Pinchy Has an Itch

Last week, I told you that small crayfish groom off their branchiobdellids.  Intermediate-sized crayfish try to groom off their branchiobdellids, but the crayfish can’t reach all of the worms.  Specifically, they can’t reach the worms that hang out on that one place on their dorsal carapaces.  Have you ever had an itch on your back that you couldn’t reach?  Yeah, that’s the story of the intermediate-sized crayfish’s life.

pinchy itch

Host Control of Symbionts

Mutualisms are kind of a big deal.  In fact, our very existence depends on mutualisms.  From the pollinators that service our crops to the bacteria that help us digest our food, we just couldn’t survive without them.

Since mutualisms are so important, you might expect us to know a LOT about them.  But we don’t know as much as you might expect.  For instance, we don’t really understand how mutualisms are maintained in the long-term.  Theory predicts that at least some mutualists should cheat, because cheaters should have better fitness than perfect cooperators.  That is, mutualists should be like that used car dealer in Matilda that glues on the car bumpers.  We know that there are cheaters in many mutualisms – like in marine cleaning mutualisms – but something prevents all the mutualists from cheating.  Something prevents cooperation from evolving into parasitism.

That “something” may be partner control.  Partners can reward or punish their mutualists for good or bad behavior, thereby selecting for the mutualists that sell good cars don’t cheat.  But as I mentioned before, the benefits of having mutualists aren’t constant across all ecological conditions.  In fact, sometimes, mutualists can even act like parasites.  So, partner control may need to vary with ecological conditions.  Thus, enter this really cool branchiobdellidan-crayfish study by Skelton et al. (2014).


Pirate worms will be groomed off and eaten on sight!

Skelton et al. (2014) wanted to know if crayfish were less resistant to branchiobdellidans – if they varied how much they controlled their worms – when the crayfish were bigger.  When crayfish are small, they molt frequently, so there isn’t much time for epibiotic material to accumulate on the crayfish.  Having cleaning worms probably isn’t very useful for small crayfish.  But when crayfish get big, they molt less frequently, so having worms around to keep them tidy might be very beneficial.  Therefore, Skelton et al. (2014) performed three experiments where they looked at how crayfish responded to worms when the crayfish were small, intermediate, or large in size.

NOW FOR THE COOLEST PART.  Crayfish ‘control’ their worms by grooming them off (and eating them).  They just reach up with their little walking legs and pluck the worms off.  To experimentally manipulate crayfish grooming, Skelton et al. (2014) just snipped off the dactyls on the walking legs so that the crayfish couldn’t pick off their worms.  That is, in each experiment, there were control crayfish with functional pinchers and other crayfish with their dactyls removed.

Small crayfish strongly resisted worms.  As soon as they had worms put on their backs, the small crayfish started trying to groom them off.  And by the end of the experiment, there were almost no worms remaining on small crayfish if the crayfish had their dactyls intact and could groom themselves.  Intermediate-sized crayfish reacted similarly, but by the end of the experiment, they still had 25% of their worms, even when they could groom themselves.  Conversely, big crayfish liked their worms – when they had their dactyls, they groomed off a few worms during the experiment, but they mostly allowed the worms to hang around.  So, large crayfish had very low resistance to worms, but smaller crayfish had very high resistance, and that’s probably because larger crayfish need the cleaning services, whereas smaller crayfish don’t need the cleaning services.

But why did intermediate-sized crayfish keep 25% of their worms, even when they had their dactyls intact?  The intermediate-sized crayfish had to keep 25% because they couldn’t groom off the worms: the worms hung out on the dorsal carapace in the one place that the crayfish couldn’t reach.  Tricky!  When the crayfish were small enough, there was no place for the worms to hide.  On large crayfish, worms would hang out in a variety of attachment sites, with few occurring on the dorsal carapace, because they could hang out anywhere without (much) risk of being groomed off.  But on intermediate-sized crayfish, they’d get groomed off if they didn’t avoid the areas that the pinchers could reach.  And what’s more, in the field, Skelton et al. (2014) also saw worms mostly hanging out on the dorsal carapace of intermediate-sized crayfish but attaching in a variety of places on large crayfish.  So, not only do crayfish change their control behavior with ontogeny, but worms also change their behavior with crayfish ontogeny.  Cooooooool.

I have a better cartoon of this, but I’m going to wait until next week.  Stay tuned!


Skelton, J., R.P. Creed, and B.L. Creed. 2014. Ontogenetic shift in host tolerance controls initiation of a cleaning symbiosis. Oikos.


How many worms is too many?

In disease ecology, we divide parasites into two groups: microparasites and macroparasites.  I have a previous post about the differences between the two groups (spoiler: size isn’t everything).  But to recap: microparasites tend to cause density-independent pathology, while macroparasites tend to cause density-dependent pathology.  In other words, the more macroparasites a host has, the more likely the host is to die or suffer reduced fitness.  Here is a graph of this concept that should make intuitive sense to everyone:


The relationship isn’t necessarily linear.

Why is it worse for hosts to have more macroparasites?  Because each one takes some energy from the host; each one steals some host resources.  So, more macroparasites means more stolen energy/resources.

But of course, hosts don’t get to choose how many macroparasites they have, and it turns out that macroparasites are not evenly distributed among hosts.  In fact, most hosts have no macroparasites, while just a few hosts harbor the majority of macroparasites.  This is called an “aggregated” distribution, and it is described by an even fancier statistical entity:  the negative binomial distribution.  One day, I’ll post about why we see this aggregated distribution of parasites among hosts, but for now, just know that aggregation of parasites is pretty much ubiquitously true in macroparasite systems.


Ok, so, some hosts are super unlucky and accumulate many macroparasites, and those hosts tend to have lower survival and fitness than other hosts.  What if instead of looking at organisms that are strictly parasitic, we look at symbionts that don’t harm their hosts but don’t help them either.  These are the commensalists (or stowaways) that I talked about last week.  Imagine, for instance, that an insect is carrying around one phoretic mite – a mite that needs to hitch a ride on another animal for dispersal.  The mite doesn’t benefit the insect, but it doesn’t hurt it, either.  Now imagine an insect completely covered in phoretic mites.  Are they still causing no harm?

phoretic mites on Sexton Beetle - Poecilochirus

That’s a lot of mites! Source: BugGuide.

And finally, what about mutualistic symbionts?  As I mentioned last week, branchiobdellidans are little worms that live on crayfish.  They can benefit their crayfish by cleaning the crayfish gill chamber, thereby presumably increasing gas exchange.  But they might also take bites of the gill tissue, which is not particularly mutualistic!  And perhaps they’re more likely to start snacking on gill tissue when other resources are low – like when there are so many branchiobellids that there isn’t enough other food to go around?

Brown et al. (2012) experimentally showed that “normal” branchiobdellid densities increase crayfish growth relative to crayfish with no worms.  But high branchiobdellid densities actually decrease crayfish growth relative to crayfish with no worms!  The relationship between branchiobdellidans and crayfish switches from mutualistic to parasitic with increasing worm density!  Very cool.

The dotted gray line represents crayfish growth in the absence of any branchiobdellids.  I humbly suggest that the authors name this THE PIRATE THRESHOLD.

The dotted gray line represents crayfish growth in the absence of any branchiobdellids. When worm densities get too high, crayfish growth actually decreases relative to the controls – we’ve crossed THE PIRATE THRESHOLD.

Like Goldilocks, crayfish need to find a worm density that is just right for them.  Next week, I’ll tell you how crayfish regulate how many branchiobdellids they have.  Stay tuned!


Brown, B.L., R.P. Creed, J. Skelton, M.A. Rollins, and K.J. Farrell. 2012. The fine line between mutualism and parasitism: complex effects in a cleaning symbiosis demonstrated by multiple field experiments Oecologia 170:199–207.

Pirate Worms

So, you know how sometimes you see another scientist’s work and you get ‘system envy’?  How you suddenly realize that everything about their system is amazing, and you want to switch to work in their system right now?  Well, today I’m going to introduce you guys to a really, really cool system, and then I’m going to do a mini-series of posts about some of the recent work that I’ve seen regarding this system.

OK, READY?  There aren’t many relevant videos on the internet, but I want you to click this link to go see some really cool worms on youtube.  And if you want to see an even more amazing video, you can click here to download it. (It is seriously worth it.)  And for pictures, check these out.

You’re looking at branchiobdellidans.  They’re annelid worms that live as ectosymbionts on crayfish.  There are 150 species and 21 genera of branchiobdellidans in the world, and they are all thought to be obligate crayfish symbionts, meaning that they can’t survive and reproduce if they aren’t on a crayfish host.  Some of the worm species will hang out anywhere on the crayfish body, while others specialize on the crayfish gill chamber or the crayfish chelae.

An ectosymbiont is just an organism that lives on another organism.  The term doesn’t imply anything about the nature of the relationship between the branchiobdellidans and crayfish.  We can assume that branchiobdellidans benefit from the relationship because they get a place to live and lay their eggs, and they also graze on the smaller organisms that live on the crayfish exoskeletons and in the crayfish gill chambers.  But what about the crayfish?  Do they benefit from the relationship?  If branchiobdellidans increase crayfish fitness, then the relationship is mutually beneficial (=mutualism).  If crayfish don’t benefit from the relationship but aren’t harmed either, then the relationship is a commensalism.  And if crayfish fitness is reduced by the relationship, then branchiobdellids are parasitic.  Or, if you’d rather see that in cartoons:

HMS Crayfish 2

Are branchiobdellids mutualists, like passengers who pay for their voyage? Are they commensalists, which get a free-ride but don’t harm their hosts, like stowaways? Or are they pirates, which board the crayfish ship by force and loot the crayfish booty? And perhaps more importantly, are there support groups for people obsessed with dressing worms up in fancy costumes?

Historically, scientists thought that branchiobdellidans were parasites or commensalists, because they are known to consume crayfish gill tissue.  In fact, the more branchiobdellidans a crayfish has, the more scars the crayfish has in the gill tissue.  So, that’s sounds rather parasite-ish!  But the branchiobdellids also clean the gill chamber, which is good for crayfish respiration.  And so the question is whether branchiobdellidans have a net positive or net negative effect on crayfish.  Next time, I’ll tell you about a paper that shows that the net effect of branchiobdellidans on crayfish depends on branchiobdellid density and ‘context’, where branchiobdellidans are more beneficial to crayfish when crayfish are in environments where their gills are more likely to be colonized by bacteria and other organisms.

Until then, check out this review about branchiobdellidans that just came out in Freshwater Science!


Skelton, J., K.J. Farrell, R.P. Creed, B.W. Williams, C. Ames, B.S. Helms, J. Stoekel, and B.L. Brown. 2013. Servants, scoundrels, and hitchhikers: current understanding of the complex interactions between crayfish and their ectosymbiotic worms (Branchiobdellida). Freshwater Science 32(4): 1345-1357.

Vaccination Coverage and Herd Immunity

I’ve talked about vaccination and herd immunity on this blog before, but I think it’s important for me to emphasize how INCREDIBLY IMPORTANT it is to get vaccinated.  The importance of vaccinating most of the population is usually explained using mathematics, because scientists study the spread of pathogens by using mathematics.  But today, I’m going to try to explain it with cartoons and pictures, instead of math.



Without explaining the math, I’ll say that there are some “magic numbers” for vaccination.  These numbers are unique to each pathogen/disease.  For instance, for whooping cough, a disease that can make make babies very sick, the “magic number” is between 92 and 94.  That is, 92-94% of people must be vaccinated in order to prevent disease epidemics of whooping cough.  If that magic number – called the herd immunity threshold – is reached, babies are indirectly protected from whooping cough.  If not, you can expect outbreaks of whooping cough.

So, you might be wondering if there will be outbreaks of whooping cough where you live.  Check out this graphic that was published in Scientific American last year.  If your state’s bar is red – that is, if you live anywhere except Nebraska – you can expect epidemics of whooping cough in your state in the near future.  And while it looks like nobody will be seeing Mumps epidemics any time soon, you can expect to see Measles epidemics in many states.

vaccination coverage

Don’t believe me?  Look at these news articles reporting outbreaks of whooping cough in the United States – here and here and here, to show just a few.

At one point, we’d pretty much eliminated whooping cough in the United States by vaccinating children with the DTP vaccine.  Here’s a graph from the CDC showing that after we started using the DTP vaccine around 1950, whooping cough (also called pertussis) almost completely disappeared.  But in the past decade or so, as people have increasingly opted out of vaccinating their children, we’ve dropped below the “magic number” for whooping cough, and we’re starting to see thousands of cases per year.


If you want to know more about the recent declines in vaccination coverage and the detrimental effects that this has on societal health, check out this recent Nature supplement for several cool articles.

Parasitic Castrators: Population-level Effects

For background info about parasitic castrators, check out the previous two posts, here and here.

As promised, this week, I’m going to talk about the effect(s) of parasitic castrators on host populations.  I’m specifically going to talk about trematode parasites (Halipegus occidualis) that castrate their snail hosts.  As a motivating statistic, 60% of snails in Charlie’s Pond (the pond studied in Negovetich and Esch 2008) may be castrated by H. occidualis trematodes.  That’s 60% of the snail population that can’t reproduce!!!  It would be hard to imagine castration at that scale NOT having an effect on snail population dynamics.

Whenever math and snails happen in the same paper, I am very happy.  In this paper, Negovetich and Esch (2008) used size-structured population matrix models to look at snail population growth.  They took parameter estimates for the size-specific growth rates, fecundity, and survival rates of snails from a previous field study.  They also took the natural prevalence of trematode infection (60%) and the natural yearly probability that overwintered snails cleared their parasite infections (35%) from the previous field study.

They calculated the natural snail population growth rate (λ) by finding the dominant eigenvalue of their annual matrix, just like you’d do for any matrix model.  Using the natural trematode prevalence and clearing rate, λ was 1.55.  They also calculated a hypothetical snail population growth rate for when there was 0% trematode infection – in that case, λ = 2.41.  So, having the natural levels of trematode infection resulted in a 36% decrease in snail population growth rates!!


I’d vote for Gary.

Negovetich and Esch (2008) also used sensitivity and elasticity analysis to see how changing the various rate parameters – fecundity, survival, growth – would affect the snail population growth rate.  They found that decreasing the size that snails reached reproductive maturity was the most effective way to increase the snail population growth rate.  You might remember from the previous posts that decreasing the size at reproductive maturity is one way to get fecundity compensation.

So, here’s where I quibble with the authors a bit.  They point out that that decreased size at reproductive maturity (=fecundity compensation) has been observed in several systems with snails and castrating trematodes.  Very cool!  But Negovetich and Esch (2008) also imply that these decreases are destined to evolve because they’re the best way to increase snail population growth rates according to this model.  And maybe if snails don’t do something to increase their population growth rate, the large-scale parasitic castration will lead to extinction.  I don’t like this explanation because selection acts at the individual level – the snail population isn’t deciding as a whole to reproduce at smaller sizes.

As we’ve talked about previously, individuals may reproduce earlier when they’re infected either because they know they’re about to be castrated or because the parasite’s manipulation of host resource allocation causes the snails to reach reproductive maturity sooner than the snails normally would.  There’s clearly some fascinating future work to be had on this topic – what’s the mechanism behind earlier snail reproduction in the presence of castrating trematodes?!  I MUST KNOW.

Until then, check out this paper!


Negovetich, N.J., and G.W. Esch. 2008. Quantitative Estimation of the Cost of Parasitic Castration in a Helisoma anceps Population Using a Matrix Population Model.  Journal of Parasitology, 94(5):1022-30.

Parasitic Castrators: A Model

Last week, I introduced you guys to the wonderful world of parasites that castrate their hosts.  This week, I want to talk about the mechanisms behind parasitic castration – both how and why castration happens – and how the wacky responses (e.g., gigantism) of castrated hosts emerge naturally from these mechanisms.  So, enter, from stage left, a beeeeeeeautiful paper by Hall et al. (2007).

Pattern Oriented Modeling:

The Hall et al. (2007) paper is a wonderful example of pattern oriented modeling. Actually, pattern oriented modeling – as championed by Grimm, Railsback, and colleagues – is an approach used to make agent based models more rigorous and more ‘applied.’  For ABMs, using just one predicted pattern isn’t a very useful way to build a mechanistic model, because many different agent behaviors might result in the emergence of the same pattern.  How would you figure out which behaviors were mechanistically appropriate?  If you instead have several expected patterns, it is unlikely that just any agent behaviors will cause all of the patterns to emerge.  So, you can determine which mechanisms are biologically appropriate by determining which agent behaviors lead to your patterns.  Anyways, Hall et al. (2007) used differential equation models, instead of ABMs, but they still used a pattern oriented modeling approach that was very powerful.  Specifically, they knew that any model with parasitic castrators in it should produce the following patterns:

  1. Gigantism.  At any given host age, hosts that are parasitized by castrators should be bigger than unparasitized hosts and hosts parasitized by noncastrating parasites.
  2. Life span.  Hosts that are parasitized by castrators should live longer than hosts parasitized by noncastrating parasites.
  3. Fecundity compensation.  Hosts that are parasitized by castrators should begin reproducing sooner than hosts parasitized by noncastrating parasites.
  4. Reproductive rates.  Hosts that are parasitized by castrators should have lower mean reproductive rates than hosts parasitized by noncastrating parasites because castrated hosts are sterilized, either partially or completely.
  5. Parasite reproduction.  Hosts that are parasitized by castrators should produce more new parasites than hosts parasitized by noncastrating parasites.
  6. [There’s a sixth one in the paper, but I’m going to let you guys go check it out.]

Not only are these patterns predicted from theory, but they had also been demonstrated empirically in a system where bacterial parasites castrate Daphnia hosts.  So, Hall et al.’s (2007) model is based on that Daphnia-bacteria system.

The Kooijman DEB model

Before thinking about parasites, Hall et al. (2007) adapted a dynamic energy budget model to the Daphnia-bacteria system (or a similar system).  In a nutshell, hosts acquire, assimilate, and store energy from their food, and then they can use that energy for maintenance of their current state, growth, development, or reproduction.  Specifically, hosts devote a fixed proportion (k) of their energy reserves to growth and ‘structural maintenance.’  They spend the other fraction of their energy (1-k) on other stuff.  If they aren’t reproductively mature yet, they spend the (1-k) on development, and if they are mature, they spend the (1-k) on reproduction and ‘maturity maintenance.’  The two maintenance things are a bit confusing, I know, but just remember that there are two types of maintenance, and organisms need to spend some energy maintaining their current condition before they can spend any energy on other things.

Host Starvation:

Using this dynamic energy budget model, if the host starts to experience ‘moderate’ starvation conditions, its reserve energy stores will decline. Eventually, the reserves will be low enough that the proportion of energy available for growth and maintenance (k) will only be enough to cover ‘structural maintenance.’  The host doesn’t have any energy left in the ‘k’ part of the budget to devote to growth.  The host still divides up the (1-k) part of the budget to development or reproduction and ‘maturity maintenance,’ depending on whether the host is reproductively mature or not.  So, at this point, the host is still reproducing or developing.

However, if starvation conditions become severe, the host might not have enough energy to devote to reproduction and development.  The host might just spend all of its k and (1-k) energy budgets on maintenance.  And if reserves get so low that the energy stores don’t even cover the maintenance costs, the host dies.

Consumer Parasite:

Now let’s add a parasite to the model!  First, let’s add a noncastrating parasite, which Hall et al. (2007) called a ‘consumer’ parasite.  The parasite takes energy from the reserve energy stores of the host.  In that way, the host and parasite are competing – they’re both using and budgeting that energy pie.

Importantly, consumer parasites can affect how hosts allocate energy, but only indirectly.  That is, if the parasite uses enough of the reserve energy that the host finds itself in moderate starvation conditions, the host stops growing.  It devotes all of the k fraction of the energy to structural maintenance.  And if the parasite uses up enough of the reserve energy that the host finds itself in severe starvation conditions, the host stops developing or reproducing.

Hall et al. (2007) also added one more assumption – if the parasite takes up more than a certain proportion of the host’s total volume (p), the host dies.  Otherwise, very efficient parasites can reach unrealistically huge population sizes.

Ok, sooooo – what happens when we run the consumer model?  After several days of normal growth and reproduction rates, the hosts stop growing because the parasites have reduced the energy stores to moderate starvation conditions.  The hosts keep reproducing for a few more days, but reproductive rates start to decline because the (1-k) piece of pie gets smaller and smaller as the parasite populations grow bigger and bigger.  Finally, the parasites cross that critical volumetric proportion (p) and the hosts die.

Parasitic Castrators:

Now let’s add a parasitic castrator to the model, instead of a consumer parasite.  To do this, Hall et al. (2007) changed just one model assumption.  Instead of leaving k as the constant proportion of energy devoted to growth and reproduction, now k is a dynamic variable.  Specifically, k is a function of the number of parasites per host.  Whereas consumer parasites could only indirectly affect host’s allocation of resources, castrating parasites can directly manipulate host’s allocation of resources by directly affecting k.  (They can also indirectly affect host resource allocation, just like consumer parasites.)  When there are no parasites, the fraction of energy devoted to growth and maintenance (k(0)) is regular old k, from the baseline model.  But as the number of parasites increases, k also increases monotonically – the host spends more and more of the energy budget on growth because castrating parasites directly cause the hosts to budget energy differently.  And because k increases with parasite density, the energy available for development or reproduction (1-k) decline with parasite density.  So, the host is castrated.  [Insert “ooooooohs” and “ahhhhhhhs” of wonder here.]

Ok, sooooo – what happens when we run the castrator model?!  For just a few days, host growth and reproduction rates are normal because parasite populations are still too small to be consuming a lot of host energy.  Then, as parasite density increases, k starts increasing, and host growth rates increase dramatically.  In fact, castrated hosts get much bigger than uninfected hosts and hosts infected by consumer parasites.  After just a few more days, hosts stop reproducing because (1-k) is so low.  Hosts keep growing until just before they die, and host death occurs later than it did when the parasite was a consumer instead of a castrator.

Some Cool Notes:

As we expected, hosts infected by castrating parasites ended up having lower reproductive rates (Prediction 4).  But did they see fecundity compensation (Prediction 3)?  It’s hard to tell from the graphs, but Hall et al. (2007) said that hosts infected by castrating parasites started reproducing sooner than snails infected by consumer parasites and uninfected hosts.  The really cool thing is that the earlier reproduction was completely emergent – it wasn’t “programmed” into the model.  Because castrating parasites increased the growth rates of the hosts, the hosts reached the reproductive maturity threshold size sooner, and thus switched from spending their (1-k) energy budget on development to spending it on reproduction earlier than other hosts did.   Super cool!

Under these conditions, being a parasitic castrator was a better strategy than being a consumer parasite because castrators ended up producing more new parasites than consumers. Consumers rapidly used up all of the available host energy reserves, while castrators kind of “stocked up” energy by getting hosts to grow bigger.  (Bigger hosts can acquire and assimilate more energy.)

Back to Patterns:

Let’s go back and see if all of the predicted patterns emerged from these models.

  1. Gigantism.  CHECK!
  2. Life span.  CHECK!
  3. Fecundity compensation.  CHECK!
  4. Reproductive rates.  CHECK!
  5. Parasite reproduction.  CHECK!
  6. NOT check! In the discussion, Hall et al. (2007) note that their sixth pattern didn’t emerge from the model.  So, there’s some future work to be had there.  It doesn’t mean that this model is bad, but there is some interesting biology and math that needs to be considered further.

So… that was flipping awesome.  In case you’re wondering, the correct thing for you do right now, if you haven’t yet, is to follow this link to the PDF of the paper.  Happy reading!

Fecundity Compensation


Hall, S.R., C. Becker, C.E. Caceres. 2007. Parasitic castration: a perspective from a model of dynamic energy budgets. Integrative and Comparative Biology 47(2): 295-309.