Chemical Communication Under The Sea

Smaller than a fingernail, the marine slug Elysia tuca may not seem like a formidable predator. But the tiny gastropod has an unwavering predilection for a rather intimidating prey. The slug hunts Halimeda incrassata, a species of seaweed that harbors toxic defense compounds and is more stone than flesh—it’s 85% calcium carbonate, the same mineral found in limestone and coral.

Undaunted by its foe’s fortifications, the slug hunts the seaweed by sniffing out two chemicals produced by the alga, namely 4-hydroxybenzoic acid and halimedatetraacetate—a discovery recently made by Douglas Rasher, a marine chemical ecologist at the University of Maine, and colleagues Julia Kubanek and Mark Hay at Georgia Institute of Technology (Proc. Natl. Acad. Sci. USA 2015, DOI: 10.1073/pnas.1508133112).

After using these cues to find its prey, the slug pierces the seaweed with a sharp sawlike appendage called a radula and sucks out the seaweed’s cytoplasm, including chloroplasts, which the slug then uses to make its own energy from sunlight. The “solar-powered slug,” as Rasher calls it, gets 60% of its fixed carbon from these stolen photosynthetic organelles. The slug also steals the seaweed’s toxic arsenal of halimedatetraacetate for its own defense.

Even though molecular-mediated, plant-herbivore relationships are well understood in terrestrial ecosystems, this is one of the first such relationships reported from a marine environment. “Marine chemical ecology has lagged for decades behind terrestrial research,” comments Henrik Pavia, a marine chemical ecologist at the University of Gothenburg, in Sweden. But the marine branch of the chemical communication field is starting to catch up. In the past several years, a handful of underwater projects have begun to show that intricate, inter- and intraspecies interactions involving sex, war, and predation are also being mediated by molecules—albeit under the sea instead of on land.

These studies are revealing that even though water ecosystems differ from their land counterparts, there are stunning parallels in the way organisms in these dissimilar habitats use chemistry. The slug-seaweed project, for example, “blows the notion that marine plant-herbivore interactions differ fundamentally from terrestrial associations out of the water,” comments May Berenbaum, a chemical ecologist at the University of Illinois, Urbana-Champaign.

When the seaweed is attacked by the slug, the seaweed uses a strategy similar to that employed by terrestrial plants under attack by herbivorous insects: It drops branches occupied by its predator, presumably to avoid getting infected and killed by a fungus found on the slug’s sawlike radula. The parallel is fascinating, Rasher says, because once herbivores and plants crept onto land, they evolved independently of those in marine environments for 400 million years, yet they developed similar sorts of chemical communication relationships.

One of the reasons marine chemical ecology has lagged behind terrestrial studies is that “observing organisms in their natural environment—the ecological dimension of chemical ecology—is orders of magnitude more difficult in marine ecosystems,” Berenbaum says. Ecological observations weren’t possible underwater before scuba diving equipment was popularized in the mid-20th century, Rasher says. By then, terrestrial chemical ecology research was already in full swing.

Without being able to directly observe their slug in its natural environment, Rasher and his colleagues at Georgia Tech might never have noticed the gastropod’s sly behavior, for instance. The researchers got interested in the slug because they knew it preyed specifically on the stony seaweed, and they had seen on scuba dives the slug’s uncanny ability to figure out when the seaweed was in the throes of its very short reproductive period. During this short window of time, only about 36 hours, the marine alga produces reproductive cells that are packed with more chloroplasts and defense chemicals than normal—making them a bountiful buffet for the slugs. Lo and behold, “during the reproductive periods, the seaweed is absolutely teeming with slugs,” Rasher says. “Somehow the slug knew the plant had these concentrated packages of chloroplasts and defense chemicals to steal.” That’s when “we suspected chemical cues were involved,” he adds.

In addition to the specialized scuba equipment required to do marine observations, another challenge to underwater chemical ecology is that “waterborne cues are inherently very difficult to isolate and identify,” Rasher says. Trapping and analyzing chemical communication volatiles in air is relatively straightforward using filters and gas chromatography compared with the vast volumes of water that must be processed in marine experiments to identify communication chemicals.

Furthermore, waterborne compounds are often too low in concentration to identify, Rasher says, or they are unstable and degrade during the purification or identification process. These challenges have “halted many efforts to discover marine parallels of terrestrial examples.”

For example, in 2012, researchers led by Georgia Tech’s Hay reported that goby fish respond to a chemical distress signal given out by coral when it comes into contact with poisonous seaweed. The goby fish come to the coral’s rescue by eating this toxic seaweed, which most reef fish deliberately avoid (Science, DOI: 10.1126/science.1225748). Although the team used marine extracts to prove that goby fish sense a chemical in the water that inspires them to protect the coral; three years later they are still working to identify the exact molecule.

Yet the sensitivity of the liquid chromatography and mass spectrometry techniques commonly used in marine chemical ecology is improving, and with these improvements come signs that the tide is turning for the field. Earlier this year a team of researchers led by Gothenburg’s Pavia, his colleague Erik Selander, and Georgia Tech’s Kubanek discovered that algae produce toxic blooms as a defense strategy. Using a suite of assays and analytical techniques, including mass spectrometry and nuclear magnetic resonance, the team found that when the algae sniff out chemicals called copepodamides produced by the algae’s zooplankton predators, the algae produce the toxic blooms to protect themselves from the zooplankton (Proc. Natl. Acad. Sci. USA 2015, DOI: 10.1073/pnas.1420154112).

Although there are only a handful of successes thus far, more are likely on the horizon. Among hundreds of presentations made at a recent conference on chemical ecology in Stockholm, several were given by researchers who discussed work in progress from the marine environment. When C&EN spoke to Pavia, he was in Liverpool, England, at a marine science meeting, looking to collaborate with biologists who suspect there’s chemical communication involved in their underwater ecosystems. It’s not just a matter of uncovering fascinating relationships among underwater plants and animals, Pavia says. As drastic chemical changes such as acidification and pollution are taking place in the ocean, he adds, researchers need to learn about endemic relationships before they are irreversibly interrupted.