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.

Advertisements

One response to “A Sea Slug Story

  1. Pingback: How Poisons Work: Tetrodotoxin | Beautiful Nightmares

Leave a Reply

Fill in your details below or click an icon to log in:

WordPress.com Logo

You are commenting using your WordPress.com account. Log Out / Change )

Twitter picture

You are commenting using your Twitter account. Log Out / Change )

Facebook photo

You are commenting using your Facebook account. Log Out / Change )

Google+ photo

You are commenting using your Google+ account. Log Out / Change )

Connecting to %s