Guard Crab Functional Diversity

Continuing my theme of Odes to Awesome systems, I want to tell you guys about one of my favorite animals: guard crabs.  These crabs live on corals and deter starfish predators from attacking the corals by pinching the starfish.  The guard crab cute factor is out of this world:

Photo credit: Bryan Mayes

I’ve been fascinated by guard crabs ever since I read the really thorough studies of Peter Glynn from the 1970’s and 1980’s.  He did all kinds of work showing that guard crabs protect corals from predation by Ancanthaster starfish.  Not all coral species have guard crabs, and Peter Glynn showed that populations of unprotected coral species are decimated during Ancanthaster outbreaks, while protected species suffer few losses.  Furthermore, protected corals sometimes indirectly defend unprotected corals, because starfish won’t cross barriers of protected corals.

Previously, it seemed like some guard crab species were a lot better at protecting corals than others.  This is true in other defensive symbiont systems, too (e.g., ants that protect Acacia trees).  But I just read a really cool study by McKeon and Moore (2014) that shows that the slacker symbionts may not be as lazy as we thought!  Specifically, small guard crabs aren’t very good at protecting corals from starfish predation.  However, small guard crabs are good at protecting corals from smaller corallivores, like predatory snails.  Furthermore, big crabs are no good at protecting against those smaller corallivores.  (This is a cool parallel to the paper I talked about last week, where hydroids protect hermit crabs from limpets but not blue crabs.)

So, corals need functionally diverse guard crab communities – communities with large and small guard crabs – to be protected from multiple corallivore species.  Awwwwesome!



McKeon CS, Moore JM (2014) Species and size diversity in protective services offered by coral guard-crabs. PeerJ 2:e574.

50 Shades of Symbionts

When we “sell” our science to journals and policy makers and even the general public, we often pitch our work in broad, abstract strokes (“trait-mediated indirect effects of…”) and/or in a highly applied context (“acid runoff tolerance of two functionally important species”).  I’m not saying that’s wrong.  But I think that most scientists – and most non-scientists – fall in love with ecology because the systems (the actual plants/animals/etc.) are cool, and then we have to gloss over the insanely awesome systems that we study in order to talk about the general applicability of our results.  Well, no more brushing cool systems under the rug!  Parasite Ecology is taking action by doing a few weeks of Odes to Awesome Systems.

The best way to prove that you have an awesome study system is to graphically illustrate the unquestionable adorableness of your study species.  EXHIBIT A – Hermit Crabs with Pink Afros:

Photo from here.

BUR-100721 Gewone heremietkreeft, Pagurus bernhardus met Ruwe zeerasp, Hydractinia echinata

Photo from here.

Did you know that hermit crabs have over 500 symbiont species?  More than 100 of those symbionts are obligate symbionts, meaning that they are only found on/in/with hermit crabs.  I learned that while perusing a heartwarming tale entitled, “The Not So Lonely Lives of Hermit Crabs: Studies on Hermit Crab Symbionts.

One of those obligate symbionts is the pink afro (also called “snail fur”) in the photos above.  Those colonial hydroids (genus Hydractinia) are found exclusively on gastropod shells, and especially shells that are occupied by hermit crabs.  Unsurprisingly, scientists who go out and find hermit crabs with pink afros just have to ask this question:  do the hydroids affect their hermit crab hosts?

As I’ve blogged about before (here and here), some symbionts protect their hosts from natural enemies.  Buckley and Ebersole (1994) wondered if the hydroids could protect hermit crabs from being eaten by blue crabs.  They found that blue crabs were just as likely to attack hermit crabs with or without hydroids, so the hydroids didn’t have any effect on predator preference.  However, blue crabs were much more successful when attacking hermit crabs with hydroids.  Having hydroids actually made hermit crabs more susceptible to predation!

BUT… gastropod shell strength wasn’t associated with the presence of hydroids.  So what was it about hydroids that made it easier for blue crabs to successfully attack hermit crabs?  Well, a second, parasitic symbiont – shell-boring Polydoran worms – decreased shell strength, and those worms were more likely to be present if the shells had hydroids.  So, one symbiont mediated the occurrence of a second symbiont, which in turn mediated blue crab predation success.  Nuts!


This could be the part of the story where we conclude that hydroids decrease hermit crab fitness.  But remember how most symbioses are context-dependent, where the strength and even the sign of the interaction depends on environmental and ecological conditions?  Well, it turns out that hydroids protect hermit crabs from a different enemy: ectoparasitic slipper limpets.  Therefore, Buckley and Ebersole (1994) suggest that the relationship between hydroids and hermit crabs changes throughout the year, depending on whether blue crabs and/or limpets are abundant.  That really emphasizes the importance of studying symbioses across broad time scales and under varying ecological and environmental conditions.

So, there you have it.  You can’t figure out hermit crab ecology without thinking about hermit crab symbionts.   Pink afros are more than just fashion statements.


Buckley WJ, Ebersole JP (1994) Symbiotic organisms increase the vulnerability of a hermit crab to predation. J Exp Mar Bio Ecol 182:49–64.

Resistance vs. Tolerance to Parasites

In disease ecology and parasitology, we often talk about a host’s ability to resist or tolerate parasites.  What’s the difference?  Resistance is a measure of a host’s ability to reduce parasite establishment.  For instance, imagine that two hosts are each exposed to 10 parasites.  In the first host, 8 of those parasites manage to evade the host’s immune system and successfully establish, and in the second host, only 2 of the parasites successfully establish.  The second host is more resistant to infection.  Tolerance is a measure of a host’s ability to “deal with” a given parasite load.  Now imagine that two hosts each have 5 parasites.  Those parasites hardly affect the first host’s ability to survive or reproduce, but the same number of parasites causes a huge reduction in the second host’s ability to survive and reproduce.  The first host is more tolerant.  (A really great figure from Raberg et al. (2007) sums this up.)

What determines a host’s ability to resist or tolerate parasites?  Good question!  This is a hot topic for research.  Body condition (i.e., overall health) likely has something to do with resistance and tolerance.  And then there is that ever-present explainer of all the things: genetics (Raberg et al. 2007).  But today, I want to talk about something else.  Do paternal effects influence resistance and tolerance?

In a recent, awesome, open access study, Kaufmann et al. (2014) exposed three-spined stickleback “sires” (fathers/dads/sperm-makers) to nematodes.  Then they used sperm from either these exposed sires or unexposed sires to fertilize strickleback eggs.  Here’s what they found: when the sires were exposed to parasites, the eggs were less likely to develop and the juveniles were less likely to survive.   But if they took surviving offspring from both exposed and unexposed sires, and then exposed some of those offspring to nematodes, the offspring from exposed sires had higher tolerance to parasites.  Specifically, parasites had a big effect on the body condition of offspring from unexposed sires, but no effect on offspring from exposed sires.  Neat!  Surprisingly, parental effects didn’t influence offspring resistance to parasites.  Unsurprisingly, genetics also played a role in both resistance and tolerance.


Raberg, L., D. Sim, and A.F. Read. 2007. Disentangling Genetic Variation for Resistance and Tolerance to Infectious Diseases in Animals. Science 318(5851): 812-814.

Kaufmann, J., T.L. Lenz, M. Milinski, and C. Eizaguirre.  2014. Experimental parasite infection reveals costs and benefits of paternal effects. Ecology Letters. (Open access.)

2014 October Parasite Ecology

Happy October, Everyone!  As you may have noticed, I’ve been slacking in the post department for the past few weeks.  I’m about to cross the finish line on a big deadline – even if I have to wade through crocodile infested swamps while battling fire-breathing dragons to get there – and then I’ll get back to my regular post schedule.  But in the meantime, I thought I’d give you guys a little parasite ecology paper parade.  So, here’s what’s new in parasite (and other symbiont) ecology:

1) If you’re a mutualistic symbiont living on a host, there’s a good chance that you’ll be at a competitive disadvantage in comparison to parasitic symbionts living on the same host.  That’s because you’re providing the host with some service – which presumably isn’t something that you can freely provide – but the parasites aren’t providing any services.  So, how is it that mutualistic species commonly coexist with parasitic ones?  How do mutualistic species evolve in the first place?  Here are some potential answers.

2) High parasite incidence in female guppies at sites with high predation risk may be explained by the fact that female guppies are more likely to shoal at high predation sites, and high host densities can lead to increased parasite transmission.

3) Speaking of the role of density in parasite transmission, for vectored parasites, we expect “encounter dilution,” where the number of vector attacks per host declines with host density (if the vector density remains constant).  Increase host density => decrease risk.  But hosts may also be stressed out and thus more susceptible to parasites at high host densities.  Increase host density => increase risk.  When you combine encounter dilution and density-dependent reductions in immune response, what happens to parasite infection?

4) Mutualists select for later flowering in plants while herbivores select for earlier flowering, so together, there’s no net selection on flowering phenology.  But both mutualists and herbivores select for longer spurs.  Uhm, awesome!

5) Are the strengths of priority effects fixed?  Of course not: everything is context-dependent!  For instance, the presence of parasites can reduce priority effects.

6) And just for fun: are pubic lice going extinct?

Preparing for Disease Ecology Prelims

Here’s a little post for all you PhD students nearing your qualifying/comprehensive/preliminary exams.  If I were asked to study disease ecology for such an exam, this is what I would know:

Who are the most influential modern day disease ecologists (or parasite ecologists)?  You might start with my list of the most prolific parasite ecologists in the 21st century.

What is the disease triangle?

What were Koch’s Postulates?

What proportion of Earth’s species are parasites/pathogens?  What proportion of the total biomass in an ecosystem is parasite biomass?  I have some related posts: here and here.

Do parasites/pathogens regulate host populations?  Somehow, I think I I’ve only blogged about this once

How do parasites affect food webs?  You might start here and here.

What are the differences between microparasites and macroparasites?  Here.

What are the differences between predators, parasites, and parasitoids?  Here.

Why are macroparasites aggregately distributed among hosts, and why does it matter?  Here and here and here.

What are the hypotheses regarding the evolution of virulence?  I haven’t blogged about that much, but there’s a bit here.

What are SIR models?  SI models?  SIS models?  SEIR models? Vector transmission models?  

What is R0?  What happens when R0 > 1 and when R0 < 1?  How can you reduce R0?  What is the critical proportion of susceptible individuals that needs to be vaccinated so that R0 < 1?  Somehow, I haven’t covered this in any detail.  But I have a cute cow cartoon about herd immunity.

What are density dependent and frequency dependent parasite transmission?  Here and here.

Are there invasion thresholds is disease systems? Link to PDF.

Is culling a viable strategy for disease management?  See previous two questions.

What role does contact heterogeneity play in disease transmission?  What are superspreaders?  What is a superreceiver? Here, here, and here.

Is disease risk related to biodiversity?  What is the dilution effect?  Amplification effect? Neutral effect?  Here and here, for starters.

What are the main types of pathogen transmission? E.g., direct vs. indirect, sexually transmitted, vectored, trophically transmitted, etc.

Explain the concept of parasite manipulation of host behavior.  Is it adaptive?  What are the consequences for communities/ecosystems?  Here and here, but there is waaay more material out there.

Do hosts and parasites coevolve?  Is there evidence of parasite-mediated selection?

What is parasite-mediated competition?  Does it happen in real systems?

Are there general laws in parasite ecology?  PDF link.

Did I miss anything?  Add in the comments or shoot me an email!

How do parasites affect tadpole behavior?

Like I said last week, I saw a cool talk at ESA about tadpole behavior and trematode parasites.  And since I liked it, I thought that YOU might like it, too!

When tadpoles can sense that predators are nearby, they alter their behavior by becoming less active.  That’s a good way to avoid getting eaten.  But do tadpoles alter their activity levels when parasites are nearby?  Preston et al. (2014) say no!  This seems counter intuitive, because some parasites, like the trematode Ribeiroia ondatrae, can cause a lot of damage to the host tadpole, and even kill it.  But like we’ve discussed before, macroparasites (like Ribeiroia) tend to have intensity dependent effects on the host, so that pathology increases with the number of parasites.  And it might not be worth altering your behavior if you’re probably just going to get a few parasites, and they probably aren’t going to do much harm to you anyways.  Furthermore, just because parasites are nearby doesn’t mean that they’ll be able to successfully infect the tadpole, because tadpoles have other anti-parasite tactics, like immune responses.


But what about after the tadpoles get infected by the parasites?  Do the parasites affect tadpole behavior then?  You’ll just have to go check out the paper to find out!


Preston, D.L., C.E. Boland, J.T. Hoverman, and P.T.J. Johnson. 2014. Natural enemy ecology: comparing the effects of predation risk, infection risk and disease on host behaviour. Functional Ecology.

Parasite Ecology at ESA 2014

I didn’t go to all of the parasite ecology talks at ESA 2014, and I can’t even fit all the ones that I went to into one blog post.  But for those of you who weren’t there – and for those who were but just want to revel in your memories of awesome ESA 2014 parasite ecology – here are some of my favorites.  Also, just for fun (and because I may or may not have an addiction that I could totally give up at any time, I swear), I gave everyone a relative parasite cartoon score.

Monday was the ESA Early Career Fellows Symposium.  Meg Duffy and Pieter Johnson both gave brilliant parasite ecology talks.  Meg Duffy showed that parasite infection can reduce host feeding rates in Daphnia, which paradoxically ends up increasing host density via interactions with the algal resource (i.e., a hydra effect).  She had some sweet Daphnia + fungus cartoons, so I give her an 8 on my cartoon scoring scale (second place!).  Pieter Johnson showed that amphibian host diversity can increase parasite richness (“diversity begets diversity”) and decrease Ribeiroia infection risk (=dilution effect), and he emphasized that parasite richness and infection risk aren’t the same thing.  (Speaking of Ribeiroia, have you guys seen this tshirt?  You’re welcome.)  I may have missed some cartoons while I was scribbling in my notebook, but I think he had some silhouettes of snails and vertebrates and some fluorescent cercariae cartoons:  4.  

Christopher Johnson talked about competition between two mutualistic species (i.e., two butterfly species) for a shared resource (i.e., nectar from the host plant) – in other words, a symbiont competition model, where the resource is the host or services/resources from the host.  And instead of R*s, there were M*s.  And then there were phase diagrams and talk of symbiont species coexistence.  Yeah.  Amazing. 

On Tuesday, I saw a talk by Eric Schauber, who used agent based modeling to consider how the “need to be social” affects among group pathogen transmission.  Awwwesome.  He had some cartoon vertebrates (goats?), so that’s a 2. 

On Wednesday, Max Joseph gave a really cool talk about how a negative relationship between “disease risk” and host richness can emerge from a model that treats hosts as habitat patches, where symbionts have different niche requirements.  Oh, and so can a positive relationship between host and parasite richness!  I’d just been lamenting the loose way that people refer to “disease risk,” so I was really glad when he stressed the importance of quantifying what we mean by disease risk when talking about the dilution effect.  Get ready, World.  Big things are happening with dilution effect theory.

Angela Brennan asked:  what is the right scale to look at the impacts of host density on disease transmission?  That’s a tricky one…

Cat Searle gave a neat talk about invasive species, their competence as hosts, and their role in pathogen transmission, using a Daphnia model system.  She had some cartoons of space aliens as her invasive species, so that’s a 6.  Oh, and for all of the undergraduates reading this blog, she’s looking for grad students!

Continuing on the Daphnia vein, Alex Strauss looked at the outcomes of introducing diluting host species that both reduce parasite transmission to the focal host species and compete with the focal host species.  And DING DING DING DING!  For his cartoons of Daphnia, algae, fungi, and other tiny organisms (score = 10), Alex wins the Best Parasite Cartoons of ESA 2014 Award!! 

Finally, on Thursday, I really liked Dan Preston’s talk about tadpole behavioral responses to predators and parasites.  But I’m going to try to blog that one next week, so you’ll have to stay tuned!