A Jellyfish’s Offense is a Sea Slug’s Defense

Arms races between predators and their prey have been common in the evolution of life. Gazelles run a little faster to help them escape cheetahs, then of course the cheetahs speed up to keep catching their meals. Bivalves (clams, scallops, etc.)  and snails have evolved some tough and elaborate shells to protect themselves, and in response the crabs, octopuses, and fishes that eat them have developed incredibly strong claws, drills, or teeth to crush, open, or bore into the shells. And of course toxins can be synthesized to ward off all sorts of enemies looking to take a bite out of you (the slow loris is by no means the only animal to do this, but it may be the cutest).

navanax eating

A cephalaspidean sea slug of the genus Navanax devours an aeolid nudibranch slug. Aeolids can sometimes steal stinging cells from their prey, jellyfish and their relatives, as a defense against predators, but that doesn’t seem to have worked in this case.
Image taken from http://www.uwphotographyguide.com/california-marine-life

But what if you’re just slow and squishy? In the case of nudibranch sea slugs, some of them make up for this vulnerability by eating cnidarians (jellyfishes, coral, sea anemones), stealing their stinging cells, and planting them in their own tissues, ready to fire at an unsuspecting predator. The process is called kleptocnidae, and even though it was discovered almost 100 years ago, it’s been the subject of very little study since then.

A while back, I wrote about kleptoplasty. It’s the process whereby sacoglossan sea slugs steal chloroplasts from their algal prey and use them for photosynthesis, essentially turning themselves into solar-powered animals. However, see a recent study calling into question the extent to which the slugs use photosynthesis for survival.

Regardless of exactly how important solar power may or may not be for the survival of sacoglossans, nudibranchs have arguably taken the art of stealing from their prey to a different level. Nudibranchia is the best known group of sea slugs, largely because their patterns are so colorful that they often look more like cartoon characters or art projects than real animals. But we all know beauty doesn’t necessarily make you nice, and nudibranchs could be considered masters of deception in that regard. In contrast to the herbivorous (i.e. vegan) sacoglossans, nudibranchs are voracious predators, devouring sponges, corals, bryozoans, or other sea slugs – some will even cannibalize members of their own species!

As aggressive as that may sound, nudibranchs are still quite vulnerable. Like all other slugs, they are essentially snails without shells, and because they lack hard parts they need some other way to defend themselves against predators. Many slugs do this by synthesizing nasty chemical compounds to make them unappetizing or even toxic. Some nudibranchs, however, take stinging organelles called nematocysts from their prey, then store the weapons in their own tissues for protection.

Nematocyst-discharged

Scanning electron microscope (SEM) image of the barb of a discharged nematocyst.

Only nudibranch species that happen to eat cnidarians are able to pull this off. Cnidaria is the phylum that includes jellyfishes, corals, anemones, hydra, and other lesser-known aquatic critters. What unites all these diverse organisms into a single group is that they all have stinging cells, or cnidocytes. Cnidocytes contain organelles with barbs that eject out from the cell when triggered, into the thing that did the triggering.

Nematocyst_discharge

The anatomy of a nematocyst.
(Try saying that ten times really fast.)

Sometimes the barbs just have sticky hairs that help capture prey – these organelles are called spirocysts, and you’ve experienced them if you’ve ever touched a sea anemone and felt the tentacles stick to your fingers. But in other species, the barbs are a means of injecting toxins to neutralize prey and/or fend off predation – these organelles are called nematocysts, which you’ve felt if you’ve ever been stung by a jellyfish or possibly just swimming along a coral reef (corals will sometimes release these stinging cells into the open water).

One of the more remarkable things about the ability of sacoglossans to steal and then use chloroplasts is that they’re able to steal from their prey intact, instead of simply digesting them with the rest of their food. Well, nudibranchs not only do the same thing with nematocysts, but they’re able to do it without triggering them. The “trigger” of a nematocyst is a single cilium, a hair-like structure that all types of cells have and are often used for locomotion (think back to middle school biology and you’ll probably remember that the single-celled paramecium uses many cilia to move around). In this context it’s a literal hair trigger that causes a nematocyst to fire at the slightest touch. And once it’s been fired, it can’t be re-loaded – one and done is the way of the nematocyst.

Even though decades passed with little knowledge gained about kleptocnidae, a recent study shed some light (both literally and figuratively) on the subject. Last year, Obermann et al. (2012) used a fluorescent stain to show exactly how one species of aeolid nudibranch, Aeolidiella stephanieae, manages to store the nematocysts of its prey in its own tissues without setting off the sensitive triggers. One suggestion for how nudibranchs in general do this has been that mucus produced by slugs during feeding allows nematocysts to be passed in tact to their storage facilities (called cnidosacs). An even older hypothesis says that slugs only capture immature nematocysts that are incapable of firing when first stolen, but then somehow mature while hanging out in the slugs’ cnidosacs. Following this premise, what defines maturity and how does it happen?

Even how nematocysts work within the cnidarians that produce them has not been well understood – water pressure, stored mechanical energy, and a proton gradient (i.e. different number of protons on each side of a cell membrane) have all been put forward as being important for helping make a nematocyst ready to fire. This last mechanism about the proton gradient caught the attention of German researchers Dana Obermann, Ulf Bickmeyer, and Heike Wägele, so they set out to test whether it was involved in kleptocnidae.

Obermann 2012 fig mod

The aeolid nudibranch Aeolidiella stephanieae (A). Cnidosacs where stolen nematocysts are stored, 7 hours (B), 24 hours (C), 48 hours (C), 72 hours (D), and 96 hours (E) after feeding. Blue fluorescence indicates low pH (i.e. abundant protons) that is likely the condition necessary for nematocysts to fire. See Obeemann et al. 2012 for proposed explanations as to why fluorescence declines from 72 to 96 hours post-feeding.
(figure modified from Obermann et al. 2012)

An increase in protons means an increase in acidity, which can be observed or measured as lower pH. By staining nematocysts in sea anemones of the genus Aiptasia, which Aeolidiella stephanieae preys upon, with a pH-sensitive fluorescent dye, their maturity could be tracked from the anemone tissue into the slug tissue. This is how the authors’ results came to support the proton gradient hypothesis.

Nematocysts that made it through the digestive process in tact did not light up in the anemone, nor in the slug when they were first stolen. Over time, more specifically 48+ hours after being eaten by the slugs, nematocysts ‘matured’ in the cnidosacs and glowed brightly. The experiment confirmed that only the immature (i.e. high or neutral pH) nematocysts were kept by the slugs, and that a buildup of protons over time helped them to reach a low-pH condition in which they were capable of firing. In other words, no matter how sensitive the hair trigger may be, the gun is effectively not loaded until enough protons have accumulated. This allows the slugs to incorporate nematocysts into their tissues without rendering them useless by causing them to fire.

Well played, slug. I’m still partial to sacoglossans because I’ve spent some time studying them, but nudibranchs are awesome and this study demonstrates, on a molecular level, one reason why that is.

P.S. If you’ve never typed the word nudibranch into Google Images, please do so immediately. Or least check out this National Geographic photo shoot. It’s 5 years old, but no less awesome than it was in 2008.
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9 thoughts on “A Jellyfish’s Offense is a Sea Slug’s Defense

  1. Pingback: A Jellyfish’s Offense is a Sea Slug’s Defense | the3rdstone

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  5. Regarding: “… that the slugs don’t photosynthesise,…“ That is not what our paper says. There has been a lot of misconception regarding the Proc B paper on slugs in the dark. Here’s an Addendum that explains things a little better: “https://www.landesbioscience.com/journals/cib/article/28029/“

  6. Pingback: Sea slug workshop at STRI in Bocas del Toro, Panama | Evolution Happens

  7. Pingback: Sea slugs in Bocas del Toro, Panama | Evolution Happens

  8. Pingback: Sea slugs in Bocas del Toro, Panama | Evolution Happens

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