by Edith Widder
Detritivores are so named because they survive on a diet of detritus, that is, the rain of food particles falling from above. Sponges constantly suck water through the tiny chambers that make up their body wall, where bits of foodstuff are filtered out before the current is expelled into the central barrel. The knobby-armed bubblegum coral and the mushroom-shaped sea pens feed by extending polyps into the water to grab passing particles. Since detritus is the primary food source, it’s logical that the giants would show up where it accumulates at an interface like the bottom. Yet such giants do not occur everywhere on the seafloor, but only in places like the Monterey Canyon and on and around seamounts and rocky outcroppings where there is just the right combination of enhanced productivity in surface waters, a hard bottom to provide solid points of attachment, and particle-carrying currents.
In 2009, the place we picked to explore was yet another Seussian garden, even more fantastical than the one I slammed into in the Monterey Canyon. This one covered the slopes of a series of parallel limestone mounds in deep waters off the west end of Grand Bahama Island. Each of these mounds is shaped like an upside-down ship’s hull, with sizes ranging from small dugout canoes to major cruise liners and oriented north-south, parallel to the Florida Current. Each was essentially an oasis surrounded by a sedimentary sea, allowing us to sample both types of seafloor habitats.
Anticipating that trip, I was of two minds about what we might expect to find in terms of the number of light emitters on the deep-sea floor. On the one hand, all those big eyes suggested a significant selective advantage for being able to see bioluminescence. On the other hand, since much of the bioluminescence in the midwater is related to playing hide-and-seek in a world without hiding places, it could also be argued that on the bottom, where there are structures to hide behind and no need for counterillumination to conceal silhouettes from upward-looking predators, bioluminescence might be much less prevalent. This is certainly the case in the coastal zone environment, where only about 1 to 2 percent of bottom-dwelling species are bioluminescent, as compared with more than 75 percent of midwater species, but in the coastal zone there is also lots of illumination from sunlight and moonlight, making bioluminescence nonessential for visual communication. The only way to find out for sure was to go look for ourselves.
This whole expedition was a visual feast, which began with my first dive on the site. As we descended at the north end of a large mound, it appeared, like a steep-sloped island encircled by a white sand ocean. As we headed upslope toward the “keel” of the mound, we encountered a fantastic-looking landscape of row after row of straw-colored stalked crinoids. More commonly known as sea lilies, these ancient creatures look more like miniature cartoon palm trees than the sea urchins and sea stars that are their closest living relatives. The mouth is located at the center of their crown of feathery palm fronds, which are their arms. Each mouth was pointing toward us as we proceeded upslope against the current, while their arms curved backward into the current, slowing the flow and making it easier for the tube feet to capture particles from the water.
There was little to no space between individuals down the length of each row, but there were large gaps between the terraced rows that were oriented perpendicular to the current, which appeared to optimize detritus collection on the down-current side of the mound. One of our collaborators on this expedition, Chuck Messing, was a leading authority on crinoids. We knew he’d be thrilled by this find, and we collected specimens for him to identify and for us to test for bioluminescence. Bioluminescence is rare in crinoids, but not unheard of, so I was disappointed when it turned out that these and all the other crinoids we examined during this expedition proved to be non-luminescent.
As we proceeded south along the top of the mound, a very different vista loomed into view—large, fanlike “trees” of magnificent golden coral*7 over three feet tall and six feet wide and ranging in color from canary yellow to rust orange to auburn brown. We knew these were very likely to be bioluminescent (as similar species are), and sure enough, when we turned out the lights and brushed the sub’s robotic arm through their soft branches, they glowed an intense turquoise. Smaller delicate sea fans were also present, forming a dense understory. Most were gold-colored, but a few were a vivid purple. These all proved to be non-luminescent.
Colonies of white stony coral,*8 also non-luminescent, studded the hillside at random intervals, their fragile branches poking out at disparate angles, making them appear disorganized compared with the delicate flattened tracery of the fans, with their intricately spaced, nonoverlapping branches always oriented perpendicular to the current. There were also feathery fronds of bamboo coral,*9 so named because their internal skeleton is made up of alternating long white and short black bands, resembling, in shape, a bamboo stalk. All of these proved to be luminescent. In some species, the coral branches glowed neon blue anyplace they were touched, while others produced twinkling displays that looked like a profusion of miniature cerulean-blue Christmas tree lights winking on and off.
Although they look like trees and bushes, all these fantastic life-forms are animals—specifically, detritivores. And perched in their branches were more detritivores: brittle stars, snake stars, sea stars, gooseneck barnacles, hydroids, sponges, anemones, feather stars, and basket stars. We collected samples of all of these and more, but in the end, fewer than 20 percent of all the animals we tested for bioluminescence proved capable of making light.
Most of those light makers were already known to be luminescent, but a few were new and wonderfully strange. My favorites were the anemones. There were Venus flytrap anemones,*10 which look like a bright orange version of Audrey II from the musical Little Shop of Horrors, but instead of sucking blood, when prodded they squirt out strings and swirls of sticky cobalt-blue luminescence. This probably deters predators that don’t want to make themselves targets for their own visual predators.
Even more wonderful were the two bioluminescent anemones that we found attached to the seashell home of a hermit crab. These glowed when stroked and brought to mind wild imaginings of a deep-sea existence toting around a mobile home adorned with elaborate Victorian lamps that light up only when rubbed like Aladdin’s lamp.
These were wonderful discoveries, but they paled in comparison with what we witnessed when we turned out the lights and sat quietly in the dark. Whenever I did this in the midwater, as long as I went dead still I saw nothing—no spontaneous bioluminescence, just absolute and complete blackness. But here, on the seafloor, there was frequent luminescence, not from the detritivores living on the bottom but from plankton carried by the current, which were mechanically stimulated when they bumped into the detritivores. I recorded some video of this with my intensified black-and-white camera, which showed brief flashes of light in the branches of the golden coral. But the best imagery came from Sönke, who used his Nikon to take a ten-second color exposure. Just before capturing the image, he had the pilot sweep the manipulator through the golden coral, causing it to glow. In the image, you can clearly distinguish the coral branches studded with distinct polyps glowing blue-green, while the plankton hitting it and passing through appear as blue streaks.
We measured the emission spectra of all the animals we collected and found that many of the bottom dwellers produced a greenish light, rather than the blue that dominates in midwater inhabitants. Suspended sediment near the bottom favors green-light transmission over blue, so the color shift may reflect selection for maximum visibility. A similar shift toward greener emissions is seen in some bioluminescent inhabitants of sediment-laden coastal waters.*11
We wondered if the bioluminescent color difference between the detritivores and the plankton that bump into them could explain another intriguing mystery that had emerged from Tammy’s research. During our Deep Scope 2005 mission, she had discovered that a squat lobster called Gastroptychus spinifer appeared to have two different color receptors in its eyes. With result
s from only one animal, she didn’t feel she could publish such an unusual finding, but on this 2009 mission she managed to get more specimens that confirmed it. To see color requires giving up sensitivity, so we were very curious about what this extraordinary adaptation might be for.
Although the flattened reddish-orange bodies of these squat lobsters make them look more like lobsters than the hermit crabs to which they are most closely related, their lifestyle and feeding strategy set them apart from either group. We saw many of these guys perched high in the branches of the golden corals, with their absurdly long arms spread to either side and their pincer-like claws splayed open. Their large eyes are on stalks that are not on either side of the head, but side by side and forward-facing in a way that would potentially allow binocular vision—in other words, depth perception.
Based on Tammy’s results and our observations of the nature of luminescence on the deep-sea floor, we speculated that they might use color vision as a way to distinguish the blue luminescence of plankton hitting the coral from the blue-green luminescence of the coral itself, their pincer claws and binocular color vision allowing them to pluck food directly out of their hosts’ mouths—making them less-than-delightful houseguests.
Being able to observe the extraordinarily alien visual environment of the deep sea is essential to understanding the life therein. Although the number of luminescent species we found on the deep-sea floor was much fewer than what we discovered in the midwater, the amount of spontaneous bioluminescence was vastly greater. It seemed very likely that food in the form of bioluminescent plankton that lights up when it encounters the deep-sea floor must be a valuable clue for many big-eyed seafloor inhabitants.
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There is still another vital food source that may light up when it encounters the deep-sea floor, and that is marine snow. The term “marine snow” was first coined by William Beebe to describe the daily slow-motion sprinkling of food into the deep sea. As usual, he nailed it. It looks very much like snow—white flocculent particles resembling everything from a slow-motion flurry to a blizzard. But if you look closer, you notice differences—single flecks, white fluffy bits, messy clumps. The Inuit supposedly have more than fifty words to describe the various forms of snow, and marine snow may be deserving of similar linguistic largesse.
Surprisingly, this diversity is sometimes visible even with the lights off. Obviously, this is possible only when the “snow” is luminescent, but in my experience a lot of it is. Bioluminescence from marine snow must be stimulated either mechanically or with light, and once stimulated it does not readily reignite, which makes sampling it a challenge.
The best way to see it is to either ascend or descend through the water column with the lights out and intermittently flash a light into the darkness. If you use a flashlight, you get a localized response. (One of the sub pilots told me about a time when the light-stimulated marine snow was so dense that he could write his name in light.) But you get a more spectacular response if you flick the sub’s floodlights on and off. When you do, as soon as your artificial light is extinguished, you are surrounded by a snowstorm where all the snowflakes simultaneously flash on and then gradually fade out. But it’s not winter snow—it’s marine snow, like the mermaid’s tears I observed on my first dive in Wasp, short strings of tiny glowing orbs encased in a wispy sheath, or fragile gossamer aggregates that look like miniature bottlebrush flowers with specks of light at the end of each filament, or some other equally fragile configuration. If you turn your lights on, the source of the light will likely be invisible. You may see flecks of marine snow, but whether they were the cause of the light is not obvious.
Marine snow is very, very important. It is the primary source of food in the deep, and therefore it seems like we should know a bit more than we do about its bioluminescence and what role it might play in the survival strategies of deep-sea fauna, but it has been an incredibly difficult phenomenon to document. With recent developments in camera technology, I have real hope that revelations may come soon—hopefully before I shuffle off this mortal coil—because it’s one of those profound mysteries at the edge of the map that not only is intensely intriguing but may also prove extremely significant.
Specifically, I would like to understand the role of marine snow in what is known as the biological pump, the carbon cycle in the ocean, which is of more than passing interest these days because of the part it plays in lowering atmospheric carbon dioxide, and thus slowing global warming.
Years of observing it firsthand have led me to believe that most of the bioluminescence I have seen associated with deep-sea marine snow is bacterial. What makes this a somewhat controversial idea is the fact that the bioluminescence needs to be stimulated. Bacterial bioluminescence is very different from most other kinds of bioluminescence, because instead of producing flashes of light, it emits a persistent glow. This is because its light chemistry is directly linked to its breathing chemistry (better known as the respiratory chain).
Most people are familiar with bacterial bioluminescence as it relates to animals like anglerfish and flashlight fish. These species don’t manufacture their own light-producing chemicals but instead co-opt the light produced by bacteria and, in return, provide the microbes with food and shelter within growth chambers. In the anglerfish, the chamber is called an esca and is located at the end of a long fin ray that serves as a fishing rod, dangling the glowing morsel within reach of the angler’s toothy maw. In the aptly named flashlight fish, the bacteria reside in a large light organ just below the eye. To turn off its flashlight, this fish actually has the equivalent of an eyelid that closes up, shuttering the shine.*12
Fish and squid that have evolved symbiotic relationships with bacteria control the light in a variety of ways, usually through mechanical shuttering, but in some cases it’s thought that the light is modulated by controlling the availability of oxygen, because without oxygen, bacteria don’t glow. The Exploratorium, in San Francisco, has a lovely demonstration of this in its exhibit of bioluminescent bacteria. When I first saw it many years ago, they were maintaining cultures of bioluminescent bacteria in flasks held on a shaker table.*13 When the table wasn’t shaking, no light came from the flasks, but when the shaker was activated, the culture was stirred, introducing oxygen that activated the glow. Recently, they came up with a more elaborate scheme to demonstrate the same phenomenon. The bacterial broth is held in a thin tank with air inlet ports that visitors can control to create swirling patterns of living light.
The point is that oxygen must be present for the bacteria to glow. In marine snow, phytoplankton and other organic matter are broken down by microbes that consume oxygen. This is a portion of the biological pump that releases carbon dioxide into the water. Although the marine snow may be surrounded by oxygen-laden water, within the particle itself there is an anoxic microenvironment. Bumping the snow floc is just like activating that shaker table, introducing oxygen and allowing the bacteria to glow. Shining light on the snow may also introduce oxygen by stimulating its production in photosynthetic bacteria, known as cyanobacteria, which are also commonly found in marine snow. That might explain how marine snow glows…but it doesn’t explain why.
When I was starting out in the field of bioluminescence, one of the hotly contested issues of the day was how bioluminescence could have ever first evolved in bacteria. In other words, how could producing light possibly help a single bacterium survive? This was especially vexing from an evolutionary perspective because a single bacterium doesn’t produce enough light to be visible to any known eye; its emission is simply too dim. The only way bacteria are visible is if there are millions of them together, so how could the first bacterium to emit light have been selected for? What is even more confounding is that if you mix together two strains of the same species, one luminescent and the other dark, the dark mutants rapidly overrun the culture, because the energy cost of producing light puts
the light emitters at a disadvantage. Any way you look at it, it seems like the deck was stacked against the evolution of bacterial bioluminescence.
A possible solution to this conundrum was revealed when some Polish scientists tried irradiating a mixed culture of dark and light-emitting mutants with ultraviolet light. When they did, suddenly the situation was reversed: The light emitters seemed to have the advantage and took over the culture. The bioluminescent strain continued to predominate as long as the UV light was on, but as soon as it was turned off, the dark strain regained supremacy. The reason was related to the fact that UV light damages DNA, which is why you should always remember to wear sunscreen.*14
A UV photon packs a significant energy punch—more than blue or green or any of the colors of the rainbow—enough to mess with DNA’s structure. Because UV light is so damaging, bacteria evolved a remarkable enzyme called photolyase, which repairs UV-damaged DNA. Intriguingly, this enzyme requires visible light—blue light, in fact—to work its magic, so apparently the selective advantage of bioluminescence is that it can stimulate DNA repair,*15 even at light levels that are too dim to be visible.
The need for cell repair mechanisms is now thought to be an underlying basis for the evolution of a lot of different bioluminescent chemistries. One of the many challenges that life on Earth must deal with is not just the destructive properties of UV light but also the damaging effects of oxygen. We think of oxygen as a good thing, because without it we would die, but it does have a downside. It’s so hungry for electrons, it will rip them from vital molecules like DNA and proteins. It is because of this destructive effect of oxygen that consuming antioxidant-containing foods like fresh fruits and vegetables is so important. Antioxidants prevent cell damage of a kind that is linked with aging and ailments like cancer, Parkinson’s, Alzheimer’s, and heart disease.
