Why are caterpillars hairy?

Why is it advantageous to be a hairy caterpillar? One answer can be found in a beautiful paper by Sugiura and Yamazaki (2014). They put five species of caterpillars with various amounts of hairiness in containers with carabid beetles that naturally prey on caterpillars. The carabid beetles were always successful when attacking the smooth/hairless caterpillar species, and it usually only took beetles one try to successfully catch the caterpillar. When attacking a short-haired caterpillar species, the carabid beetles were still always successful, but it took them more tries. And when attacking a long-haired caterpillar species, the carabid beetles were only successful ~50% of the time. Even when they were successful, it took beetles more attempts to catch the caterpillars. Therefore, it looked like long hair protected caterpillars from beetle attacks. To test that idea, Sugiura and Yamazaki (2014) gave the long-haired caterpillars haircuts, so that the hairs were shorter than the beetles’ mandibles. The beetles were then way more successful at attacking the caterpillars with haircuts than the long-haired caterpillars! Now that is sexy science.

So, long-haired caterpillars are out there multiplying like crazy while their short-haired neighbors are getting mown down by beetles, right? Actually, having hairs may be a trade-off. Hairy caterpillars are more likely to be attacked by parasitoids, and a higher diversity of parasitoids attack hairy caterpillars than smooth caterpillars (Stireman and Singer 2003)! It might be beneficial for parasitoids to stick their eggs in hairy caterpillars because the eggs+caterpillars will be less likely to be eaten by a predator before the parasitoid emerges than if the caterpillar is smooth. Or it may be that hairy caterpillars – which are usually not cryptic – are easier for parasitoids to find. Either way, these papers have changed my life.

References:

Stireman, J.O., and M.S. Singer. 2003. Determinants of parasitoid-host associations: insights from a natural tachinid-lepidopteran community. Ecology 84(2): 296-310.

Sugiura, S., and K. Yamazaki. 2014. Caterpillar hair as a physical barrier against invertebrate predators. Behavioral Ecology 25(4): 975–983.

Predator vs. Parasite vs. Parasitoid vs. Mutualist– A Simple Classification Scheme

One of the most frequently accessed posts on this blog defines the terms “predator,” “micropredator,” “parasite,” and “parasitoid” and then presents a classification scheme for differentiating among those natural enemies (Lafferty and Kuris 2002). If you haven’t read that post yet, I recommend taking a look before you read this one. I obviously fancy the dichotomous key presented in the previous post quite a bit. However, it is not be the best classification scheme for all situations. For example:

1. Check out Britt Koskella’s comments on the previous post – it is difficult to classify the bacteriophages that she studies using that classification scheme.
2. The previous key may be difficult to use for educational purposes. For instance, it requires explaining castration and trophic transmission, which are concepts that might be unnecessarily complicated for explaining the distinction between parasites and predators to non-specialists.
3. The previous key only deals with natural enemies, so we can’t use it to explain how mutualists and commensalists fit into this group of trophic relationships.
4. The previous key doesn’t show how relationships can vary with life stages, ecological conditions, and environmental conditions.
5. The previous key doesn’t have any pictures of snails on it. (Priorities.)

Therefore, having an additional classification scheme that specializes in some of the aforementioned areas would be useful. And – you guessed it – one was recently(ish) published (Parmentier and Michel 2013)! This classification scheme uses two continuous variables to designate relationships: the relative duration of the association (RDA) and the fitness effects on the ‘host.’

The relative duration of association ranges from 0 to 1, where 0 means that the ‘symbiont’ (including predators) spends none of its lifetime associated with the ‘host’ (or prey), and 1 means that the symbiont spends all of its lifetime associated with the host. For instance, predators and micropredators have RDA’s close to zero – a lion spends only a small portion of its life with a single zebra prey. Conversely, an adult trematode parasite (the worm in the orange section of the figure) will spend that entire life stage in association with a single host. The RDA is the Y axis on the figure below.

In recent months, we’ve talked a lot about the fitness effects that symbionts have on their hosts. Briefly, symbionts may have both negative and positive effects on hosts, and it is the net effect that determines how we classify the relationship. However, the net effect can vary with ecological and environmental conditions (see here, here, and here). Therefore, whenever we place a point on this graph, we need to remember that it might slide left or right as conditions vary.

Parasitoid wasps spend the entirety of their larval life stage in the host, and they ultimately kill the host. In this figure, parasitic castrators – like the trematodes that castrate snails – end up in the same region as the parasitoids. And this is where bacteriophages and Cordyceps fungi would fall out, too. However, like we discuss in the previous post, the term “parasitoid” is probably not a good one for this group, because that term is usually used to refer specifically to the unique life cycles of parasitoid wasps. In this figure, it means any parasite that reduces host fitness to zero.

Predators like lions, frogs, and crayfish also reduce prey fitness to zero. However, micropredators and herbivores (e.g., mosquitoes and cows) are special classes of predators that do not kill their prey. Then there is a group of animals that consume plants, but are probably more appropriately classified as parasites because they spend the majority of their life span (or a single life stage) on a single host plant. Therefore, things that eat plants will typically fall out somewhere between the aphids and the micropredators. (I should note that herbivores can have more than minimal impacts on host plant fitness, but many grazers have small impacts.) Similarly, Mark Siddall – the man who went on a quest for the hippo ass leech – doesn’t like classifying leeches as micropredators, because some spend most of their time on a single host. Therefore, most leeches would also fall out somewhere along that line between aphids and mosquitoes. Except, yaknow, the ones that are actually predators, and fall out near the lions.

On the mutualism side of things, we have symbionts like pollinators, which are only very briefly associated with each host; they’re like micropredators, but with positive fitness effects on their hosts. And then there are symbionts that are associated with single hosts for most of their lifespans, like ants on Acacia trees or guard crabs on corals. But again, remember that those relationships might shift left on the X axis as conditions vary.

Speaking of which, finding an example of a commensalist is hard. I used the example of epibionts on hermit crab shells, which help protect the hermit crabs from some predators but make the hermit crabs more susceptible to other predators. The net effect is unclear, but the positive and negative effects might balance out to a zero net effect.

So, there you have it. I think this figure should be really useful, especially as a general framework.

References:   

Lafferty, K.D., and A.M. Kuris. 2002. Trophic strategies, animal diversity and body size.  TREE 17(11): 507-513. (Direct link to PDF download)

Parmentier, E., and L. Michel. 2013. Boundary lines in symbiosis forms. Symbiosis 60: 1-5.

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.

Reference:

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 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!

Reference:

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.

Godzilla Parasites

WARNING: GODZILLA SPOILERS ARE CONTAINED WITHIN THIS POST.

A few weeks ago, I went to see Godzilla.  I hadn’t looked up the plot summary or anything beforehand, so imagine my surprise when out of the giant pulsing “spore” (ahem, egg) emerged something that looked a lot like a cross between a giant water bug and Alien…not Godzilla.  And then imagine my UTTER GLEE when they said that the thing that was not Godzilla was a parasite.  Swoon.  I immediately conjured up all kinds of plot possibilities, and I couldn’t wait to see how the parasites attacked Godzilla!

But then I quickly realized that the “parasites” were not parasites at all.  The parasites acquired energy from radioactive material.  For instance, they ate nuclear warheads.  And that alone doesn’t make them parasites.*  It makes them autotrophs.  I thought I might have missed the parasite explanation, so after the movie, I did some googling.  But all I could find was some people saying that the parasites (or their young) might try to feed on Godzilla’s radioactive energy.  I would totally buy that, if the parasites had searched for Godzilla in the movie.  But instead, Godzilla searched for the parasites.  In fact, he was their “predator.”  WHAT?!  Yo, Hollywood.  You need a parasite ecology consultant?  HMU.

So, I wrote you guys a different plot, with actual Godzilla parasites in it.  Except that they aren’t parasites, per se.  They’re parasitoids.*  Enjoy!

—–

The female parasitoid hatches from an egg in a mine in the Philippines.  The female parasitoid goes to the Janjira nuclear plant to feed and causes a giant explosion.  A lady dies, and it’s sad.  The female parasitoid forms a chrysalis in the wreckage.

Sometime in the next 15 years, the other egg from the mine in the Philippines is taken to the USA to be studied and whatnot.  Then the radioactive body of the male parasitoid – which is thought to be dead – is stored in Yucca Mountain.

After 15 years, the female parasitoid emerges from her chrysalis.  She has wings!  (Yes, it is the male who has wings in the movie, but I don’t like it that way.)  She destroys a bunch of stuff and kills a dude and it’s sad.

The male (he’s alive!) and female parasitoids start communicating via echolocation (ok, whatever, I’ll go with it).  They start trying to find each other, stopping only to ransack ships and whatnot so that they can eat radioactive material.  When they find each other, the male fertilizes the female.  The male also gives her a nuptial gift of a nuclear warhead, because that was really cute.  Then he dies because he’s a male and he no longer has a purpose in life.  ONE MONSTER DEAD.  Huzzah!

Now the female needs a host for her eggs.  So, while armed forces are trying to shoot her to bits, she uses her highly adapted sensory apparatus to seek out Godzilla.  When she finds Godzilla, she stabs her ovipositor (yes, she has one of those now) into Godzilla’s body cavity and deposits a single egg.

(And you guys thought my artwork was limited to snails!)

Then the female parasitoid tries to fly off to find another Godzilla so that she can lay another egg, because that’s what parasitoids do.  But Godzilla grabs her head and breathes plasma down her throat, and she dies. SECOND MONSTER DEAD.  Huzzah!

The world starts to rejoice because all the parasitoids are dead, but suddenly San Francisco is being trampled by Godzilla!  Someone left some giant war heads in San Francisco, and Godzilla is being manipulated by the parasitoid larvae into finding and eating more radioactive material!  Oh no!  But wait, one of the nuclear warheads has an analog detonator thingy, so the parasitoid’s EMP abilities can’t stop it from detonating now that it has been activated!  Godzilla eats it!  1 hour and 29 minutes later, Godzilla and the parasitoid within explode.  ALL THE MONSTERS ARE DEAD!

Some soldier and his lady kiss and stuff.  The end!

*If you don’t remember the difference between a parasite, a predator, and a parasitoid, check this out.

Some Definitions: Predator vs. Parasite vs. Parasitoid

Despite nearly one year’s worth of posts about parasite ecology, this blog has never defined the term ‘parasite.’  D’oh!  You might think, “Pft, the definition is obvious!”  But actually, it isn’t, and it isn’t without controversy, either.  I’m going to talk about a bunch of types of natural enemy, and then I’ll present a really good dichotomous key at the end.

Predator:

Let’s start with predators.  Like parasites, predators are organisms that acquire energy by taking that energy from other organisms.  Therefore, we have a relationship that positively affects one organism (the predator) and negatively affects the other organism (the prey).  Predators have these important characteristics:

1)      One predator eats multiple prey during the predator’s lifetime.

2)      Predators tend to be bigger than their prey.

3)      Predators tend to kill their prey.

Micropredator:

You’ll notice that I said that predators “tend to” be bigger than their prey and “tend to” kill their prey.  They don’t always!  A very good example of this is a vampire bat that takes blood meals from cows.  A single vampire bat will take blood meals from multiple cows during its lifetime.  It is eating multiple prey, therefore, it is a predator.  But it doesn’t kill the cows, and it isn’t bigger than them.  It’s a micropredator.

Parasite:

Parasites are different from predators because parasites only take resources from one host, whereas predators eat many prey.  A good example of this is the trematode parasite Schistosoma mansoni.  An adult schistosome parasite lives inside of just one human host.  It is never going to crawl out and go infect a different human.

You might be thinking, “Waaaaait…  Schistosoma mansoni has a complex life cycle!  It infects humans AND snails!  That’s two hosts!”  Yep.  But the rule is that parasites only infect one host during each stage of the life cycle.  One human.  One snail.

Here are some other common characteristics of parasites:

1)      They are smaller than their hosts.

2)      They don’t usually kill their hosts.*

Ok, so, the killing bit is confusing and wishywashy.  I’ll come back to it below.

Parasitoid:

Like a parasite, a parasitoid infects just one host per life stage.  But parasitoids always kill their hosts.

Parasite vs. Parasitoid:

So, what’s the difference between a parasite and a parasitoid?  If you’re about to take an exam or something and you want a quick answer, say that parasitoids always kill their hosts and parasites don’t usually kill their hosts.  You’ll find that in many introductory ecology textbooks.

In practice, we don’t really use that definition.  The term parasitoid is usually applied to certain insects that have free-living adult stages that lay eggs inside a host, and the eggs go on to parasitize and eventually kill the host.

There are many “parasites” that always kill their hosts, and we still call them parasites and not parasitoids.  Why, Scientists?  Why do you do this thing?  Well, it just doesn’t make sense to have a rule that says that parasites don’t kill their hosts.  For instance, if a parasite (say an acanthocephalan) in an intermediate host (a pillbug) makes the host more likely to get eaten by the next host (a bird) in the life cycle, then the parasite is often the cause of the host’s death.  Those kinds of parasites are called trophically-transmitted parasites.

A Very Nice Dichotomous Guide:

Lafferty and Kuris (2002) came up with a really nice dichotomous key for classifying natural enemies.  They used four dichotomies, but I’m only going to use the first three:

1. “Does the enemy attack more than one victim?”

2. “Does the enemy eliminate victim fitness?”  (‘Eliminating fitness’ could be killing the victim or sterilizing the victim so that it cannot reproduce.)

3. “Does the enemy require the death of the victim?”

Figure adapted from Lafferty and Kuris (2002) – link below.

You might remember from one of my previous posts that we tend to divide parasites into microparasites and macroparasites.  As I described in that post, for microparasites, we care about presence/absence of infection, and for macroparasites, we care about intensity of infection.  The fourth dichotomy used by Lafferty and Kuris (2002) is “does the enemy cause intensity-dependent pathology?”  They include the fourth dichotomy in their figure.  It’s really useful, but I didn’t include it here to avoid confusion. Click the PDF link below to see their version.

Reference:

Lafferty, K.D., and A.M. Kuris. 2002. Trophic strategies, animal diversity and body size.  TREE 17(11): 507-513. (Direct link to PDF download)

Parasites and Predators: Partners in Crime

This week, I wanted to post about a paper that was just too sexy to resist blogging about.  However, as I was writing my post, I stumbled across Jeremy Yoder’s even better post about the paper.  So, you should click through to the Denim and Tweed blog, read his post, and then admire my only best attempt at drawing a flea.

Raveh et al. (2011) performed an experiment where gerbils were either infested or uninfested with fleas.  They put the gerbils in field enclosures, and then exposed the gerbils to a muzzled fox predator for half of the nights that the gerbils were in the enclosures.  Gerbils were provided with sand boxes containing buried seeds, and the gerbils had to balance foraging in the sand boxes for seeds and avoiding getting pounced on by the fox.  Among other things, Raveh et al. (2011) measured the “giving up density” in the sand boxes.  That is, how much food remained in the sand box when the gerbils left the food patch?  Higher giving up densities meant that the gerbils spent less time foraging, which would be bad news for gerbil seed consumption and storage.

Gerbils infested with high densities of fleas left food patches at higher giving up densities than gerbils without fleas.  And when gerbils had fleas and a fox was present, the gerbils left food patches at the highest giving up densities.  So, fleas distracted/irritated gerbils so much that the gerbils spent less time foraging for food, and that change in foraging behavior was amplified when both parasites and predators were present.  In a world full of things trying to eat gerbils, how’s a gerbil gonna eat?

Here are some things that I liked about this paper:

1. Beautiful, mathy hypothesis testing.  Seriously, go read this paper.
2. In the wild, 97-100% of gerbils have fleas!  Wow!
3. Parasites may facilitate predation on the host, even when the parasites aren’t trophically transmitted.
4. This relates to my post about vicious circles of body condition (or susceptibility) and parasite infection.  If gerbils with many fleas forage less than gerbils with few/no fleas, their body condition might decline.  And if their body condition declines, they might be more susceptible to fleas.  Etc.  This might lead to vicious circles of declining health/fitness.  Or, perhaps the vicious circles don’t have much time to act, because foxes come along and eat the distracted gerbils.

Serious business.

Reference:

Raveh, A., B. P. Kotler, Z. Abramsky, and B. R. Krasnov. 2011. Driven to distraction: detecting the hidden costs of flea parasitism through foraging behaviour in gerbils. Ecology letters 14:47–51.

Predator-Parasite Links in Food Webs

Predator-parasite links are common in food webs.  I posted previously about how ontogenetic specialists (e.g., many parasites) increase food web connectivity, but decrease stability.  That is, when you consider a species that requires different resources at different life stages as multiple “units,” instead of lumping all of the life stages together, the properties of the food web change.

When I posted before, I was really thinking about the resources of the “ontogenetic specialists.”  For a parasite species with a complex life cycle, those resources are the different host species.  But what if instead of looking at the ontogenetic specialists’ resources, we look at their predators?  Do different life stages get preyed on more than others?

Why, yes, yes they do!  Thieltges et al. (2013) classified predator-parasite links from eight food webs into one of three categories: concomitant predation, trophic transmission, and predation on free-living parasite stages.  Briefly, concomitant predation occurs when a parasite living in a host gets consumed along with its host by a predator, and the parasite is digested.  Trophic transmission occurs when a parasite living in a host gets consumed along with its host by a predator, and the parasite successfully establishes in the predator.  And predation on free-living parasite stages is just that – the parasites are being consumed when they are not in a host.  For trematodes, these free-living stages are eggs, miracidia, and cercariae.  (I mentioned previously that larval trematodes can be abundant in zooplankton communities, and may therefore represent a lovely food resource for aquatic predators.)

Break down of predator-parasite links in eight aquatic food webs. Mmm, parasite pie.

Turns out that concomitant predation is the most common predator-parasite link.  Neat!  There’s more cool stuff in the paper, but I’ll leave it to you to go check it out.

Have you seen this done elsewhere for other ontogenetic specialists?  For instance, do we expect larval organisms (e.g., tadpoles, larval insects, etc.) to be preyed on more than adults?

Reference:

Thieltges, D. W., Amundsen, P.A., Hechinger, R. F., Johnson, P. T. J., Lafferty, K. D., Mouritsen, K. N., Preston, D. L., Reise, K., Zander, C. D. and Poulin, R. (2013), Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission. Oikos.