by Greg Marley
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.
17
WHO’S EATING THE TRUFFLES?
There are two types of people who eat truffles:
those who think truffles are good because they are dear and
those who know they are dear because they are good.
J. L. VAUDOYER
I lived in Maine for seven years before I saw my first flying squirrels, although when I saw them, they were sleeping, not flying. At the time, I was working as a caretaker and handyman on a beautiful piece of property on the shores of Lake Megunticook. It was deep winter, the middle of February 1986, and there were several feet of virgin snow blanketing the woods around the lake. The homeowner and I were in the vintage kitchen, winterized to allow for islands of comfort in an otherwise cold and drafty old summerhouse. One flue of the massive stone chimney had been relegated to a Rube Goldberg kitchen exhaust system with an old fan mounted in the 8-inch flue opening covered by a copper cap that was removed whenever there was a need for venting. The owner had heard scrabbling noises in the flue in recent days and as we removed the cover to check it out, we exposed a veritable pig pile of flying squirrels packed together in a tight furry ball, all fast asleep. There must have been at least twenty, though they were impossible to count in the jumbled mass. The wire mesh cover of the chimney had obviously come loose over time, and the adaptable rodents took advantage of this great “natural” cavity (one that came with a small level of residual heat included) and moved in for the winter. We decided to leave them in place for the remainder of the cold months and quietly replaced the cover. In April, the flue base was empty and we were able to screen off the top without affecting the survival of these shy and cute little nocturnal squirrels.
Ecology of the Northern Flying Squirrel
The northern flying squirrel, Glaucomys sabrinus, is a common, though rarely seen resident of the treetops and cavities of mature spruce fir and hemlock forests across much of the northern half of the United States and throughout the forested regions of Canada. In addition, several subspecies can be found in mountain forests in “islands of refugia” left at higher altitudes in the southern Appalachians following the last great ice age. In New England, they frequent mixed conifer and conifer-hardwood forests, preferring spruce fir forests above all others. The main reason we rarely see them is that they are nocturnal. They sleep through the day and are most active for the two hours after sunset and the 90 minutes before dawn. In between, they hole up in nesting cavities in tree hollows, constructed branch and leaf nests, and the occasional chimney flue.
The northern flying squirrel’s preferred nesting site is an abandoned tree cavity created by a woodpecker. As is suggested by our chimney flue “crash pad,” flying squirrels are social and share their cavity nests with their kin throughout the year except when females are birthing and raising new kits. Most adults travel between several nesting cavities following food supplies, and males especially will cover a wide territory in search of adequate food. The two most logical reasons for communal living seem to be the limited number of nesting cavities and, more likely, the need to share body heat in order to conserve energy through the long winter when food is scarce.
Fifty years ago, zoologists thought the diet of the northern flying squirrel consisted primarily of plants, including nuts and the seed conifers as well as other vegetation and the occasional insects, bird eggs, or fledglings. In his Revision of the American Flying Squirrels, Arthur Howell tells of northern flying squirrels taken in the traps baited with meat and designed to take the larger carnivorous fur-bearing
animals with a frequency bordering on nuisance level.1 It seems these gentle seed-eaters actively seek out animal protein including eggs and small birds to supplement their diet. Over time, and through close analysis of the stomach contents and fecal pellets of squirrels, zoologists began adding fungi into the diet mix of the flying squirrels.
By using spore analysis to identify the fungi, researchers learned that the list of fungi in the squirrels’ diet included various species of hypogeous fungi (those fruiting below ground) in addition to a number of different epigeous (above ground) fungi including russulas, boletes, Lactarius, and other common woodland species. If you’ve ever come upon mushrooms tucked into the crooks of trees and wondered how they got there, your answer may lie with the manic collection efforts of these and other foraging squirrels. Several species of squirrels in addition to the flying squirrel cache mushrooms for future use, and the best way to prepare them for storage is to air dry the mushrooms in a tree. As scientists looked closer into the flying squirrels’ diet, they began to note that at certain times of the year and in certain regions of the United States— such as the coastal forests of western Washington and Oregon where mild climates and abundant rainfall make for a mushroom paradise—fungi and lichen showed up as a main component of their diet. Indeed, in those coastal rainforests of the Pacific Northwest, flying squirrels subsist almost entirely on a wide variety of truffles and other mushrooms and lichens to the exclusion of most other foods.2 But even in regions with more extreme seasonal weather patterns and normally high snow pack, the squirrels find and consume truffles and other fungi year round. In northeastern Alberta, the winter diets of flying squirrels showed significant consumption of epigeous fungi belonging to the Boletus, Russula, and Cortinarius genera and a smaller proportion of hypogeous fungi.3 In southern New Brunswick, Canada, fecal analysis revealed fungi as a component in the diet of flying squirrels and red squirrels, ranging from a 40 percent low in winter to nearly 100 percent in summer and fall. The fungi consumed by both species over the two-year period in New Brunswick were largely species of truffles.4 The Alberta study strongly suggests that flying squirrels dry and store mushrooms for winter use, while in the New Brunswick region, the two squirrel species also were reported to include wintertime foraging for mushrooms either buried beneath the snow or in the leaf duff.
In 1990, the northern spotted owl was listed as threatened under the Endangered Species Act.5 The federal listing has triggered intensive research to determine the causes for the population decline and to identify the actions needed to protect this small owl. The northern spotted owl lives in cavities of large-diameter trees found primarily in old growth forests where their primary prey is the northern flying squirrel. Their short stubby wings are ideal for maneuvering between tree trunks and branches within the confines of a mature forest. Suddenly the survival of the rare owl seemed dependent, not only on the preservation of old growth forest, but also on the fortunes of a shy nocturnal squirrel.
The interrelationship between mycorrhizal fungi, especially various truffle species, small mycophagous forest mammals such as the northern flying squirrel, and dominant tree species in the forest is complex and significant. The symbiotic fungi play a vital role in helping the trees to procure nutrient minerals and water and, in turn, the trees supply the fungi with carbohydrate food produced through photosynthesis. The fruiting bodies of the fungi represent a significant food source for the rodents, one that is available throughout much of the year, though with significant seasonal variation. The squirrels consume the spores from the fungi along with the rest of the mushroom and, in passing them through their digestive tracts, redistribute the fungi broadly through the forest environment. This triangular inter-reliance of trees, fungi, and squirrel is called a keystone complex due to the fundamental importance the complex dynamics represent to the health of the forest and forest species.6 To forest ecologists, herbivorous and omnivorous animals can be categorized based on their consumption of fungi. There are obligate mycophagists such as the flying squirrel (in coastal forests), the California red-backed vole, and a few other small forest rodents. There are preferential mycophagists such as the northern flying squirrel (in most other forests), a number of other squirrels, and other rodents. And there are a wide variety of occasional or opportunistic mycophagists, an extensive list that includes large mammals such as mountain goats, deer, elk and moose, bears, a variety of birds, and rodents including woodchucks, pika, and many others. Opportunistic mycophagists eat aboveground fungi in the late summer and fall when fruiting tends to peak, whereas preferential and obligate mycophagists eat more truffles in addition to other above-ground mushrooms. Since truffles are slow growing and more protected from drying out than fungi above the ground, they tend to have a longer fruiting season and therefore a more consistent availability. With this increased availability, they show up with more prominence in the diets of some small animals.7
Truffles: The Almost Unnoticed Pillar of Forest Health
There are many species of fungi that establish mycorrhizal relationships with trees, shrubs, and herbaceous plants in the forest and field. I present a number of the well-known species under sections on edible, poisonous, and otherwise interesting mushrooms in this book. But even among people whose eyes have been opened to mushrooms, most move through their lives unaware of the preponderance of truffles in our forests. We almost never see and appreciate the underground vegetative growth of the mycelial colony that gives rise to the colorful and showy epigeous mushrooms we bring home for our morning omelets, but in the case of the hypogeous truffles, they are even more “out of sight, out of mind” because both the mycelial network and the fruiting bodies are completely underground. Most people associate truffles with the wildly expensive gourmet fungi that we rarely might have—shaved thin enough to see through each slice—on a plate of expensive pasta or think of them as rich, tasty chocolates. But both definitions barely scratch the surface. The term “truffle” has been popularly applied to the underground fruiting bodies of members in the genus Tuber, home to some of the most prized edible species, but also home to many other inedible or less-delectable species. Other hypogeous fungi belonging to a number of other genera have been at times referred to as false truffles or “truffle-like fungi.” It is becoming more common to refer to all underground-fruiting fungi as truffles, a practice I follow in this chapter.
At first glance, it is easy to assume that all of the hypogeous fungi share a common ancestry. For the most part, truffles are irregularly spherical, potato-like fruiting bodies with a spore mass maturing inside a toughened rind-like skin. Ranging from the size of a pea to several inches in diameter, they often resemble puffballs fruiting underground. Truffles rely on animals to locate them and, by consuming the spore mass, to spread their spores beyond the close confines of their soil duff bed. Many have spores that are larger than their epigeous fungi cousins and have thickened cell walls capable of surviving passage through an animal’s digestive system. The tough spores also are able to survive long periods of exposure in the environment. Most share another trait: Truffles, though essentially odorless when young, develop strong distinctive odors when mature, which attract animals to their locations resulting in their being eaten at just the right time to facilitate spore dispersal. Though all truffles share a common set of characteristics, we now know that the truffle growth habit has evolved many times over and has originated from a number of very different mushroom ancestral lines. Tuber, genus to most of the prized edible truffles, is a member of the sac fungi, or ascomycetes, which include that other popular edible, the morels. More than 200 ascomycete truffles have been described in the world to date. In parts of the world where truffles haven’t yet been studied extensively, including much of the continental United States, there are a number of yet-to-be described species, as more are found each year. In the process of evolving into a completely underground fruiting body, the ascomycete truffles lose their ability to forcibly eject their spores into the air since it w
ould serve no useful purpose to blast their spores into an enclosed body buried in the soil. Truffles therefore need a flying squirrel or some other mammal or insect to dig up and consume the stinky delectable morsel and later redeposit the spores in a location favorable to future growth.
Members of the basidiomycetes also have evolved fungi that form underground fruiting bodies. These “false truffles” are generally less symmetrically globose and have a very different interior anatomy than do most of the ascomy-cete truffles. The basidiomycete truffles have arisen from a number of different families including boletes, puffballs, and gilled mushrooms, such as Russula, Cortinarius, and others. One significant difference between the ascomycete truffles and those evolved from basidiomycetes, beyond the anatomy, is their durability. Like most epigeous Basidiomycete mushrooms, these false truffles are generally short lived; they form and mature their spores within a few days and quickly rot.
True truffles can take months to mature after an initial small fruit forms, and it is not unusual for some species to start development in the late fall, over-winter as immature truffles, and ripen in the spring. The strong, distinctive smell does not begin to emerge until the spores are fully mature. In Europe, ripe edible truffles are located by their smell with the aid of dogs or the occasional pig and therefore are never harvested prior to maturity. In the United States, some people rake truffles out of the soil duff layer and collect them without an adequate determination of their maturity. Since the taste and smell of raked truffles is not as predictable, the value of American truffles rarely achieves the level of the best European ones. Though lacking the marketing hype and long history of use, North America’s edible truffles are gaining in stature in the eyes of the truffle world.