The Forest Unseen: A Year's Watch in Nature

by DavidGeorge Haskell

  Snails that detect a whiff of disease on their mates will refuse to express their female side, giving but not receiving sperm. Snails that find uninfected mates, however, will readily accept sperm from their partners. This selectivity may help snails pick out genetically superior sperm for their limited supply of eggs. Hermaphrodites are also sensitive to their larger social context. When they live in an area with few potential mates, they express both their male and female sides, but in a more crowded situation their femininity is dimmed and they act more like males, freely giving sperm but saving their eggs for only the best partners. The situation is yet more complex if mates have already bred and accepted sperm from another individual. One partner may then refuse another altogether, causing the rejected partner to attempt to mate forcibly, shoving sperm packets at the unwilling partner. Love triangles are fraught; love hexagons are war zones.

  War is no metaphor. In some species, snail mating tensions have ballooned into armed conflict: bony darts shoot from one mate to another, sperm-destroying glands neutralize unwanted maleness, and muscles jostle sperm and eggs into battle lines. Even the length of the snails’ embrace may be a result of sexual conflict. The snails palpate each other with their tentacles, circle, slowly edge into position, always ready to pull back or realign. What the snails are assessing at each stage is unknown, but their extended courtship and copulation is choreographed like cautious diplomacy, a prenuptial conference over the terms of the union. Such languor must surely be costly. The snails in the mandala have lain with their bodies mostly unshelled for over half an hour, easy prey for birds or other predators.

  Hermaphroditism is an unusual sexual system for animals, most of which divide male and female functions into separate bodies. Yet all land snails are hermaphrodites, as are some sea-dwelling mollusks and a scattering of other invertebrates. The sexuality of the snails in the mandala has more in common with springtime flowers than it does with the birds or the bees. All the mandala’s spring ephemerals and trees are hermaphrodites, and many of them combine male and female in a single flower. This diversity of sexual systems is puzzling. Why should wrens be boys and girls, but the trees that the wrens live in be boy-girls? The beetles that the wrens feed to their nestlings are either male or female, but the snails that arrive in the same beakful of food are all hermaphrodites.

  Evolutionary theorists have treated this puzzle as a problem in natural economics. Just as a business manager decides how best to allocate the company’s resources, biologists conceptualize natural selection as a process that decides how organisms will invest their reproductive energies. The human manager uses foresight and reason, but natural selection works by continually throwing out new ideas, then weeding out the ineffective in favor of the fecund. Nature has no shortage of new sexual ideas: every generation of snails has a few individuals that are unisexual, just as a small number of birds, insects, and mammals are born as hermaphrodites. There is therefore plenty of raw material to stimulate nature’s free market of sexual roles.

  Every individual has a limited supply of energy, time, and flesh to devote to breeding. Organisms can act like specialist companies and invest their resources in just one sex, or they can diversify and split the investment into two separate ventures, male and female. Which strategy is best depends on the particularities of each species’ ecology. In situations where individuals face a high probability of not finding mates, it pays to be a hermaphrodite. Tapeworms that live by themselves in a gut have to self-fertilize or their genetic lineage will end. Less obviously, flowers that use unreliable pollinators to achieve sexual union may also need to self-fertilize. Hepatica plants bloom in profusion all over the mandala, but if the springtime weather is too cold and pollinating insects cannot fly, being a hermaphrodite is the only way to reproduce. The same is true of weedy species that colonize disturbed ground. Individuals from these species may find themselves as the only immigrant in a new piece of habitat, so self-love is essential. Hermaphroditism is therefore the favored sexual system of species that may have to breed without mating.

  But many hermaphrodites, including most snails, do not live isolated lives and cannot self-fertilize even if they are put into solitary confinement. Loneliness is therefore not the only cause of hermaphroditism. Evolution has also favored hermaphroditism when a generalist approach to sexuality is most fruitful. Snails defend no breeding territories and they produce no songs or colorful displays. They also provide no parental care for the eggs, laying them in shallow pits in the leaf litter, then abandoning them. This relative simplicity of reproductive duties allows snails to be simultaneously male and female without compromising the efficacy of either sex. This is not possible for species like birds and mammals with more specialized sexual roles. In these cases, natural selection favors focusing on either maleness or femaleness. In economic terms, a snail gets a better return from a mixed investment strategy that combines male and female, whereas a bird gets a better return by channeling all its investment into one sex.

  The varied ecological and physiological context of each species in the mandala has produced, through years of natural selection, a wide variety of sexual arrangements. The snails’ hermaphroditic embrace, seemingly so alien to most humans, is a reminder that sexuality in nature is more malleable and diverse than we might at first suppose.

  July 2nd—Fungi

  Rain has gushed over the mandala for two days and two nights. The storm blew in from the Gulf of Mexico, and its incessant pounding has cleared the air of biting insects, bringing relief from the throngs of mosquitoes that have been my enthusiastic companions for weeks. The hottest days of summer have arrived on the heels of the storm. The air’s fevered humidity now has a relentless, all-encompassing quality; any bodily exertion brings a sheen of sweat. The forest is held in a clammy tropical embrace.

  Specks of orange, red, and yellow, the sexual buds of fungi, glow from the sodden forest floor. The heat and rain have emboldened the belowground parts of fungi, causing them to sprout their fruiting bodies. The prettiest of this morning’s colorful fungi is a cup fungus perched on a decaying twig. Tangerine orange, shaped like a goblet, and fringed with silver hairs, it is called a shaggy scarlet cup. Although it measures less than an inch across, its color catches my attention, drawing me onto my knees to examine it more closely. Once my eyes are closer to the ground, I see tiny fruiting bodies everywhere, a colorful regatta on a sea of decaying leaves and twigs.

  These bright boats all belong to the largest division of the fungal kingdom, the sac fungi, named for the sacs in which their spores are grown. The shaggy scarlet cup in the mandala started life as a spore, measuring just two-hundredths of a millimeter across, blown onto the dead twig on which it now lives. The spore germinated, then grew a slender filament into the twig’s wood. Because fungal filaments are so skinny, they can slip between plant cell walls and snake through the minute pores between the cells. Once inside the twig, the growing filament oozed digestive juices, liquefying the seemingly tough wood. The fungus filament absorbed sugars and other nutrients from this disassembled wood soup, building new filaments that slid farther into the twig’s dead tissues. To be locked in a wooden box below the ground is the shaggy scarlet cup’s delight.

  Some of the other participants in today’s regatta also specialize in deconstructing twigs, whereas others prefer mats of dead leaves. But despite differences in taste, all these fungi grow the same way, by creeping their tentacles through dead plant material, enlarging their networklike bodies by feeding on, and ultimately destroying, their wooden surroundings. When fungi feed, they push their homes deeper into the sea of oblivion. Dead twigs are therefore sinking islands of habitat, and fungi must continually send out progeny to seek new islands. It is this imperative that brings the fungi into our sensory world. Fungi remain hidden from our eyes until their belowground filaments sprout fruiting bodies. The flotilla of yellow, orange, and red is a reminder of the vast network of life below the mandala’s surface.

  The sha
ggy scarlet cup produces propagules on the inner surface of its cup. Here lie millions of cannon-shaped sacs, each pointed at the sky with eight minute spores loaded inside. When the cannons are ripe, their tips snap off and the spores are fired into the air, gunning several inches above the cup and escaping the calm boundary layer of air that hugs the mandala’s surface. Each spore is so small that it is invisible to the naked eye, but the simultaneous eruption of millions of spores looks like a puff of fine smoke. A cup’s eruption can be triggered by a gentle touch to just one part of the cup’s surface. This makes me suspect that animals might be important dispersers of fungal spores, despite the textbooks’ assertions about “wind dispersal.” This morning, the mandala’s surface has within its circumference at least eight millipedes and centipedes (one of which is nibbling an old shaggy cup), several spiders, a large beetle, a snail, several dozen ants, and a nematode. Squirrels, chipmunks, and birds hop around the mandala’s edges. Sac fungi fruiting bodies are so densely packed on the surface that it would be hard for animals not to step on them, even if they tried.

  A small brown mushroom in the center of the mandala showers spores from open gills, instead of shooting them up from the ground as do the sac fungi. Wind is again believed to be the primary carrier of these spores, but animals have left their mark here too. The mushroom’s cap is untidily scalloped with bite marks, perhaps from a chipmunk whose nose and whiskers are now brushing spores onto leaves many meters away.

  The reproductive life of sac fungi and mushrooms is without parallel in the living world. They stretch the meaning of “sex” beyond anything we animals have achieved even in our most innovative moments. They have no separate sexes, at least none that we would recognize, and they do not make sperm or eggs. Instead, fungi reproduce by merging their filaments, literally melding their bodies to make the new generation.

  The mushroom in the center of the mandala gives the clearest view into this strange life cycle. When mushroom spores germinate, they produce baby filaments that grow through the dead leaves, seeking mates. Filaments exist not as male or female but as different “mating types.” These mating types all look the same to us, but fungi use chemical signals to sense the differences and will reproduce only with a mating type that differs from their own. Some fungus species have just two mating types, but others have thousands.

  When two filaments meet, they begin an elaborate pas de deux, coordinating their dance with alternating chemical whispers. The opening sequence involves one filament’s sending out a chemical that is unique to its own mating type. If its partner is of the same type, the dance ends and the filaments ignore each other. But if the partner is of a different mating type, the chemical binds to the filament’s surface, causing it to respond by releasing its own chemical signal. Both filaments then sprout sticky outgrowths that grasp each other and draw the filaments together. The filament cells synchronize their cellular machinery and melt into each other to make a new individual.

  The new fungus is an amalgam of its parents, but the fusion is not quite complete. The genetic material of the parents remains separate within the fungal body, existing as two distinct sets of DNA inside the cells. The mushroom maintains this united-but-separate arrangement throughout its feeding life belowground and even in the fruiting body that rises up to release the spores. Only in the gills that hang below the mushroom’s cap does the full genetic fusion finally take place, after weeks or years of separation. But the union is brief. Immediately after the genetic material joins, it divides twice over to make spores that break loose and eject from their birthplace. Each spore will blow away in the wind or be carried by an animal to start the life cycle again.

  The shaggy scarlet cup and other sac fungi follow a similar pattern, but their filaments don’t join together until they are ready to make spores. The majority of their lives are spent belowground as unfused filaments. Only in adulthood do they seek another mating type with which to join, then grow a cup and produce spores.

  The complexity of fungal sexual identity highlights the curious nature of the sexes in other kingdoms of life. Without exception, reproduction in animals and plants involves sex cells that come in two distinct forms: large and well-provisioned cells—eggs—or small and mobile cells, sperm. But fungi show us that this duality is not the only possible arrangement. Fungal mating types can number in the thousands.

  The relative simplicity of fungus bodies may explain why they have not evolved specialized sperm and egg cells. The large, complex bodies of animals and plants take a long time to develop, and so they must start life with enough food supplies to complete their early development. But fungi have no elaborate bodies to build. Their simple filaments hatch fully formed from tiny spores. Producing an egg would be a waste of energy and time. The algae provide a good test case for this idea. They come in a wide variety of body forms: some are very simple, like fungi, whereas others have complex bodies, like plants or animals. As expected, simple algae have sex cells that are the same size, but complex algae have sex cells that have specialized into sperm and eggs.

  Fungi may eschew the sexual roles of the rest of the multicelled world, but they still experience sexual divisions, with reproduction being possible only between individuals of different mating types. This seems wasteful. From the perspective of a fungal filament looking for a mate, the existence of mating types would seem to be a major hindrance, removing from the pool of potential mates up to half the other individuals in the species.

  The puzzle of mating types has yet to be fully solved, but it appears that the politics of life within the cell may be at least part of the answer. Fungal cells are built on the same Russian Doll design as the cells of animals and plants. Fungi contain mitochondria that provide energy for the cell by burning food. In normal circumstances, the relationship between the mitochondria and their host cells is cooperative. But conflict waits just offstage.

  Because mitochondria are the descendants of ancient bacteria, they retain their own DNA and multiply within the cell just like free-living bacteria. This multiplication is normally adjusted so that each cell has just the right number of mitochondria. But if things go wrong, an overgrowth of mitochondria will damage the cell. One way in which such unhealthy proliferation can happen is if mitochondria from two different fungi meet within a single cell. Under these conditions, competition among the different strains of mitochondria would favor those that divide most vigorously. Thus, a shortsighted struggle among mitochondria can destroy the longer-term success of the whole cell.

  The mating types of fungi seem to be designed to prevent this kind of conflict. Mating types come with a set of rules specifying that only one mating type will provide mitochondria to the next generation. Therefore, mating types provide a way for fungal cells to quash potentially damaging conflicts between mitochondria.

  But theories about the origins and the evolution of mating types are uncertain and much debated. The fungi exhibit such a wide array of reproductive methods that most attempts at unifying explanations have foundered. For example, a few fungi produce structures that seem almost egglike, perhaps confounding the general rule that fungi don’t produce eggs and sperm. In other species, mitochondria from different parent filaments sometimes mix together, breaking the rules about mating types. This diversity can be overwhelming, as students of fungal biology soon learn. But it also serves as a refreshing counterpoint to the rather uniform adherence to the roles of male and female in animals and plants.

  From my prostrate position, I see hundreds of small cups and mushrooms spread across the surface of the mandala’s leaf litter. Every decaying twig has one or more clusters of colored cups. Tiny brown mushrooms crown most of the dead leaves. That so many species and individuals could suddenly appear from a forest floor that I have gazed at for months is a reminder of how much of the forest’s life is invisible to us, even with close observation. But unseen does not mean unimportant: these are the engines of decay, keeping nutrients and energy moving through the forest ecosyst
em. The lush summer productivity of this forest depends on the vitality of the underground fungal network.

  July 13th—Fireflies

  My body is tense as I pick through the misty air on my way to the mandala. I’m walking in the partial darkness of dusk. I place my feet carefully, straining my eyes through the gloom, searching for snakes in my path. Copperheads, Agkistrodon contortrix, the “hooked-tooth twister,” concern me most. These snakes are particularly active on muggy summer evenings. Tonight, the copperheads’ favorite summer snack is emerging. Hundreds of cicadas crawl up from their underground larval burrows. Snakes are surely on the prowl. I am loath to scorch my eyes with the reflected glare of a flashlight, so I move slowly, seeing the copperhead’s leafy camouflage everywhere in the failing light.

  My fear of predators was likely imprinted on my psyche by millions of years of natural selection. Tropical primates with poor night vision seldom live long if they have cocky attitudes toward the dark. Like all other living creatures, I am the descendant of survivors, so the fear in my head is the voice of my ancestors whispering their accumulated wisdom. My conscious mind chimes in with zoological fearmongering: long-hinged fangs, painful blood-destroying venom, a pit near the eye that catches minute changes in temperature, a strike that lashes out in a tenth of a second. I reach the mandala, and its familiarity eases my tensions. Another whisper from the family tree: what is known is safe.

  A firefly’s flash greets me as I sit. The green light rises sharply several inches, then holds steady for a second or two. The evening has just enough daylight for me to see the beetle as well as its lantern. After the green glow dims, the animal hangs motionless for three seconds, then swoops down and across the mandala. The beetle then repeats the quick glowing ascent, lightless pause, and plunging departure.