Category Archives: Snails and Slugs

How Poisons Work: Tetrodotoxin

by Joseph DeSisto

This is the first of a series of short articles, each featuring a different type of poison or venom used by animals.

Poisons and venoms are some of the most complex substances in nature, often containing hundreds of different chemicals, each with a particular purpose. As technology advances, scientists have begun to look at some of these chemicals, usually proteins, and try to figure out what they do.

The deadly southern blue-ringed octopus (Hapalochlaena maculosa). Photo by Bernard Dupont, licensed under CC BY-SA 2.0.

The deadly southern blue-ringed octopus (Hapalochlaena maculosa). Photo by Bernard Dupont, licensed under CC BY-SA 2.0.

In some cases, the results give us a new perspective on an animal’s biology: rattlesnake venom, for example, contains a unique protein that allows the snake to track its prey after the initial strike. In other cases, we discover potentially useful surprises: giant centipede venom contains a single protein that inhibits pain in mice, using the same chemistry as morphine, but with greater efficiency. However, regardless of whether the results are useful to us, studying nature’s chemical weapons gives us a whole new appreciation and understanding of the creatures that wield them.

Tetrodotoxin is the poison of choice for a variety of animals, especially in the ocean. These include blue-ringed octopuses, cone snails, moon snails, certain angelfish, some ribbon worms, a handful of amphibians, and the puffer/triggerfish order Tetraodontiformes, for whom the toxin is named. Many of the animals that use tetrodotoxin are brightly colored, a warning to passers-by. Would-be predators, save the immune and the unlucky, heed this warning well.

An inflated pufferfish (Diodon holocanthus). Photo from Williams et al. (2010), licensed under CC BY 2.5.

An inflated pufferfish (Diodon holocanthus). Photo from Williams et al. (2010), licensed under CC BY 2.5.

Tetrodotoxin, sometimes abbreviated TTX, is a complex molecule that prevents its victims’ nerves from functioning properly. This eventually leads to paralysis, and death comes when the muscles that control breathing no longer receive signals from the nervous system. Basically, you suffocate. Humans can get TTX poisoning when they eat improperly-prepared pufferfish, but stings from blue-ringed octopuses and cone snails (both from the southwestern Pacific) are also a possibility if you are foolish enough to pick them up.

Although many animals use TTX, none of them actually manufacture the toxin themselves. Instead bacteria generate the toxin, to their host’s benefit. In exchange, the bacteria are allowed to live safely within their host’s body — the bacterium Pseudoalteromonas tetraodonis, for example, makes its home within the livers and skins of pufferfish.

A toxic moon snail (Naticarius orientalis) from East Timor. Photo by Nick Hobgood, licensed under CC BY-SA 3.0.

A toxic moon snail (Naticarius orientalis) from East Timor. Photo by Nick Hobgood, licensed under CC BY-SA 3.0.

The rough-skinned newt, from British Colombia and the western United States, has the bacteria needed to make TTX for itself — as a result, this newt has few natural predators. Two animals, however, have managed to work around and even benefit from the rough-skinned newt’s toxins, all without toxin-producing bacteria of their own.

The only animal capable of eating an adult rough-skinned newt is the garter snake. After ingesting the newt, any other predator would almost certainly die, but a few populations of garter snakes have evolved an immunity to TTX. What’s more, the snakes are able to sequester the toxins within their own bodies, so that the garter snakes themselves become poisonous (Williams et al. 2004).

The extremely toxic rough-skinned newt (Taricha granulosa). Photo by Rennett Stowe, licensed under CC BY 2.0.

The extremely toxic rough-skinned newt (Taricha granulosa). Photo by Rennett Stowe, licensed under CC BY 2.0.

Although many snakes inject toxins with their fangs, and so are venomous, garter snakes that eat rough-skinned newts are the only snakes that can truly be considered poisonous. The difference is that venomous animals have to inject their poisons into predators or prey, via fangs or stingers, while poisonous animals are laced with their chemical weapons and are dangerous to eat.

The other TTX-robber is, unexpectedly, a caddisfly. Caddisflies are insects whose larvae resemble caterpillars, but live underwater and surround themselves with cases made from pebbles, twigs, and other debris. Most are scavengers, eating decomposing plant matter and tiny invertebrates, while the flying adults are short-lived and do not feed.

A Limnephilus caddisfly larva, in its protective case made of twigs. Photo by Tom Murray, used with permission.

A Limnephilus caddisfly larva, in its protective case made of twigs. Photo by Tom Murray, used with permission.

A few predatory species in the genus Limnephilus, however, have developed an unusual appetite for rough-skinned newt eggs, which also develop in the water. These eggs are loaded with TTX, and the toxin-resistant Limnephilus larvae manage to eat so many that even the caddisfly adults are toxic (Gall et al. 2012).

Even though many marine invertebrates contain tetrodotoxin, we still don’t know how many contain the bacteria that make it, versus how many, like the caddisfly, “steal” the toxin from their TTX-laced prey. Certain sea slugs, for example, are often washed on shore where they are eaten by beach-combing scavengers such as dogs. In New Zealand, several dogs have died after eating sea slugs that contained TTX (McNabb et al. 2009), and in Argentina, a population of the same slugs appears to have become invasive (Farias et al. 2015). Yet we still do not know whether they have their own TTX-generating bacteria.

A toxic sea slug, Pleurobranchaea meckelii. Photo from Wägele and Klussmann-Kolb (2005), licensed under CC BY 2.0.

A toxic sea slug, Pleurobranchaea meckelii. Photo from Wägele and Klussmann-Kolb (2005), licensed under CC BY 2.0.

Experiments have shown that certain populations of sea slugs have TTX, while others do not (Khor et al. 2014) — just like the garter snakes of North America. Does this mean the sea slugs are obtaining TTX from some unknown, toxic prey item? The same researchers conducted a survey of all the marine invertebrates that these slugs might be eating, testing everything for TTX. The only positive result was a toxic species of sand dollar, but the sand dollars didn’t produce nearly enough TTX to explain the huge amounts found in sea slugs.

Ignorance has consequences, and there is still plenty of exploring left to do. The slugs may in fact make tetrodotoxin themselves (using bacteria). A more enticing possibility, and just as likely, is that there are still more toxic animals on the sea floor, waiting to be discovered.

One of the very first articles I wrote for this site featured the same sea slugs mentioned in this one, but that was when my only readers were a few sympathetic family members. If you’re curious about sea slugs, and/or you want to know the difference between a nudibranch and a pleurobranch, you can read that article here.

I also recently wrote about how rattlesnake’s use their venom to track once-bitten prey (mentioned in the second paragraph of this article). To learn more about that, click here. It’s amazing, I promise.

Cited:

Farias, N.E., S. Obenat, and A.B. Goya. 2015. Outbreaks of a neurotoxic side-gilled sea slug (Pleurobranchaea sp.) in Argentinian coasts. New Zealand Journal of Zoology, published online: DOI: 10.1080/ 03014223.2014.990045.

Gall, B.G., A.N. Stokes, S.S. French, E.D. Brodie III, and E.D. Brodie Jr. 2012. Predatory caddisfly larvae sequester tetrodotoxin from their prey, eggs of the rough-skinned newt (Taricha granulosa). Journal of Chemical Ecology 38(11): 1351-1357.

Khor, S., S.A. Wood, L. Salvitti, D.I. Taylor, J. Adamson, P. McNabb, and S.C. Cary. 2014. Investigating diet as the source of tetrodotoxin in Pleurobranchaea maculata. Marine Drugs 12(1): 1-16.

McNabb, P., L. Mackenzie, A. Selwood, L. Rhodes, D. Taylor, and C. Cornelison. 2009. Review of tetrodotoxins in the sea slug Pleurobranchaea maculata and coincidence of dog deaths along Auckland Beaches. Prepared by Cawthron Institute for the Auckland Regional Council Technical Report 2009/108.

Williams, B.L., E.D. Brodie Jr., and E.D. Brodie III. 2004. A resistant predator and its toxic prey: persistence of newt toxin leads to poisonous (not venomous) snakes. Journal of Chemical Ecology 30(10): 1901-1919.

Advertisements

Rat Lungworm Disease: How it Works

by Joseph DeSisto

Rat lungworm disease — even the name sounds awful. But to understand the disease, we first have to understand the life cycle of the worm that causes it which, incidentally, is as fascinating as it is terrifying.

The rat lungworm (Angiostrongylus cantonensis) is a kind of parasitic roundworm or nematode which, unsurprisingly, is mainly a parasite of rats. It’s favorite host is the brown “Norway” rat, now found throughout the world where it has been spread by human travels. The worms enter a rat as larvae less than a millimeter long, first entering the bloodstream and then migrating, like salmon up a stream, to the host’s brain. Here they gorge themselves with brain tissue until they become sub-adults. The brain-filled, sub-adult lungworms are almost half an inch in length — and still not done growing.

The brown rat, common in cities, is the primary host of the rat lungworm. Photo by  Ian Kirk, licensed under CC BY 2.0.

The brown rat (Rattus norvegicus), common in cities, is the primary host of the rat lungworm. Photo by Ian Kirk, licensed under CC BY 2.0.

Before they reach adulthood, the worms migrate again via the circulatory system, this time stopping when they reach the heart’s right ventricle, or the pulmonary arteries. In the heart tissue, the worms finally mature, mate, and lay their eggs — but the eggs, too, must migrate. The eggs are laid directly into the bloodstream, and because the pulmonary arteries lead directly to the lungs, that’s where the eggs end up. Hence, the name “lungworm,” even though they might as well be called “heartworms” or even “brainworms.”

Even now, the lungworms have yet to finish their ricochet across your — I mean, the rat’s — body systems. When the eggs hatch, baby worms travel up the respiratory tract, leaving the lungs and entering the esophagous, where they enter the digestive system.

An adult female rat lungworm. Photo from Lindo et al. (2002), in public domain.

An adult female rat lungworm. Photo from Lindo et al. (2002), in public domain.

Despite being microscopic, the baby lungworms are extremely tough. They have to be, because they are going all the way, from throat to stomach to intestines and beyond. Finally, when the rat defecates, its feces are loaded with baby lungworms, all ready to start infectious lives of their own.

If they are lucky, the scent of rat dung will catch the nose of a passing snail or slug. Land snails are usually scavengers that will eat almost any non-living biological material, from dead leaves to carrion to, yes, dung. Should a snail care to take a bite, it will quickly become infected with hordes of developing lungworms.

As any city-dweller will attest, rats will eat almost anything, including, it just so happens, snails. The life cycle of the rat lungworm continues with a rat eating an infected snail or slug, and with the worms travelling up to the rat’s brain to eat, grow, and make wormy babies of their own. For a more technical description of the rat lungworm and its strange life cycle, I recommend Cowie’s 2013 review paper.

The gray garden slug, which has been recorded as an intermediate host for the rat lungworm. In other words, if you eat them, cook them first. Photo by Bruce Marlin, licensed under CC BY-SA 3.0.

The gray garden slug (Deroceras reticulatum), which has been recorded as an intermediate host for the rat lungworm. In other words, if you eat them, cook them first. Photo by Bruce Marlin, licensed under CC BY-SA 3.0.

Rat feces aren’t just eaten by snails, and snails aren’t just eaten by rats. As a result, rat lungworms accidentally infect animals they aren’t supposed to, such as flatworms, shrimp, frogs, birds and, yes, humans. People all over the world eat snails, both on purpose and by accident. Rat lungworm disease in China is usually attributed to eating market-bought raw snails (Lv et al. 2008). During a 2002 outbreak in Jamaica, where snails aren’t as popular, infections were the result of contaminated vegetables (Lindo et al. 2002).

Eating cooked snails is fine, since the cooking process kills the lungworm larvae — it’s raw escargot that can cause problems. Snails and slugs in gardens can also leave a trail of worm larvae in their slime, so washing vegetables in lungworm-inhabited areas can be important.

What happens when a person accidentally eats a rat lungworm? In a human, the worm follows the same cycle as it does when in a rat, going from circulatory to nervous to circulatory to respiratory to digestive systems, and back out to be eaten again by snails.

A summary of the rat lungworm life cycle (click to enlarge). Figure from the Centers for Disease Control and Prevention, in public domain.

A summary of the rat lungworm life cycle (click to enlarge). Figure from the Centers for Disease Control and Prevention, in public domain.

Medical problems come from the sub-adult worms, as they eat away at the host’s brain tissue. Worms are pretty big things to have squirming around in your head, and as they burrow through nervous tissue, they can cause enough damage that the brain becomes inflamed. The result is eosinophilic meningitis, a series of symptoms of which lungworms are just one possible cause. In some cases the damage can cause behavioral changes in the host — one victim developed severe photophobia, and was terrified of light (Ramirez-Avila et al. 2009).

Rat lungworm disease is not common but can be serious, and potentially fatal. Most cases occur in the tropics, especially in Southeast Asia and the Pacific, where the worm is native. Recently, however, lungworms have become more common across the world, as rats and certain snails have been introduced by humans (Kliks and Palumbo 1992).

A small outbreak in Hawaii occurred only a decade ago (Hochberg et al. 2007) and made the news. Global trade in food has also been a factor — the contaminated vegetables that caused the outbreak in Jamaica may very well have been grown halfway around the world (Lindo et al. 2002). As the world becomes economically smaller, strange local diseases can become worldwide problems.

And yet, for all this gloom and doom, the reason I wrote this article in the first place is that the rat lungworm is actually a pretty cool animal. It’s easy to view wormy parasites like nematodes as simple and unsophisticated creatures. But if the rat lungworm can teach us anything, it’s that even “simple” animals can have incredibly complex and, yes, amazing life cycles. And maybe, just maybe, even the most nightmarish of animals can be, in its own twisted way, sort of, well … beautiful.

Have a lovely and parasite-free day.

(Disclaimer: My interest is in science education. I am not a doctor, and nothing in this article should be interpreted as medical advice. If you are here because you’re worried you might actually have rat lungworm disease, please stop browsing the Internet and talk to a real doctor. Thank you.)

Cited:

Cowie R.H. 2013. Biology, systematics, life cycle, and distribution of Angiostrongylus cantonensis, the cause of rat lungworm disease. Hawai’i Journal of Medicine & Public Health 72(6): 6-9.

Hochberg N.S., S.Y. Park, B.G. Blackburn, J.J. Sejvar, K. Gaynor, H. Chung, K. Leniek, B.L. Herwaldt, and P.V. Effler. 2007. Distribution of eosinophilic meningitis cases attributable to Angiostrongylus cantonensis, Hawaii. Emerging Infectious Diseases 13(11): 1675-1680.

Kliks M.M. and N.E. Palumbo. 1992. Eosinophilic meningitis beyond the Pacific Basin: the global dispersal of a peridomestic zoonosis caused by Angiostrongylus cantonensis, the nematode lungworm of rats. Social Science and Medicine 34(2): 199-212.

Lincoln M. 15 April 2015. Rat lungworm disease spreads fear across Hawaii Island. Hawaii News Now. Retrieved from http://www.hawaiinewsnow.com/

Lindo J.F., C. Waugh, J. Hall, C. Cunningham-Myrie, D. Ashley, M.L. Eberhard, J.J. Sullivan, H.S. Bishop, D.G. Robinson, T. Holtz, and R.D. Robinson. 2002. Enzootic Angiostrongylus cantonensis in rats and snails after an outbreak of human eosinophilic meningitis, Jamaica. Emerging Infectious Diseases 8(3): 324-326.

Lv S., Y. Zhang, P. Steinmann, and X. Zhou. 2008. Emerging angiostrongyliasis in mainland China. Emerging Infectious Diseases 14(1): 161-164.

Ramirez-Avila L., S. Slome, F.L. Schuster, S. Gavali, P.M. Schantz, J. Sejvar, and C.A. Glaser. 2009. Eosinophilic meningitis due to Angiostrongylus and Gnathostoma species. Clinical Infectious Diseases 48(3): 322-327.

Sea Butterflies: Snails with Wings

by Joseph DeSisto

When I begin a tangent I like to see it through to fruition, so why not continue our journey into the strange and wonderful world of snails and slugs, class Gastropoda? Recall that the last two articles were on carnivorous, terrestrial slugs and toxin-wielding sea slugs. Today I’m going to tell you about some more amazing gastropods I’ve been reading about: several lineages of holoplanktonic, pelagic snails. In other words, tiny snails that live and swim about in the open ocean, among plankton. The inspiration for this article comes from an extensive treatment of the biology, ecology, and evolution of the pelagic snails and slugs by Lalli and Gilmer (1989).

A heteropod snail. Note the large, well-developed eyes. This is a fast, visual hunter, relying on sight to locate its prey. Photo by C. and N. Sardet.

The term “holoplankton” refers to organisms that spend their entire lives as members of the planktonic soup that nourishes the oceans of the world. This is in contrast to meroplankton, which includes animals that spend only part of their lives as plankton. For example, crabs, lobsters, sea stars, and sea urchins all have free-swimming larval stages that are microscopic and can be considered plankton. Plankton can also be divided into photosynthetic, “plant-like” phytoplankton, which includes algae and diatoms, and zooplankton, which includes tiny animals that persist by eating either phytoplankton or other zooplankton. Phytoplankton and zooplankton form the base of virtually all marine food webs, and so are critically important to the survival of pretty much all marine life, from lobsters to mussels to whales.

Many of the large, sea-floor-dwelling snails are meroplanktonic, and have swimming, microscopic larval stages. There are however, holoplanktonic snails as well: these are diverse and often bizarre, and many appear as if they belong in another world. There are the janthinids, which live on rafts which they construct out of air bubbles bound by hardened mucous. These snails are usually blue or violent, and spend their entire lives drifting about on their flotation devices, snatching their jellyfish prey from the drifting current. Then there are the heteropods, active predators that use large, well-developed eyes to search for prey. Like the predatory slugs we discussed earlier, heteropods use a long radula to capture their food, which consists mostly of zooplankton, including other pelagic snails.

Cavolinia inflexa, a thecosome or sea butterfly. The “wings” are the flap-like structures extending up and to the left. Photo by C. Sardet.

Among their prey are some of the most beautiful and ecologically important of the planktonic snails, the sea butterflies belonging to the order Thecosomata. Their shells, often thin and transparent, range from spiral-shaped to long and needle-like, but all thecosomes have a pair of large, paddle-shaped “wings” which they use to swim rapidly through the water. This unusual strategy among snails encouraged French fishermen to refer to these snails as papillons de mer, or “butterflies of the sea,” and the common name of sea butterflies stuck.

I say rapidly, but this all relative — while most zooplankton can hardly swim at all, instead simply floating along with the current, two common genera of thecosome, Limacina and Creseis, can fly through the water at 8-12 cm per second.  This is about the same as most sea butterflies that have been studied. The fastest we know of is Gleba cordata from the northern and equatorial Atlantic — this Michael Phelps of the snail world can soar at a show-stopping 45 cm per second (Lalli and Gilmer 1989). Keep in mind G. cordata has a meager shell length of 1.5-2 cm, although the wings can be much longer. They need to be able to move fast to out-swim their predators, among which are the gymnosomes or sea angels, planktonic slugs that feed exclusively on sea butterflies.

8_Un_gymnosome_attrapant_un_creseis_C_et_N_Sardet_Gymnosome_Pneumodermopsis_paucidens_

A gymnosome or sea angel (left) attacking Creseis, a needle-shaped sea butterfly (right). Photo by C. and N. Sardet.

Sea butterflies are difficult to maintain in captivity and, as a result, not much is known about their behavior. We do know that they are generalist plankton feeders, preferring phytoplankton and bacteria, although they do occasionally take zooplankton such as copepods, which are tiny, fast-swimming crustaceans. Other organisms that have been found in the guts of thecosomes include single-celled protozoans, immature heteropods (the predatory snails from earlier), and the microscopic larvae of crustaceans, snails, and other sea-floor invertebrates (Lalli and Gilmer 1989).

We also have a pretty good idea of how they harvest prey, which was shown in detail by Gilmer and Harbison (1986). When a sea butterfly gets hungry, it secretes a sticky, mucous “net” from its mouth; plankton that floats into the net becomes trapped in sticky mucous. This net can be enormous — Cavolinia tridentata, with a shell length of only 1.5 cm, can secrete a net up to 20 cm in diameter. When the snail has harvested enough food, it simply pulls the net back into its mouth and digests the contents.

NOAA Ocean Explorer: Arctic Exploration 2002

Limacina helicina, an arctic sea butterfly. Photo by Russ Hopcroft.

Although thecosomes usually don’t make up a large portion of the zooplankton in any given location, except perhaps in the subantarctic seas (Hunt et al. 2008), they do occasionally undergo population booms or outbreaks. This can lead to a nuisance: in 2013 in Jacksonville Beach, Florida, surfers and swimmers began to report “stings” from small, sharp animals. The culprit: a needle-shaped sea butterfly, Creseis acicula, whose narrow shell helps the snail glide through the water. You can read the full story from First Coast News here.

Sea butterfly “outbreaks” can be a problem for bathers, but more often they simply mean lots and lots of fish food. Limacina is a common, worldwide genus of sea butterflies, many of which are found in the cold waters of the North Atlantic. Here they can form a substantial part of the diet of fish, including some commercially important species: Hardy (1924) estimated that Limacina form about 2.2 percent of the yearly diet of North Sea herring, for example. This may not sound like much, but the North Sea herring fishery is worth an annual 20 million euros (22.7 million U.S. dollars) to Scotland alone, 2.2% of which is pretty significant.

Limacina inflata, a sea butterfly from arctic water. Photo by C. and N. Sardet.

Limacina inflata, a sea butterfly. Photo by C. and N. Sardet.

There is plenty more to say about the natural history of pelagic snails, but I’m going to save the rest for another time. I hope I have shown you that the sea butterflies and their relatives are amazing and beautiful animals. Unfortunately, due to recent changes in ocean chemistry, sea butterflies aren’t doing so well lately.

Shells are made of calcium carbonate (CaCO3). During shell formation, snails and other marine invertebrates combine two forms of calcium carbonate: calcite and aragonite. Unlike most snails, which construct their shells mainly out of calcite, the shells of sea butterflies are mostly made of aragonite. Aragonite is found near the ocean’s surface, where it normally occurs in abundance. As you travel deeper underwater, the dissolved aragonite concentration decreases, to the point where there is not enough for sea butterflies to make their shells.

This usually isn’t a problem for sea butterflies, who spend most of their time near the surface anyway — that’s where the phytoplankton is most abundant. But in recent years the aragonite concentration in surface waters has been declining. In many locations there is not enough to support healthy populations of aragonite-based snails such as sea butterflies. While sampling for Limacina helicina in the Scotia Sea between Antarctica and Chile, Bednaršek et al. (2012) discovered several populations where the snails were unable to form complete shells — these occurred in areas where aragonite concentration had dropped below levels necessary for shell growth.

In large part due to human activities, the amount of carbon dioxide in the atmosphere has increased rapidly in the last few centuries. So has the amount of dissolved carbon dioxide in surface waters of the world’s oceans; this process is called ocean acidification. Ocean acidification has many negative effects on marine life, and will likely see its own story in the future of this blog. Just one of these is that dissolved aragonite concentrations are going down, and the oceans are quickly becoming inhospitable to sea butterflies and other organisms that incorporate large amounts of aragonite into their bodies. Orr et al. (2005) estimate that the Southern Ocean surface waters will be undersaturated with respect to aragonite by 2050, and hence be unable to support populations of sea butterflies and other pelagic snails. This area will then continue to grow, and more and more of the world’s marine habitats will become aragonite-starved.

A sea angel or gymnosome, Clione limacina, a close relative of the sea butterflies. Because sea angels lack shells, they are not as dependent on aragonite, but ocean acidification will affect them as well, since the aragonite-using sea butterflies are their only prey. Photo by Kevin Raskoff.

A sea angel or gymnosome, Clione limacina, a close relative of the sea butterflies or thecosomes. Sea angels are predators that feed exclusively on sea butterflies. Photo by Kevin Raskoff.

Whether their models are correct, only time will tell. Meanwhile, ocean acidification is happening now, and is a very real threat not only to sea butterflies but to countless other marine species and, ultimately, the humans that depend on them.

Before signing off, I would like to thank Dr. Christian Sardet for graciously allowing me to use some of his photographs of thecosomes and other planktonic gastropods. Dr. Sardet and his colleagues maintain The Plankton Chronicles, a superb collection of videos, photographs, and information on the immense diversity of animals and protists collectively known as plankton. If you are interested in plankton at all, I strongly recommend visiting the site.

Cited

Bednaršek, N., G.A. Tarling, D.C.E. Bakker, S. Fielding, E.M. Jones, H.J. Venables, P. Ward, A. Kuzirian, B. Lézé, R.A. Feely, and E.J. Murphy. 2012. Extensive dissolution of live pteropods in the Southern Ocean. Nature Geoscience 5: 881-885.

Gilmer, R.W. and G.R. Harbison. 1986. Morphology and field behavior of pteropod molluscs: feeding methods in the families Cavoliniidae, Limacinidae and Peraclididae (Gastropoda: Thecosomata). Marine Biology 91: 47-57.

Hardy, A.C. 1924. The herring in relation to its animate environment. Part I. The food and feeding habits of the herring with special reference to the east coast of England. Fishery Investigations, Series 2 7(3): 53.

Hunt, B.P.V., E.A. Pakhomov, G.W. Hosie, V. Siegel, P. Ward, and K. Bernard. 2008. Pteropods in Southern Ocean ecosystems. Progress in Oceanography 78(3): 193-221.

Lalli, C.M. and R.W. Gilmer. 1989. Pelagic snails: The biology of holoplanktonic gastropod mollusks. Stanford, California: Stanford University Press.

North Sea herring fishery recertified as ‘sustainable.’ 25 July 2013. BBC News. Retrieved from: http://www.bbc.com/news/

Orr, J.C., V.J. Fabry, O. Aumont, L. Bopp, S.C. Doney, R.A. Feely, A. Gnanadesikan, N. Gruber, A. Ishida, F. Joos, R.M. Key, K. Lindsay, E. Maier-Reimer, R. Matear, P. Monfray, A. Mouchet, R.G. Najjar, G. Plattner, K.B. Rodgers, C.L. Sabine, J.L. Sarmiento, R. Schlitzer, R.D. Slater, I.J. Totterdell, M. Weirig, Y. Yamanaka, and A. Yool. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681-686.

Turner, L. 29 August 2013. Needle-like creatures wash ashore Jacksonville Beach. First Coast News. Retrieved from: http://www.firstcoastnews.com/

A Sea Slug Story

by Joseph DeSisto

If you watch science news, or if you happen to have spent a lot of time researching slugs in the last few days like me, you might have noticed a few stories with a titles something like, “Toxic Sea Slugs Invade Argentinian Coastline.” A few days ago I wrote about terrestrial, predatory slugs and how they fit into our understanding of gastropod evolution. But although the land-dwellers are the most familiar, more than two-thirds of all gastropod (snail and slug) diversity is found in the ocean. And of course, there are marine slugs as well.

Nembrotha lineolata, an Indo-Pacific nudibranch. Photo by Nick Hobgood.

Nembrotha lineolata, an Indo-Pacific nudibranch. Note the gills (red) which are held outside the body, unlike the pleurobranchs, whose gills are internal and located on the sides of the body. Photo by Nick Hobgood.

As on land, shell-lessness evolved several times within the marine snails, but most of the “sea slugs” belong to a single lineage, Nudibranchia, which contains around 3,000 described species. Unlike most terrestrial slugs, nudibranchs begin their lives as larvae with shells, then quickly lose them during development. Many nudibranchs are predatory, highly toxic, and brightly colored, and the group includes some of the most visually stunning animals on earth.

Two individuals of the predatory nudibranch Nembrotha kubaryana, eating a tunicate colony. Photo by Nick Hobgood.

Two individuals of the predatory nudibranch Nembrotha kubaryana, eating a tunicate colony. Photo by Nick Hobgood.

The name Nudibranchia means “naked gills” and refers to the fact that in many species, the gills are held outside the body, exposed to the elements. A closely related group of sea slugs, the Pleurobranchomorpha, have internal gills on their sides. There are far fewer species of pleurobranchs than nudibranchs, and they aren’t typically quite as colorful, but many are predatory and powerfully toxic nonetheless.

Back to the story. Since 2009, a group of scientists in Argentina have been monitoring an outbreak of sea slugs off the coast of Mar del Plata, in the southwestern Atlantic (Farias et al. 2014). These sea slugs belong to Pleurobranchaea, a pleurobranch genus, and while they closely resemble P. maculata, their exact identity is unknown. Marine invertebrate diversity is poorly understood, even for relatively charismatic groups such as the sea slugs, so it wouldn’t be all that surprising if these turned out to be an undescribed species. What is known is that these mystery slugs contain a neurotoxin, also unidentified. Incidentally, P. maculata contains tetrodotoxin, 1-2 milligrams of which can kill a person, and while you might think the scientists who discovered that fact were the sea slug experts themselves, the real story contains far more intrigue, and a little tragedy, so brace yourself.

Pleurobranchia meckelii, a close relative of P. maculata. Photo by Heike Wägele & Annette Klussmann-Kolb.

Pleurobranchia meckelii, a close relative of P. maculata. Photo by Heike Wägele & Annette Klussmann-Kolb.

Pleurobranchaea maculata isn’t known from Argentina — yet. Its known range is halfway across the world, in the Pacific waters off the coast of New Zealand. In 2009 (McNabb et al.), after visiting beaches near Auckland, fourteen dogs died with similar symptoms of poisoning. Veterinarians contacted the National Centre for Disease Investigation, of the Ministry of Agriculture and Forestry, and a formal investigation began. As local media ran with the story, public interest grew and speculations were made as to the cause of these mysterious dog deaths.

Eventually, tetrodotoxin (TTX) was found in the vomit of one of the dogs, which led to suspicion that the dogs had eaten something on the beach containing the deadly toxin. TTX is used, often as a defense mechanism, by a variety of marine animals, including puffer fish (family Tetraodontidae, for which the compound gets its name), cone snails, and several species of blue-ringed octopuses (Kohr et al. 2014). McNabb et al. (2009) tested animals found on the beaches near Auckland and found that only one, the sea slug P. maculata, contained TTX in significant concentrations. The scientists then filed a report to the Auckland Regional Council, concluding that the dogs had eaten the poisonous sea slugs, and recommending that efforts be made to increase public awareness of the danger P. maculata presents to pets. Because TTX had never before been recorded in a sea slug, the investigators also implored the government to support continuing research on the biology, ecology and distribution of the slug, which at the time was very poorly known.

The gray side-gilled sea slug (Pleurobranchaea maculata) from New Zealand. Photo from McNabb et al. 2009.

The gray side-gilled sea slug (Pleurobranchaea maculata) from New Zealand. The one on the right is a female laying eggs. Figure 3 from McNabb et al. 2009.

We now know quite a lot more about P. maculata, the gray side-gilled sea slug, but to this day it is unclear whether the slugs synthesize the toxins themselves, or sequester it from TTX-containing prey. Across the world in North America, some garter snakes have evolved an immunity to the toxin and are capable of sequestering TTX from the rough-skinned newts they eat (Williams et al. 2004), and at least one species of caddisfly does the same thing by eating the newt’s eggs (Gall et al. 2012). So how do the slugs get their poison?

It turns out that only some populations of the species have TTX, and concentrations of TTX vary widely between individuals in each population (Wood et al. 2012). Khor et al. (2014) conducted an experiment in which they captured and maintained in aquariums 18 specimens of non-toxic P. maculata from South Island. Twelve of these slugs were fed a diet laced with TTX, and these specimens rapidly sequestered TTX both in the stomach and in the mantle (the fleshy “body” of a mollusk). In an interesting twist, they also found the females that were fed TTX laid toxin-laced egg masses.

The common garter snake (Thamnophis sirtalis). Some populations of garter snake can sequester tetrodotoxin by eating toxic rough-skinned newts (Taricha granulosa). Photo by Mark A. Wilson.

The common garter snake (Thamnophis sirtalis). Some populations of garter snake can sequester tetrodotoxin by eating toxic rough-skinned newts (Taricha granulosa). Photo by Mark A. Wilson.

Khor et al. then conducted a comprehensive survey of the benthic (ocean floor) invertebrates in an area where TTX-containing populations of P. maculata are known: the Auckland beaches. Despite the first experiment showing that P. maculata can in fact sequester TTX from food, the only other natural source of TTX they found was in a species of sand dollar, at concentrations far too low to explain the high toxicity of the slugs. So, while P. maculata is clearly capable of sequestering TTX from food, it still seems likely that they also produce it themselves.

The issue of whether wild populations of P. maculata manufacture their own TTX or sequester it is still very much unresolved. That said, I started this article as a report on toxic sea slugs in Argentina, and I’ve barely discussed them! So, here goes.

We still don’t really know that much about the Pleurobranchaea species in Argentina, mostly because we don’t know what species it is. The slug is readily distinguished from the only other known Argentinian Pleurobranchaea, P. inconspicua. The fact that these slugs possess neurotoxins may indicate they are an introduced population of P. maculata, or they may simply be an undescribed species that we only know about now because its population is growing. Farias et al. (2014) tested the slugs for neurotoxins, but further work is needed to determine if TTX is the toxin in question.

Pleurobranchus inconspicua (A) and the unknown Pleurobranchus (B), the two members of the genus known from Argentina. Figure 1 from Farias et al. 2014.

Pleurobranchus inconspicua (A) and the unknown Pleurobranchus (B), the two members of the genus known from Argentina. Figure 1 from Farias et al. 2014.

What we do know is that the population is indeed growing. Farias et al. claim, and rightly so, that this outbreak demands both additional research and public education, mostly because of the ecological consequences of a probably invasive sea-floor predator. In other parts of the world, invasive benthic predators such as sea stars have had disastrous consequences for local shellfish industries. However, they also emphasize that this slug is highly toxic, and the potential public health implications for the region have yet to be determined.

Sea slugs are amazing animals, and important components of the ocean floor ecosystem. Some are beautiful, some are deadly, and many are both. All deserve, and many demand, more scientific and public attention than is currently awarded them.

For a short news article that inspired me to write this one, click here.

Cited:

Farias, N.E., S. Obenat, and A.B. Goya. 2015. Outbreaks of a neurotoxic side-gilled sea slug (Pleurobranchaea sp.) in Argentinian coasts. New Zealand Journal of Zoology, published online: DOI: 10.1080/ 03014223.2014.990045.

Gall, B.G., A.N. Stokes, S.S. French, E.D. Brodie III, and E.D. Brodie Jr. 2012. Predatory caddisfly larvae sequester tetrodotoxin from their prey, eggs of the rough-skinned newt (Taricha granulosa). Journal of Chemical Ecology 38(11): 1351-1357.

Khor, S., S.A. Wood, L. Salvitti, D.I. Taylor, J. Adamson, P. McNabb, and S.C. Cary. 2014. Investigating diet as the source of tetrodotoxin in Pleurobranchaea maculata. Marine Drugs 12(1): 1-16.

McNabb, P., L. Mackenzie, A. Selwood, L. Rhodes, D. Taylor, and C. Cornelison. 2009. Review of tetrodotoxins in the sea slug Pleurobranchaea maculata and coincidence of dog deaths along Auckland Beaches. Prepared by Cawthron Institute for the Auckland Regional Council Technical Report 2009/108.

Williams, B.L., E.D. Brodie Jr., and E.D. Brodie III. 2004. A resistant predator and its toxic prey: persistence of newt toxin leads to poisonous (not venomous) snakes. Journal of Chemical Ecology 30(10): 1901-1919.

Woods, S.A., D.I. Taylor, P. McNabb, J. Walker, J. Adamson, and S.C. Cary. 2012. Tetrodotoxin concentrations in Pleurobranchaea maculata: temporal, spatial and individual variability from New Zealand populations. Marine Drugs 10(1): 163-176.

Testacella, the Shelled, Carnivorous Slugs

by Joseph DeSisto

Although we like to imagine that slugs are, by and large, peaceful herbivores, the truth is they are highly diverse and occupy a wide range of niches. It’s true, there are many slugs that persist on living plants, and can become the bane of flower or vegetable gardeners. Others are detritivores, and eat decaying organic material, including leaf litter, animal waste, and carrion. A few are fungivores and eat mushrooms — some are especially fond of plasmodial slime molds (Keller and Snell 2002). And some, such as Testacella and Selenoclamys, are carnivorous.

Testacella scutulum, a carnivorous slug from western Europe. Photo by Günter Wondrak.

Testacella scutulum, a carnivorous slug from western Europe. Photo by Günter Wondrak.

But first, a short taxonomic digression. The term “slug” doesn’t refer to any one lineage of organisms, but instead describes a number of lineages within the Gastropoda (snails), all of which independently lost their shells. Shell-lessness evolved at least seven times within the terrestrial gastropods (Wade et al. 2001). As to why so many groups lost their shells, a number of hypotheses have been proposed. The one I like best is that slugs are better adapted to living in small spaces, such as in rotten logs or underground, where large shells would be a hindrance. Alternatively, shells may simply have disappeared in taxa where they were not needed to serve their primary purpose, preventing water loss.

Although it might seem like losing shells would make slugs more vulnerable to predators, and so be a poor adaptation, it is important to remember that shells are energetically expensive to make, and not making shells might have allowed slugs to invest more energy in reproduction. Also, shell-lessness freed slugs from depending on a diet rich in calcium, which can limit the ability of snails to colonize certain habitats.

Testacella, a genus of slugs from Europe and North Africa, is unusual for a number of reasons. First, all six species of Testacella have the remnant of a shell on their posterior. This shell may be vestigial, in which case it has no function and, like a whale’s pelvis, is merely a reminder of its ancestry. Or, the shell may be a form of protection specific to Testacella‘s burrowing lifestyle. Unlike the slugs gardeners are more familiar with, Testacella spend their time underground, tunneling through the soil. Here a large, spiral shell would be a handicap, but a small, flat shell protecting the slug’s posterior might provide some defense against predators that approach from the tunnel behind. Either way, the structure is what gave the genus its name: Testacella is the diminutive form of the Latin word testaceus which means “shelled” (Scarborough 1992).

The shelled slug Testacella haliotidea. Illustration from Brehms Tierleben by Alfred Brehm.

The shelled slug Testacella haliotidea. Illustration from Brehms Tierleben by Alfred Edmund Brehm.

The reason for talking about Testacella here, however, is because it is one of the slugs best-adapted to a carnivorous lifestyle. Like shell-lessness, predatory behavior has evolved numerous times in both terrestrial and marine gastropods, but Testacella provides one of the best examples. Burrowing by day and emerging on rainy nights, they specialize in preying on earthworms. The best description I can find of the feeding strategy of Testacella, and in particular T. scutulum, comes from Liberto et al. (2011). If you are interested in this sort of thing, I strongly recommend checking out the original paper here, not just for the description but also for the photography showing each step of the feeding process. The whole affair is quite complex, but I’ve tried to summarize it here.

Like all mollusks, Testacella has in its mouth a radula, which is a hard, chitinous structure bearing rows of teeth. In most slugs, these teeth are small and used to scrape off bits of material from a leaf or other vegetable structure, but in Testacella, the teeth are large and hooked, and used in prey capture. The radula is supported by an underlying structure called the odontophore, which is made of cartilage and extensible — this is how the mollusk ejects its radula to feed.

The generalized mollusk feeding system, showing the radula (light brown), radular teeth (gray), and extensible odontophore (dark brown). Diagram by Benjamin de Bivort.

The generalized mollusk feeding system, showing the radula (light brown), radular teeth (gray), and extensible odontophore (dark brown). Diagram by Benjamin de Bivort.

When Testacella detects an earthworm, it ejects its odontophore and hooks the hapless annelid on its long radular teeth. With the worm secure, but still alive, the slug retracts the odontophore back into its mouth, and begins to swallow. At this point the radula “collapses” so that it surrounds the earthworm, eliminating any possibility of escape, and the worm is swallowed alive through a combination of suction and movement of the odontophore. The whole process can take an hour or more.

In 2006 a new species of carnivorous slug was discovered in a garden in Wales. It was named Selenochlamys ysbryda (Rowson and Symondson 2008), and received quite a lot of media attention. Selenochlamys isn’t related to Testacella; their carnivorous habit evolved separately, and ysbryda lacks the distinctive miniature shell of Testacella. However, both species are burrowers, prey on earthworms, and share a number of adaptations. Most conspicuously, both have a long, extensible odontophore and a radula lined with many rows of long, recurved teeth for use in prey capture. The specific name ysbryda translates to “ghost” in Welsh, a reflection of its striking pearly-white complexion, and the slug is popularly known as the “ghost slug.”

Ghost slugs began turning up elsewhere in Britain, always in gardens with a healthy population of earthworms. At first it was surprising that a new slug should turn up in a back garden in Cardiff, but it turns out that S. ysbryda is probably an introduced species from the Crimean Mountains, where an apparently native population was discovered by Balashov (2012) alongside its closest known relative, Selenochlamys pallida. Probably ysbryda was first introduced to British gardens in plant pots. Clearly there are many marvels left to be explored. The discovery of the ghost slug teaches us that our own backyards can be as good a place to start as any.

Cited:

Balashov, I. 2012. Selenochlamys ysbryda in the Crimean Mountains, Ukraine: first record from its native range? Journal of Conchology 41(2): 141-4.

Keller, H.W. and K.L. Snell. 2002. Feeding activities of slugs on Myxomycetes and macrofungi. Mycologia 94(5): 757-60.

Liberto, F., W. Renda, M.S. Colomba, S. Giglio, and I. Sparacio. 2011. New records of Testacella scutulum Sowerby, 1821 (Gastropoda, Pulmonata, Testacellidae) from Southern Italy and Sicily. Biodiversity Journal 2(1): 27-34.

Rowson, B. and W.O.C. Symondson. 2008. Selenochlamys ysbryda sp. nov. from Wales, UK: a Testacella-like slug new to Western Europe (Stylommatophora: Trigonochlamydidae). Journal of Conchology 39(5): 537-52.

Scarborough, J. Medical and Biological Terminologies: Classical Origins. Norman, Oklahoma: University of Oklahoma Press, 1992.

Wade, C.M., P.B. Mordan, and B. Clarke. 2001. A phylogeny of the land snails (Gastropoda: Pulmonata). Proceedings of the Royal Society of London B 268: 413-22.