was a very fun session, and I’m so excited for the new collaborative plans that we all put in motion.

Again, thanks to everyone who participated in and/or came to our parasite-themed organized oral sessions at ESA 2018! And if you want to schedule a parasite-themed OOS for next year, you’ll need to submit your proposal by September 13th, 2018. If you have questions about the process, we’d be happy to try to answer them!

Unofficial ESA 2018 Parasite Ecology Cartoon Contest

ESA 2018 is right around the corner, so it’s time to start polishing up your best cartoons for the Unofficial ESA 2018 Parasite Ecology Cartoon Contest. My favorite cartoonist will be awarded an almost entirely worthless prize (i.e., some publicity for their cool science and bragging rights for a year). I might also pick a real prize to send you in the mail, if I get some good recommendations.

To participate, all you need to do is put a cartoon in your talk. The cartoons don’t need to be funny! They also don’t need to be your personal artwork; borrowing with permission and attribution is fine. I’m just looking for cartoons that help communicate your work to the audience. That being said, anything punny is worth mega bonus points.

I believe that I’m going to be at ESA Monday-Thursday. If you have an amazing cartoon that you want me to see, you can tell me in advance in the comments, via email, or on Twitter, and I’ll try my best to be there!

To anticipate some questions:

Can you use cartoons from this site, if you use proper attribution? Yes! You don’t need to ask me in advance.

Can the judge be swayed by offers of free lattes or future academic positions? No! (Except yes. So much yes.)

Good luck!!