Life over Limb: Conversation with a Taildropper Slug

Article contributed by CVN member Véronique McIntyre.

While on a Botany Group outing we saw what is to me an extraordinary animal: a taildropper slug (two in fact).

To learn more about them, I went back to Miracle Beach and asked the taildroppers a few questions.

“Can you tell me your name and a bit about your relatives?”

“We are Prophysaon foliatum, nicknamed yellow-bordered taildroppers. There are ten species in our genus. We are molluscs that live on land. We breathe like you, with a lung. We are close relatives to snails although we have a flat, internal cuticular plate instead of a visible shell. We use it as a reserve of calcium, not for protection.”[1]

“And how do you live? What do you eat?”

“Here we have very tasty oyster mushrooms that grow on the same log we are crawling on.”

Sure enough, I was able to locate them (Fig. 1).

Fig. 1. Oyster mushroom (Pleurotus ostreatus). Photo: Véronique McIntyre

“Notice the edge of that mushroom: doesn’t it look like a cheese grater went to work on it? We have a radula in our mouth, a structure that is characteristic of molluscs and looks like a bunch of teeth, that allows us to grate our food. Maybe what you see here is slug ‘teeth marks’?”

My little friend continued. “We spread fungal spores wherever we go though our droppings. This increases mycorrhizae, which form important symbiotic relationships with the roots of trees and other plants. But the main advantage for us is that more of the fungi we eat end up growing close to where we are. Since most of us don’t live for more than one year, this is important for our young: it ensures they have a source of food right where they are born. So, each time you, humans, pick up wild mushrooms, be it to eat them or for scientific purposes, you destroy our source of food and threaten us with starvation. And you make it even worse when once you find a type of fungus you like somewhere, you start searching and collecting even more in the same area. In fact, we are just coming back from lunch. Here is a selfie I took (Fig. 2). You can see I am having a bowel movement. I did it on purpose, so you can locate my anus, under my mantle at the front, on the right side of the feces. Not at all where yours is, I believe. If I were to lose my tail, I would not have problems excreting waste that could poison me if I kept it inside.”

Fig. 2. Yellow-bordered taildropper (Prophysaon foliatum) lateral view. The thin brown thread under the plate is feces. The diamond-shaped mesh is pigmented groves. Photo: Véronique McIntyre

“And why would you lose your tail?” I asked, my curiosity piqued.

“Well, you see, there are very mean carabid beetles crawling around trying to snatch us from behind. You are not likely to spot any now, as they mostly do their dastardly deeds at night. They have a very long head, to go inside slugs’ bodies or snails’ shells to eat them. Awful name too, Scaphinotus angusticollis. One tried to eat my mom.”

“What do you mean, ‘tried to eat my mom’? Did she survive?”

“Oh yes! She was caught, but she simply dropped her tail, and that stupid carabid went for it.”

“Wait a minute, how did she do that?”

“See, if you look at my selfie again, you can see on back third a thin oblique line across my body. My tissues are a little bit brownish after that line. It is a groove that we use for self-amputation to escape our predators. Same idea as in lizards, I heard, although I have no clue what a lizard is. The part that the predator catches swells, the rest of our body before the groove contracts, and bingo! You get a shorter slug and a moving tail. To deter the predator from going after our front end (after all it is much longer than the stump), we hide it with vast amounts of sticky mucus that oozes from where the tail was lost. Messy business, but it seems insects don’t like mucus. Or maybe the mucus camouflages our shape well enough that they don’t recognize our front part as edible. And they quickly learn that by going at our tail end they get a juicy morsel to eat. This is called adaptive coevolution by the way: a prey adapts to avoid a predator, but at the same time a predator adapts its behaviour to better get at its prey. Or at part of it in our case.”

I had so many questions! How does the taildropper manage to cut its tail almost instantly? How does it avoid catastrophic bleeding? What about the organs that are inside the tail?  Does it hamper its mobility? Or its desirability to potential sexual partners? How do the lost parts regenerate and not just end in a mass of scar tissue? Can they do it over and over again or only once?

“If I did that, I would bleed to death. How do you avoid that?”

“We have what is called an open circulatory system. It means that our blood, which we call hemolymph, does not go from heart to vessels back to heart, like in your closed circulatory system, but it leaves branching vessels to bathe our cells. Then, when we contract our muscles, it is pushed back into other branching vessels to the heart. It’s slow, but it works for us. We could never move fast though, because our cells don’t get much oxygen that way. That’s why our cousins, the cephalopods like octopi, squids etc., have a closed circulatory system. Back to autotomy.”

“What is that?”

“That’s the fancy name given to the ability to sever parts of the body. From “auto “, meaning “self”, and “tomy” meaning “cut”. It evolved independently at least nine times in animals, which shows it is useful: reproduction being the most important part of life, anything that allows an organism to survive just a bit longer, thus increasing its chances to reproduce, will be selected for. The corresponding genes will then be passed down to the next generation, no matter how uncomfortable or painful the process is. Even some mice can do it, losing their skin when they’re caught.[2]  But I was talking about our open circulatory system. When we contract our muscles at the level of the self-amputating groove, our blood gets pushed toward our front end where our heart is located, safely tucked below our mantle. Very little bleeding occurs since no major vessel has been cut. The sticky mucus might act as heavy bandage as well. That avoids the risk of blood congealing en masse when trying to stop heavy bleeding. And you would not see it anyway; our blood is blue when rich in oxygen, not red like yours, because we don’t use iron to transport oxygen on hemoglobin but copper on hemocyanin. Once our blood loses its oxygen though, it turns transparent. Here, look, I found two cool pictures that some scientists took of a cousin of ours with a fancy way to colour our organs (Figs. 3a and 3b). The front is at the top.”

Fig. 3a. Inside of slugs using radionuclides[7]: Circulatory, excretory and digestive systems
Fig. 3b. Inside of slugs using radionuclides[7]: Digestive and nervous system.

The bag between the kidney and the digestive gland is the stomach.

“How do you avoid infection?”

“Because we have a preformed cleavage plane, healing is sped up, which reduces the possibility of bacteria entering the wound. Mucus reduces that risk too. Another advantage of that plane and of the mucus is that fewer water-borne molecules that could signal to a predator the presence of a wounded slug get released.”

“Don’t you have white blood cells like me?”

“We do have cells that act similarly called hemocytes that can engulf bacteria, parasitic worms and viruses, and release nitric oxide or oxygen peroxide to kill them. They also help in wound healing and nerve repair. We make those cells in the heart area, so losing our tail does not affect their production.” [3]

“On that beautiful color picture of your cousin I see a big chunk of digestive gland in your tail end. If the predator takes that, you’ll have problems digesting, won’t you?”

“That’s true, but only for a little while until we regenerate what has been lost. There is a bit of the intestine that is gone as well. Luckily, the spot where we contract our groove is where the two ends of a loop of the intestine cross. Easy to reattach them. Here, I made you a little diagram to help you understand our insides (Fig. 4).”

Fig. 4. Internal anatomy of a slug. Head on top; belly on right. Drawing and photo: Véronique McIntyre

“As you can see, sacrificing our tail end does not really endanger us. All our precious reproductive organs are at the front. Same for our brain, heart, aorta, kidney, lung, sensitive organs, mouth, etc. It’s almost as if we are built to lose our tail end! And there is an advantage to having a shorter body: as our pulmonary space is not affected, we take in the same amount of oxygen even though our tissues need less. This allows for the oxygen we take in to prioritize regeneration and to fight against infection.”

“If a predator catches you from behind, you need to drop your tail almost instantly. I don’t want to be disparaging, but you don’t look to me like you are a very swift animal. How do you do it?”

“See all the little crosses in the drawing on the belly side of our body? Those are like mini brains called ganglia (one is a ganglion). When we are caught by the tail a signal goes to the closest ganglion, which responds with an order to immediately contract our muscles and sever the end. There is no time lost with the signal going to the brain and back. Works like your reflexes, fast and very efficient. You can see the ganglia in green on the right-hand side colored picture of the insides of my cousin too.”

“OK, but when your tail is half-gone you can’t move as far, as nimbly, nor as fast as before, right?”

“Moving on a carpet of mucus is not a very fast mode of transportation to begin with. We don’t move more than maybe a hundred meters in a lifetime, except of course if we get caught in a windstorm or a flood, or if an animal picks us up and then drops us. So, having lost part of our tail does not really affect our mobility. And over time, we regenerate the lost part anyway. Although, if you picked up the mushroom I feed on, I may not be able to forage to the next one without dying of starvation before reaching it.”

“With your tail gone, you would not have much in terms of sex appeal. How do you reproduce anyway?”

“We are oviparous, meaning we lay eggs, as our albumen gland shows on my little drawing. We also are simultaneously hermaphroditic, meaning that we have both male and female reproductive organs and act both ways when we copulate. So, you can use all the pronouns with us. She/he/it/they, you are never wrong. I don’t think any of us can self-fertilize, although you never know. Notice that none of our precious sexual organs are at any risk of being damaged when we lose our tails. This organization is common to snails too, and that certainly facilitated the appearance of autotomy in our genus.”

“You mentioned regeneration, how does that work? I don’t regenerate.”

“Well, I don’t know exactly. Some of your scientists have found very high levels of insulin-like substances in the blood of some friends two months after they dropped their tails.[4] Our tails store glycogen, our source of sugar, which would be in high demand for regeneration. Beyond that, there is not much known on that topic so far. Maybe we have stem cells along the line of autotomy? It’s always possible that the energy spent regenerating our tail is energy that cannot be spent somewhere else, such as forming eggs. This would be only temporary though since regeneration does not take more than a few weeks.”

“Really?”

“Yes. Another more distant cousin of mine, one that lives in the sea, can decapitate themselves and grow a new body from the remnant of the head. Within a few days the wound is closed. After a week, it regenerates its heart, and after three weeks an entirely new body is formed. And it can do it more than once in a lifetime. Of course, I could not do that, because unlike my sea slug cousin I don’t eat algae, so I don’t incorporate some of the plant’s chloroplasts into my body, which would allow me to draw energy from the sun. Me, I need most of my organs to stay alive while I regenerate. Still, our regeneration times are similar. But not the reason: my sea slug cousin cuts its body off to rid itself of parasitic copepods. Also, it takes twenty hours to separate its body from its head, so this is useless in a predator attack scenario.”[5]

“Close to a month to get a brand-new tail seems quite a long time for animals that live maybe a year, and don’t seem to reach adulthood before the fall, only to die in the winter. Can you do it more than once like your cousin? In case another predator shows up?”

“I don’t know, and I don’t think anybody knows yet.”

“You do lose your tail to escape predators, but snails don’t. Does your ability have anything to do with your absence of a shell?”

“You mean as my kin lost their protective shell over a long period of time, foot autotomy might have been selected concurrently because it counterbalanced the weakness resulting from shell reduction? It might well be, but some remote cousins with a shell also lose their tails. Those don’t have opercula, a way to close the shell though, so they do have a weakness there.”[6]

“It is strange then that only your genus among all the slugs can lose their tail when attacked.”

“True, but don’t forget that in evolution it is not because you need something that you get it. Mutations occur at random. It is just by chance that a few of our ancestors had some DNA changes a long time ago that allowed them some – probably very limited – ability to lose a little bit of their body to escape predators. Those who survived those attacks then passed on those genes to their descendants. Further random mutations and increased survival made over time the almost perfect mechanism you observe today. Come back 200,000 years from now, and it might be even more astonishing, or it might have been lost, who knows? It depends on whether it increases our ability to reproduce. In our case, for now the carabid beetles are the agent of natural selection for a better ability to autotomize and survive the operation.”

“Well, I am very grateful to you for all that information. I wish you a good end of life.”


References

1. Henry A. Pilsbry and E. G. Vanatta (1898). “Revision of the North American Slugs: Binneya, Hemphillia, Hesperarion, Prophysaon and Anadenulus.” Proceedings of the Academy of Natural Sciences of Philadelphia Vol. 50 (1898), pp. 219-261 (51 pages). The 4th paragraph on p.1 is quite funny.
https://www.jstor.org/stable/4062409?seq=1#metadata_info_tab_contents

2. A.W. Seifert, S.G. Kiama, M.G. Seifert, J.R. Goheen, T.M. Palmer, M. Maden (2012). “Skin shedding and tissue regeneration in African spiny mice (Acomys)“. Nature 489 (7417): 561–565. Bibcode. DOI. PMC. PMID.

3. E.A. Pila, J.T. Sullivan, X.Z. Wu, J. Fang, S.P. Rudko, M.A. Gordy, and P.C. Hanington (2016). “Haematopoiesis in molluscs: a review of haemocyte development and function in gastropods, cephalopods and bivalves.” Developmental and Comparative Immunology 58: 119–128. DOIPMID.

4. Erika M. Plisetskaya and Ingridth Deyrup-Olsen (1987). “An insulin-like substance in the blood of the slug Prophysaon foliolatum (Arionidae) in the course of tail regeneration.” Comparative Biochemistry and Physiology Part A: Physiology 87(3): 781-783. DOI.

5. Sayaka Mitoh and Yoichi Yusa (2021). “Extreme autotomy and regeneration of the whole body in photosynthetic sea slugs.”  Current Biology 31(5): PR233-R234. DOI. (See also: SciTech Daily March 8, 2021).

6. Samantha D. Rupert 1 and Winfried S. Peters (2011). “Autotomy of the posterior foot in Agaronia (Caenogastropoda: Olividae) occurs in animals that are fully withdrawn into their shells.”Journal of Molluscan Studies 77: 437–440.

7.  Nicola Beindorff,  Fabian Schmitz-Peiffer,  Daniel Messroghli,  Winfried Brenner & Janet F. Eary (2021). “Radionuclide, magnetic resonance and computed tomography imaging in European round back slugs (Arionidae) and leopard slugs (Limacidae).” Scientific Reports 11: 13798. DOI.