by Edith Widder
At least that was my best guess. An awful lot of what we think we know about bioluminescence in the ocean is just guesswork. A light organ next to the eye is a flashlight. A light dangled in front of the mouth is a fishing lure. But a light organ at the tip of such a ridiculously long tail and a brilliant racing stripe that runs the full length of the fish still leaves me suffering from a failure of imagination. And yet, what a glorious puzzle to try to solve: What in the day-to-day life of a gulper eel makes these adaptations critical to its survival?
Grasping what drives adaptation is fundamental to understanding the course of evolution. In today’s world, figuring out how life can adapt in the face of rapid climate change is key to distinguishing potential evolutionary winners and losers and to knowing where to focus management efforts in order to minimize biodiversity loss. It’s also critical that we recognize our own vulnerability. Believing that the world was designed to have us in it and therefore everything is going to be all right is a dangerous folly. I think Douglas Adams put it best:
This is rather as if you imagine a puddle waking up one morning and thinking, “This is an interesting world I find myself in—an interesting hole I find myself in—fits me rather neatly, doesn’t it? In fact it fits me staggeringly well, must have been made to have me in it!” This is such a powerful idea that as the sun rises in the sky and the air heats up and as, gradually, the puddle gets smaller and smaller, frantically hanging on to the notion that everything’s going to be all right, because this world was meant to have him in it, was built to have him in it; so the moment he disappears catches him rather by surprise.*3
How is it that we or any other living creature came to be so well adapted to our environment? You can thank that old evolutionary two-step: natural selection acting on heritable variation. The transfer of information from one generation to the next is the basis of being. It is written in our DNA. Intriguingly, it is not a perfect transcription, but an imperfect one, because it is the imperfections—the experiments in how to be—that provide the framework for natural selection.
Nonlethal mutations produce offspring that can vary in form and function. You are not a perfect clone of your progenitors. There are differences. Some of these variations may prove beneficial to such a degree that your odds of surviving long enough to pass on your genes to your offspring are enhanced. The peppered moth is the classic example. During the industrial revolution, soot and pollution darkened the trunks and branches of trees favored by these moths, making the light-colored peppered moths stand out as easy prey for visual predators such as birds. As a result of increased predation on the light-colored moth, a darker-colored variant was favored, and in the course of less than fifty years it went from constituting just 2 percent of the population to predominating at 98 percent. Now that’s success!
Marine bioluminescence is a comparable evolutionary success story. Why? How did there come to be so many light makers in the ocean? The numbers are staggering. When William Beebe conducted trawls off Bermuda, in the same waters where he dove the bathysphere, he found that more than 90 percent of the fish he collected in his nets were bioluminescent. When you do the math, it turns out that we’re not talking about mere billions or even trillions but possibly quadrillions of bioluminescent fish in the ocean.
If you measure success in terms of numbers, then bioluminescent fish are the most successful vertebrates on the planet. There are also shrimp and squid, as well as plankton (like dinoflagellates and copepods) and untold numbers of fragile jelly animals, that are part of this light-spangled bouillabaisse. Their numbers vary depending on depth and location, but in the open ocean, the largest living space on the planet, there is no question that bioluminescence rules.
Why has bioluminescence arisen so many times? Logically, it seems obvious that selection for light emission must have evolved after eyeballs did. One line of thought goes that the development of vision allowed the detection of prey at a distance, which led to an explosion of diversification—the result of an arms race between predators and prey. As the ocean filled up with predators that were becoming ever swifter and nastier, prey had to be able either to outswim their pursuers or to hide from them. In open water, where there are no hiding places, the only refuge was darkness. As a result, prey, followed closely by predators, began to move into darker waters.
Surviving at the edge of darkness favored certain mutations such as improved visual sensitivity. It also favored any camouflage that made prey harder to detect, such as countershading and counterillumination. Those that didn’t counterilluminate would be more easily picked off by visual predators, just like the light-colored variants of the peppered moth.
Viewed in this light, it is not surprising that the small, unassuming bioluminescent bristlemouth fish is the most abundant vertebrate on Earth. Think of that: The numerically dominant animal with a backbone, numbering by some estimates in the quadrillions, is a three-inch fish whose most outstanding feature is the array of light organs adorning its belly—light organs that allow it to hide in a place with no hiding places. The conundrum is why the ocean isn’t filled with nothing but this one kind of counterilluminating fish. Different species arise in places where populations get broken up and must adapt to separate circumstances. In a complex environment like a rainforest, a diversity of species makes sense: Animals occupying varied habitats exhibit distinctive patterns of coloration contingent on what background they blend with and unusual mouthparts depending on what food they eat. Once populations are separated, they change in singular ways, resulting in a diversity of forms.
Genetic isolation is the necessary precursor to the development of different species and the hallmark of natural selection. But in the open ocean, where there are no obvious barriers, why would there be any diversification? The answer is…sex.
The key to success in sexual reproduction is attracting more and better mates. Living in darkness makes it harder to locate mates, so once bioluminescence arose as a means of camouflage, its redirection for mate attraction provided added value and a possible route to genetic isolation. For example, deep-sea lantern sharks, besides having a dense array of tiny belly lights for camouflage, also have light-emitting patches on their flanks that look rather like tribal stripe decals on racing cars. These are species-specific, which means that while one species sports a long, thin lightning stripe, another is emblazoned with a scythe, while others have equally distinctive markings simplifying the process of recognizing a prospective mate. These differences apparently came about not because of physical barriers but because of sexual preferences.
A great example supporting the idea that bioluminescence has played a significant role in the speciation of the ocean can be seen by comparing lantern sharks with viper sharks, who also have belly lights but no flank markings, and therefore no apparent sexual selection. While there is only one known species of viper shark, there are thirty-seven species of lantern sharks!
The diversity of bioluminescent life-forms in the ocean is all the more astounding when you compare it with the situation on land, where light producers are exceedingly uncommon. Besides fireflies and glowworms, there are also a few relatively rare click beetles, earthworms, millipedes, some mushrooms, and one particular kind of land snail. In freshwater, it’s even more scarce—the only known example is a limpet (a type of mollusk) found in the streams of northern New Zealand. Clearly, these are exceptions rather than the rule. The reason that luminescence is so uncommon outside the oceans is thought to be that the existence of more and better hiding places makes it so much easier for prey to hide from predators that they don’t need to depend on darkness.
Bioluminescence was well established in the ocean when life first invaded land, lakes, and streams. But these early colonists were not luminescent, so the ability to produce light needed to be reinvented—something that was eminently doable, given how many separate times it arose in the ocean. However, the selection pressure that f
orced animals into darkness to hide was absent in a landscape crammed with all manner of vegetation, and plenty of nooks and crannies. If animals didn’t need to live in the dark to avoid being spotted by predators, then they didn’t need to evolve bioluminescence to help them survive.
Retracing bioluminescence through evolutionary history is greatly complicated by the fact that so little of it is preserved in the fossil record. Photophores can sometimes be discerned in well-preserved specimens of fish such as lanternfish and hatchetfish, but in most cases there is no visible external manifestation in a fossil that can be definitively identified as bioluminescent—so how can we ever know for sure how bioluminescence arose? One way is to get very, very lucky.
* * *
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Getting wildly lucky is exactly what happened on a mission in the Gulf of Maine near the end of the summer of 1997. I was serving as co–chief scientist along with my former postdoc and now collaborator Tammy Frank, on my fourteenth expedition with the Johnson-Sea-Link. We were diving in a place called Oceanographer Canyon, along the southern rim of Georges Bank. Tammy and I had just returned from a daytime dive where we were running transects at different depths to document animal distribution patterns at different light levels. Between transects, if we saw anything interesting we would collect it, and on this dive we had spotted something quite unusual as we were ascending from 2,600 feet toward 2,400 feet: a strange-looking red octopus. When we first spotted it, the animal was hanging inverted with its arms outstretched. Webbing between its arms made it look like an open, upside-down umbrella. As we drew closer, the creature first attempted to escape by executing a jellyfish-like contraction, but after only one slow-motion medusoid pulse, it gave up swimming and inflated itself into a highly distended balloon. For several minutes it held that pose, and then it started slowly flapping the two large fins on either side of its head in a sculling motion while simultaneously twisting its body to deflate the balloon. That’s when the pilot managed to capture it.
Back up on the ship, we transferred the football-sized octopus into a large Plexiglas tank in the wet lab so we could observe and photograph it. It was both bizarre and beautiful, and I was trying to document it from every possible angle. Unlike every other octopus I had ever observed in a tank, it did not affix itself to the sides or the bottom, but instead hung in the center while contorting its elastic body into a series of fantastic shapes. It had just spread its arms—allowing me to get a great shot of its mouth and the underside of its web—when my current postdoc, Sönke Johnsen, leaned over my shoulder and said, “Those don’t look much like suckers.” I lowered the camera so I could look with unobstructed eyes, and I had to agree. They looked like shiny white pearls, or, more specifically, like photophores. This was a surprise, because while bioluminescence is common in squid, it’s rare in octopods. In fact, there were only two known examples, and their light emission has nothing to do with their suckers: It emanates from a peculiar yellow ring with scalloped edges that surrounds the mouth of the female, and only at certain times—likely when they’re trying to attract a mate. Bioluminescent suckers, however, were unheard of.
We immediately transferred what we were now calling the red balloon octopus*4 into a smaller container so we could carry it into a dark room. Sönke and I positioned ourselves on either side of the octopus, and then after Sönke turned out the lights, I prodded the creature gently with my finger. There was an immediate response as blue light blinked on and off from the sucker-photophores asynchronously, creating a lovely twinkling effect. This was a significant discovery all on its own, but later, when we were able to microscopically examine cross sections of the light organs, we realized it was even more momentous than we’d first imagined. We saw vestigial muscle rings characteristic of suckers. They were suckers that had evolved into photophores, which is why the photograph I was taking when Sönke leaned over my shoulder eventually ended up on the cover of the very prestigious scientific journal Nature, where we published our discovery. Here was an example of evolution caught in the act.
As with the peppered moths seeing a shift from light- to dark-colored variants in response to industrial pollution, many populations have undergone similar major evolutionary alterations due to changing environments. Charles Darwin said, “It is not the strongest or the most intelligent who will survive, but those who can best manage change.” Put more succinctly, such changes force life to adapt or die.
Therefore, as visual predators proliferated, octopods needed to find a way to hide or they’d perish. Many populations adapted by becoming masters of camouflage, but a few, like the glowing sucker octopus, took a different tack and moved to deeper, darker waters. Dimmer light makes it harder to be seen by predators, but it also makes it more difficult to locate and attract a mate. Many octopods seduce mates by throwing their arms up over their heads and displaying their suckers as if they were in a wet T-shirt contest: “Hey! Look what I’ve got!” Under such circumstances, it makes sense that sexual selection would favor mutations that made the suckers more visible.
Because food is scarcer in deeper waters, once the suckers became more detectable, they also became valuable for a wholly different function—attracting prey—which helps explain how the glowing sucker octopus developed such an unusual diet. While most octopods consume things like scallops, crustaceans, and fish, the glowing sucker octopus survives solely on a diet of copepods. Since copepods are like the insects of the sea, this food regimen is the equivalent of a Florida raccoon living on a diet of mosquitoes. Sure, they are plentiful, but how can they possibly be gathered up in sufficient numbers to make a full meal? This is where the bioluminescent suckers come in. By hanging upside down in the water and twinkling its suckers, the octopus presumably looks like a yummy patch of plankton, which will attract copepods. Once a swarm has assembled, the octopus forms itself into a balloon,*5 sealing the copepods inside. Then it pulls its arms down toward its mouth, where a mucous layer traps the copepods, which can then be consumed like a gourmet seafood aspic.
With the development of glowing suckers that could be used for enticing both mates and food, this octopus variant could abandon its bottom-dwelling existence, where its suckers were useful for hanging on to things like rocks and shellfish, in favor of an open-ocean existence where their adhesive properties were unnecessary. Once a body part becomes obsolete, it is no longer favored in the selection process and gradually degenerates over many generations, as mutations that cause dysfunction will be selected against. This is how suckers become light organs, while still retaining some vestigial properties of suckers.
According to this hypothesis, bioluminescence in the glowing sucker octopus originally came about because of sexual selection. Tinder didn’t invent sexual selection; it’s been around since the invention of sex. But, as with Tinder, sexual selection has led to some pretty bizarre adaptations. The male peacock’s tail is a particularly showy example. Could the gulper eel’s tail or its racing stripe boast similar origins? How can we ever know, when no one has ever seen it use its taillight or racing stripe in its natural environment? If that taillight is a lure, used to draw in either food or a mate, then what kind of calculus is required to turn it on? How great is the risk of revealing itself to potential predators? And, if it does, what are its chances of escape using inflation or blinding? These are all questions that could be answered if only we could observe the fish in its natural environment, but how was that ever going to be possible? I wondered. It was a notion that kept recurring in my career, like an itch I couldn’t scratch.
Skip Notes
*1 The eight Plexiglas collection cylinders mounted on the front of the sub’s lower work platform were known as detritus samplers (DS) because they were originally designed to collect detritus or marine snow.
*2 Using feet instead of meters for depth while using metric units for temperature may seem odd, but that’s because those were the units used by the dept
h and temperature systems installed on the sub. For imperialists living in England, 4.2°C converts to nippy. For imperialists living in Florida, it’s considered below the legal limit. For imperialists who prefer real numbers, 4.2°C = 39.6°F.
*3 The Salmon of Doubt: Hitchhiking the Galaxy One Last Time, a posthumous collection of writings by Douglas Adams (New York: Ballantine, 2002).
*4 Its scientific name is Stauroteuthis syrtensis, but since our discovery, its common name has become the glowing sucker octopus.
*5 Behaviors can serve multiple functions, and it’s likely that the octopus also uses its balloon inflation as an antipredator defense, as seen in the gulper eel’s trick.
Chapter 9
STORIES IN THE DARK
The drop-dead date was November 18, 1997. If the clearances didn’t come through by then, the expedition was off. The day came and went, but I hardly noticed, because when I accepted the invitation to go, I didn’t think it was really going to happen. What were the odds that Fidel Castro was going to allow an American oceanographic research vessel with a high-tech submersible into Cuban waters? This was, after all, the same Communist dictator whom the United States targeted for assassination no fewer than 638 times.*1 There were also attempts to destabilize his regime with an invasion, a counter-revolution, and an economic blockade that had effectively prevented American dollars and American tourists from entering the country since shortly after the 1959 revolution that brought him to power. The whole concept seemed preposterous. Nonetheless, if permission was granted, it would be an opportunity to explore previously inaccessible waters of the deep Caribbean. It would also be a free ride, because Discovery Channel was going to pick up the tab, so I said, “Sure.”
