Title: LIFE ON A LEAF. By: Marchand, Peter J., Natural History, 00280712, May2000, Vol. 109, Issue 4 Database: MasterFILE Main Edition LIFE ON A LEAF Section: ECOSYSTEMS Even before they emerge from their buds, and long alter they become part of the forest floor, leaves play host to ever changing communities of minuscule fungi. In a rain-drenched tropical forest canopy, where plants grow upon plants, even a single leaf serves as the staging ground for a multitude of species interactions, and competition for limited space and resources is intense. But even in the canopies of the world's less crowded temperate forests, we find parallel situations. The fungal communities that grow on healthy new leaves are a shining example. From the time a tender new leaf pushes through its protective bud scales and enters the world of intricately tangled food webs, it is colonized by fungi that have been lying in wait. Three or four species of yeast (which are unicellular fungi) often take refuge within the buds and shoots of deciduous trees. As each new leaf unfolds to greet the spring, wind- and water-borne fungal spores also arrive on the scene. For the most part, these organisms pose no greater threat to the emerging leaf than does the Spanish moss festooning the branches of live oaks in the Deep South. Except for the occasional pathogenic species, these early colonists use the leaf primarily as a platform from which to scavenge organic debris. But they may also, in fact, be beneficial to the new leaves and therefore to the tree itself. One advantage of the plant's keeping company with fungi is that some of the colonists have insecticidal properties. A few fungi have been found to excrete strong chemicals capable of interfering with insect development and even of killing the larvae outright. As a result, far fewer leaf-chomping caterpillars can feed their way into adulthood. When, for instance, a minute amount of Fusarium avenaceum (a fungus commonly found on the blades of various grasses and in the needles of fir trees suffering a budworm attack) is ground up in the laboratory and mixed into the diet of budworm larvae, it kills 80 to 100 percent of the population. There is nothing altruistic about the fungus's services, of course; a fungus that seeps insecticide is merely investing in its own survival. In the process, however, it also saves the leaf from getting devoured, although in the complex food web of the forest canopy, the coevolution of grazer and grazed inevitably results in some herbivores developing resistance and some fungi winding up as insect food regardless. Several leaf fungi produce antibiotics that hinder the growth of other fungi. After all, when many species share the leaf surface, they are competing both for food and for precious space. Scientists intensively study these interfungal rivalries in laboratory cultures, because they may hold a key to controlling the fungal diseases that commonly afflict commercial wheat, rye, barley, and bean crops. (The nonselective fungicides currently used on some commercial crops also kill the beneficial epiphytes that may naturally inhibit the proliferation of their disease-causing cousins. In fact, the use of such chemicals may sometimes lead to an increase rather than a decrease in plant diseases.) Leaves may indeed benefit from the presence of their fungal colonists, but the fungi also have a good thing going. The deceptively clean-looking surface of a fresh leaf contains a bounty of organic particles--pollen, spores, and other windblown debris--as well as nutritious materials that leak from the leaf's epidermal cells. But in nature, plentiful sources of food energy seldom go uncontested for long. About 1.5 million fungal species exist on our planet. Many of them flourish in a broad range of habitats, and nearly all of them are adapted for wide dispersal. With billions of fungal spores in the air, the pioneer populations on the leaf are quickly infiltrated by newcomers. The most successful of the early invaders are certain kinds of Ascomycetes, a large class of fungi that includes truffles and morels as well as most molds and yeasts. Cladosporium herbarum, for example, is a species that grows in velvety green, branching chains and has a notorious tolerance of extremes (one strain of C. herbarum attacks meat in cold storage and can thrive at 20 Fahrenheit). These fungi are often quickly joined by other species, including those in the genera Penicillium and Fusarium (the latter is known for its parasitic strains that commonly attack vegetable crops). These "weedy" species are capable of fast growth under relatively impoverished conditions. By the time most tree leaves have matured, several thousand fungal spores per square inch, representing many different species, may be found on their surfaces. Life on the surface of a leaf is not easy, though, and for many of the later arrivals, the stay is short. Viewed at the microscopic level, the epidermis of the leaf appears no more hospitable than the rugged canyon country of the arid Southwest, to which it bears a remarkable structural resemblance. What appears to the eye as a smooth, flat leaf surface is instead a complex landscape of erosional features that have been worn into the leaf cuticle from the gradual physical and microbiological breakdown of its waxy coating. The tiny canyons and crevices of the leaf are laden with the organic resources needed to sustain fungal growth, yet relative to the topographic features of the leaf, the newly arrived spore sits naked and exposed, like a giant boulder on a desert landscape. Of all the spores that settle on the leaf's surface (many having gotten there by wind or a splash of rain), surprisingly few are able to survive for long under these conditions. Nutritional shortages-especially on the younger leaves, which leak fewer metabolites and have not yet accumulated substantial organic debris--often bring about competition and restricted growth. And although nutrients keep accumulating as spring rolls around to summer and as the leaf ages, equally challenging new circumstances are imposed on the leaf fungi. Midsummer weather, for instance, rapidly parches the surface of a leaf fluttering in the warm breeze, and with frequent thunderstorms come torrents of rain that easily wash spores out of the canopy. To mediate such extremes, the fungal colonists secrete sticky mucilaginous sheaths that help them hang on, but it's a tenuous existence nevertheless. Some populations die; others encase themselves in thick-walled "resting structures" and weather the drought while the new arrivals try to settle in. It takes a hardy pioneering type to succeed under these circumstances. By late summer, however, fungal spore production reaches its peak, the atmospheric fallout onto the canopy becomes increasingly heavy, and new recruits on the leaf surface begin to outnumber casualties. The same sticky secretion that holds one fungus to the leaf also enables the spores of others to become attached to it. With the onset of fall, conditions become somewhat easier for the fungi. Moisture abounds as dew settles on the foliage in the chilly autumn mornings, and the cooler days mean less evaporation. These factors, along with the continuing accumulation of pollen, set the stage for yet another community shift on the leaf's surface. Many of the early colonists have by now relinquished the site to competitors better suited for these new conditions. Succession is again under way. What began as a passive partnership between plant and fungi high in the forest canopy gradually shifts emphasis. While the leaf was young and healthy, many other fungal colonists--the true saprophytes (organisms living on dead or decaying matter)--remained quiescent. But with the onset of autumn and senescence, these decomposers emerge from dormancy and soon take over. High above the ground, the annual recycling of leaf material--the ultimate return of nutrients and organic matter to the soil--begins slowly but inexorably. In the end, it appears that the plant, through its remarkable lifelong partnership with fungi, has indeed married the undertaker. Adapted from Autumn: A Season of Change, by Peter J. Marchand. Copyright Copyright 2000 by University Press of New England. Reprinted with permission. The tiny canyons and cervices of seemingly smooth leaves are fertile ground for fungi. Inset, left: The spores of Aspergillus (a common mold magnified 5,600 times by scanning electron microscope. The surface of a fir needle, below, is laden with fungal hyphae and spores. Late in the life cycle of a leaf--or more commonly, after the leaf has fallen from the tree--Aspergillus right, fruits in treelike tufts (here magnified 305 times). Like Aspergillus, the fungus Penicillium grows best on wounded leaves or in moist leaf litter. Inset: Hyphae and fruiting bodies of Penicillium (magnified 205 times). ~~~~~~~~ By Peter J. Marchand Copyright of Natural History is the property of Natural History Magazine, Inc. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.