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2004

Those Fall Outfits May Be Saving Trees
As trees across the northern United States turn gold and crimson, scientists are debating exactly what those colors are for.

The scientists do agree on one thing: the colors are for something. That represents a major shift in thinking. For decades, textbooks claimed that autumn colors were just a byproduct of dying leaves. "I had always assumed that autumn leaves were waste baskets," said Dr. David Wilkinson, an evolutionary ecologist at Liverpool John Moores University in England. "That's what I was told as a student."

During spring and summer, leaves get their green cast from chlorophyll, the pigment that plays a major role in capturing sunlight. But the leaves also contain other pigments whose colors are masked during the growing season. In autumn, trees break down their chlorophyll and draw some of the components back into their tissues. Conventional wisdom regards autumn colors as the product of the remaining pigments, which were finally unmasked. In other words, autumn leaves were a tree's gray hair.

But in recent years, scientists have recognized that autumn colors probably play an important role in the life of many trees. Yellow leaves get their color from a class of pigments called carotenoids. Another group of molecules, anthocyanins, produce oranges and reds. Trees need energy to make carotenoids and anthocyanins, but they cannot reclaim that energy because the pigments stay in a leaf when it dies. If the pigments did not help the tree survive, they would be a waste. What's more, leaves actually start producing a lot of new anthocyanin when autumn arrives.

"The reds are not unmasked-they are made in autumn," said Dr. David Lee, a botanist at Florida International University.

Evolutionary biologists and plant physiologists offer two different explanations for why natural selection has made autumn colors so widespread, despite their cost. Dr. William Hamilton, an evolutionary biologist at Oxford University, proposed that bright autumn leaves contain a message: they warn insects to leave them alone.

Dr. Hamilton's "leaf signal" hypothesis grew out of earlier work he had done on the extravagant plumage of birds. He proposed it served as an advertisement from males to females, indicating they had desirable genes. As females evolved a preference for those displays, males evolved more extravagant feathers as they competed for mates.

In the case of trees, Dr. Hamilton proposed that the visual message was sent to insects. In the fall, aphids and other insects choose trees where they will lay their eggs. When the eggs hatch the next spring, the larvae feed on the tree, often with devastating results. A tree can ward off these pests with poisons.

Dr. Hamilton speculated that trees with strong defenses might be able to protect themselves even further by letting egg-laying insects know what was in store for their eggs. By producing brilliant autumn colors, the trees advertised their lethality. As insects evolved to avoid the brightest leaves, natural selection favored trees that could become even brighter.

"It was a beautiful idea," said Marco Archetti, a former student of Dr. Hamilton who is now at the University of Fribourg in Switzerland. Dr. Hamilton had Mr. Archetti turn the hypothesis into a mathematical model. The model showed that warning signals could indeed drive the evolution of bright leaves - at least in theory.

Another student, Sam Brown, tested the leaf-signal hypothesis against real data about trees and insects. "It was a first stab to see what was out there," said Dr. Brown, now an evolutionary biologist the University of Texas. He studied 262 tree species, noting the leaf color and number of aphid species specialized on them. Dr. Brown found that trees with bright autumn leaves tended to be the victim of more specialist aphids. The correlation supported the leaf-signal hypothesis. Dr. Hamilton did not argue that the evolution of leaf signals would make all trees brilliantly colored. Instead, he said, only species that were under heavy attack experienced this evolutionary pressure.

Dr. Hamilton died in 2000 at 63 as a result of complications from malaria he contracted while doing research in Africa. Only after his death did Dr. Archetti and Dr. Brown publish their collaborations with their mentor. The leaf-signal hypothesis was so provocative that other biologists began to test it. Dr. Snorre Hagen of the University of Oslo and colleagues studied a dozen mountain birch trees over three years, observing factors like brightness of leaves each fall and the level of insect damage the next spring. They found that birches with strong colors in the fall tended to suffer less damage from insects the next spring.

Dr. Archetti is also testing the leaf-signal hypothesis. Working with Dr. Simon Leather, an entomologist at Imperial College London, he has observed aphids laying eggs on bird cherry trees in the fall. As he reported in May in The Proceedings of the Royal Society of London, aphids prefer leaves that are still green, rather than yellow or red leaves. "This is the first basic prediction of the hypothesis, that aphids are more abundant on dull leaves," Dr. Archetti said.

While evidence from such studies is preliminary, Dr. Hamilton's students are encouraged. "It is supportive, but far from being robustly conclusive," Dr. Brown said.

The leaf-signal hypothesis has also drawn criticism, most recently from Dr. Wilkinson and Dr. H. Martin Schaefer, an evolutionary biologist at the University of Freiburg in Germany. In a paper to be published in Trends in Ecology & Evolution, Dr. Schaefer and Dr. Wilkinson argue that autumn colors are not sending messages to insects. It's wrong, but compelling, Dr. Wilkinson said.

Dr. Wilkinson and other critics point to a number of details about aphids and trees that do not fit Dr. Hamilton's hypothesis. Dr. William Hoch, a plant physiologist at the University of Wisconsin, argues that bright leaves appear on trees that have no insects to warn off. "If you are up here in the north in Wisconsin, by the time the leaves change, all the insects that feed on foliage are gone," Dr. Hoch said.

In their article, Dr. Schaefer and Dr. Wilkinson argue that a much more plausible explanation for fall colors can be found in the research of Dr. Hoch and other plant physiologists. Their recent work suggests that fall colors serve mainly as a sunscreen.

The interior of an autumn leaf is a frenzy of activity. Much of the chlorophyll and other equipment necessary for photosynthesis is being carefully dismantled, while the nutrients it contains, like nitrogen and phosphorus, are shipped into the tissue of the tree. The tree will need those nutrients to grow and reproduce in the spring.

The leaves need energy to send these reserves into the tree, which they can only get through photosynthesis. But because they have dismantled much of their light-harnessing equipment, it no longer works efficiently. Autumn leaves cannot capture all the sunlight striking them, and the leftover energy can build up in the leaf and cause damage to its tissue. "Sunlight in October isn't near as intense as in July," Dr. Hoch said, "but it can do more harm to a leaf."

Anthocyanins, the pigments that produce red and orange colors, appear to protect autumn leaves by blocking some of the sunlight. Dr. Hoch and his colleagues have found the most compelling evidence for this role. They raised normal trees along with mutants that could not produce anthocyanins. While the mutants thrived in a greenhouse, they could not ship nutrients out of their leaves in autumn sunlight.

Many plant physiologists see the protection provided by pigments as so important that there is not much left over for Dr. Hamilton's leaf-signal hypothesis to explain. "You may have a few instances where insects have some sort of relationship to color changes," Dr. Hoch said, "but it's almost certainly not a broad-based explanation. It doesn't hold any water."

Dr. Wilkinson speculates that some of the recent evidence in favor of Dr. Hamilton's signal hypothesis actually supports the sunscreen hypothesis. The link Dr. Hagen found between bright fall leaves and a lack of damage in spring may not be a result of trees' warning insects. Instead, the bright leaves might belong to trees that were doing a good job of protecting their leaves as they prepared for winter.

These arguments have not swayed Dr. Hamilton's former students, who argue that the leaf-signal hypothesis is still worth investigating. Dr. Brown believes that leaves might be able to protect leaves both from sunlight and from insects. Dr. Brown and Dr. Archetti also argue that supporters of the sunscreen hypothesis have yet to explain why some trees have bright colors and some do not. "This is a basic question in evolution that they seem to ignore," Dr. Archetti said. "You go to a forest, you see one tree is red and another is green. Why? They cannot explain this point."

"I don't think it's a huge concern," Dr. Hoch replied. "There's natural variation for every characteristic."

Still, the plant physiologists have more work to do. Some trees, like birch, produce no anthocyanins. Their yellow leaves are produced by carotenoids. During the growing season, carotenoids help chlorophyll absorb sunlight, but in the fall they do not shield the leaves. Dr. Hoch suspects that trees with yellow leaves must have some other way to protect their leaves in autumn, which he is now trying to find. Meanwhile, Dr. Archetti and Dr. Brown hope they can stimulate more experiments to test the leaf-signal hypothesis. "There are a series of steps you'd want to investigate on the tree side and the insect side," Dr. Brown said. Dr. Hamilton's students and their critics agree that the debate has been useful, because it has given them a deeper reverence for this time of year.

"People sometimes say that science makes the world less interesting and awesome by just explaining things away," Dr. Wilkinson said. "But with autumn leaves, the more you know about them, the more amazed you are."


Copyright 2004 The New York Times



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