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 would 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.

Undoubtedly, it was by observing pigs and other larger mammals unearth and eat the fine European truffles that rural people began to use pigs as guides to find and expose them. One problem with using pigs as truffle hunters is that the great ravenous rooters love to find truffles for their own dining pleasure, so truffle hunters have to be quick to ensure their prize ends up in the basket and not down the pig’s throat. In the past, it was not unusual to see truffle hunters with mangled or missing fingers, the legacy of wresting truffles from the jaws of a hungry mushroom-loving pig. Today, truffle hounds have largely replaced pigs. They tend to be better companions, can ride in the front seat of the truck, and, best of all, are happy to get a dog treat as a reward rather than consume the treasure they locate and unearth. Most important is that a dog’s olfactory ability rivals that of the snuffle pig.

It’s an understatement to say that edible truffles are highly prized. There is an intense passion and mystique reserved for the best Italian and French truffles that rivals the feeling for any other food. In 2007, a new record price was set at auction for an Italian white truffle from the Piedmont town of Alba. A group of Hong Kong enthusiasts, with very deep pockets, paid 210,000 US dollars for a truffle weighing 750 grams. That was about $127,000.00 per pound! Alba, Italy, and her famous truffles were again in the news in February 2009 when an unnamed businessman and his five guests sat down to a dinner at Cracco’s, one of the world’s top restaurants, and, without looking at the menu, ordered white truffles. When the waiter presented the businessman with a $5,058.00 bill, he balked and protested, claiming he wasn’t told the cost or the weight of the fungi, but finally agreed to pay half. At last report, the matter was headed for a court resolution.

Truffle Evolution

Truffles have evolved in many regions of the world from a diversity of ancestors over geologic time. Karen Hansen, a research associate with Harvard’s Farlow Herbarium of Botany, has done extensive molecular and genetic examinations of the Ascomycete truffles and estimates that the truffle lifestyle has evolved independently at least fifteen times within six different families in the order Pezizales alone.⁸ Many epigeous members of the cup fungi form deep urn-like cups at or just below the soil surface. Others have cups almost completely enclosed with only a small opening at the apex. It involves rather small and incremental steps to form fruit remaining underground and spore sacs that no longer forcibly eject their cargo into the air. Examples exist of species in all phases of the evolutionary progression from open cup to enclosed and then to more complex and convoluted structure. Some, like most members of the genus Tuber, are compact, spherical, and dense with a network of light colored veins running through the spore-bearing gleba. Others are more simple, folded cups, with hollow spaces between but no opening.

Several morphological steps must occur in order for a fungus to be considered evolved into truffledom:

• The spore-bearing tissue must become enclosed within a skin that will protect the spores while they mature. Many of the non-Ascomycete truffle-like species have evolved from genera that have a well-developed annulus or partial veil that at times persists into maturity, covering the gills.

• The spore-release mechanism loses the ability for explosive or forcible discharge.

• The mature fruiting body develops a distinctive and strong odor, signaling to animal mycophagists that dinner is ready. The animals become the mechanism to get the spores to the surface of the ground for release into the environment.

• This last point is somewhat conjectural on my part. We know that essentially all truffle-like fungi form mycorrhizal associations with woody plants. The nature of the symbiotic relationship generally ensures that the mycelial colony of the fungus is perennial, existing for a number of years associated with the same host tree. It could be that the perennial nature of the vegetative component of the fungi confers a stability that, early in the evolution toward hypogeous status, allows for greater latitude in fruiting failure while still ensuring survival of the individual over time. If, while developing sufficient scent to attract foraging animals, there are years in which no spores make it to the soil surface, the stability of the mycelium helps to ensure survival of the fungus. An organism with a less stable life-course would have less chance of survival. As I said—conjecture.

The evolutionary pathway to a hypogeous lifestyle must be effective since it’s happened repeatedly in numerous fungal groups on several continents. Australia, which may represent the nirvana of truffle evolution, has the highest number of hypogeous fungi when measured as a percentage of the overall fungal population. This is the case, even though it is acknowledged that Australian fungi—particularly the truffles—have not been well studied. The evolution toward a hypogeal habit is reported to occur more frequently in warmer and drier climates since fungi have a harder time protecting the fragile spore-making tissue from drying. The protection afforded by underground development is a major boost in likely success.⁹

Truffle Ecology: The Pivotal Role of Mycorrhizal Fungi

Truffles are most abundant in the first few inches of soil beneath trees and other woody plants. That organic layer of soil is the most biologically active; it is where dead leaves, needles, twigs, and other organic matter are broken down and recycled and the nutrients that are bound up in their tissue are released. It is estimated that a single teaspoon of healthy forest soil might contain as much as 100 meters of fungal mycelium and that with each step we take, our feet cover several miles of fungal strands busily invigorating the forest.

We know that the mutualistic fungi-plant associations we call mycorrhizal likely began shortly after plants and fungi emerged from the primordial seas and colonized the land. Though fossil records are somewhat scant due to the delicate nature of plant tissues, we have evidence that indicates club mosses formed primitive fungus-root structures as early as 400 million years ago. Today, essentially all gymnosperms and 80 percent of angiosperm plants form mycorrhizal associations with fungi. A number of plants can live independent of fungal associations and have evolved to be successful colonizers in new territory and a number of the most invasive weeds in the world fit into this group.¹⁰ But most plants are mycorrhizal-dependent, meaning that they readily accept at least one fungal mycobiont into their tissues and that their long-term survival is dependent on the formation of these symbiotic relationships. Often these plants can function without a fungal association for brief periods of time, especially in nutrient-rich soil, but they appear nutrient deprived, stunted, and sickly.

All of the known truffle-producing fungi form mycorrhizal associations with woody plants, mostly trees and shrubs. Mycorrhizal symbionts are essential components of a healthy forest and their perpetuation is necessary for the survival of the forest. Sometimes foresters learn the hard way what an essential role mycorrhizal fungi play in the survival of trees, as happened with an outplanting of Douglas fir seedlings in a nursery field in Oregon in the 1960s.¹¹ The field, which was converted from potato cultivation, was fumigated with a strong fungicide prior to planting the tree stock because of concern about lingering fungal diseases. Because the fumigation eliminated residual soil mycorrhizal fungi for the seedlings, the firs quickly became stunted and sickly and had a high mortality rate the first year and an elevated rate the second year despite the application of fertilizer and adequate irrigation. There were, however, islands of thriving seedlings where wind-borne or residual soil spores established mycorrhizal associations with the emerging seedlings. These islands of normal vigorous growth spread out as the fungal mycelium expanded.

All fungi are examples of “more than meets the eye,” but none more so than truffles and their cornerstone relationships with the trees and animals they nourish. A significant percent of the fungal symbionts of forest trees produce underground fruiting bodies. The perpetuation of these mushroom species is vital for the ongoing health of the forests, and their perpetuation depends on the vitality of the population of animals who locate, unearth, and consume these truffles. The next time you have the opportunity to take a nighttime forest stroll, listen for the sounds of the flying squirrels as you swat the odd mosquito. The squirrels have a characteristic behavior as they collect and store nuts or fungi. They place the food in a shallow cavity or into the V formed by two intersecting branches and then rear back and jam the food item into place by vigorously hammering with their forepaws. It makes a distinct “thwak thwak thwak” sound. Remind yourself that the health of the forest might depend on the success of this seldom-seen nocturnal squirrel and its relationship with the rarely seen forest truffles.