My new favorite symbiosis: boxer crabs!

I can’t believe that I only just learned about the glorious symbiosis between boxer crabs and anemones. The crabs hold one tiny anemone in each claw, and they use the anemones to defend themselves from predators. The anemones benefit from increased access to food because they’re constantly being waved about.



And look at these dance moves!

That tiny cheerleader’s got game.

I’m in love.


Mutualism vs. Symbiosis

Ecologists sometimes use the terms “mutualism” and “symbiosis” interchangeably, and I wish that they would not do so! I recently bought a copy of Judie Bronstein’s new book about mutualism, and the first two chapters are devoted to defining the terms mutualism and symbiosis, and distinguishing between the two. Here, I’ll outline the main points. For a longer treatment of this topic, check out the book!

Mutualism is an ecological interaction between at least two species (=partners) where both partners benefit from the relationship.

Symbiosis is an ecological interaction between at least two species (=partners) where there is persistent contact between the partners.

In symbioses, one partner is often smaller, lives on or in the larger partner, and has a shorter lifespan that the larger partner. The smaller partner is a symbiont, and the larger partner is a host.

Not all mutualisms are symbioses. Some mutualisms are non-persistent, like when a pollinator very briefly visits a flower and then never returns to that flower again. Additionally, not all symbiosis are mutualistic. For instance, parasites are also symbionts.

A few months ago, I posted this useful classification scheme for thinking about different types of ecological interactions. The two axes are the “relative duration of association” and “net effect of the relationship on the ‘host.’” Mutualisms are any relationships on the right-hand/positive side of the net effect of the relationship on the ‘host’ axis, regardless of where the relationship falls on the vertical axis. Symbioses are relationships at the ‘top’ of the relative duration of association axis – where much of the symbiont’s lifespan is spent in association with the same host – regardless of where the relationship falls on the horizontal axis.


World’s coolest vector of infectious pathogens

If you weren’t born before the 1980s, you probably don’t know what an entire street lined with elm trees looks like, because Dutch Elm Disease spread through both Europe and North America in the early and middle 1900s and decimated elm populations. Pockets of elms still persist in places like Amsterdam and Winnipeg, but it is a never-ending battle to keep those trees disease free.

So, which highly virulent pathogen is responsible for totally reshaping temperate tree communities? The culprit is a fungus (well, a few fungal species, actually) that is vectored by a tiny and totally adorable beetle (well, a few beetle species, actually). Ladies and gentlemen, I present to you the horrible, terrifying, death-spreading elm bark beetle:


Joking aside, these beetles are completely amazing. They have symbiotic relationships with fungi, where the fungi range from weak parasites to commensalists to mutualists depending on the beetle species, the fungus species, and perhaps environmental conditions. In the simplest cases, bark beetles act as transport vessels for the fungi, without getting anything in return for their dispersal services. In contrast, ambrosia beetles cultivate fungus gardens in the galleries that they excavate in dead trees, and the beetles consume the fungus as their sole source of nutrition. When the young beetles emerge from their natal galleries to disperse, they take fungal spores with them to their new galleries. Isn’t that cool?! Whereas fungus farming has evolved just once each in ants and termites, it has evolved many times in the ambrosia beetles (Hulcr and Dunn 2011). And get this: at least one species of ambrosia beetle is eusocial!

If bark beetles and ambrosia beetles typically only excavate in dead trees, why did the elm bark beetle go rogue and start attacking live elms? Well, it turns out that it wasn’t an isolated event. There are more than a dozen examples of the beetles shifting from dead to live trees in recent history, with catastrophic results for some of the tree species that are being attacked (Hulcr and Dunn 2011). Humans are unintentionally shipping these beetles and their fungal associates to novel regions around the globe. And in novel regions, bark beetles searching for dead trees by following volatile cues might mistake living trees for dead trees. Or, as Hulcr and Dunn (2011) put it, some living trees might smell dead. Even if the beetles realize their mistake and don’t completely excavate a gallery in a living tree – choosing instead to go search for a dead tree – their initial boring activities might inoculate the tree with the fungal symbionts.

But here’s a conundrum: if a fungal symbiont transported by bark beetles doesn’t really affect trees in the beetle’s native range, why should the fungus be highly virulent in the introduced range? After all, the beetles can only introduce a little fungal innoculum into a giant living tree. Well, it may be that the majority of the tree pathology is caused by the tree’s response to the pathogen, rather than the direct actions of the fungus, just like the animal immune response to pathogens is often worse for the host than the actual damage caused by the pathogen. It may be that trees wildly overreact to the novel fungal pathogen by expanding the walls of the xylem so much that the tree ends up dying.


Anyways, bark beetles are really cool vectors, and I think disease ecologists should pay more attention to them.


Hulcr, J., and R.R. Dunn. 2011. The sudden emergence of pathogenicity in insect–fungus symbioses threatens naive forest ecosystems. Proceedings of the Royal Society B 278: 2866–2873.

Bears Indirectly Affect Plant Fitness

If you haven’t seen it yet, there’s a really cool paper in Ecology Letters about the indirect effects of bears on ecological communities (Grinath et al. 2015). Did you know that bears will eat ants? Well, they will! Especially during periods when they are food limited. And when bears disturb ant nests, the ants stop tending the leaf and tree hoppers (=herbivorous insects) that they farm for honeydew. Without ants patrolling nearby, tree hoppers experience higher predation pressures from other arthropod predators, like lady beetles and spiders. And when the densities of herbivorous insects decline, plant fitness increases. So, by eating ants, bears can increase plant fitness! Nuts!


I glossed over some of the details of this story, such as variation in the effects of bears across years. To get all of the details and to see some cool structural equation modeling, go check out the paper!


Grinath, J.B., B.D. Inouye, and N. Underwood. 2015. Bears benefit plants via a cascade with both antagonistic and mutualistic interactions. Ecology Letters 18(2): 164-173.

Sloths, their moths, and poo

Besides my typical holiday posts, this is going to be the last post of 2014. Where did the time go?! To celebrate the end of another awesome year of parasite ecology, I’m going to finish with one of my favorite symbiont stories of the year: sloth, their moths, algae, and poo.

I bet you guys have heard about this one, because it was in the mainstream news a bunch when the paper came out. Therefore, instead of summarizing the paper for you, I’m just going to say that it’s awesome, and you can read a summary here. You can also see a cute cartoon version of the story here. And of course, the citation for the paper is below.


Pauli JN, Mendoza JE, Steffan SA, Carey CC, Weimer PJ, and Peery MZ. 2014. A syndrome of mutualism reinforces the lifestyle of a sloth. Proceedings of the Royal Society B – Biological Sciences 281(1778): 20133006

Caterpillar Campfire

(Prepare yourselves. This post is about the sexiest paper that I have read in a long time.)

Many plants are covered in tiny hairs, called trichomes, which defend the plant by trapping insects. These can be hooked trichomes that snag insects, or glandular trichomes that produce secretions that the insects stick to. These trichomes may be beneficial because they trap and kill insects that might harm the plant. But they also seem somewhat detrimental, because predatory insects (e.g., lady beetles) that might benefit the plant by killing herbivorous insects (e.g., aphids) might also get stuck in the trichomes and die (Eisner et al. 1998).

However, some predatory arthropods can avoid getting stuck in the trichomes. For instance, the common tarweed has glandular trichomes, but it is still visited by five types of predatory arthropods (Krimmel and Pearse 2013). Interestingly, those predatory arthropods will eat both dead and living insect prey. AND GUESS WHAT?! Just like plants use extrafloral nectaries and food bodies to attract ant defenders, the dead insects trapped in the sticky trichomes of the tarweed attract those five predatory arthropods. Those predators reduce herbivory from a caterpillar by 60%, and that reduced herbivory leads to greater plant fitness.  A. Maze. Ing. Go read the paper. It’s beautiful.

Fun facts from the paper:

20-30% of vascular plants have glandular trichomes. So, this specialized predator attraction may be a widespread phenomenon.

Individual plants had up to 40 insect corpses at a time!!



Eisner T, Eisner M, Hoebeke ER. 1998. When defense backfires: Detrimental effect of a plant’s protective trichomes on an insect beneficial to the plant. PNAS 95(8): 4410-4414.

Krimmel BA, Pearse IS. 2013. Sticky plant traps insects to enhance indirect defense. Ecology Letters 16: 219–224.

The benefits of attracting many symbiont species

Textbook examples of mutualisms usually involve two interacting species; for instance, honey bees and clover. But of course, one host may have many mutualists (e.g., bees, butterflies) and one mutualist may have many hosts (e.g., clover, blueberries). In many cases, the benefits of having multiple possible host species are obvious. For instance, for ants that eat tasty elaiosomes and disperse plant seeds, it would be hard to get by while specializing on the seeds of only one plant species, because those seeds would only be available for part of the year. But how does the host benefit from having many symbiont species?

In ant-plant interactions, one plant species may have individual visitors from many ant species. For instance, the shrub Urera baccifera receives visitors from 22 facultative ant species, which visit to harvest food bodies and/or fruits (Dutra et al. 2006). Similarly, the yellow alder (Turnera ulmifolia) receives visitors from 24 facultative ant species, which visit to harvest seeds with elaisomes and/or to feed at extrafloral nectaries (Cuautle et al. 2005). While they’re on the plant, these ants can protect the plant from herbivores, like caterpillars. And finally, there may be multiple ant species visitors to a given plant species even when the associations are obligate: for instance, Acacia drepanolobium may be inhabitated by one of four ant species at any given time (Palmer et al. 2010).

Ok, but why so many species of ant visitors? Why shouldn’t the plant sanction any partners except the most beneficial species? This is still an active area of research, but at least part of the answer is that different ant species vary in the services that they provide to the plant. For instance, ant species may be more of less aggressive defenders, more or less likely to disperse seeds, more or less likely to farm scale insects, etc. (You might remember that this is true for guard crabs, too, where big crab species are good at protecting corals against starfish, while small crab species are good at protecting against vermetid snails.) Ant species also vary in how costly they are to harbor. For instance, one species may be a good defender, but it may also sterilize the host plant (e.g., Stanton 1999). So, a plant’s lifetime fitness may be determined not only by the guild of ant species that visits the plant during its life, but also on the timing and order in which those species visit the plant (Palmer et al. 2010). For instance, having sterilizing symbionts when you’re young can actually increase lifetime plant fitness. Isn’t that wild?



Cuautle M, Rico-Gray V, Diaz-Castelazo C (2005) Effects of ant behaviour and presence of extrafloral nectaries on seed dispersal of the Neotropical myrmecochore Turnera ulmifolia L. (Turneraceae). Biological journal of the Linnean Society 86: 67-77.

Dutra HP, Freitas VL, Oliveira PS (2006) Dual Ant Attraction in the Neotropical Shrub Urera baccifera (Urticaceae): The Role of Ant Visitation to Pearl Bodies and Fruits in Herbivore Deterrence and Leaf Longevity. Functional Ecology 20(2): 252-260.

Palmera TM, Doak DF, Stanton ML, Bronstein JL, Kiers T (2010) Synergy of multiple partners, including freeloaders,increases host fitness in a multispecies mutualism. PNAS 107(40): 17234–17239.

Stanton ML, Palmer TM, Young TP, Evans A, Turner ML (1999) Sterilization and canopy modification of a swollen thorn acacia tree by a plant-ant. Nature 401:578–581.

Myrmecophytic Plants and Their Ants

You can find ants and plants in almost every terrestrial habitat on the planet. Both groups can be incredibly abundant, so it isn’t surprising that ants and plants interact a lot. But some plants and ants have intimate symbiotic relationships that go far beyond the occasional interaction. Some of my favorite ecological stories involve these symbioses, and I’m going to post those stories in the coming weeks. But this week, I just want to introduce you to the system and let the insane photography skills of Alex Wild bring these organisms into your life.

Myrmecophytic plants: Who are they, and what do they provide their ant symbionts?

There are many genera of myrmecophytic plants, including flowers, shrubs, trees, and even ferns. These plants vary widely in the degree to which they invest in their ant symbionts. Below is a list of the structures that plants have evolved to provide their ants with resources, but not all ant-plants have all of these structures.

Domatia: Domatia are hollow structures that the ants can use for nests. Depending on the plant species, these domatia may be hollow stems or spines. For instance, check out this hollow thorn on an Acacia tree and the hollow base of this epiphytic plant. Both are homes for ants!


"Pseudomyrmex peperi"


Extrafloral nectaries: Many plants provide nectar rewards in their flowers in order to attract pollinators. Ant-plants may also have extrafloral nectaries – structures that provide nectar but that are not associated with flowers. On ant-plants with domatia and active ant colonies, these extrafloral nectaries can feed resident ants. On ant-plants without domatia, these nectaries can attract ant visitors. Here are two gorgeous ants feeding at an extrafloral nectary.


Food Bodies: Ants can’t just survive on nectar; they need resources other than sugar, too. Some ant-plants have evolved to produce food bodies that contain proteins or lipids that ants can harvest for those vital nutrients. Here’s an ant harvesting one such food body.


Plant-ants: Who are they, and what do they provide their plants?

There are also many genera of ants that have symbiotic relationships with their plants. These ants can be facultative or obligate symbionts (meaning that they are only found living on plants), depending on the species. In the coming weeks, I’ll talk a lot more about the services that ants do (and do not) provide to plants, but here are the main points:

Defense: Plant-ants are feisty plant protectors! They can bite and sting herbivores or even throw the herbivores off the plant. Plant-ants will also attack competing plants. For instance, they will bite encroaching vines or inject neighboring plants with formic acid. (Yeah. For real. Look up Devil’s Garden.) Here are some ants getting rid of a vine, and some different ants hauling away an intruder ant.



Nutrients: When ants die and defecate, they fertilize their plants. (I bet you can imagine this one without a photo. Also, arboreal earthworms are a thing, and plants eat their poop, too. You’re welcome.)

Seed Dispersal: Some plants produce seeds with tasty exterior food bodies called elaiosomes. The ants collect these seeds and eat off the elaisomes, then put the seeds in their waste piles. During this process, the seeds are dispersed, and they’re also protected from predators while they’re in the ant nests.


Aren’t plant-ants and ant-plants cool?! You should check out Alex Wild’s website for more awesome photos. Stay tuned for more on plant-ant ecology next week!

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.

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.

How beneficial are defensive symbionts?

(This post is late. Sorry, Folks! In my defense… snail dissection. So. much. snail. dissection.)

In my aphid cartoons thus far, Sal the Aphid has been bragging about how she has H. defensa. But just how awesome is it to harbor defensive bacteria? Like we said last time, when aphids get attacked by parasitoid wasps, aphids with H. defensa are more likely to survive than aphids without H. defensa. That seems like a pretty big bonus provided by the symbionts. We might expect natural selection to then favor aphid lineages with symbionts, leading to domination by lineages with H. defensa. But that isn’t what we see. Instead, only some aphids have H. defensa – the symbionts are maintained at intermediate frequencies. So, if defensive symbionts are so great, then why don’t all aphids have them?

In some earlier work, researchers found that H. defensa may not always be beneficial for aphids. For instance, when no parasitoids are present, the frequency of H. defensa in aphid populations declines, suggesting that H. defensa may be costly to maintain (Oliver et al. 2008). So, Vorburger et al. (2013) set out to determine whether the cost of harboring H. defensa is constitutive, induced, or both. That is, is H. defensa always costly, regardless of parasitoid presence (constitutive cost), does the cost come after a parasitoids attack and H. defensa kill the parasitoid larvae (induced cost), or both?

To test this question, Vorburger et al. (2013) exposed aphids with and without H. defensa to attacks by parasitoid wasps. The first 2/3 of the aphids that the wasps attacked were put in an “attacked” treatment group, and the aphids that the wasps did not attack were put in an “unattacked” treatment group. And then Vorburger et al. (2013) kept track of aphid survival and reproductive output.

Like we said last time, when aphids had H. defensa, they were more likely to survive a wasp attack. But when aphids weren’t attacked by wasps, the aphids with H. defensa had reduced fitness in comparison to aphids without H. defensa. That’s the constitutive cost we mentioned before. For aphids without H. defensa, attacked aphids had lower lifetime reproduction than unattacked aphids. That makes sense, of course. But get this: for aphids with H. defensa, attacked aphids had higher lifetime reproduction than unattacked aphids. That’s the opposite of an induced cost! It’s an induced benefit!

So, what caused the “induced benefit”? Well, Vorburger et al. (2013) aren’t sure. But they have one amazing hypothesis. They suggest that maybe when a wasp injects all that venom into an aphid, it kills off a bunch of the H. defensa. That is, the induced benefit is to reduce the constitutive cost of harboring H. defensa by killing off some of those costly symbionts. In that case, H. defensa isn’t sounding so nice afterall, is it? 

I rest my case: parasites and parasitoids are crazy awesome.

Oh, and the paper is open access! Check it out!



Oliver, K.M., J. Campos, N.A. Moran, and M.S. Hunter. 2008. Population dynamics of defensive symbionts in aphids. Proc. R. Soc. B Biol. Sci. 275:293–299.

Vorburger, C., P. Ganesanandamoorthy, and M. Kwiatkowski1. 2013. Comparing constitutive and induced costs of symbiont conferred resistance to parasitoids in aphids. Ecology and Evolution 3(3):706-13.