Summer World: A Season of Bounty - Bernd Heinrich (2009)
Chapter 22. Ending Summer
CHEMICALS CAN BE POWERFUL. ONE—THE CHLOROPHYLL molecule—causes the greening in spring that is the basis of the summer world. Without chlorophyll, life as we know it would not exist on Earth. Another chemical, which trees also produce, arguably causes the end of summer, because after it has done its job the caterpillars are gone and most of the birds must leave. This molecule, abscisic acid, releases the leaves’ hold on twigs and causes defoliation at summer’s end.
Just as important, of course, are the cues that cause plants to produce these key chemicals. Warming in the spring brings trees to life; but lower temperatures alone do not cause a tree to shut down and lose its leaves at the end of summer. The relatively precise timing of the leaf fall is of some importance, and it has been “calculated” by evolution through a balance of costs and benefits. Photoperiod, specifically the length of nights, is the main stimulus.
When nights become long enough, trees begin to shut down for the summer by forming a corky layer of cells between leaf and twig. This layer, the abscission layer, then blocks off the transport of materials between the branch and the tree. Chlorophyll is then no longer replaced as it breaks down with use; and as it disintegrates, the yellow and orange leaf pigments are revealed. The abscisic acid then does its job of dissolving the corky cell layer that holds the leaves to the trees, and as the connection between leaf and twig weakens, a breeze does the rest, and the leaf falls.
The appearance and disappearance of leaves may be the most conspicuous marker of the seasons and the most important events to the lives of a host of insects and birds; but to the plant, leaves are only means to an end. They provide the energy and raw materials for producing flowers, fruit, and seeds. The timing of the bloom and fruiting is critical to many animals as well. The summer schedule for the tree’s leafing is more constrained than that of the bloom, which may appear to be totally random, since it starts long before the leaves come out in some species, occurs in midsummer in others, and extends until late fall in at least one species, witch hazel. But it’s not random at all. All the deciduous trees (those that shed their leaves in the fall) that are wind-pollinated flower before the leaves come on, probably because leaves would hinder access of airborne pollen to the pistils. Wind pollination, as such, does not require early blossoming, because all the wind-pollinated conifers flower not in early spring but in the summer. Bee-pollinated flowers, such as those of black locust and basswood, flower late in the summer, when insect pollinator populations have built up. Witch hazel, which flowers in September, is pollinated by winter moths that are beginning to be active only then. Animal-pollinated trees bloom when pollinators are available, so in theory they could be pollinated all summer long, except that even in an undisturbed habitat there is competition for pollinators. Fewer pollinators are available to any one tree species if another one that blooms simultaneously draws some away to its flowers. However, divergence of species’ blooming times—so that these times space themselves out over the entire summer—is one of several solutions that reduce competition.
The timing of blooming is also tactical in part because it secondarily affects the timing of fruiting. Different species of bamboo, for example, flower and produce large seed crops not once per year, but at intervals of 60 to 100 years or more. Furthermore, when they do flower, they do so synchronously over vast areas. The naturalist George B. Schaller noted that in 1974 and 1976 umbrella bamboo—a staple of pandas—died throughout an area of 2,000 square miles in the pandas’ northern range. At least 140 of the rare pandas died. Undoubtedly, vast numbers of rodents—seed predators of the bamboo—died as well. If the bamboo were to flower and produce seed every year, the rodent populations would be permanently high and perhaps harvest all the seed produced each year. Similarly, some tree species in the woods from Maine to Vermont also time their blooming by not blooming, and thereby control the seed predator populations. In the summer of 2007, for example, the sugar maples, American ash, red oak, beech, white pine, and red spruce all failed to flower, and as a consequence there were almost no sugar maple seeds, acorns, or beechnuts—a collective absence of the mast that feeds a large variety of animals. White oaks, though rare, were apparently not affected. A friend told of finding one white oak tree near Wiscasset, Maine, that was “loaded” with acorns, and he saw there three raccoons and one porcupine at once. Bears, having no mast to fatten up on, depended heavily on apples, and a friend from Montpelier, Vermont, saw five of them at once in an apple orchard. Red-breasted nuthatches, who rely on conifer seed, were absent from my woods in Maine. Chipmunks, deer mice, and red squirrels are major predators of birds, eating birds’ eggs and young in the nest. Owing to the ripple effect, I expect a surge of forest bird populations in a year or two. In the meantime, during the next flowering cycle of the trees, the seeds and seedlings will also have a much higher survival rate.
Fig. 38. Witch hazel flowering in October.
The timing of the shedding of leaves is probably of even greater tactical significance to trees than the timing of the bloom. Indeed, we almost define the season by the status of the leaves, which are unfurled and then again shed more or less synchronously (relative to blooming times). The process is accomplished so flawlessly and regularly that it is easy to take the reason for granted. We scarcely ask why, much less how, whether or not, and when.
The complex process of leaf abscission has evolved in trees of very diverse, unrelated families. However, many members of these same tree families don’t shed their leaves at the end of the summer, raising the question why the others do. Larch is one apparent anomaly among the conifers. Its leaves turn golden in the fall and are all shed before winter, having served the tree about five months. The white pine sheds its leaves only after two years, so half its leaves are shed each year. Spruce and balsam fir may keep their leaves for five or six years. Most northern broad-leafed trees shed all their leaves every fall, though some of the more southern trees, like magnolia and some oaks, may keep them not just for an entire year but for five or six years. Since leaf shedding evolved numerous times, it must have offered a powerful selective advantage. But what is that advantage?
The advantage of not shedding undamaged leaves, all other things being equal, seems obvious. Leaves are solar panels, and discarding them every few months means having to make new ones later, using time and resources that would otherwise be available for growth. Resources invested in disposable leaves would be valuable for more growth and thus for survival in the fight for light that most forest trees wage against each other throughout their lives. These resources would also be valuable in obtaining a surplus of energy for fruit and seed production. All else being equal, it should be more economical to retain leaves for a whole year, or preferably for several years, than to discard leaves used only for four months and construct new ones every summer. Retaining leaves can serve the added advantage that they are then available for use during the occasional warm spells that almost invariably occur every winter. And as might be predicted from this rationale, many trees (as already mentioned) do indeed keep individual leaves for several years before finally replacing them.
One hypothesis regarding why trees shed leaves before winter is that the leaves would be or are killed by freezing and then are shed incidentally. But this hypothesis does not satisfy the ultimate, evolutionary, question. Frost intolerance of those leaves that are normally shed may be a proximal result of not experiencing freezing and therefore not having had a need to evolve frost-hardiness. By contrast, buds (which contain embryonic stems, leaves, and flowers) are frost-tolerant, even on trees that have frost-sensitive leaves.
Frost-hardiness has evolved in the leaves of many trees. Spruce and fir leaves, for example, withstand temperatures as low as nearly minus 80°F, and they are retained even at the northern limits of tree growth. Broad-leafed trees that grow in north temperate areas where there are commonly winter frosts and that nevertheless keep their leaves alive all winter include some species of each of the following: oaks, hollies, magnolias, rhododendrons, and viburnums. Of course, in the moist lowland tropics, most broad-leafed trees hold their leaves for many years, although in areas subjected to regular drought they shed the leaves, presumably to reduce water loss.
There must be a good reason why many northern trees shed their leaves whereas others keep them. My hypothesis regarding which trees do shed and which don’t depends on a conflict of selective pressures that trees must face in the northern hemisphere in areas where there is a lot of precipitation: a large leaf surface area is needed to intercept solar radiation and to absorb carbon dioxide in the summer; but the same leaf surface is a liability in the winter because snow loading could collapse the tree.
What we observe now is a result of evolution over hundreds of millions of years. But the selective pressures that have acted on some features in the past are now unlikely to occur every year and may be seen only rarely. Instead, they are probably witnessed only at bottlenecks. One such event occurred in New England on 26 October 2005, near our home in Vermont. The following journal entry for that date describes what happened:
It rained all day yesterday, and temperatures were dropping gradually: to 40, 39, and 35°F by evening. The sky stayed dark. Flocks of geese passed over. I woke up in the dark, and the light switch did not respond. I then looked out—SNOW! I went back to bed and waited for daylight before brewing a cup of coffee and stepping outside for a closer look. It was still snowing, and the outside thermometer then read 29°F. I saw devastation—the result of a confluence of rather precise temperature changes, wind directions, clouds, and all this weather in relation to the timing of the leaf shedding of the trees. A perfect timing, complete with proper experimental controls, had produced a rare natural experiment.
At that time, near the end of October, many trees—red oak, quaking aspen, apple, black locust, and silver maple—still retained their full complement of green leaves. Other deciduous trees, including white ash, elm, and red maple, had lost all theirs. Some of the sugar maples, black cherry, and white birches were bare, but a few still had branches that retained most of their leaves, by now golden.
The effect of the snow on individual trees was dramatic but unrelated to the species as such. Trees that retained their leaves paid a steep price. Those that had shed their leaves suffered no damage. The thin, young maples and oaks in the woods around our house were snapped in half or bent to the ground. Similarly, old sugar maples with heavy trunks had huge limbs broken off, and many of their other limbs were bent and ready to snap. The black cherry next to the house had retained its leaves; and while I was getting wood out of the shed for our stove, three of its huge limbs cracked and fell. One after another, they came crashing to the ground. From the nearby woods, I heard what sounded like muffled rifle shots followed by dull thumps: tall poplars were falling. The red oaks that had suffered the least damage during the great ice storm of 8 January 1998 were now hit the worst. Healthy oak trunks a foot or more in diameter had bent and shattered. Limbs two or more feet thick lay heaped on the ground. In sharp contrast, no trees or limbs that had shed their leaves (these trees included some maples, cherries, poplars, and oaks) were damaged. As I later learned, the same scene was enacted over a large part of northern New England, especially at the higher elevations.
Trees face the same problem of timing at the beginning of the summer, as was shown at the same location on 30 May 1996. As is typical by the end of May, all the trees had just fully leafed out. That night, it started to rain, and it got colder at the same time. By nightfall, temperatures dipped slightly below the freezing point, and the rain turned to snow. As more snow fell, it stuck to the already wet leaves and froze on. Throughout the night, temperatures continued to hover around the freezing point, so that the snow did not melt but was wet enough to stick. By morning, critical snow loads had accumulated, and I heard loud crashing throughout our woods as huge limbs snapped and came thundering down. All the large-leafed (deciduous) trees were damaged, but no trees and branches that had no leaves, and none with needles (small, nondeciduous leaves) were affected. Half a foot of snow on the ground at this time certainly did not seem usual, but it may not have been unknown to the 200-year-old trees. It would have been common in the long evolutionary history that shaped them.
These natural “experiments” demonstrate what may seem obvious: trees need solid scaffolding to hold their leaves up to the light. The costs and risks that are involved are a necessity resulting from competition. Most mature forest trees have dropped millions of viable seeds and perhaps produced thousands of seedlings in their lifetime, but of course on average, in a stable population, only one seedling can grow into another tree to replace the parent. The seedlings derived from any one tree are in an intense race to put on growth, and only one of them may grow large enough to break through the canopy and capture enough solar energy to produce seeds as well. Given such competition, one might suppose that trees would continue growing to the very end of summer. Instead, stem growth is usually completed in June, near the midpoint of summer when the ends of the twigs become capped with buds and stop growing. The buds then stay dormant through the warm weather of late summer, through the fall, and through the winter. Generally, they become ready to unfurl their leaves and flowers only in the warmth of the next year. Why do the trees stop growing taller with at least three months of warm weather still to go, long before low temperatures can put a damper on further growth?
I do not have an adequate answer to this question. However, I speculate that backup support has something to do with it. I have noticed that vines, such as Virginia creeper, grape, and blackberry, continue to grow throughout the summer, long after trees stop putting on height. During intense competition with neighbors there is a race to get the leaves up, to get priority in grabbing the sunlight, and the leaves pop out and the twigs lengthen in a short sprint early in the summer. But the tree then has to route resources to thicken the trunk and limbs—the solid scaffolding to support the new leaves and twigs. I measured the girths of five different trees of different species throughout the season and indeed found that they did not increase in circumference until the leaves came on in June, and they stopped putting on girth by mid-July or August. (This conflicts with the idea of light and large and dark and narrow supposed summer versus winter ring growth. Is it summer versus fall?) Bushes such as honeysuckle put on as much length per season as trees such as oaks, but the first grows to be only ten feet tall whereas the other grows to 100 feet. The reason is that bushes put out shoots in all directions, and these shoots die off as fast as new ones are created; but trees grow in only one direction, and one year’s growth adds to the next.
The geometry of trees is also an important aspect of leaf abscission. Deciduous trees spread their branches out and up in all directions to capture as much light as possible from above. However, long limbs, when snow-loaded, exert a huge torque that pulls them down until they may break or split the trunk. This configuration is great in the summer, for capturing lots of sunlight, but it compromises the ability to shed snow. In contrast, both spruces and firs have tough and generally short branches that bend down under a load, so that snow slides off. These trees are shaped like tents that partially collapse to the side but never split apart. The conical shape of these trees may also be an adaptation for capturing the sun’s rays in the north, where the sunshine is much more lateral than it is farther south. Could leaf behavior also be a suitable alternative to being shed?
Animals’ quick responses, though based on physiology, are called behavior. Some plants also have relatively fast responses that, though based on different mechanisms, are behavior as well. Many flowers track the sun so as to be continually warmed. A Venus flytrap leaf closes in seconds to capture an insect that lands on it. When touched, mimosa leaves droop and fold together in seconds, thus presenting less of a target for predators that might otherwise browse them. I was intrigued to learn that the leaves of rhododendrons in the mountains of northern China were curled into rolls during the winter (Schaller 2007). I could not believe my eyes when I saw the leaves of rhododendron of two species planted on our campus also rolling up. At temperatures below the freezing point of water (there are many days like that in Vermont!) the leaves drooped and rolled themselves into tight little tubes like sucking straws, and as soon as they were a couple of degrees warmer they again unrolled and raised themselves to the horizontal, looking as they do in spring and summer.
After being tightly rolled up (at minus 10°F), they could unroll and be almost totally flat and “normal” within about two to four minutes at room temperature (around 65°F). The reverse reaction occurred as well, but it was several minutes slower. I never did figure out what the mechanism underlying the curling is, but it has something to do with water, because when I cut twigs at room temperature and left their cut stems without access to water, the leaves slowly curled within about a day. When I then tried to rehydrate the curled leaves by wetting them and leaving them in either cold or warm water, they failed to respond in the winter, but did respond in the summer.
Ignoring for the time being the proximate question of the mechanism of how the leaf behaves, there is also the evolutionary question of why leaves roll up. Is there an adaptive advantage, and if so, what is it? Comparative data about the responses of other trees give clues.
One might suppose that the curling and drooping (rather than dropping) of leaves in the rhododendrons is a general response of leaves, as such, to temperature. To find out, I raided some of our collection of house plants, taking a leaf from ten broad-leafed species and laying them outside at 0°F. A few minutes later I brought them back inside. As I had expected, all were frozen brittle-solid. A few minutes after thawing they were limp mush. None had curled. So the rhododendrons that survive at minus 30°F have a different physiology and a behavior that shows that frost-hardiness is possible in broad leaves. I called out-of-state relatives and had them send me twigs of broad-leafed magnolia from North Carolina and leatherleaf viburnum (Viburnum rhytidophyllum) from Pennsylvania (though viburnum is native to China). These plants’ broad leaves, like those of the rhododendron, also survived the Vermont winter temperatures. In short, not only is it possible for broad leaves to stay alive in winter, but some broad leaves even behave in ways that greatly reduce their surface area at the temperatures where rain turns to snow.
Fig. 39. Leaves of rhododendrons drooping and curling in response to near-freezing temperatures.
The New England snowstorm of October 2005 had dumped a modest eight to twelve inches of snow in Vermont. We gauged its severity by the duration of the power outages, which in turn reflected the number of trees and branches that had fallen onto electric lines. (On our road, the power outage lasted three days. At other places throughout northern New England, it extended to more than a week.) Our costs were modest and temporary, but the lasting cost was to the trees caught with their leaves on. They paid either directly, in mortality, or in severe damage that would take decades to repair. Had the trees that shed their leaves later than others that summer made a large mistake by being off a few days in their timing, or on average is it a worse mistake to shed leaves too early?
Presumably, trees that are fully acclimatized to a generally stable climate shed their leaves at the optimum time, which is, by definition, when they get the best economic return over the long term. Their evolutionary calculation has balanced the appropriate amount of “insurance”—the cost of not gathering energy when the leaves are either shed early or delayed in being deployed, and the risk of the rare but severe injury. It seems that most of the time, many trees must shut down as though the summer has ended, long before it actually does end.