Zombie Crabs – Why Can’t We Get Us Some of Those?

I originally wrote this article for the Washington Sea Grant Crab Team newsletter, and you can read this and much more crazy things about marine life on the Crab Team webpage.

The yellow blob under the abdominal flap is not eggs, but the
extern of a female barnacle, Sacculina carcini. (By Auguste
Le Roux (Own work), via Wikimedia Commons).

In Europe, millions of zombie green crabs are roaming the shore. From the outside, you might not even realize they are brain dead, no longer truly a green crab, but have been transformed into a skittering, feasting, parasite-producing machine. Their metabolism has been co-opted, their reproductive system re-appropriated, their crabby will subjugated to the whims of the intruder they harbor – the parasitic barnacle Sacculina carcini.

Barnacle? That’s right. For these crabs infection is the stuff of horror films, but the monster in this case is not an animal we typically think of as gross or dangerous – though anyone who has tried to walk barefoot on a barnacle-encrusted rock might disagree. This species is one of a group of parasites called Rhizocephalans (meaning “root headed,” which will become clear later on). As free-swimming larvae, they look very much like other barnacles, progressing from a nauplius stage to a cypris – but here they diverge.

The great biological illustrator Ernst Haeckel visualized
what the root-like intern of Sacculina carcini would
look like inside the crab. And the blob of the extern
is exposed by the folded back abdomen (Wikipedia).

Imagine this: you are a European green crab, minding your own business, maybe poking around looking for some tasty polychaete worms or clams to eat, and you feel a slight tickle when something microscopic lands at the base of a hair on one of your legs, clinging to you by means of an antenna-like appendage. But you’re too distracted cruising around the shore to notice when the larvae — which has shed its shell, legs, eyes, and brain as it metamorphosed into a kentrogon (sounds like some kind of alien race, but is basically a sac of cells with a needle where the head used to be) — injects itself into your body through the base of that hair, and is released. Soon, the parasite attaches to your digestive system, and begins to grow thread-like structures that wrap around and along your nerves, like ivy growing up a tree – called the interna. The interna ultimately spread throughout your entire body, like the roots of a tree filling up a pot.

You might start to notice something going on when you begin to look like a female crab – that is, if you weren’t already female. One of the most bizarre effects of being infected with this barnacle is that, even though both sexes can be infected, male crabs are feminized by the parasite, causing them to have smaller claws and wider abdomens, like females (read a study on host feminization), paving the way for what happens next.

Gah! The life cycle of Sacculina carcini, from Goddard et al. 2005.

The barnacles that infect crabs are always female, and they use the crab as an egg factory, feeding off the crab and ultimately growing out through the underside of the crab to create a blobby structure called an externa, which is a large sac of barnacle reproductive tissue. The crab carries the externa just as if it were his or her own eggs. The barnacle eggs in the externa are fertilized by one or two free-swimming male cyprids, and then released as the next generation of zombifying parasites.

Needless to say, when you are carrying a sack of parasites on your abdomen, there’s no room for eggs of your own. Infected green crabs, both male and female, are fully castrated by the parasite. In addition, infection ultimately halts the process of molting, so crabs not only can’t grow any larger, but they also can’t replace any lost limbs. In spite of its gruesomeness, infection is not a death sentence for European green crabs; about half of the crabs infected in a laboratory experiment survived infection for at least 3 months. In the native range, some crabs also show scars on their carapace from carrying previous externae. However, those crabs can never recover their reproductive ability, and the female parasite can create multiple externae for the remaining life span of the crab.

How does this fit in with the global invasion of green crabs? In the native range of Carcinus maenas, about 16 percent of crabs are infected with Sacculina carcini (read the study), and given that about half of infected crabs die, this parasite could be a substantial part of population regulation. However, S. carcini has not followed European green crab to either the east or west coast of North America. It’s likely that the crabs that first traveled across the Atlantic Ocean, and later across the United States, were too young to bring the barnacle along as a hitchhiker. Additionally, because the male barnacle that fertilizes the female’s externa is free-swimming, the male and female barnacles need to make it to the new range at just the right times, but in different ways, which could be a very unlikely coincidence.

The lack of this, and other parasites, is one possible explanation for why European green crabs are larger here on the West Coast than they are in their native range (read the study). Combine a lack of parasites with relatively cold water (read the study), and it turns out that the biggest green crabs in the world have been found in the Pacific Northwest. Some claim to fame!

Your mind might already be leaping to the next logical question: Can we bring this parasite to help control populations of the European green crab on the West Coast? In the Salish Sea we do have native species of Rhizocephalan parasites, even some in the same group as this one. Nevertheless, it turns out bringing Sacculina carcini over is probably not a good idea. For those of you familiar with the history of cane toads in Australia, you’ll be relieved to hear that researchers here have been doing their homework when it comes to this parasite.

In a laboratory experiment in Santa Barbara, scientists tested whether several species of native crab could also be infected by Sacculina carcini. While more of the parasites settled on European green crab, when given the choice, they also settled on Dungeness crab and two species of shore crab that are found in our area (Hemigrapsus nudus and H. oregonensis). Dungeness crab were more likely to become infected with the parasite than any of the other species of crab, even when relatively few barnacles settled on them. What’s more, all of the native crabs that became infected died, compared to only about half of the European green crabs that were used for comparison, and many of the native crabs showed neurological impairment as a result of infection. A number of questions remain about whether the same patterns would occur in the field, but for now, the risk to native crabs is significant enough to warrant caution.

Carcinus, and the Amazing Technicolor Crab Shell OR Video Games for SCIENCE!

I think most people assume that reading scientific papers is totally boring, and that only someone who is really fascinated in some completely arcane microdiscipline could possibly get anything out of it. I wish I could disabuse you of that assumption, but, by and large, yeah, they're pretty boring unless you really get your jollies reading about "A framework to assess evolutionary responses to anthropogenic light and sound"(1). There are certainly some notable exceptions, mostly when scientists, some more successfully than others, try to demonstrate they have a sense of humor(2). But what I like is really digging to find the hidden gems in papers.

Today, for instance, I learned that, "Humans adopt a similar search pattern to birds…when looking for prey on a computer screen". Huh! Did you know that? I did not know that! And, naturally, there are citations!(3)

Sooooo, why do I need to know that? (4) Because it turns out it's easier to get humans to play a video game than to get birds to do what you want - such is the way science actually gets done.

OK, but that's really a methods question, let's get to the point of the paper:

Carcinus maenas just can't decide what it wants to wear. Images from Stevens et al. 2014

The above photos are ALL ONE SPECIES (SRSLY), the European green crab, Carcinus maenas. Notably, this species is regularly listed as one of the worst invasive species on the planet, but that really doesn't have anything to do with this variation in color(5). And it turns out this is not the only species to have this insane catalogue of costumes that undoubtedly drives undergraduate zoology students insane: Also sporting coats of many colors:

• Cancer productus (Red rock crab) native to Eastern Pacific Ocean(6)
• Hemigrapsus oregonensis (Hairy/Green/Yellow/Oregon shore crab)(7)
• Cardisoma guanhumi (blue land crab) from Brazil(8)

Then what is the deal with all these fashion-forward crabs? Well some intrepid volunteers in Singapore attempted to test the hypothesis that the variety of colors helps camouflage crabs when they are young, to keep them from getting eaten by their main predator - you guessed it, shorebirds(9). So this is where it's important to know that humans and shorebirds look at a computer screen similarly, because these volunteers got to play video games - FOR SCIENCE! 

Before we get to the shoot-em-up part (pew, pew!), let's dive into the question a bit more. First off, a quick straw poll, when you hear the word camouflage, what image pops into your head? I'm going to go out on a limb and guess it was something like this:

Out on a limb FTW! Their frowns are the best.

The camouflage that we often think of, that is literally embodied by the chameleon, is called background matching. Which sounds pretty straightforward - trying to hide by pretending you aren't there. But there is another type of camouflage that you are probably familiar with, and it looks like this:

Yes, this is also camouflage, it turns out.

This is called disruptive coloration. This type of camouflage isn't about avoiding detection, it's about making it hard for someone who wants to eat you to figure out just where you start and where you end. You can see how it works really well when you get a dazzle(10) of zebras together and your eyes start to cross, but it also works when a zebra is by itself, at least theoretically. By creating false edges and boundaries, this coloration makes it more difficult for the edge-detection software in your brain to identify and track the animal as an individual. Not convinced? Try this thought experiment. In disruptive coloration, high contrast is an asset because the strong difference in brightness between the white and black stripes overpowers or distracts the brain from detecting the weaker differences in color with the animal an its background(11). 

So let's bring it all together:

Video Games + Camouflage + Green Crab

This paper just came out in Current Zoology (by Peter Todd and colleagues) using video games to test how these white spots might contribute to camouflage in green crabs. They did this by creating fake crab shells and putting them on fake backgrounds, and having students come play their video game, which I'm calling "Nab the Crab", timing how quickly they could find the fake crab shell on the computer screen.

The researchers varied the shells and the back ground in different ways - testing several aspects of camouflage. Here is some really compelling evidence that you can learn something from video games:

Figure 6. from Todd et al.: This is how long it took game players to find the simulated crab shells (examples on the bottom).

On the far right, notice that the game players found the plain shell in no time flat (about  1 second!) - the plain shell is clearly no good at hiding this fake crab from shorebirds (because remember the thing from the beginning about visual search patterns...). Next look at the left two bars, those two shells had large spots on them, but one (LE) had large spots overlapping the edge of the shell, while the other (LI) had the spots all inside the shell. Game players were MUCH faster finding the crab when the spots were all on the inside of the shell (15 versus 33 seconds). The same was true for middle and small sized spots, but the difference in speed was less.  This is all great support for the fact that spots at the end of the shell could act as disruptive coloration!

Figure 1 from Todd et al. High and low contrast spots.

The researchers also tested whether increased contrast would help, so they made crabs with bright white spots and crabs with grey spots, and in most cases, the higher contrast crab was harder to find.

 

Figure 2 from Todd et al. Background.

Of course all of this depends on your background, and some of these effects of camouflage depended on what kind of background the crab was on. If you imagine that these crabs like to live on beaches, you can imagine these backgrounds as small pebbles (on the left) and larger cobbles (on the right). In general, game players took longer to find the crab on the small/pebble background regardless of where the spots were on the shell or what color they were - this makes sense, a busy background makes it harder to detect pattern if the brain has to do a bunch of work interpreting the busyness.

Which is all to say that humans playing video games is only very slightly similar to the process by which natural selective forces of predation by shorebirds might have altered the frequency of shell coloration in Carcinus maenas. Nevertheless, I'm all for video games for science. I found Smorball this summer (Go Piggers!) - by playing you are helping digitize the library of biodiversity literature! I also went on a few virtual safaris, one in Gorongosa National Park, and one in Samburu.

So next time you're caught goofing off playing video games, you can just just say you're doing science like a shorebird. 

YOU'RE WELCOME

References and Miscellany

1. A title I literally just pulled out of the latest issue of Trends in Ecology and Evolution, THE most important ecology journal published, but it sounds kind of interesting, don't you think?
2. This is perhaps the most inscrutable example known to man.

3. But salient to this quoted sentence is Jackson et al. Behavioral Ecology 2005

4. Also, who is adopting who's search pattern here?!

5. You'll hear more about this later, after years of trying to work with this species, I have finally found my way to a project on European green crab.

6. Krause-Nehring et al. 2010 Zoology (link)

7. Rachel Folz (link)

8. Silva et al. 2014 Braz. J. Biol. (link)
9. There is a method to my madness.
10. A group of zebras can also be called a "zeal" but "dazzle seemed more to the purpose here. 
11. Now, I should point out, the story of zebra stripes is probably more complicated than disruptive coloration, and an apparent sudden urgency of solving the "how the zebra got its stripes" question has resulted in new theories, including insect avoidance and keeping cool. I'm going to suggest that stripes probably have multiple benefits for zebras, and might have all played a role in their evolution. I use them as an example because they do make my point about disruptive coloration.