16
FUNGAL BIOLUMINESCENCE
Mushroom Nightlights

Some things which are neither fire nor forms of fire
seem to produce light by nature.
ARISTOTLE

Walking along a forest path at night is a magical pastime and an exercise in awareness. As your vision shrinks, your awareness of the sounds, smells, and tactile impressions grows. Any cone of light emanating from a flashlight is quickly absorbed by the black hole of darkness. For people who aren’t at home in nature, a mature, dense forest can seem intimidating even in the daylight with its limited vista, enveloping intimacy, and dense canopy. But at night it is altogether more intense. The crowded crush of the trees seems like its own universe and the slightest sound of a twig snapping underfoot is both magnified and insignificant. Scary childhood fairytales—with their ravenous wolves, huge hairy spiders intent on our doom, and strange wizened characters offering fruit that appears too good to be true—actually seem plausible. There is a reason that ghost stories are told around a campfire deep in the forest. We are descended from forest-dwelling ancestors, and back when we hunted in the forest, other creatures in the forest also hunted us. It was not a particularly safe place. At night we feel more strongly connected to those roots. They seem to be only one coyote howl away.

Twenty-five years ago, when I was teaching environmental ecology in a great program offered by the Tanglewood 4-H Camp and Learning Center in Lincolnville, Maine, we would liberate kids from the confines of the classroom and bring them into the living laboratory of the forest to offer hands-on education about our connections to nature. For middle schoolers, we offered an overnight program where, in the late evening following dinner, we led small groups on hikes into the night-shrouded forest. Entering a mature white pine forest at night with a group of thirteen-year-olds is like escorting them into the Cathedral of St. John the Divine. Knowing adolescents, at first I expected giggles, gibes, and horseplay, but the majesty of the dark forest always elicited a quiet reverence in groups of normally restless kids. When we had them turn off their flashlights and sit in the dark forest, the reverence deepened into a profound, though nervous, respect for their insignificance. And if we knowingly planned our nocturnal respite in an area with a stump covered by honey mushroom mycelia or colonized by the fruit of the luminescent Panellus or jack o’lantern mushrooms, the reverence turned to wonder. It always took a minute for to the kids to adjust their eyes to darkness, but then someone observant would whisper, “Hey, what’s that weird light there?” If it was honey mushroom mycelia, they were referring to streaks or patches of greenish glowing light across the surface of dead wood on damp ground. If we were lucky enough to be next to a patch of fruiting jack o’lantern or Panellus, then a pale greenish light would emanate from the gills of a dense cluster of caps.

Bioluminescence, foxfire, fairy sparks, torch wood—whatever you call it, it is a wondrous and sometimes frightening sight to come upon unexpectedly along a dark path in the forest. The word bioluminescence literally means “living light.” Close to fifty different species of fungi worldwide have demonstrated luminescence, including the three common and widespread North American mushrooms mentioned above. The number of identified luminescent species continues to grow as we explore the fungal diversity of the tropics. Recently five new species of luminescent Mycena were discovered in Brazil.¹ People always have been captivated by the phenomenon of living fungal tissue giving off light in the night. In some folk mythology, glowing wood was seen as a sign of fairy revelry, which is what gave bioluminescent fungi the name fairy sparks. And although I believed for years that the name foxfire came from the Appalachian mountains (it is, indeed, used in that region), the name originally comes from the French “faux fire” or false fire and is used to describe glowing fungal light.

There are many stories of people using luminous fungi, including accounts of soldiers in the Pacific Islands jungles in World War II who used clumps of glowing fungi for light when they wrote letters home.² These same soldiers would lace a bit of glowing mushroom onto the barrel of their rifles during night patrol or guard duty, to signal friendly status. In Europe, there are accounts of the use of clumps of torchwood to mark pathways through the forest. Perhaps Hansel and Gretel did not use breadcrumbs to mark the path out of the forest from the witch’s house. If they used Foxfire in the night, they would still be as lost in the daylight as they were if the birds ate up their trailing crumbs.

Foxfire also has earned a footnote in the annals of marine history. The first submersible boat designed to attack another ship was built in 1775 by the colonial American patriot David Bushnell and was used during the Revolutionary War. Though unsuccessful in its attempt to attach an underwater mine to sink the British naval vessel HMS Eagle, the small submersible boat marked a milestone in naval warfare.³ In early trials, Bushnell realized that use of a candle for light in the enclosed boat would quickly deplete the oxygen and shorten the boat’s underwater time limits. He turned to another great inventor of the period, Benjamin Franklin, for ideas. Franklin suggested use of foxfire, which was used to give out enough light to view the compass and depth gauge.⁴

Although no amount of knowledge can take away from the magic of sitting next to a pale, glowing bit of wood in a dark forest on a quiet fall night, scientists have made great strides in their understanding of bioluminesence—a mystery found not only deep in the dark forest in fungi, but deep in the dark ocean among other organisms as well. A mile or more deep in the ocean, where no surface light penetrates and perpetual darkness is the norm, anglerfish and dragonfish have evolved the use of luminous organs and appendages to attract unwary prey and potential mates. At depths in excess of 5,000 feet, many deep-sea inhabitants depend on dead or dying organisms, mostly microscopic in size, to filter down from the fertile surface for their food. While the deep ocean floor offers as much shelter and habitat as shallower waters do, locating a mate and, for larger carnivores, finding prey is not so simple. Among the range of remarkable adaptations to this dark sea life is the evolution of specialized light-emitting organs in a number of species of vertebrate fish and a range of invertebrates like shrimp and marine worms. Many have patterns of light-emitting organs along their heads and the sides of their bodies. Others, specialized predators with plus-sized mouths and an array of teeth sure to give young children nightmares, have developed glowing appendages that hang off their snouts in front of their gaping jaws. These inviting beacons lure the unwary to dinner. The adaptive advantage in easier access to food or to reproductive success in a completely dark world can explain the energy devoted to develop and maintain such specialized, light-emitting organs.⁵

Far from the ocean bottom, a similar wonder takes place across dark summer fields in New England. Growing up in the Southwest, I never witnessed the marvel of fireflies winking across dark fields until I spent the summer of 1971 in upstate New York. North America has no species of luminescent beetles living west of Kansas. I call fireflies beetles because that is what they truly are: They are members of several families of predaceous beetles native to many parts of the world, but most common in tropical regions of Asia, Central, and South America. Though adult fireflies are not always luminescent, the larvae and the eggs are. In larvae, the presence of luminescence is thought to communicate to potential predators that their glowing target possesses certain chemical defenses making a meal of “glowflesh” an unpleasant experience. (I have found no explanation for the glowing eggs, but perhaps they too advertise their toxic nature.) The various patterns of light emitted by the adult males as they fly serves as a bright signal to potential mates and helps in differentiating both among species and among members of the same species. The females watch the male antics and signal who they like the most with single bursts of light, like flashing a dazzling smile across a crowded dance floor.

The chemical reaction that produces light in deep-sea creatures, fireflies, and luminescent fungi is essentially the same. It involves a reaction between a substance known generically as luciferin and a generic enzyme luciferase, which in the presence of energy-releasing ATP and oxygen breaks down, thereby releasing light. Unlike the more common light-emitting reactions in nature, such as fire, almost all of the energy used in the bioluminescent reaction is released as light with almost none wasted as heat and, as a result, is sometimes referred to as cold light. In comparison, the incandescent light bulb wastes about 90 percent of its energy as heat.

There are few written records of bioluminescence from the time of Aristotle and Pliny the Elder until the mid 1600s, in part because of deep suspicion and superstition related to any strange or unexplainable phenomena. The Italians historically believed that the dancing lights of fireflies were the souls of their departed loved ones and dreaded their coming. In the late 1600s, a more thoughtful and scientific approach swept across Europe. The famous philosopher, early chemical genius, and relentless observer Robert Boyle determined that air was needed in order for luminescent fungi to glow. Using an enclosed jar, he determined that when the air was pumped out, creating a vacuum, the fungal glow stopped, and restarted only when air was reintroduced into the jar. At the time, it wasn’t known that air is composed of a mix of gases; later studies determined that the chemical reaction is dependent on the oxygen in the air. Two hundred years after Boyle’s experiments, Raphael Dubois, a French marine scientist working with luminescent clams and a species of beetle, determined that there were two components in the clams responsible for the light emission when mixed. He named these luciferin, a heat-stable chemical fuel, and luciferase, a heat-labile catalyst that, when added to the fuel, jumpstarts the reaction. Over time it was shown that each different light-emitting organism made its own unique combination of luciferin and luciferase. The reactions require the presence of oxygen that is converted into carbon dioxide.⁶

What is the adaptive significance of a fungus glowing in the dark? There must be some significant advantage conferred to the individual in expending the energy required to create light in order to explain its presence in diverse taxonomic groups and different locations across the world. The unambiguous answers remain elusive and the questions continue to drive research into bioluminescent organisms, but I will present a few published observations along with a bit of educated conjecture. Bioluminescent fungi make sense if the presence of glowing tissue signals to a potential predator that eating this mushroom or beetle will prove deleterious to its health as is the case with fire flies. Certainly some species of mushrooms that glow are known to be non-edible or toxic, at least to humans. The jack o’lantern (Omphalotus olearius) contains a number of chemicals called sesquiterpines; some are responsible for the severe gastrointestinal distress in anyone foolish enough to think it is a chanterelle. In the wild, I rarely see evidence that insects or mammals eat this mushroom despite its bright color and tendency to grow in huge, very noticeable, clusters. The smaller and less noticeable luminescent Panellus, Panellus stipticus, is hot and acrid to the taste due to astringent compounds throughout its flesh. It also has a reputation as being poisonous to humans though it is unlikely anyone would take more than a small taste of this fiery mushroom. In both of these mushrooms, the adaptive advantage of advertising toxicity through the development of luminescence might prevent them from being eaten. If an animal gets ill after eating a luminescent Pannellus, chances are it will learn to avoid them.

It’s not unlike the monarch butterfly, which, with its distinct and bright coloration, advertises the presence of the toxic cardiac glycosides concentrated from the milkweed that make up almost all of its larval diet. Predatory birds avoid these butterflies, and other, non-toxic species of butterflies have adopted similar coloring to hide behind. Of course, at first it seems like a duplication of effort for something that is toxic or unpalatable to expend additional energy to make bright coloration. If a predator takes a bite, it tastes bad or triggers unpleasant symptoms, so why bother advertising unless the point is to warn the predator off before it attacks? In the case of mushrooms, a predator’s initial onslaught might consume or destroy a significant portion of the fruiting body or mycelium and therefore prevent the release of spores. This is certainly the case in fragile butterflies, where any damage is likely to put them out of commission.

A second adaptive advantage of mushroom luminescence might be to attract invertebrates for spore dispersal. Several glowing mushrooms emit light only from their gills, while in some tropical species only the spores are luminous. It has been shown that glowing mushrooms attract more insect activity than non-glowing individuals of the same species. For example, fungal gnats lay their eggs on mushrooms and produce larvae that then eat the mushrooms. This represents a potential trade-off if some of the animals that are attracted might eat the mushroom while others move its spores into the world. Further complicating the potential trade-offs, research has shown that glowing mushrooms also attract predaceous wasps that prey on the mushroom-eating fungus gnats.⁷ It is a complex set of relationships indeed.

The question of the adaptive advantage of the glowing mycelium of the honey mushroom remains a mystery. Honey mushrooms contain a heat-labile toxin that causes gastrointestinal problems in people who eat them raw or undercooked. If the same toxin, or one even worse, is found in the mycelium perhaps the glowing light serves as a warning to insect predators. Several scientists, however, have postulated an entirely different explanation. High concentrations of oxygen are toxic for most living organisms in spite of the fact that we would all die without smaller concentrations. In the breakdown of wood lignins by the mycelium, peroxides are created as a byproduct and oxygen concentrations build to high levels. Oxygen-consuming chemical reactions in fungi may act as a cell antioxidant with light as an inadvertent byproduct.⁸⁹ If this theory is proven true, subsequent usefulness in spore dispersal or to deter fungus-eating critters would be an additional and fortuitous use of the light.

Perhaps the serendipitous gift of light-emitting mushrooms is simply magic. What other phenomenon in nature is capable of eliciting such wonder and triggering the imagination to such flights of fantasy as the sudden appearance of light in the darkness of the forest? Just think what stories we would have concocted had the fairy ring mushrooms been found glowing with otherworldly green light defining their rings in the night.