Nature's Fabric: Leaves in Science and Culture 9780226180625

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n at u r e ’s fa b r i c

nature’s fabric Leaves in Science and Culture David Lee

T H E U N I V E RS I T Y O F C H I C AG O P R E S S C H I C AG O A N D LO N D O N

The University of Chicago Press, Chicago 60637 The University of Chicago Press, Ltd., London © 2017 by The University of Chicago All rights reserved. No part of this book may be used or reproduced in any manner whatsoever without written permission, except in the case of brief quotations in critical articles and reviews. For more information, contact the University of Chicago Press, 1427 E. 60th St., Chicago, IL 60637. Published 2017 Printed in China 26 25 24 23 22 21 20 19 18 17

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ISBN-13: 978-0-226-18059-5 (cloth) ISBN-13: 978-0-226-18062-5 (e-book) DOI: 10.7208/chicago/9780226180625.001.0001 Library of Congress Cataloging-in-Publication Data Names: Lee, David Webster, 1942– author. Title: Nature’s fabric: leaves in science and culture / David W. Lee. Description: Chicago; London: The University of Chicago Press, 2017. | Includes bibliographical references and index. Identifiers: LCCN 2016056667 | ISBN 9780226180595 (cloth: alk. paper) | ISBN 9780226180625 (e-book) Subjects: LCSH: Leaves. Classification: LCC QK649 .L442 2017 | DDC 581.4/8—dc23 LC record available at https://lccn.loc.gov/2016056667 ♾ This paper meets the requirements of ANSI/NISO Z39.48-1992 (Permanence of Paper).

To Gurumayi Chidvilasananda, who has helped me see beyond the science of leaves and forests to realize a greater empathy with nature

c ontents Preface One Two Three Four Five Six Seven Eight Nine Ten Eleven Twelve Thirteen Fourteen Fifteen

ix Green Men 1 Leaf History 21 Green Machinery 43 Nature’s Fabric 66 Leaf Economics 90 Metamorphosis 107 Architecture 133 Shapes and Edges 158 Surfaces 179 Veins 200 Color 217 Food 234 Homes 251 Movements 269 Seeing Leaves 286

Acknowledgments 309 Appendix A: Leaf Terminology 313 Notes for Appendix A 331 Appendix B: Drying and Preserving Leaves for Craft Projects 334 Appendix C: Leaves for School Science Labs and Projects 340 Chapter Notes 347 Illustration Notes 426 Index 443

p re face The world does not need words. It articulates itself in sunlight, leaves, and shadows. The stones on the path are no less real for lying uncatalogued and uncounted. The fluent leaves speak only the dialect of pure being. The kiss is still fully itself though no words were spoken. dana gioia, “Words”

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eaves are present just about everywhere we live. Look at the cracks in a sidewalk, and small leaves peek out. Look at the verdant vegetation in an empty lot. Find exotic tropical foliage on the window ledge of an urban apartment. Leaves may be our most accessible means of encountering some aspect of the natural world. We surely take them for granted, and they mostly fade into the background of our consciousness. Collectively, leaves mark our planet as green. The colors mark the earth as the “emerald planet,” and leaves are the green fabric that clothes its surface. My scientific and cultural interests in leaves go back to childhood, and my first data collecting of leaves was the measurement of blueberry leaf size and shape at different elevations on a ridge in the Cascade Range, in 1964. Subsequently, leaves have figured in much of the scientific research and popular writing throughout my scientific career, even to a most recent paper published in 2013, four years after retiring from university teaching. My contributions to the science of leaves, featured in this

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book, are rather modest, but that interest has given me a perspective to appreciate the significance of the general research on leaves. My purpose in writing this book is to enhance our appreciation of leaves, and to help us form a stronger connection with nature— wherever we live. I have written stories about leaves to help us appreciate human history, the scientific method, evolution, geometry, biological function, the flux of elements on the planet, the codependence of living creatures, and the subtleties of our responses to the natural world. This book is intended for a nonscientist, teacher, student, landscape designer or architect, gardener, student of natural history, someone looking for ways to strengthen such connections, to add meaning to the elements of nature we mostly take for granted. Nature’s Fabric has two appendixes that concentrate on our connections to nature through its foliage. The first chapter details our long cultural and spiritual connections with the natural world through its foliage, using the green man and tropical foliage as guides. Chapter 15 speculates on our sensory responses to this green world, building a case for a long evolutionary relationship. This final chapter distinguishes among our two approaches in better understanding our connections to nature: one is the reductionist approach through the application of the scientific method in understanding the brain, and the other is the personal approaches we all take to understanding human consciousness and its connections to nature. The other thirteen chapters describe different facets of the science of leaves, all in the perspective of centuries of observation and speculation about their function. The appearance of leaves in evolutionary history and the evolutionary logic for their formation and function are described in the second chapter. In chapter 3, “Green Machinery,” the process of photosynthesis is described in detail, with a historical perspective. It is followed by a chapter on the roles of foliage in the global cycling of carbon dioxide, oxygen, water, and major elements (such as nitrogen), highlighting the importance of vegetation in global climate change. Fittingly, this chapter is titled “Nature’s Fabric.” The next six chapters (5–10) outline the science associated with the actual appearance of leaves, discernible from the most casual observations: their toughness and longevity; their symmetry; the architecture of their display on the plant; their edges (whether smooth, lobed, or with teeth); their surfaces (whether smooth or rough), and the new products they have inspired through biomimicry; the appearance and function of veins; and leaf colors. Chapters 11 through 14 concern the interactions of leaves with ani-

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mals in the natural and human-constructed worlds. In chapter 12, “Food,” the nutritious value of leaves is highlighted both as important for human welfare and as the principal source of nutrition for most animals. In the latter case, I highlight the kinds of defenses that plants have evolved in their leaves to reduce that consumption. In chapter 13, “Homes,” I examine leaves as habitats for all sorts of organisms. Some eat portions of the leaves, and others are recruited by plants to defend leaves against consumption by other animals. In chapter 14, “Movements,” the reader learns how leaves move, in a few cases quite rapidly (and fascinate us with this animal-like activity), focusing on carnivorous plants. In addition to the chapters, appendixes follow with information particularly useful to educators, particularly for elementary through high school teachers, and parents looking for means to involve their children in nature. The illustrated glossary of leaf terms keeps these esoteric words out of the main text and makes it less intimidating; it also provides a resource for comparing leaf form. In a second appendix, there are clear instructions on how to dry and preserve leaves. Teachers and children can collect and keep their favorite leaves, and collect the types of leaves described in the glossary. Such leaves can then be used in various craft projects. Instructions for clearing and skeletonizing leaves are provided. Along with instructions for staining leaves, these techniques enable us to heighten the beauty of leaf venation, and to compare the different patterns of venation. The third appendix provides resources, including simple techniques and inexpensive instrumentation, for using leaves in science investigations and projects. This includes simple techniques for sectioning leaves for observation in a microscope. All of these techniques involve the use of materials readily available from an art supply or hardware store. Although the chapters follow a logical progression of topics in the book, I suggest that you pick up the book and look at whatever chapter draws your attention. Links among chapters are provided by page numbers throughout the book. To further simplify the flow of the text, and yet provide a depth of scientific background that I think is absolutely necessary, the following measures have been adopted. Citations are not given in the text but can be located by the page intervals in the chapter notes, which include phrases indicating how the work was important and information provided by individuals or obtained from websites. Technical terms on leaf architecture are left out of the main text but are included in an appendix. Full lists of the scientific names of common plant names are added to these chapter

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notes. Thus, you will know when I mention rowan, I actually mean Sorbus aucuparia L. (Rosaceae). I also include a section that describes the figures in detail— that is, where the photograph was taken, the scale of the photo, and full information on the photographer, if not the author. Finally, I use past times as millions of years ago (mya) and leave out the geological names of past periods. In 2007 I published Nature’s Palette: The Science of Plant Color. Nature’s Fabric is similar in style, purpose, and intended audience, and is published by the same press. The two books provide a fairly comprehensive description of plants, their diversity, evolution, structure, development, reproduction, interactions with animals, and global importance. Both books were written with the intention of increasing our appreciation of nature. This appreciation adds to our quality of life— and may become more important as trends toward alienation from the environments in which we have evolved increase. The purpose of both books is consistent with the teaching of Baba Dioum, an environmentalist and agronomist from Senegal, who famously wrote: In the end, we will conserve only what we love, we will love only what we understand, and we will understand only what we are taught.

I hope this book helps you look behind the appearance of leaves, certainly to their beauty and elegance, and also their importance in our planet’s past, present, and future. Perhaps you will better remember your own emotional responses to leaves in a childhood or other more recent landscape, freshening your appreciation of nature and strengthening your commitments to preserve it.

Chapter One Green Men Green Man becomes grown man in flames of the oak As its crown forms his mask and its leafage his features; “I speak through the oak,” says the Green Man, “I speak through the oak,” says he. william anderson, “The Green Man”

These relationships would be no doubt sufficient to show how extended is the science which I am attempting to outline here; but the man who is sensitive to the beauty of nature will also find here the explanation for the influence exerted by nature on the peoples’ taste and imagination. He will delight in examining what is called the character of vegetation, and the various effects it causes in the soul of the observer. alexander von humboldt, Essay on the Geography of Plants

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e looked out beyond me, onto the landscape from a parapet in the Canterbury Quadrangle, at St. John’s College in Oxford, my first green man. I was ready for him. I had been fascinated with leaves, doing research on them for over thirty-five years, and was participating in a workshop at the university, in March 2008, on the subject of autumn leaf color (which I’ll discuss later), and the green man was near our meeting room. I knew a bit about green men, and I immediately recognized the shaggy visage with hair replaced by oak leaves (fig. 1.1). This was not an ancient sculpture. The quadrangle was constructed in 1635 by a wealthy benefactor, alumnus, and former ·1·

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Figure 1.1 Green men. Left, Canterbury Quadrangle, Oxford University; right, Cernunnos, Celtic god depicted on the Gundestrup cauldron, first century bce.

chancellor, William Laud. The green man, among other “grotesques,” was probably created by a stonemason, Anthony Gore. Later, in looking at my photographs of the quadrangle, I found more stylized green men in the larger friezes aside the openings to the quadrangle. Green men are shown with leaves as hair and also sprouted leaves and branches from their eyes, noses, and mouths. I didn’t consider that this green man would begin a book, let alone one about leaves, but I hope to leave you with the appreciation of the deep historical roots that make each of us a green man, whether we are aware of it or not. I didn’t see the numerous other green men in older colleges of the university and in churches of the city. J. R. R. Tolkien was a student at Oxford (but not at St. John’s) and later returned as a lecturer and professor of Old English. He and C. S. Lewis met weekly at the Eagle and Child Pub, just across the street from the college entrance and actually owned by St. John’s College, and this is where the autumn foliage participants socialized. Green men are found throughout Oxford, on pubs, churches, and college buildings. There is even a Green Man Route promoted by the local tourist board. Perhaps the green men and other figures helped the two authors to visualize characters for The Lord of the Rings and The Chronicles of Narnia, both of which I read to my children. Green men decorate European cathedrals from the Middle Ages and beyond, and they appear on civic buildings as well. The stonemasons who worked on the Canterbury Quadrangle belonged to a guild of craftsmen in

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London and likely learned about them during their apprenticeships. This European tradition made its way to the United States in the nineteenth century. There, stonemasons who were trained in Europe put green men on civic buildings and churches, as in Des Moines, Iowa. My cousin Carol Sue’s garden, near the Columbia River in Vancouver, Washington, is overseen by a green man purchased from a local ceramicist. Where do green men originate from, and what do they mean? Perhaps the earliest graphic representation of a green man decorated a temple at Hatra, in northern Iraq, constructed during the Seleucid Empire (of Greek origin) in the third century bce, probably destroyed by Islamic militants (ISIS) in 2015. Another decorates the Gundestrup Cauldron, a remarkable silver vessel excavated from a Danish peat bog and dating back to the first century bce. On the side of this beautifully and richly decorated piece are two images of the Celtic god Cernunnos; in one the beard and hair are leaf-like, and in the other a leafy branch sprouts from his antlers (fig. 1.1). The meanings of the cauldron are controversial, hinting in the yogic pose of Cernunnos of connections with the Vedic culture of early India. At the tenth-century tomb of Harald Bluetooth, the first Christian king of Denmark, a monolith is decorated with a figure entwined with plants. The commonness of green men on medieval cathedrals suggests some relationship to Christian worship, perhaps as a male counterpart to the diving feminine, entwined in the worship of the Virgin Mary. The green man motif has been around for a long time. Perhaps the first mention of a green man–like being is the monster Huwawa (or Humbaba) from the Sumerian poem The Epic of Gilgamesh, going back at least 5,000 years. Huwawa was the protector of the Cedar Forest that Gilgamesh came to cut down. Perhaps Huwawa reappeared in other forms, including in the Greek myths as Perseus and Medusa. Associated with this long history are green men in English mythology and history. Robin Hood comes to mind. From the court of King Arthur, the epic Middle English poem of Sir Gawain and the Green Knight was created by an unknown author (one of Tolkien’s first scholarly subjects). The Green Knight arrives during a Christmas feast. He and his horse are a brilliant green in color and decorated with precious jewels. Yet he wore no helmet and no chain mail either, Nor any breastplate, nor brassarts on his arms, He had no spear and no shield for thrusting and striking, But in his hand he held a branch of holly

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That is greenest of all when the groves are bare, And an ax in the other hand, huge and monstrous, A fearsome battle-ax to find words to tell of.

The Green Knight offers a challenge to King Arthur: he will allow a knight to cut off his head with his ax, on the condition that he will deliver the same blow a year later. Sir Gawain insists that he undertake the test on behalf of the court. He decapitates the Green Knight, who picks up his head and rides away. A year later Sir Gawain travels to the Green Chapel to meet the Green Knight (with head back in place!) and to undertake the test. It is really a test of chivalry, which Sir Gawain passes. The Green Chapel was apparently located in the small village of King’s Nympton, in North Devon. Its fine old Norman Church is decorated with green men. In Europe, along with green men, there is a tradition of sacred trees, often identified by their foliage. The immense world tree of Norse mythology was Yggdrasil, an ash. Trees were sacred in Celtic culture, in Ireland, Scandinavia, Gaul, and among the Germanic tribes east of the Rhine River. Predominant in sacredness was the oak. In Celtic culture, the lunar calendar was marked by trees. The Irish developed the Ogham alphabet, used from the fourth to tenth centuries, in which each letter was a tree. The high priests of the Celtic religion, the druids, were knowledgeable about the sacred uses of plants. The name druid may be derived from early Greek roots, as “oak knower.” Merlin, the wise man of King Arthur’s court, was likely a druid. The best-known story involving their priestly functions is the oak and the mistletoe, described by Pliny in his Natural History and explained by Sir James Frazer’s The Golden Bough. Frazer titled this book after the mistletoe, and he wrote: “The first thing to notice about the Golden Bough is that, being a bough, it is poised, as it were, between heaven and earth.” According to Pliny, druid priests oversaw the collecting of the rare boughs of mistletoe on the sixth day of the moon in winter, when the oak leaves had already fallen. Mistletoe was collected before it had fallen to the ground, and it was used ceremonially and medically, reputed to enhance the fertility of animals and people. Mistletoe was depicted on human heads in Celtic art. So that opportunity for a romantic kiss at a holiday party may have some hidden baggage— and certainly has an old history. Virgil wrote in the Aeneid: As in the woods by autumn frost beset The mistletoe, which springs not from the tree

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Figure 1.2 The Indo-European language tree, based on work by Thomas V. Gamkrelidze and Vjacˇeslav V. Ivanov.

On which it grows, puts forth a foliage new And rings the smooth round trunks with saffron tufts So on the dark tree shone the leafy gold And tinkled in the breeze. With eager hand Aeneas grasps and breaks the lingering branch.

The similarity of ceremony and the use of trees by these European cultures suggest a high degree of interaction among them, or perhaps a common origin of their awe of trees in the natural world. Most of them spoke languages related by similar vocabulary and sounds. Over the past two centuries, linguistic analysis has built one of our great intellectual achievements: the Indo-European language tree (fig. 1.2). A search for common (or very similar) characteristics among these languages— French, German, Greek, Latin, Persian, Sanskrit, et cetera— has made possible the construction of an ancestral Proto-Indo-European (or PIE) language, with some speculation about the culture of the PIE-speaking society. Just as biologists use molecular cues from DNA sequences to re-create the evolutionary history of plants (p. 26), linguists have found characteristics among the languages to determine their relationships. Paul Friedrich was the first to analyze these languages for their use of tree names, and he constructed a list of the most important types. This

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was certainly a conservative list, because names were lost as people settled in places where the trees would not grow, and they adopted names from tribes speaking non-Indo-European languages. His list includes oak, birch, conifers, poplar, willow, apple, maple, alder, filbert, nuts, elms, linden, ash, hornbeam, beech, cherry, and yew. Names were often broad categories, such as nuts, or trees that could be many species (willow). In other cases, the names could be two to three tree species or perhaps even unique. This PIE list of sacred trees (which Friedrich called “arboreal units”) strongly overlaps with the trees in the Ogham alphabet and the Celtic calendar. Other plants, such as mistletoe and barley, were known to the PIE speakers. The most important tree was the oak (PIE = ayg), which was revered in the high mountain passes and was the abode of the god of thunder. Also of sacred importance were the apple and ash. The ash (PIE = os) was a source of a sweet fluid that was collected and used even in the early twentieth century. There are actually two distinct plants given this name, both with similar leaves. One is the flowering ash, large trees of the genus Fraxinus, and a second is a small mountain-dwelling tree with brilliant red berries during the autumn: rowan. The two PIE words for apple, maHlo- and a˘bVl, were transformed to the Latin Malus (the generic name today) and to English as apple. With the PIE tree flora, attempts have been made to pinpoint the geographical origin of the language and people, varying from southeastern Europe to the Caucasus and adjacent areas of central Asia. Unfortunately, these arboreal units have rather broad distributions and do not allow a resolution to the problem, other than suggesting that forests were important in PIE culture. However, the distribution of these trees expanded into northern Europe after the last ice age. DNA evidence is more consistent with the arrival of the language from the central Asian region of the Altai Mountains into Europe around 4500 bce, and into England shortly after. Many trees of cultural importance in Europe and west Asia were probably not known to the PIE speakers. Holly, native to western Europe and culturally important there (the Green Knight carried a bough of holly) is not on Freidrich’s list. Two plants important in early Greek culture are also missing. The true (or bay) laurel is a tree of the Mediterranean region. It was used ceremonially by the Greeks and later by the Romans. As a wreath it was given to victors in athletic and other competitions, although wild olive was also sometimes used. We generally think of the olive branch as a peace offering. In the modern Olympics, a laurel wreath is given to every victor, along with a medal and spray of flowers; winners of the Boston Marathon receive a similar honor. The leaf of the acanthus shrub, with very

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Figure 1.3 Left, distinctive leaf of acanthus, inspiration for the Corinthian column. Center, three-lobed leaf of palasa tree, used by devotees of Lord Shiva, in India. Right, clover, sacred to Christians, especially Irish.

distinctive shape and toothed edges, was the inspiration for the design of the Corinthian column (fig. 1.3). Perhaps the Indo- European language that was geographically and ecologically the most distant was the Sanskrit language, along with Vedic culture, established in northern India around 4,000 years ago. It is probably the oldest language of the family still spoken today. Few of the sacred Indo-European trees survive in Sanskrit, mainly because the speakers only encountered a few of the trees in the high valleys of the Himalayan range. Instead, the Indo- Aryans encountered trees of a distinctly tropical flora, which were used and venerated by the indigenous people they encountered. Leaves play a rich role in contemporary Hindu religion, often placed on a tray in worship, including leaves associated with Hindu deities. Leaves with three parts are associated with the trident of Lord Shiva, such as palasa (fig. 1.3). I’m reminded of the three-leaved clover (well, rarely four-leaved), a Christian symbol to the old Irish (fig. 1.3). Also, leaves are used to commemorate the events in the lives of the great saints, such as Lord Buddha. The tree under which the Buddha received enlightenment was the bodhi (or peepul) whose distinctive shape (fig. 10.9) is easily recognized in the early religious artwork. The banyan was also important as a tree in which a seeker might find shelter. In India these trees are sacred in Jain and Hindu traditions and important to Buddhists in nearby countries. Although green men in European culture most likely came with the Celts in England and adjacent Brittany, it is possible that the figures came

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from much more ancient Neolithic culture in both places, but we have no record of their languages and little knowledge of their culture. Similar descriptions of green men and sacred uses of other leaves were present in ancient Semitic cultures, not speaking languages of the IndoEuropean tree, as in the Sumerian Gilgamesh. There is a green man associated with Islam: Al-Khidr. This mythological figure goes back to the time of Alexander the Great. Alexander was looking for the fountain of eternal life, and he commanded an assistant to throw a dried fish into a spring, thinking that the authentic water would bring the shriveled body back to life. He found the spring with the help of Al-Khidr. This same person was alleged to be the father of the prophet Moses and was recognized by the prophet Muhammad in the Qur’an, where it was revealed that when AlKhidr sat on barren ground, it soon turned green with vegetation. Hence the color green became sacred in Islam, and the flags of Islamic countries feature green. A little further afield in Asia and North Africa is the date palm, sacred to the civilizations in Asia and North Africa, but not in the PIE list. The date palm was important in the early civilizations of the Fertile Crescent, in a warmer and more arid climate that would allow date palms to grow, but not temperate forest trees. For the Jewish celebration of Sukkot, the Feast of the Tabernacles held in late September to early October, participants construct a temporary dwelling out of branches and palm fronds in which they eat and pray, and perhaps even sleep. Each day during Sukkot, observing Jews recite special blessings over the lulav and etrog. The latter is citron fruit long cultivated in the area. The lulav is the perfect young and unopened leaf of the date palm, bound with leafy boughs of willow and myrtle. These are collectively known as the four plants, mentioned in the Torah. In the United States, buyers move into the date palm groves of California and select perfect lulav to deliver to the orthodox communities near New York City. The date palm leaf covered the ground for Jesus’s triumphal entry into Jerusalem, long celebrated as Palm Sunday. Since palms were not available in much of the later expansion of Christianity, other plants (some of them sacred to the PIE culture) were substituted, including myrtle. The earliest Sumerian depictions of leaves are from the royal burial at Ur about 4,500 years ago, probably from rosewood and imported from farther to the east. Green men and sacred foliage thrive in contemporary culture. In the Lord of the Rings trilogy, written by Tolkien (and popularized by the films

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of Peter Jackson), the druid was Gandalf the magician, and the green man was Treebeard. Treebeard was the eldest of the Ents, tree-like beings who dwelled in the great woods. These deep eyes were now surveying them, slow and solemn, but very penetrating. They were brown, shot with green light. Often afterwards Pippin tried to describe his first impression of them. “One felt as if there was an enormous well behind them, filled up with ages of memory and long, slow, steady thinking; but their surface was sparkling with the present: like sun shimmering on the outer leaves of a vast tree, or on the ripples of a very deep lake. I don’t know, but if felt as if something that grew in the ground— asleep, you might say, or just feeling itself as something between root-tip and leaf-tip, between deep earth and sky had suddenly waked up, and was considering you, with the same slow care that it had given to its own inside affairs for endless years.”

In the Star Wars movies, the druid-like wise figure is Obi-Wan Kenobi, and the green man character is Yoda, who looks like he could’ve been modeled after the grotesque of a medieval cathedral. Although the examples I have provided here are part of the cultural streams that have contributed to Western culture, such leafy examples can be found in others. While living in Malaysia in the 1970s, my wife, Carol, and I took lessons in Chinese brush painting. We spent many months attempting to depict the foliage of two plants, bamboo and lotus, with a few simple brush strokes, sacred images in Chinese tradition. I was almost always unsuccessful, except in a few moments when I moved beyond frustration and the foliage seemed to appear more or less naturally, as if on its own. In Malaysia I also studied the blue color of leaves of certain rainforest understory plants. One plant, a Selaginella species (fig. 2.8), produced a particularly electric iridescent color. A linguist friend, Gérard Diffloth, studied the language of the Semalai, an aboriginal group living in the mountains. For the Semalai, the tiger was a mythical god-like creature and, according to Diffloth, this plant was given a name that translated roughly as “hair on the tiger’s rump.” The traditional Malay people, living along the coast and near rivers, called this plant paku merah (peacock fern) and used it in a medicinal tonic, ubat jambu.

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Foliage in the Garden of Paradise I shift from the foliage of natural forests and native trees to groves and gardens, strongly influenced or created by humans. With the rise of civilizations, forests were converted to croplands and were consumed as materials for construction and energy for early industry, such as the smelting of ores. Certain forest trees were particularly important for the construction of ships, for trade and defense. The remaining forests often became the reserves of royalty. Indeed, the name “forest” has no Latin or Greek roots and comes from the Middle English, to denote royal hunting grounds. In the remaining groves and in gardens, our ancestors placed plants with religious and cultural significance (and some reminders of our forest past) in them. Gardens probably were planted by all cultures practicing agriculture, just by planting useful, sacred, and attractive plants in the open spaces of their villages. From early civilizations of the Near East, the ideal of the garden of paradise arose. In the biblical Genesis, the Garden of Paradise became known as the Garden of Eden, where Adam and Eve first knew guilt and were cast out. These gardens were illuminated through writings and the visual arts during the Christian era. Such gardens were also described in other traditions, particularly in Islam with an account of the Garden in the Qur’an. Rather than the original sin and banishment from the garden, perhaps a better interpretation is that in leaving the garden humans became responsible for their actions and developed the capacity for caring and stewardship, something that tending a garden teaches. David Rosenberg has described the Garden of Eden in poetic terms (based on serious scholarship) highlighting the environmental sensibilities of the people who imagined the garden. He wrote his book The Lost Book of Paradise: Adam and Eve in the Garden of Eden and Adam’s dialogue while living in a garden: but here my creator set me to crawl ashore in a great library the texts of plants, hear the arguments of animals and the wild wind from other worlds with this restless mind moved to learn at a leaf master the map of hidden roots follow the road from nostril to flower to discover desire dusting me with its future

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Figure 1.4 Botanical Gardens at Padua, established in 1544. Left, view of main gardens, with institute building and conservatory for Goethe’s palm in background. Right, plan of the main garden from the first published description, 1591.

This powerful metaphor of the garden of paradise inspired the creation of royal and ecclesiastical gardens of form and beauty, and also guided our design of the great and beautiful botanical gardens in Europe (fig. 1.4) as well as those in the colonies of Western nations, such as Calcutta, Bogor, Pamplemousse, Peradeniya, and elsewhere. These gardens were emblematic of an imperial Christian authority in these foreign lands. The gardens became important not only in the gathering of botanical wealth from the subjugated colonies, but also the spreading of environmental knowledge about human harm to the colonial landscapes and, ultimately, about climate change (see p. 76). The plants depicted in these European gardens reflected our geographical knowledge of nature; with time and more explorations of the world, garden plants became more exotic and fantastic— part of the paradise vision. Early garden depictions were rather unexciting, with familiar plants chosen as symbols for hope, love, and chastity. I’m not sure if such paintings had much of an impact, as they were completed for the royalty and had few admirers— far more now, 600 years later. With the introduction of foliage from the tropics, gardens became more fantastic in appearance— and also ultimately had a wider aesthetic impact. The first knowledge of plants of the tropics in the West came from Alexander’s expedition to India. His military officers were instructed to collect information on natural history, plants in particular, and this infor-

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mation was used by Theophrastus, the disciple of Aristotle— who was Alexander’s tutor. The collections included citron, banyan, jackfruit, cotton, banana, ebony, terebinth, rice, date palm, pepper, and cloves. Theophrastus described them in his Enquiry into Plants, later used by Pliny in his Natural History. These manuscripts were copied by Islamic scholars and Christian monks. Cycles of copying ultimately rendered any illustrations useless, and the manuscripts were read by few, principally by medical students and professors in the early universities that appeared in the twelfth century and later. However, in the late fifteenth century and beyond, the situation changed dramatically. First, the printing press was invented, and books by Theophrastus (with commentaries) and more original contributions were printed and more widely appreciated. Second, advances in ship craft and navigation enabled explorers to move from European countries to different parts of the world— primarily in the tropics— with the aim of discovering the sources of spices. This revolutionized the study of plants, with a more global knowledge and then a generally accepted system of scientific naming by Linnaeus in the eighteenth century. Fountains of youth were also depicted in writings and paintings. The original story originated with Alexander and Al-Khidr, and was reprised by Ponce de León, who searched for this fountain in Florida. Consequently, gardens of paradise and fountains of youth were imagined destinations of explorers, and artistic depictions of them began to be populated with the fantastic foliage of tropical plants. The frontispiece of John Parkinson’s Paradisi in Sole Paradisus Terrestris is a rendition of a garden of paradise (fig. 1.5). A careful look reveals some of Alexander’s plants, a cotton plant converted into a vegetable sheep and a rather stunted banana. From the New World tropics, Parkinson added a cactus and a pineapple. The garden of paradise enjoyed by Adam and Eve was becoming “tropicalized.” With continuing tropical exploration, more and more exotic plants were introduced to the private and public gardens of Europe, and more and more people came to appreciate their unique forms and the fantastic diversity of their foliage. Friedrich Wilhelm Heinrich Alexander von Humboldt (for brevity’s sake I’ll refer to him frequently as Humboldt), the greatest scientist and humanist of the nineteenth century, read the accounts of these explorers and became inspired to organize and complete his own voyage, one of the greatest explorations in the history of science. He and botanist colleague Aimé Bonpland left Europe in June 1799, and they traveled through Venezuela, Cuba, Colombia and Ecuador, Peru, Mexico, and the United States

Figure 1.5 Garden of Paradise in the frontispiece for Paradisi in Sole Paradisus Terrestris, by John Parkinson.

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Figure 1.6 Alexander von Humboldt and Aimé Bonpland, on the Orinoco River. From the painting by Eduard Ender.

before returning to Europe in August 1804 (fig. 1.6). During the expedition they traveled near the source of the Orinoco River and its connection with the Rio Negro (a tributary of the Amazon), and they climbed to 5,300 meters near the summit of Chimborazo, the highest elevation that any European had ascended up to that time. They collected specimens of plants and animals (some 60,000 of the former) and recorded innumerable observations (temperature, altitude, latitude, longitude, barometric pressure, magnetic fields, electric discharges, the blue of the sky, and more). After returning to Europe, Humboldt spent the rest of his life analyzing and summarizing the results of this research. In so doing, he established the sciences of geophysics, physical geography, and plant geography. Humboldt was more than a scientist. Before his expedition, he had befriended some of the intellectuals of Germany, especially the great poet and natural philosopher Johann Wolfgang von Goethe. Humboldt’s goals for this expedition were lofty and included a study of the physiological and emotional responses of humans to various environments. He was particularly struck by the effects of tropical vegetation and light on the human psy-

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che. His first experiences of tropical vegetation overwhelmed him and influenced him throughout the rest of his long life. He wrote of his emotional response to tropical vegetation in the first, and most popular, book resulting from this expedition, Aspects of Nature, as well as the final five- volume synthesis of his knowledge of the world and the universe: Cosmos. Humboldt’s ideas about tropical nature in Aspects of Nature influenced European artists long before the more detailed discussions of tropical aesthetics in volume 2 of the Cosmos. In the latter, Humboldt gave detailed descriptions of tropical nature as well as specific recommendations to landscape artists. In the former, he described the plant types (forms of vegetation) that were the most important elements of tropical rainforests: palms (“the loftiest and noblest of all vegetable forms”); the mimosa form (with “delicately pinnate foliage”); bananas and the gingers (whose stems are “surmounted by long, silky, delicately-veined leaves of thin texture, and bright and beautiful verdure”); the pothos or aroids (“succulent herbaceous stalks support large leaves . . . always with thick veins”); lianas (“twining rope plants . . . the utmost vigor of vegetation”); arborescent ferns (“foliage . . . delicate, of a thinner and more translucent texture”); the orchid (“distinguished by its bright and succulent leaves and by its flowers of many colors and strange and curious shape”); and arborescent grasses or bamboos (“an expression of cheerfulness and of airy grace and tremulous lightness, combined with lofty stature”). Humboldt wrote in Aspects of Nature: It is under the burning rays of a tropical sun that vegetation displays its most majestic forms. In the cold north the bark of trees is covered with lichens and mosses, whilst between the tropics the cymbidium and fragrant vanilla enliven the trunks of the anacardias, and of the gigantic fig trees. The fresh verdure of the pothos leaves and of the dracontias contrasts with the many flowers of the Orchideae. . . . A single tree adorned with paullinias, bignonias and dendrobium, forms a group of plants which, if disentangled and separated from each other, would cover a considerable space of ground. In the tropics vegetation is generally of a fresher verdure, more luxuriant and succulent, and adorned with larger and more shining leaves, than in our northern climates.

Just as the writings and illustrations of his compatriot Georg Forster inspired Humboldt, his publications dramatically affected scientists and artists throughout Europe and in the New World. Humboldt’s influences on

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Figure 1.7 The Heart of the Andes, painted in 1859 by Frederic Church.

artistic expression in the nineteenth century were pervasive and inspired depictions of gardens of paradise that were distinctly tropical. Several European artists followed his steps in the tropics. For some, he wrote prefaces to the folio books of engravings derived from their paintings. He also influenced garden design, including the increased planting of tropical plants for interiors (despite concerns about suffocation at night, p. 49). Several factors increased his popularity. With the continued improvement in printing technology and paper making, books became less expensive and more widely distributed. Thus, Aspects of Nature appeared only three years after his return and was quickly translated into the major European languages. Furthermore, literacy had increased, and ideas were disseminated more quickly and broadly in the nineteenth century. Although paintings of tropical landscapes were generally not widely viewed, their renditions as engravings in books were. Humboldt also influenced American painting. Trained in the Hudson Valley School with Thomas Cole, Frederic Church traveled to the South American tropics in 1853 and 1857, following Humboldt’s footsteps. The most spectacular of the resulting tropical landscapes is The Heart of the Andes (1859, fig. 1.7), now residing at the Metropolitan Museum of Art in New York City. I was dumbstruck when I first saw it in 1966, as a beginning graduate student at Rutgers University, just outside of the city. The Heart of the Andes was exhibited as a single painting in a special gallery, to a ticket-buying public. Enthusiasts came in droves, first in New York and then in London.

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Church had hoped to have Humboldt see the painting in Berlin, but the old explorer and humanist died before the painting arrived in Europe. Another important American artist influenced by Humboldt was Martin Johnson Heade, who specialized in more intimate tropical paintings— particularly featuring hummingbirds; Heade and Church were close friends. I was not familiar with Humboldt’s writing as a student, but I read other authors who were surely influenced by him: Charles Darwin (The Voyage of the Beagle), Alfred Russel Wallace (The Malay Archipelago), Joseph Conrad (Heart of Darkness, Lord Jim), H. M. Tomlinson (The Sea and the Jungle), Marston Bates (The Forest and the Sea), W. H. Hudson (Green Mansions), Peter Matthiessen (The Cloud Forest), and more. Darwin took Humboldt’s early books on the voyage of the Beagle. His journal included this entry after his first visit to a Brazilian tropical rainforest: “Humboldt’s glorious descriptions are and will forever be unparalleled; but even he with his dark blue skies and the rare union of poetry with science which he so strongly displays when writing on tropical scenery, with all this falls short of the Truth. . . . I am at present fit only to read Humboldt; he like another sun illumines everything I behold.” Thus, Humboldt indirectly influenced my becoming a botanist and working extensively in the tropics. It was only after living in the tropics that I began to read him, to help me comprehend my own experience of tropical plants and landscapes. And my own research became directed toward the function of the leaves of tropical plants, their aesthetic beauty so elegantly described by Humboldt. The influences of Humboldt were magnified by international exhibitions, or world fairs, from the early nineteenth century into the twentieth century. Such fairs featured inventions and products, new technology, and culture. European nations were eager to display products from their colonial possessions and to idealize the traditional cultures of their “natives,” who were the producers of much of that wealth. Notable fairs were the Great Exhibition in London of 1851, with its Crystal Palace (p. 137), and the Exposition Universelle in Paris in 1889. Later in the century, large expositions were held in the United States: the Centennial International Exhibition of 1876 in Philadelphia, the World’s Columbian Exposition in Chicago (1893), the Louisiana Purchase Exposition in St. Louis in 1904, the Panama-California Exposition in San Diego in 1915, and several large world fairs in New York City, the first in 1853. These were huge affairs, the succeeding ones invariably larger than the previous, and they were extremely popular in the United States. The Philadelphia fair attracted 10 million visitors, or 20% of the country’s population at that time, and

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Figure 1.8 Horticultural Hall, Philadelphia Centennial International Exhibition, 1876. Left, hall exterior; right, interior planting.

27 million attended the Columbian Exposition in Chicago. The expositions generally had horticultural halls, with luxuriant displays of vegetation, both inside and outside during the summer months (fig. 1.8). Visitors even saw indigenous people, such as the Igorot of the Philippines, surrounded by the lush tropical vegetation of their homes. In the twentieth century, the rise of the movie industry added the portrayal of the tropics in Tarzan of the Apes and other films. In the United States, such visions of the tropics were employed to stimulate visits and real estate purchases in our warmer subtropical climes: Southern California, Florida, and the offshore possessions of Hawaii, Puerto Rico, and the Virgin Islands. Added to the garden of paradise theme was the legend of the fountain of eternal youth, especially with Ponce De León’s explorations in Florida. Thus, the theme of eternal youth was added to the gardens, to make them even more irresistible to cold weather people of the North, whom we in Florida began calling “snowbirds.” In Miami the selling of the landscape began after Henry Flagler’s railroad arrived in 1896. The advertisement for real estate often showed tropical landscapes with orchids, bananas, palms, bamboos, philodendrons, and other plants, along with orange fruit and beautiful mermaids. This was all very Eden-like, paradise for sale. The promise of Miami as such a garden is difficult to find when driving down US-1 or I-95 today, but it was found in the private gardens of hotels and homes, in parks and public gardens (fig. 1.9). South of the city is a large agricultural district, the Redland, making Miami-Dade County one of the most valuable agricultural counties in

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Figure 1.9 Miami tropical gardens. Left, Royal Palm Hotel, ca. 1905. Right, Judith Evans Parker at her home garden in Coral Gables, 2012.

Figure 1.10 Left, vegetable sculpture, by Philip Haas. Right, the largest leaf at the 2014 Rhubarb Festival, held by the perennial victor, Norma Koch, in Lanesboro, Minnesota.

the United States. The county’s primary agricultural commodity these days is “foliage.” Growers produce huge quantities of the plants of Humboldt’s “forms of vegetation”: bamboos, aroid vines (especially philodendrons), orchids, mimosoid trees, bananas and heliconias, tree and other ferns, and palms. These add an accent of the tropics in homes, professional offices, and shopping malls. Interest in maintaining such tropical planting in our homes began in the nineteenth century, influenced by Humboldt and the

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expositions. If we couldn’t voyage to the exotic tropics, we could install a bit its foliage in our parlors. Think about your associations with leaves and foliage today: the tree or branch topping out a new building; an evergreen wreath during Christmas, along with the evergreen tree; the bough of mistletoe; palm fronds the week before Easter; the red maple leaf on the Canadian flag or the Toronto Maple Leafs ice hockey uniform; the green flag of Saudi Arabia and greens in the flags of other Islamic countries; the cedar on the Lebanese flag; the Jolly Green Giant (that twenty-first-century green man marketeer); little green men (from Mars), Yoda (the seer of the Star Wars original trilogy); the vegetation of Avatar; Treebeard in Peter Jackson’s version of the Tolkien Lord of the Rings trilogy; Popeye and spinach; the vegetable portraits of Giuseppe Arcimboldo, reprised by Klaus Enrique and Philip Haas (fig. 1.10); the latest version of the Robin Hood legends; Kermit the Frog (a bit of druid and green man combined?); Parrot Jungle (now Jungle Island) in Miami and other amusement gardens; and rhubarb (fig. 1.10), for example, the Beebopareebop Rhubarb Pie of Garrison Keillor. Behind each of these images or memories is a long cultural history rooting us in such a green world. We are green men.

Chapter Two Leaf History In branching cones the living web expands, Lymphatic ducts, and convoluted glands; Aortal tubes propel the nascent blood, And lengthening veins absorb the refluent flood; Leaves, lungs, and gills, the vital ether breathe On earth’s green surface, or the waves beneath. So Life’s first powers arrest the winds and floods, To bones convert them, or to shells, or woods; Stretch the vast beds of argil, lime, and sand, And from diminish’d oceans form the land! erasmus darwin, The Temple of Nature

The book will try to give the child wonder Of how, in our time; we understand life came to be: Stuff flung off from the sun, the molten core Still pouring sometimes rivers of black basalt Across the earth from the fountains of its origin A hundred million years of clouds, sulfurous rain. The long cooling. There is no silence in the world Like the silence of rock before life was. robert hass, “State of the Planet”

A

point of limitless energy expands, stars and galaxies form, then planets, life, leaves, and humans appear. Leaves, the subject of this book, are the result of this long history. As inheritors of the photosynthetic machinery that originated after the origin of life, they subsequently changed the trajectory of that history. It is as Theodosius · 21 ·

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Dobzhansky famously wrote: “Nothing in biology makes sense except in the light of evolution.” The hypotheses and theories of biology are also illuminated by an examination of history.

A Brief History Edwin Hubble’s discovery that the universe is expanding led to estimates of its origin at 13.75 billion years ago, and we are still piecing together its early evolution. Light matter condensed into galaxies with billions of stars, and stars collapsed as supernovas— producing the elements of the universe (fig. 2.1). All of the elements present in leaves and people were derived from those explosions during those billions of years; we are the stuff of stars. This is an awesome history, and the precise and improbable details of this expansion (the anthropic principle) made the conditions conducive for the origin and evolution of life. The appearance of life on our planet, about 4 billion years ago, is a mystery. The laws of physics and chemistry are consistent with the nature of life, but do not predict it. Thus there is novelty in life’s origin. Some argue that life may have originated somewhere else in the universe and arrived on Earth, but that begs the question of how it originated. Steven Weinberg (a Nobel Laureate in Physics) wrote: “How surprising it is that the laws of nature and the initial conditions of the universe should allow for the existence of beings who could observe it. Life as we know it would be impossible if any one of several physical quantities had slightly different values.” Thus, life emerged from a physical universe.

Figure 2.1 Deep history. Left, Tycho, a supernova remnant and producer of chemical elements (courtesy of NASA). Right, stromatolites, living fossil reef, Shark Bay, West Australia (courtesy of Mike Heithaus).

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Our estimates for the age of the planet have increased over the centuries. Early on, they were based on the genealogy of the Old Testament. James Ussher (1581–1656), the Bishop of Ireland, calculated the most accepted estimate of the date of origin as the night preceding Sunday, October 23, 4004 bce, or over 6,000 years ago. In the ancient Vedic culture of India, creation and dissolution were envisioned as running in cycles, each cycle being 4.36 billion years. With the increase of knowledge of biology and geology in the eighteenth century, the inadequacy of the biblical estimate of time was increasingly appreciated, and Charles Darwin’s grandfather, Erasmus (whose poetry is quoted at the beginning of the chapter), said that it required many millions of years. This estimate stretched to tens of millions, and then hundreds of millions, in the nineteenth century. The present scientific estimate for the age of Earth is 4.54 ± 0.05 billion years, based on the dating of rocks from the moon, meteorites, and the oldest terrestrial rocks in Western Australia. Estimates for the timing of life’s appearance comes from fossils, residues of organisms as old as 3.5 billion years, and guesses at origins perhaps 300 million years earlier. It is hard to put a handle on such a span of time in a way we can grasp. Thinking of the age of the planet as the week of creation in the Genesis account makes each day equal to 657 million years, and each hour as 2.7 million years. That would also make the 10,000 years or so of human history discussed in the first chapter equivalent to the last 13 seconds of that week.

Making a Living At the origin of life, the atmosphere lacked oxygen, deduced from the minerals that formed then and the composition of gases from modern-day volcanoes. To make a living, these organisms had to have a source of carbon and access to some energy-giving reaction. Carbon could have come from carbon dioxide in the atmosphere, and energy could come from gases in the atmosphere, such as hydrogen sulfide and hydrogen, or from reactions in minerals, such as iron, or deposits of sulfur. Thus, quite a variety of organisms appeared, visually similar but metabolically very different. A source of energy that also could be tapped was light, or electromagnetic energy. Some early purple sulfur bacteria used hydrogen sulfide to produce usable energy, with sulfur as a by-product. However, the most important of those photosynthetic organisms were the cyanobacteria, formerly known as blue-green algae. Many of these grew as colonies, and some formed low stool-shaped concretions: stromatolites (fig. 2.1). Stromatolites

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were present very early, quickly became widespread in the fossil record, and are still found even today. Their metabolism began the transformation of the atmosphere with the accumulation of oxygen gas. The summary of this important process is 6CO2 + 6H2O + light → C6H12O6 + 6O2 Carbon dioxide and water combine, in the presence of light, to make sugars (here the formula for a 6-carbon one, as glucose) and release oxygen gas as a by-product. As oxygen became available in the atmosphere, or in small pockets in the ground, it could be the partner in the oxidation of carbohydrate molecules (the products of other metabolisms) and the evolution of aerobic respiration, which is what we do: C6H12O6 + 6O2 → 6CO2 + 6H2O + energy Respiration looks like the reverse of photosynthesis, but these are two very different processes.

True Cells The first living cells were very simple in organization, lacking a nucleus or compartments (organelles). About 2.2 billion years ago, a more complex cellular organization appeared. The process of the endosymbiosis of specialized simple cells, such as cyanobacteria and respiring bacteria, led to the evolution of such an organization. The simple cells define a domain of life, the Bacteria, and the more complex cells form the domain Eukarya. The idea of endosymbiosis (fig. 2.2) was first proposed by Konstantin Mereschkowsky and Ivan Wallin in the 1920s (and Mereschkowsky picked it up from a footnote on chloroplast division by Andreas Schimper; p. 50) but not taken seriously. It was taken up again by Lynn Margulis, with tenacity and wit, in the 1970s, and now is virtually universally accepted (Margulis died just before I began writing this chapter, in November 2011). Eukaryotic cells are capable of respiration from the activity of their mitochondria (tiny powerhouses) resulting from the uptake of previously free-living respiring bacteria. Both the bacteria and mitochondria require oxygen for the process to occur. Photosynthetic eukaryotes evolved mainly through the uptake of once free-living single-celled cyanobacteria, producing the photosynthetic organelles, chloroplasts. Some groups, such as the red algae, assimilated single-celled eukaryotic photosynthesizers and made chloroplasts from them. Thus, the cells within leaves have two organelles, chlo-

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Figure 2.2 Left, endosymbiosis diagram. Right, leaf mesophyll cell of timothy grass (courtesy of Brian Gunning).

roplasts and mitochondria, that are the result of endosymbiont events that took place some 2 billion years ago (fig. 2.2)

Advantages of Being Multicellular Cells grouped together and specialized, resulting in complex multicellular organization, which led to the evolution of many groups of organisms beyond the Bacteria (along with another later group of distinctive and often extreme environment–loving organisms: the Archaeobacteria). The multicellular ancestors of these kingdoms within the Protista— animals, plants, and fungi— appeared about 1.5 billion years ago. From the flat appearances of these groups of cells, these could have been photosynthetic. We have learned much about the evolution between and within these groups by sequencing and comparing segments of their DNA. This has enabled the construction of evolutionary trees that help us visualize the relationships and ancestry of different organisms (fig. 2.3). This tree bears some resemblance of the tree of Indo-European languages (p. 5), with similar methods of analysis. I like these tree diagrams because I began my scientific career using biochemical techniques to study the evolution of plant groups. There are a couple of trends in the branching patterns of this tree, first discernible in the protists and later in the animals and plants, which relate to the formation of leaves in plants. Specialization in cell function made

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Figure 2.3 Tree of life.

possible improvements in the capture of energy appropriate to the energy sources of different organisms. For organisms that fed on organic material and respired, rapid movement improved feeding efficiency, chasing down prey, and so forth. That meant the evolution of cells, tissues, organs, and systems to facilitate movement for the catching of prey, and then assimilation and distribution of energy to all parts of the body. For organisms that captured light, that meant the display of chloroplasts in cells and tissues to most efficiently absorb light, organs to display the photosynthetic tissues, and tissues to distribute the products of photosynthesis to all parts of the organisms. Although some algal photosynthesizers established flat structures of cells floating in water, more precise display was associated with branching and being anchored in one place. The trends in this evolution are seen among three photosynthetic phyla, the green, red, and brown algae (fig. 2.4). These groups are very distantly related. The brown algae are related to the diatoms and water molds, and they use distinct pigments for capturing light in photosynthesis, giving them a brownish color. The red algae are a little closer to the green algae, but produce a red accessory pigment that gives them their distinct appearance. The green algae, with

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Figure 2.4 Examples of red, brown, and green algae with flattened photosynthetic structures. Left, Halimeda, a green alga, on a coral. Center, sea palm, brown alga. Right, flat photosynthetic surfaces of Mesophyllum mesomorpha, a circumtropical red alga (left and right photos courtesy of Ligia Collado-Vides).

the same pigments for photosynthesis as green plants, are their ancestors. Similar strategies for the capture of light evolved in each, having extensive flat surfaces that capture light efficiently, much like leaves. The leaves of plants, the subject of this book, are inheritors of the photosynthetic machinery evolved in simple cyanobacteria over 3 billion years ago. Mitochondria, those cellular powerhouses, are likewise inheritors of energy-processing pathways evolved in simple aerobic bacteria some time later.

Plants and Animals on Land The land surface began to be populated by plants, animals, and fungi about 500 million years ago (mya), or at about 5:30 a.m. of the last day of creation’s week. The land surface presented new challenges for life, the danger of desiccation, the requirement of more mechanical strength, and protection from the harsh sunlight. The accumulation of oxygen was associated with a rise in UV-protecting ozone, and that additional protection probably controlled the timing of organisms’ colonization of this new habitat. Land plants, derived from the green algae, inherited their characteristic of cell structure, including a wall of cellulose, their biosynthetic capacity, and the general features of reproduction most suited to an aquatic environment. Green algae generally reproduced in a cycle that included both spore-producing and gamete-producing stages, with an alternation between them. Land plants reduced the size of the gamete- producing

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Figure 2.5 Bryophytes, with leaf-like structures. Left, giant Dawsonia moss (up to 50 cm high!) from Mount Kinabalu, Borneo. Right, yellow ladle liverwort from the Cascade Mountains of the Northwest.

phase so that a small amount of water would allow the male gamete to swim to the female egg. The first land plants were likely ancestors of bryophytes, the small mosses and liverworts persisting today. These produce leaf-like structures, but without the conductive cells of the vascular plants (fig. 2.5). They probably were abundant enough to raise the oxygen concentrations to present levels. Plants as we know them today appeared about 430 mya. These plants had expanded biochemical capabilities to produce molecules that served both as UV sun blocks (in fact, some of those compounds are used in the sunblock creams sold today) as well as components of the wall cement that made the cellulose cell walls extremely strong: lignin. Lignin also appeared in cells specialized for the transport of water and nutrients throughout the plant. In early plants, these cells— tracheids— provided both strength and conduction, forming a tissue called xylem. Later on, conducting cells became more specialized for efficient transport, as vessel elements and as fibers specialized for mechanical support. Another tissue, phloem, appeared and provided the translocation of synthesized molecules (mainly sugars and some amino acids) throughout the plants. These first land plants also acquired a special waxy layer, cutin, to prevent water loss and a tough covering protecting their spores, sporopollenin. In these plants, the spore-producing generation became dominant, but the early plants were only a few centimeters tall. At this time the animals that ate these plants, if at all, were primarily arthropods, ancestors of the insects.

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Figure 2.6 Left, Cooksonia, plant appearance in diorama at the Smithsonian Institution National Museum of Natural History. Right, whisk fern, detail showing sporeproducing structures and projections.

A good example of such an early plant is Cooksonia, its shape and size nicely depicted in a diorama at the Smithsonian Institution National Museum of Natural History (fig. 2.6). These early plants consisted only of stems; roots and leaves were absent. The stems were photosynthetic, and nothing like such plants survives today. There is an existing plant that looks like Cooksonia and its relatives: the whisk fern (fig. 2.6). It has no leaves, other than tiny scales beneath the spore-producing structures, no roots, and its branches split dichotomously. We all wanted this plant to be a living fossil, a representative of those early times over 400 mya, and we quietly ignored the evidence suggesting that it was related to more advanced plants, until the molecular data placed it as most directly related to the ferns (fig. 2.6). However, studying the physiology of this simple plant did show that this simple growth form severely reduced its capture of light energy and its rate of growth.

The Transition to Leaves These early land plants were small and grew slowly, but they lived under very mild conditions of warm temperatures, a general lack of animals eating them, and with few other plants to compete for resources of light and moisture. They grew slowly because they absorbed light inefficiently, took in water slowly through the fungi that infected their underground stems, and rather easily absorbed carbon dioxide because of its extremely high concentrations in the atmosphere. Examination of stored carbon in fossil

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Figure 2.7 Two early plants with and without leaves. In Sawdonia (top), from about 395 mya, the stems have sharp projections (left and center), and these are without veins leading to the reconstruction (right) (fossil images courtesy of Pat Gensel). In Baragwanathia (bottom) from Australia, as early as 420 mya, the projections did have a single vein and were true leaves. Left, a stem impression; and right, a plant reconstruction from the Victoria Museum in Australia.

soils of those times suggests carbon dioxide concentrations of more than twenty times of that today (which helped to elevate temperatures throughout the planet). Those high temperatures favored the kinds of plant bodies present during those times, with less heat absorbed by the vertical cylindrical shoots. However, over the next 40 million years, new forms of plants appeared that grew taller and competed more effectively for light. Mosses and liver-

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Figure 2.8 Lycophytes. Left, a ground pine; and right, a spike moss.

worts were almost certainly present (but were poorly fossilized) and were limited in size because of their need for water at the tips of shoots where the sex organs were located. Among the vascular plants, more extensive branching allowed for more effective light absorption, as did projections from the stems as well (fig. 2.7). Then the first group of plants with small leaves appeared, the lycopsids— represented today by the ground pines and spike mosses. Such simple leaves could have been derived from the simple projections of photosynthetic tissue or from the spore-producing structures. The earliest of such plants was Baragwanathia (fig. 2.7). These plants produced small leaves in regular arrangements along their stems, in spirals with ground pines and flat planes in spike mosses (fig. 2.8). These generally tiny leaves had a vascular connection with the stem of a single bundle of cells, allowing for some transport of water and nutrients. The surfaces of these leaves were populated with special pores, stomates (p. 185), which regulated the exchange of gases (carbon dioxide, water vapor, and oxygen) between the leaves and the atmosphere. Stomates had appeared earlier on the stems of the earliest land plants. Another evolutionary innovation in these, and other plants, was the establishment of roots. Roots provided a much improved supply of water and nutrients, a prerequisite for the formation of more complex leaves, with their more active physiology. Such

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leaves were an important innovation and supported the growth of much taller plants. The first known forests, excavated in sediment beds of upstate New York State near the village of Gilboa, contained a rooted fern-like tree with densely branched and photosynthetic crowns (but no leaves) along with lycopsid plants with simple leaves. These forests were present around 380 mya, 40 million years after the first vascular plants (fig. 2.9).

Real Leaves Appear Competition for light among early plants led to taller plants, ultimately trees, and also promoted a developmental strategy that produced really large leaves with extensive vascular connections, what we technically call “megaphylls.” Intermediate plants in the evolution of these new organs suggest the changes leading to their formation (fig. 2.10). The first shift was from a strongly three- dimensional occupation of space by the small branches at the tips of the plant into flat two-dimensional planes of branches. Then these flat planes of branches produced outgrowths on the edges to increase the photosynthetic surface. Finally, a single photosynthetic surface with multiple branches (major veins) appeared, a large leaf

Figure 2.9 Early trees. Left, leafless cladoxylid tree from the early Gilboa forests. Center, Lepidodendron, a tree related to the present ground pines and with microphylls. Right, Archeopteris, a widespread tree with fern-like foliage (megaphylls).

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Figure 2.10 Transitions to the formation of megaphylls.

that could spread out and efficiently capture light energy. A consequence of this evolutionary change was that the leaf was supplied by the extensive plumbing (the xylem) of the stem. Coupled with supply from the roots, such leaves were well supplied with water and nutrients, captured light efficiently, and were able to exchange gases through the densely packed pores (the stomates) on the undersurface of the leaf. This novel organ gave such plants a huge advantage in physiology and growth over their ancestors. Extensive forests of such large-leaved plants spread within 40 million years or so after the arrival of the first land plants. One conspicuous member of this flora was the impressive tree, Archaeopteris (fig. 2.9). The photosynthetic capacity of these plants profoundly affected the planet. The high concentrations of carbon dioxide in the atmosphere when land plants first appeared fell rapidly with the appearance of this new vegetation. Temperatures also plummeted, leading to the ice ages at around 400 mya. These leaves and small branches fell to the ground, mixed with minerals, and supported the formation of the first soils. This was a dramatic change, because the soils harbored a rich diversity of bacteria and fungi that processed the nutrients and made them available to other organisms. With the energy sources of the leaves and branches, bacteria evolved that could remove nitrogen from the atmosphere and oxidize it to nitrate, dramatically more than could be produced from lightning storms and such. These nutrients could be used by organisms in the soil— as well as be recycled by the plants— but some of it could be flushed into coastal waters by the out-

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flow of streams and rivers. This might have promoted the growth of algae in coastal waters and harmed some marine animals, as seen in extinction of certain groups at the same time. Another consequence of the deposit of dead plant matter on and in the soils is that in ideal conditions of a lack of oxygen, higher pressure, and higher temperatures, the dead plant materials were turned into coal deposits around 300–320 mya, one of the major sources of carbon fuels we are burning today. The final chapter in the evolution of leaves was the appearance of the highly efficient leaves of the flowering plants (the angiosperms). The high vein densities and efficient plumbing of their leaves allowed more rapid changes of gases, and their higher water loss helped create the climates in which the broad-leaved trees of temperate regions and, particularly, the rainforests of the tropics flourished. These plants originated about 140 mya, and they became dominant after the large extinction event about 65 mya, which also killed off the last dinosaurs. Ever since their appearance, leaves have played a central role in regulating our planet’s climate and in responding to climate changes caused by physical events, such as asteroid impacts and volcanic activity. Today, changes in vegetation (and leaf surface area) due to human activity are integrally involved in the climatic changes we are beginning to experience.

Leaf Structure With this evolutionary background, it is useful to describe the structure of a typical leaf. Leaves of all the different plants I’ll mention— ferns, cycads, conifers, and flowering plants— all share these basic traits. Leaves are first formed from outgrowths of tissue at the tips of plant shoots. The timing of the development of the leaf and the lengthening of the stem determines the position of the leaf, the same pattern within a particular species. In seed plants, the leaf is connected to the stem by multiple bundles of vascular tissue, leaving a gap above the leaf along the stem. Since leaves generally age and die before the rest of the plant, particularly so in longer- lived woody ones, most fall from a zone— of abscission— at the base of the leaf. Leaves typically consist of a connecting structure, the petiole, and the actual blade. In transverse section (fig. 2.11), the anatomical organization of the leaf is revealed. The leaf surfaces are covered by a single-cell layer, the epidermis. These cells secrete a waterproof waxy coating, the cuticle. On the undersurface (or rarely on both sides), stomates appear at high density. Their

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Figure 2.11 Transverse section of a holly fern leaf.

opening and closing regulate the flow of gases in and out of the leaf. The cells of the interior of the blade are photosynthetic, typically of two shapes and positions. Nearest the surface, palisade cells are responsible for most of the photosynthetic activity; chloroplasts crowd the cytoplasm around the central vacuole, and spaces between adjacent cells promote gas exchange. Below is a generally thicker layer of irregularly shaped spongy cells, also photosynthetic. The spaces between these cells promote gas exchange and are connected to the chambers adjacent to the stomates. Amidst the photosynthetic middle are bundles of vascular tissue (the xylem and phloem), or veins. The xylem supplies water and nutrients from the roots to the leaves, and the phloem delivers products of photosynthesis from leaves to different parts of the plant. On the undersurface of the leaf, the stomates, each with two inflatable guard cells, are distributed. Of course, leaves vary enormously in size, shape, edges, patterns of veins, chemical composition, and more. These features will be the subjects of later chapters in the book.

Plants versus Animals To comprehend the differences that divide animals and plants into two groups, it is useful to think of the implications of how these very different

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organisms make a living— that is, harvest energy. Animals may catch prey or eat plants at frequent times during a day. We may grab a quick lunch of a cheeseburger, fries, and a milk shake. The 1,500 calories (or kilocalories) of that meal are about half the daily requirements of a reasonably active adult. We may bolt that down in less than ten minutes, and then spend hours assimilating it in the digestive tract, with projections (or villi) that present an enormous surface for absorbing the digested foods. Other animals may take a large meal at very infrequent intervals, spend a long time digesting and assimilating the food, and then an even longer time fasting and looking for another meal. A spectacular example is an old tropical Asian “friend,” the Burmese python. A large adult snake attains 100 kilograms in weight and 6 meters in length. Such a snake, hungry and waiting, can attack, constrict, and swallow a deer of the same weight in an hour. This deer has the energy value of 600,000 kilocalories, or 400 cheeseburger lunches. To digest this large prey, the snake quickly increases the size of all internal organs, increases the length of intestinal villi, and dramatically increases the internal surface for assimilation. It digests its prey over 2½ weeks, increasing its oxygen consumption to forty times its fasting rate. After six months, the snake may take another large prey. The costs of digestion, along with the efficiency of respiration, yield about 30% energy useful for the organism, a little less efficient than a large electricity power plant. Plants are dependent on sunlight, a much less concentrated source of energy. A square meter of surface in Miami (like a beach umbrella), in midJune when the sun casts no shadow at midday, receives light energy at a heat equivalent of 14.4 calories per minute. Half of that energy is not absorbed by the plant. Furthermore, the efficiency of conversion of the absorbed energy to useful work is about 2% (see p. 60, for an explanation), or onetenth that of the animals. Imagine that your umbrella of 1 square meter captures sun during the day. That solar collector captures around (reduced by clouds and less intensity in the morning and afternoon) 2,300 calories per day. The actual energy yield will be (at 3% efficiency) only 46 calories. It takes a lot of surface area (leaves) to capture energy equivalent to the metabolism of an animal. Thus, a mature street tree might have the metabolism similar in calorie use of a human adult, but can only do so with an enormous surface area for capturing energy, about 150 square meters. Imagine trying to hold up 150 beach umbrellas to the sun at the same time. This surface requires a branch system to display the leaves, and a root system to anchor the plant and absorb water to service the leaves. So, it is not surprising that plants are such immobile creatures. A consequence of stay-

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ing in one place is that plants generally don’t behave to avoid being eaten by animals or to escape the harshness of the physical environment, such as suffering a drought. The cells of plants more ably resist the vagaries of such rapid changes by making cell walls; these prevent the cells from bursting when they receive too much water or collapsing when they desiccate.

Plants and Animals In comparing plants and animals, I have left out the possibility of some sort of compromise between these two groups, so dramatically different from each other. Despite the relative inefficiency of the plant lifestyle and the requirement for such large surfaces for capturing energy, that energy is present every day (except near the poles in the winter) and is “free for the taking,” meaning that it does not require an active expenditure of energy to capture it, only the investment of a surface. Since all organisms have surfaces, why not make those surfaces photosynthetic, to boost the energy capture efficiency in an animal— something like a hybrid automobile with photovoltaic cells on the roof. Perhaps such an opportunity would be seized in natural selection, producing a Yoda-like creature, green and with large ears, for a little photosynthetic boost— an energetically efficient green man. We do have green creatures, an excellent camouflage in animals (I’m thinking of frogs and lizards) that spend a lot of time in foliage. Those animals, however, are not photosynthetic and use yellow pigments obtained from eating plants, at least indirectly, along with cells producing blue color structurally (more about this in chapter 11); thus, yellow and blue produce the green of these animals. The most pervasive partnership that harnesses the metabolisms of photosynthesis (autotrophy) and the consumption of organic food (heterotrophy) is that between certain fungi and green algae or cyanobacteria: lichens, or lichenized fungi. This is such a perfect symbiosis that specialists interested in life on other planets have speculated that lichens might be successful on Mars. The tubular organization of the fungi (the mycelium) is organized into a flat surface or branched structure, and cells of the algae/ cyanobacteria are distributed beneath the surfaces amidst the mycelium. The fungus breaks down carbohydrates in the presence of oxygen, and it produces carbon dioxide and water. It also supplies some nutrients, as phosphorus and nitrogen, to the algae/cyanobacteria. The embedded algae capture sunlight, absorb the water and carbon dioxide, and produce sugars (carbohydrates) along with some oxygen as a by-product. This is a per-

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Figure 2.12 Leaf lichens. Left, a rock tripe from Massachusetts. Right, a freckle pelt lichen from the Cascade Mountains of Washington State.

fectly balanced partnership. Look around in a forest setting, particularly on rocks with some exposure to the sun. You will see lichens that are foliose (foliage-like!). Two leaf-like lichens are the rock tripe, with its flat graygreen photosynthetic surface suspended from a single stalk in the middle and attached to the rock surface, and the green freckle pelt, loosely attached to a rock (fig. 2.12). When I was studying biology in college, the diversity of life was divided between plants and animals, as the two kingdoms of life. This was partly the result of the academic divisions of colleges and universities in those times, of botany and zoology departments. Botanists also claimed the fungi. Some schools had the sense to add microbiology departments. The Plant kingdom was defined by photosynthesis and cell walls, and it included all of the algae, including the reds, browns, and greens, as well as the diatoms, dinoflagellates, and other single-celled photosynthetic organisms. There was one controversial group of single-celled organisms, the euglenoids, claimed by botanists and zoologists. These are elongated single- celled organisms that move around by swiveling flagella at their anterior ends. They have an apparatus for ingesting food particles, and some of them also contain a large chloroplast. So, they are both heterotrophic (feeding on organic material in the environment) and autotrophic (capturing light and photosynthesizing). The revolution in classification, fueled by the rediscovery

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of the symbiont hypothesis, resolved the classification of the euglenoids; it was all a matter of the transformation of a photosynthetic organism into a chloroplast, and endosymbiosis. A few photosynthetic green animals are fascinating for their use of photosynthetic cells and organelles obtained from algae or cyanobacteria. Their photosynthetic activities are the results of symbioses, unusual partnerships between organisms. However, they are not organisms that are photosynthetic by themselves. Hard corals are colonial coelenterate animals that secrete a calcium carbonate matrix that slowly builds the architecture distinct for each coral species. Although corals feed on small organisms in the water, they also rely on a partnership with single-celled algae, dinoflagellates, or zooxanthellae to be more precise. The corals take in the zooxanthellae, which are embedded in the animal hosts near the surfaces of the branches of coral, giving the living coral a yellow-brown appearance due to the pigments in the algal cells. The dinoflagellates obtain carbon dioxide and nutrients from the wastes of the host animal cells, but it is not clear whether this is a true partnership, or more that the corals take advantage of the zooxanthellae. The algae produce oxygen and carbohydrates, and both of the latter are used by the coral polyps, which may obtain the majority of their energy needs from this partnership. When the water temperature rises too high, most strains of the dinoflagellates cannot survive, causing the corals to bleach. If the water does not cool and the corals are not soon repopulated by the photosynthesizers, the entire coral will die. Bleaching and coral death, along with the acidification of seawater, threaten the future of reefs today. Zooxanthellae also partner with other organisms, such as the single- celled radiolarians and foraminiferans. Thus, it is not surprising that such partnerships take on the appearances of trees, with distinct architectures as strategies for capturing light (fig. 2.13; and see chapter 7). Sixteenth-century descriptions of plants often featured corals. Among other interactions between animals and algae, the tiger salamander takes in algae that are associated with its embryos in the gelatinous eggs. The embryos provide nutrients, particularly nitrogen, to help in the growth of the algal cells. In turn, the elevated level of oxygen around the algae benefits the development of the embryos; these have higher survival rates when developing in the presence of algae. So this appears to be a mutually beneficial interaction. The best example of such animal-algal interaction is that between algae and marine sea slugs, with the latter looking very much like leaves (fig. 2.13).

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Figure 2.13 Marine examples of photosynthesis in animals. Top left, photosynthetic sea slug feasting on a bed of green algae (courtesy of Patrick Krug); bottom left, iridescent and photosynthetic mantle of a giant Tridacna clam; and right, coral reef, with coral species of different architectures (courtesy of Walter Goldberg).

These animals move slowly in the shallow waters of coastal regions in many parts of the world, and a particularly well-studied species is found in temperate coastal waters of the eastern United States. They feed almost exclusively on siphonous algae, organisms that are tubular in organization but are essentially single multinucleate cells. These large cells contain numerous chloroplasts distributed throughout the length. The sea slugs (marine gastropods lacking external shells) feed on these algae, digesting all of the cellular material except the chloroplasts. The chloroplasts are stowed away in the numerous side pockets of the sea slug’s digestive system. There they maintain their photosynthetic activity for many months, adding to energy assimilation of the animal. Under optimal conditions, the photosynthetic activity inside the slugs provides all of their energy requirements, and the individuals do not have to take in any food during the year or so of their adult lives. Some of the genetic information necessary for the survival of the chloroplasts, and present in the nucleus of the alga, ends up in the nuclei of cells in the sea slug, a remarkable example of horizontal gene transfer. For instance, the slug actually makes the chlorophyll a molecules that are necessary for photosynthesis, transferring them to the algal chloroplasts in the digestive tract.

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Figure 2.14 Left, Francis Hallé’s drawing of himself with photosynthetic ears (I added the green). Right, three-toed sloth, with green coat from green algae (courtesy of Revital Katznelson).

Another example, this time from a mammal like us, is the three- toed tree sloth from the American tropics. The fur of these odd animals is usually green from colonization by green algae along grooves in the sloth’s hairs. The sloths also are the habitat for a specialist moth that lives in the fur. Once a week, the sloths slowly descend from the crowns of trees, defecate, and then return to the crowns. Biologists at the University of Wisconsin have shown that the sloths eat the algae, an excellent source of nutrition. Furthermore, the moths that live in the fur defecate and die, providing the algae with an important source of nutrients. The moths lay their eggs on the sloth poop, and the larvae develop into adults that fly up into the canopy to find other sloths and move into their furry homes (fig. 2.14). Only a bit of imagination in this brave new world of biotechnology brings us new plant and animal combinations that could turn animal surfaces into leaves, making them solar powered. At the least, this is an inspiration for some good science fiction. Olaf Stapledon imagined a plant man as an erect organism, like ourselves. On his head he bore a vast crest of green plumes, which could be either folded together in the form of a huge tight cobb lettuce, or spread out to catch the light. . . . By day the life of these strange beings was mainly vegetable, by night animal. Every morning, after the long and frigid night, . . . each individual sought out his own root, fixed himself to it, and stood through the torrid day, with leaves outspread. Till sunset he slept, not in a dreamless sleep, but in a sort of trance, the meditative

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and mystical quality of which was to prove in future ages a well of peace for many worlds. . . . When the sun had disappeared once more behind the crags, . . . he would wake, fold up his leaves, close the passages to his roots, detach himself, and go about the business of civilized life.

Perhaps Stapledon’s green man was an inspiration for Tolkien’s Ents (p. 9); Stapledon’s book appeared in 1938, long before the Lord of the Rings trilogy was published. Other authors envisioned viral infections or endosymbionts producing photosynthetic skin (Geoff Ryman and Walter Jon Williams). Francis Hallé (much more about Hallé in chapter 6) drew such a hybrid, of himself with ears like giant Monstera leaves (fig. 2.14), but those ears would supply much less than 1% of his caloric needs, even if he basked in the Mediterranean sun all day. That we are not photosynthetic, and that plants are, makes for a profound divide between us. That is part of our indifference toward them (they are so unlike animals to which we are particularly attached), and yet part of our enormous debt to them.

Chapter Three Green Machinery We have however good reason to be diligent in making further and further researches; for tho’ we can never hope to come to the bottom and first principles of things, yet in so inexhaustible a subject where every the smallest part of this wonderful fabrick is wrought in the most curious and beautiful manner, we need not doubt of having our inquiries rewarded, with some further pleasing discovery; but if this should not be the reward of our diligence, we are however sure of entertaining our minds after the most agreeable manner, by seeing in everything, with surprising delight, such plain signatures of the wonderful hand of the Divine Architect, as must necessarily dispose and carry our thoughts to an act of adoration, the best and noblest employment and entertainment of the mind. stephen hales, Vegetable Staticks

a loud decree of missing greens, trees looking for their quench of fiery wet, lusting infinity that runs clear and bright light, of an unsavored heaven. filling up on meaningless quench. waiting for the deepest inspiration. to reach reach and reach and then to bow, sway of mirth below the earth. above the towered clouds. growing with muted abstinence— dancing a viral glee. Awaiting the hour of sungazing safety, of something new. robin ross, “Trees with the Hidden Gold”

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W

e owe our lives to leaves. The carbon atoms produced by exploding stars billions of years ago mostly enter organisms through leaves to become the backbones of all of the molecules that make life possible. Leaves account for about half of the carbon dioxide fixed via the process of photosynthesis; the vast oceans account for a bit less, but most of the carbon in us as terrestrial animals arrives via leaves. The carbon molecules in the meat we consume (as a cheeseburger, p. 36) are derived from plants. Michael Pollan has written that about 60% of the carbon consumed in a Burger King meal is ultimately derived from the carbon dioxide fixed by maize plants. Despite the importance of leaves in the provision of carbon, our understanding of their function was gained rather recently, and the history of the discovery of photosynthesis is a story embedded in the revolutions of scientific understanding that emerged during the Renaissance.

The History of Green Machinery We began to learn about the function of leaves late in the eighteenth century. Photosynthesis is a biological and chemical process, and understanding it has relied on discoveries in chemistry. Actually, discoveries with leaves helped establish the emergence of the science of chemistry early in the nineteenth century. That chemical understanding was thwarted by the persistence of ancient ideas about the construction of the world. The Greeks believed that the world consisted of four elements: earth, water, air, and fire— sometimes adding ether as a fifth one. Similar concepts were held by the Babylonians, Egyptians, and in ancient India, and were accepted by Europeans through the Middle Ages and into the Renaissance. Another concept was added in the sixteenth century, that of phlogiston, a substance in air that was consumed in combustion. Phlogiston was a big stumbling block to the understanding of chemical elements and of photosynthesis. Theophrastus, the father of botany, never mentioned any function for leaves. This was not for a lack of observation, for he described the variations of size and form in detail, particularly in relation to the ecology of certain plants. He did not feel, as his mentor Aristotle did, that the function of leaves was to benefit humans. Perhaps he believed that the understanding of function would slowly emerge through continued and careful observation. From Theophrastus on, scholars often compared plants and animals, trying to find similarities in form and function between these very

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Figure 3.1 Early students of plant physiology. Left, portrait of Jan Baptista van Helmont. Center, portrait of Stephen Hales. Right, Hales’s experiment on water flow in a plant.

different organisms. However, until the seventeenth century, no experimentation informed any of these opinions. William Harvey (1578–1657), an English physician, reported on the circulation of blood in 1628. Harvey’s discovery influenced later research in plants. In 1648 the Flemish physician Jan Baptista van Helmont (1577– 1644; fig. 3.1) published the results of an experiment with a willow seedling, keeping track of the mass of the soil and plant during its five- year period of growth. He demonstrated a substantial increase in the mass of the plant (about 46 kilograms), and yet an almost imperceptible loss of mass in the soil (of 57 grams), putting into doubt the Greek understanding of soil as the source of food responsible for plant growth. Helmont helped establish a field of study, pneumatic chemistry, which inspired research on plants in the eighteenth century. How do plants grow, and what roles do leaves play in this process? Partial answers to these questions were found in the remarkable researches of two English clergymen, Stephen Hales and Joseph Priestley. Hales (1677– 1761) studied at Cambridge and was influenced by Isaac Newton, completing a master of arts degree in 1703 (fig. 3.1). He stayed at Cambridge until 1709, when he became the Curate of Teddington in Middlesex for the rest of his life. There he experimented on the physiology of animals and plants. Following Harvey, he is perhaps best known for his studies of blood circulation, being the first to measure blood pressure. His parallel studies on

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plants were devoted to understanding the flows of fluid and gas, involving ingenious means of measuring pressures and volumes of fluids and gases. He developed a technique for collecting gases, the pneumatic trough, used by scientists in later decades. In 1727 Hales published Vegetable Staticks (the latter word signifying the accurate measurement of gases, fluids, and materials), the first book in plant physiology. In it he described experiments showing that leaves were the site of “perspiration” (what we now call transpiration) of large quantities of water out of the plant, that stems generate pressures to move sap, and that plants produce gases. He suggested that a function of leaves was to move water through and out of the plant. Throughout his career he was influenced by the writings of Newton, whom he quoted in the plant text: “Are not gross bodies and Light convertible into one and another? And may not bodies receive much of their activity from the particles of Light, which enter their composition? The change of bodies into light, and of light into bodies, is very informable to the course of nature, which seems delighted with transmutations.” Hales was inducted into the Royal Society of London (established in 1660 and the most influential scientific society of the eighteenth century), and he received the Copley Medal— the society’s most distinguished honor— in 1739. Yet Hales knew nothing of photosynthesis. Hales’s simple observation of the production of gas bubbles by plants was further studied by Charles Bonnet (1720–1793) and described in his Recherches sur l’usage des feuilles dans les plantes (1754). Bonnet observed these bubbles coming from the undersurfaces of aquatic plants and speculated that in addition to the leaf’s supporting the movement of fluids in the plant, leaves also promoted the intake of gases into the plant. It fell to a more renegade and less affluent clergyman than Hales, Joseph Priestley (1733–1804), to make the observation that opened the door to a revolution in our understanding of plants and chemistry (fig. 3.2). Priestley was born in Yorkshire in 1733. He came from a family of dissenting Christians, and he wrote about Christian doctrine and theology for much of his life. He became interested in science first as a schoolboy and then as an instructor at Warrington Academy. His writings on electricity attracted the interest of Benjamin Franklin, and he was elected to the Royal Society in 1767. However, his legacy is his work on air, Experiments and Observations on Different Kinds of Air (1774–86), published by the Royal Society. It was completed while he lived in Birmingham; there he became a member of the Lunar Society, where he met Erasmus Darwin (p. 49). Priestley knew about the experiments of the Scotsman Joseph Black (1728– 1799), who

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Figure 3.2 Joseph Priestley. Left, his portrait; right, the pneumatic trough used in his experiments on gases.

had shown that animals and candles altered a closed volume of air, extinguishing a flame and suffocating other animals. Black called this changed air “fixed,” a term used by Priestley and other scientists. In his experiments on gases, Priestley showed the means by which they could be collected. He adopted the technique of Hales’s pneumatic trough (fig. 3.2). In a critical experiment, he showed that plants produce a substance that enable a candle to burn (or a mouse to live longer) from fixed gas. He collected the air in which the candle was extinguished and the mouse perished, and put the sprig of a mint plant in the enclosure: I took a quantity of air, made thoroughly noxious, by mice breathing and dying in it, and divided it into two parts; one of which I put into a phial immersed in water; and to the other (which was contained in a glass jar, standing in water), I put in a sprig of mint. This was about the beginning of August 1771, and after eight or nine days, I found that the mouse lived perfectly well in that part of the air in which the sprig of mint had grown, but died when it was put into the same original quantity of air; and which I had kept in the very same exposure, but without any plant growing in it.

Priestley’s simple observations precipitated a revolution. He did not capitalize on them very much; there were some complications in his results (green algae growing in the water, for one) that he never resolved.

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Furthermore, he referred to the air refreshed by plants as phlogistonized, an understanding that stood in the way of truth in these matters. Priestley received the Royal Society’s Copley Medal in 1773. At that ceremony, his friend John Pringle said: “From these discoveries, we are assured that no vegetable grows in vain, but that, from the oak of the forest to the grass in the field, every individual plant is serviceable to mankind; if not always distinguished by some private virtue, yet making a part of the whole which cleanses and purifies our atmosphere.” Priestley had been a supporter of the American cause for independence and later supported the French Revolution. These opinions, along with his controversial theological writings, forced his emigration to the United States in 1791. He ceased scientific experimentation, but he continued to write on theology and helped to establish the Unitarian Church in the United States. He became friends with eminent Americans, including John Adams and Thomas Jefferson, and he died in Northumberland (in central Pennsylvania) in 1804. Priestley’s results quickly came to the attention of Antoine Lavoisier (1743–1794), an eminent French scientist and the father of modern chemistry. Priestley visited Lavoisier in Paris, and he shared the results of his experiments on gases. To Lavoisier, Priestley’s results indicated that there were two gases making up air, one (which he later named oxygen) responsible for the combustion by the candle that was replaced by the activity of the plant, and another inert gas he named azote (later called nitrogen). He thus disproved the phlogiston theory assumed by Priestley and others. He wrote about these ideas as part of a new system of chemistry, relying on the experimental results of others, in the first chemistry textbook, Traité élémentaire de chimie (1789); he is widely heralded as the father of chemistry. Tragically, he was wrongly accused of treason during the year of terror of the French Revolution and was beheaded in 1794 at the height of his scientific powers. Priestley’s discovery was also quickly taken by the Dutch physician and scientist Jan Ingen-Housz (1730–1799) to extend the understanding of the production of oxygen by plants, published in a book, Experiments upon Vegetables, in 1779. He duplicated many of Priestley’s results and conducted other experiments to resolve some of the problems in the Englishman’s results. He showed that plants under water produced bubbles of dephlogisticated air (soon to be called oxygen). He showed that this gas production required light. In the absence of light, plants produced fixed air (later to be called carbon dioxide) but in much smaller amounts than the oxygen produced in light. He also showed that only the green parts of plants produced oxygen.

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He thus demonstrated that some of the gain in weight of plants was due to the uptake of gases. Soon discoveries in chemistry identified fixed air as containing carbon dioxide, and dephlogisticated air as containing oxygen. Priestley’s Lunar Society friend Erasmus Darwin celebrated the discoveries of these three great scientists in his long poem, The Botanic Garden (1789): sylphs! from each sun-bright leaf, that twinkling shakes O’er Earth’s green lap, or shoots amid her lakes, Your playful bands with simpering lips invite, And wed the enamour’d oxygene to light.— Round their white necks with fingers interwove, Cling the fond Pair with unabating love; Hand link’d in hand on buoyant step they rise, And soar and glisten in unclouded skies. Whence in bright floods the vital air expands, And with concentric spheres involves the lands; Pervades the swarming seas, and heaving earths, Where teeming Nature broods her myriad births; Fills the fine lungs of all that breathe or bud, Warms the new heart, and dyes the gushing blood.

Other important discoveries followed in the nineteenth century. Jean Senebier, a Swiss pastor and botanist, showed that green plant tissues, particularly leaves, simultaneously evolved oxygen and took up carbon dioxide in the presence of light. In 1804 the Swiss botanist Nicolas-Théodore de Saussure wrote that the amount of carbon dioxide taken up by plants was approximately equal to the oxygen produced, that the increase in plant mass was due in part to the increase in carbon from carbon dioxide, and in part due to the uptake of water. Thus, in three decades or so after Priestley’s discovery, the basic outline of photosynthesis had been established, as understood by a fifth-grade student today. That the respiration processes in animals also took place in plants, first reported by William Cruikshank (1745– 1800) in 1797, was quickly amplified by Ingen-Housz. His caution led to a more alarmist concern later in the nineteenth century about the danger of plants in the bedrooms of Victorian homes, where keeping tropical plants had become fashionable (p. 20). Edward Kemp wrote in 1851, in his Handbook of Gardening, “Plants convert the oxygen and carbon which they receive from the soil and air into carbonic acid, while they exhale at night. This being a deadly and dan-

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Figure 3.3 Andreas Schimper’s discovery of the chloroplast. Left, his photograph; right, an illustration of chloroplasts in a plant cell, from his 1885 publication.

gerous gas to human beings, plants and flowers are not considered healthy in a sitting or bed room during the night.” This suspicion lingered, but as Ingen-Housz had advised, it would take a lot of plants and a tightly sealed room for any effect to be felt. With the improvement of microscopy as a tool for biological research, the cellular basis of photosynthesis was revealed. In the seventeenth century, both the anatomist Nehemiah Grew and the microscopist Antonie van Leeuwenhoek (1632–1723) had observed small green bodies in plant cells but had not named them. The pigment chlorophyll (Greek chloros-, for green, and -phyll, for of the leaf ) was first extracted and isolated in 1817 by two French pharmaceutical chemists, Pierre-Joseph Pelletier (1788– 1842) and Joseph Bienaimé Caventou (1795–1877). Although many scientists observed and described chloroplasts, the actual name of this organelle (Greek chloros-, for green, and -plastis, for the one who forms) was proposed by the French Alsatian botanist Andreas Schimper (1856–1901) in 1885 (fig. 3.3). Schimper began his career as a cell biologist and worked for many years in the laboratory of the great Eduard Strasburger, where he studied chloroplasts. He worked at Johns Hopkins University in 1880, and from there he traveled to Florida and then the Caribbean. This began his interest in plants of the tropics (p. 69). He traveled in Asia, including a stay at the famous Foreigner’s Laboratory in Bogor. He died of malaria in Cameroon at forty-five years of age. For all of this time, there was not a proper name for the process of fixing carbon. “Assimilation” was commonly used, but that also described the digestion of food in animals. The word “photosynthesis” was proposed as late as 1893 by the American botanist Charles Barnes. It caught on quickly,

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Figure 3.4 The structure of chlorophyll.

although Barnes preferred the word “photosyntax.” The structure of chlorophyll (fig. 3.4) was determined by the eminent German organic chemist Richard Willstätter (1872–1942) in 1913, for which he received the Nobel Prize in Chemistry.

The Black Box At the beginning of the twentieth century, we knew photosynthesis as 6CO2 + 6H2O + light → C6H12O6 + 6O2 We also knew that chlorophyll was required, and the process took place in chloroplasts (fig. 3.5), but the chloroplast was essentially a black box. During that century, leading up to the present, thousands of researchers publishing tens of thousands of scientific articles have steadily opened up that box to reveal its inner workings, and the model for photosynthesis is outlined in the following paragraphs. The structure of the chloroplast was revealed through electron micros-

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Figure 3.5 Left, transverse section of a spinach leaf with chloroplasts. Right, ultrastructure of a chloroplast (both courtesy of Brian Gunning).

copy, after World War II (fig. 3.5). The photosynthetic cells of a typical leaf hold 20–50 of these organelles, all in the cytoplasm surrounding the large central vacuole. Chloroplasts are about 5 microns long and 2 microns wide, and are bound by two membranes. Within, there is a single loop of DNA, which contains the information for 50 or so genes. Remember that chloroplasts are the end process of the endosymbiosis of a free-living cyanobacterium into a host cell (p. 25), and most of the genes of the cyanobacterial ancestor have been transferred to the nucleus of the host cell. Thus, most of the components of the green machine are produced in the cell from information stored in the nucleus. Much of the volume of the chloroplast is taken up by an internal membrane, the thylakoid, which is organized in stacks (which can be envisaged as a pile of pancakes) termed grana, and connected by single thylakoids that stretch across the interior of the chloroplast, as the stroma. Progress in understanding the biochemistry of photosynthesis has ultimately meant locating the individual steps in parts of the chloroplast.

Light and Dark A better physical understanding of light produced a better understanding of photosynthesis. Theodor Wilhelm Engelmann (1843–1909) used a prism to produce a spectrum of visible radiation to determine of the sensitivity of photosynthetic responses of a filamentous alga to different wavelengths of light. Serendipitously, Engelmann observed that oxygen-consuming bacte-

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Figure 3.6 Theodor Englemann’s algal experiment, determining the action spectrum of photosynthesis (courtesy of Holly Gorton and the American Society for Photobiology).

ria were attracted to portions of the filaments, particularly in the red and blue regions, where oxygen evolution was greatest (fig. 3.6). Counting the density of bacteria along the prism was an indirect means of measuring the extent of photosynthesis, producing the first action spectrum. Pulses of light were also used to investigate the process. The discovery that flashes of light could decouple parts of the process led the English physiologist Frederick Frost Blackman (1866–1947) to determine that the light reaction was little affected by temperature, compared to the dark reaction. The discovery of light and dark reactions in photosynthesis was the first opening of the black box, allowing the gradual dissection of the components of the process. Blackman’s results influenced the German physiologist Otto Warburg (1883–1970) to work on photosynthesis for part of his illustrious career. Warburg published papers in 1919–23 that established new quantitative techniques of measurement to estimate the efficiency and the effects of wavelength on photosynthesis.

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In 1925 a young American scientist, Robert Emerson (1903– 1959), was attracted to study in Germany, which had emerged as the best place for the study of physiology. He joined Otto Warburg in Berlin. After returning to the United States, he built an illustrious career in the study of photosynthesis. His most important discovery, among many, was that the light reaction consisted of at least two components. He conducted careful experiments on the effects of wavelengths of light on photosynthesis, and he observed that the extent of photosynthesis dropped abruptly above 680 nm, even though chlorophyll absorbed light well above that wavelength. However, if he used two sources of light, one at 680 nm and another at 700 nm, the rate was greater than the two wavelengths separately. He also observed a drop in photosynthesis with a single source of light below 660 nm that was increased much more than the total of the two, when he added a separate source at longer wavelengths. Emerson rightly concluded that the light reaction consisted of at least two systems, one activated at shorter wavelengths (photosystem I, or PSI) and one activated at longer wavelengths (photosystem II, or PSII). This model opened up research leading to our present understanding of the light reaction.

Radioisotopes Nuclear physics helped open the black box of photosynthesis with the discovery of isotopes in the 1930s. Isotopes are atoms of an element with the same atomic number and charge, but with different atomic weights, due to the addition or loss of neutrons in the nucleus. Oxygen 18 (18O) is a stable isotope with two extra neutrons, and does not emit radioactivity. Others break down into another isotope, or even another element, releasing radioactivity as high-energy decay particles. During World War II, the U.S. government set up government laboratories for the production and study of radioisotopes; one associated with the University of California, Berkeley, was headed by Ernest Lawrence. In 1937 he hired two young scientists, Samuel Ruben and Martin Kamen. They used radioisotopes as powerful tools in solving research problems in photosynthesis. It was at the ceremony for Lawrence’s Nobel Prize that Ruben and Kamen’s discovery of carbon 14 (14C) was announced. Its moderate rate of decay made it ideal for tracing pathways in which carbon compounds were involved, as well as for dating artifacts in human history. Ruben and Kamen used isotopes to make two fundamental discoveries in photosynthesis. Ruben reasoned that if 14CO2 were administered to a plant, the ra-

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dioactivity should show up in all of the carbon atoms of a glucose molecule, which they demonstrated. Kamen used the stable isotope 18O to show that the oxygen produced in photosynthesis was derived from water and not carbon dioxide. Their partnership was short-lived, however; Ruben tragically died from work-related exposure to phosgene gas at the age of twenty-nine. To trace the details of the pathway of carbon into the plant, it was necessary to adapt techniques of rapid inoculation of the isotope, short incubation periods, and rapid killing of the cells. Under the leadership of Melvin Calvin (1911–1997), at the Lawrence Laboratory, these problems were solved and the intricacies of the pathway were revealed. Calvin worked with Andrew Benson (1917–2015), who coauthored most of the important articles with Calvin, and then James Bassham (1922–2012) who completed his PhD with this research and published later papers with Calvin. For this accomplishment, Calvin received the Nobel Prize for Chemistry in 1961. Surprisingly, the first intermediate in the pathway to carry the label was a 3-carbon acid, phosphoglyceric acid (PGA). Soon Calvin and colleagues discovered that a 5-carbon sugar, ribulose bisphosphate (RuBP) was the molecule to which the labeled carbon was attached. Various other reactions can regenerate this molecule, and six such additions produce the equivalent of a single molecule of glucose, C6H12O6 (fig. 3.7). These discoveries

Figure 3.7 The fixation of carbon and products of the dark reaction.

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revealed other problems, such as isolating the enzymes involved in fixing of carbon, and the sources of energy driving the process.

Putting It Together: The Z-Scheme and the Chloroplast How does the energy of light produce sugars? According to quantum theory, we can look at light (electromagnetic radiation) in two ways: (1) as a particle, or photon; and (2) as a wave propagated through space. Thus, the photons have particular wavelengths and increase in energy with shorter wavelengths. It is useful to view light as photons, because these particles physically interact with chlorophyll molecules. The process by which light energy is converted to chemical energy is known as the Z-scheme (fig. 3.8), and our understanding of this process has unfolded over the past sixty years, particularly from the study of algae, and by using mutants (see p. 116) deficient in parts of the photosynthetic mechanism. Photosynthesis occurs with a single chlorophyll molecule receiving the energy of a single photon, exciting an electron that leaves the chlorophyll molecule (fig. 3.8). This electron moves through an electron transport path-

Figure 3.8 The Z-scheme and light reaction in relation to chloroplast structure.

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way of four intermediates, from higher to lower energy. This circuit uses the energy of the electron flow to pump hydrogen ions (H+) from the outside of the thylakoid membrane in the chloroplast grana to the inside. The acidity of the interior of these hollow membrane vesicles increases. This difference in charge and acidity are the forms of energy that activate an enzyme that converts adenosine diphosphate (ADP) and a phosphate ion to adenosine triphosphate (ATP). This high-energy compound (we can think of it as the most common energy currency) is coupled to many reactions in the cell and is used to drive the dark reaction of photosynthesis. This mechanism was unknown until the 1960s when the chemiosmotic theory was proposed by Peter Mitchell (1920–1992), a British scientist who received a Nobel Prize in Chemistry in 1978, explaining both the production of ATP in mitochondria (respiration) and in chloroplasts (photosynthesis). Chlorophyll is organized into light- harvesting complexes (LHC), consisting of many proteins and pigments, including chlorophylls a and b, and carotenoids. These are antennae that feed energy into the light reaction centers. The light reaction center of photosystem II (or P680) splits a molecule of water, H2O, yielding an atom of oxygen, two hydrogen atoms, and two electrons. The electrons are passed through the circuit described above, and the hydrogen ions are pumped across the membrane to provide energy for the formation of ATP. The antennae, chlorophyll molecules, and electron transport chain are located on the surface of the thylakoids of the grana stacks. This partly de-energized electron is taken by the active chlorophyll molecule of photosystem I (or P700), energized by its light-harvesting complexes, which has two paths of electron flow. The predominant path has three acceptors and terminates in the addition of two electrons and two hydrogen ions to another energy carrier, NADP (nicotinamide adenine dinucleotide phosphate), to form two molecules of NADPH. There is also a cyclic electron flow that results in the production of some ATP. The antenna and action center of this photosystem, along with the acceptors, are located on the surfaces of the membranes of the thylakoids in the stroma (fig. 3.8). The details of this pathway have been worked out, and are still being studied, by hundreds of scientists performing very elegant, I would say beautiful, research— too many to be acknowledged in my summary. However, I would be remiss not to mention the research of Jan Anderson, a New Zealand plant biologist, in physically locating the components of the light reaction on the chloroplast membranes. The light reaction requires a balance of energy supplied to both photosystems for optimal efficiency, and the ratios of the two systems in a

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Figure 3.9 The products of photosynthesis and their fates.

chloroplast (and the thickness of the grana stacks) are altered by different spectral qualities of light. Back to the dark reaction. The enzymes that catalyze the reactions producing glucose, and even the chains of glucose— or starch— are located in the liquid portion of the chloroplast, or the stroma. The limiting step in the dark reaction is a large, slow-acting enzyme of many subunits that attaches a carbon dioxide molecule to a 5-carbon sugar: ribulose bisphosphate carboxylase (or RuBisCO— sounds a little like a breakfast cereal). This is the most abundant protein on our planet (and chlorophyll is also the most abundant pigment). If the oxygen concentration increases, the enzyme converts the sugar to 2- and 3-carbon compounds, reducing its carboxylase activity. The ATP and NADPH produced in the light reaction provide energy for various reactions in the dark cycle. The summary of these requirements are 6 CO2 + 6RUBP + 18 ATP + 12 NADPH → C6H12O6 (glucose) + 18 ADP + 16 Pi + 12 NADP Glucose, the 6-carbon sugar molecule, is central to the fate of carbon within the plant (fig. 3.9). Glucose can be stored within the chloroplast

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Figure 3.10 Protein interactions in a plant cell: an interactome. It shows the proteins involved in the metabolism and action of abscisic acid (ABA), a plant growth regulator, permission of Developmental Cell.

or stored as starch— a simple polymer of this sugar— in special plastids in other parts of the plant. Starch can later be broken down to release the glucose, which can quickly be converted to other molecules in the cell, such as amino acids, et cetera. Glucose can be efficiently moved (translocated) from leaves to different parts of the plant as the very stable 2-sugar molecule, sucrose— or table sugar. This involves the simple conversion of glucose to fructose and the joining of these two molecules. The majority of carbon fixed through photosynthesis ends up as cellulose, surrounding every plant cell. Cellulose is also a polymer of glucose, but the linkages are different and very resistant to breakdown. Cellulose is indigestible fiber in our diet. However, some organisms— such as bacteria, fungi, termites, and cockroaches— can digest cellulose. Despite the dramatic breakthroughs in our understanding of the process in the past sixty years, and despite the details of the green machine that I have just outlined, there is much more to be learned. What are the mechanisms by which the enzymes operate, their three-dimensional structures, the ways that different enzymes may form complexes to operate together more efficiently, the details of the components of electron transport on membranes, and interactions of the hundreds of proteins within the cell (fig. 3.10)?

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Efficiency The energy content of these compounds and of photons can be used to calculate the overall efficiency of the process. Exposing a portion of a leaf to a beam of light (of a wavelength usable in photosynthesis) under optimal conditions allows the measurement of photosynthesis (as the production of O2 or consumption of CO2 ) in response to varying intensities, producing a light response curve (fig. 3.11). In such a curve, carbon dioxide is released in darkness (respiration) and reaches a compensation point under dim light. Response then increases with more light intensity, in a linear slope that reflects the optimal efficiency of the process. At higher intensities, the slope flattens out and reaches a maximum (saturation point) and may even decline under full sunlight. In ideal conditions, eight active photons provide energy for the capture of one carbon. This allows the simple estimation of the optimal efficiency of photosynthesis, as the energy value of forty- eight active photons (or 2,285 kcal, the energy currency, p. 36) in relationship to the energy value of glucose in its conversion to carbon dioxide (684 kcal), or 684/2,285 = 30%. That is high, but less than the maximal energy efficiency of the “burning” of glucose in aerobic respiration, of 38%— and also less than the 40% of an electricity-generating gas turbine. In photosynthesis, many factors reduce this efficiency to low values, of 2% or less (fig. 3.12). First, almost half (47%) of solar electromagnetic radiation is not in a range to be absorbed by chlorophyll in leaves. Second,

Figure 3.11 Photosynthetic light response curve.

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Figure 3.12 Factors limiting the efficiency of photosynthesis.

15% of the visible and photosynthetic range is transmitted through, or reflected by, leaves. After all, leaves look green from reflected and transmitted light. Third, most plants are saturated by low levels (10– 30%) of sunlight. Most of that portion is absorbed, converted to heat, and re-radiated. Much of that heat is also lost through the evaporation of water, in transpiration. High light intensities promote the oxidase activity of the RuBisCO enzyme, reducing carbon uptake, and high light may inactivate the light reaction through photoinhibition. Finally, some light is not absorbed by plants, because of leaf orientation and placement, and passes through the foliage. Most plants use about 1% of the solar energy, or even less. Our best estimates are from crop plants, where the production is a commodity (as oil or cane sugar) that is only part of the total plant growth, and efficiencies approach 2%. Typically, around half of the carbon taken up in photosynthesis is released by plants in respiration, occurring day and night. Our reliance on plants for food and other products has stimulated much research to increase that efficiency. So far, photosynthesis has not been elevated in any crop plant, improvements in yield coming in other ways. There still is hope for tweaking the process through better understanding of its regulation— but it will take time. A weak link in the process is RuBisCO, and research is aimed at increasing its efficiency without upsetting the delicate interactions with other proteins. The process has also inspired research in photonics (making devices that use or produce light) and materials science to produce artificial leaves. For instance, Dan Nocera, presently at Harvard, and his colleagues developed a catalyst that, on a film, absorbs

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light and splits water, producing hydrogen and oxygen gas— much like a leaf. Another approach is to modify chloroplast function by using carbon nanotubes inserted in the chloroplast to introduce catalysts and other molecules to improve the efficiency of photosynthesis. Nocera and colleagues recently combined portions of the light reaction to produce hybrid fuel cells.

Plasticity and Adaptation Leaves function in many habitats. Determined by their general shape, size, and structure, leaves within species develop characteristics that improve function in particular environments— such as a species that starts out in deep shade and emerges into sunlight. In shade, leaves are often larger, lobed less, and thinner than leaves developed in sun (fig. 3.13). Thicker leaves have more internal photosynthetic tissue to handle more light. In shade, leaves use the cues of low light and changes in light quality produced by surrounding leaves to alter the balance of pigments between the two light-harvesting complexes, grana thickness, and leaf anatomy. Leaves in the sun increase the density of stomates, for higher rates of gas exchange (p. 186). Even with such acclimation, leaves in full sun may close their stomata and shut down photosynthesis in the heat of midday. Leaves, both within and between species, vary in the thickness of the mesophyll (p. 35), the shapes of cells, and the degree and shapes of air spaces. These anatomical differences affect two aspects of leaf function.

Figure 3.13 Leaf anatomical plasticity in sun (left) and shade (right) leaves in the merawan tree, of Southeast Asian forests.

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Figure 3.14 Examples of the anatomy of leaves from different environments. Left, monkey plant, tropical rainforest shade; center, a light and drought-adapted plant, oleander (p. 317); right, hot and dry climate grass, sugarcane.

Vertical air spaces and columnar cells (with a large vacuole in the center of each) allow for light to better penetrate into the interior of the cells exposing deeper cells to light for photosynthesis (fig. 3.14). This effect is aided by the location of pigments in plastids; these spaces may allow for light to penetrate (a sieving effect). Air spaces cause the light to scatter within the interior, increasing the likelihood that wavelengths weakly absorbed by pigments (as the green wavelengths) will be more effectively absorbed (a path-lengthening effect). These spaces also promote the exchange of CO2 into and O2 out of the photosynthetic cells. In plants adapted to extreme shade, the chloroplasts are often densely located in a single layer (reducing the sieving effect), and air spaces are reduced in extent (fig. 3.14). These anatomical features and their plasticity have been important in increasing the photosynthetic capacity of terrestrial plants, compared to their aquatic and green algal ancestors. These traits have generally been neglected by materials scientists using organisms as models (the research described as “biomimicry” and “bioinspiration,” p. 180). However, Tongxiang Fan and colleagues at Shanghai Jiaotong University have duplicated the threedimensional structure of leaves and shown that photochemical activity can be enhanced on those internal surfaces. In desert plants, as well as those of hot dry grasslands from the tropics, a remarkable metabolic adaptation has appeared many times: the initial uptake of carbon dioxide on a 3-carbon molecule to produce a 4-carbon compound (fig. 3.14). The products of this fixation are organic acids, malate and aspartate. The fixation takes extra ATP, so is metabolically costly. However, the crucial enzyme, PEP carboxylase, has a much stronger attraction to CO2 than RuBisCO and can pull that gas into the cell more efficiently.

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For tropical grasses (and two good and well- studied examples are maize and sugarcane) the stomates open less and reduce the loss of water. Cells adjacent to the photosynthetic cells fix the CO2 and deliver the malate or aspartate to the photosynthetic cells, where the CO2 is removed and delivered to the chloroplasts; the separation is spatial. For desert plants (and orchids and bromeliads growing on high branches in tropical rainforests), the stomates open at night when temperatures lower and relative humidity increases, dramatically reducing water loss. Since this process was first discovered in alpine stonecrop succulent plants (in the genus Crassula), it was named crassulacean acid metabolism, or CAM for short. Humboldt made some remarkable early observations on these plants during his stay at Lake Valencia, in Venezuela (p. 77). He noticed that leaves of the pitch apple did not produce gas bubbles when immersed in water in sunlight, as ordinary leaves would. However, he also noted the exudation of oxygen- rich bubbles pushed out of the petiole of these leaves under water. His observations were consistent with our modern understanding of the process. Cells in the succulent leaves store the 4-carbon acids at night and produce high concentrations of CO2 in the leaves during the day, when photosynthesis occurs with the stomata shut; the separation is chronological. In many aquatic plants, where water limits the rate of diffusion of CO2 into leaves, a variant of this physiological adaptation occurs. Perhaps the most spectacular succulent plants with this adaptation are the living stones of South African deserts, where the leaves are under soil except for the small stonelike portions at the soil surface among similarly appearing rocks, with uptake of CO2 at night and the penetration of light into the leaves and under the soil surface during the day (fig. 3.15)

Design and the Green Machinery “Green machinery” (the chapter title) evokes the views of scientists during the Renaissance who saw physiological processes as constructions of the divine designer. In biology these days, using words such as “machine” (or even “mechanism”) has become controversial because of the rise of the intelligent design movement, on the heels of an earlier creationist push. Yet because designing is part of our humanity (p. 302), it is natural for us to think of physiological processes in such terms. Before the Renaissance, our lack of comprehension of the physical world (e.g., the five elements of creation) made it impossible to even think of a function of leaves. However, during the Renaissance, as scientists conducted experiments on plants, we began

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Figure 3.15 CAM plants. Left, a living stone from South Africa (Lithops optica); right, sections through the plant.

to see the ideas of intelligent design in their writings. It was particularly natural for Stephen Hales and Joseph Priestley to use such a vocabulary because both were clergymen, but similar statements were also made by others. In the nineteenth century, the dialogue changed. With the theory of natural selection by Darwin and Wallace, the injection of a “superior intelligence” or “designer” into discussions of function in biology went to the back burner. We now see the evolution of adaptations for capturing light energy to drive processes in the cell and organism beginning soon after the origin of life, over 3 billion years ago— plenty of time for the beautiful and elaborate green machinery of leaves to have appeared. I am impressed by the passion and dedication of those who have moved our understanding of photosynthesis forward during the last three centuries. I am reminded of what Albert Einstein wrote about the motivation of scientists to learn about the unknown. I have never imputed to Nature a purpose or a goal, or anything that could be understood as anthropomorphic. What I see in Nature is a magnificent structure that can be comprehended only very imperfectly, and that must fill the thinking person with a feeling of humility

Einstein believed that scientists shared a conviction about the rationality of the universe and the possibility of its comprehension. Immersion in its details gave him a “cosmic religious feeling,” which was a noble motive for conducting scientific research. The elegance of the green machinery, so essential for life and human welfare, inspires such a feeling.

Chapter Four Nature’s Fabric See dying vegetables life sustain, See life dissolving vegetate again: All forms that perish other forms supply, (By turns we catch the vital breath, and die,) Like bubbles on the sea of Matter born, They rise, they break, and to that sea return. alexander pope, “An Essay on Man”

But why not play it cool? Why not survive By Nature’s laws that still keep us alive? Let us enlighten, then, our earthly burdens By going back to school, this time in gardens That burn no hotter than the summer day. By birth and growth, ripeness, death and decay, By goods that bind us to all living things, Life of our life, the garden lives and sings. The Wheel of Life, delight, the fact of wonder. wendell berry, “A Speech to the Garden Club of America”

T

hat distinct green tinge covering much of Earth’s land surface, seen from outer space, shouldn’t be a surprise; the green color is due to a continuous layer of leaves over much of the land. The annual production of leaves on the land surface (and even a bit under water) is enormous. At around 39 billion tons per year, it is about the same mass as our extraction of petroleum. Understanding the contributions of leaves to all of life and the · 66 ·

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Figure 4.1 NDVI image of the planet Earth. The degree of greenness corresponds to the density of foliage on our planet (courtesy of NASA).

global climate, an important task, means shifting up from the function of individual leaves, to communities and the entire planet. The images that best document this green layer of leaves, what I’m calling “nature’s fabric,” are from satellites with special cameras that detect the amount of chlorophyll as a substitute for the leaves (the normalized difference vegetation index, or NDVI; fig. 4.1). They show the darkest colors and thickest layering of leaves in the humid tropics and moist temperate regions, the lightest shades where deserts appear, and no color at all from permanent ice and snow. The values for NDVI are strongly correlated with the thickness of the leaf layers on the ground, as the layers of foliage are more than a single continuous layer. The ratio of leaf area in relationship to land surface is the leaf area index (or LAI). The traditional method estimating the LAI in a forest required vertical sampling through the vegetation, quite a laborious task. In a Costa Rican tropical rainforest, such an estimate of LAI was 6.09, somewhat higher than the mean of sixty-one previous estimates at other similar sites, of 4.90. NDVI images, combined with direct observations, give us a good remote estimate of LAI. Since these leaf layers take up CO2, and emit O2 and a tremendous amount of H2O, the images help to estimate the relative capacities of exchanges in different plant communities. The high leaf areas of forests increase the average LAI for the entire land surface (including permanent ice) to 2.7, and for the entire planet (including the 70% covered by water) to 0.8. So we have the equivalent of almost a continuous

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leaf layer covering our planet’s surface. The majority of leaf production is by trees, and the total number of trees was recently estimated as 3 trillion: more than the stars in the Milky Way galaxy, half of the number present before the beginning of agriculture, and 422 for every person on our planet. Learning about this fabric and its interactions with the atmosphere has never been more important in this time of global climate change. Leaves affect climate in several ways. Through photosynthesis, they remove CO2 and add O2. Through transpiration, they add H2O. Their surfaces absorb more radiation than ice or soil, and they emit chemicals that reduce the transparency of the atmosphere and promote cloud formation. Leaves are the most important interface between life and the physical world.

Leaves and Functional Types Earth’s vast land surface is covered by communities of plants with different appearances; Alexander von Humboldt called them “physiognomies.” This excellent word, little used today, has an old history. It comes directly from the Greek phusiognomo¯nia ( phusis = nature, gno¯mo¯n = interpreter) and means (from the Oxford Dictionary): “The art of judging character from the features of the face and form of the body; the general appearance or external features of a thing, as of a plant community.” Humboldt had been exposed to some ideas about plant physiognomies by botanist friends, particularly Georg Forster and Carl Ludwig Willdenow, but he developed them further from his extensive explorations. He wrote: “This is the science (plant geography) that concerns itself with plants in their local association in various climates. This science, as vast as its object, paints with a broad brush the immense space occupied by plants.” He observed the similarities among communities under the same physical influences, as the broad- leaved deciduous forests in the eastern United States with those in Europe, and added fresh information and observations in subsequent editions of his books. He published a remarkable diagram, the “Tableau of Nature” with his Essay on the Geography of Plants (1805; fig. 4.2). It was unprecedented, with its graphic description of the distributions of plants, the agricultural activities of natives, and the physical factors of the environments correlated with altitude on the great Mount Chimborazo, in Ecuador. In the twentieth century, Humboldt’s widely distributed communities were renamed as biomes, and the physiognomies renamed as plant functional types. Of all of the communities, the tropical rainforest and its functional types impressed him the most (p. 15). Inspired by Humboldt, others added knowledge of

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Figure 4.2 Detail of the Tableaux de la nature, by Alexander von Humboldt. This image describes the distribution of plants on Mount Chimborazo, in Ecuador, including human cultivation. Other parts of the table indicate various physical observations at different elevations.

geography and plant diversity. Andreas Schimper (pp. 24 and 50) wrote the influential Plant-Geography upon a Physiological Basis. Botanical gardens and laboratories were established throughout the tropics, part of colonial strategies to capitalize on the botanical wealth of these places. Schimper worked at Buitenzorg, in Java. Christen Raunkiaer (Denmark, 1860– 1938) also worked in the tropics and established a classification of physiognomical types based on leaf sizes and locations of their development. Under different physical conditions, different functional types of plants have evolved, with their leaves often distinctive for each type. Some functional types, such as temperate deciduous (or summer-green) broadleaf trees, dominate temperate broad leaf forests, and tree cacti (arborescent stem succulents) are associated with hot deserts. In the latter example, cacti

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are native to New World deserts; in Old World deserts, other stem succulents (as spurges) replace cacti. Eugene Box pioneered the contemporary descriptions of these functional types, which are used widely by plant ecologists.

Plant Behavior: Phenology A feature of plants, easy to observe and descriptive of plant functional types, is the timing of the production and death of short- lived organs, as leaves, flowers, and fruits. Leaf production and senescence is closely related to climate and determines the ability of the plant to exchange gases and grow. Tropical rain-green broadleaf trees are leafless during the dry season in monsoon forests. In temperate deciduous forests, buds open and make leaves during the springtime, and leaves age and drop during autumn, often producing a burst of color. Even in these forests, such as the New England woods, a few trees keep their long-lived leaves during the winter (p. 219). In the uniform climates of the wet tropics, home of tropical rainforests, tree phenology is particularly interesting and seemingly chaotic. Lord Medway, the Fifth Earl of Cranbrook, worked in Malaysia from 1956–70 as a field biologist, graduate student, and as a faculty member at the University of Malaya. (I worked there three years after he left.) He kept records of the phenology of rainforest trees, because the availability of flowers, fruits, and tender young leaves affected animal behavior, his principal interest. He set up an observation platform on an emergent tree in the Gombak Valley rainforest, near Kuala Lumpur. In the eight species he studied, the phenology of each was unique (fig. 4.3). In tropical deciduous forests, the timing of leaf production and senescence is tied to the patterns of rainfall. In the forests of western India, where I spent a couple of years observing the seasonal changes, the four- month monsoon season (June–September), delivers 2,500 mm of rainfall (enough to fill a room); there may be no rainfall the rest of the year. The rain-green trees of this forest lose their foliage at varying times after the rains stop, and gain their leaves back at different times before and after the rains arrive. In temperate areas, the timing of leaf production and loss is determined by the changes in temperature and day length. Leaf loss is generally associated with color change and can be observed by satellite photography as a red wave that moves along the northern woods from north to south, in the northeastern United States. With the onset of climate change, we are beginning to see changes in the timing of leaf production and fall. Henry David

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Figure 4.3 Diagrams showing the phenology, timings of foliage production, flowering, and fruiting among five tree species in a Malaysian rainforest; research conducted by Lord Medway.

Thoreau kept such records around Concord, Massachusetts. In the 160 years since, leaf buds of the common woody plants are now opening about 18 days earlier. The nice thing about studying phenology is that it doesn’t require any fancy equipment— it’s something that a middle school science teacher can do with students. In the United States, the National Phenology Network (http://www.usanpn.org) was established in 2007. Its aim is to coordinate the collection of phenological data among academic institutions and government agencies, and to promote the involvement of citizen scientists in collecting such data. It seems to be off to a good start. The longest records were started by the Englishman Robert Marsham in 1736 and continue to be taken by his descendants and others to the present day.

Climate and Biomes Earth is a climate engine. Its tilt and daily rotation, along with its annual orbit around the sun, determine the distribution of solar energy, more along the equator, and heating up land more than water (with more heat capacity). These factors create the climates occurring in different parts of our fair planet and influence the layers of leaves covering the land. In the same climatic conditions, very similar annual distributions of temperature and precipitation, plant communities have evolved with the same functional types. These similar communities are collectively described

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Figure 4.4 Global map showing the distribution of biomes, legend on the map (courtesy of Colin Prentice).

as biomes. The distinctions between biomes are somewhat arbitrary, and here I use the biome names that are most widely employed, and the scheme based on functional types by Colin Prentice and colleagues (fig. 4.4). In the tropics, conditions of uniformly high temperatures and relatively even distribution of precipitation form the tropical rainforest biome, where I have conducted most of my botanical research over the past forty-five or so years, and which particularly enchanted Humboldt. In areas away from the equator, where seasonal rains are carried by winds that move from cooler ocean waters onto warmer land masses, large regions of tropical deciduous forests have established. These forests can be burnt during the dry season and have been heavily used by humans. These two tropical biomes contain the largest stocks of carbon above ground and the greatest annual removal of carbon from the atmosphere. In areas with longer dry seasons, and much less rainfall, closed forests cannot be supported. We occasionally find drought-tolerant and deciduous trees, but most of the area is covered by drought-tolerant C4 grasses (p. 64). Humboldt described the expanse of the savanna (llanos) of southern Venezuela, and we are most familiar with those of East Africa, with spectacular herds of migrating grazers and their predators. Away from the equator and more on the edge of the tropics, a hot and dry mass of air descends from a circulation cell that rises from the moist and heated air mass along the equator. This is a region with little or no rainfall, and the location of the hot desert biome. Mostly a thin cover of drought-tolerant plants (often with CAM photosynthesis, p. 65) persists,

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but no trees at all— unless their deep roots reach an underground water source. Away from the tropics, and mostly north of the Tropic of Cancer (and south of the Tropic of Capricorn, at 23.5°), seasonal changes in temperature become biologically important. These latitudes are not a hard distinction between tropical and temperate zones; geographical features such as oceans and mountains may modify the climate. What seems to be the difference is the absence of killing frosts; many plants characteristic of the tropics, such as epiphytic orchids and palms, are particularly sensitive. My recent home in Miami, at 25.5° N, is essentially tropical, and many of our invasive animals— like the Burmese python (p. 36), the Nile monitor, and various iguanas— are of tropical origin. At higher latitudes with seasonal climates, the amounts and distributions of rainfall (and snow) are important in circumscribing temperate biomes. With abundant precipitation from summer rain and winter snowfall, temperate deciduous forests establish. These include the colorful forests of New England and the Great Smoky Mountains, as well as the beech forests of Europe. There may be evergreen conifers among the broadleaf deciduous trees (and a few of the conifers are also deciduous). In the interiors of continents, insulated from the moist ocean winds, there is not enough moisture to allow forests to grow— except along rivers and wetlands. These regions are dominated by grasses (of the normal C3 type, p. 63) with a variety of wildflowers and shrubs: prairie (or steppe). The prairies of North America have largely been converted to agriculture, and there are few left in Europe, more in central Asia. In temperate and cold climates, lack of rainfall during the summer and abundant rainfall during the winter produce conditions for two other biomes. At warmer latitudes and higher water loss, the biome of Mediterranean scrub occurs. It consists of mostly thorny and well- defended drought- tolerant evergreen shrubs. Although it is best known from the Mediterranean region (think of fragrant rosemary, thyme, lavender, and sage, p. 250), we also find this biome on the coast of Southern California, in parts of Australia and South Africa, and the coast of Chile. The same conditions, at higher and cooler latitudes, promote the establishment of cool coniferous forests, such as in the Northwest of the United States. Where the moist prevailing winds are intercepted by mountains, regions of very dry climates occur, such as the Great Basin Desert east of the Sierra Nevada range and the Columbia Plateau east of the Cascade Range; these constitute a biome of cold deserts.

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The final two biomes are restricted by the short growing seasons and low winter temperatures at high latitudes, mainly in the northern hemisphere where land is available. If the growing season is sufficient, a biome of trees (primarily conifers) establishes: the taiga or boreal forest. This biome is distributed in the north of North America, Europe, and Asia. Where the growing season is insufficient to support trees, yet is long enough to melt the snow, a biome of low shrubs, sedges and grasses, and mosses and lichens occurs: the tundra. The soils underneath these two biomes are frozen (mainly water) at deeper levels: permafrost. They store enormous amounts of organic material and methane. Tundra- like communities are found at high elevations at lower latitudes, even at the equator.

The Changing Climate The climate is beginning to change and biomes to shift; the warmer weather and sea level rise are due to a slightly increased absorption of energy by

Figure 4.5 Spectral distribution of solar radiation, shown above the atmosphere and at sea level. Shaded area is the portion of the spectrum detectable by human vision and used by plants in photosynthesis. The dips in the spectrum, particularly in the infrared region, are absorbed by specific greenhouse gases, with the gas formula by the particular dip. Carbon dioxide = CO2; methane = CH4; nitrous oxide = N2O; ozone = O3; and water = H2O. Units of radiation are watts per square meter per nanometer wavelength increment (W.m−2.nm−1). Wavelengths are in nanometers (nm).

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Figure 4.6 The flows in radiant energy in the atmosphere, showing the factors influencing them. The initial value at TOA (top of the atmosphere) is an annual mean for the planet as a whole, considering different solar angles. The solar constant is 1.262 kW/m2. Courtesy of M. Wild et al., and published in the UN Intergovernmental Panel on Climate Change (IPCC), Fifth Assessment Report (AR5), as figure 2.11.

Earth’s atmosphere. Gases in the atmosphere absorb small amounts of radiation in the infrared spectrum (fig. 4.5). Particularly important are carbon dioxide, methane, nitrous oxide, ozone, and water vapor. Bands absorbed by those gases absorb infrared radiation returning through the atmosphere, heating it. Thus the yearly increase of CO2 of 2 parts per million, or 2 ppm (including equivalent effects of other greenhouse gases), can be interpreted as a “forcing” of 0.028 W/m2. A watt is a unit of work performed over time. The watt multiplied by hours (a kilowatt-hour) measures our electricity consumption. The annual increase of forcing is tiny, equivalent to the battery expenditure of five smartphones, and it increases the annual temperature very slightly. The total forcing from all greenhouse gases accumulated since 1750 is about 3 W/m2 (about what it takes to run a small clock radio). All of this is minuscule in relation to the amount of solar energy our planet absorbs (342 W/m2, out of 1,361 W/m2 arriving at the outer atmosphere), equivalent to a toaster oven (fig. 4.6). The same greenhouse gases have historically been important in moderating our climate in

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support of life, keeping the average temperature above freezing. The most important greenhouse gas is actually water vapor.

Leaves, Cycles, and Climate As the principal connection between life (the biosphere) and the physical environment, leaves move vital elements. The carbon that is the basis for life on land is fixed by leaves. Animals eat the plants, often eating leaves directly. Animals eat animals, and fungi and bacteria consume living and dead animals and plants. These flows of elements through nature form cycles. The cycles of different elements are similar, based on the location of pools and the rates of flow from one to another. Leaves are particularly important in the cycling of water, carbon, and nitrogen.

Water The earliest predictions of climate change concerned water. The Greeks and Romans dramatically altered their landscapes, cutting forests for new farmland, for producing charcoal, and for constructing their merchant and naval fleets. They became aware of the effects of forest clearance in drying and flooding rivers, adding silt to their coastlines, and changing rainfall and temperature patterns. Theophrastus noted that the draining of a wetland in Thessaly decreased the winter temperatures of the area, killing the old olive trees, and he saw that the cutting of forests in Philippi dried up the streams and made the weather warmer. In the eighteenth century, the loss of vegetation with climate change was scientifically documented. John Pringle, Joseph Priestley’s friend and secretary of the Royal Society, was so taken by Priestley’s discovery that plants produced oxygen (p. 47) that he used his position to influence others to take up the study of these “virtues,” in England and also its distant colonies. He supported young scientists/physicians who went abroad to serve in England’s commercial trading companies, such as the East India Company (EIC); the foundations of the British empire formed in the following century. Thus, meteorological records from the colonies were published in the proceedings of the Royal Society. Scotland was an important source of these young men, with some 800 young physicians, largely of Scots origin, hired as East India Company surgeons in India by 1830. They harbored strong environmental sentiments and were often not only against the central EIC administration, but were anti-English as well. One of these scientists and administrators, William Roxburgh (the father of Indian bot-

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any), had been in India when a drought caused the starvation of millions. He observed firsthand that streams persisted longer when coming from intact native forest, and he worked hard to reforest areas that had been cut to produce teak timber for His Majesty’s navy. Humboldt and Bonpland interviewed local residents in Venezuela and Ecuador, and confirmed the dramatic lowering of lake levels following extensive deforestation, as at Lake Valencia in Venezuela in 1801. Humboldt wrote: By felling the trees which cover the tops and the sides of mountains, men in every climate prepare at once two calamities for future generations; want of fuel and scarcity of water. Trees, by the nature of their perspiration, and the radiation from their leaves in a sky without clouds, surround themselves with an atmosphere constantly cold and misty. They affect the copiousness of springs, not, as was long believed, by a peculiar attraction for the vapours diffused through the air, but because, by sheltering the soil from the direct action of the sun, they diminish the evaporation of water produced by rain. When forests are destroyed, as they are everywhere in America by the European planters, with imprudent precipitancy, the springs are entirely dried up, or become less abundant. The beds of the rivers, remaining dry during a part of the year, are converted into torrents whenever great rains fall on the heights.

The French botanist and agronomist Jean-Baptiste Boussingault followed Humboldt’s footsteps some thirty years later and noticed that the level of Lake Valencia was rising, after the uprising of the Venezuelans against the Spanish and the partial recovery of vegetation. His memoirs, published in the Edinburgh New Philosophical Journal in 1838, influenced many of those young Scottish physicians. The loose network of young professionals, called “dessicationists” and using tropical botanical gardens as centers of communication, contributed to environmental movements that ebbed and waned, precursors of those formed in the second half of the twentieth century. Vegetation has long been considered essential for the supply of water. However, the knowledge that water that could be collected as runoff (water yield) and stored in reservoirs to be tapped when needed led some water managers to think of ways to reduce the transpiration (through plant removal) to increase runoff for later use in agriculture or to support cities. For most of the world, however, the total amount of runoff is less impor-

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Figure 4.7 The global water cycle. Numbers by different compartments in the cycles are flows when connected by arrows and pools when surrounded by a box. The units of the amounts of water are in 1,000 cubic kilometers (km3).

tant than its persistence during a dry season or drought: meaning survival or famine. In the global water cycle (fig. 4.7), the largest storage pool is the salt water of the oceans, not directly useful for most of the biosphere. The amounts in the water cycle are so great that we use another common currency for comparison, 1,000 km3. Imagine a cube of water with the height and width of 18 One World Trade Center buildings end on end, or the island of Manhattan as a container of water 17 m (56 feet) deep. Over land and sea, a total of 13 such water units as vapor are present in the atmosphere at any time. Our common reference to this volume is the humidity of our air. In Miami the humidity (the relative humidity that is) is occasionally 65%, at 1 p.m. on a sunny and hot (92°F, or 33.5°C) June day. In early morning, when the temperature drops to 78°F, the lawn furniture and cars are covered with condensed moisture because the dew point has been reached, the temperature at which the air is oversaturated with water vapor, and some condenses. These values are in reference to the absolute humidity, or the capacity of air to hold water as vapor, given as units of mass per volume (or grams per cubic meter, g/m3); for those hot conditions in Miami, the value

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is 35 g/m3, and the amount of moisture in the air on that hot sunny afternoon is 0.65 × 35, or 22.75 g/m3. One of the first students of water vapor in the atmosphere was Leonardo da Vinci, who was particularly interested in the influence of atmosphere on the quality of light, and thus on his ability to render atmospheric effects in his paintings (p. 134). He constructed the first instrument for measuring humidity, a hygrometer. The water cycle (fig. 4.7) reveals the storages and flows of water between our atmosphere, oceans, and land. Note the enormous storage in sea water (1,338,000 units), the large flows (units per year) into and out of the atmosphere in relationship to its small storage (13 units), and the large flows between the biosphere (grassland, cropland, agriculture, forests) and the atmosphere. Leaves are the largest source of these flows. Leaves are the surface for the movement of water into the atmosphere through the processes of transport and transpiration. Evaporation is magnified by the very large internal surfaces of the photosynthetic cells inside the leaves, some 30 times the area. The force for the movement of water from soil surrounding roots to passage out of the leaves via the stomates is provided by the evaporation of water inside the leaf and through those pores (p. 205). Stomates are numerous; plants I’ve studied, with densities of 200–300 stomates per square millimeter of leaf, are typical. When water is available and stomates are open, plants move tremendous amounts of water through the crowns and into the atmosphere; a large oak tree might use a ton (1,000 liters) of water a day. It is difficult to measure the transpiration of a single tree in the ground, as Van Helmont did for that single willow sapling in a pot some 350 years ago (p. 45). It takes a larger area of the landscape to analyze the flows. A standard approach in the science of the water cycle (hydrology) is the study of water in a small valley (a watershed), where all of the water exits through a single stream. Precipitation can be measured by several gauges in the study area, and the water leaving the watershed can be estimated by constructing a small weir (a special dam) to measure the flow of water. If the underlying rocks are impermeable to water, we can assume that water is not moving downward to recharge an aquifer. Then, the simple equation for the water balance is runoff = precipitation − evapotranspiration ± change in underground storage (zero) It looks simple, but often the work is laborious and remote from easy access. In Malaysia J. B. Kenworthy analyzed the water dynamics of intact

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Figure 4.8 The hydrology of two Malaysian watersheds. Left, undisturbed tropical rainforest in the Gombak Valley; and right, suburban development with highly disturbed vegetation, Damansara, Kuala Lumpur. Bottom, summary of comparisons of runoff and evapotranspiration in the two watersheds.

forest in the Gombak watershed and compared it with a heavily disturbed watershed in the Damansara suburbs of nearby Kuala Lumpur (fig. 4.8). These two catchments had similar annual rainfalls but very different runoffs. The cause of this difference is the dramatically increased evapotranspiration (ET, or evaporation + transpiration) in the Gombak watershed of 1,778 versus 993 millimeters. On a larger scale, the major tropical rivers, such as the Congo and the Amazon, also have reduced runoff compared to precipitation. The Amazon basin, with a runoff of about 6.7 units returns a similar amount into the atmosphere. Such basins are said to be recycling, because that evaporated water is condensed and returned to the basin as rainfall. Thus, the tropical rainforest biome helps create the climate for its continued existence. Tropical rivers disturbed by loss of forest, mining, or a strong wet and dry season recycle much less. Since lakes and rivers take up a small percentage of the land area, and deserts and ice evaporate little, the majority of the planetary ET is due to transpiration. Evidence supporting the importance of transpiration comes

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from the use of stable isotopes (p. 54), because the uptake of water by plants distinguishes among isotopes. In the Amazon Basin, such research has shown that about 80% of the water vapor moving into the atmosphere is due to transpiration. In the water cycle (fig. 4.7), about 39 units of water (80–90% as transpiration) are returned to the atmosphere by leaves. This is well over twice the flow of all rivers (including the Amazon at 20% of the world’s total) into the ocean. Transpiration has another important effect on the world’s climate: it absorbs an enormous quantity of heat— thereby cooling the atmosphere by at least 50 W/m2 (fig. 4.6).

Nitrogen The nitrogen cycle has an enormous storage pool in the atmosphere (around 80% of the total). Leaves are not the primary means of the movement of this element into the biosphere. Nitrogen, a chemically stable twoatom gas (N2 ), is fixed by bacteria that principally live in the root nodules of plants of the legume family. Some nitrogen is fixed by cyanobacteria living in oceans, on the leaves of tropical plants, and— in one case— at the base of leaves of the large-leaved Gunnera, a plant of tropical mountains (p. 173). However, leaves are important in the cycle, because a disproportionate amount of nitrogen is allocated to leaves as a requirement for photosynthesis (p. 56); in a tree, about 80% of nitrogen is in foliage. This storage varies with the loss of leaves, when quite a bit of nitrogen is stored in branches. Leaves, and also seeds, are particularly good sources of nitrogen for animals feeding on them. So, nitrogen moves through the biosphere from leaves, to animals, to decomposing bacteria and fungi, some back into plants, and some by denitrifying bacteria back into the atmosphere. The nitrogen cycle has been distorted by human activity, particularly in the artificial fixing of nitrogen into fertilizer, and the movement of nitrogen into streams and lakes, and then back into the atmosphere. Nitrous oxide (N2O) is a greenhouse gas, even more potent than methane. An excess of it, through human effects on the cycle, contributes to global warming. When leaves age and fall off of the plant, 45–55% of the nitrogen is resorbed back into storage tissues of the plant. This nitrogen is redeployed in the next growing season, contributing to the growth of new leaves. Consequently, 45–55% of the nitrogen is retained in the fallen leaves, particularly the by-products of the breakdown of chlorophyll. This is an important source of nutrition for soil bacteria, and much of that nitrogen is reabsorbed by plant roots.

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Figure 4.9 The global carbon cycle. Numbers by different compartments in the cycle are flows when connected by red arrows and pools when surrounded by a black or white box. The units of the amounts of carbon are in picograms of carbon (1015 tons) in pools. And picograms carbon per year in flows. Diagram was adopted from the IPCC’s Fifth Interim Report, figure 6.1.

Carbon We learned of the greenhouse effects of gases on climate, particularly carbon dioxide, more recently than our appreciation of the importance of water in climate change. Svante Arrhenius, a Swedish physicist and chemist (1859–1927), first proposed in 1896 that excess human production of carbon dioxide could increase global temperatures. Despite the widespread denial of the danger of carbon dioxide accumulation by the American public, even President Lyndon Johnson spoke out about the problem in 1965! In the carbon cycle (fig. 4.9), carbon dioxide in the atmosphere is converted by plants into sugars. Photosynthesis is estimated in an ecosystem by measuring the accumulation of dried plant parts over a year; carbon is calculated as half of the dry mass. Belowground carbon, especially in roots, can be estimated as a portion of the aboveground biomass. Various factors limit the total yield of photosynthesis. Net primary production (NPP) is what is left when plant respiration has been subtracted. Primary production is further reduced from consumption by animals and

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microbes in the soil, and respiration outside of the plant that puts CO2 back into the atmosphere. Leaves make up 30– 40% of NPP, but they break down quickly and do not contribute much to the carbon stored long term. In the Gombak forest, the annual production of leaves was about 6 tons per hectare, with little leaf litter on the forest floor at any time. As a plant community establishes in a new location, biomass slowly accumulates and reaches an equilibrium where increase is offset by the death of trees and the activity of animals. The accumulated biomass in all of the biomes— as carbon in the woody mass of trunks, branches, and roots— is very large, and tropical forests contribute the most. If the forest is cut down and converted to another use, the amount of stored carbon is dramatically reduced and carbon dioxide released: about a quarter of the increase of greenhouse gases into the atmosphere each year. Developing countries with large storages of carbon in their tropical forests are paying attention to these amounts, as they may receive payments from developed countries with higher productions of CO2. We need to use a single unit of measurement to understand the relationship of these flows to the atmospheric pool (fig. 4.9). The Intergovernmental Panel on Climate Change (IPCC) uses the petagram, or 1015 grams (one followed by 15 zeroes). Each petagram (Pg) is equivalent to 1 billion metric tons (a ton = 1,000 kilograms). Atmospheric carbon dioxide is presently at a concentration of 400 ppm, which translates as a total pool of around 846 Pg of carbon, with a yearly addition of 4 Pg (from the ~2 ppm added each year). This compares with the yearly total of terrestrial photosynthesis at 120 Pg (54% of the global total, despite the small portion of land surface, 29%), and another 92 Pg from oceans and coastal areas. Respiration, decomposition, and fires reduce the land carbon sink to 2.6 Pg per year. The total amount of stored biomass is about 4,200 Pg of carbon, the majority in soils or permafrost, not including fossil fuels and the deep ocean. The annual sinks of carbon (land at 2.6 Pg and ocean at 2.3 Pg) are now outpaced by the additions from burning fossil fuels (7.8 Pg) and cutting down forests (1.1 Pg) to produce the total yearly increase of carbon at 4 Pg, and global warming increases. The sensitivity of the atmospheric pool to the activity in the biosphere is seen in the famous Keeling curve, from the measurement of CO2 concentration on Mauna Kea, in Hawaii, during the past sixty years (fig. 4.10). Each year the atmospheric concentration increases but shows a seasonal dip, which is a consequence of the seasonality of NPP in the northern temperate deciduous forests.

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Figure 4.10 Keeling curve of the gradual increase of carbon dioxide in the atmosphere, from measurements at Mauna Loa, in Hawaii. Measurements over the entire time period. Inset, example of individual measurements over a single year, showing the seasonal changes of CO2, the dips due to leaf production and photosynthesis of the northern temperate deciduous forests (courtesy of NASA).

The destruction of biomes, such as conversion to agriculture, results in a large amount of stored carbon moving into the cycle, about 1.1 petagrams per year, mostly from tropical forests. In Indonesia during the past decade, large swathes of forest, particularly on the islands of Sumatra and Borneo, have been cleared for the establishment of oil palm plantations; Indonesia recently surpassed nearby Malaysia as the largest global producer of palm oil. Forest has been removed at the pace of 340,000 hectares per year, now some 14 million hectares for both countries. Peat forests, with over seven times the stored carbon underground, have been particularly targeted, and the forests burn and spread a haze over all of Southeast Asia every spring. Palm oil is used in the human diet, but also has been touted as an economically profitable biofuel. It is a sad commentary on our ignorance that a market for biofuels, alleged to be renewable and carbon neutral, is an incentive for the destruction of tropical rainforests— and a large contribution to the increase of carbon dioxide. Methane (CH4 )— the primary constituent of natural gas and a natural product of bacterial metabolism— is an additional carbon- based greenhouse gas. It is much less prevalent (now at 1.8 ppm in the atmosphere) but about 50 times as effective a greenhouse gas as carbon dioxide. Trace amounts of methane may be emitted by leaves, but little compared to the

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flatulence of farm animals and bacterial production in rice cultivation and marshes, as well as emissions from drilling for natural gas.

Leaves and Global Climate Change Clearly, the global climate engine is exceedingly complicated. In the past, our interest in climate was largely academic, supported by curiosity more than necessity. Now its study is urgent. Although we have learned much about our climate in the past quarter century— largely driven by our concern about greenhouse gases and global warming— we have a long way to go. Climate research will help us understand the long history of climate change and help to predict what might happen in the future. Our two major challenges are to predict human behavior and to fully understand how the biosphere (and foliage in particular) interacts with climate. The composition and temperature of the atmosphere has fluctuated in history, and so has the biosphere, with five major episodes of extinction (fig. 4.11). Their causes are poorly understood except for the last two. Sixty-five million years ago, dinosaurs became extinct and the flowering plants flourished. This extinction was most likely caused by a meteorite impact near the Yucatán Peninsula. The latest extinction event is caused by us. Atmospheric carbon dioxide, steadily dropping during the early evolution of land plants and the appearance of leaves, varied in concentration—

Figure 4.11 Estimates of carbon dioxide concentrations and estimates of mean global temperature during the past 500 million years of Earth history. Blue blocks show times of extensive glaciation, and brown vertical lines are points of large extinctions of organisms during this history.

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and the mean temperature with it. The greenhouse effects of CO2 may have been supplemented by the release of methane, as mixtures of water and methane solidified under pressure in ocean sediments and were released in warmer water. Oxygen also varied in concentration, increasing to a high of around 35% about 300 million years ago, supporting the evolution of some really large reptiles and amphibians. We do depend upon the oxygen produced by leaves, but it will not change quickly; the yearly output of oxygen is about 154 gigatonnes per year, a small portion of the 1.2 million gigatonnes of oxygen in the atmosphere (21% of its composition). Through the movement of continental plates, the single continent of Pangaea was assembled (by around 250 million years ago) and formed the climates and geography for dinosaurs to flourish, and the establishment of great forests at its northern and southern ends (seen in fossils from northern Greenland and the evergreen Glossopteris forests of Antarctica). Later on, starting 120 million years ago, the plates began to wander toward their present locations. This movement produced areas of intense volcanic activity, possibly altering the atmosphere by adding more CO2 and also sulfur dioxide and hydrogen sulfide. Throughout this time, there were also episodes of glaciation, culminating in the multiple events during the past million years. So there have been some dramatic changes. Yet life continued, rebounding resiliently with climate change and after each extinction event. Leaves were important in climate history and will be important in future climates as well. Leaves initially reduced the high concentrations of atmospheric CO2 after the origin of land plants, which led to the first forests. The high transpiration of broad-leaved flowering trees after the extinction of dinosaurs added to the cycling of water and made the origin of tropical rainforests possible. Leaves also contributed to the activity of soil in providing nutrients (leaf litter) and protecting the soil surface from heat and direct rainfall; the soils helped to regulate CO2 concentrations. Leaves reflect radiation less effectively than soil or rock surface and water, much less than snow or ice, slightly affecting temperature. They also emit a rich brew of volatile organic compounds (VOCs). Isoprene is the most important among them and can react with other molecules to produce ozone. Ozone, reactive and short-lived, is a strong greenhouse gas but contributes to the breakdown of methane. These VOCs can condense to nuclei to promote cloud formation, and they reduce the transparency of the atmosphere and increase its reflectance. Leaves have also adapted to changes in climate. Leaves have evolved among species and in plasticity within the lifetime of the plant, improv-

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ing function in different climatic conditions. Changes in stomate density affected photosynthesis and water use. Structures to increase reflectance, as hairs, reduced the heating of leaves. Increases in VOC emissions also helped leaves reduce heat stress. The adoption of CAM and C4 metabolisms (p. 63) helped leaves function in hotter and drier environments, and will do so in the future. Leaf phenology responds to climate because both temperature and day length can affect leaf production and drop. Changes in leaf development among species will change forest ecology, and longer life spans would increase NPP. We are particularly ignorant of the complex interactions in tropical biomes. Leaf traits are important indicators of the global climate and are used to help establish the climatic record (fig. 4.10). The density of stomates in a leaf is influenced by the concentration of CO2, independent of temperature, so densities of fossil leaves have helped fill in the blanks on the CO2 record. Smooth leaf margins are correlated with higher temperature (p. 169) and have helped to reconstruct the temperature record, which generally tracks the CO2 record. What role will plants— and leaves— play in future climates? Perhaps the most obvious effect is the increase in photosynthesis with the rise of CO2 (p. 60). This could increase NPP and store more carbon, but is restricted by the amount of available nitrogen. Elevated CO2 will reduce the density of stomata (and gas exchange), and the related increase in temperature, especially at night, will also increase the rate of respiration. Increased temperatures will allow for greater storage of water vapor in the atmosphere (a powerful greenhouse gas), but leaf changes may reduce the amount of transpiration. Higher temperatures will increase the emissions of VOCs, increasing the albedo of the atmosphere (more reflectance and less transmission) and forming clouds, and increasing ozone production (and destroying more methane). Vegetation will change; deserts will expand at lower latitudes, with more broadleaf forests and farmlands at higher latitudes. Loss of vegetation decreases transpiration and cloud formation, and increases direct reflectance of radiation back into the atmosphere. Hotter and drier climates will increase of the savanna biome area in the tropics, with more C4 grasses, not the first time in the planet’s history. Increased temperatures on mountains may promote the extinction of alpine plants on summits (nowhere to go up), and the slow rates of migration may prevent plants from relocating to newly available habitats. The vegetation zones on Mount Chimborazo observed by von Humboldt (fig. 4.2) have risen 500 meters in the past

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210 years and will continue to do so. Plant responses will be complex, both promoting and reducing the rate of climate change. According to satellite imagery, CO2 enrichment is causing the earth to become a greener place, and that means greater capacity to store carbon. Despite that, loss of forest cover is increasing daily temperatures, adding to global warming. The interaction between biosphere and climate was famously addressed by James Lovelock in the Gaia theory. Lovelock (born 1919) is a highly respected Earth and planetary scientist, who was made a Fellow of the Royal Society in 1974. He first developed the Gaia hypothesis in the 1960s and published it in a widely read book in 1979. Later he collaborated with Lynn Margulis (the champion of the endosymbiont hypothesis, p. 24), who amplified many of the biological details. To Lovelock, “Gaia is a tightly coupled dance, with life and the material environment as partners. From the dance emerges the entity Gaia.” To Margulis, Gaia is “an emergent property of interaction among organisms.” Lovelock had also used the metaphor of Gaia as a “super-organism,” incurring the disapproval of scientific colleagues and the affection of deep ecologists (p. 297). Eventually, the scientific community embraced Gaia as an “earth-system behaving as a single, self- regulating system comprised of physical, chemical, biological and human components.” Although Lovelock saw the mechanisms that promoted a climate suitable for the maintenance of life on our planet, in the long run he was not optimistic about her capability. He was an early spokesman about global climate change (The Revenge of Gaia) but then changed his opinion. In the long run, Lovelock saw a lowering of CO2, eventually to a concentration that would not support photosynthesis. That would mean the end of life as it has evolved on planet Earth— in perhaps 500 million years. We are now on track to add enough CO2 to the atmosphere to reach 1,000 ppm by the end of the twenty- first century (the highest since 80 million years ago). Such concentrations will elevate the average global temperature by ~3°C, will alter the distribution and patterns of rainfall, will disproportionately increase temperatures at nighttime and at high latitudes, and will raise the sea level by 1 meter, probably more. The impacts on us will be large. Inhabitants of coastal regions within 2.5 meters of sea level will need to live somewhere else. Others may need to relocate from regions with a lack of water, but there will be opportunities at higher latitudes. Shifts in productivity will be important to us; we now rely, directly and indirectly (through farming, grazing, forestry and more), on about a quarter of the global terrestrial production. It won’t all happen at once, but still the

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costs of adaptation will be enormous, and perhaps too great for the majority of humanity living in poverty. Everyone will be affected. What to do? We need to support efforts to mitigate against climate change at every level, from our neighborhoods, nations, and the planet as a whole. On a personal level, we all need to change our habits, to conserve energy use, grow our own food, follow the examples of those (such as Wendell Berry) with the optimism and energy to try to change our destructive habits. The Paris Agreement of December 2015 was a step in the right direction.

Chapter Five Leaf Economics And what if all of animated nature Be but organic Harps diversely fram’d, That tremble into thought, as o’er them sweeps Plastic and vast, one intellectual breeze, At once the Soul of each, and God of all? samuel coleridge, “The Aeolian Harp”

Nature’s economy shall be the base for our own, for it is immutable, but ours is secondary. An economist without knowledge of nature is therefore like a physicist without knowledge of mathematics. carl von linné (linnaeus)

I

n July 1984 I was invited to participate in a conference, “Evolutionary Constraints on Primary Productivity: Adaptive Patterns of Energy Capture in Plants,” at the Harvard Forest, in central Massachusetts. That is quite a long title for a conference, and the book resulting from it had a much shorter name: On the Economy of Plant Form and Function. The speakers at the conference included some of the big names in plant physiological and functional ecology at the time: Hal Mooney, Jim Ehleringer, Park Nobel, Martyn Caldwell, John Pate, and John Raven, among others. The convener was a very bright and promising young scientist, Tom Givnish (p. 171). Needless to say, I was surprised to be included— and a bit intimidated as well. When I asked Tom, “Why me?,” he responded that · 90 ·

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the plants I studied were very interesting. These were tropical rainforest understory plants with “ingenious” mechanisms to optimize energy capture. The conference was my first direct experience in biology where economic models provided an intellectual underpinning to the research, but the connection between economics and the study of nature goes back two and a half centuries. Much later, I would spend many months at the Harvard Forest, studying the color changes of foliage during the autumn (chapter 11). In the eighteenth century, studies of the functions of organisms suggested a finely tuned and designed machine, like a watch. Students of natural history saw that these organisms interacted with one another and the environment, much like a superorganism. Natural philosophers began to compare the operations of nature to human institutions or saw nature as the basis of all human economy. Two botanists were important in such comparisons. Nehemiah Grew, famous as the father of plant anatomy, wrote a manuscript on the economy of England for the queen. Far more important were the ideas first described by Carolus Linnaeus (or Carl von Linné), the father of the classification of organisms, and the scientific binomial system of naming organisms (fig. 5.1). In our name, Homo sapiens L., the “L.” stands for Linnaeus as the authority. In 1749 Linnaeus wrote Oeconomia Naturae (The Economy of Nature). In it, he described the orderly processes that bind organisms into a single system, perhaps the first real work of ecology. Linnaeus wrote: Whoever directs his attention to those things, that occupy our terraqueous globe, will finally admit, that it is necessary, that all and each are arranged in such a series and in such mutual nexus, that they aim at the same end. . . . So that natural things may last in continued series, the wisdom of the highest Being has ordained, that all living beings perpetually work for the production of new individuals, and that all natural bodies reach out a helping hand to their neighbor for the conservation of each species, so that what serves the ruin and destruction of one of them, serves the others’ restitution.

It is interesting to examine the words “economy” and “ecology.” Both share the root eco- (Greek oikos), pertaining to the house or household. The word “economy” refers to the management of the household. “Ecology” refers to the knowledge (logos) of the household, a term later coined by the German biologist Ernst Haeckel. Today the most used textbook in ecology, by Robert Ricklefs, has the title The Economy of Nature.

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Figure 5.1 Carl von Linné (Linnaeus), the father of classification and the “author” of the Economy of Nature.

Linnaeus’s Economy of Nature profoundly affected intellectual ideas in the eighteenth century. It was a guideline for the development of the national economy in Sweden. The book was owned and read by Adam Smith, who was influenced by his studies of natural philosophy; Smith wrote the first real economic treatise—The Wealth of Nations—and was the first to use the term “economics.” This nature and economics connection was substantially based on the importance of natural products— for example, timber, fiber, food, dyes, spices, and so on— that were the primary commodities in trade and the sources of wealth. Charles Darwin took the Economy of Nature on the voyage of the Beagle, and it influenced his ideas. It even influenced the literary currents of the late eighteenth century, including the poetry of Coleridge and Wordsworth.

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The Economics of Leaves To see how we might profit from looking at leaves from an economic perspective, it is useful to look at the economics of a factory. Consider a medium- size factory that manufactures widgets, just established in my hometown of Ephrata, Washington (the town fathers would be thrilled by the news!). Land is purchased and prepared, utilities installed (electricity, sewer and water, telephone/Internet), and a building constructed with loading docks and roads. All manufacturing equipment is purchased and installed. Staff is hired by the human resources department to fulfill labor needs for all aspects of the business: manufacturing, financial oversight, purchasing, maintenance, warehousing, shipping, marketing, and security. All of these costs represent a capital investment, and widgets are the gross sales. Sales of widgets must be in excess of the payoff on the loan with interest for the initial investment plus direct and continuing production costs in materials, utilities, and labor. Over time, the facility is maintained with repairs and upgrading of equipment. Ultimately, the facility will become obsolete, because of changes in tastes for widgets and production technology that cannot be housed in the present faculty. And the plant will be closed. Perhaps, a more economical location will be found, as another country, and a new plant built there. Accounting of the entire process is simplified by the use of a single currency for all costs, the U.S. dollar, including purchase of power, water, and raw materials. Using such a simple economic analogy, I will explore two important features that have important implications for leaf and plant function. The first is the period that a leaf is active, or leaf life span. The second is the size of a leaf, how costs and economies of construction might be related to scale.

Leaf Construction Costs We can use much of the same terminology for the functioning of leaves, other plant organs, or even the plant in its entirety. The leaf is produced from an apical meristem, at the tip of a shoot. Its production, including the petiole and blade, has a cost. We already know the raw materials of production for the leaf: carbon dioxide, water, and a few minerals (notably nitrogen, phosphorus, and potassium). We also know the product: fixed carbon as glucose (p. 58). However, the leaf is quite complicated in its organic chemical composition, containing DNA, RNA, proteins, and a diversity of

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small compounds (thousands of them). The costs of making these different compounds vary, and we need a common currency to determine costs, as a substitute for the dollar. The methodology of such costs was originally worked out by Fritz Penning de Vries in the 1970s and Kimberlyn Williams in the 1980s when she was a graduate student at Stanford University (with Hal Mooney). The method was improved by Hendrik Poorter at the University of Utrecht, in the Netherlands, and most researchers follow his protocol. Poorter’s unit of currency, his “dollar,” is the amount of glucose needed to make a compound, as grams of glucose to make a gram of the compound. The major categories of compounds are given below, with their construction costs in grams of glucose: Lipids (fats)

3.03

Soluble phenolics (tannins)

2.60

Protein (from nitrate)

2.48

Lignin

2.12

Structural carbohydrates (mainly cellulose)

1.22

Non-structural carbohydrates (sugars and starch)

1.09

Organic acids

0.91

Minerals

0.00

These components represent different construction costs of the leaf factory. The structural carbohydrates are the factory building. The protein is mainly involved in photosynthesis, equivalent to the factory machinery, as are lipids (in membranes). Lignin is the cement that makes the structural carbohydrates strong and durable, and adds to the security of the building. Non-structural carbohydrates are products of the manufacturing processes, as are organic acids. Minerals are inexpensive and are used in manufacturing and in building construction costs. The soluble phenolics are defensive compounds and are part of the security costs of running the factory. By determining the concentrations of these groups of compounds, it is then possible to figure out the construction costs of a leaf. Starting out with the dry mass of the leaf, the technique involves making extractions. The dry leaf powder is used to determine carbon and nitrogen from the dry leaf with an automated analysis machine, and to determine the amount of nitrate in the total of nitrogen. Two extractions yield the other components in the list. A significant problem is determining the forms of ni-

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trogen present in the leaf. If plants get all of their nitrogen from nitrate dissolved in the water transported into the leaves, it must be reduced (hydrogen added to it) before it is incorporated into amino acids and other nitrogen-containing compounds. That takes a lot of energy, such as ATP and NADH obtained from “burning” glucose. If plants obtain their nitrogen already reduced (as ammonium), there is a much smaller metabolic cost in assimilating it. Generally, most of the nitrogen is absorbed as nitrate, and that cost goes into the calculation. Once the construction costs are known, then it possible to calculate costs of maintenance of the leaf (from dark respiration), and the amount and time of photosynthesis that will pay off the construction costs (the payback time), and the profits from leaf function during its life span. Some of the costs related to leaf function are not calculated. There is the small cost of pulling in mineral nutrients in water from the soil, but the cost of moving the materials into the leaf is small, except that the leaves rely on the pathway of vessels for transport (transport of raw materials): roots and stems. There is also a cost of translocating sugars and amino acids to other parts of the plant (shipping and warehousing). Some of the compounds in the leaf are toxic to animals that might eat them. These often contain nitrogen (as alkaloids) and are expensive to make. Finally, if the location for production is no longer costeffective, such as having a lack of sunlight, the leaf will die and be replaced by another new leaf in a more favorable location. As an example, I’ll use a recent study on the economics of coffee leaves published by scientists at the Universidade Federal de Viçosa, Brasil. Coffee leaves are a bit different from most plants in their high concentration of defensive compounds, mostly caffeine (fig. 5.2). The principal objective of this study was to determine environmental effects on construction costs, but I’ll use typical growth conditions of partial shade and abundant water as an example. Leaf construction costs were 1.35 g glucose/g of dry leaf tissue. Of this total cost, 11% was from the production of cellulose, 9.6% from proteins, and 7.5% from defensive compounds (caffeine and tannins). The maintenance cost for the leaf was 13.2 mg, about 1% of construction costs per day. The payback time for a leaf, based on averages of photosynthesis measurements during the day, was 37 days. The researchers found that construction costs increased if plants were grown in more sunlight, and payback times were also longer. In the shade, coffee leaves lasted about 430 days, much less under higher light. This means that the leaf during its life span can make a significant income for the plant, over ten times the initial construction costs— a pretty good profit.

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Figure 5.2 The coffee plant. Left, leaves, flowers, and fruit of the plant; right, structure of caffeine, an important defensive compound on all parts of coffee, including the leaves.

The literature on leaf construction costs is not huge; calculating costs for a single species is laborious. Nonetheless, some general conclusions about construction costs can be made. In general, leaves of species that prefer shady environments, or more shade-acclimated leaves within the crown of a sun-loving species, have much longer life spans and also greater payback times. Even with low rates of photosynthesis in deep shade, the payback times are half the life spans or less. Those low irradiance leaves have lower construction costs, but much of the economy in such leaves is due to the reduction in materials per unit area of the leaf. In general, species with long-lived leaves are evergreens, and these often grow in full sunlight. These include needle leaves of conifers, but also broad- leaved trees, as in tropical rainforests. Evergreen species generally have higher construction costs, but some component costs offset each other. Longer-lived evergreen leaves have higher costs in lignins and defensive compounds, and shortlived leaves have higher protein costs.

Longevity An important leaf economic trait is longevity: how long the leaf functions on the plant. The range is enormous. You might think that evergreen plants have longer-lived leaves, but that is not necessarily the case. Evergreen-ness is the appearance of the entire plant and is determined by the timing of leaf fall. It is possible for a deciduous tree to grow in an evergreen tropical rainforest; its leaves may fall at the same time— and leave the crown bare

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Figure 5.3 Long-lived leaves in gymnosperms. Left, leaves of Welwitschia mirabilis, native to the deserts of South Africa and Namibia; center, bristlecone in White Mountains of California; and right, needles of bristlecone pine.

at least briefly before it refills with new leaves. In the same forest, another tree may produce shorter-lived leaves that fall at different times— leaving the crown evergreen. The longest-lived leaf is certainly that of the remarkable gymnosperm plant, Welwitschia mirabilis, native to the Namib Desert of southwest Africa (fig. 5.3). After producing two embryonic leaves (the cotyledons), the young plant produces two leaves that grow continuously from meristems at the leaf base. These two leaves last the entire life of the plant, which may exceed 1,000 years. The tips of Welwitschia leaves eventually split and become frazzled, but the base continually produces fresh photosynthetic tissue. Almost as remarkable, the leaves probably use CAM photosynthetic metabolism (p. 63), the only gymnosperm to do so. The next oldest leaves survive for almost two orders of magnitude less than the Welwitschia. The needle leaves of conifers are long-lasting, and the record for this group is the tough needles of the bristlecone pine, which last around 40 years (fig. 5.3). This is the oldest documented single plant in age, at over 4,800 years, although some clonally reproducing trees, such as the aspen, may be older. Other conifers produce needles lasting from a decade to as little as 1.5 years. Leaves of broad-leaved trees are less durable, lasting 1–5 years. The leaves of tropical rainforest trees typically last at least 1–3 years, and often less than a year (p. 70). Leaves of deciduous trees typically last for 6–9 months, depending upon the duration of the growing season, controlled by temperature or rainfall. The shortest leaf durations are found in herbs and aquatic plants, where leaves may last as little as 2–3 weeks.

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The age of a leaf is typically determined by when the blade opens and when the leaf falls from the tree. However, what may be more important is the time when the leaf is physiologically active and can continue to benefit the parent plant by exporting glucose. Typically, leaves are productive throughout most of that life span, but lose their productivity toward the end of their lives. This leaf productivity is important for working out the economics of the leaf and the plant.

The Leaf Economics Spectrum Botanists have been studying and speculating about the roles of different leaf traits in optimizing function for well over a century, and that was a primary task of the physiological anatomists in the late nineteenth century (p. 160). These optimality arguments have been criticized by evolutionary biologists. One serious issue is the currency in the optimality arguments. The currency for optimality is some measure of performance, as amount of energy absorbed, amount of glucose made, and so on. In evolution, what really matters is the number of offspring produced. If a trait is advantageous, it should result in producing more babies or, in the case of plants, more viable seeds/spores. Increased energy capture and glucose production should make the production of more seeds likely, but not necessarily so. In the past twenty-five years, the thinking about testing the adaptive significances of leaf traits has sharpened, as has the means for studying them. An important improvement has been the availability of portable instruments for measuring the exchanges of gases by plants, particularly CO2. It is now quite feasible to carry an instrument weighing ~4 kg into a remote environment and measure photosynthesis and dark respiration in leaves on plants for the day, and then return to a camp and download the data into a computer. This has made it relatively easy to estimate the levels of physiological activity throughout the leaf life span and to collect physiological data in relationship to other plant traits. Other technological developments have spurred the kind of research on leaf traits I’ll discuss in the following paragraphs. The availability of sophisticated statistical programs running on small computers also emerged during that quarter of a century, as has the availability of the Internet in facilitating rapid and frequent contact between researchers from throughout the planet. Thus, the amounts of data analyzed and the numbers of collaborators (and authors on papers) have dramatically increased. However, some leaders were necessary to pull the collaborations to-

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Figure 5.4 The plotting of leaf traits reveals a strong relationship between them, revealing a “leaf economics spectrum.”

gether. That person in the United States was Peter Reich, of the University of Minnesota, and he was joined by Ian Wright and Mark Westoby of Macquarie University in Australia. The first article laying out the approach to analyzing leaf traits was published in 1997, and it inspired the broader collaboration and the huge data set that led to the pathbreaking article published in Nature in 2004: “The Worldwide Leaf Economics Spectrum.” This article was authored by 33 scientists from 15 countries. Leaf traits were measured from 2,548 species from 175 sites from virtually every biome from throughout the planet, approximately 1% of all vascular plants. Participants had to use similar protocols for collecting data on the following plant traits (narrowed down from previous research): maximum photosynthesis (p. 60), dark respiration (p. 60), leaf life span, leaf blade mass/area, leaf nitrogen content, and leaf phosphorus content. Analysis of this data set revealed a continuous “spectrum” in the distribution of traits in relationship to mass/area and life span (fig. 5.4). At one end of the spectrum, there are short-lived leaves with relatively high levels of nutrients, low mass/area, high rates of photosynthesis, and higher dark respiration. At the other end are long-lived leaves with low nutrient levels, higher mass/area, but with lower rates of photosynthesis and dark respiration. Leaves with combinations of these traits were not limited to a single biome or geographical

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region, but different leaves were found together within biomes. These results suggested that there were “rules” of construction that spanned size, habitat, and geography. In this age of informatics, scientists now have the means of assessing the impact of a discovery by totaling the number of citations of the article in subsequent publications. For this article, in 2015 the total number of citations was 2,500— and rapidly growing. It has spawned the publication of other influential articles examining evolution, geography, climate, litter decomposition, using traits to predict photosynthesis, and using the same approach to study stems and roots. Another global database has been established, TRY (www.try-db.org), covering 69,000 plants species and 3 million trait entries. The paper that described TRY had 135 authors; so far, 344 partnerships and 173 institutions have enrolled. In other areas of ecology, such as the Center for Tropical Forest Science (CTFS) with a global network of 50 hectare forest sites (and records on tens of millions of trees) and the National Ecological Observatory Network (NEON), with a coordinated strategy for collecting environmental data at different sites, the potential for analysis and synthesis are even greater. We are beginning to see the scientific papers with scores of authors, much as the articles coming from the Large Hadron Collider (LHC) in France. Studying leaf economics is a growth industry in plant biology. One implication of the spectrum is that some of the leaf traits determine the rate that leaf litter decomposes, thereby influencing the cycling of nutrients. Longer-lived and tougher leaves last longer. In some cases, such leaves are particularly common in certain evolutionary lineages of plants, provoking speculation about the role of leaves in the function of ecosystems. The data and analysis of the leaf economic spectrum have helped us understand the differences between evergreen and deciduous leaves. Evergreen leaves (with exceptions mentioned below) are long- lived and are produced by trees on poor sites, with inadequate nutrients. At Manaus, on the Brazilian Amazon, two rivers come together. The Rio Negro, draining a large forest area on white sand soils, pours its dark clear waters, colored by the tannins leached from the tough evergreen leaves, into the greater Amazon supplied by forests on richer soils, with its water turned muddy from the suspended sediments. Evergreen does not always mean longlived, however. In some cases, trees of evergreen forests may drop their leaves (with the same life spans of deciduous trees) and simultaneously produce new ones. In Miami the live oaks in my neighborhood lose lots

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of leaves during the dry “spring” weather, but simultaneously produce new ones. Tom Givnish has subjected such plants to an exhaustive cost-benefit analysis and has found combinations of extended growing season length and lower nutrients that favor such ever-green strategy. The high latitude boreal forests in North America are dominated by evergreen coniferous trees, although areas of broad-leaf deciduous trees may occupy sites with more nutrient-rich soils. Within the boreal evergreen forests, stands of larch trees— conifers whose needles turn yellow during the autumn and fall from the trees— may establish. Larches grow in wet areas with higher nitrogen supplies than where evergreens grow, and they have a greater ability than evergreen conifers to resorb nitrogen before needles fall from trees. Larches also invest less in branches because the bare branches carry less snow and ice during the winter. These differences favor larches in local habitats in the boreal forest.

Leaf Size An issue in economics, I guess, is determining the size of an entity, as a factory or corporation, in predicting efficiency and profitability. The assumption is that bigger is more efficient. Henry Ford made the biggest and most efficient integrated manufacturing complex. Walmart created huge stores and an even bigger organization that helped drive down retail costs and led to sales volume and profits. Perhaps becoming bigger has social costs, but those are “externalized” and paid by individuals or the society at large. Others have argued that too large a size leads to breakdowns in communication, lower worker productivity (related to less job satisfaction). Years ago I was influence by E. F. Schumacher’s book Small Is Beautiful, which argued for keeping things small and simple. I know that some industrialists have been influenced by these ideas, by limiting the size of production units and multiplying them as business increases, or by splitting up factory organization into production teams. Thus, businesses, and even manufacturing plants, come in a large range of sizes. So do leaves. The smallest leaves— as on the tiny Lemna or azolla water plants or the filmy ferns from the tropical rainforest understory— are just a millimeter or two long (fig. 5.5). The largest leaves are those of palms. The longest such leaf is from the African raffia palm, at over 25 meters. Perhaps as big, if not as long, is the frond of the talipot palm, whose leaves are nearly 7 meters long with a much broader blade (fig. 5.6). Palms are a special case for large leaves. They produce a single trunk with a single meristem that

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Figure 5.5 Among the smallest of leaves are those of two aquatic plants. Left, leaves of duckweed; right, leaves of water fern (with leaves of duckweed for comparison).

Figure 5.6 The largest leaves are those of palms. Left, among the most massive are produced by the talipot palm, native to South Asia; the giant-leaved caryota (center and right) produces leaves about 7 meters long and 6 meters wide.

is the source of all leaves and the vertical growth of the tree. Equally impressive are the floating leaves of the Victoria lily, from the Amazon basin (p. 137). Its circular leaves are up to 2.4 meters in diameter (4.5 square meters), and photographs of a small child sitting in the middle of such a leaf come to mind (fig. 7.2). In general, leaf size is the result of the rates of cell division early in de-

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velopment as well as the degree to which such cells expand. Leaf size is a characteristic of a plant, with some plasticity of leaf size within a species, such as larger leaves produced in the shade. For tall trees, the size of leaves at the tip is limited by the capacity of the plant to supply carbohydrates for growth (p. 210). A commonsense view of leaf size is that larger leaves should be cheaper to make and more cost-effective. If that were true, then we might expect a trend toward fewer and larger leaves on plants, perhaps even a single large leaf. I know of such a plant in Southeast Asia, Monophyllaea, a genus of tropical rainforest understory herbs in the African violet family (p. 121). In this plant’s development, a single cotyledon continues to grow and becomes the single large leaf. Flowers and then fruits develop from the base of the leaf. This plant is an odd exception to the rule. In reality, there are a number of constraints on leaf size. First, consider the role of the leaf in the life of a plant. Leaves are produced in locations where their probability of capturing light is the greatest. Leaves generally grow larger under shadier conditions. Leaves of flowering plants always develop in association with meristems at their base, which may develop into shoots. The more meristems on the plant (and some think of a plant as a sort of “population” of meristems), the greater potential for future growth there is. Second, as leaves grow larger, there is a thicker layer of still air, the boundary layer, on the surface. This layer is a resistance to gas exchange and cooling when in direct sunlight, and large leaves may heat up so much that photosynthesis is reduced (p. 170). Third, the construction costs of larger leaves are actually greater per unit area. All leaf surfaces require support tissue in veins, petioles, and stems. Large leaves have more support tissue in the leaf itself. Since the leaf is a disposable organ, more permanent and costly tissue is lost when a large leaf falls from the plant. Larger leaves are associated with larger stems; this relationship was first proposed by the great tropical botanist E. J. H. Corner over sixty years ago— now known as Corner’s rule. Most large leaves are compound— that is, the leaf itself consists of several segments (app. A), but the leaf develops and falls from the plant as a single unit. Most large-leaved trees in the tropics grow quickly as pioneer plants when forests are cut down or disturbed. These trees produce thick twigs and branch sparingly. The leaves are highly productive and short- lived, and the trees are shaded out by slower- growing and more shade-tolerant trees. Plants with the largest leaves are all members of the palm family, almost exclusively tropical. The leaves of palms are almost always compound, and the narrow segments help them to dissipate

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excess heat. Since palms grow from a single meristem, its leaves are produced at quite regular intervals, in a predictable arrangement, and palms slowly increase in height. The leaves of bananas and their relatives among the gingers are large, but their edges tear and produce much smaller segments, much like compound leaves. So, leaf size is constrained within the economics spectrum. Some environments, particularly in dry climates or at high altitudes, may favor small leaves.

Economic Leaves Leaves may be economically valuable. We eat lots of leaves in salads or as cooked vegetables (see chapter 12). Furthermore, we use leaves as fiber, in ornamental horticulture, and as thatching for house construction in the tropics. For lettuce and kale, leaves are harvested at the end of the life of the plant, and harvesting does not affect the future growth of the plant. Other leaves, particularly in tropical forests, are produced continually, so their harvesting may affect the future growth of the plant. For the most efficient harvesting, the frequency, number of leaves taken, and their age may be important considerations. The most economically important leaf harvested for our use is tea; the young tender leaves are carefully plucked from

Figure 5.7 Tea plantations, as seen here in the Munnar region of Idukki district in southern India, have a distinct appearance because of the periodic harvesting of young leaves (photos courtesy of Lilly Margaret Eluvathingal). Left, tea picker; right, tea worker and estate.

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the highly pruned shrubs of tea plantations in mountains of the tropics (fig. 5.7). Tea cultivation is economically important in a number of countries with at least a foothold in the tropics: China, Vietnam, India, Bangladesh, Sri Lanka, Malaysia, Indonesia, and even a bit in Hawaii. The long history of cultivation has resulted in good knowledge of how to manage leaf production in this flowering shrub. Today there are many technical journals reporting on improvements in cultivation and in “tea plucking policies”: Two and a Bud, Tea and Coffee Trade Journal, Planters’ Chronicle, International Tea Journal, and so on. The best quality is still picked manually by skilled pluckers, mostly women, working in the early mornings. In high-quality tea, the bud and second and third leaves are plucked carefully and laid on flat basketry; such labor is a major cost in tea production. Mechanical harvesting results in lower-quality tea and some damage to the shrubs. With the proper plucking frequency, around once a week, and care not to damage other leaves, the practice is sustainable. Even the same uniform variety of tea will vary in yield and quality depending on the location grown, and plantations have to adjust fertilization and plucking frequency to optimize their profits. Other leaves are economically valuable in different ways. Leaves of species of wild hollies (Ilex species) have been important sources of caffeinerich teas, the most important of which is yerba maté, grown in southern South America. Now some attention is paid to the frequency of harvest, and trees are even grown with other species in agroforestry plantations. The tendu leaves of an Indian tree (related to persimmon) are wrapped around tobacco to produce the Indian bidi (cigarette). This leaf collection supports the livelihoods of millions of rural tribal people. Leaves are also collected as raw materials for crafts (fiber), for roof thatching, and as decorations in the international flower trade. Throughout the tropics, palm leaves are always important contributors to the income obtained from non-timber forest products. In south Florida, the Miccosukee and Seminole Indians construct the roofs of their open pavilion homes from the thatching of the sabal palm, still quite common in the remaining wilds (fig. 5.8). Such thatching is employed in home construction throughout the tropics (p. 254). Although not as durable as corrugated metal roofs, palm thatching is cooler and a lot quieter during the frequent rainstorms. The sustainability of palm harvests for home construction requires some discipline in the frequency of harvesting palm fronds from individual plants, and research in those areas may help preserve those harvests. Small understory palms are also collected as foliage for floral bouquets, particularly in

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Figure 5.8 Traditional housing of the Miccosukee and Seminole tribes in south Florida. Left, sabal palm; center, pavilions with thatched palm roofs; right, roof details.

Mexico. Again, care in the frequency of harvests, along with the numbers and ages of fronds, will ensure that the collection of these palms can continue. Often collections are not sustainable. Occasionally, young PhD students from North America and Europe spend a couple of years collecting data on the production of leaves and their harvest. In the case of leaves for thatching, they are determining the lifetime of their use. This is information on the economics of leaves, and it may provide the collectors with the information they need to maintain the populations of palms for harvesting into the future. I began this chapter discussing the application of economic principles to understand the biology of leaves. Now I end it by discussing the application of biological research on leaves for an economic purpose. We’ve come full circle.

Chapter Six Metamorphosis The rich profusion thee confounds, my love, Of flowers, spread athwart the garden. Aye, Name upon name assails thy ears, and each More barbarous-sounding than the one before— Like unto each the form, yet none alike; And so the choir hints a secret law, A sacred mystery. Ah, love could I vouchsafe In sweet felicity a simple Answer! johann wolfgang von goethe, “The Metamorphosis

of Plants” The question spirals down his throat and lodges in his ribcage. It is conch; a flowering artichoke; a cochlea that hears only pulse. As he wanders the cathedral gardens of Pisa he sees it in everything. The tower straining for it. He feels its pressure when he inhales: a bruise, a colour breathing into life, the small ache of coming back to himself while spinning further away. sharon black, “Fibonacci Takes a Walk to Clear

His Head”

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t may seem a little odd to begin a chapter about the development of leaves with the title “metamorphosis,” a word we commonly associate with the development of an adult butterfly from its caterpillar. Yet the word has a long history and, subsequently, a much deeper and broader meaning than its limited use today. It comes from the Greek metamorphoun, meaning transform or change shape and contains two roots, meta (above or besides) and morphe¯ (pertaining to form), and it means “the action or process of changing in form, shape or substance, as by more fundamental or higher means.” Leaves have inspired much study along the latter lines, traditionally part of the fields of morphology and morphogenesis; these are less popular topics of study today and have been integrated into the field of plant development. Leaves, because of their remarkable symmetrical shapes and the patterns of their arrays on stems, have engendered much classical research and continue to inspire us. Greek philosophers set the context for much of that research. Pythagoras of Samos (c. 570–495 bce) may have been the first philosopher (actually coining the name philosophos). He established a school of mathematics and philosophy with a strong spiritual bent. Aristotle (384– 322 bce) wrote: “The so-called Pythagoreans, who were the first to take up mathematics, not only advanced this subject, but saturated with it, they fancied that the principles of mathematics were the principles of all things.” This philosophy has been succinctly summarized as “all is number.” Since numbers could explain the patterns of nature, from small to large, Pythagoras has often been associated with the Hermetic tradition and the saying “as above so below.” The Pythagoreans influenced Plato, who established the theory of forms (or ideas); he taught that refined and abstract ideas, and not the world of perception, provide the most fundamental experience of reality— and only their study yields genuine knowledge. This philosophical position was illustrated by his famous “Allegory of the Cave,” which was assimilated by a succession of philosophers and was an influence when the scientific method was established in sixteenth-century Europe. In his Natural History of Plants, Theophrastus described in some detail the leaves of the Greek plants he observed. He knew that leaves developed from buds on plants and noted the differences in timing and the rapidity of the opening of leaves among different plants. Yet he knew nothing of what went on inside of the buds; careful dissection would have revealed the varying sizes of young leaves, even with the naked eye. His use of careful observations to build up broader principles about plants was a very different method than that advocated by Plato. Theophrastus was influenced

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Figure 6.1 Royal Society portraits of Nehemiah Grew (left) and Marcello Malpighi (right).

by his teacher Aristotle, who left Plato’s Academy to observe nature on the island of Lesbos. In the seventeenth century, a scientific understanding of the development of leaves was established by the research of two remarkable scientists, Nehemiah Grew and Marcello Malpighi. Both were influenced by the earlier research of Robert Hooke, and they collaborated amicably during their careers. Nehemiah Grew (1641–1712; fig. 6.1) grew up in Warwickshire, England, under the influence of his father, a “nonconformist” clergyman persecuted for his religious views. Grew graduated from Cambridge in 1661, and then he studied medicine at Leiden in the Netherlands, an important center of learning, for botany in particular. He had a long and illustrious career as a physician. His botanical research was conducted as a “hobby,” beginning in 1664. He was elected a member the Royal Society of London in 1670 for his plant anatomical contributions and was appointed a secretary of the society in 1677. His remarkable Anatomy of Plants, a summary of his work during the previous eighteen years, was published by the Royal Society in 1684. He was an extremely industrious and energetic person, of very pleasant disposition. Marcello Malpighi (1628–1694; fig. 6.1) grew up in a wealthy family near Bologna, Italy. At seventeen, he studied philosophy and physics at the University of Bologna. After caring for his terminally ill parents, Malpighi

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returned to the University of Bologna in 1654 to study human anatomy and medicine. In 1656 he began an academic career, first at Pisa and then the Academy of Messina. In 1663 he returned to the family villa near Bologna, to practice medicine, beginning his research on plant anatomy that same year, partly as a comparison with his research in human anatomy. He published his discovery of capillaries (which completed the circulatory cycle suggested by Harvey) in 1661 and became a corresponding member of the Royal Society of London in 1668. His book on plants, Anatome Plantarum, was published in 1675 and 1679. He finished his distinguished career as a papal physician, dying from a stroke in Rome at sixty-six years old. As members of the same scientific society, it was easy for these two illustrious men to obtain information about each other’s research. Their relationship was remarkably cordial, especially in comparison to Malpighi’s vitriolic treatment by Italian rivals. The works of Grew and Malpighi were not merely a series of microscopic observations, taking advantage of new technology. They did use microscopy extensively, but coupled that with careful direct visual observations of the plants. This integration of different observations helped them establish an approach to investigating the de-

Figure 6.2 Drawings of seed bean seedlings by Nehemiah Grew in his Anatomy of Plants, plumule (and developing leaves) clearly visible.

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velopment and function of plants, what they both called the economy of plants (see p. 91). They established the modern science of botany. Both scientists determined the structure of the embryo, or future plant, in the seed (fig. 6.2). They observed the embryonic leaves, or cotyledons. They also observed the initial growth of the seedling and the formation of adult leaves. Grew called this developmental structure the plume (today known as the plumule): “Divided, at its loose end, into divers pieces, all very closely couched together, as feathers in a bunch; for which reason it may be called the Plume.” Close observation revealed a succession of leaves of smaller sizes toward the interior of the buds as “central and minuted Leaves, which are five hundred times smaller than the outer: both which in the Cautious opening of Germen may be seen.” Grew called this developmental structure in the embryo, at the tips of branches in the growing plant, the “germen” and also the bud. Both scientists documented the structure of the bud, with developing leaves, as in Malpighi’s drawing of the bud of an edible fig (fig. 6.3); they were aware that the leaves were formed within the buds many months prior to their opening. Both scientists documented the vascular tissue as veins in leaves, and also the continuous connection

Figure 6.3 Renderings of an edible fig stem, by Marcello Malpighi from his Anatome plantarum, showing young leaves (left) and the vascular connections between leaf and stem (right).

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Figure 6.4 Leaf vessels. Left, revealed in grape leaf dissection; right, in young borage leaf, from Nehemiah Grew, The Anatomy of Plants.

with vessels in the stems. Malpighi’s rendering of a fig stem (fig. 6.3) shows his drawing style of leaving out extraneous details and emphasizing the functionally important structures, in this case the vessels connecting leaf to stem. In contrast, Grew included a detailed drawing of a young borage leaf, with vessels shown in detail. He also made an imaginative drawing of a grape leaf dissection, with vessels exposed between two intact portions of the blade (fig. 6.4). Both men knew human and animal anatomy well, particularly Malpighi, and contrasted the veins of animals with the vessels of plants, speculating on the movement of air and sap through them. At the end of Malpighi’s plant anatomy book, he added the dissection of a chick embryo, illustrating the network of veins around the yolk. Grew also revealed the numerous ways in which compact leaves in buds could unfold and expand. He was aware of the circular unfolding of fern leaves, the un-crumpling of other leaves, the unrolling of long leaves, and

Figure 6.5 Leaf expansion within buds. Center, uncurling of Angiopteris fern leaf; left, uncrumpling of leaves of the wild coffee plant; right, direct expansion of robusta coffee leaves.

Figure 6.6 Geometric illustrations by Nehemiah Grew. Left, diagram of large-leaved laserwort, showing the constancy of leaf proportions with development; right, drawing of mallow leaf, showing the constant angles of veins.

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the flat extension of some small leaves (fig. 6.5). He was struck by the uniform development of plant leaves, keeping their form independent of the final size (fig. 6.6). He was also interested in the way that secondary veins were produced in lobed leaves at very fixed angles (fig. 6.6). Grew was a very religious man and saw the details of geometry in leaves as signs of the artistry of the divine Creator, suggesting a little Pythagorean influence. The discoveries of Grew and Malpighi were unmatched for some 150 years. During that time the bud remained a black box, much as the chloroplast was for students of photosynthesis. Perhaps the bud was more like one of those wooden Russian Easter eggs, where removing the outer one reveals another inside, and so on. In the nineteenth century, advances in microscopy and the staining of biological tissues helped to reveal more details in the structures of organisms, to elucidate the cell theory, followed by the discovery of cell division. Staining also helped reveal the process by which leaves were developed in the buds.

Leaf Formation For all seed plants, the bud contains a small region of dividing cells (a meristem, or the plant’s equivalent to stem cells in animals). These cells divide and produce other cells that form the organs of the shoot. The terminology for parts of the meristem has changed over the years, and today we see the organization as layers, termed L1, L2, and L3 (fig. 6.7). These layers, particularly L1 and L2, divide in a direction parallel to the surface (periclinally). Beneath the tip there is a region of little cell division, and below that a central region whose cells primarily divide to produce the cells of the growing shoot. Leaves form when cells of the outer shoot layers divide, causing the tissue to swell and protrude (fig. 6.7). These protrusions, leaf primordia, develop into leaves. The elongated primordium of a dicot flowering plant is like a post, and that of a monocot grass, like maize, forms a collar around the meristem. In grasses and related plants, that region continues to produce new cells near the base and the leaves continue to grow in length— as any suburbanite who mows a lawn will appreciate. In broad leaves, cells in regions of the primordia divide, producing the blade toward the tip, and the petiole at the base. Cells at the edge of the blade continue to divide to produce the full blade, and different rates of cell division and expansion along the edge help to establish the shape of the blade. The layers of the shoot meristem contribute to the different tissues of the leaf. The L1

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Figure 6.7 The shoot apical meristem (SAM). Top left, diagram, double-ended arrows indicate directions of cell division; top right, SAM of castor bean, with leaf primordia; middle right, scanning electron micrograph of green champa SAM (courtesy of Usher Posluszny); bottom left, celery cross-section; bottom center, detail of previous with SAM at center; bottom right, scanning electron micrograph of celery SAM (courtesy of Roger Meicenheimer), showing the locations and sizes of leaf primordia.

layer produces the outer layer or epidermis, and the L2 layer produces the interior photosynthetic tissue. The veins, or vascular tissues (xylem and phloem, p. 204) are mostly derived from the L3 layer. Leaves generally have an upper and lower side, and the lower side (the undersurface) develops stomata in varying patterns (fig. 9.7). Meristematic cells persist at the base of the young leaf and develop into buds for future shoot growth. Buds, conspicuous in temperate trees in the spring, enclose the young leaves and future shoot. They are not so conspicuous in tropical plants, where leaf development proceeds more rapidly, and may help explain the differences in leaf shapes between tropical and temperate plants. As the leaves de-

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velop, the shoot elongates, from the production and expansion of cells from the central apical zone. The positions of primordia on the meristem, their rates of expansion, and the rate of shoot elongation all help determine the arrangements of leaves on the stem. This simple process, verified by numerous microscopic studies of many plants, begs some more fundamental questions: How are positions determined for the formation of leaves on the meristem? How are cell division and expansion controlled during development? How does the leaf determine its upper and lower side? How does a leaf determine its size and shape? These questions have been at least partially answered for some plants by the application of the techniques of molecular genetics. It helps to review some of the history behind those techniques before describing some of the mechanisms.

Mutants and Models For the organisms important to us, we have always been sensitive to differences among individuals that would improve their value, as greater crop yield, easier harvesting, better taste, or attractive appearance. In my front lawn there is a variety of the copperleaf, a tropical ornamental shrub, with extremely narrow and variegated leaves. Occasionally the plant produces a shoot with much wider leaves, one that has reverted to its original and less attractive condition (fig. 6.8). Naturalists and scientists were interested in such odd features, whether due to accidents of development or due to mu-

Figure 6.8 Mutants. Left, the copperleaf plant, variety “marginata,” in my front yard, which produces the preferred narrow leaves and occasionally reverts to the ancestral wide leaves. Right, a plant “monster,” depicted by Michael Masters (1869), leafy stamens from a peony.

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tations (heritable changes), and they were often horticulturally valuable. Freaks of nature made their way into the curiosity cabinets of wealthy European merchants during the Renaissance, along with rare shells and dried specimens of tropical organisms. Many of these plant monstrosities were documented and popularized by Michael Masters, an English naturalist in the mid-nineteenth century (fig. 6.8). After Mendel’s laws of inheritance were rediscovered at the end of the nineteenth century, biologists could cross organisms to determine the inheritance patterns of such mutations. In order to work out patterns of inheritance, certain organisms were studied in more detail. Among plants, these tended to be important crops. Among animals, these tended to be organisms that had short life spans (so that results of crosses could be analyzed quickly) and different properties that made them biologically interesting. Increasingly, research focused on these few model organisms whose names may be familiar to many of you: the house mouse, the domestic rat, E. coli (a common human intestinal bacterium), the fruit fly, yeast, the slime mold, and, more recently, the roundworm (Caenorhabditis elegans) and the stickleback fish. Unfortunately, plant research was focused on important crops that didn’t have optimal properties for laboratory research: rapid growth, small size, and a short life cycle that would allow thousands of them to be quickly and conveniently grown in or very near the laboratory throughout the year. A small European herb, the thale cress (Arabidopsis thaliana; fig. 6.9) was suggested as an ideal plant for research in the late nineteenth century, championed by the German botanist Eduard Strasburger and his student Friedrich Laibach. Arabidopsis, as it is now widely known, was an ideal research plant for many reasons. It is a small compact annual herb of the mustard family, related to kale and other crop plants. It is a compact plant growing from a rosette of flat leaves, and matures in about forty days. Arabidopsis has naturalized in many locations, including the temperate regions of North America, and has produced many different forms. It has only five pairs of chromosomes. Its genome was sequenced in 2000 and is of moderate size. Mutants, as of leaf forms (fig. 6.9), have been identified and produced. Slow to be adopted, Arabidopsis became important in plant genetic and molecular biological research around 1980. Most of what we now know about plant— and leaf— development has been derived from research on Arabidopsis, and then applied to other species. A pioneer in such research has been Elliot Meyerowitz, a professor at Caltech, whose research I’ll mention later on in this chapter. The widespread use of this little plant followed the revolution in mo-

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Figure 6.9 Photographs of the thale rock cress, more commonly known as Arabidopsis and scientifically as Arabidopsis thaliana. Top left, flowers; bottom left, a typical plant; and right, a composite diagram showing leaf mutants in Arabidopsis.

lecular biology, where techniques were developed to isolate and amplify genes (segments of DNA). It became possible to identify the DNA of the variant gene of a mutant plant, isolate and amplify it, use it to identify the normal gene, and then to study the protein products of the genes and their functions in plant cells. This DNA sequence could also be used to produce the messenger RNA for the gene, and it was then possible to add a dye molecule or radioactive label and use it to hybridize with the native molecule in the tissue where it was expressed. This in situ hybridization technique made it feasible to localize the activity of genes in specific tissues and cells. Thus, a “tool kit” of techniques involving the manipulation of DNA and RNA became available in the 1980s and made possible the discovery of the other “tool kit”— of the regulatory genes that control the development of leaves. Using these techniques, genes that regulate the formation of leaf primordia were discovered. KNOX1 genes are expressed in the meristem and suppress the development of primordia. As the primordium is established, ASYMMETRIC LEAVES1 (a gene of the ARP type) is expressed (fig. 6.10) and suppresses the activity of KNOX1. YABBY and KANADI genes determine the upper and lower leaf surfaces. ANT and AN3 promote the de-

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Figure 6.10 Diagram showing the interaction of various genes influencing leaf initiation and early development of leaf primordia.

velopment of the leaf blade, made possible by the asymmetry in thickness. These form gene regulatory networks with still other elements. And so on. Their names are mostly acronyms describing defective mutations. Thus the KN in KNOX1 is an acronym for knotted roots. Knowledge gained from Arabidopsis development can be applied to other plants, looking for the same, or similar, regulatory genes. The new field of evolution and development (or evo- devo) has emerged with the goals of learning how these developmental processes have evolved. In plants, these regulatory genes have deep evolutionary roots, some related to genes with different functions in ancestral algae. Most of these genes have been “sequenced” (their nucleotide sequences determined) and their evolutionary histories, origins, and duplication and divergence into gene “families” can be traced. Alejandro Barbieri, a friend and colleague, is a cell biologist who works on “trafficking” between human cells. He has helped trace the genetic controls on the production of vesicles, by which products are moved into and out of cells. One of the key regulatory genes he studied is Rab5, a member of a family of regulatory genes that was first studied in guard cells of stomates; RAB = responsive to abscisic acid, a plant growth regulator that controls the opening of stomata. The KNOX and ARP genes are found in all land plants, and they are involved in the establishment of leaf

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primordia in Selaginella to produce microphylls (p. 31) as well as the more common megaphyll leaves in ferns and flowering plants. The same genes may control branching in mosses. Leaf size is also under developmental control, through cell division and cell expansion after division. Leaf size is influenced by the environment— light and moisture in particular. Two regulatory networks, partially overlapping, control rates of cell division and cell expansion and maturation. Thus, the leaf of a given size may have fewer and larger cells, or more and smaller ones. Leaves developed under water stress generally have more and smaller cells. Larger leaves developed in shade may have larger cells. The

Figure 6.11 A rare exception to the rule: continuing growth by leaves. Top left, compound leaves of Chisocheton, a mahogany family member from Borneo (courtesy of Jack Fisher, with unnamed graduate student for scale); and top right, detail of leaflet growth at leaf tip. Bottom, continuing growth in leaves of Lygodium, the Old World climbing fern; left, fern covering vegetation in south Florida (courtesy of Tony Pernas); and right, growing tip uncurling from leaflet.

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production of stomates on the leaf surface is also under genetic control and influenced by moisture stress (higher density) and shade (lower density). These processes are interesting to study because they provide an opportunity to learn how the physical environment influences genetic expression. Light, moisture, and other environmental factors influence leaf size by affecting the plant as a whole, as well as the leaf primordium directly, so it is a bit simplistic to say that cell division and cell expansion are the sole factors. Part of my past research studied the influence of shading (both the intensity of light and its quality) on leaf size. Some leaves are simple (with a petiole and single blade), and others are compound (with a petiole and multiple leaf segments; see Appendix A). The development of compound leaves is influenced by additional genetic controls. Yet both leaf types originate from primordia and are determinate in growth; they grow into mature organs of a small range of sizes and do not produce flowers and fruits. Every time such a rule is written, exceptions quickly come to mind. For instance, in compound leaves of a few tropical trees, a meristem is retained at the tip and additional segments are produced; my good friend Jack Fisher has studied this in detail (fig. 6.11). In the Old World climbing fern Lygodium, the leaf tip maintains the ability to develop further. The leaf continues its compound growth as a relay of segments, and it eventually reaches lengths of 50 meters (fig. 6.11), helping to make it an invasive exotic in south Florida. Just as rarely, leaves in a few plants maintain the ability to produce new cells at maturity, producing flowers on the upper surface or plantlets on the leaf margins (fig. 6.12).

Figure 6.12 Epiphylly. Left, flowers are produced on leaves in the tropical Asian plant Monophyllaea; right, young plantlets are produced on the leaf margins of bryophyllum plants.

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Figure 6.13 Juvenile and adult leaves (heteroblasty). Left, Monstera tenuis, Costa Rica: juvenile shingle leaves and large highly lobed adult leaves. Right, cat’s claw vine: bottom, juvenile single leaves; center, intermediate two-part leaves and tendrils; right, adult, larger single leaves and flowers.

Most plants alter the shape or size of leaves during the progression from juvenile to adult stages, a phenomenon called heteroblasty. The most obvious change in leaf shape is between the embryonic leaves, or cotyledons, and subsequent leaves produced from the meristem. Even from the meristem, leaf morphology may change during development, as in Arabidopsis. In many vines, leaves quite abruptly change morphology at a certain stage, shifting from juvenile to adult. These changes are often associated with plant height and exposure to more light (fig. 6.13). Finally, because we have defined a leaf by its position on the meristem and its determinate development, in some

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cases the result is a structure quite different than what we’d think of as a leaf, such as a twining tendril, a spine (as in cacti), or even an insect trap (Appendix A). These structures are all the products of development from primordia on a shoot apical meristem— and of regulation by genes.

Phyllotaxis Leaves, produced from the shoot apical meristem, appear on the mature stem in many patterns; such leaf production is called phyllotaxis. The patterns are influenced by the size of the meristem, the rate of leaf development, and the rate of shoot expansion. None of the regulatory genes that I’ve previously discussed explain how these patterns unfold. The position and sequence of primordial establishment is important, yet the mechanisms of gene activation and suppression do not explain this pattern. If you look at the plants in your garden or in a nearby park, you will see a variety of arrangements among very common plants: leaves in alternate positions down the stem, several leaves at a single position (whorled), and pairs of leaves opposed on the stem (Appendix A.6 ). In palms and their relatives, these differences produce quite spectacular patterns (fig. 6.14). In the majority of palms, the positions are alternate, but crowded together on the tips of trunks. The triangle palm from Madagascar arranges leaves in three vertical rows. In the traveler’s palm, also from Madagascar and related to bananas, the leaves are produced in two opposing vertical rows. In the screw pines, native to the Old World tropics, those vertical rows of succeeding leaves spiral around the stem.

Figure 6.14 Leaf positions at trunk tips in woody monocots. Left, spiral leaf positions in a screw pine from tropical Asia; center, three rows of leaves (tristichous) in the triangle palm from Madagascar; right, two rows of leaves (at 180°, or distichous) in the traveler’s palm, also from Madagascar.

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Figure 6.15 Flower and leaf arrangements, or phyllotaxis. Left, disk flowers in the sunflower show spirals clearly; center, succeeding leaves in the dinner plate plant from the Canary Islands reveal spirals similar to the sunflower; and right, young and mature leaves of an ornamental kale plant.

In the alternate leaf arrangements seen in most plants, a spiral is also formed but is not easy to see because of the long distance between succeeding leaves on the stem. However, there are a few plants where the shoot elongation is slow and leaves are close together; in such plants, the spiral arrangement is easy to see. Thus, some of the work on phyllotaxis has used compound flower heads, as the sunflower (fig. 6.15). However, an excellent example is a small succulent cushion plant growing in the mountains of the Canary Islands and cultivated in rock gardens: the dinner plate plant (fig. 6.15). The compact heads of ornamental kale also suggest these spiral patterns (fig. 6.15). Patterns of phyllotaxis are established in the shoot apical meristem, and there has been much speculation and research on this subject. Wilhelm Hofmeister (1824–1877), perhaps the greatest botanist in the nineteenth century, noticed that subsequent primordia develop away from the first one, in a position of available space, eventually filling the meristem and producing spiral patterns. Later on, packing efficiency was suggested as the basis for phyllotactic patterns. Alan Turing— known for his crucial work in cryptography during World War II and his contribution to the conception and construction of computers— proposed a “morphogenetic field hypothesis” in which inhibition of development in certain regions could be broken. He actually was writing a manuscript on phyllotaxis when he ended his life. Soon, attention turned to the potential role of auxin, the first growth regulator discovered. Its function was first suggested from experiments by Charles and Francis Darwin, and further revealed by the Dutchman Frits

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Went in 1926. We now know that the genes associated with leaf primordial establishment help this molecule accumulate, reducing its concentration in nearby tissues and thus inhibiting the development of new primordia nearby. French physicists Stéphane Douady and Yves Couder developed an elegant system for demonstrating this pattern of development. It consisted of a shallow plate of silicone oil, magnetized along its edges. When droplets of a magnetic fluid were deposited on the fluid, they moved away from the previous droplets to a position at a very precise angle to the previous one: 137.5°. This is the golden angle that is associated with the golden ratio and the Fibonacci series. The golden ratio in a rectangle is a distance that cuts the rectangle into a smaller one, and the ratio of the total length to the dissected position is an irrational number (one whose length is infinite) of 1.61803. . . . The circle of the radii of the successively smaller squares forms a logarithmic spiral— seen in galaxies, cyclonic storms, snail shells, in the flower positions of the sunflower head, and in the placement of leaves in the dinner plate plant (fig. 6.16). This number was used by the Greeks in architecture and has been given the symbol Φ, or phi. Take a diagram of that same dinner plate leaf pattern, and look at the positions of leaves in order of appearance on the shoot apical meristem. The angles of subsequent leaves are about 137.5°. It is possible to find the spirals, or parastichies, moving out from the center (fig. 6.16). The leaves (or petals, or flowers), in contact with each other, form spirals seen in both directions. Typically the leaf number of successive leaves in contact looks like this: 1 2 3 5 8 13 21 34 55 89 144 233 377 and on

If you create a ratio with the larger number as numerator over the previous number as denominator: 2/1 = 2, 3/2 = 1.5, 5/3 = 1.67, 8/5 = 1.625 13/8 = 1.625, 21/13 = 1.616, et cetera, the ratio approaches the golden mean of 1.61803. . . . This number sequence was known to Indian mathematicians in the seventh century but was independently discovered and disseminated by Leonardo of Pisa (better known to us as Fibonacci and poetically described at the beginning of this chapter) in the thirteenth century. Take a little time to Google “Fibonacci,” “Φ (phi),” and the “golden mean”; a whole world (tens of thousands) of sites reveals itself, presenting ideas on the science and quasi-science of these numbers. Although many plants produce easily seen Fibonacci series, divergence angles, and elegant spirals, many do not. It may be difficult to accurately measure the angles and leaf positions because the primordia sizes may vary

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Figure 6.16 The logarithmic spiral and the golden mean. Top left, illustrated by a diagram; top right, seen in the shell of a chambered nautilus; bottom right, the positions of successive leaves and the Fibonacci series seen in a diagram of the dinner plate leaf (courtesy of Rolf Rutishauser); bottom left, the galaxy M74 (courtesy of NASA).

and the packing on the meristem may also vary. In many plants the divergence angles are quite different than 137.5°. Other numerical series can explain the phyllotaxes of different plants. The divergence angles and spirals in some plants may even change with growth. Stems often twist as they grow; these are a few of the many factors that reduce the likelihood of such mathematically elegant Fibonacci spirals. However, a divergence angle of 137.5° does ensure that leaves are less likely to occur beneath the leaf just above— and be shaded against capturing adequate sunlight. The succession of leaf primordia on the apical meristem can unfold to the left or the right, so the spirals can be left- or right-handed. In most plants, the handedness is random, about 50% for each direction. However, in some plants the direction can change during development, such as the lodgepole pine, or may be primarily in one direction, as with Alstroemeria. Remarkably, in coconut palms, the handedness of the spirals varies

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geographically. At northern latitudes, the spirals are predominately lefthanded, and right-handed at southern latitudes; variation in the geomagnetic field has even been suggested as an explanation for this distribution.

All Is Leaf We must ultimately turn to the botanical writings of Johann Wolfgang von Goethe (1749–1832; fig. 6.17), one of the greatest figures in the history of German culture. Goethe (for brevity’s sake) is best known for his literary work; The Sorrows of Young Werther (perhaps the first global best-seller) and Dr. Faustus are the best known. Goethe also was interested in science, particularly in physics (in his theory of colors), geology, and botany. His approach to science was a mixture of the poetic and empirical, which resulted in some goofy speculation and some important ideas. After early work in law and success in writing, Goethe joined the court of Karl August, Duke of Saxe-Weimar-Eisenach, and he began to study plants, inspired by the ideas of Linnaeus (p. 91). In 1786–88 he traveled in Italy to study plants and artistic traditions. It was there that his ideas about plant form matured and resulted in his short work The Metamorphosis of Plants, first published in 1790. Goethe searched for the fundamental rules behind the construction of

Figure 6.17 Johann Wolfgang von Goethe. Left, his portrait, completed during his Italian voyage in 1786. Right, a version of his Urpflanze, rendered by Pierre Jean François Turpin.

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plants. He looked in private and public gardens for the ideal plant, the Urpflanze, which would explain the diversity of plant form in the natural world (fig. 6.17). Implicit in his idea of form was its generative nature— that form would produce other forms, and that a certain form could be the organizational basis for an entire organism. It was during a visit of the Botanical Garden of Padua that he saw a venerable European fan palm (p. 11). Goethe determined this to be the archetypal plant, but how he did so is a mystery. Recently, scientists have revealed a contemporary archetypal plant, or a “sister to all flowering plants,” in a small tree growing only on a few ridges in New Caledonia: Amborella trichopoda. More importantly, Goethe raised the argument that the leaf is the archetypal organ of plants, resulting in the formation of the parts of the flower. Goethe used a method, outlined in his little book, of studying metamorphosis— change from one organ into another. Irregular metamorphoses were particularly useful to him, and they call to mind mutations transforming one organ into another, used by contemporary plant molecular biologists. In 1787 Goethe wrote: “I have realized, namely, that in that organ of the plant which we are usually accustomed to address as ‘leaf,’ the true Proteus lies hidden that can conceal and reveal itself in every formation. Anyways you look at it, the plant is always only leaf, so inseparably joined with the future germ (Keim) that one cannot think the one without the other.” It is not clear how influential this idea was; Goethe eagerly looked for supporters among scientists of the day, partly as a vindication of his research approach combining poetry and empirical observation. He did influence the young Alexander von Humboldt (p. 14), who met with Goethe before his epic voyage of exploration. Goethe admired Humboldt greatly. The odd prediction of Goethe, “all is leaf,” has been verified by research on the molecular genetics of flower development, pioneered by two outstanding scientists, Elliot Meyerowitz and Enrico Coen. Meyerowitz looked at homeotic mutants in Arabidopsis, and Coen in the snapdragon. In these mutants, flower parts are transformed into leaves or into other flower parts. Applying molecular techniques (p. 118), Meyerowitz developed a model for the control of flower development, soon verified by Coen in snapdragons: the ABC model (fig. 6.18). Flowers occur from the conversion of apical meristems at the tips of shoots. They consist of concentric whorls of flower parts. The outer whorl consists of sepals, and the next in of petals; these two parts are accessory to the actual reproduction of the flower. The inner two whorls consist first of the stamens and finally an inner whorl of one or more pistils. In the ABC model, genes interact

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Figure 6.18 Arabidopsis flowers. Top, diagram of the ABC model of floral development, first elucidated in Arabidopsis and snapdragon flowers; bottom left, normal flowers of Arabidopsis, Beth Krizek; bottom right, homeotic mutant in which flower parts have been converted to leaves (courtesy of Elliot Meyerowitz).

to produce the whorls of normal flower structures. Genes of the A and B classes specify the establishment of the outer whorl of sepals. Genes of the B and C classes specify the establishment of the second whorl of petals. Genes of the C class produce stamens, and a subset of those C class genes make pistils. Mutations of those genes, or loss of expression of normal genes, produce whorls with different organs. Certain mutations can produce “flowers” only with leaves (fig. 6.18). Further evidence for the relationship between leaves and flower parts is found in the influence of genes controlling leaf development; the YABBY and KANADI A genes that specify upper and lower leaf surfaces also influence the development of petals. The ABC model, with added D and E classes of genes influencing further flower development, seems to work in all flowering plants. It is pres-

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ent in the archetypal Amborella trichopoda. This small tree produces male and female flowers; the transitions between floral organs are gradual; and an ABCE model controls floral development. Thus, the general control of floral development was anticipated by Goethe, and most eloquently argued by Enrico Coen. In his Metamorphosis of Plants, Goethe wrote, “Whether a plant grows vegetatively, or flowers and bears fruit, the same organs fulfill nature’s laws throughout, although with different functions and often under different guises. The organ that expanded on a stem as a leaf, assuming a variety of other forms, is the same organ that now contracts in the calyx, expands again in the petal, contracts in the reproductive apparatus, only to expand finally in the fruit.” The earliest diverging plants (p. 29) consisted only of stems, and the earliest leaves were projections from the stems (microphylls) or the formation of blades from flat branching networks. Thus, the leaf cannot be the primordial organ in a deep evolutionary sense. However, the reproductive structures in early seed plants seem to have been derived from leaves (some of which bore spore-producing organs) near the branch tips. Since none of these plants exist today, we cannot delve into the genetic mechanisms the produced such structures. However, certain anatomical patterns seen in fossil plants may suggest the hormonal mechanisms of control— so, a careful examination of such plants may help.

Rules and Numbers In leaf development, we have seen attempts to find sets of simple rules that explain their formation, and simple mathematical expressions that explain their forms and patterns on branches. All things being equal, such simple explanations should be preferable to more complicated ones. This idea was raised by William of Occam in the fourteenth century, and it is a rule often applied to choosing among alternate explanations (Occam’s razor). Thus, simple geometric rules have been used to explain the form of a leaf (fig. 6.19), mathematical series and Φ to explain the arrangement of leaves on a stem, or even the application of fractal algorithms to explain the edges of leaf blades (p. 126). These simple mathematical explanations are attractive, even beautiful. For the visual patterns of organic form, as in leaves, we may have additional motivation for recognizing them, perhaps supported by aesthetic principles and geometric patterns intrinsic to our brain (p. 306). However, the enormous diversity and complexity of life makes the operation of simple rules throughout the tree of life difficult to discern. This

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Figure 6.19 Attempts to explain leaf shapes mathematically. Left, simple equation describes the expansion of a violet leaf (D’Arcy Wentworth Thompson); right, expansion of vein networks describes a fern leaf (Przemysław Prusinkiewicz).

diversity of forms of life suggests complexity not easily reducible to simple mathematical rules. We do have a rather simple explanation, the Darwin/ Wallace theory of natural selection, as to the process of how that diversity and complexity emerged. I am partial to the idea of the physicist David Bohm, that chaos is really the reflection of higher orders of complexity.

The End As a general rule, leaves live for a fraction of the life of the plant to which they are attached. Thus, a process of degradation (or senescence) is part of the leaf ’s overall development. In annual plants, the first leaves may be shaded out by the next leaves as the plant increases in height. In longlived trees, leaves may be produced during a growing season terminated by drought or cold. During the life span of a leaf, its form results from the developmental processes described in the previous paragraphs. Then there is a static period of maturity, when the physiological processes operate at greatest efficiency, followed by a slow decline in efficiency. The final stage in the life of a leaf involves the highly coordinated breakdown of organelles

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Figure 6.20 Two leaves in which disintegration of tissue is vital to leaf development. Left, holes in leaves of a Swiss cheese vine. Right, holes between veins in leaves of the window plant are due to the controlled disintegration of cells (courtesy of Arunika Gunawardena).

within cells and releasing nutrients (particularly nitrogen and phosphorus) for resorption by the parent plant. In chloroplasts, chlorophyll is broken down in a sophisticated process that minimizes damage by light-activated breakdown products, which end up in the cell vacuoles. At the same time, proteins involved in photosynthesis are broken down to amino acids, and those nitrogen-containing molecules are moved back into woody tissue, for reuse the following year. The metabolic pathways making pigments, as carotenoids and flavonoids, are also activated. Just as growth-regulating molecules, particularly auxin, are involved in the development of leaves, other molecules, particularly ethylene and abscisic acid, help regulate the death of leaves. The latter molecule derives its name from its promotion of the detachment of the leaf from a special zone, the abscission layer. Occasionally, this senescence process is involved in leaf development, in the production of holes and deep lobes of leaves, such as the numerous holes between veins of the lace plant, an odd aquatic plant from Madagascar, and the irregular holes and deep sinuses of the Swiss cheese plant, a vine of tropical rainforests (fig. 6.20). Even in these leaves, the end of leaf development is ultimately senescence and death. Then new leaves once more spring to life, either from expanding embryos in seeds or the resting buds of a plant.

Chapter Seven Architecture And see peaceful trees extend their myriad leaves in leisured dance— they bear the weight of sky and clouds upon the fountain of their veins. kathleen raine, “Envoi”

Perhaps the purpose of leaves is to conceal the verticality of trees which we notice in December as if for the first time: row after row of dark forms yearning upwards. linda pastan, “Vertical”

A

lthough leaves are often described individually by their architecture, this chapter is more about the architecture of plants, particularly trees, because it is primarily the display of leaves I am concerned about here. Leaf display profoundly affects their function and, collectively, the function of the entire plant. Architecture determines the amounts and timing of light absorption, and affects the exchange of gases by leaves.

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Art, Architecture, and Plants The study of plant architecture is intimately linked with the visual arts including architecture. Examining the history of art reveals the first attempts to study plant architecture. Later on, our understanding of the architecture of buildings gave us insights on the architecture and function of plants. The origin of the word “architecture” comes from the Greek architekto¯n, with its roots arkhi = forming and tekto¯n = builder. It means “the art or science of building, especially the art or practice of designing and building edifices for human use, taking both aesthetic and practical factors into account”— and this definition can be extended to other constructions, such as computer networks and trees. I enjoyed sketching and watercolor painting in my youth, painting landscapes of the canyons and mountains near my home. Drawing was also an important scientific practice in my early courses in biology. I quickly learned that my ability to render an organism with accuracy depended upon my ability to emphasize what was important and neglect the unimportant. In teaching, I introduced drawing exercises in my courses dealing with basic plant structure. Early scientists were often adept at drawing and used that skill to record observations and illustrate their work. Artists also attempted to draw plants with accuracy in landscapes and for still- life paintings. Drawing a tree accurately was a particular challenge. I’m amused by some illustrations of early expeditions to totally new places, such as Madagascar, and the inability of the accompanying artists to render the vegetation accurately (making plants look like their temperate relatives) or people (making them look like European peasants). Leonardo da Vinci (1452– 1519; fig. 7.1) was the first artist/scientist to make an effort to understand the architecture of trees. We know of him as a painter and perhaps as the most accomplished person in history. His drawings and written descriptions of tree architecture were published as A Treatise on Painting. Leonardo attempted to establish scientific principles, based on observations, for the accurate renditions of the human figure and of trees and landscapes. In his description of trees, Leonardo wrote that “all the branches of a tree at every stage of its height when put together are equal in thickness to the trunk,” and he used a lettered tree diagram to explain the relationship (fig. 7.1). Leonardo described basic relationships of succeeding branches in trees, and then compared the branching of trees

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Figure 7.1 Leonardo da Vinci. Left, portrait made around 1512, when he was actively working on plants. Right, illustration from his notebooks (letters reversed as was his practice), accompanying his comments on the branching of trees

to the branches of a river system. Leonardo did not base his comments on a single species and gave detailed descriptions of trees likely to be present in a European landscape. The elm always gives a greater length to the last branches of the year’s growth than to the lower ones; and Nature does this because the highest branches are those which have to add to the size of the tree; and those at the bottom must get dry because they grow in the shade and their growth would be an impediment to the entrance of the solar rays and the air among the main branches of the tree. The cherry-tree is of the character of the fir tree as regards its ramification placed in stages round its main stem; and its branches spring, 4 or five or 6 [together] opposite each other; and the tips of the topmost shoots form a pyramid from the middle upwards; and the walnut and oak form a hemisphere from the middle upwards.

I am reminded of those “how to draw” books, perhaps now replaced by “drawing for idiots,” with graphic instructions on how to draw a tree. Leo-

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nardo anticipated this need by showing artists how to draw plants, not just the architecture of a tree, but also in the ways that the tree crown and individual leaves reflect sunlight (p. 226). Leonardo drew various civil projects, including bridges, flying machines, military weapons, and so forth— but no buildings. However, other artists spent time in nature drawing and painting, and drew architectural inspiration from plants. A leader in this movement in Europe was John Ruskin (1819– 1900). In his long life, he attempted to fuse his love for art and nature with that for society. And art included architecture. Ruskin wrote, “It is not possible to find a landscape, which if painted precisely as it is, will not make an impressive picture. No one knows, till he has tried, what strange beauty and subtle composition is prepared to his hand by Nature.” The four architects and designers discussed here were strongly influenced by Ruskin, and all used various plant motifs in their designs. Owen Jones (1809–1874) was an English architect and designer who studied design in all periods of history, but particularly Islamic design as exemplified by the Alhambra, in southern Spain. His lifelong pursuit of design led to the establishment of the Victoria and Albert Museum, built around his collections, and the publication of The Grammar of Ornament, an authoritative compendium of design throughout the ages, still reprinted and used today. Plant motifs were conspicuous in this volume, but always rendered into a more abstract geometric form. Joseph Paxton (1803–1865) was a friend and collaborator of Jones. In his early teens, he worked as an apprentice in several gardens. His work attracted the attention of William Cavendish, the Duke of Devonshire, whose nearby Chatsworth Garden was one of the finest in England. The

Figure 7.2 The Victoria lily. Left, young girl sitting on a floating leaf, at Bok Tower Gardens in Florida; right, detail of venation from undersurface of the leaf.

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Figure 7.3 The Crystal Palace, constructed for the London Exposition of 1851. Left, exterior view; right, interior and landscaped view.

duke offered Paxton, at the age of twenty, the position of head gardener— which he held for thirty- five years. Paxton redesigned and expanded the gardens, and constructed some large glass houses for the display of plants. One of these houses was constructed to display the Amazon lily, a remarkable plant with huge circular floating leaves (p. 102), buoyant and strong enough to keep a child afloat. Paxton was inspired by the strong venation of this plant, particularly noticeable from the spiny undersurface (fig. 7.2). His knowledge of this leaf structure, plus experience in designing greenhouses, inspired his successful proposal, design, and construction of one of the most remarkable and successful buildings in human history: the Crystal Palace of the London Exhibition of 1851 (fig. 7.3). It was constructed of repeating (and mass-manufactured) elements of cast iron and plate glass. Although requiring thousands of workers, the building was completed in only ten months. It was 564 meters long, with a maximum height of 36 meters. Its 96,000 square meters (22 acres) of space housed more than 14,000 exhibitors. Owen Jones guided the interior decoration and organization of exhibits. His choice of primary colors of red, yellow, and blue (based on his studies of ancient Greek and Egyptian as well as Islamic design) was at first criticized— and then acclaimed. The Crystal Palace stood for eightyfive years, until it was destroyed by fire. Architectural designs based on plants are infrequent. However, the contemporary French architect Vincent Callebaut has proposed the construction of floating modules, like water lily pads, that could make up a

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Figure 7.4 Leaf-inspired contemporary architecture projects. Left, Lilypad, a conceptual design by Vincent Callebaut. Right, a Brazilian residence with a leaf-inspired roof by the Brazilian architects Mareines and Patalano.

marine city or be anchored near coastal cities (fig. 7.4). This remains a pipe dream, but on a smaller scale the Brazilian architectural firm of Mareines and Patalano has designed a unique home near Rio de Janeiro, with a leafinspired roof (fig. 7.4). More often than informing the design of buildings, plants inspire their decoration. No architects are better known for such embellishment than Antoni Gaudí and Louis Sullivan, both of whom lived and worked at the end of the nineteenth century (fig. 7.5). Gaudí (1852–1926) was raised in rural Catalonia and practiced architecture in Barcelona for most of his life. Gaudí spent much of his early summers in the natural setting of the family home. His experience informed the shapes of the projects he often undertook in an organic, seemingly undetermined fashion; the boundaries between the ornamentation and morphology of his projects were often indistinct. The most famous of his projects was the famous and unfinished cathedral Sagrada Familia, but numerous other examples of this work, such as the Park Güell (fig. 7.6), survive in the Barcelona region. Louis Sullivan (1856–1924) was born of immigrant parents and spent much of his childhood at his grandparents’ farm in Massachusetts, observing and sketching nature. He worked as an architect in Chicago, interrupted by studies at L’École des Beaux-Arts in Paris, and continued in Chicago and adjacent cities for most of his career. He is remembered for his design of the first “skyscrapers” and his influence on younger architects, particularly Frank Lloyd Wright. Sullivan had a clear idea about the impor-

Figure 7.5 Two late nineteenth-century architects inspired by plants. Left, Louis Sullivan; right, Antoni Gaudí.

Figure 7.6 Architectural design details. Left, detail of elevator gate from the Chicago Stock Exchange, designed by Louis Sullivan in 1893. Right, detail of gate at Park Güell, Barcelona, designed by Antoni Gaudí in the early 1900s.

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tance of decoration in his building projects, and he borrowed heavily from nature. His building decorations, both exterior and interior, often used leaves and foliage and are admired for their lasting beauty— a highlight in the illustrious architectural history of Chicago (fig. 7.6). Sullivan wrote: But for this we must turn again to Nature, and hearkening to her melodious voice, learn, as children learn, the accent of its rhythmic cadences. We must view the sunrise with ambition, the twilight wistfully; then, when our eyes have learned to see, we shall know how great is the simplicity of nature that it brings forth in serenity such endless variation. We shall learn from this to consider man and his ways, to the end that we behold the unfolding of the soul in all its beauty and know that the fragrance of a living art shall float again in the garden of our world.

Francis Hallé and the Architecture of Tropical Trees Two contemporary biologists, Francis Hallé and Henry Horn, have contributed greatly to our understanding of tree architecture, Hallé with a morphological approach to the architecture of tropical trees, and Horn with a pioneering mathematical approach. Francis Hallé (figs. 2.14 & 12.3) grew up with his family on a twohectare parcel in the countryside outside of Paris in the years before and during World War II, and his love of nature was nurtured by his mother’s gardening, exploring the woodlot at the rear of the property, and his elder brothers, both of whom worked in the tropics. In school he developed an interest in architecture and spent some time sketching chateaux in the Loire Valley. He then pursued university studies in botany and began visiting the tropics. He continued drawing, maintaining an interest in the art of French comic books (la bande dessinée). In the field, he filled notebooks with drawings of plant phenomena, something he continues today (fig. 15.10). In his work for the French overseas development agency, Hallé was able to observe trees of the African and New World tropics, and later on in Southeast Asia, and his drawing helped him observe trees in novel ways. Hallé was influenced by the eminent English botanist, E. J. H. Corner, who also drew plants from nature. Hallé observed the different processes for the growth of branches, along with the types of branches composing a tree, and he developed the concept of tree architecture. He wrote, “The concept of architectural modeling is a dynamic one, since it refers to the genetic infor-

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mation which determines the succession of forms of the tree, analogous to the blueprint which is the plan of a machine.” His approach provided the classification of models of architecture into different categories.

Branches To understand his architectural models, it is necessary to understand the types of branches a tree— or plant— can produce. Any branch has an apical meristem (fig. 6.7), which produces leaves or flowers and elongates to allow the leaves to be positioned along its length. Additional meristems establish from the base of each leaf. The dividing meristem cells (“stem cells” in animal parlance, p. 114) represent the future growth of the plant. They maintain some autonomy, yet are under some control from other parts of the plant via the influence of growth regulators. Thus, the concept of individuality in a plant is different than most animals, and a plant is sometimes considered as a “metapopulation” of these semi-autonomous units, the shoot apical meristems and underlying stems. We now know that individual meristems may rarely be genetically differentiated from each other, and such differences were detected early in the discovery of new tree fruit varieties. Shoots can vary in a variety of ways. First, they differ in the positions of leaves. Shoots may produce leaves around the stem, seen as a spiral whether in an alternate or opposite position. Shoots may also produce leaves in a flat plane, whether due to the position of the leaf on the stem, or by the bending of the petiole (fig. 7.7). Second, shoots vary in their patterns of growth. Some shoots grow continually, and then apical meristems some distance below the tip may produce secondary shoots. As long as the apical meristems are not damaged, the shoot can grow indefinitely, perhaps even for centuries (fig. 7.8). However, the apical meristem can become reproductive, producing a flower (or inflorescence— many flowers) and fruit. This stops the future growth of the shoot tip. Thus, the positions of flower production can dramatically alter the growth of a plant (figs. 7.8 & 7.10). In some cases, the shoot extends very slowly at first and more rapidly later. Alternatively, the shoot may extend rapidly at first and very slowly later on. The slow growth then crowds the leaves at the tip of the shoot. Finally, some shoots may only grow very slowly, showing little branch extension but producing many leaves together. The architectural models of plants are assembled from one or more of these types of branches. The branching of plants varies as a consequence of the activity of the apical meristem in relationship to those meristems farther down the shoot,

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Figure 7.7 Leaf arrangements on stems. Left, in a spiral around the stem in the prickly paperbark; right, as a flat plane on a horizontally oriented branch in American beech.

Figure 7.8 Diagrams of tree architecture, after Hallé. Left, monopodial growth and the model of Rauh; right, evenly divided terminal branching and the model of Leeuwenberg.

at the leaf bases. Typically, secondary branches originate from one of the leaf base meristems, and flowers also originate from some of those lateral meristems. Thus, the branches are always subsidiary in relationship to the leader, which grows indefinitely. Most temperate trees branch in this manner, such as oaks, and Hallé defined this pattern as monopodial (fig. 7.8). In some trees, the growth in height, or at the tips of lateral branches, is terminated, perhaps by flowering or slowing the extension growth to crowd

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Figure 7.9 Sympodial growth and the model of Aubréville. Left, Hallé’s diagram; right, an example: the Indian almond tree, growing in Miami.

leaves together at the tip. If the growth of the shoot tip meristem ceases, subsequent elongation of the branch or trunk is due to the activation of a lateral meristem just beneath the tip. Here, the vertical growth of the trunk or lateral extension of branches is a relay of individual branches replacing each other, a pattern defined as sympodial (fig. 7.9). Finally, subsequent growth of the trunk or branch is due to replacement by two or more lateral meristems beneath the tip (fig. 7.8). In several palms, a true dichotomous growth pattern is caused by the actual splitting of the apical meristem. These shoot types and branching patterns were the simple units that Hallé used to establish a system for comparing and classifying architectural models of trees. He conducted his research by observing seedlings and saplings of adult trees in the tropics, as snapshots in a long developmental process, where a diversity of architectural types could be discovered. If he had initiated this project in his native France, the patterns would not have been available. In many cases, the growth patterns had been described by experts of individual tree species, and he named his architectural models after those experts. Hallé originally described this system of tree architecture with Roelof Oldeman, his Dutch graduate student, in 1970. The expansion of these ideas, with the additional expertise of Barry Tomlinson, led to the publication in 1978 of what is now one of the classical works in tropical botany, Tropical Trees and Forests: An Architectural Analysis. The authors described twenty-three such architectural models; in more recent years, Hallé has added several more. Still, the number of models is not large. The simplest architectural model is a single shoot, with no lateral

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Figure 7.10 Palm architecture. Right, the model of Corner (after Hallé), with the example of the foxtail palm, where flowering does not affect continuing growth. Left, the model of Holttum, with the example of the talipot palm, where flowering and fruiting ends the activity of the apical meristem, and the plant dies.

branches and a single apical meristem at the tip. That is the architectural model of many of the palms studied by Tomlinson throughout his long career and named by Hallé after his tropical botanical mentor, Corner (fig. 7.10). Their often huge leaves are produced in a cluster at the tip of the trunk. The trunk is uniformly thick from base to tip, due to the single meristem and a thickening region just below it, and the absence of any secondary growth. This means that the growth of a centuries-old palm is due to the continued activity of that meristem, and, as Tomlinson has pointed out, the living cells in the trunk of the palm are thus centuries old, the longest-lived cells in any organism. In a few palms, and even quite massive ones, after forty or so years of growth, the apical meristem becomes reproductive and produces an inflorescence and fruits; the entire tree then dies (that model is named after another tropical botanist, R. E. Holttum; fig. 7.10). Branched trees are produced by different architectural models. Many consist of identical branching units. Some trees split from previous branches that have flowered. This process repeats itself to produce a tree that looks a little like a candelabra. A common temperate tree with such architecture is the sumac, and a common tropical tree is the frangipani (fig. 7.8). Another model with identical branch units is seen in many legume trees, that of Troll. Here, the initial shoot produces a flat plane of leaves. After some vertical growth, this shoot bends and is replaced by a second one, and so on (fig. 7.11), and the bases of the succeeding shoots produce a vertical trunk. A

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Figure 7.11 Left, the model of Troll (after Hallé); right, the example of a poinciana tree.

common and spectacular flowering tree, the Poinciana, is a good example of this model, as is the beech tree, common in temperate deciduous forests. In most temperate trees, such as oaks, the initial shoot with spirally arranged leaves becomes the vertical trunk, and secondary branches with spirally arranged leaves are produced at intervals, the model of Rauh (fig. 7.8). In more complicated architectural models, trees consist of two branch types. In the architectural model of Aubréville, vertical growth of the trunk is continuous from the initial apical meristem. At intervals, lateral branches are produced. These consist of relays of shoots that terminate in clusters of leaves, and subsequent growth is produced by two branches, one that is dominant and results in a zigzagging lateral branch with flat planes of foliage (fig. 7.9). These examples suggest the diversity of ways by which plant architecture unfolds. Such models are also seen in smaller plants, such as herbs. Many understory plants grow by underground stems, or rhizomes. These grow and branch in regular architectural patterns. The branches produce erect leaves, and the pattern of branching produces leaves that exploit the space available in the understory. Extension under the soil is promoted by sympodial growth, and exploitation of space is promoted by dichotomous branching (fig. 7.12). All of the above models are strategies for displaying leaves and establishing the crown of the tree, or smaller plant. Interestingly, some of the Hallé models have been observed in corals, where the branching strategies are seen as more efficient means for the zooxanthellae (p. 40) to capture light.

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Figure 7.12 The architecture of herbs with underground stems (rhizomes). Top left, the rhizome extension and lateral growth of the Indian cucumber plant. Top right, branching network of rhizomes of the shell ginger. Bottom left and center, Indian cucumber. Bottom right, shell ginger.

Henry Horn and Quantitative Models of Architecture In Malaysia in 1973, I read a recently published and revolutionary little book by Henry Horn, entitled The Adaptive Geometry of Trees. He also grew up in a family that supported his love for nature and an intellectual interest in natural history. Horn was a young faculty member at Princeton and a recent PhD graduate from the University of Washington, where he was mentored by the eminent ecologist Gordon Orians, who encouraged him to improve his mathematical and engineering skills by taking courses in other departments. He came into contact with the brilliant and influential ecologist Robert MacArthur, and MacArthur encouraged him to apply for an ecology position at Princeton, which he obtained. His mathematical approach to the study of tree architecture was strongly influenced by MacArthur, and this approach helped explain crown differences among some temperate trees. Horn analyzed the passage of light through the crown in relationship to the photosynthetic properties of leaves and derived some ingenious ex-

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Figure 7.13 Penumbra and branch layering. Left, diagram of light penetration into canopy, showing penumbra. Center, planes of lateral branches in an American beech tree, growing in the understory of the Harvard Forest, in Massachusetts. Right, lateral branches of a dogwood tree at Bowman’s Hill Wildflower Preserve in Pennsylvania, both trees studied by Henry Horn.

planations for the spacing of foliage within canopies. Leaves are extremely opaque to light; typically, only 5% of usable sunlight passes through a leaf. For a tree with many layers of leaves (see leaf area index, p. 67), light passing through two leaves would be only 0.25%, not enough for photosynthesis. However, Horn noted that light is not produced from a pinpoint, but from the disk of the sun, which has a diameter of a nickel held out at arm’s length (or, more technically, a diameter of 0.5°). The slightly diffuse source of sunlight means that a leaf is not a perfect absorber of that light, and that diffuse light will be detected at a level below the leaf, equivalent to about 70 diameters of the leaf. This diffuse light will support photosynthesis in the interior of the crown. Horn hypothesized that sun-adapted trees produce crowns with vertical branches that allow some penetration into the interior, and shade-adapted plants produce flat tiers of branches at distances above and below that allow for diffuse penumbral light to be used by the trees (fig. 7.13). Horn then examined typical trees in the eastern woodlands and noted that shade-tolerant species, such as the red-osier dogwood and the American beech, produced flat tiers of branches, with leaves spread out flat. In contrast, more shade-intolerant species, such as red oak and red maple, produce a dense outer crown from vertical branches with most leaves near the tips. Although his analyses generated some disagreement about specific predictions, the approach generated much excitement. Horn’s little book inspired a succession of more sophisticated attempts of using mathematics to generate realistic architectural models of trees. He also wrote a short

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Figure 7.14 Examples of quantitative tree models, generated by computer algorithms. Left, Scots pine generated with stochastic model by Feng Wang and colleagues. Center, tree silhouette generated using L-systems by Masaki Aono and Tosiyasu Kunii. Right, model of Aubréville produced with L-systems and petri nets, by Przemysław Prusinkiewicz and Neil Pomphrey.

passage in the beginning of his book that captured his enthusiasm for trees in general and has been quoted by many authors of books on trees. “Indeed, thinking of trees as crafty green strategists has given me many new insights, and simplified assumptions have allowed me to test these insights.” These mathematical approaches spanned the levels of organization and function of plants, and generally came from two directions, “top down” (a general mathematical explanation) and “bottom up” (empirical observations of trees), or a compromise between them. Trees are not just particular to plants, but are also abstract constructions of interest to mathematicians and computer scientists; the latter use trees for the storage and accessing of data. Thus, some architectural models of trees, with varying degrees of realism, have been constructed mathematically, or from radar or photographic imagery (fig. 7.14). Some of these models followed Horn’s lead and used a physiological understanding of plant function to generate predictive models. A good example of a bottom-up model is the Indian almond or pagoda tree, a ubiquitous tropical tree. It is a member of the genus Terminalia, and its flat planes of branches (the model of Aubréville, fig. 7.9) are characteristic of the tropical trees in this genus. In this model the main trunk grows monopodially and at intervals produces flat branches that extend sympodially (fig. 7.15). A closer look at branch extension reveals that once the shoot stops extending (but continues to generate leaves and flowers at the tip), two new shoots are produced just behind the tip. Jack Fisher, a structural botanist specializing in tropical plants, measured the lengths and angles of the two branches extending outward, as well as the angles of the main

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Figure 7.15 Examples of terminalia branching. Top left, detail of lateral branch extension in the pagoda tree; top right, diagram of branching, with unequal angles; bottom left, Hisao Honda’s computer-generated model of the pagoda tree; and bottom right, simulation of optimal leaf overlap in the branching of an actual tree.

branches extending out from the young trunk. His measurements allowed his colleague Hisao Honda to construct a model of the tree (fig. 7.15). Later Honda again collaborated with botanists to produce a quantitative model of a dogwood, similar to Henry Horn’s tree of interest.

Environmental Effects on Plant Architecture When scientists became aware of the diversity of architectural models in trees, particularly in the tropics, naive optimism developed that we could find the adaptive significances of these models. A plant’s architecture displays the leaves that often optimize their function (and sometimes not). A model has a certain cost to the plant; the strength of the materials determines the kinds and extent of branching. Thus, the degree to which a model promotes efficient energy capture by leaves is akin to the efficiency in leaf economics (chapter 5). The unique evolutionary history of the plant

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may developmentally limit the branching patterns and architecture. Finally, energy and materials put into branching compromises allocation to roots, leaves, and flowers; allocation constraints may affect the architecture. On the benefit side, the architecture should optimize light capture and, thus, energy gain by the plant, which should promote reproduction (the longterm fitness of the plant), reduce the risk of physical damage, and promote longevity. Most research has focused on the light capture by different architectural models. Flat tiers of branches seem adaptive in shady environments, and the pagoda crown shape of the Indian almond should allow for light penetration into the interior in the high light conditions of ocean shorelines, where the tree thrives. The actual crown of a tree is affected by many environmental factors. Disease may destroy buds that cannot develop to produce the model. Shade, drought, and wind may affect the dimensions of the model. Even in such a distinct model as that of Aubréville, other trees produce crowns that are not pagoda-like at all, such as the Central American chicle tree, a traditional source of latex for producing chewing gum. Although many trees that grow by the model of Troll tend to grow low and wide (fig. 7.11), some members may become quite lofty. Another variation that can dramatically affect the function of the crown is the angle at which leaves are attached to the branch. If leaves are more vertical (sticking up or drooping down), more light will penetrate into the crown. As trees age, they are more likely to be damaged by their environments. In many trees the initial model of the tree may be repeated to fill in the site of damage, a process discovered by Roelof Oldeman, which he termed reiteration (fig. 7.16). As trees grow taller, the high branches grow smaller, the leaves smaller, and the units of reiteration smaller as well (p. 210). Even under ideal conditions, as in a tropical rainforest, trees grow toward a maximum height. When that height is reached, signs of aging creep in, and the tree eventually dies of old age. That age may vary from a century to a millennium. Light seems to be the most important of factors that could affect architecture, and most functional tree models examine the efficiency of light capture by the plant. Modeling each pagoda tree leaf rosette as a disk, Fisher and Honda examined the effects of major branch number, extension branch lengths, and the angle of those two branches from the line of the previous branch. The first branch was thicker and longer than the second one, and its angle from the branch line was smaller. By varying the model inputs, they were able to show the optimal branch lengths and angles for the best cap-

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Figure 7.16 Diagram showing how reiteration can help fill in the damaged part of a crown produced by the original model.

ture of light energy, and their values were very close to those that Fisher had measured in the actual trees (fig. 7.15). In the underground rhizome growth of the plants studied by Adrian Bell, the branching angles of some gingers were the 120° that would produce a perfect hexagon. In Indian cucumber, a slightly different angle allowed for the shoots to be distributed with less overlap, more efficiently for the capture of light (fig. 7.12).

From Leaf to Crown to Canopy The growth of a large forest tree begins as a seedling, eventually attaining the canopy. There it joins its own kind, especially in temperate forests of low tree diversity, or joins a great diversity of species in tropical forests, with neighbors that are other species. Crowns may compete, and we are beginning to understand plant traits that correlate with crown success. As crowns rub against one another, shoot tips may be damaged or inhibited. This results in a space between branches and crowns, something we call “shyness” (fig. 7.17). This space allows more light to penetrate into the forest canopy, and degrees of shyness may relate to the competitive abilities of different trees in the canopy. Shyness is also seen among reiterations within a crown. In tropical forests, the individual tree crowns are packed, much as florets in a head of cauliflower (fig. 7.17). Trees die, producing gaps in

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Figure 7.17 Forest canopies. Left, example of crown shyness in the European pine, in southern France. Right, canopy of tropical forest in Queensland, Australia (courtesy of Francis Hallé), showing the close packing of individual crowns.

the canopy, and these are filled in by the expansion of adjacent crowns, or by the vertical growth of trees underneath. Crowns persist against smaller competitors, aided by strong trunks and roots against windfall. Crown packing and forest productivity may improve with species diversity. Forests are very dynamic in their canopy structures, and there is much to learn.

Engineering and Plant Architecture As the techniques of design improved in buildings and civil structures, such as bridges, a technology developed to determine the properties of the construction materials. How strong are they? How do they resist compression (as in a high wall), tension (as in the cables of a bridge or members of a truss), and bending (as with a roof or second-story floor). The early designers used intuition and constructed buildings of stone or timber, but Newton’s mechanics stimulated the analysis of the strength of materials in the eighteenth century, which led to the civil and military engineering of the nineteenth century. Thus, structures could be designed with the strength of materials in mind, to provide economies of construction, and prevent the structural failures that occasionally doomed earlier projects. These advancements eventually led to the development of biomechanics and the mechanical analysis of plant architecture. In history, plants have informed architecture, and, later, architecture (or engineering) has informed our understanding of plant construction.

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Two mechanical structures that help describe plant function are columns (the trunk or vertical axis) and cantilevers (branches and leaves, both the petioles and blades). How strong are they, especially in response to environmental stresses from winds? How “safe” are they in construction, insuring against mechanical failure? The mass and bending of columns may lead to buckling, and the mass and bending of branches and leaves produce strains (compression below and tension above) causing failure, or breaking. Finally, how do plants provide sufficient strength with the most efficient deployment of materials? Karl Niklas, a professor at Cornell University, has led in the quest to build a quantitative understanding of plant form, including biomechanics. He grew up in New York City, and his fascination for nature was stimulated by childhood visits to his grandmother’s farm in rural New Jersey. His research has touched on the subjects of at least half of the chapters in this book. It is easy to see the biomechanical strategies of plants from their appearances in different light environments, and I have been particularly interested in the strategies on display in forest understories. If there were no competition among plants, the most efficient strategy would be to lie flat on the forest floor, with no need for support, like the rosettes of Arabidopsis (p. 118). Competition among plants selects for taller individuals, more able to capture light. However, greater height entails greater costs, eventually canceling the advantage in light capture. Among understory plants, a variety of architectural strategies have evolved. One such strategy is employed by two very different plants, the May apple of eastern North American forests and the Amorphophallus of tropical Asian forests. The May apple produces a single hollow stem that splits to form two umbrella-like leaves with the petiole inserted so the leaf blade’s mass is balanced around it. The Amorphophallus, famous for the stinky inflorescence that pushes out of the ground at certain times of the year, produces a single massive leaf, with a lobed blade perched on a very thick petiole. The May apple shoot and Amorphophallus petiole both have mechanically strong tissues just beneath the surface of the cylinder where stresses and strains are greatest. Leaf blades are mostly displayed parallel to the ground in these understory plants, effective in capturing light. The leaf mass has a tendency to bend the blades downward, and leaf structures help keep the blade erect. The veins of strong leaves span most of the thickness of the leaf, but additional tissues consisting mainly of fibers are produced above and below. Such features look very much like an “I” beam, as used in the construction

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Figure 7.18 Bridge-leaf constructions analogies. Left, 836 interchange, Miami, showing both I-beams and box beams as structural elements. Center, major vein and blade of thatch palm. Right, blade of an argun palm (palm images courtesy of Jack Fisher).

Figure 7.19 Cell pressure provides structural rigidity. Left, Tokyo Dome, Japan, with inflated roof. Center, Costus scaber, Costa Rica. Right, leaf section, with inflated subepidermal cells.

of a skyscraper (fig. 7.18). Reinforcing materials are energetically expensive, and often leaves of the most shade-tolerant plants have no fibers associated with veins and produce stiffness through the pressure of water in cell layers, very much like an air mattress or the roof of some stadiums. Plants with leaves relying mostly on water pressure (or turgor) are most prominent in protected environments (fig. 7.19). Most leaves, even in exposed environments, wilt to some extent in response to drought— due to losing water in leaf tissues. For a leaf held out laterally from an erect stem, the greatest stresses

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Figure 7.20 Contrasting architectures in herbs. Left, the panicled aster (flowers and drawing); right, the Canada goldenrod (drawing and flowers).

occur near the base of the petiole, because of the leverage of the entire leaf bearing on this position. Many leaves, the most spectacular examples of which are seen in palms, produce bases of petioles that are distinctly U shaped in section, like the steel-reinforced concrete box girders of a highway overpass bridge (fig. 7.18). For palms, such girders not only provide the vertical strength of resistance to both compression below and tension above, but they also resist torsions particularly important to palm fronds twisting in the breeze. Similar reinforcement is seen in petiole of a large rhubarb leaf (fig. 1.10). Many herbs have very simple architecture, with a single vertical shoot displaying leaves. Others produce lateral branches. The implications for branches are that they produce more shoot apical meristems, and such plants have much greater capacities to produce leaves. Two common North American herbs, the branchless Canada goldenrod and the branched panicled aster, have different strategies for capturing light (fig. 7.20). The goldenrod produces larger and longer leaves at a steady rate during its annual growth. The aster exponentially increases its leaves during the year, with a much greater loss of leaves, as well. The aster plants take up more area and have longer underground rhizomes. The aster plants invest their photosynthetic production in more leaves, and the goldenrod plants invest more of that production in producing taller shoots. The architectures of many economically important crop plants, particularly trees, are well studied. Architectures can optimally display leaves and

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Figure 7.21 The architecture of fruit crops. Left, traditional orchard trees at Smith Brothers Orchard, in rural West Virginia. Right, apples trees in training for espalier, Columbia Basin Project, Washington.

thereby improve the capacity for a plant to grow. The growing of apples comes to mind. Traditionally, apples were grown as individual trees in orchards, the heights of trees limited to promote ease in the harvesting in fruits, as in traditional fruit-growing areas in the United States (fig. 7.21). However, in Europe techniques of training trees into continuous low rows were developed over the centuries, now known by the French word espalier. This arrangement exposes individual trees to more light, increases yields, and reduces harvesting costs.

From Plant Architecture Back to Art Plants’ structure and architecture influence each other. Experts in biomechanics continue to look for equivalents to architectural design in plants, and architects continue to be inspired by plants and other natural forms. Leonardo da Vinci observed in the branching of trees that the diameters of the new branches of a tree equaled the diameters of the branches from which they developed. The pipe model, which views the vascular tissue of trees as collections of pipes moving from roots to the trunk, and on to the tips of branches, depends upon a ring of such tissue around the trunk and branches, and should not scale with diameter. Nor should the deflection of branches be proportional to length. Christophe Eloy recently came up with

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an explanation for the simple rule formulated by Leonardo da Vinci. He postulated that the branching rule is explained by analyzing them as beams affected by winds, and he has calculated that branch thicknesses should vary in relation to the loads imposed by winds. His research is probably not the last word, because he has assumed that wind speeds are uniform and that trees uniformly grow in response to the pressures of wind. And the dialogue between art and science continues.

Chapter Eight Shapes and Edges Look up at the tree-tops and see how finely Nature finishes off her work there. See how the pines spire without end higher and higher, and make a graceful fringe to the earth. And who shall count the finer cobwebs that soar and float away from their utmost post, and the myriad insects that dodge between them? Leaves are of more various forms than the alphabets of all languages put together; of the oaks alone there are hardly two alike, and each expresses its own character. henry david thoreau, “A Week on the Concord and

Merrimack Rivers” Thomasina: Do we believe nature is written in numbers? Septimus: We do. Thomasina: Then why do your equations only describe the shapes of manufacture? Septimus: He has mastery of equations which lead into infinities where we cannot follow. Thomasina: What a faint heart. We must work outward from the middle of the maze. We will start with something simple (she picks up an apple leaf ). I will plot this leaf and deduce its equation. tom stoppard, Arcadia

V

olkmar Vareschi was the father of plant ecology in Venezuela. Inspired as a child by the travels of Humboldt, he was determined to follow in his footsteps and studied and received a PhD in plant ecology in Austria. Following World War II, Vareschi visited Vene· 158 ·

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Figure 8.1 Left, tropical rainforest profile diagram, Rancho Grande, Venezuela. right, sample of leaf outlines from the same tropical rainforest, one of three published by Volkmar Vareschi.

zuela in 1950. He stayed and became a professor at the Universidad Central in Caracas. In his adopted country, Vareschi studied its tropical vegetation and wrote many books about plants and ecology, both scientific and popular. Here we see the profile diagram of the forest canopy and an accompanying figure of leaf outlines at Rancho Grande, a tropical rainforest research station to the west of Caracas (fig. 8.1). Humboldt’s first visit to a tropical rainforest was east of this site, in the same mountain range. The diagram gives us an impression of the diversity of leaf form in the forest, and yet a predominance of species with a narrow range of form: oval and of moderate size, smooth edged and with a distinct point at the tip. In this chapter I’ll discuss the function of shape and the edges of leaves, as traits that vary greatly in different environments. In subsequent chapters, I’ll discuss other leaf traits: surfaces, veins, and color. Humboldt put the study of all of these traits in motion, and it is useful to trace the path of discovery that he inspired. If we look at Humboldt and Bonpland’s Physical Table of the Andes and Neighboring Regions (p. 69), note that he wrote down the names of plants at different elevations, all the way to the tropical alpine. He observed the reductions in leaf size at the higher elevations, but did not comment on changes in leaf shape. Vareschi was surely inspired by this table.

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Much earlier, Theophrastus wrote detailed descriptions of the leaf shapes and edges from the trees of his native Greece and knew the distributions of the different trees, but he did not write about the functions of leaf traits, nor did other authors until the late nineteenth century. A confluence of factors led to the formation of a research movement, or “school,” of physiological plant anatomy, largely based in Germany but international in its experience. First was the influence of the theory of natural selection, proposed by Darwin and Wallace, and written about in detail by Darwin in his On the Origin of Species (1859). Many German biologists became enthusiastic supporters of this theory, and they began to see plant traits as adaptations to natural selection. Second, research disciplines and advanced degrees in academic specialties emerged in Germany and became the model for Europe and, later, North America. A surplus of trained scientists was available for work abroad. Third, European countries with colonial aspirations established botanical gardens in their tropical possessions (see p. 69), with research laboratories that attracted visits by these young scientists. Most notable were the gardens of the British and Dutch colonial enterprises, and the most famous among them was the Foreigner’s Laboratory established by the Dutch biologist Melchior Treub in the colonial gardens at Buitenzorg (now Bogor, Indonesia) with its high-altitude extension on the slopes of the Mount Gede volcano. Young scientists from Europe and the United States were welcome to work at Buitenzorg. I visited the gardens as a young lecturer at the University of Malaya in the 1970s and dined with scientists from throughout the world, still using the gardens for research. Research at Buitenzorg on the functions of plant and leaf traits was summarized by Gottlieb Haberlandt in his Physiological Plant Anatomy, which went through several editions, from 1884 until 1924. Particularly influential was the work by Schimper (pp. 50 and 69) and his Plant-Geography upon a Physiological Basis. Many novel explanations about leaf function were proposed and occasionally experimentally tested. We have learned much about leaf shape and function in the last half-century, adding much to this tradition, partly because of the development of portable instruments for measuring physiological processes.

Variations in Leaf Edges and Shapes Outside in your garden or in a park or public garden, you could collect a similar diversity of shapes and could trace a similar diagram as Vareschi (fig. 8.1). These leaf traits are illustrated in Appendix A. Leaves can vary

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Figure 8.2 Diagram of leaf development showing roles of genes and auxin.

quite dramatically in shape within plant genera, suggesting that their evolution can be relatively rapid. Even within species, leaf shape can be affected by growth conditions, such as shading within a crown. Differences in leaf shapes and edges are established well after the production of the leaf primordium (p. 114), with its position and lengthwise orientation. The distal portion becomes the leaf blade, my main concern here. The young leaf blade is a meristematic structure, with cell divisions throughout, particularly at the margins. When the dorsal-ventral orientation is established, the edges of the blade can grow out, and cells divide in the interior to produce the photosynthetic tissues and veins (p. 115). The palisade cells divide at a similar rate to the surface (epidermal) cells, but they elongate in a dorsal-ventral direction. The spongy mesophyll cells divide less rapidly and are pulled apart as the blade expands (p. 35). The dramatic variations in leaf shape are produced rather simply by the control of cell division along the edges (fig. 8.2). Cell division is promoted by the flow of auxin in cells by the gene PIN1, and auxin production inhibits the expression of the gene CUC2, which is produced in locations on the blade edge. A broad area of synthesis results in a depression in the adult leaf, producing lobes. Alternating narrow areas without CUC2 promote the development of teeth along the blade edge. The most dramatic differences among leaves are between simple and compound leaves. In the latter, the leaf is divided into leaflets that may be arranged like fingers on a hand or as segments along a strong extension of the petiole (Appendix A). The mechanism of producing such a leaf is similar to producing lobes or teeth on a simple leaf: extended ac-

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tivity of auxin to promote further cell division and differentiation. However, additional genes are active, such as KNOX and LFY/UNI, and the different mechanisms reflect the production of compound leaves from ancestral simple leaves in different groups throughout the evolution of plants. However, the leaf itself was derived from a branching system early in plant evolution (p. 33). My description of the genetic control of leaf development is certainly an oversimplification, but it does show that the changes producing a toothed or lobed leaf from smooth- edged leaf are relatively simple, and there are lots of examples demonstrating this variation. In addition, vein formation in leaves (chapter 10) influences lobing and tooth formation. Major lobes in leaves are always associated with major veins.

Plasticity and Variation Checking out the foliage of a tree in your neighborhood will reveal the variation within the crown, particularly between the sun-exposed outer leaves and the shade-tolerating interior ones. Shade leaves are typically thinner and larger than sun leaves. If the tree has lobed or toothed leaves, the grooves (or sinuses) between the lobes will be shallower. A good example is the red oak, common in eastern forests of the United States. Maciej Zwieniecki and colleagues followed development in leaves at the Harvard Forest in Massachusetts. Leaves at the tops of the crowns were smaller and more lobed than those at the bottom. In the papaya plant, the large handsome leaves are deeply lobed, with lobes on the lobes. However, the leaves in shade conditions are much less deeply lobed and are thinner (fig. 8.3). Shade has two components, less light for photosynthesis and an altered quality from light passing through or reflected from foliage that reduces the ratio of red to far-red wavelengths (fig. 4.5). The latter affects a sensory pigment that controls leaf development. Daniel Buisson, a graduate student working with me, showed that the lobing under shade was suppressed by both components of the shade light. Leaf shapes also vary during the life of plants, especially in aquatic plants and vines. Dramatic variation in leaf shape is the most common manifestation of heteroblasty (p. 122), when it occurs in a developmental sequence. In some root-climbing vines, the initial leaves are pressed to the surface of the tree on which the vine grows. Then, much higher and more exposed to sunlight, larger and thicker leaves are produced away from the trunk (fig. 6.13, p. 120). Other plants produce different leaves on the same

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Figure 8.3 Leaf shapes vary in response to exposure. Leaf outlines of papaya grown in sun (left) and deep filtered shade (right).

shoot or in response to environmental conditions. Some aquatic plants produce normal leaves when growing above the water surface, but highly divided leaves that develop submerged (fig. 8.4). Some shade plants with flat planes of leaves on their branches produce two types of leaves, larger ones that spread out laterally and smaller ones that cover the branch, as in Selaginella (fig. 8.4). In sassafras, a common tree of temperate forests in the northeastern United States, three types of leaves are produced: a normal oval leaf, an otherwise oval leaf with a single lobe, and a three-lobed leaf. Karl Niklas (p. 153) has shown that the different leaves are produced from different positions on the stem. Most leaves are quite symmetrical, although mechanisms by which asymmetry can be produced will be discussed later in this chapter. Even leaves that appear symmetrical may not be exactly so, just as a human face appears symmetrical but differs slightly from left to right. When plants are under stress, from lack of moisture, too much sunlight, or excessive temperature, their normal development is distorted as the leaf primordia expand into mature leaves. Detecting such fluctuating asymmetry is a means of assessing the kinds of stresses that can distort normal development, but these differences are relatively small compared to differences between shade and sun leaves, or in heteroblastic leaves. The best documentation of the variability of leaf shape in plants is demonstrated in the study of genera of plants, some with commonly per-

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Figure 8.4 Two or more leaf shapes at the same time. Left, three leaf types on the same stem in sassafras; bottom right, spike moss; and top right, an aquatic buttercup.

ceived and even iconic shapes— like oaks, maples, violets (including pansies), and even geraniums— and examining the variation among different species. Some leaves have changed little over evolutionary history. Ginkgo, the “living fossil” gymnosperm tree native to China, has very distinctive leaves that decorate many an urban street (fig. 8.5). These leaves are similar to fossils that have been found in various parts of the world in sedimentary rocks some 170 million years old. In northeast Washington State, the Stonerose fossil site preserves leaves and flowers of a diverse warm-temperate forest that flourished about 55 million years ago, also seen in deposits in southern British Columbia, both part of the Okanogan Highland. Several hundred different species have been identified from Stonerose, including leaves easily identified as maple, beech, sassafras, plane tree, and black gum— trees common in temperate broadleaf forests in North America today (fig. 8.6). Ginkgo was found there and conifers too. In slightly younger deposits to the west, the fronds of sabal palms, identical to those of palms presently native to Florida, grew in forests (fig. 8.6). When hiking on the high exposed ridges of mountains in Malaysia, I often came across a distinctive fern, Matonia. Its

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Figure 8.5 Fossil leaves and living fossils. Ginkgo leaves: Top left, Ginkgo huttonii, ~170 mya, England; top center, modern G. biloba; right, 600-year-old G. biloba tree from Taihua Temple, near Kunming, China. Matonia fern: bottom left, leaves of related Laccopteris elegans, Germany, ~160 mya; bottom center, living Matonia pectinata, Gunung Ulu Kali, Malaysia.

frond is almost identical to fossil leaf impressions found in Greenland and northern Europe, going back to the same age as the fossil Ginkgo (fig. 8.5). However, many familiar plants and leaves— like oaks, maples, geraniums, and violets— have evolved a great variety of different leaf types in more recent times. In addition to the variety of lobed and toothed oak leaves that have appeared, some of the southern oaks produce leaves without any lobes or teeth, such as the live oaks in the southeast (fig. 8.7). Yet the earliest oak leaves seen in the fossil record, 50 million years ago, look much like the characteristic lobed leaves today, such as the English oak leaves decorating the heads of the green men of medieval Europe (p. 2). Maples are similar in this respect; their earliest leaves about the age of the fossil oak leaves are easily identified as maples, with their characteristics lobes. Maples have also evolved to produce a variety of leaf shapes, from the ones like sugar maples, to compound leaves, to smooth and oval leaves on tropical mountains in Southeast Asia (fig. 8.8).

Figure 8.6 Stonerose fossil site, Republic, WA. Top left, maple, top center, ginkgo; top right, beech. Middle left, sassafras; middle right, fir. Bottom left, living sabal palm, Miami; bottom right, fossil sabal from near Bellingham, WA, ~35 mya.

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Figure 8.7 A range of oak leaf shapes. Top left, oriental white oak; top right, white oak; bottom left, red oak; bottom right, shingle oak.

Both geraniums and violets have similar evolutionary stories. Violets originated in the Andes of South America about 20 million years ago. They then spread to North America, Europe, and Asia, with about 400 species today. There are many violets in the United States, and they vary from those with the familiar heart-shaped leaves, to narrow lance-shaped leaves, and even to highly divided leaves (fig. 8.9). The geraniums of the genus Pelargonium total about 280 species in the world: about half of these grow in the Cape Floristic Region of South Africa, and half of those are unique to this special ecosystem. Again, in addition to the oval-round leaves we think of when we envision a geranium, other species have lance-shaped or highly lobed and divided leaves (fig. 8.10). Thus, leaves have evolved as quite

Figure 8.8 A range of maple leaf shapes. Left, sugar maple; center, box elder; and right, laurel maple (from Southeast Asia).

Figure 8.9 A range of violet leaves. Left, common blue violet; center, sagebrush violet; and right, tree violet.

Figure 8.10 A range of South African Pelargonium (geranium) species with remarkably different leaves. Left, P. fulgidum; center, P. laxum; right, P. peltatum hybrid.

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different shapes from a single ancestor. Why did such a variety of shapes evolve? What might be the various functions of these different shapes?

The Functions of Leaf Edges and Shapes In 1915 and 1916, two Harvard botanists made a discovery about leaves that suggested that shapes and edges might have different functions, and that their frequency could be a potent tool in predicting climates, both present and past. Irving Bailey and Edmund Sinnott reported that the frequency of leaves with toothed and lobed edges was correlated with colder climates. The frequency of such leaves plotted nicely with the mean annual temperatures of the locations from where they were collected. They also reported that fossil floras had different frequencies of leaves with lobed and toothed edges. Bailey and Sinnott speculated that this frequency could be used to estimate the climates where these fossil plants once grew. More recently, this technique has been revisited and refined, and is now an important means of estimating the climates where those fossil plants grew. Based on leaf edge analysis, the mean annual temperature of the Stonerose forest was about 14°C, equivalent to present forests at low elevation in the Southeast of the United States. Where fine impressions were made or cuticles were preserved, it has also been possible to compare the density of stomata on leaf undersurfaces, to estimate what the carbon dioxide concentrations were (see p. 87). Again, these strong associations with climate suggest that shapes and edges have important physiological functions. We’ve begun to understand these functions in the past fifty years through the application of our understanding of fluid dynamics. This subject was developed over a century ago by physicists, to design faster ships and more efficient pipes. Water is obviously a fluid that resists ship movement and pipe flow. Air is less obviously a fluid (but think of the resistance air gives to your arm waved outside the window of a moving car), and an understanding of how to reduce such resistance helps us to continually improve the design and efficiency of aircraft. Plants that grow in moving water develop streamlined leaves that reduce the drag from currents, such as seagrasses and plants specialized for the habitats of rivers and even waterfalls (fig. 8.11). Fluids have an additional, and subtler, effect on organisms, particularly on leaves. A thin layer of non- moving fluid sticks to the surface, the boundary layer. The thickness of the boundary layer is affected by several factors, including the viscosity of the fluid, its velocity across the surface,

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Figure 8.11 Plants growing in moving water. Left, neptune grass, from the Mediterranean. Right, members of the family Podostemaceae grow on rocks in streams throughout the tropics, as this species from Venezuela.

and the distance across the surface. The boundary layer thickness increases with that distance. For still air, the thickness of the boundary layer of a leaf 5 centimeters across is about 14 millimeters, and increases to 43 millimeters for a leaf ten times that length. The thickness of those layers is sharply reduced when wind moves across the surface. The boundary layer is extremely important in the function of leaves (fig. 8.12). Leaves exchange gases and heat with the atmosphere, mainly via the stomates; water vapor out, carbon dioxide in, and oxygen out and also via the leaf surface. Heat moves in or out of the leaf, depending upon the difference in temperature between the leaf and the atmosphere. The rates are determined by the size of gradients of each. The gradient of water from inside to outside of the leaf is often large, and the flows are rapid. The opposite is true for carbon dioxide (p. 60). Resistance to these flows are found within the leaf, from cell to cell, cell to atmosphere, and then through the stomates. The boundary layer forms another resistance. Flows there are produced by diffusion and convection, where circular flows of air move molecules and heat around. A thicker boundary layer resists more, slowing rates of gas movement and preserving differences in temperature between the leaf and atmosphere. Consider the energy flows of a leaf on a warm and sunny day. Sunlight hitting the leaf is about half of the energy throughout its spectrum (fig. 3.12). About 85% of that energy is absorbed by the leaf (p. 61); however, only a small portion is used in photosynthesis. A larger portion evaporates water inside of the leaf, which is transpired with some resistance to flow by the boundary layer. If the temperature rises too high,

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Figure 8.12 The leaf boundary layer. Left, a diagram showing its function. Right, the trembling aspen reduces the effects of this layer by promoting leaf movement through its flat petiole and wide leaf shape.

gas flows cease, and the leaf may be damaged by the heat. Heat escapes the leaf by the emission of infrared wavelengths through the atmosphere and by diffusion and convection— the latter impeded by the boundary layer. This imposes limits on the size of a leaf. A round leaf has a single dimension producing a uniform boundary layer. An oval leaf with a length of 10 centimeters and width of 5 centimeters has an effective boundary thickness determined by the smallest dimension. With a lobed leaf, the smallest lengths across lobes determine the thickness, and not the overall leaf size. The actual effective leaf size, which determines boundary layer thickness, is important for leaf function. On a whole plant scale, where the total leaf area fixes sugars and makes growth possible, the way area is split into more small leaves versus fewer large leaves is important. Another way to reduce effective leaf size is by dividing a leaf into individual segments, as in compound leaves (Appendix A). Our current understanding of leaf form and function is very much the result of early efforts by Tom Givnish, of the University of Wisconsin. Growing up in the Philadelphia area and exposed to nature and gardens through his family, he decided to combine his ability with mathematics and his love for plants in his college studies. Givnish entered Princeton University, majoring in mathematics as an undergraduate and then pursu-

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ing a PhD in biology in 1977. There he was exposed to the work of Robert MacArthur and Henry Horn (p. 146). He combined sophisticated thinking about how plants function in their natural environments with mathematical modeling to formulate testable hypotheses about leaf form and function. This led him to observe plants in natural environments and inspired him to study leaf size and shape at Rancho Grande, the same forest documented by Vareschi (fig. 8.1). Recently he has directed his attention more to the phylogeny of plants and, thus, to the evolution of plant traits, including leaves. Why do some leaves have ragged edges (teeth and/or lobes) and others have smooth edges? I’ll start with lobes. Lobes reduce the effective leaf size and boundary layer thickness, and they occur more commonly in larger leaves. Most of the “charismatic” leaves described by Humboldt (p. 15) are highly divided, such as palms and the adult leaves of aroid vines. The leaves of bananas and their relatives the heliconias and prayer plants are easily torn because of an absence of veins that parallel the leaf margin. Those tears reduce the effective leaf size and promote greater transpiration in wet and sunny tropical rainforest environments. They may also move in winds, and the flapping of leaves may reduce the boundary layer thickness. Some leaves have evolved structures that help them move in even slight breezes, such as the trembling aspen, promoting heat and gas exchange (fig. 8.12). The largest leaves, those of palms, are generally highly divided with relatively small effective leaf dimensions. Good physiological evidence associating leaf lobing with function comes from comparative studies of the South African geraniums (fig. 8.10). Here closely related species with quite different leaves and growing in different environments have different physiological properties. Species with the highly dissected leaves have higher rates of photosynthesis and growth and greater transpiration than round leaves. Thus, the species with the dissected leaves have evolved a strategy to grow rapidly during short periods of water availability. Furthermore, leaf dissection may protect against higher leaf temperatures when stomata close during times of drought. More limited evidence supports a similar advantage in narrow violet leaves, growing in open meadows, compared to the more round and heart-shaped ones, growing in the shade of woods. Leaves with teeth on the margins are most common on trees in temperate forests. They are rare in tropical rainforests (fig. 8.1), but more frequent in the understory plants of these forests. The strong negative correlation of ragged-edged leaves with mean annual temperature suggests some func-

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Figure 8.13 Left, giant rhubarb leaf, from South America. Right, guttation from a strawberry leaf.

tion, but the explanation has been long in coming. Teeth are associated with the tips of veins, so their function may be associated with the supply of water and nutrients. Teeth are also often associated with hydathodes, structures that secrete water from the interior of the leaf (fig. 8.13). So after a century of speculation, we now have some solid ideas actually backed by experimental evidence. The edges of leaves, particularly the teeth, have a very thin boundary layer and potentially greater loss of heat and gas exchange capacity. These teeth enhance rates of photosynthesis early in the growing season in temperate forests, compared with smooth-edged leaves of other species. This may provide these species a growth advantage in colder climates. Toothed leaves may also provide a means of releasing water from the interior to prevent flooding of the spaces between cells, promoting gas exchange. In cooler forests with high moisture during the springtime, guttation (and teeth) may promote photosynthesis and growth. Viburnum is a genus of shrubs (and a few small trees) with a broad distribution in the tropics and temperate areas, and it is popular in temperate gardens. These plants are similar in their flowers and fruits, but vary dramatically in shape and edges of leaves (fig. 8.14). Erika Edwards from Brown University and collaborators have been analyzing leaf shape, comparing their physiology in species placed in an evolutionary tree. They have observed that changes in the internal anatomy of leaves has enabled greater photosynthetic capacity in certain species, and tropical viburnums that have evolved from temperate ancestors have lost lobes or teeth, and temperate species from tropical ancestors have gained those characters. The “pioneer” trees of tropical rainforests, those that grow quickly

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Figure 8.14 Dramatically different leaves in viburnum, understory shrubs in northeastern United States. Left, maple-leaved viburnum; center, hobblebush; and right, wild raisin.

in gaps where trees fall, generally produce large-lobed leaves on thick branches. In Vareschi’s leaf outlines (fig. 8.1), the large examples are from such pioneers. These pioneers are exposed to high light but have access to plentiful moisture, and they are light in construction and have short lives. Also, many of the oval leaves in this diagram have long narrow tips. These have been called “drip tips,” and they are interpreted to quickly remove water from the leaf surface. Some simple but clever experiments have shown that drip tips actually function in water removal, and that may help prevent fungal infections. The most remarkable contrasts in leaf form are between typical “simple” leaves in comparison to “compound” ones (Appendix A). Leaves are defined as organs in the way they develop, their short life spans compared to the plant as a whole, and their positions on stems with buds at their base. Compound leaves look superficially like a branch with lots of small leaves attached, but they fit that definition. Their leaflets are typically small with thin boundary layers. Compound leaves produce lots of effective surface for capturing sunlight rapidly, compared to a branch producing simple leaves. They seem like such a good “idea” (p. 103) that it is surprising that they are generally uncommon in a forest, either temperate or tropical. Givnish argued that such leaves are seen mainly in tropical dry forests, where they can be produced quickly to take advantage of the rains, and they drop quickly to reduce water loss when the rains cease. Perhaps the most characteristic trees of the dry monsoon forests and savannas of the tropics are the acacias, such as those browsed by giraffes in East Africa. However, compound-leaved trees are also seen in 10–15% of moist temperate forests and are present in tropical rainforests, primarily in the immature

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forests recovering from clearing or disturbance. I know of no experimental research revealing differences in function of compound versus simple leaves, and their advantages in certain environments are still controversial. Most of the discussion about the functions of leaf shape is still speculative, and certain plants defy any explanation. On high mountains in South and Central America, the huge leaves of Gunnera plants (sometimes misnamed as giant rhubarb) are seen (fig. 8.13). This is an odd plant by any accounting; its leaves, for instance, have sites for nitrogen-fixing bacteria, and all of the surrounding plants have small leaves. These explanations have relied on our understanding of physiology and physics. Since leaves are eaten by animals (chapter 12), leaf shapes and edges may be signals or defenses to prevent their being recognized by animals. In the case of teeth, they may be a physical barrier to insects that chew on leaves from the edge in. The availability of nutrients in the soil may also be a constraint on the evolution of certain types of leaves. Low nutrient levels are found in certain tropical areas and on high mountains. If soils accumulate organic material (as under low temperatures), they become more acidic and provide less nitrogen to the plants. Leaves of plants in these conditions are typically thicker, tougher, and much smaller than plants under normal conditions. Finally, a factor in the production of leaf shape is the evolutionary history of the species. Its ancestors may have evolved vein patterns that limit the shape changes in the descendants.

Geometry Many refer to the shapes of leaves and their edges, along with veins and other characters, under the umbrella of architecture, suggesting their classification and production are amenable to strict mathematical rules. We have been interested in the geometry of leaf shape for a long time, as shown by the seventeenth-century diagram of Nehemiah Grew (fig. 6.6). A bridge between early and modern appreciations of the geometry of leaf shape was built by D’Arcy Wentworth Thompson, a Scottish biologist with mathematical background and a deep appreciation for classical literature. He described the outlines of leaves occupying a surface of Cartesian coordinates and suggested simple equations that would describe some leaf shapes. He used this surface to project angles coming from a point (fig. 8.15) to describe leaf geometry. Some of the specialists who have worked on tree architecture have also proposed mathematical explanations for leaf shapes (fig. 8.15). For instance, L-systems, or Lindenmayer systems, were used to

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Figure 8.15 Mathematical descriptions of leaf shape. Top left, generation of a horse chestnut leaf by D’Arcy Wentworth Thompson; top center, fractally generated Barnsley fern frond; top right, rose leaf programmed by an L-system; wavy margins can be explained by fractal algorithms. Bottom left, lettuce; bottom right, kale.

describe the branching and architecture of plants, but also are applicable to the descriptions of leaves. Aristid Lindenmayer, who primarily studied fungi, described a sort of grammar of symbols that produce strings according to simple rules; these were used first to describe the growth of his favorite organisms. Later they were used to produce trees and quite complex leaves. Since most biologists who study form actually study animals, including humans, it should not be surprising that a field of study, morphometrics, is the umbrella for that research. One type of analysis, of the elliptic Fourier series, has been particularly employed for leaves of varying degrees of complexity. Since the mathematical operations are complex, most experts use computer programs for the analyses, and outputs are used to describe difference in shapes within, and between, species (fig. 8.15). A type of analysis that has become particularly popular for the beauty of its graphic products is that of fractals, popularized by Benoit Mandelbrot. A fractal

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is “a mathematical set that has a fractal dimension that usually exceeds its surface dimension.” The fractal dimension is a ratio describing how a pattern changes with the scale at which it is measured. Fractal objects are thus those that are similar in pattern at different scales. The classical example is the island of Britain. If the scale of measurement is decreased (a smaller section of the coast is analyzed), the estimate of the length of the entire coastline is increased, and this distance approaches infinity. Leaves are not very self-similar, although a compound leaf might seem so. Nonetheless, botanists will apply fractal software to compare leaves, with varying degrees of success. One aspect of leaf form that does seem fractal is the rippling of the leaf edge above and below the surface, as in a head of lettuce (fig. 8.15). Impressive as such analyses may seem, especially to me with my limited mathematical sophistication, they may have little to do with our understanding of the function, development, and evolution of leaves. More collaboration between biologists and mathematicians (or computer scientists) might help. An imperfect example is an article about leaf shape co-written in the Journal of Morphology by the cosmologist Sir Fred Hoyle. He proposed some mathematical descriptions for such shapes, suggesting an explanation for their evolution. Unfortunately, the simple fact that in the production of leaves, cells divide and expand makes his proposals completely untenable, as pointed out by Karl Niklas (p. 153). Many leaves are quite asymmetrical in shape. Often leaves that form on flat branches in the forest understory are lopsided in shape. This makes the packing of such structures, to absorb the limited light, more efficient (fig. 8.16). A group of mostly shade-loving plants, the begonias, are good

Figure 8.16 Asymmetrical leaves. Left, diagram of such a leaf by D’Arcy Wentworth Thompson; center, asymmetrical leaf display in population of parataniwha, in New Zealand; right, asymmetric leaves in the peacock begonia, Malaysia.

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examples. Thompson suggested that such asymmetry could be explained by the different rates of blade expansion in the different vector angles of a begonia leaf (fig. 8.16). Others have analyzed begonia leaves and, using his approach as a starting point, have expanded our understanding of the complexity of the production of lopsided leaves. Finally, all of this analysis of leaf shape, even if poorly grounded in biological understanding, may have an important application in the identification of plants. Mathematical methods including fractal analysis, Fourier analysis, neural network analysis (from biology to computer science and back to biology!) have been applied to describe leaves for identification purposes. The most widespread and accepted tool is the Leafsnap software developed by scientists at the Smithsonian Institution, Columbia University, and the University of Maryland. There, computer scientists adapted software used in facial recognition to identify leaf shapes. Implicit in such software is the ability to “learn” as images are added to the database. The program can be accessed from a cellular phone by sending a photograph of a leaf taken by the same device. The user can then learn the name of the plant. It is a brave new world, but at least the technology that poses dangers of social control inherent in the ability to recognize faces in a crowd is put to a more innocent purpose in learning to identify a plant through its leaf shape.

Chapter Nine Surfaces All you really need is skin. Skins the thing that if you got it outside, It helpst keep your insides in. alan sherman

Like dew drops on a lotus leaf I vanish. shinsui

G

eorge de Mestral returned with his dog from a hunting trip in 1941. They had been in the forests of the Alps outside of the city of Lausanne, where he worked as an engineer. Mestral combined a lifelong love for nature and an interest in technology and invention. At the end of that hunting trip, he focused his attention on the burrs, particularly cockleburs, attached to his socks and to the coat of his dog (fig. 9.1). He examined the burr under his microscope and observed the hooks that attached them to his socks . . . and aha! He thus conceived of a means of fastening clothing, eventually making the fasteners. He submitted the patents and established the fastener and company we know today as Velcro. Few inventions have had such a large and universal effect on us, fastening clothes, shoes (changing the lives of little children and senior citizens), astronaut suits, and on. The global company con· 179 ·

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Figure 9.1 Left, burrs (seeds) of the wild licorice, forming hooks that fasten to the loops of thread on these socks; right, a genuine Velcro fastener close-up.

tinues today, long after the expiration of the original patent in 1978 and after De Mestral’s death in 1990. Velcro is the condensation of the two French words: velour (velvet) and crochet (hook), et voilà, Velcro! Velcro is an excellent example of using phenomena and structures in nature to create novel inventions and technologies, which today we refer to as biomimicry and bioinspiration. Although the scope of technologies is very broad, from artificial muscles to aerodynamic ships, particular attention has focused on the surfaces of organisms. Their interaction with the fluids in which they live, whether liquid or gaseous, has led to the evolution of a variety of features that are attracting the interest of people like George de Mestral: physical scientists and engineers with an interest in nature. Leaf surfaces have been the interest of many such people, some coming more from the physical science side, yet others (even myself, in a small way) from the biological side. This has led to some interesting scientific discoveries, and some have attracted public interest through efforts of the discoverers to gain publicity (and start-up capital!). Here, I’ll focus on the surfaces of leaves (their “skins”) to help explain their properties and the attempts to create inventions from them. That also simplifies discussing the functions of different surface features. Given the simple anatomy of the leaf discussed earlier (p. 34), I’ll limit my descriptions to the outer cell layer, the epidermis, and will particularly focus on the outside (or surface) cell wall and its covering, the cuticle.

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Epidermis and Cell Walls An outer layer of cells, covering the leaf (and all plant organs), is established very early in leaf development, from a single layer of cells in the apical meristem (fig. 6.7). It is distinct from other layers in the leaf; its cells generally produce no plastids. Most of the cells have a fairly flat surface, but the side walls may be quite convoluted, which may provide mechanical strength to the leaf blade. Several cell types are produced from the epidermis, through cell division. Two guard cells form to establish the stomates, scattered across the surface— but mainly on the lower leaf surface. Hairs, scales, and glands— mostly multicellular structures above the surface— are produced from the epidermis. In cell division, the plate that establishes the new cell wall is produced by primary thickening. Further cell wall thickening is due to the addition of cellulose. Cell walls thicken with the influence of cellulose microtubules from special structures in the cell membrane (fig. 9.2). Cellulose is a linear polymer, consisting of individual molecules of the sugar glucose (fig. 3.9). Cellulose differs from starch in that the linkages between glucose molecules are inverted, making it difficult to break down. The enzyme that performs this task, cellulase, is not produced by us or any vertebrate animal. A few invertebrates (such as termites and their detested cousins, cockroaches), along with fungi and bacteria, can produce the enzyme and break down the fibers. Cellulose is made at the cell membrane from six protein complexes that form a ring (fig. 9.2). Each complex produces three separate polymer chains, for a total of eighteen, forming a quasi- crystalline strand with greater tensile strength than steel wire the same thickness (a few bil-

Figure 9.2 Primary cell wall growth. Left, diagram of cell surface showing sites of microfibril production; right, orientation of microfibrils determines pattern of cell expansion.

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Figure 9.3 Epidermal cell expansion and surface shape determine surface appearance. Left, flat cells and thick cuticle produce the mirror-like surface of Indian rubber tree. Center, rounded cell surfaces help produce a glossy appearance in the peacock fern. Right, conical cells in Hoffmania produce a velvety surface.

lionths of a meter thick). The microfibrils are loosely connected to each other by hemicelluloses and other sugar polymers. Cells expand from the pressure of water (turgor) entering via osmosis. The direction of expansion is important for cell function and the appearance of the leaf surface, and it is dependent upon the resistance of walls to the expansion pressure. The directions that the microfibrils are extruded onto the thickening wall determine the directions in which the cell expands (fig. 9.2). The wall will not expand in the direction the microfibrils are produced, but will expand at right angles to it. The direction the microfibril extends parallels the direction of individual microtubules, components of the cytoskeleton near the cell membrane. That orientation is under the control of the cell, partly through the production of small growth-regulating molecules. This is quite an elegant mechanism for controlling the final shape of the cell, also constrained by the simultaneous expansion of its neighbors. Subsequent layers of microfibrils can be produced at a constantly varying angle for each layer that creates a helicoidal appearance of the cell wall (fig. 9.17) and produces an arrangement, like plywood, that has equal tensile strength in all directions. Cell expansion is also promoted by some cell wall loosening, partly by the special expansin proteins that break crosslinkages between cellulose and other polymers, as hemicellulose. Epidermal cells may have outer surfaces that are flat, rounded, or even lens-shaped or conical in appearance (fig. 9.3), related to their expansion

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during development. Lens-shaped and conical cells are often seen on leaves of plants adapted to deep shade. Although we don’t know the exact mechanisms, presumably these shape differences are due to the density and directions of microfibrils in the wall. The production of conical cells has been best studied in petals (again, we owe much to those snapdragons, p. 128). Mutants of the MIXTA gene produce flat cells, which optically produce a duller color and weaker attachment for pollinating insects. Such plants have less fitness— that is, don’t produce as many seeds. Perhaps these genes control cell shape in leaves, but we don’t have such elegant studies to suggest the mechanisms of control as for petals, let alone how such changes would affect the function of the plants. Although cell walls are effective in maintaining cell shapes in tissues where cells do not move around (in dramatic contrast to human cells), they do not keep things outside or inside the leaf. Cellulose absorbs water, which can quickly move through the wall— certainly not acceptable in the normal functioning of the leaf.

Cuticle In plant evolution, some of the critical innovations were chemical, such as the production of the lignins that made cell walls and tissues mechanically strong (p. 28). Equally important was the production of a waterproof coating that allowed plants to conserve water in the harsh terrestrial environment. That coating is the cuticle (fig. 9.4). The cuticle consists of

Figure 9.4 Cuticle details. Left, leaf epidermal cells of Gnetum gnemon, showing thickened surface wall and cuticle. Center, detail of leaf epidermal cell wall of a Brazilian Xyris cell wall, showing cuticle (c) and cell wall (cw). Right, epicuticular wax particles in a cabbage leaf.

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Figure 9.5 Molecules of the cuticle. Top, cutin polymer; bottom, wax.

polymers of quite a different sort than cellulose, long-chain (16 or 18 carbons in length) fatty acids, with alcohol (-OH) groups along that length (fig. 9.5). The acid group (-COOH) can react with the alcohol group to form a very stable bond, an ester. These fatty acids and alcohols are produced in the epidermal cells and moved across the membrane to the outer part of the cell wall. There they react with one another to form an elaborate cross- linked network of very stable water- repelling carbon chains. This covering dramatically slows the movement of water outside of the leaf. Leaves produce other chemicals that can move from the cytoplasm to the surface. These can repel attacks by insects and fungi (and can also signal their attraction to the leaf ). Leaves can also pick up nitrogen and other nutrients from rainfall; these can pass across the cuticle and can be leached from the leaf (p. 81). In particularly dry environments, the epidermal cells produce other long- chain hydrocarbons that form an even more water- repelling layer at the surface of the leaf: waxes. These are deposited at the surface, above the cuticle, often in crystalline patterns (fig. 9.4). A little wax goes a long way in waterproofing the leaf, and the additional layers may add to the strength of the cuticle; and the wax surface structures increase the reflection of light and reduce the heat load on the leaf. In some leaves the amount of surface wax produces a spectacularly thick cuticle, accounting for perhaps a quarter of the leaf mass. Some leaves produce economically important quantities of wax. Wax of the carnauba

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Figure 9.6 Carnauba wax palm. Left, young palm; right, detail of frond surface, with fold to reveal wax thickness.

palm, from South America, has been exported to, and consumed in, industrial countries for a century or more (fig. 9.6), used in automobile and floor waxes, and to coat pills and candies. The cuticle also produces a mechanically strong surface of the leaf, so much so, that the epidermal layer can determine the final size of the expanding leaf.

Surface Structures Epidermal cells may divide to produce quite elaborate structures. These structures are typically spaced from each other, although the lineages of cells may contribute to these patterns. Stomates (from the Greek, stoma = mouth) are truly the lips of the plant. They consist of two guard cells and sometimes subsidiary cells. Closed, the guard cells stop the transpiration of water vapor and the entry of carbon dioxide. Opened, they allow gas exchange (p. 62). The mechanism of the establishment of the guard cells is not completely understood. Precursor cells express a gene, SPCH, but what activates it? Later on many other genes are involved, and auxin (p. 119) is involved in the unequal division that produces the initial cells and subsequent equal divisions to produce the guard cells. Additional cell divisions ensure that stomates are spatially separated,

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Figure 9.7 Patterns of stomates on leaf undersurfaces. Top left, rows of stomates in purple heart; top right, stomate in the queen sago (courtesy of Barry Tomlinson). Bottom left, clusters of stomates in a begonia; bottom right, stomates in fossilized cycad cuticle, 30 mya. (Courtesy of Bogláka Erdei.)

which optimizes the efficiency of gas diffusion across the leaf. In many monocots, files of cells develop into stomates (fig. 9.7). Pressure in the guard cells determines whether the stomates are closed (deflated) or open (swollen). Stomates are sensitive to temperature, CO2 concentration, drought, and light (photosynthesis in guard cells promotes their swelling). Dry air quickly induces genes that promote the synthesis of abscisic acid (ABA) in the guard cells, and stressed roots may also send ABA to leaves, which triggers their deflation. Swelling and deflation of these cells is promoted by the active movement of ions across guard cell membranes. Species vary in the size of stomates, and individual leaves vary in their density, influenced by shade and water availability. Larger stomates are less efficient in transpiration than small ones, on an area basis, because

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of the longer path through the openings. Smaller stomates are able to respond to environmental changes more quickly than larger ones. Although the spacing of stomates is generally fairly regular, more may be produced in different parts of the leaf blade and even may be produced in clusters (fig. 9.7). Stomates are absolutely essential for leaf function and plant survival. Their history, and probably the mechanisms regulating their opening and closing, goes back to the beginning of the land plants (p. 31). The reason we know of this long history, and our use of their size and density to estimate past atmospheric concentrations of carbon dioxide, is that their patterns are preserved by the cuticles laid down above the cell walls of the epidermis of fossil plants (fig. 9.7). Students of these fossil plants have developed a complicated system of naming stomatal shapes and patterns, enabling them to identify fossil plants and, in some cases, to relate them to plants surviving today.

Figure 9.8 Leaf trichomes. Top left, scales on leaf undersurface in the looking-glass mangrove; top right, scales in the resurrection fern. Lower left, star-shaped hairs in leaves of the Broome bloodwood (courtesy of Brian Gunning); lower right, normal and glandular hairs in a sage leaf.

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Individual epidermal cells may also develop into other surface structures, collectively called trichomes. An individual cell may develop a projection that becomes a single hair. More typically, it divides to produce a single emerging cell. That cell may continually divide to produce a long hair or an elaborately branched one (fig. 9.8). Finally, rather than producing branches, the files of outwardly produced cells may fuse together, forming an umbrella-shaped structure, or scale. Some hairs may produce a single large cell at the tip, or a cluster of smaller cells, filled with chemical compounds. Or the single cell may enlarge to store such compounds near the leaf surface. These structures can be detected indirectly by rubbing the leaf surface to release a strong aromatic smell, such as with a citrus or sage leaf (fig. 9.8). These structures may provide various advantages to plants. They may reflect excess sunlight to keep the leaves cool. They may provide an insulating layer that prevents leaves from cooling off too much at night. They also may protect the leaf interior from being consumed by chewing insects, and previous damage by insects may induce the production of more hairs or scales. In the air plants (of the bromeliad family) native to the New World tropics and north into Florida, the scales also help the leaves to absorb water, through protected cells at the base of the scales. It is often difficult to determine the exact functions of hairs and scales, because they may benefit leaves in more than one way, or harm one insect and benefit another. Or

Figure 9.9 Stinging nettle. Left, flower detail; right, hypodermal hairs on leaf vein.

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Figure 9.10 Mullein and edelweiss. Left, mullein plant; center, detail of mullein leaf with stellate hairs. Top right, leaves and flowers of the edelweiss; bottom right, SEM of hairs of leaf, with striations.

there may be novel and overlooked functions, as the directions of hairs promoting directions of movement of animals on the surface. One such leaf hair with obvious defensive capability is the hypodermal trichome of the stinging nettle (fig. 9.9), also seen in a few other plants. The nettle grows in shady spots of moist woods in the temperate northern regions. Brushing against the plants produces an instantaneous stinging sensation, as the sharp trichomes penetrate the skin and inject histamine and other biologically active compounds. Humans have traditionally used nettles as food, fiber, and medicine, particularly in alleviating symptoms of arthritis. It seems like a particularly effective defense, but the larvae of several butterflies feed on the foliage Scales and hairs are particularly common on leaves in alpine tundra, as well as many desert plants, and sometimes spectacularly so. There is something about the wooliness of their leaves that is reminiscent of a small animal, making them more attractive to us, seeing the fusion of animal and vegetable qualities in a single organism. The old story of the vegetable sheep, reported by Alexander’s soldiers, is a good example (p. 12). Two such silvery-leaved plants have become iconic in European culture: mullein and edelweiss. Most common is mullein, as it has spread through-

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out all temperate regions from its original home in Europe and central Asia. It lives two years, the first with a low rosette of furry dull-green leaves and then a second year with a high spike of fragrant yellow flowers (fig. 9.10). When crushed, leaves produce a mild medicinal fragrance. Its herbal medicinal uses probably go back to the proto-Indo-European culture— and extend today to the medicinal shelves of Whole Foods supermarkets. Poet Molly McQuade wrote about mullein in a hypothetical letter to Emily Dickinson: “. . . prepare to regard a kind of outsize rabbit’s throne, like a spare cush for a pope with a pompom tail: a low thatch, sage-serene, robustly upholstered with a rococo hairy skin . . .” She listed the common names for this widespread weed that I also know as Verbascum thapsus (one of 250 species in that genus): velvet dock, our lady’s flannel, old man’s blanket, et cetera. She saw mullein as a metaphor for something mysterious and inexplicable. Mullein leaves make an excellent trailside substitute for toilet tissue. Edelweiss is less widespread but equally emblematic. An inhabitant of the high alpine of the European Alps, with its densely hairy leaves around the small composite flowers (fig.9.10), it first was symbolic of that inhospitable and unattainable world. Then, as more people visited the Alps in the nineteenth century, it became symbolic of the pure beauty of the alpine. It was embroidered on military uniforms, including the high ranks of the Swiss armed forces and the Nazi Alpine troops, and was the name of the renegade anti-Nazi youth: the Edelweiss Pirates. My mind occasionally plays the refrain “blossom of snow, may you bloom and grow” (from The Sound of Music). The hairs that make the edelweiss so white have some unusual optical properties (fig. 9.10), protecting against ultraviolet wavelengths.

Biomimicry Leaf surfaces— with their varying cell shapes, waxy cuticles, and projections— have quite an amazing array of physical properties, and it is not surprising that they are being examined by physical scientists and friendly biologists as inspirations for new inventions. Even in the case of that original invention, Velcro, recurved leaf hairs might be inspirations for more refined attachments. In bedstraw (Galium), a common temperate weed, the leaves produce two kinds of surface hooks, larger and stronger hooks pointing toward the leaf base on the underside, and smaller and weaker hooks on the upper side, pointing in the opposite direction. Those on the underside help the plant attach to others and climb higher. Those on

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Figure 9.11 Common bedstraw. Top right, appearance of whole plant; top left, transverse section of leaf showing different types and directions of hairs on upper and lower surfaces. Bractless blazing star. Bottom right, flowers and leaf; bottom center, leaf detail; bottom left, trichomes.

the upper side protect the leaves and allow them to slide over other plants (fig. 9.11). In stick leaf, trichomes produce whorls of tiny recurved hooks along their sides; they kill beetles that feed on aphids, so they are perhaps not so useful for the plants. Trichomes with hooks at their tips can immobilize insects on the leaf surface, including bedbugs (fig. 9.12). Bedbugs have dramatically expanded their distribution into hotel rooms and our private bedrooms in recent

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Figure 9.12 Bean leaves and bedbugs. Left, bedbug caught on bean leaf. Center, bean leaf surface, showing the hooked trichomes. Right; leg of a bedbug pierced by trichome hook, the apparent cause of bedbug mortality (courtesy of Catherine Loudon).

years, increasingly immune to pesticides previously used to kill them. Their presence has long been promoted by warmer bedrooms, lack of cleanliness, and increased travel. In southeastern Europe, peasants placed leaves of the common bean on the floor around beds, and bedbugs were stuck on the leaves the following morning; the leaves could then be swept up and the bugs destroyed. The mechanism for the attachment is hooks on trichomes, piercing bedbug legs. However, bio- inspired replicate surfaces of the leaves were much less effective than the natural cellulose polymers in the trichome walls. Leaves of a legume, the townsville stylo, produce hairs that trap and kill ticks, but this discovery has not yet produced any new tick control strategy. The ability of leaves to attract or repel water has captured the most attention, and primarily because of the research of Wilhelm Barthlott. For years, he had studied the surface properties of leaves, leading to his (and his colleagues’) discovery of the “lotus effect” (as it is widely called) in 1997. The sacred lotus that he studied is an iconic plant, revered among eastern religions. In lotus, water drops stand on the leaf surface and roll off the edge at the slightest tilt (fig. 9.13). Barthlott measured the angle of the edge of the water droplet as it stands on the leaf. He observed that a few plants, including the lotus, were super- repelling (super-hydrophobic). Then he noticed that such leaves, with water rolling off the surface, were extremely clean. The water droplets picked up dust and spores, and removed them from the leaves. Thus, a by-product of water repellency was a self-cleaning mechanism. The lotus leaf has two surface characters that contribute to these properties, convexly curved cells with deposits of tubular crystals of

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Figure 9.13 The sacred lotus. Top left, the plant; top center, leaf with a bead of water; upper right, detail of raised epidermal cells, by SEM; middle right, detail of tubular wax crystals on cell surface. Salvinia. Bottom left, floating plants with hairs visible from surface; bottom right, detail of hairs by SEM.

wax (fig. 9.13). Patent applications were submitted and granted, licenses negotiated, and we now have a few products on the market using superhydrophobic surfaces in paint. So, the promise of biomimicry has definitely been realized in this case, although perhaps not so dramatically as Velcro. Later, Barthlott and colleagues extended the idea of super-hydrophobicity to Salvinia, an aquatic fern, whose specialized trichomes capture an air layer when submerged (fig. 9.13). Such layers aid in the function of submerged plants, particularly in gas exchange; such properties may inspire new commercial products, that is, the “Salvinia effect.” It used to be common knowledge among gardeners not to water plants

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on a sunny day, because the water droplets act as lenses to focus highintensity light onto leaves and damage plants. We now know, from empirical research, that this does not happen. Given the problems that machines with moving parts have with friction and wear, and the emergence of the discipline of “tribology” to study slipperiness, researchers have been looking for such surfaces among plants. They found them on the inner trap surfaces of carnivorous plants. In the New World pitcher plants, the slipperiness is caused by the dense layer of downward-pointing hairs (fig. 9.14), making it impossible for insects to climb out of the trap. That wasn’t cause for much inspiration, but the mechanism in the Old World pitcher plants was far more interesting.

Figure 9.14 Top, slippery surfaces in the traps of pitcher plants, Nepenthes bicalcarata. Top left, the leaf trap; top center, ridges under lip that are slippery to insects; top right, structures within ridges that hold water to create a slippery surface. Bottom, Sarracenia flava. Bottom left, detail of trap lip; bottom right, hairs pointing downward prevent insects from escaping.

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These plants grow primarily in the mountains of Southeast Asia, where the low- nutrient soils that develop in these cold climates promote the nitrogen-capturing strategies of these plants. Three mechanisms were discovered. First, most mountain species rely primarily on a sticky and slippery fluid that was most effective with flies. Second, most lowland species produce a higher concentration of waxes as flat erect plates, and these are most effective in trapping ants. However, trapping success was seen in some mountain pitcher plants with little wax and sticky fluid, suggesting another mechanism. In 2004 Holger Bohn and Walter Federle described a novel mechanism: a layer just beneath the lip of the trap, consisting of a waxy structure that attracted a stable fluid layer that produced the desired slipperiness (fig. 9.14). This discovery was used by Harvard and MIT researchers to develop the technology of slippery liquid-infused porous structures (SLIPS, a very catchy acronym), which they envisage as a biomimetic solution to the problems of friction. Think of the waste (about 15% of contents) of an “empty” ketchup bottle, avoidable with these new surfaces. At the other end of the water-repellency scale, some leaves have the capacity to absorb water, the air plants (Tillandsia) with their specialized scales being the best-known examples. Plants with leaf hairs may repel or attract water, depending upon the characteristics of the hairs. In deserts with virtually no rainfall but frequent night fogs, plants have evolved the capacity to remove fog from the atmosphere and absorb the small droplets of moisture. Two examples of such deserts are those of northern Chile and in Southwest Africa, both near the coast and influenced by the cold ocean currents. Both leaf shape and hairs promote the condensation of fog into water droplets that are absorbed by the plants. Particularly spectacular in this regard are the strange plants of Namaqualand, in South Africa (fig. 9.15). Various technologies have been devised to harvest water, particularly using wing covers of a desert beetle from Namibia, but I bet that much more can be learned from those water-absorbing plants, including the Namibian desert grass and the curly-whirlies of Namaqualand. Leaf hairs are efficient reflectors of sunlight, and more careful studies of such hairs may reveal new properties. Those of the edelweiss produce a white reflected color and also much more than that. The Belgian physicist Jean-Pol Vigneron turned his lab’s attention to the little alpine plant. They found that the hairs were particularly effective in reflecting ultraviolet light, more intense at high altitude. The hollow hair surfaces have projecting fibers, and their distribution forms a grating that is particularly effective in scattering the UV radiation most damaging to plants (fig. 9.10).

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Figure 9.15 Water-absorbing leaves of fog desert plants. Top, the curly-whirlies of Namaqualand, Africa; bottom, Tillandsia landbeckii from the Atacama Desert of Chile.

The cuticle and cell wall are, for the most part, transparent to visible light. If the cuticle is smooth, some radiation is reflected from the surface, like a mirror. Many leaf surfaces are not smooth because each epidermal cell is convexly curved, and the individual cells look like the lenses of an insect’s compound eye. The physiological anatomists (p. 69) speculated that such cells might function as lenses, focusing light onto specially oriented chloroplasts beneath. Indeed, more recent research (some that I’ve participated in) has shown more precisely how such lenses might function in the degree of concentration and the depth of focus. Such features are particularly common in plants of the shady rainforest understory. Such cells would not help much in collecting more diffuse radiation; however, epidermal cells with sharper cone shapes would not focus light effectively, but would be more efficient in absorbing more diffuse radiation (fig. 9.16). The surfaces of organisms, not just leaves, are now being scrutinized for such prop-

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Figure 9.16 The leaf cell surface of satin pothos as an optical device. Left, the growing plant; center left, leaf section, with lens-shaped epidermal cells; center right, a diagram suggesting how light can be focused by such cells; right, light spots focused by these cells.

erties for use in optical devices, like photovoltaic cells, where the reduction of light reflection is important to their efficiency. I’m also reminded of the value in bumpy surfaces in aerodynamics. Frank Fish, a biomimicist more from the biological side, has shown that raised scales in shark skin contribute to their efficiency of movement, an observation of interest to the designers of ships and swimsuits. The cell wall immediately beneath the cuticle may have special optical properties. In many, the microfibrils are laid down at a constant angle for succeeding layers, which produces a helicoidal, or chiral, organization. In not-quite transverse sections, the walls have a distinct periodically curved appearance (fig. 9.17). In a few tropical understory plants, the thickness of these layers interferes with light and produces a brilliant blue color, much like that of a peacock feather or the wing of a morpho butterfly. The mechanism of color production in some plants is due to the twisting of light as it passes through this layer, becoming circularly polarized. The mechanism of circular polarization is used in the RealD glasses used to view 3- D films. My early articles on this mechanism led to correspondence with Jean-François Revol, who was working with his supervisor Derek Gray on the production of iridescent color by the artificial layering of cellulose fibers to produce paper. They patented this invention, as such paper might be counterfeitproof (useful for currency). A scientist at the National Institutes of Technology working on paper technology wrote to me that “nature has beaten

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Figure 9.17 Helicoidal cell walls and structural color in Mapania, a Malaysian tropical rainforest understory plant. Left, the plant; left center, details of leaves; center, section of cell wall showing helicoidal structure and layers of silica nanoparticles; center right, diagram of helicoidal deposits of cellulose microfibrils; right, detail of intense iridescent color from leaf surface.

Figure 9.18 Begonia maculata. Left, appearance of plant and leaves; left center, close-up of silver spots; right center, section of silver spots showing spaces between epidermal and palisade layers; right, leaf surface showing transmission of light through cell side walls.

us to the punch.” Revol and Gray worked on the problem independent of me. I contacted Gray a couple of years ago. He informed me that no one ever paid for any license to use the patent, and other less expensive means were invented to produce counterfeit-proof paper. So that is the closest I ever got to biomimicry. More recently, I worked with colleagues on an understory sedge plant from Malaysia that produces a brilliant blue color by a helicoidal cell wall, along with layers of silica nanoparticles (fig. 9.17); the blue color is lost when the silica is removed. Here we have the use of a time-tested nanophotonic material, silica, used in all sorts of electronics and photonics applications, functioning optically in a plant. My final example of a possibly biomimetic optical property from the

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leaf surface is not exactly at the surface but at the junction between the epidermal cells and the palisade layer immediately beneath. If the layers are separated by a thin space of air, penetrating light is reflected back toward the surface before it encounters the chlorophyll pigments and produces a silver color. This is one mechanism of producing variegated color patterns in leaves, particularly common in begonias. In Begonia maculata (fig. 9.18), a strong silver color is produced, visible both to the naked eye and under the microscope. The reflection is enhanced because the angles of the bottom of the epidermal cells funnel scattered light into the side walls. These act like fiber-optic guides, efficiently emitting the light at the leaf surface. The leaf thus looks very much like the reflection disks on traffic signs. I can imagine a mechanism where the side walls are pigmented to produce a pixilated effect with the colored light of the side walls contrasted with the uncolored light from the interior of the cells. But you can see that I am overly optimistic, more of a marketer than a scientist; I’ve caught the bug of biomimicry and bioinspiration!

Chapter Ten Veins The same stream of life that runs through my veins night and day runs through the world and dances in rhythmic measures. It is the same life that shoots in joy through the dust of the earth in numberless blades of grass and breaks into tumultuous waves of leaves and flowers. rabindranath tagore, “Stream of Life”

This constant stream of qualia we feel in our stomachs. The big-leafed plant lifts its wings to greet the planet’s chemistry, the sun arrives on rooftops like a gentle stranger, rain rushes us love to love, stop to stop, these veins of leaf, hand, storm and stream, as if in pursuit of us and what we are becoming. w. s. di piero, “Only in Things”

T

he veins of leaves have long fascinated us. They seem a miniature of the branches of the trees that produce them. They remind us of our own veins, and the cycling of blood and all materials through life. We see their parallels in a river basin, the evidence for water erosion on the planet Mars, veins on Jupiter’s moon Europa, and even hints of veins in outer space, as the crab nebula. The strikingly beautiful patterns of veins, seen when leaves are closely examined, suggest to us the unifying patterns · 200 ·

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Figure 10.1 Leaf veins and natural land features. Top left and right, major veins of the Senegal River delta, Africa, and a Swiss chard leaf. Bottom left and right, the drainage patterns of Gabilan Mesa, CA, imaged by aerial photography, and incised veins and raised leaf surface of the red-flowered sea grape.

that operate at different scales throughout Earth, and even the universe (fig. 10.1). Beyond such unifying patterns, veins among leaves vary greatly. At their simplest, the leaf-like blades of liverworts and algae have no veins at all (p. 28). The small leaf of a ground pine (p. 31) has a single vein running down the middle of the small leaf, and the needles and scales of conifers (as pines and junipers) have a single leaf vein. As plants evolved, leaves and vein patterns changed along with them. The most plausible explanation for the evolution of the leaf of ferns and later plants was of the modification of a branch into a flat and webbed photosynthetic surface (p. 33). In them the secondary veins branched from the single principal midrib, often dichotomously (fig. 10.2). In other plants those single secondary veins produced tertiary veins, and then veins anastomosed, forming loops. The complexity of leaf veins culminated in the evolution of flowering plants, with five or more orders of veins and complex looping patterns of high density

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Figure 10.2 Different types of vein patterns. Left, dichotomous veins of a maidenhair fern; right, net vein pattern of scarlet passion flower leaf.

(fig. 10.2). In order to discuss the biological importance of vein patterns, an understanding of what individual veins are made up of, and how they function, is essential.

The Formation of Veins Veins appear during the development of the leaf blade. The primary vein, or midrib, appears very early in development and connects to conductive tissue in the stem. The secondary and higher orders of veins establish later as the leaf blade expands. The development of veins, as complex patterns, is a basic research problem that bears some similarity to the initial formation of leaf primordia on the shoot apical meristem (p. 119), the production of leaf shape (p. 161), and the distribution of stomata in the leaf epidermis (p. 185). In all of these processes, the growth regulator auxin and gene networks are involved. Also, the pattern of vein formation, particularly the midrib and secondary veins, is closely related to the shape of the leaf. All veins develop from specialized narrow cells that form strands, and these are the immediate products of cell division. A family of genes, PIN, is expressed in these cells, which have higher concentrations of auxin. Although it is clear that the spacing of veins is partly a result of the concentration of auxin in the developing veins, compared to intervening tissues, the mechanisms that produce the great variety in patterns of veins are not understood. As is usual, we best understand the production of veins in Arabidopsis.

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It is interesting that the genes that control all of these developmental processes in leaves are related to genes that control branch development in more early diverging plant lineages and their algal ancestors. Given the long parallel interest in leaf veins and circulatory systems, it is interesting to compare the developmental controls on their production. As some biologist friends tell me, “Hey, it’s all DNA”— emphasizing the core controls in biology, going back to bacteria and the origin of life. Early in my scientific career, I worked as a postdoctoral fellow at the Ohio State University, on the formation of plant embryos from clumps of wild carrot cells. After removing an auxin-like chemical in the growth medium, the clumps of cells produced veins of conductive tissues. One of my collaborators, William Sharp, became the CEO of the first plant biotechnology company, DNA Plant Technology. However, I didn’t like the windowless and laboratory-bound research, somewhat divorced from nature. I was inspired to live and work in Malaysia, where I studied leaves and plants in tropical rainforests. Although leaf veins look similar to the pattern of blood vessels in a chick or other embryos, those blood vessels develop quite differently. First, there are two different processes: angiogenesis, where vessels are produced from existing vessels or cells that produce vessels, and vasculogenesis, where the precursor cells are derived from stem cells. The major focus of NIHfunded research has been on the formation of blood vessels in tumors, as only with such a supply system can the tumors grow and then metastasize. The primary physical factor that sets both processes in motion is an oxygen deficit in the tissue, which promotes the activity of many genes, but particularly VEGF. This sounds suspiciously plant-like, but the acronym means “vascular endothelial growth factor,” for it is the endothelial cells that produce the vessels. So, leaf veins and blood vessels are only similar in the general appearances noted by Grew and Malpighi in the seventeenth century (p. 109), not in function or origin. And I see no NIH funding to study leaf vein patterns.

The Functions of Veins Although veins have been observed in leaves for millennia, we have only developed a good understanding of their function in the past century. The stimulus to study veins in leaves was William Harvey’s discovery of the circulation of blood in animals, first published in 1628. The early anatomists (p. 112) saw the similarities between blood vessels and leaf veins and spec-

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ulated about their functions. It was Malpighi who actually discovered capillaries, the connection between arteries and veins, making the anatomical description of circulation complete. Malpighi then began his study of plant anatomy. He conducted the first girdling experiments, showing that downward flows of sap fed the roots of plants; more sophisticated experiments later on showed the anatomical basis for girdling. In the eighteenth century, Stephen Hales (p. 45) studied the movement of sap in plants but made no anatomical studies of the tissues where sap was conducted, and he also worked on blood circulation. In the nineteenth century, mainly in Germany, the structure of leaf veins and their connections to tissues in stems and roots were completed— essentially the descriptions in the basic textbooks of biology today. Water and mineral nutrients flow from roots, through stems, and throughout the leaves via its veins, in a specialized tissue called xylem. The cells responsible for the flows are dead at maturity and have spectacularly thickened walls strengthened by lignin (fig. 10.3). In early diverging plant lineages (p. 28), individual and overlapping cells, tracheids, are the basis for water and mineral transport; but in flowering plants, vessel elements form longer tubes, or plumbing, that connect to each other to form the continuous conduits of water movement in the xylem tissue. Sugars, principally sucrose, and a few other molecules (including amino acids) flow from their places of production in leaves (p. 28) into veins, down the stems and main trunk, and to the highly active water- and

Figure 10.3 The structure of leaf veins, using the Indian almond leaf as an example (p. 149). Left, portion of old leaf, showing vein pattern. Center, transverse section of leaf, showing an individual minor vein, with sieve tube, vessel elements, and fibers identified. Right, section revealing a secondary vein lengthwise.

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mineral-absorbing portions of the root system. The tissue responsible for this movement (translocation) of the products of photosynthesis is the phloem. The active cells of the phloem are sieve cells in ferns and conifers, and sieve tube elements in flowering plants. Students of anatomy noticed that the sieve tube elements were without nuclei, but were adjacent to thin and densely stained cells with nuclei: companion cells. In the nineteenth century, scientists observed that such tissues exuded sugar-rich fluids when cut, while xylem tissues exuded water and minerals. All leaf veins are composed of xylem and phloem tissue (p. 35). Since the phloem tissue is normally produced toward the outside of the stem (why girdling experiments did not immediately cause wilting), in the connection between leaf and stem, the traces that connect to veins have phloem tissue on the underside and xylem tissue on the upper side. Associated with the upper and lower sides of veins, mechanically strong fibers may be produced, and these add much to the strength of veins in supporting the leaf blade (fig. 10.3 and p. 153). It wasn’t until the twentieth century that the accepted mechanisms for the pressures that cause translocation and transport were proposed, and these are still being debated and fine-tuned today. In 1930 Ernst Münch published the pressure gradient hypothesis. He postulated that translocation was an active metabolic process in which sucrose and other molecules were loaded into sieve elements near the sites of their production, and the concentration moved them toward the sites of consumption of sucrose, as in the roots or young developing fruits. This remains the most accepted explanation for translocation today— it is a mechanism that explains how sugars produced in the green photosynthetic tissue of the leaf blade can end up in the tip of the root of a tree, perhaps 100 meters below. Certain poisons, which inhibit the breakdown of ATP, halt translocation. On the other hand, the transport of water and dissolved minerals— great quantities of water moved up the trunk and through the leaves for 100 meters in the tallest trees— is a passive process despite the enormous amount of work performed in lifting that water. John Joly and Henry Horatio Dixon first proposed the transpiration- cohesion hypothesis in 1894. Water moves into the roots, to the xylem tissue, through osmosis. Plants actively take in metallic ions, nitrate, ammonium, and phosphate across cell membranes. This decreases the concentration of water in the cells, and water moves in passively via diffusion. This osmotic pressure can raise a column of water a few centimeters, but not enough to explain its rise to the treetop. Dixon and Joly proposed that a negative pressure lifting

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the water was created by its evaporation from cells within the middle of the leaf walls (think of their walls as absorbent paper tissue), and then its movement outside of the leaf via transpiration, through the stomates. This negative pressure has several consequences. First, the vessels transporting the water must resist collapse, hence the elaborate wall thickenings in the vessel elements. Second, a major threat to plants is the formation of air bubbles under negative pressures, cavitation, which can break the continually rising columns of water in individual vessels. These cavitation events can actually be detected from tiny “popping” noises detectable by ultrasensitive microphones, part of the strange arsenal of equipment used by the physiologists who study these processes. Third, the continual movement of water up the trunk is commonly envisaged as an electric circuit, with a series of resistances that slow the movement of water. The resistances are low in the roots and trunks and stems, rise a bit as water enters the leaf via the petiole and major veins, and are highest as water moves into the smallest veins. These small veins are the least efficient at moving water, partly because the water leaks out of the veins to supply the adjacent green tissues. Water is an essential ingredient of photosynthesis, and so are nitrogen (as in the proteins and chlorophyll pigment molecules), phosphate (for ATP production), magnesium (at the heart of every chlorophyll molecule), and other ions with essential functions (p. 236). Final resistances to the pathway of water movement are the stomata and the boundary layer adjacent to the leaf surface (p. 170). For optimal function, vein and stomatal densities should be in balance. Thus, the rates of photosynthesis and growth are determined by the rates of water and mineral transport to these active tissues. Theoretically, such a negative pressure can raise water through the xylem to a height of 130 meters, a bit higher than the tallest known trees, the coastal redwoods in Northern California. Veins have other functions in leaves. First, veins are mechanically strong, particularly if buttressed by fibers on the upper and lower sides. Thus, veins help strengthen the leaf blade, and that structure may be particularly robust in large leaves— as in palms (p. 154). Second, veins replace areas of photosynthetic tissue present in the leaf blade. Thus, greater supply of nutrients comes with a compromise in the amount of tissue for photosynthesis. Finally, veins isolate segments of the leaf blade, so that they may function relatively independently of each other in a leaf.

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Martin Zimmerman In the past century, no one has been more important in promoting our understanding of the functions of veins and these two processes, translocation and transport, than Martin Zimmerman, trained in a very interdisciplinary and quantitative way at the Federal Institute of Technology in his home country of Switzerland. He was a Harvard professor from 1960 on, and later director of the Harvard Forest, until his premature death from cancer in 1984. I remember arriving at the Harvard Forest in 1998 to work on autumn leaf color and encountering his photograph among the biological luminaries in the Biological Laboratories at the Cambridge campus (fig. 10.4). Among all of the stuffy and stiff portraits, Martin stood out as

Figure 10.4 Martin Zimmerman, when he was director of the Harvard Forest.

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he looked up from his microscope with glee. Not just a scientist, he was an accomplished artist and musician, constructing the harpsichords played in the weekly musical evenings at his home in Petersham, with delicious Old World pastries baked by his wife, Elvira. My FIU colleague, Jennifer Richards, remembers those evenings. As much as his own accomplishments, equally important was his influence on students and colleagues. Many of them went on to make new discoveries in the field of plant hydraulic architecture, as Martin named that field of research. Barry Tomlinson, whom I have mentioned for his contributions to tree architecture (p. 143), was an early collaborator with Martin in teasing out the water transport networks in palms. In the development of an academic discipline, participants often view each other as part of a genealogy of ideas. Zimmerman was central to the development of the science of transport and translocation. His students and collaborators— including Mel Tyree, Barry Tomlinson, Frank Ewers, John Sperry, and Noelle (“Missy”) Holbrook— taught other students in the network of researchers. Missy was first influenced by Martin as an undergraduate, and she influenced others whose work is mentioned in this book (and names listed on papers in the chapter notes), including Maciej Zwieniecki and many students, including Lauren Sack, Tim Brodribb, Taylor Feild, Kevin Boyce, and Jeanine Cavender- Bares. I believe, more than merely the communication of scientific ideas, it was Martin’s interdisciplinarity (lack of fear in stepping beyond research boundaries) and his open-hearted collaborative spirit that have influenced the ideas discussed later on in this chapter, as well as the more accurate estimates of transport and translocation in large trees.

From Veins to Trees Veins supply water and nutrients to, and remove sugars and amino acids from, the photosynthetic tissues of a leaf. They occur in a very high density, particularly in smaller leaves, to support those tissues. It is now fashionable to measure this density as their length per unit area of leaf. In a sugar maple leaf, this density is 9.7 mm/mm2 (fig. 10.5). In a large maple sugar tree of 40 centimeter trunk diameter and 20 meters height, the leaves (each with about 60 cm2 area) total an area of 194 square meters (or ~32,000 individual leaves in the crown). The entire length of veins in this crown is around 186 kilometers. The transport and transpiration of water of individual stomata from leaves totals around 70 liters (or 70 kilograms = 160 pounds) of water per day. A less familiar but more spectacular example

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Figure 10.5 Sugar maple tree during autumn. Left, tree in rural New Hampshire; right, individual leaf.

is the Australian mountain gum, the tallest flowering tree in the world. Several trees were measured for water use, including an example with a diameter of 41 centimeters and height of 56 meters, and a leaf area of 219 square meters, totaling some 121,000 leaves. Daily water use was 174 kilograms. Those values scale up to a forest, or biome, and to the huge amounts of water cycling (chapter 4). The rise of water up through the roots may make some water available for other smaller plants, a recently discovered phenomenon called hydraulic lift, but most of it moves out of the leaves via the finest veins and associated stomata. The pull of evaporating water molecules generates very large negative pressures. It is convenient for us to describe them in terms of the standard atmospheric pressure, at sea level, which is (depending upon humidity, temperature, and weather) 1 kilogram per square centimeter (or 14.7 pounds per square inch), the weight of all of the atmosphere above pressing down on us. At the flight altitude of a commercial aircraft (of ~10,000 meters), the weight would be reduced to ~0.24 of that pressure at sea level. On the other hand, descending into water will increase the pressure, by adding that of the water and the atmosphere, of 2 atmospheres at 10 meters and almost 11 atmospheres at 100 meters depth. The pressure differences that pull water up to the tip of a large tree, like the gum tree, are over 20 atmospheres. Such great pressure differences limit the capacity of really tall trees to lift water and nutrients to the very tips, because of the resistance to flow and the danger of cavitation. These may impose theoretical limits on tree height, and the availability of carbohydrates may also

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Figure 10.6 Coastal redwoods and comparison of foliage at the base and tip of a tree. Left, tall tree of 120 m height, on Redwood Creek. Top right, foliage at approximately 100 m, studied by George Koch. Bottom right, branch tips at different heights, in meters, sizes indicated by scale in centimeters.

be important. In the coastal redwoods, with heights of over 120 meters (like a 35-story building), the shoots and leaves at the tip are miniaturized, as if they were subjected to drought— close to the theoretical limits imposed by hydraulics, with negative pressures of up to 30 atmospheres at the tops (fig. 10.6).

Comparing Vein Patterns A bewildering variety of vein structures has evolved among leaves. You may have learned in a basic biology course or horticulture book that the two branches of flowering plants have two basic vein patterns. The monocots, like a grass, have parallel veins, and the dicots, like a maple tree, have

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Figure 10.7 Leaf venation in monocots. Cleared surface view through the pinna of an African oil palm, showing vascular traces connecting major and minor parallel veins.

net venation. We now divide up the flowering plants differently, with two major dicot groups and the monocots (p. 26). Furthermore, a closer look at the monocots reveals that there are many members with net venation. Although monocots that evolved in sunnier and more exposed environments consistently have parallel venation, many other groups, particularly the aroids, evolved in shady environments and produced wide leaves with net venation (fig. A.23). Among palms, clearing the leaves shows the parallel veins connected by much smaller cross veins (fig. 10.7). Among the flowering plants, a complex system of classification of vein structures has been devised, well beyond the scope of this discussion, and certain to squelch your slightest interest in veins. The reason is the value of vein patterns in identifying leaves. Students of fossil plants use the slight differences in veins of fossil leaf impressions to identify plants. For instance, vein patterns were useful in identifying the diverse tree flora in Re-

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public and the Okanogan Highland (see p. 166), as they are less subject to evolutionary change than leaf shape. Vein patterns result from veins joining together with other veins of different sizes. By convention, the midrib of a simple leaf is the primary vein, and large veins connecting to it are secondary, and so on (fig. 10.8). In a large leaf, there may by seven to eight orders of veins in this hierarchy. The higher-order veins join together in a variety of ways. In some plants, the smallest veins end by forming loops. In others, a single vein terminates in the sinus formed by loops from lower- order veins, and in still others the vein in the sinus may branch once or twice more (fig. 10.9). Veins in leaves are reminiscent of the patterns formed by water flowing over land: the weathering of the surface into mountains, ridges, and valleys, and the movement of water into trickles, rivulets, streams, to rivers and lakes, to oceans, and then returning through rain and snow. Leonardo da Vinci noted the similarity between streams and the branches of a plant (p. 134). In the 1940s Robert Horton and Arthur Strahler measured the branching of streams in a watershed, and the simple rules they derived are still an inspiration for mathematical studies of all networks, including leaves. The similarities between vein patterns and stream networks are more obvious in the higher orders of leaf veins; the primary and secondary veins are typically very regular and straight, as in a peepal leaf (fig. 10.9). In contrast, the courses of major rivers meander. The superficial similarities between the veins of some leaves, particularly those with raised blade tis-

Figure 10.8 Orders of veins in a typical flowering plant leaf, a red maple; closer views toward the right.

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Figure 10.9 Skeletonized peepal leaf. Left, whole leaf; right, detailed view of primary, secondary, and higher-order veins. Loops have multiple vein projections inside.

sues between veins, and then patterns of streams in a watershed were noted by botanists with a mathematical bent, as well as geologists, physicists, and mathematicians (fig. 10.1). Both leaf veins and streams are strongly fractal (p. 176), repeating their patterns at different scales. Thus, a mathematical expression can be easily devised that reproduces such patterns, looking very much like the fine vein structure of a leaf. However, in both watersheds and leaves, it is likely that a much higher- order vein may branch from a primary or secondary nerve, just as a small creek may enter a large river near its mouth, and mathematicians have altered the equations to account for such “behavior.” Streams and leaf veins are examples of networks found throughout nature and culture: blood circulation, root systems, neural networks, bronchial systems in lungs, and complex human-built systems as economies, the Internet, and computer architecture. It is certainly tempting to search for common rules of organization and the optimization of efficiency of flows among all of these networks. I recently read such a book, Design in Nature (2012) by Adrian Bejan and J. Peder Zane, that is a summary of such an intention. They postulated a constructal law that came to Bejan in a sort of epiphany: “For a finite- size flow system to persist in time (to live), its configuration must evolve in such a way that provides easier access to the currents that flow through it.” A flow system is one in which currents (which can be everything from energy to water, air, or even information) move, and the branches occur to maximize the efficiency of such flows.

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The authors then apply this universal rule to all sorts of phenomena from animal movement to the design of academia and, yes, trees and forests. On the book jacket are snippets of enthusiastic praise by various authorities, such as “an elegant exposition of a unifying principle so simple that it demystifies our comprehension of the flow of the universe.” Wow! Well, is the constructal law the best thing since sliced bread? I Googled the constructal law to learn more, and there were reviews both positive and very negative, but few thoughtful pieces by fellow scientists and engineers. I remain a little skeptical that such a rule explains everything. Thinking a bit more about leaf veins, there may be problems unique to them that make it difficult to apply such a law. The first is that veins actually facilitate two flows, that of water and minerals up through the trunk and into leaves, and that of sugars from leaves to distant parts of the plant. The rates of flow and the source of energy are dramatically different in these two different flows. Also, these veins also function in mechanical support. There is also the matter of networks that include loops. Loops make possible the reversal in direction of the flow, both for transport and translocation, and they also allow for a redundancy in flows, which may add a safety factor to veins under such negative pressures. Thus, safety is an additional factor built into the “design” of such networks, not just efficiency. Loops are not unique to veins, although they do not occur in streams. Loops may be found in all sorts of complex systems, and they may require some additional explanation, physically and mathematically. Also, veins in networks are, to some degree, a more complex system. Should we not find some emergent properties with this increase in complexity, properties not predictable from individual veins or flow efficiencies? Bejan and Zane’s theory must have the possibility of being false, which makes it more interesting scientifically. And maybe that is why few colleagues have taken up the idea. Such simple patterns, no better and beautifully exemplified by leaf veins, have engendered much serious thought and differences of opinion (fig. 10.10).

The Evolution of Veins Veins evolved in the earliest leaves, from their branch- like progenitors. These changes in vein structure and density over time have had profound implications for the evolution of life and climate. First, veins supply the photosynthetic tissues with some of the raw materials for growth and development, specifically water and minerals (the latter used in small amounts for making chlorophyll and other essential intermediates in the process).

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Figure 10.10 A mathematical model of leaf veins, using a fractal algorithm to produce a vein-like network.

Thus, the density of veins is strongly correlated with the highest rates of photosynthesis among plants. Ferns have very low vein densities and low rates of conductance, and also lower rates of photosynthesis. Conifers also have similar properties to ferns, and lower rates of photosynthesis. In the flowering plants, vein densities vary greatly, as do their conductance and photosynthesis. However, conductance and photosynthesis are strongly correlated with vein density, and typical flowering plants have much higher densities and productivity than ferns and conifers. This discovery led to flurry of research on venation in fossil and existing plants, and has dramatically increased our understanding of the evolution of flowering plants; most of this research was performed by plant biologists influenced by Missy Holbrook and, ultimately, by Martin Zim-

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merman. The next step was to increase the number of plants analyzed for vein density and physiological function, and to begin the analysis of vein density in fossil plants of all kinds. The flowering plants diversified in the Cretaceous period, from 145 to 60 million years ago. Leaves of the nonflowering plants all had low vein densities, less than 5 mm per mm2 of leaf area (remember that the sugar maple had densities of over 9, typical of most flowering plants). However, the vein densities of the early flowering plants increased, and increased dramatically about 65 mya. The densities of flowering plants have been high ever since, and those of non-flowering plants (as ferns) have remained low. These higher vein densities were associated with a modification of the xylem tissues of flowering plants from tracheids in the early diverging families to vessel elements— more efficient in conducting water (p. 28). The capability of leaves to produce higher vein densities was associated with a shift in the developmental patterns of leaves, in which cell division persisted far later into blade expansion and permitted the establishment of more minor veins. Under the low CO2 concentrations of the atmosphere 65 mya, the higher vein density permitted much higher rates of photosynthesis and growth, at the cost of transpiring dramatically more water vapor into the atmosphere. This changed the regional climates, particularly along the equator, promoting the establishment of tropical rainforests and the rapid increase in biological diversity after the extinction at the end of the Cretaceous period, when dinosaurs vanished. Higher vein density, along with increased “loopiness” of the vein networks, is associated with the rapid growing and short-lived end of the leaf economics spectrum (p. 99). Thus, leaf vein density has provided still another way of using leaf fossils to learn about the ecology of life in those early times, along with leaf margins and stomatal densities. Enjoy those patterns of veins of the leaves you encounter virtually every day; remember that the patterns may provide clues to understanding all networks, including the elaborate ones we have constructed for life in the twenty-first century.

Chapter Eleven Color This spring as it comes bursts up in bonfires green, Wild puffing of emerald trees, and flame-filled bushes, Thorn-blossom lifting in wreaths of smoke between Where the wood fumes up and the watery, flickering rushes. I am amazed at this spring, this conflagration Of green fires lit on the soil of the earth, this blaze Of growing, and sparks that puff in wild gyration d. h. lawrence, “The Enkindled Spring”

How innocent were these Trees, that in Mist-green May, blown by a prospering breeze, Stood garlanded and gay; Who now in sundown glow Of serious colour clad confront me with their show As though resigned and sad, Trees, who unwhispering stand umber, bronze, gold; Pavilioning the land for one grown tired and old; Elm, chestnut, aspen and pine, I am merged in you, Who tell once more in tones of time, Your foliaged farewell. siegfried sassoon, “October Trees”

A

lthough the color green (but how many hues?) is the rule for leaves, there are times when leaves change color, or when colorful leaves have been selected for horticultural beauty. I began writing this chapter while traveling through the northeastern United States, from the · 217 ·

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Delaware Valley to the Catskills Mountains, early in the month of May. Years ago I had studied the color changes during autumn, but more recently I have taken to observing the color changes in the spring, from bare brown branches, through breaking buds and expanding leaves of various colors, to the final mature green of foliage. I find the colors not quite as spectacular, but with a great diversity of vibrant pastel hues, with rapid changes from day to day (fig. 11.1). In the Catskill woods, the first to produce leaves is the juneberry, with warm chocolate colors followed by white flowers. The second tree to open its leaves is the red maple, whose vivid reds produce a light pink crown. This quickly turns to green, but the young red fruits add red color a bit later. The oaks generally produce very light young leaves, often even creamy in color, whose green chlorophyll is produced after the leaves begin expanding, and some with streaks of red in them. The same is true for the American plane tree. Amidst the tender green crowns are the delicate white and very upright forms of black cherry trees. Young shoots of sumac also produce pinkish crowns. The expanding leaves of the beech are a brilliant lime green color, much like D. H. Lawrence’s “bonfires green.” In contrast to the colors of autumn, very little has been written about these spring colors.

Figure 11.1 Spring foliage color. Left, farm and forest, Beaverkill, NY, in mid-April. Top right, juneberry foliage and flowers; middle right, red maple fruits; bottom right, beech buds opening.

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Figure 11.2 Variegated leaves. Left, caladium, with whole leaf as inset. Right, flame violet, with variegated detail as inset.

A close look at the canopy of these forests in summer reveals the slightly different hues of green, comparing oak to maple, or ash to beech. These colors are often modified by the leaf surfaces, with hairs, scale, or wax. A few plants in the understory produce variegated colors. A notable example in the spring is the trout lily, with brown mottling like its namesake. Another is the white-streaked clover (fig. 1.3). Other plants produce pinkish-red or silvery streaks or spots, such as those from tropical forests decorating our temperate interiorscapes (fig. 11.2). Our desire for color in our foliaged landscapes has been fulfilled by horticultural tinkering to produce variegated leaves in all sorts of plants. In addition, our gardens are full of trees with purple or red leaves, such as varieties of Japanese maple and European beech (fig. 11.3). During the autumn, as the leaves begin losing chlorophyll in preparation for senescence and fall (the season’s name describing the fate of leaves), a more brilliant and less subtle pageant of color unfolds (fig. 11.4). In these forests, most crowns turn red or bronze, or sometimes even purple, and many turn a brilliant yellow. Often individuals of the same species, such as sugar and red maple, turn very different colors, or even the different leaves and sections on the same tree. Oaks turn color also, some brilliantly red like the scarlet oak, or a duller red, such as white and red oak, peaking after the maples have lost many of their leaves. Then all of the crowns of deciduous trees are empty of leaves, except for the persistent yellow and then withered leaves of beech. During both spring and autumn, crowns of evergreen trees— such as pines, firs, spruce, and hemlock— maintain a dark green, in strong contrast to the broadleaf trees.

Figure 11.3 Purple and red leaves in mature leaves of trees. Left, European beech; right, Japanese maple.

Figure 11.4 Autumn foliage in the Appalachian Mountains. Left, forest canopy on the slopes of Waterrock Knob, along the Blue Ridge Parkway; top right, leaves of sourwood; bottom right, leaf of scarlet oak.

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Figure 11.5 Leaf color in tropical trees, both Asian and photographed in Miami. Left, young foliage of the iron wood (or nag champa) tree; right, flowers, mature and old foliage of the rudraksha tree.

The canopies of all broadleaf forests change colors during the year, including tropical deciduous forests and even tropical rainforests (fig. 11.5; p. 72). The observation of these changes is part of the study of phenology (p. 70). How are these colors produced, and what might the function be, if any, of such color? That is the principal subject of this chapter.

How Color Is Produced in Leaves In explaining color production, I’ll use the example of an artist, a watercolorist, painting on paper. The watercolor pigments are dissolved in water and applied to the paper by brush. The paper is thick and white. The white of the paper is due to the reflectance of all wavelengths of visible light (all colors) by the cellulose fibers that comprise the paper. In the same manner, a leaf devoid of any pigments, and therefore also consisting primarily of cellulose fibers in cell walls, is white (fig. 11.6). In watercolor, the pigments produce color by absorbing all of the wavelengths except those that are scattered by the paper fibers and are reflected back out of the surface. We call such color production subtractive, and it is the opposite of color produced by a television screen. As almost everyone knows, or will remember from using crayons or pastels in childhood, the primary colors are red, yellow, and blue. Combining yellow and blue produces green, red and yellow

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Figure 11.6 Color production in leaves. Left, almost unpigmented, or white, leaves of the snowbush, a tropical shrub; right, subtractive colors produced by primary colors, plus green: oil pastels on paper.

produces orange, and so on (fig. 11.6). In the variegated leaves of the croton, a shrub from the islands of eastern Indonesia, the ways that pigments can interact to produce greens, yellows, oranges, and reds can be observed with hand sections that show the presence of these different classes of pigments. Combining all of the primary colors (or red and green) makes a brown, or if enough pigment is applied, a black color (fig. 11.7). Plant pigments combine to produce the different colors and hues seen in the croton as well as spring and autumn canopies (fig. 11.8). Green is obviously produced by the two chlorophyll pigments, a and b. Each separately produces a slightly different hue, and varying proportions might also produce slight differences. In leaves, yellow and orange colors are produced by a class of pigments (or compounds produced by the same metabolic pathway), the carotenoids. These are water-repelling molecules and are produced in specialized plastids in cells. Some carotenoids, such as the lycopene present in tomatoes, produce reds— but these are not present in leaves. The pinks and reds of leaves are produced by a third class of molecules, the anthocyanins. The most common such pigment in leaves is the same as that producing the pinks and reds of roses and apples. Blues are rarely present in leaves, and in flowers and fruits these are made by specially altered anthocyanins. In a few leaves in the shade of tropical rainforests,

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Figure 11.7 Variegated leaves of the croton, a shrub native to the eastern islands of Indonesia. Transverse leaf sections show the color and pigment combinations producing the surface color.

blues can be produced without pigments, by structures that interfere with the absorption of certain wavelengths (p. 198). Some compounds related to anthocyanins can produce creamy and yellow hues in flowers, but not in leaves. That pretty much does it for leaf color, with one exception. In a group of families— including cacti, spinach, amaranths, and pokeberry— anthocyanins are not produced; quite different pigments, the betalains (containing nitrogen), produce yellows and reds in flowers, and reds in leaves. If both anthocyanins and chlorophylls are produced, the result should be brown, and such bronze or brownish leaves may be seen early and late, like the chocolate leaves of the juneberry or the occasionally bronze autumn leaves in the ash. At high concentrations of both chlorophyll and

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Figure 11.8 The subtractive colors of leaves produce the variety of colors seen during development, at maturity, and during senescence. Top left, chlorophylls; top right, carotenoids; bottom left, anthocyanins.

anthocyanin, leaves that are almost completely black have been bred by horticulturists (fig.11.9).

Why Green? The pigment active in photosynthesis, chlorophyll, makes leaves appear green. Sometimes the color is masked or altered by other pigments, but chlorophyll captures sunlight and uses it to convert CO2 and H2O into sugar molecules (chapter 3). Why should these leaf pigments always be green? Is it possible to envision other functional colors on our planet, or perhaps on habitable planets in other solar systems? Science fiction authors

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Figure 11.9 Black leaves. Left, surface view of this pseuderanthemum; right, transverse leaf section, showing layers with anthocyanins (red) and chlorophylls (green).

and astrobiologists (p. 41) have speculated about the possibility of other colors fostering photosynthesis (p. 23) elsewhere in the universe. There are some compelling reasons for the evolution of green pigments in photosynthesis on our planet. First, the range of light absorption by chlorophyll covers about half of the energy of electromagnetic radiation passing through our atmosphere. This is a pretty effective range for the two chlorophyll molecules. The photons within that range have adequate energy content to funnel their energy to the photosystem molecules that are responsible for splitting water and completing the light harvesting cycle, but not too much to destroy the molecule. Furthermore, only one molecule has evolved on our planet with the capability of photosynthesis, and plants acquired the capacity of using this molecule through endosymbiosis much earlier in evolution (p. 25). The pigment in purple sulfur bacteria (bacteriochlorophyll, which does produce a purplish color in colonies) is a variant that absorbs energy at slightly longer wavelengths. At first glance, it appears that chlorophyll a and b are not adequately efficient in absorbing light; they only very weakly absorb the green wavelengths. This concern is misplaced for two reasons. First, the selection in photosynthetic mechanisms among plants for the intensity of sunlight and partial shade has primarily been to develop protection against high light intensities. Thus, photosynthetic efficiency is less important than protection against the inhibition and damage of chloroplasts. Second, the opti-

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Figure 11.10 Leaf optics. Top left, leaves of heart leaf philodendron. Bottom left, interior of a fuchsia leaf, revealing the air spaces that scatter light. Right, section of a leaf, illustrated with ray traces of light into the leaf. (A) partially absorbed by chloroplast and reflected out through the surface; (B) partially absorbed by chloroplast and transmitted through the leaf; (C) reflected by walls and air spaces and reflected out the surface; (D) scattered within leaf without encountering a chloroplast and transmitted through the leaf; and (E) reflected from the surface of the leaf.

cal characteristics of leaves even out the absorption of light. The presence of chlorophyll in bodies (chloroplasts) increases the probability that some light may not be absorbed at the peak wavelengths (the sieving or flattening effect; fig. 11.10). Also, the presence of air spaces between the chlorophyllcontaining cells within leaves increases the scattering of light at weakly absorbed wavelengths, and this increased “path length” increases the probability that green wavelengths will be absorbed. Thus, the absorption of light by a leaf is quite different than that by the chlorophyll molecule in solution. The result is that the green wavelengths are relatively effective in promoting photosynthesis, partly due to the greater penetration of this color into the interior layers of the leaf, increasing their contribution. Black leaves (chlorophyll and anthocyanin) are less efficient photosynthetically;

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the anthocyanin molecules are transported into the cell vacuole and absorb blue and green wavelengths, but they are not able to transfer that energy to chloroplasts. It may be that a very different type of photosynthesis has evolved in other planets, particularly those with very different light environments than those on Earth, and we might eventually find evidence of such differences with more sensitive telescopes. However, leaves on plants have evolved on planet Earth, and they are almost always green.

The Functions of Leaf Color We are conditioned to consider that the colors produced by pigments in leaves serve biological functions, such as for the functions of color by flowers and fruits, attracting pollinators and dispersers. Our ideas about the biological function of color were inspired by the studies of nineteenthcentury naturalists in tropical rainforests. They discovered that brightly colored animals often advertise their toxicity to deter being eaten. The coral snake comes to mind. Other animals have evolved similar colors to avoid predation even though they are not toxic. Color has also evolved as a strategy to avoid being seen, such as green insects living on plants (which may also help them be more effective hunters, like the green praying mantis). Does warning (or aposematicism) or camouflage occur in leaves? Simcha Lev-Yadun, of the University of Haifa, has thought a great deal about plant colors and their potential functions. He has hypothesized that green color could contrast with an insect and make it more vulnerable to being eaten by other insects. He has even suggested that green color, rare on plants in deserts, could warn of thorns and toxic compounds to potential consumers. Leaf color other than green would stand out and might guide the same insects to nearby flowers and fruits, much as the colorful bracts of the bougainvillea attract butterflies to the inconspicuous tubular flowers. Collectively, such colors might attract insects to the plants when individual flags do not. Leaf colors might also camouflage foliage, making them appear less attractive, or even dead or un-leaflike (like a trout lily in the northeastern woods; fig. 11.2). In New Zealand, where many trees have strikingly different juvenile leaves, the dull un-green color of the juvenile leaves may have helped camouflage the leaves to avoid being eaten by the now-extinct flightless moa. White or silver spots on leaves might discourage leaf-mining insects that lay eggs on leaves. The larvae burrow through the nutritious interiors and produce areas of similar color by removing the

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pigments (p. 259). These silver-white areas may “suggest” to the insect that the leaf is already inhabited. In a wild caladium, painting white flecks on green leaves reduced attack by leaf miners, and painting white flecks green on variegated leaves increased attack. Colorful leaves might also repel insects, such as aphids, as an advertisement of toxicity or low nutrient value. Such potential functions are particularly interesting to evolutionary biologists. On the other hand, color produced by pigments may only be a byproduct of some other function of the molecule. What may be important for the plant is that potentially harmful wavelengths of light are absorbed by the molecules, and thus reflected light that is not absorbed (the color) is a consequence of that absorbance. For instance, the white blotches in the middle of a leaf may reduce the temperature increases by reflecting sunlight. Pigments may have other biological properties not related to light absorbance at all. Many pigments are strong antioxidants. When reactive oxygen species (ROS) are produced within cells and tissues, they attack membranes and are harmful. These ROS have been linked to aging in organisms, including humans. The anthocyanin and carotenoid pigments both have antioxidant capacities. The anthocyanin that makes blueberries blue is cyanidin-3-glucoside (the pigment molecule attached to a glucose sugar). It is also the most common anthocyanin producing pinks and reds in leaves. After nutrition scientists at the USDA laboratory at Tufts University showed that mice fed blueberry supplements were better able to remember mazes at older ages— and showed fewer physical signs of brain damage associated with aging— the blueberry marketers publicized the work, and eating lots of blueberries became more popular among senior citizens. In nutrition terminology, cyanidin- 3- glucoside became simply C3G, and you can purchase it as a supplement at health food and nutrition stores. This brings me back to my visit to Oxford University (and the green men, p. 1). I had become interested in the functions of anthocyanins in leaves while working at the University of Malaya and studying tropical rainforest plants in the 1970s. In those forests, young expanding leaves are often pink or red in color due to the accumulation of anthocyanins when the leaves are expanding (fig. 11.5). At maturity the anthocyanins are lost. I had hypothesized that the pigments could protect the young leaves from damage by high light when the photosynthetic machinery is being assembled and when the compact leaf tissue is more vulnerable to pene-

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trating light. This hypothesis became more attractive with the discovery of photoinhibition in leaves by high light intensity (p. 61). Research on photoinhibition was supported by the development of non-destructive instruments that could examine light emitted by leaves— and its rapid decay— after leaves were subjected to a pulse of intense light. This phenomenon, an instance of fluorescence (familiar to us from the glowing images or minerals exposed to “black” light, from ultraviolet lamps) has become a sort of plant stethoscope used by physiologists to examine photosynthetic function under different stresses. The brilliancy of autumn foliage, particularly in the Northeast and Appalachian Mountains of the United States, has created a lucrative tourist industry and no end of speculation and idle conversation on the weather conditions producing peak color and, more recently, whether there might be a biological function behind the color display. Autumn color is a botanical equivalent to the “charismatic megafauna” (like tigers and elephants) that arouse such interest among animal lovers— which is just about everyone, since we, too, are animals. The difficulty of explaining the function of color in autumn leaves, whether a physiological and/or a biological one, is that the leaves are nearing the end of their life spans. The color comes just before they fall to the ground and decompose. It makes no sense for the production of an elaborate protection mechanism to be established just before the death of the leaves. However, if the color improves the function of the tree the following spring, then such a mechanism could make sense. Two such hypotheses have been raised during the past fifteen years. First, William Hamilton— a British evolutionary biologist known for his earlier work on sexual selection— proposed that the brilliant autumn color could serve as a warning (an honest signal) that such leaves contain poisons or low food value, to repel insects that might visit the leaves and lay their eggs for feeding the next spring. The advantage of the brilliant colors would then be to prevent a buildup of insects (and Hamilton was thinking particularly of aphids) that could damage the trees and reduce the production of seeds the following year, thus reducing the fitness of such trees. His original work consisted of a survey of the scientific literature, showing that aphids could respond to leaf colors (particularly yellow). Hamilton tragically died of malaria in 2000 while conducting field research in Africa, and it was up to young collaborators, particularly Marco Archetti, to keep the ball rolling. Archetti was a visiting undergraduate student at Cambridge University,

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where Hamilton was a professor. With an interest in modeling and evolution, Archetti approached Hamilton, who brought him into his intellectual circle. Marco then created and tested models of autumn leaf function and, later on, did some original field research on the subject. In 1998 I teamed up with three Harvard scientists, Missy Holbrook (p. 208), John O’Keefe at the Harvard Forest, and Holbrook’s PhD student at that time, Taylor Feild. We hypothesized a physiological function that the red leaf color in many New England trees, such as the red and sugar maples and the red and pin oaks, could protect the leaves from damage by high light during sunny and cold autumn days when leaves would be particularly vulnerable to photoinhibition and damage. Too much light could damage the leaves in a variety of ways, by directly damaging chloroplasts and by disrupting the process of the breakdown of chlorophyll to produce intermediate compounds that could further damage the leaves. When leaves change color in the autumn, chlorophyll is being carefully broken down, and its by- products are pumped into the cell vacuoles where they can do no harm. Simultaneously, the proteins— enzymes and molecules to which the pigments attach on the chloroplast membranes— are being disassembled into their amino acid building blocks. Those amino acids are then translocated via leaf veins, down the petioles and into the branches and trunks of the trees. They are stored for the winter and then released for tree and leaf growth the following spring. We hypothesized that the anthocyanins (red leaf color) protected the leaves during this resorption process, and that leaves with anthocyanins would end up with less nitrogen (more going into the parent tree) than those without. We characterized the general changes of colors of trees at the Harvard Forest in central Massachusetts. Feild documented the photoprotection by anthocyanins in red leaves of the red-osier dogwood, and we showed that there was a tendency among all trees for red color to be correlated with lower nitrogen contents. While we were preparing this for publication, William Hoch, then a graduate student at the University of Wisconsin, published a review on autumn color, advocating this protection hypothesis in some detail. Later he copublished a paper showing that anthocyanins could protect senescing leaves and reduce the residual amount of nitrogen in the leaves. These two hypotheses were not mutually exclusive, and neither was supported by very much evidence. Nevertheless, a controversy arose about which one was right. I like to think that less data creates the conditions for more hot air and invective, seen in some recent reviews on autumn coloration in the evolutionary and ecological journals.

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This brings us back to that meeting in Oxford in 2008 (p. 1). It was essentially due to Archetti’s goodwill in bringing together participants in the research, representatives of both sides of the argument, where all of the most current data could be shared and discussed . . . and just perhaps some sort of consensus could be reached. A key participant in the discussion was Simcha Lev-Yadun. When all was said and done, we agreed that (1) we didn’t know very much, but there was some evidence for both hypotheses; (2) we needed to learn more to better test the hypotheses; and (3) we collaboratively wrote a comprehensive review on the subject. Just as important, we spent some valuable time getting to know each other by sharing food and drink at the nearby Eagle and Child Pub (owned by St. John’s College, where we had held our meeting), the same place where C. S. Lewis and J. R. R. Tolkien discussed language and mythology many decades earlier (p. 2). In the past few years, new details about leaf senescence have been uncovered. In some evergreen plants, such as those in the Appalachian Mountains, leaves turn red in the winter, and anthocyanins are physiologically protective. In a New Zealand tree, horopito, leaves vary in color, due to the accumulation of anthocyanins. These anthocyanins neutralize the hydrogen peroxide that is produced when leaves are damaged. In such leaves with red edges, red color is associated with a known insect toxin, polygodial. Thus, in this plant the red color was an honest signal that the plant could repel herbivores. In sugar maple, red leaves (1) have lower residual nitrogen (consistent with the photoprotection hypothesis); (2) last longer than green or yellow leaves; and (3) also have higher sugar levels. This raises the possibility that color is associated with longer leaf life. Longer leaf life could be important in returning more sugars and starch to the parent plant. In a subtropical mountain forest in southwest China, the majority of species are evergreen, but one common deciduous tree produces red leaves lasting most of the winter. Anthocyanins protect the leaves, allowing them to function longer in the winter months, and produce more sugar and starch for the next year. Longer leaf life may be a factor in the responses of different plants to climate change, giving exotic invasive species a leg up in the competition for space in forests. Spring red leaf color is more common in the forests of Japan, Finland, and Israel than autumn color, and the color of a tree in the spring is not predictive of its color in the autumn; thus leaf color function may vary with season. What works for a tree might also work for an herbaceous perennial plant, but not for an annual plant where nitrogen could not be resorbed in

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storage tissues. The leaves of many wildflowers turn red during the autumn, but not as commonly as trees. The mechanisms of photoprotection during the autumn may vary among species, such as between maples and oaks. Leaves turn yellow, like some oaks, and leaves turn red, like the sugar maple. These trees have different protective mechanisms during senescence. Gradually we are adding information to the phenomenon of autumn color change, partly addressing these two hypotheses, and also not predicted by either hypothesis. Who knows; other explanations may be at play. Our knowledge of the phenomenon is pretty superficial at this point. These plants are not diseases, and they are not generally economically important, so they get little attention— no NIH grants here. The vividness of forest color during the autumn, and perhaps during the springtime, varies in different regions. Perhaps nowhere is the display of autumn color more spectacular than in New England, although residents along the Appalachian Mountains in the Southeast might dispute that (and I’d have to agree with them). What makes for attractive color in these forests is the proper mixture of trees that produce the autumn colors. In New England the bulk of the peak color is caused by red and sugar maples, with some deep purples added by the ash, and later and duller reds produced by oaks. In the Appalachians, maples and oaks are important, but sassafras and sourwood also produce brilliant oranges and reds (fig. 11.4). Simcha Lev-Yadun and Jarmo Holopainen have concluded that the brilliance of red autumn color in North American forests compared to the yellows of European forests is a consequence of the species compositions of the different forests. Some trees, such as oaks and maples, produce more reds, while beeches and birches produce more yellows. In a similar way, historical changes in the composition of North American forests have affected autumn color. At the beginning of the twentieth century, the color was dominated by yellow, because of the importance of the American chestnut and the American elm in those forests. Both of these species were removed by disease— the chestnut blight and the Dutch elm disease— and were replaced by more red and sugar maples. Now even present species that contribute to autumn color may die out: maples by the Asian long-horned beetle, ashes by the emerald ash borer, and oaks by sudden oak death. So the future may produce less reds and more yellows in our forests. Furthermore, increases in temperature caused by global climate change are delaying the changes in leaf color and their fall, and in the future may shift the distributions of trees. The sugar maples may be removed from southern New England but will grow farther north in Canada. The sassafras and

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Figure 11.11 Increasingly, remote observations of color changes in forests are being used to assess the effects of climate change on the delay in leaf fall and the increase in leaf life spans. Color changes in the temperate forests of northern Michigan (courtesy of Ted Fleming).

maleberry trees may also grow more to the north. We will document these changes by remote sensing, from airplanes or satellites (fig. 11.11). Leaf colors surround us, even in very urban places. Above all, the color green attracts us, but the subtle differences among greens allow us to distinguish among hundreds of different leaves. When other leaf colors appear, it is cause for notice and, even, celebration.

Chapter Twelve Food Oh, spinach is one of my favorite foods; I savor each wonderful bite. I eat it each day served up every which way. I also enjoy it at night. I love every leaf, every seed, every sprout; Each plant in the vegetable phylum. I like to consume them right here in my room at the lunatic mental asylum. kenn nesbitt, “Spinach Is One of My Favorite Foods”

Eat mostly plants, especially leaves. michael pollan, In Defense of Food

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s a side benefit from studying tropical plants, I’ve learned about the cuisines of the people living in the tropics. I’ve learned about their foods by visiting the markets in the towns near my field sites. The unusual fruits, root and leafy vegetables seen in these countries, with some tropical plants shared among them all, mirror the complexity of their forests. Certain vegetables and fruits are strongly identified with particular cultures, such as the durian— a fruit of Southeast Asia. Leafy vegetables are important in their cuisines, and they vary considerably from region to region (fig. 12.1). In Malaysia the markets sell the ingredients of the cuisines for the Tamils, · 234 ·

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Figure 12.1 Vegetable vendor, Chiang Mai Market, Thailand, 2005.

Hokkien, Cantonese, Thai, Malay, and European. In Western diets, it is fairly easy to list the leafy vegetables— for example, spinach, Swiss chard, kale, collard greens, and so on. I’ll leave out lettuce, as it doesn’t add very much in the way of nutrients to our diets. In the tropics, these temperate vegetables may be sold (grown at higher altitudes and shipped to the lowlands), but there is a bewildering variety of others. Many of them look like spinach, which is now our most popular leafy vegetable, and are given spinach names, as New Zealand spinach, Malabar spinach, water spinach, Palak (Hindi and Urdu for spinach, which includes many species besides the

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common spinach), African spinach, and more. From the “foodie” movement, we are seeing a greater variety of such leafy vegetables in our diets. My first contact with the spinach of American diets was not a very positive one. In the 1950s, spinach was available canned and, later on, as frozen bricks. In our home, spinach was heavily cooked, dull olive green in color, and barely palatable. As kids we followed the adventures of Popeye in the movie and TV cartoons, and knew the miraculous benefits of one of those cans of spinach. Only much later did spinach become available as a fresh vegetable, unless you grew your own in a home garden. The spinach in our diets is a species, Spinacea oleracea (named by Linnaeus), in the Amaranth family, one of those with unusual pigments, the betalains (p. 223), and originally from central Asia. From Persia it spread to India and China, and into Europe via Arabian influence in the Mediterranean. Spinach is valuable because of its combination of vitamins and minerals, as well as proteins, carbohydrates, and even some lipids. In our diets, we require many nutrients, essential because we cannot make them ourselves. We make our own proteins, but nine of their amino acids have to be obtained in our diets: essential amino acids. We make fats through our metabolism, but certain unsaturated fatty acids, as those in fish oils (and in spinach) are obtained in our food. Out of a list of fourteen vitamins essential to human nutrition, spinach has appreciable amounts of nine: A (β-carotene, retinol), B1 (thiamine), B2 (riboflavin), B3 (niacin), B6 (pantothenic acid), B9 (pyridoxal), C (ascorbic acid), E (alpha-tocopherol), folic acid, and K (phylloquinone). Out of the sixteen minerals that are also essential, spinach supplies eight: calcium, phosphorus, potassium, sodium, zinc, iron, magnesium, and manganese. Spinach is also a valuable source of protein, with an excellent balance of the essential amino acids. So, it is no surprise that Popeye got such a boost from them, although their contribution of iron was exaggerated. Leaves have always been important in human diet, going back to the origins of our primate group, the hominins (p. 295). Three million years ago our ancestors were living in forests, eating leaves and fruits, as well as small animals that ate the same. About 1.5 million years ago, human ancestors moved out into the open savanna and ate grasses and grains, also along with the animals that ate them. The diets of contemporary humans in traditional cultures were rich in leafy vegetables and fruits. Within the past century, with the rise of commodity agriculture and processed foods, the portion of fresh fruits and vegetables in our diets has declined, and our health (poor nutrition, obesity, diabetes) has suffered.

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Although spinach may be the most nutritious among the popular leafy vegetables, others provide different nutrients and may complement those of spinach. For instance, Swiss chard provides some copper and zinc minerals, and kale adds choline. Spinach is presently a major agricultural crop in the United States, particularly in California and Arizona, and we are second to China in production globally. There is a negative side to our commercial production: occasional illness from harmful E. coli strains and contamination by heavy metals and pesticide residues. Leaves are important sources of nutrients because of their high metabolic activity, the most concentrated in the plant. Leaves are the sites of photosynthesis, much respiration, the export of sugars to other parts of the plant, and the synthesis of a range of chemical products that may accumulate in the leaf or be exported to other parts of the plant. The vitamins and minerals in leaves are essential for this metabolism. Every chlorophyll molecule has magnesium at its heart. Phylloquinone (our vitamin K) is a part of the electron transport chain, and other molecules may use iron and manganese. All living cells contain potassium, calcium, and sodium. Some minerals and vitamins— such as thiamine, manganese, and zinc— are necessary for the catalytic functions of essential enzymes. Other vitamins are protective of the photosynthetic mechanism in plant cells. Carotene transfers light to chlorophylls. Carotene and similar molecules, along with ascorbic acid and alpha-tocopherol, protect the chloroplasts against oxidative damage from excessive light absorption. We are discovering how important these plant pigments are to human health. Three of the carotenoids present in leaves— lutein, zeaxanthin, and β-carotene— are crucial for human vision. Lutein and zeaxanthin are sequestered in the macula of the retina, the place of highest visual acuity. There they protect the visual receptor cells from damage from high light, through absorption of blue wavelengths and as antioxidants. β-carotene is the most important of the pro-vitamins. Animals, such as humans, produce an enzyme that splits the molecule in half, producing two molecules of retinol (we also obtain retinol by eating meat from animals who have consumed β-carotene and other pro-vitamin carotenoids). When converted to retinol, it becomes the light-absorbing unit in the visual pigments. Retinol may also be converted to retinoic acid, which is essential for bone and tooth growth, as well as skin health. Red anthocyanins are present in some leafy vegetables, and they are also strong antioxidants. Although the structure of the most common pigment, chlorophyll, is similar to the oxygen- carrying ring in hemoglobin and other molecules

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with a tetrapyrrole structure (p. 51), it has no such function in humans and quickly loses its central magnesium atom in the acidic environment of the stomach. Several light-activated intermediate compounds may form. These are assimilated in the human digestive tract and are present in the serum and in the body tissues. These molecules are generally of a dull green color, explaining the color of that canned spinach I detested as a child. However, if treated with zinc or copper ions to replace the magnesium, the molecule is stabilized and retains its bright green color. There are thousands of claims of the benefits of chlorophyll in humans, including reducing the foul smell of passed gas! It does appear that chlorophyll can defend against a variety of cancers, as in the colon and, in particular, liver cancer caused by the intake of the fungal aflatoxin. There is certainly much more to be learned about the beneficial effects of plant pigments to our health.

Herbivory I once heard a biologist in a seminar say, “Biology is the study of plants and their parasites,” another way of explaining that carbon and other elements move into food chains via plants and photosynthetic algae— mostly through the consumption of leaves. Plants are thus under intense pressure from diseases (fungi, bacteria, and viruses) as well as parasites and larger animals. Leaves, metabolically active and full of nutrients, are particularly vulnerable. As long as leaves have existed, they have been subjected to attacks by organisms, especially insects. Thus, it is not surprising that plants produce an amazing diversity of defensive structures. Spines prevent herbivores from feeding on leaves; sharp teeth along the edges deter those chewing insects that start out on the edges. Hairs and scales prevent smaller insects from feeding. Even the cuticle, particularly with a thick covering of waxes, may prevent sucking insects from reaching the nutritious inner tissues. Fibers, stone cells, and crystals inside leaves mechanically deter chewing insects. There are limits on such defenses protecting leaves. The surface must remain transparent to allow sunlight to penetrate the leaves; and the stomata, mostly on the undersurfaces of leaves, allow fungal hyphae and bacteria to enter when they are open and exchanging gases. Another defensive strategy of plants to reduce leaf consumption is camouflage. Color may disguise leaf appearance, chlorophyll and anthocyanin producing a brown color that makes leaves look dead (p. 223). A remarkable woody vine, Voquillo, native to forests of temperate Chile, has the ca-

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pacity to change leaf shape to resemble those of the tree on which it grows. It changes leaf morphology to match different species of trees, and a single vine changes accordingly when it spans more than a single tree crown. This is a baffling but well-documented camouflage growth response, which defies any traditional mechanism. The most extensive and diverse defenses of leaves against being eaten are chemical ones, and they reflect the amazing biochemical diversity of plants, with numerous pathways that are not present in animals. Pathways producing pigments, such as the flavonoids (particularly the red anthocyanins, p. 224), are unique to plants. Other pathways produce a bewildering variety of bitter, smelly, fragrant, or toxic compounds. The chemical products of leaves, important in human culture such as tea and coffee (theophylline and caffeine), tobacco (nicotine), and coca (cocaine) are some examples. These molecules are synthesized by different pathways, but those with nitrogen present in their carbon structures are alkaloids. Alkaloids generally affect the nervous systems of animals; nicotine is an effective insecticide, but there are many other classes of toxic compounds. Non-protein amino acids are taken up by animals and render their proteins non-functional. Some leaves induce hallucination, used by shamans in tropical America, such as the leaves of ayahuasca, a South American vine. Cyanogenic glucosides in many leaves release a potent respiratory poison, hydrogen cyanide, when they are broken down in the digestive systems of animals. Some terpenoid and flavonoid molecules mimic the steroid molecules of animals and disrupt their development and reproduction. Other terpenoid molecules may affect heart function in animals; some are useful to us at low doses in stimulating heart function, as with the cardiotonic glucosides of foxglove, or are fatal at high doses, such as poisoning from oleander. Members of the mustard family (Brassicaceae) include some leafy vegetables (cabbage, kale, mustard greens, brussels sprouts) that share some unique chemical compounds: the mustard oils or glucosinates. When these break down during digestion, they produce some pungent sulfurcontaining by- products. Although most animals are repelled by these molecules, some specialists do quite well with them. Leaves also exude chemical compounds that have an essentially mechanical effect on insects (fig. 12.2). In addition to veins, many plants develop systems for the storage and delivery of latex and resins. These are under pressure in leaves, so that when insects chew on the leaves, these compounds are pushed out and gum up the mandibles of insects. Toxic compounds may also be present along with these viscous fluids. Resins and

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Figure 12.2 Resins and latexes as leaf defenses. Left, latex in leaf of banyan fig; right, resins in leaf of frankincense.

latexes may be industrially important, such as the latex of the Brazilian rubber tree used to make natural rubber, still essential for the production of aviation and automobile tires. Students of plant-animal interactions have classified these molecules and defensive strategies in a variety of ways, reflecting the roles in defense. Some molecules are not toxic, but may reduce the palatability or digestibility of food. Tannins may complex with vegetable proteins, making it difficult for animals to digest them. Other compounds may inhibit the activity of digestive enzymes as amylases (starch breakdown) and proteases (protein breakdown). The effects of these defenses are quantitative, depending upon the amounts for the effects, while qualitative defenses are toxins, killing the invader at low doses. Some chemical defenses are always present at a certain concentration, while others may be induced to high concentrations after the attack of the herbivore. Fast- growing and shortlived plants may not have any defenses at all, and rely on rapid growth to outpace the herbivores; long- lived plants rely more on defenses, particularly chemical ones. The traditional explanation for these differences was that slow-growing plants are more apparent, more likely to be found in the environment, than ephemeral plants. A more recent explanation is that the costs of defenses related to the benefits of reduced leaf consumption by herbivores are high in short-lived plants (high investment and not enough time to make a profit) compared to long-lived ones. Perhaps this is an oversimplification from the thousands of papers, both experimental and theoretical, written about herbivory.

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Chemical defenses in plants are also influenced by the environments in which they live. We assumed that defenses would be more common and elaborate in tropical plants, where biological interactions seem more intense. At least this specificity may hold true for butterflies. However, mechanical and chemical defenses, in bewildering combinations, are found in plants in all communities and at all of the latitudes where plants grow. The amounts of these chemicals may be influenced by the physical environment, such as light and temperature. In 1998 Francis Hallé (p. 140) contacted me about his desire to test a long- held opinion about tropical rainforests. These forests were being prospected for potentially valuable drugs by botanists collecting plants in the understory of these forests, where access to the plants is easy. However, Hallé felt that the real place to search was in the forest canopies, including epiphytes and the foliage of large trees, where sunlight might promote their production and pressure by herbivores would be greater. Plant biochemist colleague Kelsey Downum and I worked with Hallé during one of his canopy raft expeditions in Gabon (fig. 12.3). We selected four tree species, with saplings in the understory and large canopy-level adults. We analyzed foliage extracts to determine the diversity and relative concentration of molecules, and also

Figure 12.3 The canopy raft in Gabon. Left, the team (left to right), Francis Hallé, Gilles Ebersolt, and Danny Cleyet-Marrel. Right, Kelsey Downum under the dirigible, collecting foliage.

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determined if the extracts had biological activity against different bacteria. We found that Hallé was correct, that the canopy foliage had about four times as many molecules at about three times the total concentration. We also found considerable antibacterial activity in extracts of three of the four trees. Thus, defensive compounds may vary considerably under different conditions within the same plant. Plants are also sensitive to changes in the spectral quality of light under foliage shade, to reductions in the red to farred ratio (p. 162), which reduce plant investments in defensive chemistry, compared to full sunlight.

Defending an Attack Many plants produce defensive compounds after being attacked by herbivores, making them better defended afterward. Some plants are even sensitive to the vibrations on leaves being chewed by herbivores. Furthermore, the signaling of the attack can be communicated to other parts of the plant, to other plants of the same species, even to other species in the neighborhood, to induce a more effective defense to leaves that have not been attacked. Through extra- hereditary changes to their DNA, some species increase defensive responses in the next generation. We rely on our immune system to specifically defend against foreign molecules and organisms that invade our bodies. This defense involves special attacking cells and circulating antibodies to remove the foreign invaders. Furthermore, our system is capable of “remembering” an earlier attack, making it able to more quickly and specifically respond to a later attack. Although plants have evolved sophisticated defense systems, they do not have this specific capacity of “memory,” and each attack, whether from the same or a different organism, is treated in much the same way. I am looking at my tomatoes, envisioning the fat vine-ripened fruit to be enjoyed in a month’s time. There are lots of things that consume the leaves: spider mites (which make small white spots), leaf miners (which produce silvery maze-like trails as they burrow through the edible interiors of leaves; p. 260), the Colorado beetle (adults and larvae feed on potatoes and tomatoes), and cutworms. What takes the cake are big green and fat hornworms (fig. 12.4). These are the caterpillars of a sphinx moth, and they specialize on foliage of the nightshade family, including potatoes, tomatoes, and tobacco. One of those large hornworms will defoliate a single plant in a day or so. I pick them off, looking underneath the leaves as well. They are so big and green with those “horns” at the tail end, that I’m reluctant to

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Figure 12.4 Tomatoes and hornworms. Top left, tomato foliage, fruits and flowers; top right, defensive hairs on tomato leaf; bottom left, a tobacco hornworm on a tomato plant; bottom right, a hornworm with pupae from a parasitoid wasp.

grab them— and so are birds, I guess— but the hornworms are harmless to me and devastating to my future tomatoes. I notice that the plants give off a pleasant leafy smell, and I get a bigger dose of that fragrance if I gently crush the glandular hairs on the leaves. These contain the small molecules that easily and quickly evaporate and diffuse in the atmosphere, imparting that characteristic tomato smell. We call them green leafy volatiles. The volatile organic compounds (or VOCs; p. 86) produced by the fruit tell me when it is ripe. Some of those molecules are quite toxic to most insects, but not to the hornworm. That same caterpillar, when it feeds on tobacco, stores the nicotine and releases it into the atmosphere, repelling some of its predators. We actually know quite a bit about the responses of tomatoes to these pests, quite similar to its cousin the tobacco hornworm, which feed on a once more economically important plant than it is today. The female sphinx moth and other insects that visit my tomatoes pay a lot of attention to those leafy green volatiles. The female sphinx moth senses the volatile molecules with special cells in its antennae. It can accurately detect the

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relative concentrations of many volatile molecules. Some two thousand of these molecules have been identified in various plants so far, although the moth detects the molecules of its preferred hosts. It lays its eggs on leaves of the tomato plant at night, attracted by the array of volatile chemicals. However, if leaves have been visited by insects that are predators of the hornworm or have already been attacked by a hornworm, the moth will look elsewhere for a plant on which to lay them, because the concentrations of volatile molecules have altered slightly. Those eggs hatch into small caterpillars that quickly grow as they feed on the plants. As the hornworms chew on the leaves, the plants respond to an ingredient in the saliva that combines with one of the volatile compounds in the leaf to produce an elicitor, volicitin. Volicitin activates a complex signaling network that results in the production of jasmonic acid. Jasmonic acid then triggers the production of a number of defensive compounds in the leaf, including alkaloid toxins and inhibitors of the enzymes that break down starch and proteins. The concentration of tannins may also be increased. Similar mechanisms occur in other plants and also in response to attacks by fungi.

Spreading the News Plants, such as the tomato, have the capacity to communicate the attack information to other parts of the plant and to other plants. The jasmonic acid produced in the tomato leaf cells can move to adjacent cells via connections between cells (the plasmodesmata) to spread the response to the entire leaf. The acid can also be translocated via the phloem tissue to other branches and leaves. Chemically altered, it becomes more volatile and can move through the atmosphere. A remarkable story of defensive communication in acacia trees was derived from the research of Wouter van Houten, a wildlife scientist at the University of Pretoria, in South Africa. Although his evidence falls far short of that for tomatoes, it is ecologically more interesting. Wildlife biologists had observed that the lesser kudu, an antelope native to the region, was selective in its browsing on the many common trees, especially hook thorn (fig. 12.5). The kudu browsed on the tree for a short time, then moved to another tree, and they always moved downwind from the previous tree. Giraffes, which also browsed the acacias, behaved in a similar way. Van Houten hypothesized that the browsing elicited the increased synthesis of tannins, which made the foliage less palatable. Not only did the browsing

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Figure 12.5 Lesser kudu in southeast Africa.

affect adjacent branches but it had also signaled to the plant to produce a volatile chemical (he speculated that it was ethylene, a growth- regulating gas that plants make). Van Houten showed that when the kudu was impounded in fenced-in savanna with the acacias, animal mortality was directly correlated with both the density of animals and the levels of tannins in the leaves. He even conducted feeding experiments where he showed that the tannins in the crops of the kudu decreased the production of vegetable fatty acids. These results led to success in the raising of wild kudu by insuring that there were enough trees to be browsed and then left alone for the tannin levels to eventually drop down. Communication between trees, allowing for the induction of leaf defenses, occurs through direct root connections, and even via the mycelia of mycorrhizae— fungi that are so prevalent in helping roots obtain phosphorus from the soil. We also know that a variety of volatile chemicals,

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particularly ethylene and methyl jasmonate, can communicate information about attack to other trees. Volatile molecules also signal plants that are parasitic on other plants, as with dodder being attracted to tomatoes. Since the volatile compounds are the products of various metabolic pathways, the actual responses of the plants are extremely broad and complicated and are connected to the production of the major growth regulators, such as auxin. When the common cutworm attacks its tomato host, the plant ups its production of VOCs. One of them is converted by neighboring plants into a potent insecticide nicknamed hex-vic. Thus the signal molecule quickly becomes the defensive compound. A common whitefly, feeding on tomatoes, takes in a bacterium that suppresses the jasmonate defensive pathway, and it can successfully suck the sap from the leaves. We have learned enough about these defensive chemicals to begin to generalize that chewing insects elicit more defensive compounds than sucking insects and that domesticated plants produce fewer defensive compounds but more of terpenoid molecules than wild plants.

Recruiting Animal Defenders Just as insects can detect volatile molecules to know where to lay their eggs, plants can also produce volatile molecules to recruit other insects that are predatory on the herbivores. Tomatoes are a good example. These molecules diffuse into the atmosphere, where other insects can detect them. Hornworms are attacked and killed by big- eyed bugs, lacewings, and parasites. Wasps are also attracted to the leaves, looking for caterpillars on which to lay their eggs (fig. 12.4). The eggs then hatch, and the larvae burrow into the caterpillars and consume the soft interiors, killing them. The saliva of the caterpillars changes the leafy green volatiles in ways that attract the attention of the big-eyed bugs, and they make quick work of the hornworms. In a similar way, the spider mites that damage leaves of tomato plants attract predatory mites that kill the herbivores. There is a complex dialogue of odors occurring as my tomatoes grow, providing mechanisms for direct protection by the plants, and indirect protection by enlisting the help of other insects. Adversely, parasitoid wasps change the VOC mix to attract still other insects that attack the wasps. The previous examples are of insects that are recruited temporarily. If there are no herbivores, these predators will not be attracted to the plants. Additionally, plants attract insects (mostly ants) by providing food and drink— and sometimes even a place to stay (more about that in chapter

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Figure 12.6 Ants and plants. Top left, bullhorn acacia, ants collecting a Beltian body from a leaflet (courtesy of Judy Gallagher). Bottom left, Inga, ants at nectaries between leaflets, Ecuador (courtesy of Alexander Wild). Right, the adultery tree with its ferocious ant defender, in Gabon.

13). The ants may be attracted by green leaf volatiles, but what keeps them there are the nutritive rewards, at a modest cost to the plant. In return, the ants attack any animal that approaches the leaf. This is often a mutualistic interaction; both partners benefit. The classical example, first studied in Mexico by the eminent tropical biologist Daniel Janzen, is the association between the bullhorn acacia and the acacia ant (fig. 12.6). The acacia provides nectar (Gatorade, really) from glands, or nectaries, along the compound leaves; starchy food bodies (called Beltian bodies after their discoverer, Thomas Belt) at the tips of leaflets, and nesting sites within the hollow spines. The ants ferociously attack any interloper, from cattle to caterpillars. Cattle can apparently sense the ant pheromones (volatile compounds the ants produce) and avoid those trees. Janzen showed that small bullhorn acacia trees could not survive in the absence of the ants. In the savanna of East Africa, ants living on acacia trees can even repel elephants. Apparently, the elephant trunk interiors are sensitive to those little stinging ants. Nectaries are not such a radical evolutionary change, since veins, when chewed on by an insect, can ooze sugar water and attract defending ants, as in the bittersweet nightshade. One of my colleagues, Suzanne Koptur, is an acknowledged expert on

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these interactions, particularly from her study of ant-plant interactions in Inga, a genus of leguminous trees in Central America. At the Monteverde Field Station, Koptur studied the distribution of ants and individuals of Inga at different elevations (fig. 12.6). In Inga densiflora and I. punctata, ants were recruited at lower elevations and defended the trees against herbivores. At higher elevations, fewer ants were available and the foliage had higher concentrations of chemical defenses. At the higher elevations, parasitoid wasps were attracted by the nectaries and deposited eggs on the herbivore caterpillars, killing them and reducing the loss of leaves. In Gabon, Francis Hallé led Kelsey Downum and me on long walks in the understory and taught us much about the plants we encountered. I was particularly struck by a small understory tree of the passion fruit family, the ant tree (fig. 12.6). This tree attracts a particularly ferocious ant, Tetraponera aethiops, which lives in the hollow stems and rushes out at the slightest vibration. It defends the tree against any invader and even prunes away branches of neighboring trees. It kills many insect invaders, dropping some to the ground and eating others. Hallé told us that a single sting by this ant would put us out of commission for a day, and that the tree was also known as the adultery tree because the guilty would be tied to the tree as a lethal punishment. Some ants are attracted to leaves because of the activity of sucking insects, as thrips and aphids. The ants actually maintain those herbivorous insects so that they can extract the sugar-rich plant sap from them. These interactions are often easy to find in a garden because the excess sugar water attracts molds, turning the foliage black.

Plant Intelligence The “behaviors” of plants toward their herbivore enemies, and the sophisticated biochemical and genetic mechanisms behind them, suggest a form of “intelligence” in the responses. The plants can sense the presence of different herbivores and respond with chemical defenses, and they can enlist the aid of predators in killing the herbivores. By intelligence, I do not mean the operation of a central nervous system and brain— and consciousness; rather I mean that the sensitivity of detection and deterrence are built into the complex control networks in the plants, involving various signal systems that operate through small and mostly volatile molecules. The “intelligence” is part of natural selection and the evolution of the signal pathways, not any evidence for intelligent design. Even the use of the word

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“intelligence” in describing plant responses is viewed with alarm by many. Anthony Trewavas, an eminent plant physiologist at the University of Edinburgh, has argued just that; the sophistication and sensitivity of these signal networks display characteristics of intelligence, embedded within the very networks. Trewavas, along with Jack Schultz (some of whose work was cited in the previous paragraphs) and many other plant biologists have formed a society, initially called the Society of Plant Neurobiology. Neurobiology seems a stretch, as we think of it in terms of neurons and nervous systems. However, we have known for some time that plants produce electrical signals, or action potentials, in response to outside stimuli (p. 274). Even the etymology of the word “neurobiology” has a strong plant connection. In early Greek, neuron meant vegetable fiber. Neuron was then used in animal biology to describe specialized cells that could be excited to produce action potentials. Such cells, organized collectively to different degrees in different animals, are the basis for the organization of the nervous system. After all, the human brain consists of 100 million neurons that form connected networks (1,000 trillion connections, or synapses). Something emerges from the vast number of cells and incomprehensible number of connections. The cellular networks in plants are comparable, if considerably more simple. At any rate, after some criticism, the organizers of this new scientific discipline changed its name to the Society of Plant Signaling and Behavior, the same as its new journal. No matter the name, everyone can agree that the signal pathways of plants, seen in the responses of leaves to herbivores, are beautifully complex and sophisticated. Truly awesome.

Flavor and Fragrance From the volatile chemistry of leaves, I return to the subject of leaves in our diet. Many of our popular leafy vegetables came from ancestors with toxic chemicals, such as cyanogenic glucosides, and those chemicals were bred out of them through human selection. Some of the flavors of these vegetables, as members of the mustard family (like cabbage and mustard greens), retain some of those pungent volatile chemicals that give them a peculiar attractiveness. Some molecules give certain leaves special fragrances and flavors. In many cases we know the most common volatile compounds imparting flavor, and we use that knowledge commercially. In vanilla, the predominant volatile compound is vanillin; it is used in flavoring foods and creating perfumes. In leaves and fruits of cloves and allspice, the principal aromatic oil is eugenol. In thyme, it is thymol. The actual

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Figure 12.7 The garrigue, home of herbs. Left, general habitat above Saint-Guilhem-leDésert, southern France. Right, close-up of vegetation near Salubreña, southern Spain. Plants there included rue, thyme, sage, and rosemary.

natural products, the herbs and spices, have subtler flavors, from the contributions of dozens of volatile compounds. We generally consider aromatic leaves as herbs, and aromatic fruits (allspice), bark (cinnamon), and flower buds (cloves) as spices. The evolution of such compounds in plants, in response to herbivores, has given us the flavors of our foods, particularly enriched in the cuisines of the Mediterranean. Such aromatic plants evolved in a climate of cool wet winters and hot dry summers, with defenses against herbivores and possibly defenses against competing plants (fig. 12.7; p. 79). The list from this vegetation, called by the French garrigue (or mattoral in Spanish), is impressive: rosemary, thyme, oregano, bay leaf, tarragon, coriander, lavender (yes, wonderful in cooking), rue, and sage. The search is still on for new plant odors, often secretively because of their commercial importance, as in perfumery. During the canopy raft expedition in Gabon (p. 241), Kelsey Downum and I worked alongside odor chemists from the Swiss corporation Givaudan; they guarded their information. I remember Francis Hallé recounting a disappointing conversation with one of their perfume chemists. Perfumist: “I made an amazing discovery today.” Hallé: “Wonderful, what was it?” Perfumist: “I can’t tell you, it’s a secret.” I like the leafy vegetables from my garden, such as the pungent Chinese cabbage (bok choy) and collard greens, cooked quickly, steamed with a little water in the pan. Then I eat them after sprinkling a little olive oil and aged tarragon vinegar on the vegetable. Nutrition and flavor.

Chapter Thirteen Homes And now the green household is dark. The half-moon completely is shining on the earth-lighted tops of the trees. To be dead, a house must be still. The floor and the walls wave me slowly; I am deep in them over my head. The needles and pine cones about me james dickey, “In the Treehouse at Night”

An affinity for shade, trees, the nebulous glimmering of the forest interior, the tracery of branches against homogeneous surfaces, climbing, the dizzy childlike joy of looking down from a height, looking through windows and into holes, hiding, the mystery of the obscure, the bright reward of discovered fruits are all part of the woody past. Restfulness to the eyes and temperament, unspoken mythological and psychic attachments, remain part of the forest’s contribution to the human personality. paul shepard, Man in the Landscape

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tree house floating beneath the canopy of a northwestern forest appeared on the TV screen adjacent to the computer I was working on, downloading articles for this chapter. My grandson had the TV on the Animal Planet Channel. There we saw an episode of Treehouse Masters, hosted by Pete Nelson, who builds tree houses. The owners of these fantastic houses were interviewed; I be· 251 ·

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Figure 13.1 View of tree house designed for children, at the Morris Arboretum, in Philadelphia, PA.

came aware of their deep desire to have dwellings connected to the crowns of trees, with the filtered light illuminating their elevated rooms (fig. 15.7). I was reminded of the quote by Paul Shepard (above, and p. 298) in which he speculated about our connection to trees through our recent evolutionary history, as apes living in forests. It recalled my childhood playing on the simple platform we erected on the branches of our weeping willow tree (fig. 13.1). One of the students in my “Meaning of the Garden” course did her project on the tree houses in Miami, photographing them and interviewing the kids about their experiences in the tree crowns. Nests in trees are important in the lives of all of the great apes, with the exception of gorillas, who are too heavy for such elevated nocturnal rests. Chimpanzees, orangutans, and bonobos all build daily nests at varying elevations in trees, depending upon the animal’s gender and age. Leaves form

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cushions for comfort during sleep. For the bonobos, who erect their nests close to one another, they add a foliage canopy to deflect the rainfall not intercepted by the crowns above their nests. Orangutans, more solitary in behavior, make separate nests with similar protective canopies. The afternoon tropical rainforest thunderstorms produce torrents of rain; it seems difficult to breathe for the deluge. Within the forests, the power of those storms is attenuated by the thick layer of foliage. In my rainforest wanderings, I often found that the forest would protect from a brief storm, but I was soaked and cold after a longer one. The nests also help protect the apes from predators and give quicker access to nearby fruit trees. They construct the nests in just a few minutes at the end of the day, and the youngsters learn the techniques from adults. Perhaps the nest-building capacity came from the tendency of apes to pull branches together to effectively support their weight when they reached for the ripe fruits at the tips of branches. No matter its origins, the nesting behavior seems to have been an important invention in the evolution of the great apes, and perhaps the foremost tool-making skill— something our ancestors likely mastered as well. A secure porch allowed them to sleep more soundly in a prostrate, rather than standing, position. This deeper sleep provided mechanisms for greater physical rest and enhanced retention of memories during the episodes of REM (rapid eye movement), which may have facilitated the social activity that made the apes so successful. The tendency of some chimpanzees to construct terrestrial nests may have been a precondition for humans to do the same. Apes protecting themselves with foliage are very photogenic, as are people doing the same thing with bananas or other large leaves (fig. 13.2). We humans have taken advantage of plants and foliage to construct shelters, particularly when living within or on the edges of forests. The Temuan are a tribal group living in the Malayan Peninsula, or West Malaysia. They are a forest people and traditionally made a living by collecting food from the forest and practicing some shifting agriculture, whereby they temporarily grew crops after clearing a small area of forest. In forest trips, I occasionally hired them as guides and porters, as for a trip in the adjacent Ulu Kenaboi, in 1975. There a small group, who fled the “noise” of Ulu Langat, established a clearing and built this house (fig. 13.3). It is a simple structure, built on a raised platform with hardwood posts and split bamboo walls and floor. Its roof consists of leaves of a rare palm, Johannesteijsmania altifrons, from a genus unique to Southeast Asia. The second shelter was constructed by members of a tribe in India, the Warli, who live in

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Figure 13.2 Leafy protection in the great apes. Left, transplanting rice with umbrellas of banana leaf and bamboo strips, Maharashtra, India. Right, Guinean chimpanzee nest (courtesy of Kathelijne Koops).

Figure 13.3 Two leafy houses. Left, family and small Temuan hut in Ulu Kenaboi, West Malaysia, 1975. Right, Warli house in the village of Gayagota, India, 1989.

semi-forested areas of the state of Maharashtra, northeast of Mumbai. This Gayagota house (fig. 13.3) was built on a raised earthen platform and has walls built of a wattle (karvi) covered with a plaster of cow dung and clay. The roof consisted of the thatching of various palm leaves and grasses, and even rice crop residues on the surface, but the real waterproof covering underneath was the tough and durable leaves of the teak tree. The Gayagota villagers valued these trees, for the timber and roofing material. Thus, leaves have long provided shelter for us, and these stories are a good introduction to the wider subject of leaves as homes to a great diver-

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sity of organisms. Frequently the leaf dwellers offer services of benefit to the leaves and plants, and they receive benefits. So we often refer to the relationships as mutualistic.

Leaf Roosts and Nests Different plant parts, and especially twigs and leaves, are materials for the construction of nests by birds and rodents, and sometimes the materials are put into quite sophisticated structures, such as those by the weaving birds. Here, I focus on the construction of roosts and nests where leaves are the primary material. Although we mostly think of bats as nocturnal creatures that roost in dark caves during the day, some bats roost in cavities in tree trunks, in bark furrows, and are protected underneath leaves. The large “flying foxes” of the Asian tropics roost in tree crowns surrounded by foliage, but eventually may remove much of the latter from their roosting activity (fig. 13.4). Individual leaves provide several benefits to the small fruit-consuming bats that live underneath them: protection from rain and sunlight, concealment from predators, and a view of predators from below or above. Furthermore, the swaying and vibration of the leaf roost give a non-visual warning of predators. Bats modify leaves to make them suitable roosting spaces. They may curl leaves to provide a hollow vertical roost. They may join

Figure 13.4 Leafy bat roosts. Left, a giant flying fox roosting in an Asian palm. Center, Honduran white fruit bats roosting under a cut heliconia leaf in Costa Rica. Right, a Spix’s disk-winged bat roosting in a coiled heliconia leaf in Costa Rica.

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several leaves together to produce an umbrella. Mostly, they clip veins of suitable leaves, causing lobes to hang down and provide more concealment and better protection against rain and sunlight. The poster child for such roosts is the Honduran white bat, one to six individuals of which roost under specially clipped Heliconia leaves, abundant in the rainforests of Central America (fig. 13.4). I like it that the Honduran white bat is a member of a taxonomic group known as the leaf- nosed bats (or Phyllostomidae). A Central American neighbor, Stix’s disc-winged bat, lives in rolled-up leaves of Heliconia, using suction disks to stick to the sides. Its special roost amplifies sounds, improving the bat’s ability to detect predators. Most notable among the insects that make nests in foliage are the weaver ants of the Old World tropics. One species is native to tropical Africa, and another widespread species lives in Southeast Asia and Australia. Weaver ants establish complex colonies with dozens of nests on different trees, up to a half million or so individuals. Each colony has a nest with one or more egg-laying queen, and the eggs are transported to different nests. The eggs develop into small workers living entirely within nests, and large workers that defend the nests from the outside, attacking and consuming insect prey. Both workers also take honeydew from sapsucking insects. The large workers have special pads on their legs that allow them to adhere to other workers, forming chains and helping them adhere to leaves. When the leaves are pulled together, the workers hold larvae, which produce a silk filament that cements the leaves in place (fig. 13.5). An

Figure 13.5 Weaver ants, Tasik Bera, West Malaysia. Left, ant nest; right, detail of ants defending the nest, with large soldiers and small workers easily seen.

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attack on a nest, like a stick poked by a curious observer (me), provokes a swarm of stinging ants, and the venom also attracts even more ants. Weaver ants dramatically reduce the population of insects feeding on trees. Subsequently, they are beneficial to the growth of a variety of tropical tree crops, such as cashews.

Tanks In many tropical epiphytes, leaves form watertight rosettes that allow water to accumulate. Most notable are the tank bromeliads of the forests of the American tropics (fig. 13.6), although other plants, such as the bird’s-nest ferns, grow similarly in the Asian tropics. The tank bromeliads have been intensively studied, and the water forms a habitat in which a variety of organisms, including frogs, live. These unique ecosystems are collectively named “phytotelmata” (from the Greek phyton = plant and telm = pond). The nutrient and energy source for these little communities is the litter fall of leaves and other materials that collect in the tanks. This provides a source of food that supports the animal communities, which can consist of

Figure 13.6 Leaves as phytotelmata, providing aqueous habitats for animals; neotropical tank bromeliad with flowers poking through the water.

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up to a total of about twenty species in a tank: protozoans (particularly Paramecium), many different insects (especially mosquito larvae), crustaceans, spiders, worms, frog tadpoles, and occasionally mollusks. These organisms arrive in a variety of ways; mosquitoes lay eggs in the tanks, and adult frogs deposit the young tadpoles in them. The communities alter the composition of nutrients in the tank water. The host plants have specialized scales that allow them to assimilate phosphorus and nitrogen from the tanks, more than is absorbed by the roots (p. 188). The total amount of biomass in these tanks may approach half that of the canopy in some forests. Some bromeliads live as epiphytes in ant gardens. These are sites on branches where ants have established colonies, which have partially decomposed into a nutrient-rich litter on which the bromeliads grow. The ants even recruit seeds of these plants (whose seeds have a nutritious covering on the outside), and they develop in the ant gardens. The difference between a tank that absorbs nutrients from the community of organisms living in it and a carnivorous plant is rather small. If the tank has specialized structures, especially a narrow opening and slippery walls that prevent the prey from escaping, the prey will die and the nutrients can be transferred to the plant. Add specialized glands that secrete digestive enzymes, and the transformation is complete. In the bromeliad family, on the high plateaus of southern Venezuela, such a plant has evolved: Brocchinia reducta. Its narrow tanks, made from rosettes of leaves, produce waxes near their tips that prevent insects from escaping. The leaves emit a pleasant odor that attracts ants and flying insects. The water- absorbing scales are modified to absorb amino acids and proteins, but no digestive enzymes are secreted into the tank. A similar feeding mechanism is found in the southern Catopsis, native to south Florida and Central America. In the more widespread carnivorous trap species, such as the North American pitcher plant (fig. 9.14) and the Asian pitcher plants (or Nepenthes), the tanks are produced by individual leaves, with a lip at the tip to prevent rainwater from entering the trap. Special adaptations have evolved to make the walls slippery (p. 195); glands secreting digestive enzymes and the same structures absorbing nitrogen-containing compounds make carnivory possible.

Epiphylls Leaf surfaces provide opportunities for other organisms to colonize. Although a generally hostile environment, these surfaces attract many microorganisms, particularly bacteria; some are beneficial and some are harmful.

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Figure 13.7 Epiphylls. Left, an old palm frond in the understory of a rainforest in French Guyana is covered with liverworts, lichens, and algae. Right, lichens cover the leaf scales of a western red cedar in evergreen forests near Lynwood, WA.

Bryophytes (especially liverworts) and lichens are also important, particularly because of their capacity to take up nitrogen (fig. 13.7; p. 28). Epiphylls are particularly abundant in forests of high and frequent rainfall, in locations with partial exposure to sunlight. As the leaves age, the epiphylls accumulate. They may cover so much of the leaf surface that they reduce the photosynthetic capacity of leaves and contribute to their aging and fall. Green algae and slime molds may also accumulate. In the New World tropics, leaves are often removed from trees by the ubiquitous leafcutting ants. These take the leaves to their underground nests, where they cultivate fungi. Apparently, the epiphylls are harmful to the fungal growth because these ants avoid cutting leaves with epiphylls on them. Although epiphylls grow on a variety of leaf surfaces, from smooth to rough, they are less abundant on long-lived leaves, perhaps because of their defensive chemical compounds. Epiphylls also occur in temperate rainforests, on leaves of evergreen trees.

Leaf Miners and Galls Organisms, almost exclusively insects, make homes within leaves by feeding on the inside tissue. They therefore avoid exposure to many potential predators on the surface. Leaf-mining insects are conspicuous in leaves because in consuming a trail of nutritious green tissue, they leave a clear and light- colored trace. Well-preserved fossil leaves provide evidence of such mining activity for

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Figure 13.8 Insects living in leaves. Left, the citrus leaf miner burrowing just under the leaf surface is the larva of a moth. Right, the silk spangle gall, found on many oak leaves, is caused by the larva of a wasp.

at least 300 million years. The pattern produced by their trail of excavation is often distinctive for the particular miner. All leaf miners are larvae that germinate from eggs deposited by female insects, and the insects that mine leaves are most common among beetles and butterflies, and to a lesser extent flies and sawflies. A careful inspection of leaves in just about any setting— garden, field, or forest— will reveal the telltale trail of mining insects (fig. 13.8). Although easy to find, such miners are generally not very harmful to the host plants, and their trails generally remove only a small percentage of leaf tissue. Various factors influence the egg-laying of these insects. Often they are repelled by trichomes and/or by the chemistry of the leaf (but also may be attracted by that chemistry). The presence of an existing trail network may suppress the egg-laying activity, and the silver variegation patterns on leaves may also fool the insect into flying to another leaf (p. 228). Often, only a single leaf miner works a leaf, although large leaves may attract more than one miner, separated by a major leaf vein. Although the larvae are relatively well-protected, they are susceptible to tiny parasitoid wasps, which lay eggs that can burrow into the mining larvae and eventually kill them. In the evolutionary play of life, some miners have evolved trail-making strategies to confuse potential predators, such as creating trails around the edge of a leaf or producing a highly branched network of trails. Other insects lay eggs on leaves, and the larvae move inside of the tissue and produce galls. These larvae produce growth-regulating molecules that mimic the activity of those produced by plants, or they provoke the host

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plant to make them. These molecules induce the division of cells and their later differentiation into thick structures of varying shapes. Galls are particularly formed by midges and wasps, but also by aphids, mites, and even occasionally by fungi and bacteria. Galls are often seen on the leaves and twigs of oaks (fig. 13.8) and are also produced in a variety of plants. Fossil evidence for the production of galls goes back some 300 million years. The tissue produced by the leaf is consumed by the larva, which develops inside of the gall. Eventually an adult insect emerges from the gall, to fly, find a mate, reproduce, and continue the cycle. The larva makes a trail inside of the gall, rather than across the surface of the leaf. In large galls, several larvae may complete their development. Interestingly, some leaf miners produce a growth- regulating molecule, kinetin, which keeps leaf tissues green in an otherwise senescing leaf. This provides an opportunity for a leaf miner to complete its life cycle late in the growing season of temperate forests. As with miners, galls are not generally harmful to the host plants, and some have economic value, such as those used in producing dyes. Quite a variety of gall forms are produced in plants, even among groups such as the oaks. Just like miners, the insects that produce galls also are attacked by natural predators. Perhaps the shapes of the galls have evolved to avoid such attacks; spines or hard surfaces could be viewed as such defenses (or even nectaries produced to attract ants, p. 247).

Domatia Plants with domatia complete the story of leaves as houses; the word comes from its Greek equivalent, domatium, meaning small house or bedroom. Domatia are small chambers that have evolved as refuges for ants and mites. The dramatically different sizes of these two organisms have led to the evolution of domatia of very different sizes, from less than a millimeter in length to several centimeters in length in a few cases. Although domatia may occur in stems, they are particularly common in leaves. Mite domatia are very common in plants. Mites are tiny spider relatives, less than a millimeter in length and commonly about the thickness of a fingernail. Consequently, the domatia are very small, often produced at an angle between two veins, and often associated with tufts of hairs (fig. 13.9). To a mite, the surface of a leaf is a vast territory. Any examination of a leaf with a strong pocket lens will reveal mites traveling across the leaf surface; hairs and raised cells would appear much as a forest of tree trunks on hills

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Figure 13.9 Mite domatia on leaves. Top left and center, avocado, in angles of veins. Top right, pocket on undersurface in coastal Coprosma. Bottom left and right, auricles of leaflet bases in Brazilian pepper. (All photos except avocado courtesy of Robert Pemberton.)

for a mite in this miniature landscape. Mites can be seen as functioning in different guilds: herbivores (consuming the leaf material), carnivores (consuming insects and other mites), and specialists consuming fungal spores. We do not know very much about the interactions among these different organisms. However, if the domatia are closed up experimentally, such leaves generally suffer more from herbivory. The fungal spores might otherwise germinate and ultimately penetrate the cuticle and enter into the interior of the leaf. Hairy leaves may also be important in promoting mites while repelling many of the insect herbivores. Some mites, such as the spider mites, are extremely damaging to plants, yet smaller mites may help to control the spider mites. In some plants, including avocado and camphor trees, different-sized domatia can house different- sized mites. In camphor, there are four different-sized domatia. These domatia are generally found on different parts of the leaf undersurface and are associated with different mite families of herbivores, predators, and spore eaters. Sachiko Nishida

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of the University of Nagoya and other Japanese colleagues believe the different-sized domatia support a complex interaction among the mites, optimizing the removal of herbivorous species by predatory ones, supporting the activity of those removing the fungal spores to reduced damage by disease, and providing for the survival of a few herbivorous species as food to maintain the predatory species. We know little about such widespread and potentially useful phenomena, because the organisms are tiny. Leaf domatia that house ants are less common, principally found in the tropics, and yet have attracted the attention of biologists who see them as systems for testing hypotheses about evolution and ecological interactions. Ants often defend leaves against damage by insect pests. In exchange, plants provide nectar and food, as bodies rich in carbohydrates, fats, and proteins (p. 247). Additionally, plants may produce homes, such as the hollow thorns in the bull thorn acacia and the hollow stems in Barteria. In leaf development, hollow living spaces within the blade or petiole may establish as domatia for insects. A number of air plants also produce swollen leaf bases that may be inhabited by ants. Some 110 ant species inhabit the domatia of about ten times as many plant species. With the ant colonies established inside of the leaf, the interactions are even more involved and sophisticated because this close proximity makes possible the exchange of materials produced by the two partners. Dischidia grows in the Old World tropics, members of the milkweed family (now in the Apocynaceae). There are some eighty species, ranging from Southeast Asia into the eastern Pacific, and varying in the shapes and structures of their leaves. Some species produce flat and round leaves, others have dome- shaped leaves, and still others have hollow and rather cylindrical leaves (fig. 13.10). Ants have long been associated with species producing the latter two leaf types. Although we do not yet have an understanding of evolution within the genus, the general speculation has been that the flat-leaved species evolved into the dome-shaped leaved species, and such species evolved into the cylindrical species by the strong curving of leaf edges to produce a hollow interior. One such species with domeshaped leaves, D. astephana, has been studied in the mountain forests of West Malaysia. It often grows on a common tree of high mountain slopes, gelam bukit. Ants are easily observed under the leaves of the vine, and disturbing the plants brings them out in droves. However, the ant-Dischidia partnership is complicated by the ant’s interaction with the tree. The ants remove other epiphytes from the tree, other than Dischidia. The stems of the tree are partly hollow and provide spaces for the colonies of the ants to thrive.

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Figure 13.10 Ant plants of the genus Dischidia, in West Malaysia. Left, cupped leaves of D. nummularifolia with ants. Center, D. major growing on tree (courtesy of Kathleen Treseder). Right, hollow leaves of D. major, showing penetration of roots into leaf cavity, but no ants (courtesy of Francis Hallé).

The roots of the Dischidia plant penetrate into the tree stems and are found adjacent to the ant colonies. Apparently, the roots of the Dischidia vine obtain nutrients from the organic material adjacent to the ant colonies. The ants collect the Dischidia seeds and transport them to their colonies. There they germinate and grow to the surface. These habitats, at high altitude and with acidic and very poor soils, are homes of several other ant plants, and this relationship is a means of providing plants with supplies of critical nutrients, particularly nitrogen and phosphorus. For instance, ant plants of a fern and a member of the coffee family grow nearby. The undersurface of the conical leaves forms a domatium where the ants spend their time when on the surface of the tree. In the hollow- leaved species, the ant interacts directly with the vine and not with the tree. Dischidia major, a widespread species in Southeast Asia, produces both flat disc-shaped and hollow cylindrical leaves. The hollow leaf interiors are the sites of the colonies of ants of the genus Philidris. The ants consume insects they encounter on the vine and adjacent trees, and those insect parts and their own dead contribute to the detritus around the colonies. Access to the colony is via an opening at the base of the hollow leaves, and the plants extend their roots into the hollow cavities (fig. 13.10).

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Evidence for the exchange of materials between ants and plants has been estimated using the stable isotope techniques (p. 54). Kathleen Treseder and her colleagues determined that plants obtain about 39% of their carbon as CO2 from respiration in the ant colonies of the domatia. In addition, the plants obtain about 29% of their nitrogen from the ant colonies. Leaves with swollen sacs at their base are frequently encountered in understory shrubs of rainforests in the American tropics. Such species are common in the family Melastomataceae, and particularly in one genus of shrubs and small trees: Tococa (fig. 13.11). The association between the plants and ants in these domatia has long been noted, and it has been the object of much more research during the last couple of decades, particularly by Fabian Michelangeli, of the New York Botanical Garden, In Tococa, domatia are produced at the base of developing leaves. At least thirty species in the genus produce the domatia. Various ant species, including those in Azteca and Pheidole, establish colonies in the domatia. As feces and debris accumulate, ants generally raise their broods in the youngest domatia. The domatia produce specialized hairs that are a source of food for the ants. The ants effectively defend the plants against herbivores, including the leaf-cutting ant (p. 266). When ants are removed from the shrubs, the rate of leaf loss from herbivory increases substantially. In some cases, ants remove other plants from the forest, leaving only the Tococa shrubs; they may accomplish this by biting off leaves and spraying a toxin onto the leaves.

Figure 13.11 Ant domatia in the genus Tococa, a shrub native to tropical rainforests in the neotropics. Left and center, swollen petioles as ant domatia in T. guianensis. Right, ants nesting within a domatium seen when cut open (courtesy of Fabian Michelangeli).

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Domatia and ant-plant interactions are particularly prominent in some forests. In addition to tropical rainforests, domatia are common among pioneer trees in the tropics, in snakewood (Cecropia sp.) in the Americas, and in Macaranga in the Old World tropics. In the latter, attack by herbivores increases the recruitment of ants to the trees. In the snakewood, up to 93% of the tree’s nitrogen is obtained from its ant partner. The study of these insect- plant partnerships occasionally leads to totally unanticipated discoveries, and this is part of its attraction to biologists, particularly those working in the tropics. Not so long ago, our sole example of ants cultivating fungi was the leaf- cutting attine ants of the American tropics. These ants cut up leaves from the crowns of forest trees and transport them back to their underground nests, where they cultivate fungi as a source of food. In Amazonian rainforests, a small tree, Hirtella physophora, produces domatia that are inhabited by the ant species Allomerus decemarticulatus. It is a small species and unable, except in large numbers, to capture larger prey. However, in this species a remarkable strategy has been selected. The ants collect hairs on the stems near the domatia, and they cement them together to form an aerial platform that sits above the stem. The structure is strengthened by the ants’ cultivation of a fungus in the domatia. In the absence of the ants and the fungus, the structure collapses. The ants hide underneath the trap in special holes, mandibles open. When a large insect arrives, they collectively grab it in different parts with their mandibles, stretch the insect on the platform, and then cut it up and consume it (fig. 13.12). In the African tropics, and probably elsewhere, ants cultivate fungi in the domatia of leaves of forest trees. The “food” for the fungi consists of dead ant parts, ant poop, and the parts of other insect prey. It is puzzling why ants go to such trouble, but perhaps the fungal gardens assist in the efficient cycling of nutrients between ants and the host trees. Rather than a simple partnership between an ant and a plant, we need to add the fungi as an additional participant. Vincent Bazile and colleagues in Montpellier, France, have revealed the symbiosis between an Asian pitcher plant and a symbiont ant. The ant inhabits a domatium from a modified tendril, receives nectar secreted by the plant, and consumes some food items from the pitcher, employing a specialized swimming activity. The plant grows faster and produces more pitchers when inhabited by the ant, partly from the feces and dead prey (nitrogen sources) deposited in the traps. The ants keep the lip of the pitcher clean, thus enhancing the efficiency of prey capture. In a related pitcher plant, the lip and orifice

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Figure 13.12 An insect trapping mechanism involving a neotropical understory tree, Hirtella physophora, and its ant partner, Allomerus decemarticulatus. The plant provides domatia, but the small ants also build passageways (left) and a trapping platform outside (right), partly out of the hairs that cover the domatia (courtesy of Alain Dejean and Jérôme Orivel).

help bats echolocate and roost in the pitchers, thereby adding feces and nitrogen to the plant. Quite a few biologists study the symbiotic relationships between plants and animals, and a good number focus on insects living on, or in, leaves. Perhaps there is something particularly attractive about studying such detailed, seemingly trivial, phenomena and finding that their effects may be large. The presence of an insect may mean the survival or death of a plant in an ecosystem, which could change the function of that ecosystem as a whole. Such interactions approach the so-called “butterfly effect,” where a trivial movement such as the waving of butterfly wings could allegedly affect large-scale weather patterns. I am reminded of the ascent of Mount Analogue, as written by the French poet and philosopher René Daumal. The book (and my quote) ends midstream, since he was writing the book the very day of his death from tuberculosis in 1944. In his story, a guide in the ascent of this mythical mountain, faced with starvation during bad weather, killed and consumed an old rock rat. Later he was disciplined by a tribunal of guides and prohibited from ascending the mountain for three years, with the requirement that he repair any damage. He finally was able to ascend the mountain once more and brought another rock rat to repair the damage. When arriving at the site, he encountered the collapse of a side of the mountain, with avalanches and rockslides that obliterated a large section of the trail (causing

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the deaths of several climbers). The Council analyzed the event and informed him about the effects of killing the rock rat: The old rat I had killed fed principally on a species of wasp common on that spot. But beyond a certain age a rock rat is no longer agile enough to catch wasps on the wing. Therefore, he lived for the most part on the sick and weak insects which dragged themselves on the ground and could barely fly. In this way he destroyed the wasps that were malformed or carriers of disease. His unsuspecting intervention protected the colonies of these insects from the dangerous afflictions spread by heredity or contagion. Once the rat was dead, these afflictions spread rapidly, and by the following spring there was scarcely a wasp left in the region. These wasps, visiting flowers in search of nectar, also fertilized them. Without the wasps, a large number of plants which play an important part in holding the terrain in place . . .

Chapter Fourteen Movements But none ever trembled and panted with bliss In the garden, the field, or the wilderness, Like a doe in the noon-tide with love’s sweet want, As the companionless Sensitive Plant. percy bysshe shelley, “The Sensitive Plant”

soft lipped pitchers pouring in, not out, and florid staffs, erect and veined as flesh, that rise above the spread of flytraps’ fringe and flange to guard those gaping gates that once one enters none may emerge, but only deep and deeper delve into that secret, sweet, and drunken death. christina lovin, “In the Garden of Carnivorous Plants”

I

n southwest China in 2005, on the search for iridescent blue leaves (p. 198), I visited the Xishuangbanna Tropical Botanical Garden in southern Yunnan, where China dips into the tropics. The garden is a very popular destination for tourists from the more populous north, the Chinese equivalent to the Caribbean or Costa Rica, or even south Florida. Hundreds of busloads of tourists arrive each day for an experience of the tropics. It is an impressive garden and also important for research. Tourists are attracted by the symbols of the tropics— bananas, necklaces and bracelets made of tropical seeds— and by the opportunities for photography. The garden’s most · 269 ·

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Figure 14.1 Semaphore plant at Xishuangbanna Tropical Botanical Garden, in southern Yunnan, China.

photogenic destination is the semaphore or dancing plant, a small legume shrub native to tropical Asia (fig. 14.1). Tourists believe that if they dance in front of the plant, it will move its leaves in rhythm. In fact, the plant does move its leaves in a very unconventional way. Its leaves are composed of three leaflets; the two basal ones are much smaller than the larger one at the tip. The two basal leaves move slowly and steadily in a sweeping motion (like a semaphore sailor on a navy ship), and the larger tip leaf moves even more slowly, up during the day and down at night. Run a Google search on “semaphore,” “telegraph,” or “dancing” plant, and you are certain to find links to articles and videos about this plant. These are often Chinese videos, some probably taken at XTBG. I hadn’t heard of the semaphore plant before my visit to the garden, although I knew of other plants capable of rapid movement. Charles Darwin grew the semaphore plant in his hothouse, and he devoted a chapter to its “behavior” in the book The Power of Movement in Plants, written with his son Francis and published in 1880. We are fascinated by such plants with moving leaves, because they remind us of ourselves. Plants are sessile creatures. Lack of motion is a basic

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characteristic, and it sets plants apart as fundamentally different from animals. From the Greeks on, a basic scale of nature had been devised, revealing the sophistication of organisms and culminating in humans. Traditionally, plants were placed near the base of this scale. However, the revelation that a plant could display such an animal-like behavior called for the radical revision of the scale of nature; it was a challenge to the orthodox Roman Catholic Church (which made that scale part of its theology) and was a shock to educated Europeans’ understanding. In fact, there were examples of leaf movements in European plants that were known to herbalists, both the sleep movements of legumes as well as the tentacle movements of the sundew plants. Such movements were not studied by natural philosophers (scientists); perhaps their sensitivity was dulled by their belief in the scale of nature. However, two plants with dramatic leaf movements were introduced to Europe and excited the controversy: the sensitive plant and the Venus flytrap. The sensitive plant was the first to be studied. It was brought to Europe in the sixteenth century from the American tropics and was easily grown in the hothouses of European royalty and wealthy merchants. In 1661 King Charles II was so stricken by the movements of a sensitive plant in his own garden that he charged the Royal Society to sponsor research to find the mechanism. They commissioned a committee to study the plants, and their report was summarized in Robert Hooke’s Micrographia in 1665 (fig. 14.2).

Figure 14.2 Early research in plant movements. Left, a branch of a sensitive plant from Robert Hooke’s Micrographia (1665). Center, Charles Bonnet, 1779. Right, one of Bonnet’s experiments on irritability.

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The plant was further studied by other noted scientists and became the touchstone for the “irritability” movement in Europe during the seventeenth and eighteenth centuries. A key figure in this research was Charles Bonnet (1720–1793; p. 48; fig. 14.2), who studied leaf and shoot responses to environmental stimuli and was the first to describe visual hallucinations, using his elderly grandfather as a case study. Much later, and more dramatic, was the introduction of the Venus flytrap to Europe in 1768 (fig.14.10). This plant had been discovered by Arthur Dobbs, governor of North Carolina, in 1759, in areas near Wilmington. The Philadelphia naturalist William Bartram visited Dobbs in 1762 and brought back plants to his father, John Bartram, who added to the descriptions. Living plants were collected and brought to London in 1768 by the Philadelphia nurseryman William Young. The Venus flytrap had a huge impact in Europe, both culturally and scientifically. It was the inspiration for writers of Gothic and Victorian fiction, and continued in the twentieth century in the fanciful reports of man-eating trees from various tropical countries. In the fiction of J. R. R. Tolkien, the Old Man Willow of the Fangorn Forest of Middle-earth threatened Frodo and his companions. In J. K. Rowling’s Harry Potter and the Half-Blood Prince, the dangerous carnivorous plant Snargaluff disguised itself as a dead tree trunk and shot out thorny vines to catch its prey. Some carnivorous plants had human names, such as Cleopatra in The Addams Family TV series and Audrey in The Little Shop of Horrors. Annie Proulx, known for her fiction about the American West, published a short story about a carnivorous shrub, the “Sagebrush Kid.” From frontier days to gas and oil exploitation, the plant ate cowboys, rustlers, cooks, roustabouts, and a botanist. Being a botanist and coming from the sagebrush steppe, I was attracted to her story. As he [the botanist] came closer he saw that the ground around it was clear of other plants. He had only a six-foot folding rule in his backpack, and as he held it up against the huge plant it extended less than half its height. He marked the six- foot level with his eye. He had to move in close to get the next measurement. “I’m guessing thirteen feet,” he said to the folding rule, placing one hand on a muscular and strangely warm branch.

Research on moving plants originated just after their introduction in Europe and expanded with the discovery of other moving leaves (such as those of the telegraph plant), sleeping and sun-tracking leaves, and more

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carnivorous plants. Charles Darwin is most famous as the co-discoverer of natural selection, but also widely respected for his research on moving and carnivorous plants (fig. 14.3). He was quite modest about his botanical knowledge, perhaps comparing it to the vast expertise of his close friend Joseph Hooker; but his books on various aspects of plant biology cemented his reputation as one of the great botanists of the nineteenth century. Three of these books dealt with the movement of plants and leaves: The Movements and Habits of Climbing Plants (1865), Insectivorous Plants (1875, and revised by his son Francis in 1888; fig. 14.3), and The Power of Movement in Plants (with Francis, 1880). What Darwin showed is that movement is part of the rapid growth of all plants, and that it is the timescale that makes us consider plants as motionless. I’ll limit myself to discussing such movements on the order of a day or less, and even down to a few milliseconds. The field of research is full of eccentric scientists doing what often seems as oddball research— but quite brilliant as well (notable is the research of Roger Hangartner and his students at Indiana University)— and much useful work done by amateurs, organized by energetic local to international organizations promoting their study and popularization. In this field the most basic research has a tendency to become twisted into the most tantalizing half- truths, particularly for carnivorous plants. For instance, a giant pitcher plant with among the largest leaf traps was discovered in the Philippines, and one of the researchers mentioned to the press that it might be big enough to trap a rodent— that comment soon spread

Figure 14.3 Later students of plant movements. Left, Charles Darwin (in 1878); center, Charles Darwin’s son, Francis (in 1910); right, Darwin’s young colleague John BurdenSanderson (in 1870).

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on the Internet as the discovery of a rat-catching plant! Previous research on even larger pitcher plants on Mount Kinabalu (in Borneo) revealed that the traps attracted small rodents and bats (p. 194) who left their feces in the traps. Then there was the publication on the “visco-elastic” properties of the fluid of another pitcher plant, which was translated as the “toxic saliva” of the plant (p. 195).

Electrical Signals In the nervous systems of animals, nerve cells (neurons) are connected to each other by synapses, from the cell extensions, axons (where signals depart), and more numerous dendrites (where signals arrive). The “firing” of the neuron involves the depolarization of the cell membrane, which allows the rapid movement of ions through special channels, termed an action potential. This change in charge is propagated rapidly down the length of the cell, and subsequent cells are excited, to complete a neural circuit. An astonishing fact about action potentials and electrical signals is that they were discovered in plants at about the same time they were discovered in animals, in the Venus flytrap in particular. Charles Darwin had corresponded with an English physician physiologist, John Burdon-Sanderson (fig. 14.3), who detected such a signal when the trap was triggered and determined its rate of propagation (at 20 cm/second, slow compared to nerve conduction in animals of around 100 m/second) as early as 1873. This was controversial work that assaulted traditional views about life as embodied by the great chain of being, and as the tree of life in evolutionary terms. Burdon-Sanderson received a Royal Society Medal for this work, as well as his research on the relationship of microorganisms to disease, in 1882. Much later, action potentials were discovered in relationship to the moving leaves of the sensitive plant, of the sundew, and in a great variety of plants without such leaf movements. Action potentials were first measured by clamping electrodes to the exterior of organs, plant or animal, much in the way that we perform an electroencephalogram (EEG). An early pioneer in this research on plants was the remarkable Indian scientist Jagadish Chandra Bose (fig. 14.4). Later, techniques were devised to place micro-electrodes into tissues and cells, but these techniques were difficult in plants because of the presence of cell walls. However, an ingenious technique was developed for plants, taking advantage of the feeding activities of aphids. These tiny insects, the bane of gardeners, suck the sap of plants by injecting their stylids (feeding

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Figure 14.4 The landmark studies on electrical signals in plants conducted by Jagadish Chandra Bose. Left, Bose in the laboratory, 1925. Right, an experimental protocol for measuring the velocity of electrical impulses in the sensitive plant.

tubes) into the organ and directly into the phloem tissue. Plant electrophysiologists figured out how to isolate the feeding stylids from the insect (by zapping it with a laser) and connecting the stylid droplet to the voltage measuring instrument (fig. 14.5). The plant cell wall also isolates adjacent cells and prevents the conduction of the electrical signal. However, plants provide the needed connections in two ways. First, cells that are formed at the same time can produce intercellular connections of the cytoplasm with special bridges of fluid, the plasmodesmata. More importantly, the functional cells of the phloem (pp. 28, 214), the sieve tube elements, are connected by cytoplasm for their entire lengths (often of many meters) due to the special connections between cell elements of the tube. This provides a means for long- distance electrical signaling. We now know that electrical signaling is widespread in plants, and that it has other similarities to animals. Signaling in animals is regulated and

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Figure 14.5 Left, oleander aphid, feeding with stylet (arrow) (courtesy of Lisa Sells). Center, diagram of feeding stylet and an electrical penetration graph. Right, section of the pulvinus of a sensitive plant, showing the large outer cells capable of rapid change in inflation.

enhanced by neurohormones (such as L-dopa, glutamate, serotonin, and GABA). Psychotropic drugs, now valuable in treating depression and psychosis, work by modifying the influence of neurohormones. In nerve cells, these molecules regulate ion channels that allow the rapid change of voltage. In Arabidopsis, glutamate receptor genes are involved in the electrical signal produced by wounded leaves that spread throughout the plant. This suggests a similar function of glutamate as a signal regulator in animals and plants. GABA (gamma-aminobutyric acid) affects cortical activity in the brain. Think of Neurontin (a fat-soluble form of GABA, gabapentin) as a pain suppressant. GABA is an important developmental signal in plants, as well. Thus, there are quite a few similarities between electrical signal production in plants and animals.

Leaf Movements As the Chinese tourists could see in the semaphore plant at XTBG (p. 269), its leaves move in two ways. The large terminal leaflet moves to an upright position during the day, and then moves to a downward position at night, in a daily rhythm. The smaller leaves at the base move continually in a circular motion, completing their circuit in about four minutes, affected by temperature. Both movements, slow and rapid, require an effector, or motor. In leaves, this motor is a swollen structure at the base of the leaf or leaflet, the pulvinus (fig. 14.5). The pulvinus contains thin-walled cells underneath

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the surface that can rapidly move ions, especially potassium and calcium, across the cell membrane. A loss of these ions is accompanied by a rapid movement of water into the cells and an increase of cell pressure. A gain of these ions causes the reverse, and a loss of cell pressure. Gain of pressure on one side and loss of pressure on the other side can change the leaf position slowly or very rapidly, in less than a second. Most leaves move up and down, when opposite sides of the pulvinus deflate and inflate. However, the small leaves of the semaphore plant rotate in a circle as the cells of the pulvinus change in a wave that rotates around the structure. Thus, in the overall process of leaf movement, a stimulus is aroused by the environment, touch, light, temperature, and damage. The organ that is sensitive to the stimulus can be the leaf blade or the pulvinus itself. The arousal produces an electrical signal that moves to adjacent pulvini, causing cells to lose or gain ions, and to lose and gain pressure— resulting in the movements. Daily leaf movements are actually quite common among plants, especially in members of the legume family. On my street in Miami, several ornamental trees produce such sleep movements every evening (fig. 14.6). Leaves of many plants track the sun as it moves across the sky during the day, including many important crop plants, such as soybean, beans, and cotton. Arctic and alpine plants often track the sun, increasing their exposures to sunlight— and their temperatures— in these extreme climates. In the tropics, under higher temperature and humidity, leaves of some plants may reduce their exposure to sunlight, by moving to a vertical position during the hottest times of the day, and they assume a flatter position morning and

Figure 14.6 Sleep movements in the lead tree, native to Central America. Left, compound leaves at 3 pm in the afternoon; center, the same leaves at 7:30 pm; right, close-up view of pulvinus at base of leaflet.

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afternoon. The angle of the leaf is its most effective way to rapidly control the amount of radiation it receives. In addition to legumes, two other plant families contain species with such leaf movements. First is the prayer-plant family (Marantaceae), whose members produce a pulvinus in the middle of the petiole that can promote leaf movement during the day. Second is the sorrel family (Oxalidaceae). Sorrels are common as weeds in lawns and gardens, and they often fold their leaves at night. The most spectacular movements in the sorrel family are seen in the life plant. Its leaflets can rotate in a fashion similar to the semaphore plant, and they drop down at night. The most common daily leaf movements are the folding or “closing” of leaves at night— sleep movements. These movements were observed in tamarind trees by Androsthenes, one of Alexander’s ship captains, during their invasion of the Indian subcontinent, fourth century bce. Sleep movements have been the focus of quite a bit of research in the past century. The sleep rhythms of leaves are circadian (circa = about, and dies = day, in Latin), and the first circadian rhythms among organisms were documented in the sensitive plant in the eighteenth century. Circadian rhythms are approximately a day in length but need to be entrained by light to be maintained at 24 hours. Keep bean plants in continuous light, and their leaf positions change in a 27-hour cycle. Keep humans in uniform and carefully controlled light conditions, and they adopt a sleep- activity cycle of 24.18 hours. In plants the endogenous free- running condition is maintained by feedback loops in the genetic machinery of cells, and light detected by a red-sensitive pigment (phytochrome) and a blue- sensitive pigment (cryptochrome) adjusts the daily cycle to 24 hours. Shifts in gravity fields associated with the lunar cycle may also influence some leaf movements. What is the advantage of adopting such a position at night? There is little research and much speculation on this subject. Closed leaves may radiate less heat at night and thus maintain warmer temperatures. Charles Darwin was the first scientist to produce supporting evidence for this. Such a mechanism might be particularly valuable in climates where the temperatures dip to freezing. Just as plants can position their leaves during the day to control the energy balance, they may also do it at night. Closed leaves at night may be less susceptible to damage by insects. Maybe we need to think more creatively. With regard to the leaf movements of the semaphore plant, Simcha Lev-Yadun (p. 231) has suggested that the small leaf movements in the semaphore plant could mimic insect activity and could deter butterflies from laying eggs or even attract birds looking for insects.

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The rapid leaf movement of the sensitive plant has attracted the most curiosity and study over the centuries (fig. 14.7). In addition to the fast responses of this plant to touch, heat, electric shock, and physical damage, its leaves also “sleep” (or close up) at night. Furthermore, there are two mechanisms for the transmission of signals in this plant. The classical mechanism is that of touch. Touching a single leaflet with a hair induces it and neighboring leaflets to collapse. A more vigorous disturbance may affect adjacent leaves as well. In these cases, an electrical signal is generated that affects the nearby pulvinus, causing cells on opposite sides to lose or gain ions (especially calcium, potassium, and chloride). This process requires energy, in the form of ATP, and the actual change in pressure is due to the rapid movement of water through special passages in the cell membranes, the aquaporins. This is a very rapid response, occurring in a fraction of a second. The leaves eventually return to their original position after ten minutes or so, and are ready for a second stimulation. A second response is slower and more variable, and the mechanism for it is still under debate. If a leaflet is damaged (burned, cut, or chewed by an insect), a slower signal is transmitted throughout the plant. The cells targeted by this signal, as in the rest of the leaves of the plant, produce jasmonic acid (p. 244), which in turn stimulates a cascade of defensive reactions, one of which is a protein that inhibits protein-digesting enzymes. Such a signal is by no means unique to sensitive plants, and it has been studied in tomatoes (p. 242) and Arabi-

Figure 14.7 Touch response of the sensitive plant. Left, untouched plant; right, touched plant, leaflets pressed together.

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dopsis. This signal has a pressure, as well as an electrical, component. In the sensitive plant, cut stems that were reconnected by tubes filled with water were able to pass the signal, suggesting that the electrical changes were a by-product and that the signal passed via the xylem tissue. Thus, the controls may not be by electrical circuits, more likely by hydraulic systems, like brakes or the clutch for a standard transmission in your car.

Movements to Trap Insects Leaf movements in a few plants help them trap insects, which they digest to obtain essential nutrients: carnivorous plants. They are restricted to locales with very low supplies of phosphorus and nitrogen in the soil or water, and they can compete successfully with other plants by obtaining these elements from the insects they trap. These nutrient- poor sites include acid bogs and the acid peat soils on tropical mountains. Most carnivorous plants are in two genera, Drosera (the sundews) and Utricularia (the bladderworts). Bladderworts are aquatic plants, and they produce suction traps that pull in small invertebrate animals that touch hairs and trigger the trap closing. It is not clear what the bladders are; they are not modified leaves, so I am leaving them out of this discussion, even though they are awesome plants and widely distributed on the planet (well over 200 species, by far the largest such group; fig. 14.8). The carnivorous plants with moving leafy traps are within a single family, the sundews. This family includes a genus, Drosera, with about 100 species worldwide; a single species of the Venus flytrap, native to bogs of the Carolina coast; and an aquatic species with traps similar to the Venus flytrap, the waterwheel plant (fig. 14.8). To get a better feel for the diversity of these plants, and the interesting community of growers and hobbyists who concentrate on them, I drove up the coast and visited Sunbelle Exotics, a carnivorous plant nursery in Boca Raton. Its proprietors, Michelle and Trent Meeks, have all sorts of such plants but really focus on the North American and Asian pitcher plants. They collect rare species and varieties, and make crosses to multiply the diversity of pitcher colors and shapes. Trent started out with orchids, which seems true for many growers of carnivorous plants, and then switched later. They meet locally with other growers in the area and are on guard for “rustlers” who steal rare plants and sell them to collectors. Charles Darwin studied all of the carnivorous plants in this family, but he focused on the trapping mechanisms of the sundews. Sundews produce

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Figure 14.8 Two aquatic trapping carnivorous plants. Top left, a bladderwort, common in the Everglades of south Florida; top right, bladderwort traps; bottom left, a waterwheel plant.

leaves in a variety of shapes, from almost round, to long filaments, and to branching filaments. These are pretty common plants in North America, if you know where to look for them— but you need to get down on your knees to see them, as most of them are pretty small. Sundew leaves produce hairs on their upper surface and edges (fig. 14.9). Each of these hairs terminates in a clump of cells that secretes a sweet and sticky mucilage. Small insects, such as mosquitoes and flies, are attracted to the rosette of leaves and get stuck on these hairs. The touch of these living— and nitrogen-containing— organisms triggers the turning of that hair toward the prey. Soon other hairs turn toward the insect, and ultimately the leaf edges turn toward the insect as well (fig. 14.9). Entangled in the mucilage, the insect dies, the hairs secrete digestive enzymes, and the insect’s body tissue is broken down. The same hairs then function to assimilate the nitrogen- and phosphorus-containing molecules into the

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Figure 14.9 Two sundew plants. Top left, round-leaved sundew; top right, detail of trapping leaf. Bottom, filamentous-leaved sundew: left, leaf; center, leaf detail with trapping hairs; right, detail of trapping hair.

plant. Once digested, the husk of the insect is blown from the leaf; the tentacles secrete a new drop of sticky mucilage; and the leaf trap is ready for another prey. This is a highly coordinated activity, and the plant uses electrical signals and other control devices to trap and digest its prey. One tentacle’s contact with an insect produces an action potential that moves down its length and affects neighboring tentacles. A cascade of tentacle movements ensnares the insect. Tentacle movements are probably caused by changes in cell pressure in these multicellular structures, but are not very well understood. These same tentacles, along with shorter ones, secrete digestive enzymes.

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The tentacles on the outer edge of the leaf may be capable of more rapid movements; those in an Australian species can catapult the insect into the sticky middle of the leaf. The leaf blade can also change curvature in response to insect trapping. However, these are slower movements (hours rather than minutes) and are mediated by the synthesis of growth regulators. Shape changes are produced by auxin, but jasmonic acid (the molecule associated with leaf defenses against herbivory, p. 244) is also involved. All of these carnivorous trapping plants have similar glandular hairs. The two active trapping plants, the Venus flytrap (fig. 14.10) and the waterwheel plant (fig. 14.8), produce specialized structures at the tips of photosynthetic leaves, consisting of two lobes that snap shut. These surround insects, partly through the meshing of long curved hairs on the edges of

Figure 14.10 Venus flytrap. Top left, whole plant; top right, trap with three trigger hairs visible. Bottom left, trigger hair detail; bottom right, digestive glands, from above surface.

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the lobes. Trigger hairs on the trap surfaces are stimulated by the insect to produce action potentials that activate the closing of the trap, usually three such hairs in the Venus flytrap (fig. 14.10) and twenty or so of them in the waterwheel plant. Two consecutive touches in the former plant produce an action potential that moves quickly throughout the leaf, causing its partial closure in less than a second. The trap can reopen in a few hours if triggered by a non-digestible object. Additional touches insure long-term trap closure, activate digestive enzymes from specialized glands, and even facilitate sodium collection from larger prey (fig. 14.10). After ten days or so, the insect is digested, the trap reopens, the insect husk blows away, and the trap is ready for business again. Despite decades of study by botanists, physicists, and engineers, the mechanism of trap closure is still under debate. It is certain that the action potential affects cell pressure in tissues, but those changes are likely to act only as a trigger for larger mechanical forces. Trap closure is associated with a change in its curvature and a release of mechanical energy. Such mechanisms, and even the stickiness of the mucilage, are of interest to engineers looking for nature as clues to new inventions (“bioinspiration,” p. 180). The movable leaf traps of the sundews, the Venus flytrap, and the waterwheel plant share the same family membership, the Droseraceae. The sundews are probably the plants from which the leaf trap mechanism evolved, splitting into these two genera. How did the sundew plant trap-

Figure 14.11 Lead plant, plumbago. Left, flower detail with sticky hairs on sepals at base of flowers; right, detailed view of sticky hairs.

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ping mechanism originate? A clue is in a related and ancestral family, the Plumbaginaceae, of which the Plumbago, or lead plant, is the best known member (fig. 14.11). The bases of the flowers of this plant have sticky hairs that look very much like those on sundew leaves. These hairs may trap insects and absorb nitrogen that can be used by the plants. Perhaps the hairs originated as a defensive barrier against insects attempting to steal nectar from the flowers and reduce their reproductive efficiency. Other plants, as geraniums and gooseberries, also have such hairs that may function in a similar manner. Leaf movement, an animal-like activity in a plant, has not only inspired writers and poets, but also scientists and engineers. Add hairs to those moving leaves, making them furry in appearance, and maybe a variegated leaf or flower looking like a face, and we would have a universally fascinating plant— more like us.

Chapter Fifteen Seeing Leaves For I have learned To look on nature, not as in the hour Of thoughtless youth; but hearing oftentimes The still sad music of humanity, Nor harsh nor grating, though of ample power To chasten and subdue.— And I have felt A presence that disturbs me with the joy Of elevated thoughts; a sense sublime Of something far more deeply interfused, Whose dwelling is the light of setting suns, And the round ocean and the living air, And the blue sky, and in the mind of man: A motion and a spirit, that impels All thinking things, all objects of all thought, And rolls through all things. william wordsworth, “Lines Written a Few Miles above

Tintern Abbey” The years to come— this is a promise— will grant you ample time to try the difficult steps in the empire of thought where you seek for the shining proofs you think you must have. But nothing you ever understand will be sweeter, or more binding, than this deepest affinity between your eyes and the world. mary oliver, “Terns”

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uring adolescence, I often backpacked in the Cascade Mountains of Washington State, particularly in the Alpine Lakes Wilderness. I remember a hike in 1960 up the Surprise Creek Trail to Trap Pass, at 5,800 feet, on the edge of the alpine. I walked off the trail in a northerly direction along the ridge to get a good view of Glacier Peak. The greens of the clumps of firs and the sphagnum bogs intensified: I became ecstatic in that expanse, and time stopped. My limited sense of self dissolved into the immensity of nature. Such experiences in nature changed my life. They inspired me to take up the study of plants and to venture to the tropics to study them. What about nature kindles these experiences, intense, luminous, spiritual in a broad sense, in so many people, particularly at a young age? This book, with its scientific and cultural perspectives, was inspired by those experiences. Fifty years after those youthful explorations, the world is a different place. Our connection to the natural world has changed dramatically since the times that cultures created green men, or later, when we were awestruck by the forms of nature in the tropics, explained to us by Humboldt. Without defining in detail the meanings of “nature” or “natural,” let me say that nature is that which is little influenced by modern (industrial) human culture. All life on the planet is now affected by humans, by toxins moving through food chains, greenhouse gases influencing global water chemistry and climate, by the loss of habitat for organisms, by the appropriation of resources that could support those organisms, and by collecting rare organisms to satisfy our avidity to possess them. We are in the midst of a collapse of biodiversity, similar to those extinctions that erased life in earlier epochs (p. 85). Nature, as we once knew it, has vanished. The economic and social forces responsible for these changes are extremely powerful, and it is difficult to be optimistic about changing the trajectory of climate change and biodiversity collapse. Most biologists, acutely aware of these problems, live in perpetual grief for this loss. I am not optimistic about our cultural penchant for technological fixes to these problems, worsened by the growth of the human population. My hope resides more in changes in human attitudes about nature, by expanding human awareness. Baba Dioum’s famous quote on environmental conservation (p. xii) works in two directions. In one direction, the conservation of nature comes through education and understanding, which engender love. In the other direction, we love nature first, and then are taught to understand it and to work intelligently to conserve it. The latter course is the way I think it works; we need emotionally driven commitments to

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change our behavior. It is thus useful to explore the sources of those emotional experiences. My motivation in writing this book was to increase our awareness of one aspect of the natural world, of leaves and foliage, of their beauty and potential to touch us.

The Benefits of Nature When our grandson Shaun was a little more than a year old, my wife, Carol, and I cared for him for a couple of years. This was an opportunity to introduce him to nature through visits to gardens in Miami, especially Fairchild Tropical Botanic Garden and Parrot Jungle (now Jungle Island) (fig. 15.1). Both were beautiful, with varied landscapes of lush foliage and profound leafy shade interrupted with sunny open areas. These were safe places, so I could let him run around with minimal worry about poisonous plants or snakes, or speeding cars. I told him little except to enjoy himself. I had learned quite a bit in the twenty years since my kids were the same age. In 1988 Florida International University (where I was a professor) had hosted a rainforest conference, with the Rainforest Action Network and a cast of environmental activists and Amazonian tribal chieftains. I learned about the deep ecology movement, with its extensive literature on our connections to nature and the early influences of nature on children.

Figure 15.1 Our grandson Shaun in gardens. Left, Shaun in a mango tree in our yard. Right, a sylvan setting at Parrot Jungle, in Miami, where he often wandered.

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Figure 15.2 Prison nature murals. Left, dining room mural at the state penitentiary McNeil Island, WA, painted by Clifford Vernon Vincent (photo by Mike Watkins). Right, a nature mural at the Central Florida Reception Center, part of the state corrections system near Orlando; painted by Al Black (photo by Gary Monroe).

Four years later, we experienced Hurricane Andrew and were forced out of our badly damaged house for months. We observed the emotional toll from the loss of trees and landscapes. That storm inspired me to teach a new course, “The Meaning of the Garden,” in which the garden became a metaphor for our relationship with nature. Through readings, student projects, and conversations with guest speakers, I learned more about the effects of natural settings on our well- being. I continue to learn about them: increased healing from natural window views in hospitals, less tension in prisons from nature-themed murals (fig. 15.2), less tension in office environments, less aggression among youth in inner cities, reduced ADHD symptoms in children from playing in green settings, and reduced dementia among Alzheimer’s patients with forest visits (something I personally experienced when I took a childhood friend to a Maryland state park a few years ago). I ask my colleagues in meetings, including some whose research is included in this book, what inspired them to take up scientific careers studying plants. Invariably, they share their experiences as children in nature, even in a small woodlot behind their home or a summer visit to a grandparent’s farm. Such experiences may start very early. At three years old, I remember sitting at the edge of our lawn, by a flower bed my mother was tending in the springtime, of the brilliant green spears of iris leaves and the vibrant hue of a western blue racer. The psychoanalyst Carl Jung’s first memory was also a strongly felt impression of nature:

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I am lying in a pram in the shadow of a tree. It is a fine warm summer day, the sky blue, and golden sunlight darting through green leaves. The hood of the pram has been left up. I have just awakened to the glorious beauty of the day, and have a sense of indescribable well- being. I see the sun glittering through the leaves and blossoms of the bushes. Everything is wholly wonderful, colorful, and splendid.

We struggle to experience nature, animals, plants, and leaves, in a more authentic fashion— against the conditioning of a conventional education, largely isolated from the natural world. This may be easier for children and traditional people living in nature unencumbered by the technology of modern culture. Paul Shepard, an evolutionary ecologist, wrote about his own childhood. Trees were made for climbing, a return to quadrupedal motion, touching a chord in our genetic memory of an arboreal safety. The rough texture of bark against the chest and arms, the smell reminiscent of a time so long ago that we still had whiskers, the gift of nests and fruit, the green galleries and corridors, the vestibular possibilities in being rocked by the wind or bouncing on a limb are part of my own childhood recollections that go deep.

Jane Goodall’s childhood nature experiences in England inspired her to travel to Africa and study the behavior of chimpanzees. Throughout my school days I spent many hours in the garden, often taking my homework into our little wooden summerhouse, or even up into the top of my favorite tree, Beech. I loved that tree— so much that I persuaded Danny to sign a piece of paper leaving it to me in her will! There high above the ground, I could feel part of the life of the tree, swaying when the wind blew strongly, close to the rustling of the leaves. The songs of the birds sounded different up there— clearer and louder. I could sometimes lay my cheek against the trunk and seem to feel the sap, the lifeblood of Beech, coursing below the rough bark.

Although during early childhood we may have a capacity for a deeper relationship than we are capable of as adults, such early memories may also affect our attitudes as adults toward the natural world. Richard Louv has

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Figure 15.3 The Tacoma rap artist C.A.U.T.I.O.N. worked with Nalini Nadkarni at Evergreen State College in Olympia, WA; here he is interacting with students after descending from a tree.

summarized much of this childhood fascination with nature, and the problems when children are deprived of it, and he has helped to establish the Children in Nature Network. Among biologists, I have been inspired by Nalini Nadkarni, a tropical ecologist who studies rainforest canopies. She also pioneered the use of nature in rehabilitation of prison inmates, as well as adolescents in inner city schools. I was particularly taken by her leading these students to a forest site with rap musicians (fig. 15.3), where they used climbing gear to ascend to the forest canopy. One of them sang: Wet and green moss I’m at a loss To describe the beauty Falling on my booty. But held up by strings Came up here to do some things. But no pressure, I’m feeling free.

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“I, We, and It” Are these beneficial effects of nature on our well-being the products of cultural history, early childhood memory, the consequence of parental teaching, or ordinary learning? Or are they the consequence of the structure of the brain and the interactions of its parts? If that is the case, there may be deep historical precedents that condition our experiences in nature. We experience the world as conscious self-aware beings, with highly complex thoughts and insights. A fundamental shortcoming of the scientific method, as pointed out by the philosopher Ken Wilber (who summarized the issue as “I, We, and It”) is its deficiencies in examining mind and consciousness. We use the scientific method to study objects (the “its”) that are measurable. For studying objects, through the formulation of hypotheses and experimentation, this method has been the basis for the modern scientific understanding of nature and the universe. Studying the function of the brain is an approach to finding a neurological (and an “it”) correlation to our personal responses to nature. However, the method falls short in the study of human behavior, particularly relating to consciousness. Since consciousness is not directly measurable, it is not “real” in a scientific sense. Yet it is through the mind that our full relationship to the physical universe, including nature, can be appreciated. Wilber’s “we” concerns the study of behavior of humans in groups. “We” is amenable to study by the social sciences, often through the subjective evaluation by human subjects (usually groups of college students!) or measurements of activities. Many benefits of nature to human health have been studied by social scientists. Philosophy enters into the arena of “we” in the study of ethics. We examine “I,” or human consciousness, through introspection, philosophy, psychoanalysis, and the arts: literature, (especially poetry), music, and the visual arts. A discipline that bridges the divide between “it” and “I” may be mathematics. Mathematicians work with concepts within the mind and often without any reference to the physical world, yet mathematics is the foundation upon which the study of “it” rests. Mathematics emerges from the inner space of our minds and encompasses the universe.

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Nature and the Brain What is behind the experiences of immersion in nature, with their psychological benefits? It is certainly scientifically appropriate to search for evidence of physiological changes associated with them, or evidence for the neural correlates of these experiences, as specific sites of activity in the brain and interactions between such sites. Scientifically, that would be evidence of the physical existence of the experience. Roger Ulrich and colleagues, who first showed that hospital windows with views of trees hastened the healing of surgical patients, also demonstrated that nature videos reduced blood pressure and heartbeat rate in blood donors, one among several studies showing that cardiac function after stress is improved with experiences in, or views of, nature. Time in vegetation decreases stress by reducing cortisol levels. In Japan and Korea, there is a long tradition of visiting the forest to reduce stress, known as shinrin-yoku (forest bathing). Being in forests reduces blood pressure, cortisol production, and even modulates immune responses. In addition to the visual effects of being in the forest, volatile organic compounds (VOCs, forest odors from leaves and wood, p. 86) also promote these responses. Presently, the strongest evidence for involvement of areas of the brain in encountering nature comes from the measurement of electrical fields in the cerebral cortex by electroencephalography (EEG) and more recently and precisely through imaging by functional magnetic resonance (fMRI). EEGs give evidence of very rapid responses. For instance, British researchers outfitted joggers with portable EEGs and monitored their brain waves while they passed through vegetated park-like and hard urban sectors of their routes. In shifting from urban to nature, they noted changes in brain waves indicative of “reductions in frustration, arousal and engagement.” High-resolution spatial information is provided by fMRI, by detecting changes in brain tissue blood oxygen levels (fig. 15.4). With fMRI, Stanford researchers showed that walks in nature affected brain activity and reduced “self-focused behavioral withdrawal.” Thus, experiences in nature may activate certain areas of the brain. Michael Hunter and colleagues at the University of Sheffield used images of natural scenes compared to urban ones to compare effects on the brain. They showed greater connectivity between the auditory cortex and other brain areas during exposure to natural scenes. Similarly, researchers from the University of Heidelberg have shown how experience in nature might ameliorate responses to social stress. Subjects who had spent their child-

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Figure 15.4 fMRI images of a dorsal slice of the brain, comparing activated (colored) areas while viewing faces or houses. R-values are correlations between samples of images, showing significant values among faces, and among houses, and negative values between the two images (courtesy of the National Institute of Mental Health).

hood in rural areas were compared to those who had lived in cities, and the experiment was repeated with subjects presently living in rural areas or cities. In both cases, rural subjects revealed less arousal in a stress-inducing trial, as revealed by increased activity in the cingulate nucleus of the amygdala, an emotion-processing location in the brain. Their research was motivated by the well-known association of schizophrenia with urban population densities.

Biophilia and Evolutionary Psychology The idea of biophilia, of our deep connections to other organisms, was first popularized by the biologist E. O. Wilson in 1984. His was a scientific view (but difficult to test), and much speculation has been written about the psychological, neurological, and biological basis for this connection. We need to consider biophilia in the light of human evolutionary history. We share much genetic information with other organisms, going back

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to the origin of life on our planet, and we have progressively more in common with the lineage of organisms that are direct ancestors, starting with terrestrial vertebrates (300 mya), then the mammals (originating 200 mya), then primates living in trees of tropical forests (60 mya), then more directly in the great apes, family Hominidae (20 mya). The Hominidae include gibbons, gorillas, chimpanzees, and orangutans. Most of them are tropical forest inhabitants, tree dwellers with broad appetites, and able to make and use simple tools. The hominines, the group in which humans evolved and which includes the chimpanzees and their close relatives the bonobos, appeared about 6.8 mya in Africa. These were partially arboreal animals. The genus, Homo, to which we belong, originated around 2.3 mya in Africa. Although still largely arboreal, the anatomy of the skeletal remains suggests that these ancestors walked erect and had much larger brains. Around 0.2 mya, modern humans, Homo sapiens, originated in the savannas of East Africa. They lived on the ground but still had the ability to climb trees. Accompanying this history was the evolution of the brain. The basic “reptilian” brain was established in the early evolution of vertebrates. In mammals a second overlaying brain, the forebrain with the limbic system (including the hippocampus and amygdala), evolved. It supported the functions of motivation, olfaction, emotion, long-term memory, and behavior. These are functions we share with our pets, such as dogs and cats. The neocortex evolved in mammals and became particularly prominent in the primates, the hominines, and us. With this expansion, short-term memory, abstraction, and consciousness appeared. Do we have the capacity in our brains to retain “memories” of our evolutionary history, as the biophilia hypothesis suggests? Research with fMRI on phobias, on color values, facial recognition, and scene detection suggests such a possibility. Phobias are anxiety disorders fixed on a broad array of phenomena or situations. Some people have phobias of height (fear of falling), small spaces (claustrophobia); most of us have some aversion to spiders and snakes, and for a few that repulsion is pathological. In humans there is no evidence supporting an inherited memory of snakes and spiders, but both babies and adults learn to detect snakes as hostile much more rapidly than a neutral object, like a flower. In the rhesus monkey, there is an inherited neural pathway that mediates the fight-or-flight response to snakes. Phobias are partly located in two areas of the brain. My son loves snakes; I don’t like to handle them— perhaps because of repeated warnings about rattlesnakes during my childhood. We are both quick to recognize them.

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The recognition of faces, whether threatening or friendly, is another important trait that likely helped animals to survive. Darwin argued in his book The Expression of Emotions in Humans and Animals that the expressions are universal among different cultures. At the very least, humans are predisposed to detect threatening expressions, and infants learn to detect and mimic facial expressions very early in development. We now know that two areas of the cortex are employed in facial identification. Geometric shapes are associated with facial expression, and a downward V conveys anger; activating the same neural pathways that an angry face does. The association of color with emotion in humans is weak in general, although a lot is written about the roles of color in architectural and interior design. Our color preferences and emotional associations are heavily influenced by experience and language. However, the color red is broadly associated with excitement among different races and cultural groups, and the colors blue and green are pacifying or calming. Red is particularly interesting because its perception is not widespread in primates but is among apes (and most of us humans). Evolutionarily, detection of red may have been important in food collecting by arboreal primates, to select tender young red leaves and red fruits in tropical forests. Red color is also associated with blood (recalling injury and prey). In detecting scenes, sensory pathways and locations of scene detection have been found in the brain and cerebral cortex, and there appears to be a pleasure reward associated with the detection of natural scenes. Thus, some tendencies in behavior are physically located in the brain and could be inherited. These predispositions may have been of selective advantage to our ancestors up to a few centuries ago.

Consciousness and Nature Our scientific understanding of the brain, sensation, and perception actually rests on a philosophical foundation, beginning with the writings of John Locke (1632–1704). Locke was influenced by Thomas Willis, the first neuroanatomist. Thus, Locke wrote about the philosophical implications of sensation and perception, which led to our modern understanding of the perception of the surrounding world. Our brains create the perceived world through the reception of energy (chemical, electromagnetic radiation, touch, and atmospheric pressure waves) by sensory organs and the processing of information. That world includes the scientific understanding of our brains and perception. V. S. Ramachandran wrote:

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How can a three-pound mass of jelly that you can hold in your palm imagine angels, contemplate the meaning of infinity, and even question its own place in the cosmos? Especially awe inspiring is the fact that any single brain, including yours, is made up of atoms that were forged in the hearts of countless, far-flung stars billions of years ago. These particles drifted for eons and light-years until gravity and change brought them together here, now. These atoms now form a conglomerate— your brain— that can not only ponder the very stars that gave it birth but can also think about its own ability to think and wonder about its own ability to wonder. With the arrival of humans, it has been said, the universe has suddenly become conscious of itself. This, truly, is the greatest mystery of all.

Given the complexity of the brain and its plastic responses to the environment by each individual, it is certain that each of us perceives the world slightly differently than everyone else. Yet we share approximately the same views of the world. The philosophy of phenomenalism, particularly important in Europe in the twentieth century, investigated our experiences of the world and their relationships to consciousness. It emphasized the properties of the objects and their contributions to perception. One of the leaders of this philosophy, Maurice Merleau-Ponty, used the leaf, both as a plant organ and the printer’s term of a leaf (“feuille,” a large sheet of paper printed and then folded into itself to form part of a book), as a metaphor for perception. “Nature: an ontological leaf— the thin leaf of natureessence is divided in folds, doubled, even tripled. By examining it, we have retrieved everything, not that everything is mature, but because everything is or becomes natural for us. There are no substantial differences between physical nature, life, and mind.” He wrote of a matrix that enveloped both the perceiver and the perceived, and the possibility, such as through the arts, of having a truer understanding of both. The deep ecology movement of the late twentieth century borrowed from phenomenalism, through the philosophy of Arne Næss. Its roots were also in the psychedelic and utopian movements. Many deep ecologists, harboring a strain of organicism (that the universe at different scales consists of intelligent organic systems), sympathized with the views of James Lovelock and Lynn Margulis concerning Gaia (p. 88). Ideas in the new field of evolutionary psychology also contributed to the deep ecology movement. Our experience in nature, influenced by our history in the forests and savanna of Africa, may contribute to archetypes,

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predispositions to perception, and behavior. On the one hand, predictions of evolutionary psychology could possibly be tested by more research in brain imagery, looking for locations and networks associated with experiences in nature. On the other hand, psychoanalysis, established by Sigmund Freud and his student Carl Jung, included the notion that evolution produced archetypes revealed in the investigations of their patients’ subconscious. Many of Jung’s archetypes referred to the social structure of mother, father, brother, sister, uncle, so forth, and also to natural phenomena important to survival, either attractive or repulsive (like snakes and spiders). Influenced by Eastern teachings, Jung developed his concept of the self as the heart of consciousness. Murray Stein, a student of Jung’s teachings, wrote of Jung that “the self is responsible for the underlying unity of the psyche as a whole.” Jung’s ideas influenced philosophy (neurophenomenology) and ecotherapy. Two writers influenced by Jung are the psychoanalyst Anthony Stevens (The Two Million-Year-Old Self ) and the human ecologist Paul Shepard (p. 251, Coming Home to the Pleistocene). Shepard wrote of the forest and its associated archetypes in our deep memory. The dense forest has its gothic side and smell of danger too, perhaps as the visceral fear of an open-country vertebrate. The solitude, silence, dim light, and cool quiet of that great interior is profoundly calming. Tree climbing itself is very important. . . . The forest limitation of our movement is different from the sense of freedom that open country gives us, and its roots go much deeper into our past, as though the forest were part of our brain, a silent mnemonic reminder, especially for children who have not asked the question of meaning and continuity with the natural world, a reminiscence emerging later in life.

In The Spell of the Sensuous, David Abram shared his experiences with the shamans of traditional societies in Bali and Nepal, and described their heightened awareness of nature. While living in the Asian tropics, I encountered the Temuan of Ulu Langat, in Malaysia (p. 254); and the Warli from the Tansa Valley, in the state of Maharashtra, India (p. 254). In Malaysia, I employed several village elders for plant-collecting trips into the rainforest at the head of the valley where we lived. The Temuan collected medicinal plants, fruits, and agallocha (the highly prized fungal-infected heartwood of a tree, used in perfumery), which they sold to middlemen.

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Figure 15.5 Traditional forest people of the author’s acquaintance. Left, Temuan guides, in primary rainforest of the Ulu Kenaboi, West Malaysia, 1975. Right, Warli collaborator, Shantaram, in deciduous forest at the base of Mondagni Peak, Tansa Valley of West India, 1985.

They knew virtually every tree in the forest, why it was there, and how it was used. When we encountered a fruit tree in the forest, as a durian, they knew when a village had been established and abandoned there. They enjoyed these trips (fig. 15.5); the forest was clearly their home, and they were content and respectful traveling in it. The Warli (p. 254) are a distinct Indian tribe, oppressed by centuries of contact with Hindu society. I often visited a Warli village, Gayagota, adjacent to a tropical deciduous forest site I studied. I hired Shantaram, an elder respected by the villagers as the most knowledgeable of the forest and its plants (fig. 15.5). He helped me to learn the trees, to set up the experiments, and to protect the forest from any wood gathering while I worked there. I continued to visit him years later. In Shantaram and my Temuan guides, I saw a close connection with the forest and its organisms, of biophilia. Whether it was innate, embedded, or learned from childhood, I don’t know. They didn’t display any fear of snakes but certainly would’ve been alarmed if a leopard was stalking them. Both tribes had religions with complex mythologies (the tiger figured large in both) and long lists of taboos. The Temuan were particularly careful at dusk, when forest spirits were on the move, and the Warli guarded their village with stone totems

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along its boundary and with a shrine to the god Wagya (the tiger). It takes time and a receptive mind to learn deep attitudes from people in another culture— let alone people in our own society. There is a danger in projecting an image of the “noble savage” onto these people. Certain individuals had deep connections to their environments, yet others lacked them. Having been both a scientist, working with the world of “it,” and a contemplative human being in the world of “I,” I live in and between both worlds and try to reconcile the contradictions between them. There will be continued discoveries in the locations of centers and links in the brain that are necessary for consciousness, fed by research initiatives in the United States and Europe. British scientists even have located centers for “Christmas spirit” in the cortex. More importantly, this research will help to decipher pathologies of the brain, such as epilepsy and dementia. However, the frustration of using the scientific method to study the mind directly will continue, as in studying our emotional responses to nature. In the “it” approach, the functioning of consciousness should ultimately be reducible to the laws of biology, and then of chemistry and physics. Consequently, hallmarks of consciousness, as freedom of choice, may be illusions. However, the phenomenon of life is not fully explainable by those laws; certain properties emerge, or unexplainable residues persist (p. 22), and mind and consciousness in humans is the most radically emergent property of all. In parallel, I have explored my mind at the “I” level, through the personal investigation of my own consciousness. My early experiences in nature inspired me to examine Eastern religions and take up the practice of meditation some thirty-five years ago. It has helped me to clear my mind through conscious effort. When I have a focused intent to experience nature, such as sitting in a special place or walking on a trail, it is important for me to remove extraneous thoughts to receive as direct a perception as my consciousness allows. I do employ the normal organs of perception, but I use them with the highest clarity I can achieve, and with my mind still. It is interesting that meditation practices in these spiritual traditions are closely aligned with nature; Buddha received enlightenment under a tree. And both nature and meditation change the function of the brain— perhaps by similar mechanisms. I hope to make more headway in the fields of “I,” with philosophy (still very important in the neuroscience literature), psychoanalysis, meditation (now also popularly taught as “mindfulness”), and the arts (poetry, visual art, and music), an alternative means of investigating consciousness and our relationship to nature.

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Nature: Design, Fakery, and Art When our grandson Shaun started school, we exposed him to nature again. We went to Everglades National Park, where he became fascinated by alligators. We also visited Washington State; there we walked to one of my favorite places in the Alpine Lakes Wilderness. The trail to Stuart Meadows followed a gentle grade along Stuart Creek in the shade of forest, mainly big Douglas fir with some red cedar near the creek (fig. 15.6). Shaun remembers the rushing water and the fragrance of trees. Perhaps we should expect the strongest experiences of nature in such places, with more biodiversity and isolation from human activity. However, even our experience along Stuart Creek was altered by the location of the trail and past protection from forest fires. Our attempts to manage natural ecosystems— especially to restore damaged ones, such as the huge project now under way in the Everglades— are a sort of fakery. Perhaps some of the values of those ecosystems can be brought back, as bird populations in the Everglades, but there is no real reversal of those alterations and the attempt at restoration is fakery. The most pristine natural places will be affected by climate change, meaning that new combinations of species may establish there in the future. Forests infiltrated with exotic species are another form of fakery, but they still may be experienced as beautiful places. We also tend to perceive nature as the direct or indirect product of ar-

Figure 15.6 Left, Stuart Meadows and Mount Stuart, North Cascades of Washington State. Right, grandson Shaun along Stuart Creek.

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tifice or design. The impulse to design is a part of us, just as much as our connection to nature. It is a natural impulse, and we are quick to detect design in nature, as the features of leaves (surfaces, veins, edges, sizes, shapes, etc.). We have also taken inspiration from nature to invent new devices. It is natural for us to appreciate the design of leaves, and yet we can accept the forces of natural selection and evolution at the same time. Some will see such patterns as evidence of intelligent design. I disagree with their conclusions, but accept that they may be so influenced to respect and protect nature. Years ago Martin Krieger’s essay and book, What’s Wrong with Plastic Trees, discussed this fakery. To Krieger, we create facsimiles of nature through design, from organisms or whole ecosystems, with varying degrees of success. For instance, a tree— with bark texture, branches, and green foliage— can be produced with a good visual approximation of a real one (but no photosynthesis and exchange of gases). He controversially argued that such designs could be for the common good if they helped to preserve nature elsewhere, and if they benefited humans psychologically and socially. Producing nature artificially is in full swing these days. High-quality artificial foliage, coming from Chinese workshops, is available in craft stores. Cell phone towers are disguised to look like trees. Scenes of nature— such as photographs, landscape paintings, or images on flat- screen televisions— are commonly used to soften work environments. Peter Kahn, a psychologist at the University of Washington, has studied these fakes of nature— testing if they are a substitute for the real thing. He has compared flat-screen views with a real view through a window, robotic animals with living pets, and artificial remote gardening with real gardening. He has found that artificial nature provides some benefits (as in stress reduction), but not nearly as much as real nature. The more completely we can fake nature, as in foliage, the more likely the experience will affect us. However, our perception of leaves is multi-sensorial and influenced by our memory, which is not easily fooled. Children use digital technology to substitute images of nature for the real thing. It seems that the past generation of children has been robbed of direct experiences of nature, their birthright, substituting a safer and highly regulated environment of home and school, and placing the visual stimulus of screens— of computers, tablets, smartphones, and TVs— as a substitute for exploring that natural world. Screen interactions can become addictive, pulling children and adults away from human activities and socially isolating them. Various therapy programs have been established to treat this

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Figure 15.7 This tree house, located in a forest setting outside of Seattle, is a location for nature therapy by reSTART to help clients combat their addictions to games and other computer activities.

pathology, and most of them incorporate experiences in nature. In Seattle, reSTART incorporates a forest tree house as one of the natural locations for its therapeutic practices (fig. 15.7). An old friend, Tom DeFanti, designs environments of virtual reality in his laboratory at Calit2, on the campus of the University of California, San Diego. Several years ago, he showed me around the lab, placing me in the virtual environment of his summer home in Wisconsin, and had me fly above a simulation of the planet Mars. These representations are getting better and better, yet Tom is an avid outdoor enthusiast. We climbed Gunung Nuang, the highest mountain in our Malaysian valley with the help of those Temuan guides. Virtual reality productions are now making the rounds of film festivals, such as one for the film Wild, and the technology is improving rapidly. Patrick Blanc is a French botanist/artist whom I first met in the tropical rainforests of French Guyana, where we both were fascinated by the leaves of understory plants. He has channeled his love of tropical nature toward the design of artificial landscapes on building walls, using special irrigation systems and assemblages of living plants. His murs végétaux have

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Figure 15.8 Patrick Blanc in front of one his green walls (murs végétaux).

become an artistic sensation (fig. 15.8). In Miami’s Wynwood Art District, I entered a small gallery, Plant the Future, which sells small sculptures with living plants plus walls of mosses ($300/square foot) and of tropical plants obviously inspired by Patrick (at $150/square foot): high- priced walls for a little tranquility. The strongest art form for engendering an emotional connection to nature (and the subtlest form of fakery) may be film, which can combine sound, music, moving images, and dialogue to tell a story. Its potential has seldom been realized for an environmental purpose, although there is no shortage of spectacular nature documentaries (which my grandson enjoys viewing). Francis Hallé (p. 140) had wanted to make a film about tropical rainforests for decades. He finally found a collaborator in Luc Jacquet; Il était une forêt is a beautiful film and has won several awards (fig. 15.9).

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Figure 15.9 Il était une forêt. Francis Hallé sitting on a tree branch in a tropical rainforest in Gabon.

Beauty, Art, and Nature The first week of every December, Miami hosts an art festival surrounding the international art exposition Art Basel. It is the largest display of art in North America. I spend a couple of days every year at the fair, wandering through the exhibits. In the visual arts, nature is an important subject of many contemporary artists, and they employ elements of natural design and fakery to achieve a desired expression of some aspect of nature. I am on the lookout for such artists. Their work could be a sublime and rich landscape, or the most minimal of landscape elements. It could be a natural object or scene made up of the most unnatural materials. It could express love, or even fear, of some aspect of nature. As I walk among crowds of thousands at the different shows, I am surrounded by those who have a different sense of beauty than mine. Mine is associated with nature, utility, love, proportion, form (as Plato), symmetry, truth (like Keats), virtue (Aristotle), color, humor, irony, and much more. Some argue that the notion of beauty is totally subjective, and others hold that the key to beauty

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Figure 15.10 Julie Hedrick, who creates abstract atmospheric paintings, exhibited Into the Forest at Art Miami, a satellite fair during Art Basel Miami 2013.

is in the structure of the brain (neuroesthetics). My search for beauty continues. I find a minimalist landscape by Julie Hedrick (fig. 15.10). I encounter one of Naomi Fisher’s strong and troubling photographs of a woman submerged in plants (fig. 15.11). I particularly look for leaves, expecting the details I wrote about in previous chapters (edges, shapes, veins, patterns, complexity in function and interaction, culture, archetypes) in the art. Some artists are inspired by science, and that is beautiful to me as well. Beauty is an important part of the scientific quest. Simple yet far-reaching ideas are beautiful. Forms and rules that are symmetrical are beautiful. The awe-inspiring complexity of a leaf, of all life, of the entire universe, is beautiful. Ending my career of scientific research, I take that beauty with me as I become more involved in artistic pursuits. This past year our grandson, now eighteen, began a downward spiral, dropping out of school, hanging out with kids with similar problems, moving toward criminal behavior. We enrolled him in a wilderness therapy program in Utah. In two challenging months of sleeping under the stars,

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Figure 15.11 Art and leaves, photograph by Naomi Fisher and on display at the Pérez Art Museum, Miami.

climbing up and down canyons, ascending mountains, learning how to cook and care for himself, and participating in individual and group therapy, he turned his life around. He finished his GED at a school that integrates nature activities with normal academics. His future once again looks bright. What arouses his love of nature? His earlier experiences may have helped. Perhaps the arts helped maintain his connection, especially the documentaries. For me, amidst the grim reality of our environmental problems, I find truth and beauty in the work of artists of all sorts. I’ve watched Naomi Fisher grow in her artistic vision. Hearing Nalini Nadkarni speak about her work connecting young people with nature inspires me. Seeing Patrick Blanc add an artistic dimension to his love of tropical plants inspires me. Seeing Francis Hallé realize his decades-long dream of producing a beautiful film about tropical rainforests inspires me. The amazement of witnessing the world’s leaders convene in Paris to pass a comprehensive agreement to limit temperature increases through the control of green-

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house gas emissions, a beginning, inspires me. Along with the science, I believe that the attitudes and emotions of these leaders were important in passing the Paris Agreement. I will continue to explore my own responses to nature, through travels, and I will pay attention to the more accessible nature close at hand, such as the beauty of leaves. My sadness about the destruction of nature will be leavened by my continued amazement of that beauty, and gratitude for my ability to be touched by it. I will continue to be fascinated, and often amazed, by the advances in scientific research. And I will continue to attempt to reconcile the worlds of “I,” “we,” and “it.”

acknowle d g m e n t s

M

y fascination in leaves was promoted by many teachers along the way. As a college student at Pacific Lutheran University, I was influenced by the teaching of Professors Jens Knudsen and Harold Leraas during field courses at Holden Village, in the North Cascades of Washington State, and later by John Gordon at Victoria University of Wellington, New Zealand. As a graduate student at Rutgers University, Barbara Palser instructed me in the details of leaf structure and morphology, and Carl Price in their physiology. In later work at the University of Malaya, Ben Stone helped introduce me to the diversity of plant form in the tropics, Brian Lowry to their chemical diversity, and Peter Ashton to their ecological importance. As a visiting scientist at the Université Montpellier II, I learned much about leaves from Francis Hallé, particularly during fieldwork in French Guyana and, many years later, in Gabon. Once established at Florida International University, in Miami, I learned about leaves from colleagues there and at other local institutions. At FIU, these included Jennifer Richards (morphology and development), Steve Oberbauer (physiology and climate change), Suzanne Koptur (ecology and plant/animal interactions); Brad Bennett (ethnobotany); Kelsey Downum (phytochemistry), Javier Francisco-Ortega (history) and Eric von Wetburg (plasticity). At Fairchild Tropical Botanic Garden, I learned much about many aspects of leaves from Jack Fisher and Barry Tomlinson (also at the Kampong of the National Tropical Botanical Garden), and Leo Sternberg from the University of Miami.

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FIU provided financial support for the use of color in the book, from the Division of Academic Affairs (Doug Wartzok and Ken Furton), the College of Arts and Sciences (Ken Furton and Michael Heithaus), and the Department of Biological Sciences (Tim Collins and Steve Oberbauer). I was aided in my search for inspirational and appropriate poetry quotes from my membership in Sam Droege’s listserv: https://beta.groups.yahoo .com/neo/groups/naturepoem/info. The final chapter was particularly difficult for me, and benefited from the comments of Swami Anantananda, Bill Sutherland, and my wife, Carol. Brian Gunning generously provided a number of illustrations. I received technical advice, personal comments, and the offering of images from many people, given here in alphabetical order: Etwin Aslander, Wilhelm Barthlott, Virginia Berg, Patrick Blanc, Holger Bohn, Bob Brennan, Ann Burkly, Vincent Callebaut, Maria Martin Calvo, Ligia ColladoVides, Tom Defanti, Alain Dejean, Rita Duncan, Diane Edwards, Lilly Margaret Eluvathingal, Boglárka Erdei, Walter Federle, Taylor Feild, Naomi Fisher, Ted Fleming, Bobi Froscher, Judy Gallagher, Friederike Gallenmüller, Annie Garcin, Pat Gensel, Tom Givnish, Walter Goldberg, Holly Gorton, Kevin Gould, Maria das Graças Sajo, Patrick Griffith, Arleta Griffon, Arunika Gunawardena, Julie Hedrick, Mike Heithaus, Basil Hiley, Nick Hobgood, Missy Holbrook, Henry Horn, Chad Husby, Cynthia Jones, David Jones, Revital Katznelson, Andrea Keller, George Koch, Norma Koch, Kathelijne Koops, Lidia Kos, Patrick Krug, Akhlesh Lakhtakia, Claudio Latorre, Craig Layman, Tim Layman, Jason Lopez, Catherine Loudon, Tracy Magellan, Frank Mannoli, Mikel Manthey, Nancy Martinson, Trent and Michelle Meeks, Roger Meicenheimer, Fabian Michelangeli, Gary Monroe, Nalini Nadkarni, Karl Niklas, John O’Keefe, Paulo Oliveira, Jérôme Orivel, John Palenchar, Robert Pemberton, Jorge Pena, Tony Pernas, Taylor Perron, Sidney Pierce, Usher Posluszny, Colin Prentice, Cosette Dawna Rae, Gray Read, Carol Sue Rigano, Dana Royer, M. E. Rumpho, Scott Russell, Rolf Rutishauser, Brad Seymour, Thomas Speck, William Stein, Dennis Stevenson, Philip Stoddard, Greg Strout, Kathleen Treseder, David Wacey, Mike Watkins, Michael Wenzel, Alexander Wild, Scott Zona, and Maciej Zwieniecki. Christie Henry, Editorial Director, Sciences, Social Sciences & Reference at the University of Chicago Press, and her associates enthusiastically supported this project at all stages. Erin DeWitt, Senior Manuscript Editor, did a terrific job of the final editing, finding the smallest errors

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and straightening out my often twisted scientific syntax. Ryan Li, Senior Designer, helped to bring out the beauty in the book. I was particularly impressed by the indefatigable critiquing by two anonymous reviewers of the 425 manuscript pages. Thus, “it took a village” to complete this book. Despite all of this help, as the saying goes, the incorrect statements and sins of omission likely to occur in this book are certainly mine.

ap p e ndi x a: le af te r m i n ol o g y

A

ccording to the Shorter Oxford New English Dictionary (1993), a leaf is “the organ of a plant. Any of the broad flat usually green outgrowths of a vascular plant, produced laterally from a stem or branch or springing from the base of the stem, which function as the principal organ in photosynthesis.” Expanding on this definition (p. 34), I add that leaves are determinate organs derived from meristems, at the tips of shoots or at the bases of existing leaves. Here, I describe the features of leaves in considerable detail using the terminology of the authoritative Manual of Leaf Architecture, which goes well beyond the chapter text in describing leaf structures, and also surveys the past literature. Technical terms are italicized and are defined by the surrounding text. Common plant names (underlined) are used for the illustrations, but their scientific equivalents are listed in the notes at the end of the book. In gaining a better appreciation of leaf features, one can see that identification keys based on leaf features are relatively easy to construct. Even if the trees are deciduous and have fallen from the tree, the fallen leaves can be examined and their places of attachment on a stem can be discerned.

A Generalized Broad Leaf I begin with the leaf of a typical eudicot plant, hackberry (fig. A.1). Beyond the typical broad leaf, there is a dramatic range of leaf types (fig. A.2), some characteristic of large and important plant groups. Leaves develop as spines in cacti, such as nylon hedgehog cactus. Leaves de· 313 ·

APPENDIX A

· 314 ·

Figure A.1 The general structures of a leaf, with the example of the young leaf of a hackberry.

velop as tendrils in climbing plants, cat’s claw creeper. Leaves develop as traps in carnivorous plants, as in the North American pitcher plant. Leaves collectively form a bulb, as with the onion. General leaf types (fig A.3). A “normal” or broad leaf is like the labeled photograph (fig. A.1) (as in live oak). A general monocot leaf has a sheathing base and parallel veins, such as that of the ti plant. Palm leaves are large and tough, and their bases form sheaths or thicken and widen. Palmate leaves (with segments and hastula) are exemplified by licuala. Pinnate leaves (their leaflets with sheath— and crownshaft, or swollen base) are typified by the coconut. Costapalmate leaves (segments with extension of petiole, or costa, extending toward tip) are shown for sabal. Fishtail fronds (highly divided leaflets) are rare, seen in the fishtail palm. Banana leaves are long, with single midrib and parallel secondary veins and a sheathing base, seen in most members of the ginger order, including bananas and the traveler’s palm. Needles are exceedingly thin and long, such as those on the slash pine (fig. A.4). Scales are exceedingly small (Australian pine, fig. A.4) and often fit together to form a flat surface, as in the oriental cedar (fig. A.4). Attachment of leaf to the stem can vary (fig. A.5). Leaves may be directly at-

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Figure A.2 Leaves with different functions. Top left, spines of nylon hedgehog cactus; top right, leaf traps of the North American pitcher plant; bottom left, tendrils of cat’s claw creeper; bottom right, storage leaves of onion bulb.

tached without petiole (sessile), as in vegetable leather. Leaves are usually attached via petiole, long or short. Petioles attached to the edge of blade (marginate) include edible fig. Leaves are rarely attached to the interior of blade ( peltate), as in lotus. Where leaves attach to the stem can vary (fig. A.6). In the example of beech, alternate leaves attach singly to stem. Opposite leaves attach in pairs on opposite sides of stem, as in coffee. Sub-opposite leaves attach very near each other, but not exactly opposite, as for crepe myrtle. Whorled leaves attach to the stem in groups of three or more, many at the tip of the stem, as in the sapodilla tree; and three at intervals along the stem length, as in oleander. Organization of leaf blades varies from a single blade per leaf, to many blades;

Figure A.3 General leaf types in broad-leaved plants. Top left, typical leaf of a live oak; top center, parallel veins of monocot, a ti plant; top right, pinnate palm frond of a coconut. Bottom left, palmate frond of a licuala palm; bottom right, costapalmate frond of sabal palm; bottom center, fishtail frond of a clumping fishtail palm.

Figure A.4 General leaf types among all plants. Left, banana-like leaf in the traveler’s palm; left center, whitish leaf scales around stems of Australian pine; right center, scales of the oriental cedar; right, needles in a slash pine.

Figure A.5 Leaf attachment to stem. Left, in most leaves, the blade is attached via a petiole, as in the edible fig. Center, in vegetable leather, the leaf blade is attached directly to stem. Right, in the sacred lotus, the leaf blade is attached at its center.

Figure A.6 Positions of leaf attachment to stem. Top left, American beech leaves are arranged alternately; top center, coffee leaves are arranged oppositely; top right, three leaves are inserted at the same position in oleander. Bottom left, queen crepe myrtle leaves are arranged not quite oppositely (so we say “sub-opposite”); bottom right, leaves are concentrated at the ends of branches, or in whorls, in sapodilla.

APPENDIX A

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Figure A.7 Simple versus compound leaves. Top left, simple and alternate leaves of an American linden tree. Top center, pinnately compound leaves of an American walnut, with two (even) terminal leaflets. Top right, in Brazilian pepper, seven leaflets are pinnately arranged with a single leaflet at the tip. Bottom left, in verawood the even pinnately compound leaves are oppositely arranged. Bottom right, the palmately compound and alternately arranged leaves in the Ohio buckeye.

leaves are simple or compound (fig. A.7). The leaf is defined by the way it develops from a bud, with an axillary bud at its base. Simple leaves are by far the most common: linden. Compound leaves have many blades in various arrangements making up a single leaf. They can be arranged on the stem either alternately or oppositely, and the leaflets as well. In palmate leaves, leaflets are joined together at the base, like fingers in a hand: Ohio buckeye. In pinnate leaves, leaflets (or pinnae) are arranged along the midrib, or rachis, of the leaf, in several arrangements. Once-pinnate leaves produce two rows of leaflets, of varying numbers, as in walnut. The tips of these pinnate leaves can have paired (verawood) or single leaflets (Brazilian pepper). Twicepinnate leaves have an additional order of leaflets, joined to the main rachis,

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Figure A.8 Pinnately compound leaves vary in the orders of leaflets, as first order in fig. A.7, to second and third order. Left, a second-order compound leaf in copperpod; and right, a third-order compound leaf in the Amorphophallus.

as in copperpod (fig. A.8). Thrice-pinnate leaves have a third order of leaflet organization and are rarely encountered, as the Amorphophallus (fig. A.8). The proportions of a leaf blade, whether simple or compound, can be placed in one of the following categories (fig. A.9): elliptic, with the widest part in the middle, cinnamon; obovate, with the widest part near the tip, black olive; ovate, with the widest part near the base, leaflet of poison ivy; oblong, with the widest part for half or more of the length, mango; and linear, with a very narrow leaf blade, lucky nut. The symmetry of the leaf blade can be bilateral (the same on each side of the midrib), such as all of the leaf blades described above (fig. A.9), or asymmetrical, where one side is different than the other, as in linden (fig A.7), begonia (fig. A.10), or the Florida trema (fig. A.10). The shape of the leaf blade can be unlobed, or simple, as the examples above, or it can be lobed (fig. A.11). The terminology for lobing is like that used for compound leaves. In palmate-lobed leaves, lobes radiate from near the base, like fingers on a hand, papaya. In pinnate- lobed leaves, lobes occur along the length of the leaf, white oak. In bilobed leaves, the two lobes divide along the midrib, as in the purple orchid tree. In lobed leaves, the indentation, or sinus, may be round or angular, as may also be the tips of the lobes (fig. A.12); for angular, sweet gum; and for rounded, sassafras. Leaf margins, whether the leaf is lobed or entire margins may be smooth, like all the simple leaves illustrated above, or toothed, like the castor bean (fig. A.13). The teeth on these margins can be of the same size, as with the

Figure A.9 The proportions of the leaf and leaflet blade. Top left, obovate in black olive; top right, linear in lucky nut; bottom left, oblong in mango; bottom center, elliptic in cinnamon; bottom right, ovate in poison ivy.

Figure A.10 Asymmetric leaf blades. Left, Florida trema; right, begonia.

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Figure A.11 Leaf shapes also vary in lobing, from unlobed to lobed pinnately or palmately, just as for compound leaves. Edges may also undulate. Left, papaya leaf lobes are palmately arranged, and each is also lobed. Center, lobes in white oak are arranged pinnately. Right, in the purple orchid tree (Bauhinia), each leaf has two lobes separated along the midrib.

Figure A.12 More leaf lobing. Left, in sweet gum the sinuses of the five lobes are angular. Right, the sinuses are smooth in the twice- or three-lobed leaves of sassafras.

castor bean, or of two orders of size (essentially teeth on teeth): western alder. The shapes of the teeth also vary. If the teeth are sharp but stick straight out from the margin, they are dentate, as in Christmas berry. If the teeth are pointed toward the apex, they are serrate, as in this aechmea bromeliad. If the tips of the teeth are rounded, they are crenate, as in the Indian pennywort. The plane of the leaf blade is also an important distinguishing character (fig. A.14). In many leaves, the blade is flat but varies in other species. The surface of the blade may undulate, as in bakuli. The edge of the leaf may curve toward the undersurface, revolute, as in allspice. More rarely, it may also curve toward the upper surface, involute, as in cocculus.

Figure A.13 Edges (margins) vary from smooth (entire) to strongly toothed. Top left, teeth point straight out (dentate) in Christmas berry. Top center, heavily armed teeth on leaf edges of the aechmea bromeliad point toward the base (serrate). Top right, teeth on teeth in western alder. Bottom left, lobes produce teeth in castor bean. Bottom center, edges are sinuate in the chestnut oak. Right, teeth are blunt (crenate) in the Indian pennywort.

Figure A.14 Most leaves are relatively flat (such as fig. A.5), but surfaces vary in many. Left, in snail seed leaf edges turn up (involute); center, edges turn toward the undersurface in allspice; right, margins are undulate in bakuli.

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Leaf tips vary in several ways (fig. A.15). The tip may be straight, narrowing toward the point in a straight line, teak. The narrowing may produce a convex shape, as in Spanish stopper. The narrowing may be more concave, producing an acuminate tip, peepal. The tip may actually be a small and shallow depression, retuse, as Madagascar olive. The angle leading to the tip may be narrow (acute), larger (obtuse), or producing a depression (revolute), as in the tulip tree. In addition, the tip may terminate in a very sharp and dangerous spine, as in the agave. Leaf bases also produce valuable diagnostic characters, similar to the tips (fig. A.16). The narrowing of the blade margin can be straight, as for white ironwood. It may also be concave, as for beautyberry, or convex in mamey apple. The base may also be lobed. A rounded extension (cordate) is relatively common, as in dombeya. Other arrangements, such as straight across (truncate), occur, as in trembling aspen, or arrow-shaped (sagittate) in Sagittaria.

Figure A.15 Leaf tips. Top left, convex curvature in Spanish stopper; top center, concave curvature and long narrow tip in the peepal; top right, narrow and very sharp tip in the agave. Bottom left, straight edges toward tip in the teak tree; bottom center, slightly recessed in the Madagascar olive; bottom right, wide and moderate depression in the tulip tree.

Figure A.16 Leaf bases. Top left, edges narrow toward base in a straight line in white ironwood; top center, edges curve convexly toward base in mamey apple; top right, edges curve concavely toward base in beautyberry. Bottom left, round lobes at base as in dombeya; bottom center, base is a straight line, as in aspen; bottom right, lobes at base are sharply pointed (sagittate) as in Sagittaria.

Figure A.17 Leaf surfaces. Top left, smooth surface in autograph tree; top center, sandpaper surface (scabrous) in rough velvet seed; top right, velvet (papillose) surface in Hoffmania. Bottom left, raised glands in dotted wild coffee; bottom center, spines in devil’s club; bottom right, densely hairy as in sagebrush.

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Leaf surfaces (fig. A.17) are usually smooth (as in the autograph tree), but depart from that considerably in some species. Leaves may have a rough, even sandpaper-like texture (rugose or scabrous) due to stiff hairs or raised veins; a good example is the rough velvet seed. A velvety surface is due to the rounded shapes of the cell surfaces (termed papillose) as in Hoffmania. Leaf surfaces may have depressions or projections (pitted) from glands, dotted wild coffee, or may be softly hairy ( pubescent), as in the sagebrush. Finally, sharp prickles may be present on the leaf surfaces, as in the devil’s club. Leaf texture (fig. A.18) is an important characteristic, often reflecting

Figure A.18 Leaf texture. Top left, thin and flexible (membranaceous) in stinging nettle; top right, tough and leathery (coriacious) in black mangrove; bottom left, succulent in bay cedar. These, and most, leaves are bifacial (top different than bottom). An exception is the unifacial leaf of the iris plant (bottom right).

APPENDIX A

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the ecology of the plant, but must be examined in fresh leaves. Thin and flexible leaves are membranaceous and mostly very short-lived, as in stinging nettle. Thick and tough leaves (coriaceous) are longer-lasting, black mangrove. Thick and juicy leaves are succulent, bay cedar. Most leaves are very different in appearance between the upper and lower surfaces: bifacial leaves. Stomates are limited to the undersurface, which is lighter in color because of the extensive system of air spaces. A few leaves, often in species growing in high light areas, are unifacial; they develop differently, and they have the same structures, including stomata, on both sides. A good example is the iris (fig. A.18). Petioles vary in characters (fig. A.19) and in some leaves are completely ab-

Figure A.19 Petiole characters. Top left, the short petiole of the strangler fig; top center, the long petiole of the short leaf fig; top right, nectaries present in the white mangrove. Bottom left, a thick structure ( pulvinus) may be seen at the base, in the poinciana and many other legumes; bottom right, a sheathing petiole base forms the crown shaft in some palms, as this foxtail palm.

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Figure A.20 More petiole characters. Top left, wings are present in petioles, particularly in the citrus family, as in this key lime. Top right, flattened petiole forms the photosynthetic surface in koa, and members in the genus Acacia. Bottom, sections of petioles, revealing their shapes left to right: square, Anthurium hybrid; triangular, licuala palm; channeled (caniculate), zedoary; winged (alate), fern-leaf tree; semi-round (semi-terete), blue-sky vine; round (terete), cardboard zamia.

sent, as with vegetable leather (fig. A.5). Petiole length varies greatly and is a diagnostic feature for identifying the two native Florida figs, the strangling fig with short petioles and the short-leaf fig with long ones. Petioles may have stipules at their base (as in coffee, fig. A.6), or not— usually absent when leaves are mature. The base of the petiole becomes a sheath in the leaves of many monocots, as with the foxtail palm, and glands may be present near their connection to the leaf blade as in the white mangrove. The base of the petiole in legume leaves is enlarged to form a pulvinus, as in poinciana. Cross sections of the petioles reveal their different structures (fig. A.20). In some, such as the key lime, the petiole is winged (alate). In others, the shape varies from round, or terete (cardboard zamia), semi-circular (semiterete, blue-sky vine), with a channel, caniculate (zedoary), to angular (square in Anthurium hybrid or triangular in licuala palm). In the evolution of some plants, such as the koa and some acacia relatives, the petiole has become

APPENDIX A

· 328 ·

Figure A.21 Stipule characters. Top left, in figs stipules form a sheath around the developing leaves, as the red structures in the Indian rubber tree. Top right, stipules persist as small leaf-like structures between the opposing leaves of the noni. Bottom left, hollow spines in the bullhorn acacia are derived from stipules. Bottom right, tendrils in the climbing smilax are developed from stipules.

flattened and leaf-like (a phyllode), being the principal means of the photosynthesis of the tree. Although most stipules (fig. A.21) look like small leaves (such as noni), and many form a protective covering for the developing leaf, as in the rubber tree, some take on quite different functions. Some become spines, as in the bullhorn acacia, and others become tendrils to aid in climbing, as in smilax. Leaf venation (fig. A.22) has been intensively studied and classified, particularly as an aid in identifying fossil plants (p. 166). All leaves produce

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veins, and most leaves have a principal vein associated with the midrib (fig. A.1). Deep in the evolutionary tree are the simple leaves of ancient lycopods, whose leaves (microphylls, p. 31) only have a single midrib and no other veins. Some leaves have several principal veins, as in Tibouchina. Veins are distributed to serve all leaf areas, so in lobed leaves, veins serve those lobes, which may be arranged pinnately, as in the breadfruit, or palmately in the spinach tree. In the Alexandrian laurel, the single main vein connects to a dense network of parallel secondary veins. In some ferns, and a few flowering plants, the veins branch dichotomously and remain open, as in the maidenhair fern. In most broad-leaved plants, the tertiary veins form a closed reticulated network, as in the purple orchid tree (p. 337). Such reticulate veins may also terminate in free veins at higher orders in the sinuses, as in the peepal. In grasses and other monocots (fig. A.23), the veins are largely parallel,

Figure A.22 Venation. Top left, primary vein feeds secondary veins serving major lobes in the breadfruit leaf. Top left center, five primary veins serve the palmately arranged lobes of a spinach tree. Top right center, veins in the angiopteris fern are open and branch dichotomously. Top right, in the Alexandrian laurel, the midrib serves numerous parallel and densely arranged secondary veins. Bottom left, three major veins serve the leaves of the Tibouchina, and other members of its family, the Melastomataceae. Bottom center, closed reticulate venation of the purple orchid tree. Bottom right; in the peepal leaf, each terminal sixth-order vein ends in the middle of a sinus.

APPENDIX A

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Figure A.23 Veins in monocots. Left, parallel venation in leaves of the black bamboo, a member of the grass family. Left center, veins are reticulate in the velvet leaf Anthurium. Right center, veins originate from the leaf base and are roughly parallel in the Canada mayflower. Right, in banana, a strong midrib serves a dense network of secondary and parallel veins.

as in the black bamboo, one of the characters of the monocots learned by every beginning botany student. However, many monocots have other vein patterns. In some species, all veins depart from the leaf base and spread in relationship to the leaf shape, as in Canada mayflower. In the banana leaf, the strong midrib contains the traces of the parallel secondary veins that depart throughout the length of the leaf. A variety of venation patterns, even reticulate, are produced in the monocot aroid family, as in the velvet leaf Anthurium.

note s f or appe n di x a

T

he authoritative source for leaf character descriptions, used extensively in the appendix, is Beth Ellis et al., Manual of Leaf Architecture (Ithaca, NY: University of Cornell Press, 2009). The scientific names of plants described in the text and figures follow in order of appearance. Hackberry = Celtis laevigata Willd. (Ulmaceae); nylon hedgehog cactus = Echinocereus viridiflorus Engelm. (Cactaceae); cat’s claw creeper = Dolichandra unguis- cati (L.) L. Lohmann; North American pitcher plant = Sarracenia purpurea L. (Sarraceniaceae); onion = Allium cepa L. (Alliaceae); live oak = Quercus virginiana L. (Fagaceae); ti plant = Cordyline fruticosa (L.) Goeppert (Asparagaceae); licuala = Licuala grandis H. Wendl. (Arecaceae); coconut = Cocos nucifera L. (Arecaceae); sabal = Sabal palmetto (Walt) Lodd. ex Schultes (Arecaceae); fishtail palm = Caryota mitis L. (Arecaceae); traveler’s palm = Ravenala madagascariensis Sonn. (Strelitziaceae); slash pine = Pinus elliotii Engelm. (Pinaceae); Australian pine = Casuarina equisetifolia L. ex J.R. & G. Forst. (Casuarinaceae); oriental cedar = Platycladus orientalis (L.) Franco (Cupressaceae); vegetable leather = Euphorbia punicea Swartz. (Euphorbiaceae); edible fig = Ficus carica L. (Moraceae); lotus = Nelumbo nucifera Gaertn. (Nelumbonaceae); beech = Fagus sylvatica L. (Fagaceae); coffee = Coffea Arabica L. (Rubiaceae); crepe myrtle = Lagerstroemia indica L. (Lythraceae); sapodilla = Manilkara zapota (L.) P. Royen (Sapotaceae); oleander = Nerium oleander L. (Apocynaceae); linden = Tilia americana L. (Malvaceae); Ohio buckeye = Aesculus glabra Willd. (Sapindaceae); walnut = Juglans regia L. (Juglandaceae); verawood = Bulnesia arborea Jacq. Engl. (Zygophyllaceae); Brazilian pepper · 331 ·

NOTES FOR APPENDIX A

· 332 ·

= Schinus terebinthifolius Raddi (Anacardiaceae); Copperpod = Peltophorum pterocarpum (DC) K. Heyne (Fabaceae); Amorphophallus = Amorphophallus paeonifolius (Dennst) Nicolson (Araceae); cinnamon = Cinnamomum aromaticum Nees (Lauraceae); black olive = Bucida buceras L. (Combretaceae); poison ivy = Rhus toxicodendron L. (Anacardiaceae); mango = Mangifera indica L. (Anacardiaceae); lucky nut = Thevetia peruviana (Pers.) Schumann (Apocynaceae); begonia = Begonia egregia N. E. Br. (Begoniaceae); Florida trema = Trema micanthum (L.) Blume (Ulmaceae); papaya = Carica papaya L. (Caricaceae); white oak = Quercus alba L. (Fagaceae); purple orchid tree = Bauhinia purpurea L. (Fabaceae); sweet gum = Liquidambar styraciflua L. (Hippocastanaceae); sassafras = Sassafras albidum (Nutt.) Nees (Lauraceae); castor bean = Ricinus communis L. (Euphorbiaceae); western alder = Alnus rubra Bong. (Betulaceae); Christmas berry = Lycium caroliniensis (Solanaceae); aechmea bromeliad = Aechmea sp. (Bromeliaceae); Indian pennywort = Centella asiatica (L.) Urb. (Apiaceae); bakuli = Mimusops elengii L. (Sapotaceae); allspice = Pimenta dioica (L.) Merr. (Myrtaceae); cocculus = Cocculus laurifolius DC (Menispermaceae); teak = Tectona grandis L. (Verbenaceae); Spanish stopper = Eugenia foetida Pers. (Myrtaceae); Peepal = Ficus religiosa L. (Moraceae; Madagascar olive = Noronhia emarginata Stadtm. (Oleaceae); tulip tree = Liriodendron tulipifera L. (Magnoliaceae); agave = Agave sp. (Agavaceae); white ironwood = Hypalete trifoliata Sw. (Sapindaceae); beautyberry = Callicarpa americana L. (Verbenaceae); mamey apple = Mammea americana L. (Clusiaceae); dombeya = Dombeya wallichi x ‘perrine’ (Lindl.) Benth. (Malvaceae); trembling aspen = Populus tremuloides Michaux (Salicaceae); Sagittaria = Sagittaria montevidensis Cham. & Schltdl. (Alismataceae); autograph tree = Clusea rosea Jacq. (Clusiaceae); rough velvet seed = Guettarda scabra (L.) Vent. (Rubiaceae); Hoffmania = Hoffmania refulgens (Hook.) Hemsl. (Rubiaceae); dotted wild coffee = Psychotria punctata Vatke (Rubiaceae); sagebrush = Artemisia tridentata Nutt. (Asteraceae); devil’s club = Oplopanax horridus (Sm.) Miq. (Araliaceae); stinging nettle = Urtica dioica L. (Urticaceae); black mangrove = Avicennia germinans (L.) L. (Verbenaceae); bay cedar = Suriana maritima L. (Surianaceae); iris = Iris sp. hybrid (Iridaceae); strangling fig = Ficus aurea Nutt. (Moraceae); short-leaf fig = Ficus citrifolia Mill. (Moraceae); foxtail palm = Wodyetia bifurcata Irvine (Arecaceae); white mangrove = Laguncularia racemosa (L.) Gaertn. f. (Combretaceae); poinciana = Delonix regia (Boj. ex Hook.) Raf. (Fabaceae); key lime = Citrus aurantiifolia (Christm.) Swingle (Rutaceae); cardboard zamia = Zamia furfuracea L.f. (Zamiaceae); blue-sky vine = Thunbergia grandiflora (Rottler) Roxb. (Verbenaceae); zedoary = Curcuma zedoaria (Christm.) Roscoe (Zingiberaceae); fern leaf tree = Filicium decipiens (Wight

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NOTES FOR APPENDIX A

& Arn.) Thw. (Sapindaceae); Anthurium hybrid = Anthurium sp. (Araceae); licuala palm = Licuala grandis H. Wendl. (Arecaceae); koa = Acacia koa A. Gray (Fabaceae); rubber tree = Ficus elastica Roxb. ex Hornem. (Moraceae); noni = Morinda citrifolia L. (Rubiaceae); bullhorn acacia = Vachellia cornigera (L.) Seigler & Ebinger; smilax = Smilax rotundifolia L. (Smilacaceae); breadfruit = Artocarpus altilis (Parkinson) Fosb. (Moraceae); tree spinach = Cnidosculus chayamansa McVaugh (Euphorbiaceae); maidenhair fern = Adiantum raddianum C. Presl. (Adiantaceae); Alexandrian laurel = Calophyllum inophyllum L. (Clusiaceae); Tibouchina = Tibouchina urvilleana Cogn. (Melastomataceae); purple orchid tree = Bauhinia purpurea L. (Fabaceae); peepal = Ficus religiosa L. (Moraceae); black bamboo = Gigantochloa atroviolacea Widjaja (Poaceae); velvet leaf Anthurium = Anthurium warocqueanum T. Moore (Araceae); Canada mayflower = Maienthemum canadensis Desf. (Asparagaceae); and banana = Musa acuminata Colla (Musaceae).

ap p e ndi x b: dry ing an d pr e se rvi ng l e av e s for cr af t pr oj e c t s

D

ried, or otherwise preserved, leaves make beautiful materials for handicraft projects, both for children and adults. This section provides instructions on how to preserve leaves and some suggestions about creative projects. Sources of materials, particularly websites, are provided at the end of the appendix.

Drying Leaves The key to drying flattened leaves is to dry them quickly at moderate temperature. This means not placing them within the pages of a book, where they will likely become moldy and discolored, but in a simple plant press. Such a plant press can be made from easily obtained materials (fig B.1). The materials consist of flat corrugated cardboard, thick blotting paper, newsprint, and thick cord or straps that can be tightened to keep the press together and put pressure on individual leaves. The cardboard can be obtained from shipping cartons or can be purchased as flat pieces from an art supply store. The blotting paper can also be purchased from the same store. The best newsprint is the normal paper where the news is actually printed and not the glossy advertising sheets. Straps that can be tightened can be purchased from a hardware store or a craft supply store such as Michael’s. If you are in a location where the market is too small for such specialty stores, these can be purchased on the Internet. The corrugated cardboard and blotting paper can be cut in the dimensions of 11.5 × 12 inches (use the approxi· 334 ·

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Figure B.1 Pressing and drying leaves. Center, a handmade press made by the author of corrugated cardboard, blotter paper, and newsprint. Left, a detail showing the corrugations all in the same direction to increase warm air passing through the specimens. Right, some examples of pressed and dried leaves.

mate dimensions of your local newspaper). Use two layers of cardboard for the outside of the press, with corrugations of each layer at 90 degree angles, to provide stiffness in all directions. For the inside of the press, the openings of the corrugations of the cardboard should be in the 12-inch direction of all pieces (those openings allow the flow of moist air and the rapid drying of leaves. Build up the layers of paper in the press, starting with blotting paper, then a double layer of newsprint with leaves placed inside, then blotting paper and a layer of cardboard. Repeat the process with more leaves to dry, and place a double layer of cardboard at the top (fig. B.1). Locate the press above a gentle source of heat, which can be a water heater, lightbulb, or an electrical appliance that provides some mild heating. Check within 24 hours. If the leaves are thick, it may be necessary to replace the blotting paper once or twice, until the leaves are completely dry. Once dry, they can then be stored in the newsprint, in a large flat envelope. Leaves, in their original three-dimensional positions on branches, can be dried in a granular medium that can be gently poured around them, such as silica gel, borax, or fine sand (available in a craft store). Silica gel is a chemically inert granular material that is used as a desiccant in a variety of industrial and commercial applications. It can be purchased from commercial suppliers with stores in large cities or on the Internet. Commercially available silica gel has a cobalt dye that is blue when dry and pink when hydrated. When hydrated, the gel can be regenerated by pouring it on a flat tray and heating it in an oven at 250°F for 2 hours. Cat litter consists of silica gel and clay, and can be used as an acceptable desiccant (look for the composition of materials on the packaging to be certain that silica gel

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is present). Place the branch in a large container and gently pour around it. Keep the container at room or slightly elevated temperature. It may be necessary, especially for thick leaves, to repeat this process with regenerated gel each day for several days.

Skeletonizing Leaves The soft living tissue of leaves can be removed to reveal their veins and other tough tissues. This makes it possible to see the delicate patterns of veins, and to use them in various craft projects. The most popular skeletonized leaves are from the sacred peepal trees of India, cleared and used for small religious paintings, and sold to pilgrims in India and in some Asian specialty shops in the United States and Europe (p. 213). There are several techniques for skeletonizing leaves, but I have chosen a method with the least caustic materials and most suitable for working with children under parental supervision. Collect the leaves for skeletonizing. The leaves should not be too leathery or tough, and use the more tender young leaves. Some leaves are too difficult to skeletonize, but some of the leaves where you live should work. Make a solution of baking soda in tap water (4 teaspoons of baking soda in 1 pint of water, or 20 grams in 500 ml of water). Place the leaves in the solution and heat gently, not allowing the solution to boil. Keep at this temperature for two hours; some leaves will require more time to be tenderized. Allow solution to cool and remove leaves from the solution. Put a single leaf on wet toweling on a flat dish. Use a serving knife with a smooth dull edge (not sharpened or serrated) and a brush (a soft toothbrush is ideal). Gently scrape the blade across the softened surface, removing the pulp of the leaf; turn the leaf over and repeat. Do the same with the brush. Every leaf type requires a slightly different technique. Wash the leaf gently under the faucet, rubbing gently on stubborn spots. Repeat until green or discolored tissue is removed to reveal the remaining tough veins. Once the leaf is clean, it can be immersed in bleach solution (1:10 dilution of commercial bleach, or sodium hypochlorite). Check on the leaf and remove after the leaf turns a whitish color. To bring out the vein patterns with more contrast, the skeletonized leaves can be colored with a commercial fabric dye using the instructions for cotton (remember, those veins are made up of cellulose just like the cotton fibers). You will find a good selection of dyes in a fabric store or large discount store. Dyed wet leaves can be dried

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Figure B.2 Clearing and skeletonizing leaves. Left, a shallow dish with leaves softened in the sodium carbonate solution, and in the process of losing their soft tissue. Center, leaves of the orchid tree, both cleared and skeletonized. Right, a portion of a skeletonized peepal leaf.

and flattened using the plant press. Use plastic gloves with the bleach and dye solutions. I skeletonized leaves of a pink orchid tree (fig. B.2).

Clearing Leaves If you fill the air spaces between interior cells of a leaf and remove the pigments, the leaf becomes translucent and the finest veins are visible, more so than for the skeletonized leaves where the finest veins are lost in the processing. For the documentation and study of veins, various procedures for clearing leaves have been developed. However, most involve the use of caustic and toxic solutions, and will not be described here. The tissue is softened, bleached, and stained to reveal the veins, with chemicals that bind exclusively to the lignin associated with the veins. Then the leaf is infiltrated with a solvent or solution with about the same refractive index as the tissue, so that the leaf is highly transparent. Leaves infiltrated with water or alcohol are also highly transparent. To clear leaves, use the same initial technique as for skeletonizing, making sure not to “cook” them too long. Remove the softened leaves, rinse with water, and then place the leaves in the 1:10 bleach solution as for skeletonizing. Visual inspection will reveal if the bleaching has proceeded adequately. Use tweezers to remove leaves from the bleach solution, and wash them in tap water. Be careful working with the bleach solution, as any

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contact with your clothes will produce white bleached spots; use of plastic gloves is important. Soaking in water, the bleached leaves should be fairly transparent, but the veins will not be very visible. They must be stained with a dye specific for lignin, otherwise the entire leaf will be dyed. For that, use the biological stain, Safranin O, which is available from biological supply companies (see information at the end of this appendix). Make a solution of 0.5 g of dye powder in 200 ml of denatured alcohol. This solvent can be purchased at a hardware or paint store, or in the paint department of Home Depot or Lowe’s. This is ethanol diluted with some methanol. The methanol is very toxic to drink, but the solvent is relatively safe to use in a well-ventilated area. Place the leaf in the dye solution in a shallow container (flat Tupperware is ideal). Leave it in the solution 30 minutes or more, depending upon the leaf. Remove the dyed leaf from the container, allowing excess dye to drip from the leaf back into the container. Place in a clean denatured alcohol solution, and repeat this process until the solution is barely pink. You should be able to see the veins as pink to light red on a clear background (fig. B.2). If commercial dye is used, the veins are dyed, but so also is the rest of the tissue. Cleared leaves can be kept in a ziplock bag for some time. Cleared leaves can also be dried in a plant press. They are relatively transparent and thin, like cellophane. They can also be embedded in plastic; acrylic would be the safest for use with older children. If left in water indefinitely, the leaves will decay but will be preserved in the denatured alcohol. Depending on the embedding process, leaves may soaked in water or alcohol.

Projects with Preserved Leaves Your imagination is the limit for how such leaves can be used in craft projects. Fresh leaves can be rolled or sponged with printing ink, and pressed against paper to produce an impression of the leaf with major veins and the outline highlighted. Dried leaves can be glued to sheets intact, or cut into shapes and glued onto sheets. Skeletonized leaves can also be glued onto sheets. Branches with attached leaves can be used in permanent dried arrangements, perhaps including flowers. Cleared or skeletonized leaves can be embedded in plastic. Leaves can be spray- painted in colors or metallic coatings. These can also be glued to sheets in pleasing arrangements.

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Supplies and Instructions There are quite a few websites with suggestions on using leaves in craft projects. Explore leaf crafts (http://www.pinterest.com/explore/leaf-crafts) “How to Preserve Flowers with Glycerine” (www.ehow.com/how_5456 _preserve-flowers-with.html); lovely leaf crafts for children (www.parents .com/fun/arts -crafts/kid/lovely -leaf -crafts -for -kids); and the National Gardening Association (garden.org) are among the best. For pressing leaves, I have provided instructions for making a simple plant press for little cost. Prepared plant presses can be purchased. Inexpensive presses are available in different sizes from Nature’s Pressed Flowers (https://www.naturespressed.com/) and traditionally constructed presses with hardwood frames from Carolina Biological Supply (www .carolina.com/) and (www.onlinesciencemall.com/). For drying branches with leaves on them, to preserve the three-dimensional organization, see “How to Dry Leaves with Silica Gel” (www.ehow.com/how_2040860_dry -flowers-silica-gel.html) and ways to dry flowers (www.wikihow.com/Dry -Flowers). For skeletonizing leaves, there are a number of Internet sites that describe the methods I have provided, but nothing different. For skeletonizing and clearing leaves, I recommend the excellent site prepared by Ben Blonder (http://benjaminblonder.org/The_secrets_of_leaves/) Bonder includes the PDF of a good unpublished article on clearing leaves by Walter Buehler, “Alternative Leaf Clearing and Mounting Procedures.” The authoritative method on clearing leaves is included in Beth Ellis et al., Manual of Leaf Architecture (Ithaca, NY: Cornell University Press, 2009), available as a link from the Blonder website. Safranin O is a more readily available stain for veins, sold by Carolina Biological, cited above.

ap p e ndi x c : le ave s f or s c ho ol s c i e nc e l a b s and p r oj e c t s

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here are many advantages for using plants in labs and projects. Since they are not animals, particularly without backbones, no special permission is needed to work on them. Although various plant structures can be studied— for example, branching and architecture, flowering, fruiting, rooting, and so on— no structures are more convenient than leaves. Leaves respond to inheritance and the environment in easily measured ways. Leaves can be studied with varying degrees of sophistication, useful for elementary science exercises and for high school students as well. Here, I describe a variety of projects using leaves and cite the pages in this book that discuss the particular structures and responses. Then I describe the minimal equipment necessary to study leaves, and suggest some inexpensive sources of equipment.

A List of Potential Projects and Exercises

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Phenology: When leaves are produced and when they fall from plants (p. 70). The observations are simply made, but need several years to begin to have any meaning. This is a good school project where students can observe the leaf changes in trees on the school campus, or children in a family can observe leaf changes in their neighborhood. The resources of the National Phenology Network (https://www .usanpn.org/) will help.

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Fluctuating asymmetry: Under stress new leaves are produced that are asymmetrical. The asymmetry is a consequence of abnormalities in the shoot apical meristems as the leaves begin to develop (p. 163). The degree of asymmetry can be assessed by comparing the areas of the two sides of a given leaf. Plants under experimental stress (such as drought) might produce more asymmetrical leaves. For growing seedlings, you can choose the stress and look for changes in leaf symmetry. Herbivory: The amount of herbivory on a leaf can be assessed by a reduction in area after the maximum leaf size has been reached (p. 238). The type of herbivory, from leaf edge or by eating holes in the middle of the leaf, can be measured. Leaf size: Various environmental factors may affect the maximum leaf size in a particular plant (p. 120). Comparing leaf size, or even length, in plants experimentally grown in different degrees of shade, or differing amounts of water, can easily be completed. Leaf lobes: In plants producing lobed leaves, the degree of lobiness can vary in plants grown in different conditions (p. 162). The degree of lobing can be assessed by drawing a line between the tips of adjacent lobes, and then measuring distance from this line to the base of the sinus. Leaf mass/area: Growth conditions affect the leaf mass/area ratios among different plants, or differing leaves within a plant (p. 62). These estimates require the measurements of both the mass of the leaf blade and its area. Leaf anatomical structure: Both the physical environment or growing conditions can influence the anatomical structure of leaves (p. 62). Plants vary in their capacity to change anatomy during leaf development. Anatomical changes are also reflected in the total thickness of the leaf. Stomatal distribution and density: Stomata are crucial for controlling the intake of carbon dioxide and loss of water vapor from leaves, thus they control the physiological processes in a leaf (pp. 185, 62). Simple techniques allow for the determination of both distribution and density on the leaf surface.

The techniques for pursuing these projects are not too complicated or very expensive. They are described in the following paragraphs.

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Measuring Leaf Mass Advances in technology have led to the introduction of digital scales that are relatively inexpensive, some of which may be used in cooking. Since leaves are relatively light, you need a scale with an accuracy of at least 0.01 g. Measuring leaf mass allows you to determine the percentage dry weight of a leaf and, along with estimating leaf area, to determine the leaf mass per area. Several small portable scales, with accuracy to 0.001 g, are available for less than $25. In using such scales, plastic weighing “boats” are helpful to keep the leaves from touching the non-weighing parts of the scale, and placing the scale in a protected area, such as in a plastic container, protects against air movements that reduce the accuracy in weighing leaves.

Leaf Area Measurements Copy machines or flatbed scanners provide a relatively simple means of measuring the areas of leaves. Scan the leaves and print an image. Make sure the size you print is that of the original by using a ruler as a scale; if the scale on the printed image and the original scale are the same size, you know that the image is correct. Scan a square piece of the same copy paper of a predetermined size, leaving the line marks at the outside as a border to give you an outside boundary. Weigh that paper on the balance to give the relationship between mass and paper area. Then, cut out the leaves that you have scanned and weigh them in the balance. Then it is easy to calculate the area of each leaf. By measuring the mass of the leaf, fresh or dried, and then determining the area, it is also easy to determining the mass, as mg/cm2, of the leaf either fresh or dried. If the thickness of the leaf has been measured, as through microscope observations described below, other leaf characteristics can be determined. Mass per unit leaf volume can be calculated with the fresh leaves. Furthermore, if the fresh leaves are soaked for a couple of days in water, they become translucent from the replacement of the interior air spaces by water. Remove the leaf from the water, gently removing surface moisture with soft toweling. Then weigh the leaf again. The difference in mass between the fresh and soaked leaf is the volume of air spaces within the leaf, as 1 g of water mass is equivalent to 1 cm3 of water volume.

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Microscopic Observations The digital revolution has also produced a new generation of microscopes. These can be used as dissecting scopes, observing the sample from above, or as transmission light microscopes, by passing light through a thinly sectioned sample and into the lens of the scope. Rather than using a compound microscope, it is now feasible to use a high-powered lens that directly connects to a computer via a USB cable, or to attach a special lens to a smartphone, such as an iPhone 5 or 6. To examine leaf transverse sections, so as to determine the thickness of leaves, you need magnifications of 100– 200 times, easily achieved by these devices. A stumbling block in microscopy is determining the actual magnification of the image. For a compound microscope, special rulers and stage micrometers provide a scale in the microscope image. These rulers are quite expensive, however. The most accurate measurement for these purposes is a plastic vernier caliper; these can be purchased for less than $5 and provide accuracy to 0.01 mm. You can determine the width of your field by adjusting the calipers. Then you can calculate the size of any object in your image.

Techniques in Preparing Samples for the Microscope You need some simple supplies for preparing specimens. Microscope specimen kits are available in educational stores or on Amazon that provide slides and cover slips, a water dropper bottle, stain, and forceps. I recommend the purchase of fine steel jeweler’s forceps for $2–$5 and possibly a bottle of toluidine blue to stain the tissue a bit. Most digital microscopes have a built-in LED lamp to illuminate the surface under observation. Cutting across a leaf exposes its thickness, and a digital microscope will permit the measurement of thickness in microns (or 0.001 mm increments). A typical leaf will be 300–400 microns thick. Using a digital microscope or smartphone microscope to image the cells exposed in a transverse cut requires that the sections be thin, and that the illumination passes through the specimen. Starting with sectioning, I recommend one of two hand-sectioning techniques. The first employs double-edged razor blades, like those used in a barber shop, which can be purchased at a drugstore. This needs to be done with adult supervision because the razor blades are very sharp. Snap the blade in two, so that the two edges are exactly adjacent and parallel to each other. Use transparent

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tape to hold the edges together. Place a small piece of the leaf, about 5 mm square, onto a plastic surface, like a jeweler’s box or Tupperware lid. Add a drop or two of water to keep the sample wet. Press the edges of the razor blade down on the leaf surface, making contact with the plastic. The distance between the adjacent edges produces a leaf section of about the right thickness. Try this several times, and use the fine forceps to lift sections onto a drop of water on the microscope slide. Alternatively, use a singleedge razor blade, such as one purchased inexpensively in the paint department of a hardware store. Obtain a sheet of soft flexible plastic; cutting up a ziplock bag will work well. Place the leaf sample in a drop of water on the plastic surface, as in the first method. Cover the sample with a square of the plastic sheet. It makes contact with the sample and water droplet, helping to keep the sample in place. Gently cut parallel strips across the sample, through the plastic sheet and making slight contact with the plastic surface underneath. Make dozens of cuts, as close together as possible. Then, lift up the plastic sheet, remove the thinnest cuts with the jeweler’s forceps, and place them in the water droplet on the microscope slide (fig. C1). Cover the samples with a cover slip by placing one edge adjacent to the water droplet and sections, and gently drop the cover slip from that side and across. Place the sample on top of the illumination, as a small LED illumination box, and focus the

Figure C.1 A simple technique for producing hand sections of leaves. Left, the materials assembled: plastic dish, plastic film, single-edge razor blade, fine-tipped forceps, stage micrometer (ruler), microscope slide, and cover slip. Right, a hand section of a red maple leaf produced by this technique, showing the location of anthocyanins and the midrib vein.

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microscope or smartphone from above it. You should see a sample that looks like fig. C1, showing the upper and lower epidermal layers, as well as the photosynthetic cells within, with the long palisade cells near the surface and the irregular spongy mesophyll cells beneath. Stomates can be observed in two ways. By carefully cutting parallel to the leaf undersurface, a small translucent area is produced. That can be quickly placed in the water droplet on a microscope slide, revealing the epidermal cells interspersed with guard cells and stomates. Alternatively, using a dry but fresh leaf, coat an area of the undersurface with clear nail polish. Let the polish dry and, using the jeweler’s forceps, carefully work the layer free by gently lifting from one edge. Place the transparent nail polish layer on a water droplet centered in a microscope slide and cover with a cover slip as described above. The nail polish makes a detailed impression of the stomata and epidermal cells, although you may need to alter the light position to see it best. With such impressions you can measure the size of stomata as well as the density of their distribution.

Supplies There are many websites specializing in microscopes and accessories, but most are rather expensive. By far the best source of instruments and supplies for these experiments is Amazon.com. There you can find a precision portable battery-operated jeweler’s balance, and a variety of digital microscopes and smartphone lens attachments. There you can also purchase vernier calipers, jeweler’s forceps, and microscope supplies— all at very reasonable prices. There are numerous Internet sites demonstrating how to turn an iPhone or a smartphone into a microscope, and inexpensive attachments available on Amazon.com.

chap te r n ot e s For brevity’s sake, I have altered articles citations in these notes in two ways. First, I have provided author names when there are no more than five co-authors, and used only the first author name with six or more co-authors. Second, I have abbreviated journal title names for those cited frequently in the notes: AER = Advances in Ecological Research; AJB = American Journal of Botany; AN = American Naturalist; APR = Annual Plant Reviews; AREES = Annual Review of Ecology Evolution and Systematics; ARES = Annual Review of Ecology and Systematics; ARPB = Annual Review of Plant Biology; ARPP = Annual Review of Plant Physiology; ARPPPMB = Annual Review of Plant Physiology and Plant Molecular Biology; BG = Biogeosciences; BiolJLS = Biological Journal of the Linnean Society; BotJLS = Botanical Journal of the Linnean Society; BR = Botanical Review; CB = Current Biology; CJB = Canadian Journal of Botany; COPB = Current Opinion in Plant Biology; DB = Developmental Biology; EB = Economic Botany; EL = Ecological Letters; EM = Ecological Monographs; ENVB = Environment & Behavior; ER = Ecological Research; FE = Functional Ecology; FHN = Frontiers in Human Neuroscience; FPB = Functional Plant Biology; GCB = Global Change Biology; GEB = Global Ecology and Biogeography; IJPS = International Journal of Plant Science; JAE = Journal of Applied Ecology; JE = Journal of Ecology; JEB = Journal of Experimental Botany; JEP = Journal of Environmental Psychology; JEVB = Journal of Evolutionary Biology; JHB = Journal of the History of Biology; JM = Journal of Morphology; JRSI = Journal of the Royal Society Interface; JTB = Journal of Theoretical Biology; JTE = Journal of Tropical Ecology; NP = New Phytologist; NYT = New York Times; PC = Plant Cell; PCE = Plant Cell and Environment; PCP = Plant Cell Physiology; PE = Plant Ecology; PNAS = Proceedings of the National Academy of Sciences U.S.; PP = Plant Physiology; PPl = Physiologia Plantarum; PR = Photosynthesis Research; PRE = Physical Review E; PRL = Physical Review Letters; PRSB = Proceedings of the Royal Society of London B, Biological Sciences; PSE = Plant Systematics and Evolution; PTRSA = Philosophical Transactions of the Royal Society of London A, Physical Sciences; PTRSB = Philosophical Transactions of the Royal Society of London B, Biological Sciences; TP = Tree Physiology; TPS = Trends in Plant Science; TREE = Trends in Ecology & Evolution · 347 ·

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David Mabberley’s Mabberley’s Plant Book, 3rd ed. (Cambridge: Cambridge University Press 2008), was particularly helpful in checking names, authorities, and terminology.

Preface The quote at the beginning of the chapter is from Dana Gioia, Interrogations at Noon (St. Paul, MN: Greywolf Press, 2001). Baba Dioum’s original publication of his famous quote seems lost in history, although it is quoted on innumerable websites.

Chapter One: Green Men For the quotations at the beginning of the chapter, see William Anderson, Green Man: The Archetype of Our Oneness with the Earth (London: HarperCollins, 1990); and Alexander von Humboldt, Aspects of Nature in Different Lands and Different Climates with Scientific Elucidations (Philadelphia: Lea and Blanchard, 1850). The excellent book by Anderson also provided much information on the history of the green man, with many good photographs.

For information about St. John’s College, the Canterbury Quadrangle, and William Laud, I used Howard Colvin, The Canterbury Quadrangle (Oxford: Oxford University Press, 1988). For information about J. R. R. Tolkien, I consulted Joseph Pearce, Tolkien: Man and Myth (London: HarperCollins, 1998), including his friendship with C. S. Lewis. For information about Tolkien and Oxford as well as locations of green men, consult the website www.bejo.co.uk/greenmantrail/html /tradition.html. For the Gundestrup Cauldron, I looked at the work by Anderson, above, as well as Hilda Ellis Davidson, The Lost Beliefs of Northern Europe (New York: Routledge, 2007). For Harald Bluetooth, I consulted Anderson, and the Wikipedia article at https://en.wikipedia.org/wiki/Harald_Bluetooth. I also used information from Wikipedia for Gilgamesh: https://en.wikipedia.org/wiki/Epic_of_Gilgamesh including text of tablets, and general information from W. S. Merwin, cited next. I quoted from the modern English translation of the Middle English poem Sir Gawain and the Green Knight by Merwin; his lengthy introduction was very helpful: Sir Gawain and the Green Knight, translated by W. S. Merwin (New York: Knopf, 2002). Anderson’s book also provided some information on this epic poem, including the location of the Green Chapel. For Norse mythology, including Yggdrasil, I consulted Davidson, above. The story of mistletoe on the oak gave Sir James Frazer’s book its title: The New Golden Bough (Garden City, NY: Anchor Books, 1961)— a new abridgment of the classic work, edited and with notes and foreword by Theodor H. Gaster. The excerpt from Virgil was The Aeneid, trans. Robert Fagles (New York: Viking, 2010). For Indo-European language and Proto-Indo-European (PIE) culture, I consulted the following works: J. P. Mallory and D. Q. Adams, The Oxford Introduction to Proto-Indo-European and the Proto- Indo-European World (Oxford: Oxford University Press, 2006); Thomas V. Gamkrelidze and Vjacˇeslav V. Ivanov, Indo-European and the Indo-Europeans: I. A Reconstruction and Historical Analysis of a Proto-Language and a Proto-

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Culture: Part I: The Text (New York: Mouton de Gruyter, 1995); and Paul Friedrich. Proto-Indo-European Trees: The Arboreal System of a Prehistoric People (Chicago: University of Chicago Press, 1970). Friedrich is acknowledged for his pioneering research on trees and linguistics. Four articles were helpful in assessing the origin and migration of the Indo-Europeans and their languages: R. D. Gray and Q. Atkinson, “Language-Tree Divergence Times Support the Anatolian Theory of IndoEuropean Origins,” Nature 426 (2003): 435–39; J. Adams and M. Otte, “Did Indo-European Languages Spread before Farming?” Current Anthropology 40 (1999): 73–77; Wolfgang Haak et al., “Massive Migration from the Steppe Was a Source for Indo-European Languages in Europe,” Nature 522 (2015): 207–11; and Will Chang, Chundra Cathcart, David Hall, and Andrew Garrett. “Ancestry-Constrained Analysis Supports the Indo- European Steppe Hypothesis,” Language 91, no. 1 (2015): 194–244. Information on Al-Khidr was obtained from The Encyclopedia of Islam, vol. 5 (Leiden: E. J. Brill), http://www.Khidr.org/encyclopedia.islam.khidr.htm. For a description of the leaf decorations of Ur, see M. Tengberg, D. T. Potts, and H.-P. Francfort, “The Golden Leaves of Ur,” Antiquity 82 (2008): 925–36. I consulted Richard E. Blackwelder, A Tolkien Thesaurus (New York: Garland, 1990), to find quotes in Tolkien’s works, and the quote about Treebeard and the Ents is from J. R. R. Tolkien, The Two Towers (Boston: Houghton Mifflin, 1954). For my coverage on leaves with special sacred significance, see the following. For date palms and Sukkot: Jennifer Medina, “Holiday Near, Time Again to Track Down Perfect Fronds,” NYT, October 7, 2011, A13; for Egyptian plants: F. N. Hepper. Pharaoh’s Flowers: The Botanical Treasures of Tutankhamen (London: Her Majesty’s Stationery Office, 1990); for Greek plants: Helmutt Baumann, The Greek Plant World in Myth, Art and Literature (Portland, OR: Timber Press, 1993). For general natural history of the old world, see Roger French, Ancient Natural History: Histories of Nature (London: Routledge, 1994). Theophrastus’s description of Indian plants is in his own writings: Theophrastus, Enquiry into Plants, trans. Sir Arthur Hort (New York: G. P. Putnam’s Sons, 1906), book IV: 309–23; and is also summarized by French above, and by J. D. Hughes, “Early Ecological Knowledge of India from Alexander and Aristotle to Aelian,” in Nature and the Orient: The Environmental History of South and Southeast Asia, ed. R. H. Grove, V. Damodaran, and S. Sangwan (Delhi: Oxford University Press, 1998), 70–86. For the names and uses of Malaysian plants, I consulted I. H. Burkhill, A Dictionary of the Economic Products of the Malay Peninsula, vols. 1 and 2 (Kuala Lumpur: Minister of Agriculture and Cooperatives, Governments of Malaysia and Singapore, 1966). The classical decline of forests is well described in John Perlin, A Forest Journey: The Story of Wood and Civilization (Cambridge, MA: Harvard University Press, 1989); Robert Pogue Harrison, Forests: The Shadow of Civilization (Chicago: University of Chicago Press, 1992); and George Perkins Marsh, Man and Nature (Seattle: University of Washington Press, 2003), from the original edition of 1864, annotated and edited in 1965 by Harvard University Press. Harrison revealed the derivation of the word “forest” and the control of forests by royalty.

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For a fresh insight on the meaning of the Garden of Eden, read Robert Pogue Harrison, Gardens: An Essay on the Human Condition (Chicago: University of Chicago Press, 2008); and David Rosenberg, The Lost Book of Paradise (New York: Hyperion, 1993). For a review of Alexander von Humboldt’s life, I consulted the illustrated biography by Douglas Botting, Humboldt and the Cosmos (New York: Harper and Row, 1973); for the insightful essays on his voyage and its aftermath, see Michael Dettelbach, in Felix Driver and Luciana Martins, eds., Tropical Visions in an Age of Empire (Chicago: University of Chicago Press, 2010); Alexander Von Humboldt and Aimé Bonpland, Essay on the Geography of Plants, ed. Stephen T. Jackson and trans. Sylvie Romanowski (Chicago: University of Chicago Press, 2009). Humboldt’s writing in Aspects of Nature, already cited, is important as is his last book: Cosmos: A Sketch of the Physical Description of the Universe, vol. 2 (Baltimore: Johns Hopkins University Press, 2009), with an insightful essay by Michael Dettelbach. Many of the painters influenced by Humboldt are mentioned by name in The Cosmos. For a look at Frederic Church and his connection to Humboldt and to other painters, see Franklin Kelly, ed., Frederic Edwin Church (Washington, DC: National Gallery of Art, 1989). An essay by Stephen Jay Gould is particularly relevant. I had read some general books on world fairs and consulted some of the collections of the Wolfsonian Art Museum at Florida International University, Miami Beach. The colonial influences and the “human zoos” incorporated in some expositions are well covered by Bob Mullan and Marvin Garry, Zoo Culture: The Book about Watching People Watch Animals, 2nd ed. (Urbana: University of Illinois Press, 1998); and Sadiah Qureshi, Peoples on Parade: Exhibitions, Empire, and Anthropology in NineteenthCentury Britain (Chicago: University of Chicago Press, 2011). For the influence on landscapes in south Florida, the Florida theme issue of the Journal of Decorative and Propaganda Arts 23 (1998) is useful, particularly the article “Perfumes, Postcards, and Promises: The Orange in Art and Industry,” by Helen L. Kohen. Lastly, and most recently, Christian A. Larson, Philodendron: From Pan- Latin Exotic to American Modern (Miami: The Wolfsonian, 2015). The scientific names of plants, in order of appearance in the chapter: English oak = Quercus robur L. (Fagaceae); European ash = Fraxinus excelsior L. (Oleaceae); mistletoe = Viscum album L. (Santalaceae); barley = Avena sativa L. (Poaceae); apple = Malus pumila Mill. (Rosaceae); filbert = Corylus avellana L. (Betulaceae); linden = Tilia cordata Mill. (Malvaceae); hornbeam = Carpinus betulus L. (Betulaceae); beech = Fagus sylvatica L. (Fagaceae); cherry = Prunus avium (L.) L. (Rosaceae); yew = Taxus baccata L. (Taxaceae); rowan = Sorbus acuparia L. (Rosaceae); holly = Ilex aquifolium L. (Aquifoliaceae); laurel = Laurus nobilis L. (Lauraceae); olive = Olea europaea L. (Oleaceae); acanthus = Acanthus spinosus L. (Acanthaceae); bilva, bael = Aegle marmelos (L.) Corr. Serr. (Rutaceae); palasa = Butea monosperma (Lam.) Kuntze (Fabaceae); clover, shamrock = Trifolium dubium Sibth. (Fabaceae); bodhi, peepul = Ficus religiosa L. (Moraceae); banyan = Ficus benghalensis L. (Moraceae); date palm = Phoenix dactylifera L. (Arecaceae); rosewood, shisham = Dalbergia sissoo Roxb. ex DC (Fabaceae); citron

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= Citrus medica L. (Rutaceae); lotus = Nelumbo nucifera Gaertn. (Nelumbonaceae); peacock fern, paku merah = Selaginella willdenowii (Desv.) Bak. (Selaginellaceae); akar sĕrau malam = Phyllagathis rotundifolia (Jack) Blume (Melatomataceae); jak fruit = Artocarpus heterophyllus Lam. (Moraceae); cotton = Gossypium arboreum L. (Malvaceae); banana = Musa acuminata Colla (Musaceae); ebeny = Diospyros ebenum Koenig. ex Retz. (Ebenaceae); terebinth = Pistacia terebinthus L. (Anacardiaceae); rice = Oryza sativa L. (Poaceae); pepper = Piper nigrum L. (Piperaceae); cloves = Syzygium aromaticum (L.) Merr. & Perry (Myrtaceae); pineapple = Ananas comosus L. (Bromeliaceae).

Chapter Two: Leaf History The quote at the beginning of the chapter is from Erasmus Darwin, The Temple of Nature (London: J. Johnson, St. Paul’s Churchyard, 1803), and the second is by Robert Hass from “State of the Planet,” from his book Time and Materials: Poems, 1997– 2005 (New York: Ecco Press, 2007). For a poetic view of the origin of the universe and life, I recommend Brian Thomas Swimme and Mary Evelyn Tucker, Journey of the Universe (New Haven, CT: Yale University Press, 2012). The quote from Steven Weinberg is from “Anthropic Bound on the Cosmological Constant,” PRL 59 (1987): 2607– 10. The age of the universe is based on a Wikipedia article (https://en.wikipedia.org/wiki/Age_of_the_universe) that cites N. Jarosik et al., “Seven- Year Wilkinson Microwave Anisotropy Probe (WMAP) Observations: Sky Maps, Systematic Errors, and Basic Results,” Astrophysical Journal Supplement Series 192 (2011): 14. The age of Earth is based on a review article by G. Brent Dalrymple, “The Age of the Earth in the Twentieth Century: A Problem (Mostly) Solved,” Special Publications, Geological Society of London 190 (2001): 205– 21. For the quote on the emergence of properties in the evolution of life, see Stuart Kaufmann, At Home in the Universe: The Search for the Laws of Self-Organization and Complexity (New York: Oxford University Press, 1996); and a discussion of emergence by Massimo Pigliucci, “Between Holism and Reductionism: A Philosophical Primer on Emergence,” BiolJLS 112 (2014): 261–67.

For the early history of life and the likely types of metabolisms, see Michael M. Tice and Donald R. Lowe, “Hydrogen-Based Carbon Fixation in the Earliest Known Photosynthetic Organisms,” Geology 34 (2006): 37–40; Abigail C. Allwood, Malcolm R. Walter, Balz S. Kamber, Craig P. Marshall, and Ian W. Burch, “Stromatolite Reef from the Early Archaean Era of Australia,” Nature 441 (2006): 714– 18; David Wacey, Matt R. Kilburn, Martin Saunders, John Cliff, and Martin D. Brasier, “Microfossils of Sulphur- Metabolizing Cells in 3.4- Billion- Year- Old Rocks of Western Australia,” Nature Geoscience 4 (2011): 698– 702; Emanuelle J. Javaux, Craig P. Marshall, and Andrey Bekker, “Organic- Walled Microfossils in 3.2-Billion-Year-Old Shallow-Marine Siliciclastic Deposits,” Nature 463 (2010): 714–18; Nicolas Beukes, “Early Options in Photosynthesis,” Nature 431 (2004): 522–23; Michael M. Tice and Donald R. Lowe, “Photosynthetic Microbial Mats in the 3,416-MYR-Old Ocean,” Nature 431 (2004): 549–52; Pascal Philippot, Mark Van Zuilen, Kevin Lepot, Christophe Thomazo, James Farquhar, and Martin J. Van Kranendonk, “Early Archaean Microorganisms Preferred Elemental Sulfur, Not

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Sulfate,” Science 317 (2012): 1534–37. Any general biology textbook will provide a good overview. For the endosymbiont hypothesis, see any biology text, and the solid review of the history of the idea in Wikipedia (https://en.wikipedia.org/wiki /Symbiogenesis). For a description of the domains and kingdoms of life, and the evolutionary tree, consult a modern biology text. Again, for a discussion of the adaptations of plants to the land surface, consult that biology book. Recent evidence for the appearance of the first multicellular organisms: Shixing Zhy et al., “Decimetre-Scale Multicellular Eukaryotes from the 1.56- billion-year-old Gaoyuzhuang Formation in North China,” Nature Communications 7 (2016): 11500. For details on the timing and types of plants first present on land, see Thomas N. Taylor, Edith L. Taylor, and Michael Krings, Paleobotany. The Biology and Evolution of Fossil Plants, 2nd ed. (Burlington, MA: Academic Press, 2009); and Timothy M. Lenton et al., “Earliest Land Plants Created Modern Levels of Atmospheric Oxygen,” PNAS 113 (2016), doi:10.1073/pnas.1604787113. For Cooksonia, see D. Edwards, K. I. Davies, and I. Axe, “Vascular Conducting Strand in the Early Land Plant Cooksonia,” Nature 357 (1992): 583–685. An excellent book on the early evolution of land plants and subsequent events is David Beerling, The Emerald Planet: How Plants Changed Earth’s History (Oxford: Oxford University Press, 2007). I summarize some of his arguments here and stress that Beerling is an author, or coauthor, of some of the seminal research papers in this field— which are used in my discussion: D. J. Beerling, C. P. Osborne, and W. G. Chaloner, “Evolution of Leaf-Form in Land Plants Linked to Atmospheric CO2 Decline in the Late Palaeozoic Era,” Nature 410 (2001): 352–54; C. P. Osborne, D. J. Beerling, B. H. Lomax, and W. G. Chaloner, “Biophysical Constraints on the Origin of Leaves Inferred from the Fossil Record,” PNAS 101 (2004): 10360–62. For evidence of the early carbon dioxide record, see C. I. Mora, S. G. Driese, and L. A. Colarusso, “Middle to Late Paleozoic Atmospheric CO2 Levels from Soil Carbonate and Organic Matter,” Science 271 (1996): 1105–7; and D. D. Ekart, T. E. Cerling, I. P. Montanez, and N. J. Tabor, “A 400 Million Year Carbon Istotope Record of Pedogenic Carbonate: Implications for Paleoatmospheric Carbon Dioxide,” American Journal of Science 299 (1999): 805–27. For background on the earliest leaves, see books by Beerling and by Taylor, Taylor, and Krings, both cited above, as well as H. Shougangb, C. B. Beck, and W. Deming, “Structure of the Earliest Leaves: Adaptations to High Concentrations of Atmospheric CO2,” IJPS 164 (2003): 71–75. For early land plants and leaves, see the monograph by Taylor, Taylor, and Krings, cited above; P. G. Gensel, H. N. Andrews, and W. H. Forbes, “A New Species of Sawdonia with Notes on the Origin of Microphylls and Lateral Sporangia,” Botanical Gazette 136 (1975): 50–62; and Diane Edwards, “Xylem in Early Tracheophytes,” PCE 26 (2009): 57–72. For the Gilboa forests, see W. E. Stein, F. Mannolini, L. V.- A. Hernick, E. Landing, and C. M. Berry, “Giant Cladoxylopsid Trees Resolve the Enigma of the

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Earth’s Earliest Forest Stumps at Gilboa,” Nature 446 (2007): 904–7; and W. E. Stein, C. M. Berry, L. V. Hernick, and F. Mannolini, “Surprisingly Complex Community Discovered in the Mid- Devonian Fossil Forest at Gilboa,” Nature 483 (2012): 78–82. For forests in general, see S. E. Schekler, “Afforestation— the First Forests,” in Palaeobiology II, ed. Derek E. G. Briggs and Peter R. Crowther, 67–71 (Oxford: Blackwell Science Ltd., 2001). For the evolution of megaphylls, see books by Beerling and by Taylor, Taylor, and Krings et al., both cited above; and Jean Galtier, “The Origins and Early Evolution of the Megaphyllous Leaf,” IJPS 171 (2010): 641–61. The importance of forest formation in climate regulation is described by Thomas J. Algeo and Stephen E. Scheckler, “Terrestrial- Marine Teleconnections in the Devonian: Links between the Evolution of Land Plants, Weathering Processes, and Marine Anoxic Events,” PTRSB 353 (1998): 113–30; Benjamin Blonder, Dana L. Royer, Kirk R. Johnson, Ian Miller, and Brian J. Enquist, “Plant Ecological Strategies Shift Across the Cretaceous-Paleogene Boundary,” PLOS Biology 12 (2014), doi:10.1371/journal.pbio.1001949. For the most recent estimate of the origin of flowering plants, see Susana Magallón, Sandra Gómez-Acevedo, Luna L. Sánchez-Reyes, and Tania Hernández-Hernández, “A Metacalibrated Time-Tree Documents the Early Rise of Flowering Plant Phylogenetic Diversity,” NP 207 (2015): 437–53. General descriptions of leaf structure will be found in a general botany or biology text, and are also summarized in the book by Taylor, Taylor, and Krings, cited above. The best discussion of the differences between plants and animals is by Francis Hallé, In Praise of Plants (Portland, OR: Timber Press, 2001). The description of the digestive processes of the Burmese python is from S. M. Secor and J. Diamond, “A Vertebrate Model of Extreme Physiological Regulation,” Nature 395 (1998): 659–62. The assimilation efficiencies of digestion were given in Ellen S. Dierenfeld, Heather L. Alcorn, and Krista L. Jacobsen, “Nutrient Composition of Whole Vertebrate Prey (Excluding Fish) Fed in Zoos,” www.naturalpetproductions.net /articles/npp.wholepreymodel.pdf, May 29, 2002. For a detailed description of the symbiosis between zooxanthellae and corals, see S. A. Wooldridge, “Is the Coral- Algae Symbiosis Really ‘Mutually Beneficial’ for the Partners?” BioEssays 32 (2010): 615–25. For the symbiosis between algae and tiger salamander eggs, see R. Kerneva, E. Kim, R. P. Hangarter, A. A. Heiss, C. D. Bishop, and B. K. Hall, “Intracellular Invasion of Green Algae in a Salamander Host,” PNAS 108 (2012): 6407–2. For the sea slug/algal chloroplast symbiosis, see M. E. Rumpho et al., “Horizontal Gene Transfer of the Algal Nuclear Gene psbO to the Photosynthetic Sea Slug Elysia chlorotica,” PNAS 105 (2008): 17867– 71; Julie A. Schwartz, Nicholas E. Curtis, and Sidney K. Pierce, “FISH Labeling Reveals a Horizontally Transferred Algal (Vaucheria litorea) Nuclear Gene on a Sea Slug (Elysia chlorotica) Chromosome,” Biological Bulletin 227 (2014): 300– 312; and D. K. Bhattacharya et al., “Genome Analysis of Egg DNA Provides No Evidence for Horizontal Gene Transfer into the Germ Line of This Kleptoplastic Mollusc,”

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Molecular Biology and Evolution 30 (2014): 1843– 53 (note: there is some controversy in this research). The amazing story of the tree sloth was uncovered by Jonathan Pauli and colleagues: “A Syndrome of Mutualism Reinforces the Lifestyle of a Sloth,” PRSB 281 (2014), doi:20133006. For photosynthetic animals in science fiction, see Olaf Stapledon, Star Maker (Middletown, CT: Wesleyan University Press, 1937); Geoff Ryman, The Child Garden (Easthampton, MA: Small Beer Press, 2011); and Walter John Williams, Green Leopard Plague and Other Stories (San Francisco: Night Shade Books, 2010). Scientific names of plants mentioned in order in the chapter: cactus alga = Halimeda sp. (Halimedaceae, Chlorophyta); sea palm Postelsia palmaeiformis Ruprecht (Laminariaceae, Phaeophyta); coral alga = Mesophyllum mesomorpha Pratz (Corallinaceae, Rhodophyta); giant dawsonia moss = Dawsonia longifolia (Bruch. & Schimp.) Zant. (Polytrichaceae); yellow ladle liverwort = Scapania bolanderi Austin (Scapaniaceae); ground pine = cf. Lycopodium clavatum L. (Lycopodiaceae); Cooksonia = Cooksonia hemisphaerica W.H. Lang (classification uncertain); Rhynia = Rhynia Gwynne-vaughanii Kidst. & W.H. Lang (Rhyniopsida); whisk fern = Psilotum nudum (L.) P. Beauv. (Psilotaceae); Sawdonia = Sawdonia ornata (Dawson) F.M. Hueber (Zosterophylopsida); Baragwanathia = Baragwanathia longifolia (Lang & Cookson) (Lycopodiopsida ); spike moss = Selaginella willdenowii (Desv.) Bak. (Selaginellaceae); cladoxyloid tree = Wattiezia sp. Stockmans (Cladoxylopsida); Lepidodendron = Lepidodendron sp. (Lepidodendraceae, Lycopodiophyta); Archeopteris = Archeopteris sp. (Archeoptieridaceae, Progymnospermophyta; holly fern = Cyrtomium falcata (L.f.) C. Presl. (Dryopteridaceae); umbilicaria, rock tripe = Umbilicaria americana Poelt. & T. Nash (Umbilicariaceae, Ascomycota); freckle pelt lichen = Peltigera aphthosa (L.) Willd. (Peltigeraceae, Ascomycota).

Chapter Three: Green Machinery For the epigraph quotes: Stephen Hales, Vegetable Staticks (London: Macdonald, 1727), reprinted in 1961 by American Elsevier, New York; and the poem “Trees with the Hidden Gold” by the artist Robin Ross, which appeared in 2015 (www.robinross.com/blog). For the reference to corn from carbon in the human diet, see Michael Pollan, Omnivore’s Dilemma: A Natural History of Four Meals (New York: Penguin, 2007). For ancient philosophy and the vital elements, see Roger French, Ancient Natural History: Histories of Nature (London: Routledge, 1994); I also consulted an excellent article on the classical elements in nature in Wikipedia (en.wikipedia.org/wiki/Classical_element). There is a sound account of the history of botany with good coverage of the history of photosynthesis in A. G. Morton, History of Botanical Science: An Account of the Development of Botany from Ancient Times to the Present Day (London: Academic Press, 1981). For history, I relied on biographies of important figures from C. G. Gillespie, ed., Dictionary of Scientific Biography, in 16 volumes (New York: Charles Scribner’s & Sons, 1970–80), including, in order of coverage: Theophrastus, William Harvey, Jan Baptista van Helmont, Stephen Hales, Joseph Priestley, Charles Bonnet, Joseph Black, Frederick Frost Blackman, Antoine

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Lavoisier, Jan Ingen- Housz, Jean Senebier, Nehemiah Grew, Antonie van Leeuwenhoek, Pierre-Joseph Pelletier, Joseph Bienaimé Caventou, Andreas Schimper, Richard Willstätter, and Theodor Wilhelm Engelmann. I supplemented those biographies with articles from Wikipedia (useful for facts and bibliographies) and added other biographies for scientists covered in more detail. For Hales, I read Vegetable Staticks, cited above. For Priestley: Joseph Priestley, Autobiography of Joseph Priestley (1832; reprint, Teaneck, NJ: Fairleigh Dickinson University Press, 1931); Anne Holt, A Life of Joseph Priestley (London: Oxford University Press, 1931, reprinted by Greenwood Press (Westport, CT: 1970), with a valuable introduction by Francis W. Hirst; Robert E. Schofield, The Enlightenment of Joseph Priestley. A Study of His Life and Work from 1733 to 1773 (University Park, PA: Pennsylvania State University Press, 1997). Priestley’s own experimental descriptions also are good reading: Experiments and Observations on Different Kinds of Air, 2nd ed. (London: J. Johnson, 1776). For Ingen-Housz: Howard Gest, “A ‘Misplaced Chapter’ in the History of Photosynthesis Research: The Second Publication (1796) on Plant Processes by Dr. Jan Ingen-Housz, MD, Discoverer of Photosynthesis,” Photosynthesis Research 53 (1997): 65– 72; Norman and Elaine Beale, “Sunlight at Southall Green. Dr. Ingen- Housz Discovers Photosynthesis,” Perspectives in Biology and Medicine 44 (2001): 333–41; Geerdt Magiels, From Sunlight to Insight: Jan IngenHousz, the Discovery of Photosynthesis and Science in the Light of Ecology (Brussels: Brussels University Press, 2010). His monograph on assimilation also is valuable: Experiments upon Vegetables (London: P. Elmsly and H. Payne, 1779). For Jean Senebier: J. C. Bay, “Jean Senebier, 1742–1809,” PP 6 (1931): 87–193.

For a review of the creation of the word “photosynthesis,” see Howard Gest, “History of the Word Photosynthesis and Evolution of Its Definition,” PR 73 (2002): 7–10. For a review of the discovery and study of the chloroplast: Brian Gunning, Friederike Koening, and Govindjee, “A Dedication to Pioneers of Research on Chloroplast Structure,” in The Structure and Function of Plastids, Advances in Photosynthesis and Respiration, vol. 23, ed. R. R. Wise and J. K. Hoober (Dordrecht: Springer, 2007), xxiii–xxxi. For plant respiration, see Ingen-Housz, Experiments upon Vegetables, cited above; Walter Stiles, “A Footnote to the History of Plant Respiration,” Protoplasma 15 (1932): 301–5; and Edward Kemp, The Handbook of Gardening (London: Bradbury and Evans, 1851). Bibliographic information on twentieth-century pioneers in photosynthesis is a little less accessible. Oliver Morton’s Eating the Sun (New York: HarperCollins, 2008) has a nice description of these twentieth- century discoveries, and most are covered in standard plant physiology texts, such as L. Taiz and E. Zeiger, Plant Physiology, 4th ed. (Sunderland, MA: Sinauer Associates, 2006). I used additional articles for individual contributions. Robert Emerson: E. Rabinowitch, “Robert Emerson, 1903–1959,” PP 34 (1959): 179–84; Govindjee, “Robert Emerson, and Eugene Rabinowitch: Understanding Photosynthesis,” in No Boundaries: University of Illinois Vignettes, ed. Lillian Hoddeson (Urbana: University of Illinois Press, 2004), 181–94. Richard Willstätter’s autobiography: From My Life: The Memoirs of Richard Willstätter (New York: W. A. Benjamin, 1965). For Otto Warburg: Hans Adolf Krebs, Otto Warburg: Cell Physiologist, Biochemist, and Eccentric (Oxford: Oxford Univer-

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sity Press,1981); Ron Chernow, The Warburgs: The Twentieth-Century Odyssey of a Remarkable Jewish Family (New York: Random House, 1993); and K. Nickelsen, “The Construction of a Scientific Model: Otto Warburg and the Building Block Strategy,” Studies in the History and Philosophy of Biology and Biomedical Science 40 (2009): 73– 86. For Samuel Ruben and Martin Kamen: Howard Gest, “Samuel Ruben’s Contributions to Research on Photosynthesis and Bacterial Metabolism with Radioactive Carbon,” PR 80 (2004): 77–83. For Melvin Calvin: Melvin Calvin, Following the Trail of Light: A Scientific Odyssey (Profiles, Pathways and Dreams) (New York: John Wiley, 1992). For Peter Mitchell: Anthony Crofts, “Peter Mitchell, 1920– 1992,” PR 35 (1993): 1–4. For Jan Anderson, see her review “Insights into the Consequences of Grana Stacking of Thylakoid Membranes in Vascular Plants: A Personal Perspective,” Australian Journal of Plant Physiology 26 (1999): 625–39. For Daniel Arnon: see R. Malkin, “Arnon, Daniel I. (1910–1994),” PR 43 (1995): 77–80. For information on the Z-scheme and chloroplast structure, I consulted Taiz and Zeiger, cited above, as well as information on chloroplast ultra-structure from the same text and Ray F. Evert and Susan E. Eichorn, Raven Biology of Plants, 8th ed. (San Francisco: W. H. Freeman, 2012). For efficiency of the photosynthesis process, see R. E. Blankenship et al., “Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement,” Science 332 (2011): 805–9; N. R. Baker, J. Harbinson, and D. M. Kramer, “Determining the Limitations and Regulation of Photosynthetic Energy Transduction in Leaves,” PCE 30 (2007): 1107–25; X. G. Zhu, S. P. Long, and D. R. Orr, “Improving Photosynthetic Efficiency for Greater Yield,” ARPB 61 (2010): 235–61; D. O. Hall and K. K. Rao, Photosynthesis, 6th ed. (Cambridge: Cambridge University Press, 1999); and Xinyou Yin and Paul C. Struik, “Constraints to the Potential Efficiency of Converting Solar Radiation into Phytoenergy in Annual Crops: From Leaf Biochemistry to Canopy Physiology and Crop Ecology,” JEB 66 (2015): 6535–49. Information on C4 and CAM photosynthesis is well covered in Taiz and Zeiger, cited above, as well as Jessica Gurevich, Samuel M. Scheiner, and Gordon A. Fox, The Ecology of Plants, 2nd ed. (Sunderland, MA: Sinauer Associates, 2006). Humboldt’s observation of a CAM plant were interpreted by Ulrich Lüttge, “CO2ĕConcentrating: Consequences in Crassulacean Acid Metabolism,” JEB 53 (2001): 2132–42. For RuBisCO engineering: Elizabete Carmo-Silva, Joanna C. Scales, Pippa J. Madgwick, and Martin A. J. Parry, “Optimizing Rubisco and Its Regulation for Greater Resource Use Efficiency,” PCE 38 (2015): 1817–32. For Dan Nocera’s research on artificial photosynthesis: Daniel G. Nocera, “The Artificial Leaf,” Accounts of Chemical Research 45, no. 5 (2012): 767–76, doi:10.1021/ar2003013; American Chemical Society, “Secrets of the First Practical Artificial Leaf,” ScienceDaily (2012), https://www.sciencedaily.com/releases/2012/05 /120509123900.htm; and Joseph P. Torella et al., “Efficient Solar-to-Fuels Production from a Hybrid Microbial-Water-Splitting Catalyst System,” PNAS 112 (2015): 2337–42. For Tongxiang Fan’s research to duplicate leaf structure in optimizing photosynthesis, see Han Zhou et al., “Biomimetic Photocatalyst System Derived

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from the Natural Prototype in Leaves for Efficient Visible- Light-Driven Catalysis,” Journal of Materials Chemistry 19 (2009): 2695–703; Han Zhou et al., “Artificial Inorganic Leafs for Efficient Photochemical Hydrogen Production Inspired by Natural Photosynthesis,” Advanced Materials 22 (2010): 951–56; Kevin P. Lucht and Jose L. Mendoza-Cortes, “Birnessite: A Layered Manganese Oxide to Capture Sunlight for Water-Splitting Catalysis,” Journal of Physical Chemistry C 119 (2015): 22838–46; and Jessica Marshall, “Springtime for the Artificial Leaf,” Nature 510 (2014): 22–24; and for inserting catalysts into chloroplasts: Juan Pablo Giraldo et al., “Plant Nanobionics Approach to Augment Photosynthesis and Biochemical Sensing,” Nature Materials 13 (2014), doi:10.1038/NMAT3890. Consult chapter 4 from my book Nature’s Palette (Chicago: University of Chicago Press, 2007) for a summary of optical properties of leaves. For a description of C4 and CAM metabolism, consult Taiz and Zeiger, cited above, as well as the Evert and Eichorn text (or another text). For the quotation by Albert Einstein, see Alice Calaprice, ed., The Expanded Quotable Einstein (Princeton, NJ: Princeton University Press, 2000). Scientific names of plants mentioned in this chapter in order: maize, corn = Zea mays L. (Poaceae); sugarcane = Saccharum officinarum L. (Poaceae); Crassula, stonecrop = Crassula sp. (Crassulaceae); pitch apple = Clusia rosea Jacq. (Guttiferae); living stone = Lithops optica (Marloth) N.E. Br. (Aizoaceae); peperomia = Peperomia rotundifolia (L.) Kunth (Piperaceae).

Chapter Four: Nature’s Fabric The first epigraph is from Alexander Pope, “An Essay on Man,” epistle 3, in An Essay on Man and Other Poems (New York: Dover Press, 1994). The second epigraph is from a poem by Wendell Berry, “A Speech to the Garden Club of America,” New Yorker Magazine, September 28, 2009.

For the normalized difference vegetation index (NDVI), see the NASA website: http://earthobservatory.nasa.gov/features/MeasuringVegetation/. Note that the actual equation for the ratio is (NIR – VIS)/(NIR + VIS), where VIS is 580–680 and NIR is 725–1,100 nanometers. For the leaf area index (LAI) and many other ecological terms in this chapter, consult Jessica Gurevich, Samuel M. Scheiner, and Gordon A. Fox, The Ecology of Plants, 2nd ed. (Sunderland, MA: Sinauer Associates, 2006). For the actual global data on LAI, I consulted J. M. O. Scurlock, G. P. Asner, and S. T. Gower, “Worldwide Historical Estimates and Bibliography of Leaf Area Index, 1932– 2000,” ORNL Technical Memorandum TM-2001/268 (Oak Ridge, TN: Oak Ridge National Laboratory, 2001). I specifically described the work of D. B. Clark, P. Olivas, S. F. Oberbauer, D. A. Clark, and M. G. Ryan, “First Direct Landscape-Scale Measurement of Tropical Rain Forest Leaf Area Index, a Key Driver of Global Primary Productivity,” EL 11 (2008): 163–72. For the global tree census: T. W. Crowther et al., “Mapping Tree Density at a Global Scale,” Nature 525 (2015): 201–5. Humboldt’s early writings show his interest in plant “physiognomy” and geography: Alexander Von Humboldt and Aimé Bonpland, Essay on the Geography of Plants

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(Chicago: University of Chicago Press, 2009)— the editor, Stephen T. Jackson, wrote an insightful essay; Alexander Von Humboldt, Aspects of Nature, in Different Lands and Different Climates, with Scientific Elucidations (Philadelphia: Lea and Blanchard, 1850). The derivation of “physiognomy” is from L. Brown, ed., The New Shorter Oxford English Dictionary (Oxford: Clarendon Press, 1993). For Andreas Schimper, I consulted his classic book Plant-Geography upon a Physiological Basis, trans. R. A. F. Fisher with appreciation by P. Groom (Oxford: Clarendon Press, 1903). Groom’s essay provided useful biographical information, as did the short article in The Dictionary of Scientific Biography (New York: Charles Scribner & Sons, 1970–80). For Christen Raunkiaer: G. D. Fuller, “Raunkiaer’s Ecological Papers,” Ecology 16 (1935): 111–13; and the article in Wikipedia: https://en.wikipedia .org/wiki/Christen_C._Raunkiaer. For descriptions of plant functional types, see E. O. Box, Macroclimate and Plant Forms: An Introduction to Predictive Modelling in Phytogeography (The Hague: W. Junk, 1981); I. Colin Prentice et al., “A Global Biome Model Based on Plant Physiology and Dominance, Soil Properties and Climate,” JB 19 (1992): 117–34; and T. M. Smith, H. H. Shugart, and F. I. Woodward, eds., Plant Functional Types: Their Relevance to Ecosystem Properties and Global Change (Cambridge: Cambridge University Press, 1997). For a more accessible introduction, see the book by Gurevich, Scheiner, and Fox, cited above. These authors also describe plant phenology, and the website cited in the text will be useful. Also, see Elizabeth M. Wolkovich, Benjamin I. Cook, and T. Jonathan Davies, “Progress towards an Interdisciplinary Science of Plant Phenology: Building Predictions across Space, Time and Species Diversity,” NP 201 (2014): 1156–62. For the phenology of a Malaysian rainforest, see Lord Medway, “Phenology of a Tropical Rain Forest in Malaya,” BotJLS 4 (1972): 117–46. For the phenology of a tropical deciduous forest: David W. Lee, “Canopy Dynamics and Light Climates in a Tropical Moist Deciduous Forest,” JTE 5 (1989): 65–79. For the oldest phenological records: T. H. Sparks and P. D. Carey, “The Responses of Species to Climate over Two Centuries: An Analysis of the Marsham Phenological Record, 1736– 1947,” JE 83 (1995): 321– 29, much earlier than Thoreau’s observations: Caroline Polgar, Amanda Galinat, and Richard B. Primack, “Drivers of Leaf-Out Phenology and Their Implications for Exotic Species Invasions: Lessons from Thoreau’s Concord,” NP 202 (2014): 106— 15. For the definition of biomes and their descriptions, see Gurevich, Scheiner, and Fox, cited above; and the article by Prentice et al., cited above, defining biomes by the physiological responses of plant functional types. For a description of the subtropical nature of Miami’s urban environment, see David W. Lee and Stacy West, Wayside Trees of Tropical Florida (Mebane, NC: Tellus Books, 2011). For the basics of global climate change, I have used the Fourth and Fifth Assessment Reports by the IPCC: R. K. Pachauri and A. Reisinger, eds., Synthesis Report on Global Climate Change, 2007 (Geneva: Intergovernmental Panel on Climate Change, 2007); and IPCC, Climate Change 2013: The Physical Science Basis, Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change

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(New York: Cambridge University Press, 2013). I’ve also used the technical reports, which can be purchased as books or sections and can be downloaded at the IPCC website. For the carbon cycle, the definitions of net primary productivity, and so on are in Gurevich, Scheiner, and Fox, cited above. The pools and fluxes in the carbon cycle are obtained from the IPCC Working Group I Report, The Physical Science Basis, cited above. For allocation of carbon in plants, I cite L. E. Aragao et al., “Above- and Belowground Net Primary Productivity across Ten Amazonian Forests on Contrasting Soils,” BG 6 (2009): 2759–78; J. R. Bray and E. Gorham, “Litter Production in Forests of the World,” AER 2 (1964): 101–58; J. Chave et al., “Regional and Seasonal Patterns of Litterfall in Tropical South America,” BG 7 (2010): 43–55; M. L. Creighton, J. W. Raich, and M. G. Ryan, “Carbon Allocation in Forest Ecosystems,” GCB 13 (2007): 2089–109; B. Shipley and D. Meziane, “The Balanced-Growth Hypothesis and the Allometry of Leaf and Root Biomass Allocation,” FE 16 (2002): 326–31; and Y. Malhi et al., “Comprehensive Assessment of Carbon Productivity, Allocation and Storage in Three Amazonian Forests,” GCB 15 (2009): 1255–74; H. Poorter and H. Lambers, “Is Interspecific Variation in Relative Growth Rate Positively Correlated with Biomass Allocation to the Leaves?” AN 138 (1991): 1264–68; E. J. Veneklaas and L. Poorter, “Growth and Carbon Partitioning of Tropical Tree Seedlings in Contrasting Light Environments,” In Inherent Variation in Plant Growth: Physiological Mechanisms and Ecological Consequences, ed. H. Lambers, H. Poorter, and M. M. I. Van Vuuren (Leiden, Netherlands: Backhuys, 1998), 337–61. For carbon storage in tropical forests: Saasan Saatchi et al., “Benchmark Map of Forest Carbon Stocks in Tropical Regions across Three Continents,” PNAS 108 (2011): 9899–904. For some perspective on measuring the rise in carbon dioxide: Charles D Keeling, “Rewards and Penalties of Monitoring the Earth,” Annual Review of Energy and the Environment 23 (1998): 25–82; and see the continual monitoring on the NOAA’s website: http://www.esrl.noaa.gov/gmd/ccgg/trends/. For deforestation due to oil palm plantation development in Indonesia: Ben Block, “Global Palm Oil Demand Fueling Deforestation,” Worldwatch Institute: www.worldwatch.org/node /6059; and Elisabeth Rosenthal, “Once a Dream Fuel, Palm Oil May Be an EcoNightmare,” NYT, January 31, 2007. For general information on the nitrogen cycle, see Gurevich, Scheiner, and Fox, cited above. For information about nitrogen allocation in plants, leaves in particular, see R. Habib, P. Millard, and M. F. Proe, “Modeling the Seasonal Nitrogen Partitioning in Young Sycamore (Acer pseudoplatanus) in Relation to Nitrogen Supply,” AB 71 (1993): 453– 59; E. Garnier, O. Gobin, and H. Poorter, “Nitrogen Productivity Depends on Photosynthetic Nitrogen Use Efficiency and on Nitrogen Allocation within the Plant,” AB 76 (1995): 667–72; T. Watanabe et al., “Evolutionary Control of Leaf Element Composition in Plants,” NP 174 (2007): 516–23; K. S. Pregitzer, D. I. Dickmann, R. Hendrick, and P. V. Nguyen, “WholeTree Carbon and Nitrogen Partitioning in Young Hybrid Poplars,” Tree Physiology 7

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(1990): 79–93. For the loss and retention of nitrogen in falling leaves: K. T. Killingbeck, “Nutrients in Senesced Leaves: Keys to the Search for Potential Resorption and Resorption Proficiency,” Ecology 77 (1996): 1716–27; B. Hättenschwiler, M. Aeschlimann, M. Coûteaux, J. Roy, and D. Bonal, “High Variation in Foliage and Leaf Litter Chemistry among 45 Tree Species of a Neotropical Rainforest Community,” NP 179 (2008): 165–75; Z. Yuan and H. Y. H. Chen, “Global Trends in Senesced-Leaf Nitrogen and Phosphorus,” GEB 18 (2009): 532–42; G. I. Agren, “Stoichiometry and Nutrition of Plant Growth in Natural Communities,” AREES 39 (2008): 153–70; R. Aerts, “Nutrient Resorption from Senescing Leaves of Perennials: Are There General Patterns?” JE 84 (1996): 597–608; T. Watanabe et al., “Evolutionary Control of Leaf Element Composition in Plants,” NP 174 (2007): 516–23. For nitrogen assimilation in Gunnera: G. Campbell et al., “Gunnera tinctoria: An Unusual Nitrogen-Fixing Invader,” BioScience 41 (1991): 224–28. For nitrogen assimilation from leaf surfaces: B. L. Bentley, “Nitrogen Fixation by Epiphylls in a Tropical Rainforest,” Annals of the Missouri Botanical Garden 74 (1987): 234–41. For a summary on the global water cycle, including pools and fluxes, I used T. Oki and S. Kanae, “Global Hydrological Cycles and World Water Resources,” Science 313 (2006): 1068– 72. For specific papers on hydrology and global climate change: Nicola Gedney et al., “Detection of a Direct Carbon Dioxide Effect in Continental River Runoff Records,” Nature 439 (2006): 835–38; L. J. Gordon et al., “Human Modification of Global Water Vapor Flows from the Land Surface,” PNAS 102 (2005): 7612–17. For estimates of internal leaf surface area, see F. Turrell, “The Area of the Internal Exposed Surface of Dicotyledon Leaves,” AJB 23 (1936): 255–64; P. S. Nobel, “Relation between Mesophyll Surface Area, Photosynthetic Rate, and Illumination Level during Development for Leaves of Plectranthus parviforus Henckel,” PP 55 (1975): 1067–70; and from my own research, David W. Lee et al., “Effects of Irradiance and Spectral Quality on Leaf Structure and Function in Seedlings of Two Southeast Asian Hopea Species,” AJB 87 (2000): 447–55. For a summary of water and mineral transport in plants, see Gurevich, Scheiner, and Fox, cited above; and L. Taiz and E. Zeiger, Plant Physiology, 4th ed. (Sunderland, MA: Sinauer Associates, 2006). Examples of stomatal density from my own research are seen in David W. Lee, K. Baskaran, M. Mansor, H. Mohamad, and S. K. Yap, “Light Intensity and Spectral Quality Effects on Asian Tropical Rainforest Tree Seedling Development,” Ecology 77 (1996): 568–80. The following references were used to describe the history of our understanding of the effects of vegetation on water supply. For early Greek and Roman descriptions, I used J. Donald Hughes, Pan’s Travail. Environmental Problems of the Ancient Greeks and Romans (Baltimore: Johns Hopkins University Press, 1994); Clarence J. Glacken, Traces on the Rhodian Shore: Nature and Culture in Western Thought from Ancient Times to the End of the Eighteenth Century (Berkeley: University of California Press, 1967); and J. D. Hughes, “Theophrastus as Ecologist,” Environmental Review 4 (1985): 291–307. Documentation of the transmission of knowledge about hydrology from

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the Royal Society to the colonies is seen in Richard Grove, “The East India Company, the Raj and the El Niño: The Critical Role Played by Colonial Scientists in Establishing the Mechanisms of Global Climate Teleconnections, 1770–1930,” in Nature and the Orient: The Environmental History of South and Southeast Asia, ed. R. H. Grove, V. Damodaran, and S. Sangwan (Delhi: Oxford University Press, 1998), 301–23; Richard Grove, Ecology, Climate and Empire: Colonialism and Global Environmental History, 1400– 1940 (Cambridge: White Horse Press, 1997). In addition to a short Wikipedia article, there is now a full-length biography of William Roxburgh: Tim Robinson, William Roxburgh: The Founding Father of Indian Botany (Edinburgh: Phillimore and Company, 2008). I quoted Humboldt’s Personal Narrative of Travels to the Equinoctial Regions of the New Continent 1799–1804, vol. 4, trans. H. M. Williams (New York: Amsterdam, 1972, from original edition of 1819). Other articles consulted include J. B. Boussingault, “Memoir Concerning the Effect Which the Clearing of Land Has in Diminishing the Quantity of Water in the Streams of a District,” Edinburgh New Philosophical Journal 24 (1838): 85–106; and Engelhard Weigl, “Alexander von Humboldt and the Beginning of the Environmental Movement,” International Review for Humboldtian Studies 11, no. 2 (2001). For articles on water retention and hydrology: Robert R. Zimmer, “Water Yields from Forests: An Agnostic View” (California Watershed Management Conference, West Sacramento, CA, November 18– 20, 1986), 74– 78; V. Sahin and M. J. Hall, “The Effects of Afforestation and Deforestation on Water Yields,” Journal of Hydrology 178 (1996): 293–309; J. M. Bosch and J. D. Hewlett, “A Review of Catchment Experiments to Determine the Effects of Vegetation Change on Water Yield and Evapotranspiration,” Journal of Hydrology 55 (1982): 3–23. For Kenworthy’s study of a watershed in the Gombak valley: “Water and Nutrient Cycling in a Tropical Rain Forest,” in The Water Relations of Malesian Forests, ed. J. Flenley (Hull, UK: University of Hull Department of Geography Miscellaneous Series, 1, 1971), 49–65; and for tropical regions in general, see J. Balik, Hydrology and Water Resources in Tropical Regions, Developments in Water Science, vol. 18 (New York: Elsevier, 1983); and P. W. Richards, The Tropical Rain Forest: An Ecological Study, 2nd ed. (Cambridge: Cambridge University Press, 1996), with information on hydrology and nutrient cycling. Stable isotope support for strong recycling in the Amazon system was published by my friend Leo Sternberg and colleagues: M. Z. Moreira et al., “Contribution of Transpiration to Forest Ambient Vapour Based on Isotopic Measurements,” GCB 3 (1997): 439–50. The same approach was more recently applied globally: Scott Jasechko, “Terrestrial Water Fluxes Dominated by Transpiration,” Nature 496 (2013): 347–51. For a general discussion about the effects of climate change on the water cycle: B. Bates, Z. W. Kundzewicz, S. Wu, and J. Palutikof, eds., Climate Change and Water: Technical Paper VI, I (Geneva: IPCC Working Group II, 2007); and for the Amazon, R. A. Betts et al., “The Role of Ecosystem-Atmosphere Interactions in Simulated Amazonian Precipitation Decrease and Forest Dieback Under Global Climate Warming,” Theoretical and Applied Climatology (2004), doi:10.1007/s00704004-0050-y.

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An overview of climatic and evolutionary history is summarized in general biology texts. David Beerling’s The Emerald Planet: How Plants Changed Earth’s History (Oxford: Oxford University Press, 2007) treats segments of that history in detail, partly based on his and colleagues’ research. A comprehensive review of paleotemperatures and carbon dioxide concentrations is provided in two articles by Dana Royer and colleagues: D. L. Royer, R. A. Berner, I. P. Montanez, N. J. Tabor, and D. J. Beerling, “CO2 as a Primary Driver of Phanerozoic Climate Change,” GSA Today 14, no. 3 (2004): 4–10; D. L. Royer, R. A. Berner, and J. Park, “Climate Sensitivity Constrained by CO2 Concentrations over the Past 420 Million Years,” Nature 446 (2007): 530–32. The record of extinctions over this time is covered by D. Raup and J. Sepkoski, “Periodic Extinction of Families and Genera,” Science 231 (1986): 833–36; J. J. Sepkoski, “Patterns of Phanerozoic Extinction: A Perspective from Global Data Bases,” in Global Events and Event Stratigraphy, ed. O. H. Waliser (Berlin: Springer Verlag, 1996), 35– 51; J. Alroy, “Dynamics of Origination and Extinction in the Marine Fossil Record,” PNAS US 105 (2008): 11536–42; P. R. Mayhew, G. B. Jenkins, and T. G. Benton, “A Long-Term Association between Global Temperature and Biodiversity, Origination and Extinction in the Fossil Record,” PRSB 275 (2008): 47–53. Other variations for oxygen in the climate record over this time are documented by D. J. Beerling, R. A. Berner, F. T. Mackenzie, M. Harfoot, and J. A. Pyle, “Methane and the CH4-Related Greenhouse Effect over the Past 400 Million Years,” American Journal of Science 309 (2009): 97–113; R. A. Berner and Z. Kothavala, “Geocarb III: A Revised Model of Atmospheric CO2 over Phanerozoic Time,” American Journal of Science 301 (2001): 182–204; for plants: J. C. McElwain and S. W. Punyasena, “Mass Extinction Events and the Plant Fossil Record,” TREE 22 (2007): 548–57. The discovery that stomata can be used to track atmospheric CO2 concentrations began with the original discovery made in relation to physiological studies in alpine plants by Ian Woodward: “Stomatal Numbers Are Sensitive to Increases in CO2 from Pre-Industrial Levels,” Nature 327 (1987): 617–18. He showed in reduced CO2 concentrations of high altitudes, produced in chambers at low elevation, that leaves with lower stomatal concentrations were produced, and that old herbarium specimens of leaves had lower stomatal concentrations in pre-industrial times than the same species at present. This made possible the research on climate history we are relying on in this discussion: Julie E. Gray et al., “The HIC Signaling Pathway Links CO2 Perception to Stomatal Development,” Nature 408 (2000): 713–17; P. J. Franks and D. J. Beerling, “Maximum Leaf Conductance Driven by Atmospheric CO2 Effects on Stomatal Size and Density over Geologic Time,” PNAS 106 (2009): 10343–47; D. J. Beerling and D. L. Royer, “Convergent Cenozoic CO2 History,” Nature Geoscience 4 (2011): 418–20; David J. Beerling, “Atmospheric Carbon Dioxide: A Driver of Photosynthetic Eukaryote Evolution for over a Billion Years?” PTRSB 367 (2012): 477– 82; and John A. Raven, “Selection Pressures on Stomatal Evolution,” NP 153 (2002): 371–86. For other properties of leaves relevant to climate change, I have consulted these articles. For volatile organic com-

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pounds (VOCs): Sandy P. Harrison, “Volatile Isoprenoid Emissions from Plastid to Planet,” NP 197 (2013): 49–57; Magda Claeys et al., “Formation of Secondary Organic Aerosols through Photooxidation of Isoprene,” Science 303 (2004): 1173– 76; Andy R. McLeod et al., “Ultraviolet Radiation Drives Methane Emissions from Terrestrial Plant Pectins,” NP 180 (2008): 124–32; Joshua S. Yuan, Sari J. Himanen, Jarmo K. Holopainen, Feng Chen, and C. Neal Stewart Jr., “Smelling Global Climate Change: Mitigation of Function for Plant Volatile Organic Compounds,” TREE 24 (2009): 323–33; and an important paper on the role of VOCs in cloud formation: Mikael Ehn et al., “A Large Source of Low-Volatility Secondary Organic Aerosol,” Nature 506 (2014): 476– 79. For phenological effects of climate change: Danielle A. Way and Rebecca A. Montgomery, “Photoperiod Constraints on Tree Phenology, Performance and Migration in a Warming World,” PCE 38 (2015): 1725–36; Adrian M. I. Roberts, Christine Tansey, Richard J. Smithers, and Albert B. Phillimore, “Predicting a Change in the Order of Spring Phenology in Temperate Forests,” GCB 21 (2015): 2603–11; Trevor F. Keenan and Andrew D. Richardson, “The Timing of Autumn Senescence Is Affected by the Timing of Spring Phenology: Implications for Predictive Models,” GCB 21 (2015): 2634–41; A. D. Richardson, A. S. Bailey, E. G. Denny, C. W. Martin, and J. O’Keefe, “Phenology of a Northern Hardwood Forest Canopy,” GCB 12 (2006): 1174–88. For the need to study tropical biomes: Jeff Toleffson, “Climate Modellers Take Tropical Approach,” Nature 519 (2015): 398–99; and Gabriel Potkin, “Weighing the World’s Trees,” Nature 523 (2015): 20–22. For effects of temperature and CO2 on photosynthesis, see Taiz and Zeiger, cited above; Elizabeth A. Ainsworth and Stephen P. Long, “What Have We Learned from 15 Years of Free-Air CO2 Enrichment (FACE)? A Meta-Analytic Review of the Responses of Photosynthesis, Canopy Properties and Plant Production to Rising CO2,” NP 165 (2005): 351–72; S. Piao et al., “Forest Annual Carbon Cost: A Global-Scale Analysis of Autotrophic Respiration,” Ecology, 91 (2010): 652–61; O. K. Atkin, I. Scheurwater, and T. L. Pons, “Respiration as a Percentage of Daily Photosynthesis in Whole Plants is Homeostatic at Moderate, but Not High, Growth Temperatures,” NP 174 (2007): 367– 80. NP published a virtual issue on “plant respiration in variable environments,” with an introduction by O. K. Atkin: NP 191, no. 1 (2011). For the effects of oil palm expansion in Southeast Asia on deforestation and carbon emissions: Doug Boucher et al., The Root of the Problem: What’s Driving Tropical Deforestation Today? (Cambridge, MA: Union of Concerned Scientists Publications, 2011). For past history of C4 photosynthetic plants: C. P. Osborne and D. J. Beerling, “Nature’s Green Revolution: The Remarkable Evolutionary Rise of C4 Plants,” PTRSB 361 (2006): 173–94. For albedo: Daniel A. Lashof and Benjamin J. DeAngelo, “Terrestrial Ecosystem Feedbacks to Global Climate Change,” Annual Reviews of Energy and the Environment 22 (1997): 75–118; G. B. Bonan, “Forests and Climate Change: Forcings, Feedbacks, and the Climate Benefits of Forests,” Science 320 (2008): 1444–49; and Ning N. Zeng and Jinho Yoon, “Expansion of the World’s

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Deserts Due to Vegetation- Albedo Feedback under Global Warming,” Geophysical Research Letters 36 (2009): 17401, doi:10.1029/2009GL039699. For effects of climate change on forest phenology and carbon balance, see S. Piao, et al., “Net Carbon Dioxide Losses of Northern Ecosystems in Response to Autumn Warming,” Nature 451 (2008): 49–52; J. D. Fridley, “Extended Leaf Phenology and the Autumn Niche in Deciduous Forest Invasions,” Nature 485 (2012): 359–62; John B. Miller, “Sources, Sinks and Seasons,” Nature 451 (2012): 25–27; Zoe A. Panchen et al., “Substantial Variation in Leaf Senescence Times among 1360 Temperate Woody Plant Species: Implications for Phenology and Ecosystem Processes,” AB 116 (2015): 865–73. Although there do not seem to be very direct effects, there has been quite a bit of discussion on potential vegetation feedbacks moderating climate change. See David J. Beerling and Robert Berner, “Feedbacks and the Coevolution of Plants and Atmospheric CO2, PNAS 102 (2005): 1302–5; M. Pagani, K. Caldeira, R. A. Berner, and D. J. Beerling, “The Role of Terrestrial Vegetation in Limiting Atmospheric CO2 Decline over the Past 24 Million Years,” Nature 460 (2009): 85–88; F. I. Woodward, M. R. Lomas, and R. A. Betts, “Vegetation-Climate Feedbacks in a Greenhouse World,” PTRSB 353 (1998): 29–39; Robert A. Berner, “The Carbon Cycle and CO2 over Phanerozoic Time: The Role of Land Plants,” PTRSB 353 (1998): 75–82; and D. L. Royer, M. Pagani, and D. J. Beerling, “Geobiological Constraints on Earth System Sensitivity to CO2 during the Cretaceous and Cenozoic,” Geobiology (2012), doi:10.1111/j.1472-4669.2012.00320.x. For the documentation of vegetation shifts on Chimborazo: Naia Morueta-Holm et al., “Strong Upslope Shifts in Chimborazo’s Vegetation over Two Centuries since Humboldt,” PNAS 112 (2015): 12741–45; and Evan M. Rehm and Kenneth J. Feeley, “The Inability of Tropical Cloud Forest Species to Invade Grasslands above Treeline during Climate Change: Potential Explanations and Consequences,” Ecography 38 (2015): 1167–75. For the implications of extreme events on global climate change: Markus Reichstein et al., “Climate Extremes and the Carbon Cycle,” Nature 500 (2013): 287–95; and L. V. Gatti et al., “Drought Sensitivity of Amazonian Carbon Balance Revealed by Atmospheric Measurements,” Nature 506 (2014): 76–80; Randane Alkama and Alessandro Cescatti, “Biophysical Climate Impacts of Recent Changes in Global Forest Cover,” Science 351 (2016): 600– 604; and Zaichin Zhu et al., “Greening of the Earth and Its Drivers,” Nature Climate Change 6 (2016): 791–95. For the human appropriation of the products of photosynthesis: P. M. Vitousek, P. R. Ehrlich, A. H. Ehrlich, and P. A. Matson, “Human Appropriation of the Products of Photosynthesis,” BioScience 36 (1986): 368–72; S. Rojstaczer, S. M. Sterling, and N. J. Moore, “Human Appropriation of Photosynthesis Products,” Science 294 (2001): 2549–52; M. L. Imhoff et al., “Global Patterns in Human Consumption of Net Primary Production,” Nature 429 (2004): 870– 73; H. Haberl et al., “Quantifying and Mapping the Human Appropriation of Net Primary Production in Earth’s Terrestrial Ecosystems,” PNAS 104 (2007): 12942– 47; and

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Jonathan A. Foley, Chad Monfreda, Navin Ramankutty, and David Zaks, “Our Share of the Planetary Pie,” PNAS 104 (2007): 12585–86. For James Lovelock’s Gaia hypothesis, his books are the best places for background (some of the exaggerated criticisms could’ve been softened if his enemies had read them more carefully): Gaia: A New Look at Life on Earth (Oxford: Oxford University Press, 1979); and The Revenge of Gaia: Why the Earth Is Fighting Back—and How We Can Still Save Humanity (New York: Basic Books, 2006). For Gaia’s prediction of the end of life on our planet: James E. Lovelock and M. Whitfield, “Life Span of the Biosphere,” Nature 296 (1982): 561— 63; Ken Caldeira and James F. Kasting, “The Life Span of the Biosphere Revisited,” Nature 360 (1992): 721–23; and Timothy M. Lenton and Werner von Bloh, “Biotic Feedback Extends the Life Span of the Biosphere,” Geophysical Research Letters 28 (2001): 1715–18.

Chapter Five: Leaf Economics The Coleridge quote is from “The Aeolian Harp,” in Samuel Taylor Coleridge, Selected Poems (New York: Penguin Classics, 2000). The quote by Linnaeus was translated by Lisbet Koerner, Linnaeus, Nature and Nation (Cambridge, MA: Harvard University Press, 2001), from “Tanka rom grunden til oeconomien” (1740). The book from that 1984 conference: Thomas J. Givnish, ed., On the Economy of Plant Form and Function (New York: Cambridge University Press, 1986).

For Nehemiah Grew’s contribution to economics: Julian Hoppit, ed., Nehemiah Grew and England’s Economic Development: The Means of a Most Ample Increase of Wealth and Strength of England, 1706–7 (Oxford: Oxford University Press, 2012). Linnaeus’s Economy of Nature was actually published by his student Isaac Isaacson Biberg, defending a thesis in 1749 at the University of Uppsala, as Specimen academicum de Oeconomia Naturae. For information on Linnaeus and the economy of Nature: Frank N. Egerton, “A History of the Ecological Sciences, Part 23: Linnaeus and the Economy of Nature,” Bulletin of the Ecological Society of America, January 2007, 72–88; Lisbet Rausing, “Underwriting the Oeconomy: Linnaeus on Nature and Mind,” History of Political Economy 35 (2003): annual supplement 173–203; Stefan MullerWille, “Nature as a Marketplace: The Political Economy of Linnaean Botany,” History of Political Economy 35 (2003): annual supplement 154–72; and Geir Hestmark, “Oeconomia Naturae L.,” Nature 405 (2000): 19. For the connection of his ideas to Coleridge: James C. McKusick, “Coleridge and the Economy of Nature,” Studies in Romanticism 35 (1996): 375— 92; Robert Mitchell, “Adam Smith and Coleridge on the Love of Systems,” Coleridge Bulletin 25 (2005): 54–60. For Linnaeus’s connections to Adam Smith and Charles Darwin: Trevor Pearce, ‘‘A Great Complication of Circumstances— Darwin and the Economy of Nature,” JHB 43 (2010): 493– 528; Margaret Schabas, “Adam Smith’s Debts to Nature,” History of Political Economy 35 (2003): annual supplement 262–81; and Margaret Schabas, The Natural Origins of Economics (Chicago: University of Chicago Press, 2005). For my discussion of leaf construction costs, see F.W.T. Penning de Vries, A. H. M. Brunsting, and H. H. van Laar, “Products, Requirements and Efficiency

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of Biosynthesis: A Quantitative Approach,” JTB 45 (1974): 339–77; Kimberlyn Williams, F. Percival, J. Merino, and H. A. Mooney, “Estimation of Tissue Construction Cost from Heat of Combustion and Organic Nitrogen Content,” PCE 10 (1987): 725–34; and Hendrik Poorter and Rafael Villar, “The Fate of Acquired Carbon in Plants: Chemical Composition and Construction Costs,” in Plant Resource Allocation, ed. Fakhri A. Bazzaz and John Grace (New York: Academic Press, 1997), 39–71. For general trends in construction costs: Hendrik Poorter, Steeve Pepin, Toon Rijkers, Yvonne de Jong, John R. Evans, and Christian Körner, “Construction Costs, Chemical Composition and Payback Time of High- and Low-Irradiance Leaves,” JEB 57 (2006): 355–71; Rafael Villar and José Merino, “Comparison of Leaf Construction Costs in Woody Species with Differing Leaf Life-Spans in Contrasting Ecosystems,” NP 151 (2001): 213–26; Kimberlyn B. Williams, C. B. Field, and H. A. Mooney, “Relationships among Leaf Construction Cost, Leaf Longevity, and Light Environment in Rain Forest Plants of the Genus Piper,” AN 133 (1989): 198–211; and Z. Baruch and G. Goldstein, “Leaf Construction Cost, Nutrient Concentration, and Net CO2 Assimilation of Native and Invasive Species in Hawaii,” Oecologia 121 (1999): 183–92. For the more detailed discussion of coffee: Paulo C. Cavatte, Nelson F. Rodrıguez-Lopez, Samuel C. V. Martins, Mariela S. Mattos, Lılian M. V. P. Sanglard, and Fabio M. DaMatta, “Functional Analysis of the Relative Growth Rate, Chemical Composition, Construction and Maintenance Costs, and the Payback Time of Coffea arabica L. Leaves in Response to Light and Water Availability,” JEB 63 (2012): 3071–82. For leaf longevity, I consulted the following papers: Barbara L. Bentley, “Longevity of Individual Leaves in a Tropical Rainforest Under-Story,” AB 43 (1979): 119–21; Brian F. Chabot and David J. Hicks, “Ecology of Leaf Life Spans,” ARES 13 (1982): 229–59; P. B. Reich, M. B. Walters, and D. S. Ellsworth, “Leaf Life-Span in Relation to Leaf, Plant, and Stand Characteristics among Diverse Ecosystems,” EM 62 (1992): 365–92; R. W. Rogers and H. T. Clifford, “The Taxonomic and Evolutionary Significance of Leaf Longevity,” NP 123 (1993): 811– 21; and K. Kikuzawa and M. J. Lechowicz, Ecology of Leaf Longevity (Tokyo: Springer, 2011). For specific information about Welwitschia, see Klaus Winter and Michael J. Schramm, “Analysis of Stomatal and Non-Stomatal Components in the Environmental Control of CO2 Exchange in Leaves of Welwitschia mirabilis,” PP 82 (1986): 173–78; and John R. Henschel and Mary K. Seely, “Long-Term Growth Patterns of Welwitschia mirabilis, a Long-Lived Plant of the Namib Desert,” PE 150 (2004): 7–26. The following articles describe the path to the establishment of the worldwide leaf economics spectrum: Peter B. Reich, “Reconciling Apparent Discrepancies among Studies Relating Life Span, Structure and Function of Leaves in Contrasting Plant Life Forms and Climates: ‘The Blind Men and the Elephant Retold,’ ” FE 7 (1993): 721–25; Peter B. Reich, M. B. Walters, and D. S. Ellsworth, “From Tropics to Tundra: Global Convergence in Plant Functioning,” PNAS 94 (1997): 13730–34; and Ian J. Wright et al., “The Worldwide Leaf Economics Spectrum,” Nature 428 (2004): 821–27. For subsequent research and implications for this study: Ian J.

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Wright et al. “Modulation of Leaf Economic Traits and Trait Relationships by Climate,” GEB 14 (2005): 411–21; Bill Shipley, Martin J. Lechowicz, Ian Wright, and Peter B. Reich, “Fundamental Trade-Offs Generating the Worldwide Leaf Economics Spectrum,” Ecology 87 (2006): 535–41; William K. Cornwell et al. (30 coauthors), “Plant Species Traits Are the Predominant Control on Litter Decomposition Rates within Biomes Worldwide,” EL 11 (2006): 1065–71; P. S. Curtis and D. D. Ackerly, “Moving Beyond the Economics Spectrum?” NP 179 (2008): 901– 3; David Ackerly, “Conservatism and Diversification of Plant Functional Traits: Evolutionary Rates versus Phylogenetic Signal,” PNAS 106 (2009): 19699–706; Lisa A. Donovan, Hafiz Maherali, Christina M. Caruso, Heidrun Huber, and Hans de Kroon, “The Evolution of the Worldwide Leaf Economics Spectrum,” TREE 26 (2011): 88–95; J. Kattge et al. (134 coauthors), “TRY: A Global Database of Plant Traits,” GCB 17 (2011): 2905–35; Christoph Kueffer et al., “Fame, Glory and Neglect in Meta-Analyses,” TREE 26 (2011): 493–94; and Peter D. Reich, “The World-Wide ‘Fast-Slow’ Plant Economics Spectrum: A Traits Manifesto,” JE 102 (2014): 275–301. For the relation of the spectrum to plant evolution and litter fall decomposition: Guifang Liu et al., “Understanding the Ecosystem Implications of the Angiosperm Rise to Dominance: Leaf Litter Decomposability among Magnoliids and Other Angiosperms,” JE 102 (2014): 337–44; Erika J. Edwards, David S. Chatelet, Lawren Sack, and Michael J. Donohue, “Leaf Life Span and the Leaf Economic Spectrum in the Context of Whole Plant Architecture,” JE 102 (2014): 328–36; and William K. Cornwall et al., “Functional Distinctiveness of Major Plant Lineages,” JE 102 (2014): 345–56. For evergreen versus deciduous leaves: C. D. Monk, “An Ecological Significance of Evergreen-ness,” Ecology 47 (1966): 504–5; P. Moore, “The Advantages of Being Evergreen,” Nature 285 (1980): 535; Rien Aerts, “The Advantages of Being Evergreen,” TREE 10 (1995): 402–7; and Thomas J. Givnish, “Adaptive Significance of Evergreen vs. Deciduous Leaves: Solving the Triple Paradox,” Silva Fennica 36 (2002): 703–43. On the range of leaf sizes, I consulted Wayne Armstrong, “Wayne Armstrong’s Treatment of the Lemnaceae,” Palomar College San Diego, CA, 2012, http://waynesword.palomar.edu/1wayindx.htm; Elias Landolt, “204. Lemnaceae Gray. Duckweed Family,” in Flora North America, vol. 22 (www.floranorthamerica .org); and Francis Hallé, “The Longest Leaf in Palms?” Principes 21 (1977): 18. For the costs of larger leaves, see David E. Parkhurst and O. L. Loucks, “Optimal Leaf Size in Relation to Environment, “ JE 60 (1970): 505–37; Thomas J. Givnish and Geerat J. Vermeij, “Sizes and Shapes of Liane Leaves,” AN 110 (1976): 743–78; M. Pickup, M. Westoby, and A. Basden, “Dry Mass Costs of Deploying Leaf Area in Relation to Leaf Size,” FE 19 (2005): 88–97; David Kleiman and Lonnie W. Aarssen, “The Leaf Size/Number Trade- Off in Trees,” JE 95 (2007): 376– 82; Rubén Milla and Peter B. Reich, “The Scaling of Leaf Area and Mass: The Cost of Light Interception Increases with Leaf Size,” PRSB 274 (2007): 2109–14; and U. Niinemets, Angelika Portsmuth, David Tena, Mari Tobias, Silvia Matesanz, and

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Fernando Valladares, “Do We Underestimate the Importance of Leaf Size in Plant Economics? Disproportional Scaling of Support Costs within the Spectrum of Leaf Physiognomy,” AB 100 (2007): 283–303. For Corner’s rules on the size of branch tips and leaves, see David D. Ackerly and Michael J. Donoghue, “Leaf Size, Sapling Allometry, and Corner’s Rules: Phylogeny and Correlated Evolution in Maples (Acer),” AN 152 (1998): 767–91; and Mark E. Olson, Rebeca Aguirre-Hernández, and Julieta A. Rosell, “Universal Foliage- Stem Scaling across Environments and Species in Dicot Trees: Plasticity, Biomechanics and Corner’s Rules,” EL 12 (2009): 210–19. For controls on leaf size, see Kaare H. Jensen and Maciej A. Zwieniecki, “Physical Limits to Leaf Size in Tall Trees,” PRL 110 (2013); and Nathalie Gonzalez, Hannes Vanhaeren, and Dirk Inzé, “Leaf Size Control: Complex Coordination of Cell Division and Expansion,” TPS 17 (2012): 332–340. For articles on tea and yerba maté, I consulted Michael Harney, The Harney & Sons Guide to Tea (London: Penguin, 2008); for tea plantation agronomy: “Introduction to Harvesting or Plucking of Tea Shoots,” 2011, http://tea-plucking.blogspot .com/; Owuor P. Okinda, David M. Kamau, and Erick O. Jondiko, “Responses of Clonal Tea to Location of Production and Plucking Intervals,” Food Chemistry 115 (2009): 290–96; B. Eibli, R. A. Fernandez, J. C. Kozariki, A. Lupii, F. Montagnini, and D. Nozzii, “Agroforestry Systems with Ilex paraguariensis (American Holly or Yerba Mate) and Native Timber Trees on Small Farms in Misiones, Argentina,” Agroforestry Systems 48 (2000): 1–8; and “Yerba Mate,” Wikipedia, http://en .wikipedia.org/wiki/Yerba_mate. For representative articles on the economic importance of leaves as minor forest products, I consulted Henrik Balslev, Tina R. Knudsen, Anja Byg, Mette Kronborg, and César Grandez, “Traditional Knowledge, Use, and Management of Aphandra natalia (Arecaceae) in Amazonian Peru,” EB 64 (2010): 55–67; Samuel G. M. Bridgewater et al., “Chamaedorea (Xaté) in the Greater Maya Mountains and the Chiquibul Forest Reserve, Belize: An Economic Assessment of a Non-Timber Forest Product,” EB 60 (2006): 265–83; Leonel Lopez-Toledo, Christa Horn, and Antonio López-Cen, “Potential Management of Chamaedorea seifrizii (Palmae), a Non-Timber Forest Product from the Tropical Forest of Calakmul, Southeast Mexico,” EB 64 (2011): 55–67; J. Robert Hunter, “Tendu (Diospyros melanoxylon) Leaves, Bidi Cigarettes, and Resource Management,” EB 35 (1981): 450–59; Isabel B. Schmidt, Lisa Mandle, Tamara Ticktin, and Orou G. Gaoue, “What Do Matrix Population Models Reveal about the Sustainability of Non-Timber Forest Product Harvest?” JAE 48 (2011): 815–26; Maurício Sampaio, Isabel Belloni Schmidt, and Isabel Benedetti Fugueiredo, “Harvesting Effects and Population Ecology of the Buriti Palm (Mauritia flexuosa L. f., Arecaceae) in the Jalapão Region, Central Brazil,” EB 62 (2008): 171–81; Steven G. McKean, “Toward Sustainable Use of Palm Leaves by a Rural Community in Kwazulu-Natal, South Africa,” EB 57 (2003): 65–72; Michael Harney, The Harney & Sons Guide to Tea (London: Penguin, 2008); and Donald L. Hazlett and Jennifer C. Torres-Herrera, “Socioeconomic Value and Growth of Naturalized Musa balbisiana L. A. Colla Leaves in Honduras,” EB 66 (2012): 60–70.

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Scientific names of plants mentioned in order: coffee = Coffea arabica L. (Rubiaceae); Welwitschia = Welwitschia mirabilis Hook.f. (Welwitschiaceae); bristlecone pine = Pinus aristata Engelm. (Pinaceae); azolla = Azolla filiculoides Lam. (Salviniaceae); wolffia = Wolffia microscopica (Griff.) Kurz (Lemnaceae); raffia palm = Raphia farinifera (Gaertn.) N. Hylander (Arecaceae); talipot palm = Borassus flabellifer L. (Arecaceae); Victoria lily = Victoria amazonica (Poeppig) Sowerby (Nymphaeaceae); Monophyllaea = Monophyllaea horsefieldii R.Br. (Gesneriaceae); banana = Musa acuminata Colla (Musaceae); lettuce = Lactuca sativa L. (Asteraceae); kale = Brassica oleracea L. (Brassicaceae); tea = Camellia sinensis (L.) Kuntze (Theaceae); yerba maté = Ilex paraguariensis Aiton (Aquifoliaceae); tendu = Diospyros melanoxylon Roxb. (Ebenaceae); sabal palm = Sabal palmetto (Walter) Schultes & Schultes f. (Arecaceae).

Chapter Six: Metamorphosis The first quotation is from Goethe’s poem “The Metamorphosis of Plants,” translated and included in Johann Wolfgang von Goethe, The Metamorphosis of Plants (Cambridge, MA: MIT Press, 2009). The poem was written by Goethe in 1819 in reaction to Erasmus Darwin’s The Botanical Garden, and this response is discussed by Lisbet Koerner, “Goethe’s Botany: Lessons of a Feminine Science,” Isis 84 (1993): 470– 95. The second quote is from Sharon Black’s poem “Fibonacci Takes a Walk to Clear His Head,” published in her first book of poetry, To Know Bedrock (Kent, UK: Pindrop Press, 2011).

I used the definition for metamorphosis in the New Shorter Oxford English Dictionary (Oxford: Oxford University Press, 1993). For general information about early history, I used the articles on Plato, Aristotle, Socrates, and Pythagoras in Wikipedia. I cited Aristotle’s quotes from his “Metaphysics” 1– 5, from Aristotle’s Metaphysics, trans. H. Lawson-Tancred (New York: Penguin, 1998). Also see Robert J. Scully, The Demon and the Quantum (New York: Wiley, 2007); and Armand Marie Leroi, The Lagoon: How Aristotle Invented Science (New York: Viking, 2014). I was influenced in my discussions about the early history and philosophical underpinnings behind leaf development by the writings of Agnes Arbor, particularly her books The Natural Philosophy of Plant Form (Cambridge: Cambridge University Press, 1950) and The Mind and the Eye (Cambridge: Cambridge University Press, 1954). See Rudolph Schmid, “Agnes Arber, née Robertson (1879– 1960): Fragments of Her Life, Including Her Place in Biology and in Women’s Studies,” AB 88 (2001): 1105–28. For the comments of Theophrastus on leaves, see his Enquiry into Plants (New York: G. P. Putnam’s Sons, 1906). For Nehemiah Grew, his own great work is relatively easy to read and understand: Anatomy of Plants (London: W. Rawlings, 1682); and also see Jeanne Bolam, “The Botanical Works of Nehemiah Grew, F.R.S. (1641–1712),” Notes and Records of the Royal Society of London 27 (1973): 219–31; Brian Garrett, “Vitalism and Teleology in the Natural Philosophy of Nehemiah Grew (1641– 1712),” British Journal for the History of Science 36 (2003): 63–81; and Julian Hoppig, ed., Nehemiah Grew and England’s Economic Development: The Means of the Most Ample Increase of the Wealth and Strength of England, 1706–7 (Oxford: Oxford University Press, 2012). For Marcello Malpighi,

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I consulted his book Anatome plantarum (London: Johannis Martyn, 1675); and Domenico Bertoloni Meli, Mechanism, Experiment, Disease: Marcello Malpighi and SeventeenthCentury Anatomy (Baltimore: Johns Hopkins University Press, 2011). Agnes Arber wrote an analysis of their work and relationship: “Nehemiah Grew (1641– 1712) and Marcello Malpighi (1628– 1712): An Essay in Comparison,” Isis 34 (1942): 7–16. For general principles of leaf development, I used three recent publications throughout the discussion: Alison M. Smith et al., Plant Biology (New York: Taylor and Francis, 2010); Adrian Bell, Plant Form: An Illustrated Guide to Flowering Plant Morphology, new ed. (Portland, OR: Timber Press, 2008); and Quentin Cronk, The Molecular Organography of Plants (Oxford: Oxford University Press, 2009). For the crucial contributions of Wilhelm Hofmeister in the mid-nineteenth century: Donald R. Kaplan and Todd J. Cooke, “The Genius of Wilhelm Hofmeister: the Origin of Causal-Analytical Research in Plant Development,” AJB 83 (1996): 1647–60. For the historical interest in “monsters,” see M. T. Masters, Vegetable Teratology (London: Ray Society, 1869). For background on the use of Arabidopsis: G. P. Redei, “Arabidopsis as a Genetic Tool,” Annual Review of Genetics 9 (1975): 111–27; David W. Meinke, J. Michael Cherry, Caroline Dean, Steven D. Rounsley, and Maarten Koornneef, “Arabidopsis thaliana: A Model Plant for Genome Analysis,” Science 282 (1998): 662–81; and Elliot M. Meyerowitz, “Prehistory and History of Arabidopsis Research,” PP 125 (2001): 15– 19. For the molecular genetic controls on leaf primordium establishment and blade development, I consulted the books by Cronk and by Smith et al., both cited above, plus the following articles and reviews: Mary E. Byrne, “Making Leaves,” Current Opinion in Plant Biology 19 (2012): 24–30; Y. Eshed, A. Izhaki, S. F. Baum, S. K. Floyd, and J. L. Bowman, “Asymmetric Leaf Development and Blade Expansion in Arabidopsis Are Mediated by KANADI and YABBY Activities,” Development 131 (2004): 2997–3006; C. Jill Harrison et al., “Independent Recruitment of a Conserved Developmental Mechanism during Leaf Evolution,” Nature 434 (2005): 509–14; Stefan Jouannic, Myriam Collin, Benjamin Vidal, Jean-Luc Verdeil, and James W. Tregear, “A Class I KNOX Gene from the Palm Species Elaeis guineensis (Arecaceae) Is Associated with Meristem Function and a Distinct Mode of Leaf Dissection,” NP 174 (2007): 551–68; GyungTae Kim and Kiu-Hyung Cho, “Recent Advances in the Genetic Regulation of the Shape of Simple Leaves,” PPL 126 (2006): 494–502; and Brad T. Townsley and Neelima R. Sinha, “A New Development: Evolving Concepts in Leaf Ontogeny,” ARPB 63 (2012): 535–62. For the Rab gene family: Andrew Brighouse, Joel B. Dacks, and Mark C. Field, “Rab Protein Evolution and the History of the Eukaryotic Endomembrane System,” Cellular and Molecular Life Sciences 67 (2010): 3449–65; and Tobias H. Klöpper, Nickias Kienle, Dirk Fasshauer, and Sean Munro, “Untangling the Evolution of Rab G Proteins: Implications of a Comprehensive Genomic Analysis,” BMC Biology 10 (2012): 71–88. For the discussion of the evolution and development of leaves, I used the Cronk book, cited above, and the following articles: Paolo Piazza, Sophie Jasinski,

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and Miltos Tsiantis, “Evolution of Leaf Developmental Mechanisms,” NP 167 (2005): 693– 710; A. Hay and M. Tsiantis, “The Genetic Basis for Differences in Leaf Form between Arabidopsis thaliana and Its Wild Relative Cardamine hirsuta,” Nature Genetics 38 (2006): 942–47; C. A. Kidner, “Leaf Evolution: Working with What’s at Hand,” Evolution & Development 9 (2007): 321– 22; Tomoaki Nishiyama, “Evolutionary Developmental Biology of Non-Flowering Land Plants,” IJPS 168 (2007): 37–47; M. Alejandra Jaramillo and Elena M. Kramer, “The Role of Developmental Genetics in Understanding Homology and Morphological Evolution in Plants,” IJPS 168 (2007): 61– 72; Alexandru M. F. Tomescu, “Megaphylls, Microphylls and the Evolution of Leaf Development,” TPS 14 (2007): 5–12; and Jo Ann Banks, “Selaginella and 400 Million Years of Separation,” ARPB 60 (2009): 223–38. For controls on leaf size, particularly cell division versus cell expansion: books by Cronk and by Smith et al., cited above; and articles by Sarah Jane Cookson, Amandine Radziejwoski, and Christine Granier, “Cell and Leaf Size Plasticity in Arabidopsis: What Is the Role of Endoreduplication?” PCE 29 (2006): 1273–83; P. M. Donnelly, D. Bonetta, H. Tsukaya, R. E. Dengler, and N. C. Dengler, “Cell Cycling and Cell Enlargement in Developing Leaves of Arabidopsis,” DB 215 (1999): 407– 19; Michael Marcotrigiano, “A Role for Leaf Epidermis in the Control of Leaf Size and the Rate and Extent of Mesophyll Cell Division,” AJB 97 (2011): 224–33; Todd J. Cook and Bin Lu, “The Independence of Cell Shape and Overall Form in Multicellular Algae and Land Plants: Cells Do Not Act as Building Blocks for Constructing Plant Organs,” IJPS 153 (1992): S7– S27; Nathalie Gonzalez, Hannes Vanhaeren, and Dirk Inze, “Leaf Size Control: Complex Coordination of Cell Division and Expansion,” TPS 17 (2012): 332–40; and Christine Granier and François Tardieu, “Multi-Scale Phenotyping of Leaf Expansion in Response to Environmental Changes: The Whole Is More than the Sum of Its Parts,” PCE 32 (2009): 1175–84. For controls on stomatal density, see books by Cronk and by Smith et al.; plus Erica Klarreichy, “Computations of a New Leaf: Plants May Be Calculating Creatures,” Science News 165 (2004): 123–24. For control of compound leaf development, see book by Cronk, cited above; plus D. Hereven, D. T. Gutfinger, A. Parnis, Y. Eshed, and E. Lifschitz, “The Making of a Compound Leaf: Genetic Manipulation of Leaf Architecture in Tomato,” Cell 84 (1996): 735–44; Minsung Kim, Sheila McCormick, Marja Timmermans, and Neelima Sinha, “The Expression Domain of PHANTASTICA Determines Leaflet Placement in Compound Leaves,” Nature 424 (2003): 438–43; and Alexander D. Tattersall, Lynda Turner, Margaret R. Knox, Michael J. Ambrose, T. H. Noel Ellis, and Julie M. I. Hofer, “The Mutant Crispa Reveals Multiple Roles for PHANTASTICA in Pea Compound Leaf Development,” PC 17 (2005): 1046–60. For compound leaves with growing tips, see David A. Steingraeber and Jack B. Fisher, “Indeterminate Growth of Leaves in Guarea (Meliaceae): A Twig Analogue,” AJB 73 (1986): 852–62; and Richard F. Mueller, “Indeterminate Growth and Ramification of the Climbing Leaves of Lygodium japonicum (Schizeaceae),” AJB 70 (1983): 682–89.

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For a review on epiphylly, see T. A. Dickinson, “Epiphylly in Angiosperms,” BR 44 (1978): 181–232. For plantlets in Bryophyllum leaves: H. M. Garcês et al., “Evolution of Asexual Reproduction in Leaves of the Genus Kalanchoë,” PNAS 104 (2007): 15578–83. For flowers on leaves: Kwiton Jong, “The Evolution of Morphological Novelty Exemplified in the Growth Patterns of Some Gesneriaceae,” NP 75 (1975): 297–311. For information on heteroblasty, see book by Bell, cited above; and David W. Lee and J. H. Richards, “Heteroblastic Development in Vines,” in The Biology of Vines, ed. H. A. Mooney and F. H. Putz (New York: Cambridge University Press, 1991), 205–43. For general information on phyllotaxy, see book by Bell, cited above; and an early summary by C. Wright, “On the Uses and Origin of the Arrangements of Leaves in Plants,” Memoirs of the American Academy of Arts and Sciences 9 (1873): 379– 415. For the generation of phyllotaxis from primordia, especially the physiological mechanism, see M. Aida and M. Tasaka, “Morphogenesis and Patterning at the Organ Boundaries in the Higher Plant Shoot Apex,” Plant Molecular Biology 60 (2006): 915–28; Jan Traas Bennet, Jiĕi Friml, and Cris Kuhlenmeier, “Regulation of Phyllotaxis by Polar Auxin Transport,” Nature 426 (2003): 256– 60; D. J. Carr, “Positional Information in the Specification of Leaf, Flower and Branch Arrangement,” in Positional Controls in Plant Development, ed. P. W. Barlow and D. J. Carr (Cambridge: Cambridge University Press, 1984), 441–60; J. M. Chapman and R. Perry, “A Diffusion Model of Phyllotaxis,” AB 60 (1987): 377–89; S. Douady and Y. Couder, “Phyllotaxis as a Physical Self-Organized Process,” PRL 68 (1992): 2098–101; S. Douady and Y. Couder, “Phyllotaxis as a Dynamical Self- Organizing Process: Part II. The Spontaneous Formation of a Periodicity and the Co-existence of Spiral and Whorled Patterns,” JTB 178 (1996): 275–94; A. J. Fleming, “Formation of Primordia and Phyllotaxy,” COPB 8 (2005): 53–58; J. Friml, “Auxin Transport— Shaping the Plant,” COPB 6 (2003): 7–12; J. W. Mattsson. W. Ckurshumova, and T. Berleth, “Auxin Signaling in Arabidopsis Leaf Vascular Development,” PP 131 (2003): 1327–39; Richard S. Smith et al., “A Plausible Model of Phyllotaxis,” PNAS 103 (2006): 1301–6; and C. W. Wardlaw, “A Commentary on Turing’s DiffusionReaction Theory of Morphogenesis,” NP 52 (1953): 40–47. For the mathematics behind phyllotaxis, see the following articles in Wikipedia: Fibonacci, Fibonacci Number, and the Golden Ratio; as well as Paramand Singh, “The So-Called Fibonacci Numbers in Ancient and Medieval India,” Historia Mathematica 12 (1985): 229–44; and W. Schooling, “The Φ Progression,” in The Curves of Life, by T. A. Cook (London: Constance, 1914), 441–47. For more on phyllotaxis, especially history and limitations, see the good description by Philip Ball, Nature’s Patterns: Shapes (Oxford: Oxford University Press, 2011), chap. 6; L. Adler, D. Barabé, and R. V. Jean, “History of the Study of Phyllotaxis,” AB 80 (1997): 231–44; and Todd J. Cooke, “Do Fibonacci Numbers Reveal the Involvement of Geometrical Imperatives or Biological Interactions in Phyllotaxis?” BotJLS 150 (2006): 3–24. The following articles describe the mechanisms of packing to generate spirals: R. O. Erickson, “Tubular Packing of Spheres in Bio-

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logical Fine Structures,” Science 181 (1973): 705–16; Paul B. Green, C. S. Steele, and S. C. Rennich, “Phyllotactic Patterns: A Biophysical Mechanism for Their Origin,” AB 77 (1996): 515–27; and Didier Reinhardt et al., “Packing Efficiency in Sunflower Heads,” Mathematical Biosciences 58 (1982): 129–39. That phyllotaxis arrays leaves to maximize energy capture was argued by Karl Niklas in “The Role of Phyllotactic Pattern as a ‘Developmental Constraint’ on the Interception of Light by Leaf Surfaces,” Evolution 42 (1988): 1–16; and Karl Niklas, “Light Harvesting ‘Fitness Landscapes’ for Vertical Shoots with Different Phyllotactic Patterns,” in Symmetry in Plants, R. V. Jean and D. Barabé (Singapore: World Scientific, 1998), 759–73; and later by W. King, F. Beck, and U. Lüttge, “On the Mystery of the Golden Angle in Phyllotaxis,” PCE 27 (2004): 685–95. For more critical takes on phyllotactic spirals, see the Bell book and article by Cooke, cited above. For handedness, or chirality, in the direction of phyllotactic spirals, see A. Hudson, “Development of Symmetry in Plants,” ARPPPMB 51 (2000): 349–70; Antony Davis, “Fibonacci Numbers for Palm Foliar Spirals,” Acta Botanica Neerlandica 19 (1970): 249–56; Arthur L. Fredeen, Jeanne A. Horning, and Robert W. Madill, “Spiral Phyllotaxis of Needle Fascicles on Branches and Scales on Cones in Pinus contorta var. latifolia: Are They Influenced by Wood-Grain Spiral?” CJB 80 (2002): 166–75; Peter V. Minorsky, “Latitudinal Differences in Coconut Foliar Spiral Direction: A Re- evaluation and Hypothesis,” AB 82 (1998): 133– 40; and Peter V. Minorsky and Natalie B. Bronstein, “Natural Experiments Indicate that Geomagnetic Variations Cause Spatial and Temporal Variations in Coconut Palm Asymmetry,” PP 142 (2006): 40–44. For general background on Goethe’s life, I used the article in Wikipedia (http:// en.wikipedia.org/wiki/Johann_Wolfgang_von_Goethe); Johann Peter Eckerman, Conversations of Goethe with Johann Peter Eckerman (1848; reprint, New York: Di Capo Press, 1998); and Gordon L. Miller’s introduction in Johann Wolfgang von Goethe, The Metamorphosis of Plants (Cambridge, MA: MIT Press, 2009, from translation by Douglas Miller, of the 1790 edition). For the discussion of Goethe’s contributions to botany and morphology, see Enrico Coen, “Goethe and the ABC Model of Flower Development,” Comptes Rendus de l’Academie des Sciences Series III: Sciences de la Vie [Life Sciences] 324 (2001): 523–30; Astrid Orle Tantillo, The Will to Create: Goethe’s Philosophy of Nature (Pittsburgh: University of Pittsburgh Press, 2002); Brady Bowman, “Goethean Morphology, Hegelian Science: Affinities and Transformations,” Goethe Yearbook 18 (2011): 159–81; Elizabeth Millán, “The Quest for the Seeds of Eternal Growth: Goethe and Humboldt’s Presentation of Nature,” Goethe Yearbook 18 (2011): 97–114; Lisbet Koerner, “Goethe’s Botany: Lessons of a Feminine Science,” Isis 84 (1993): 470–95; Thomas Pfau, “All Is Leaf: Difference, Metamorphosis, and Goethe’s Phenomenology of Knowledge,” Studies in Romanticism 49 (2010): 3–41; and Nicolas Robin, “Heritage of the Romantic Philosophy in Post-Linnaean Botany: Reichenbach’s Reception of Goethe’s ‘Metamorphosis of Plants’ as a Methodological and Philosophical Framework,” JHB 44 (2011) 44: 283–304. For the establishment of Amborella as sister to the earliest angiosperms: Sarah

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Mathews and Michael J. Donoghue, “The Root of Angiosperm Phylogeny Inferred from Duplicate Phytochrome Genes,” Science 286 (1999): 947–50; and M. J. Zanis, D. E. Soltis, P. S. Soltis, S. Mathews, and M. J. Donoghue, “The Root of Angiosperms Revisited,” PNAS 99 (2002): 6848–53. For the ABC model of floral development, see Elliot M. Meyerowitz, D. R. Smyth, and J. L. Bowman, “Abnormal Flowers and Pattern-Formation in Floral Development,” Development 106 (1989): 209–17; and Enrico S. Coen and Elliot M. Meyerowitz, “The War of the Whorls: Genetic Interactions Controlling Flower Development,” Nature 353 (1991): 31–37. For the application of the ABC model to all flowering plants, see M. Buzgo, P. S. Soltis, and D. E. Soltis, “Floral Developmental Morphology of Amborella trichopoda (Amborellaceae),” IJPS 165 (2004): 925–47; and D. E. Soltis, A. S. Chanderbali, S. Kim, M. Buzgo, and P. S. Soltis, “The ABC Model and Its Applicability to Basal Angiosperms,” ABS 100 (2007): 155–63. For fossil evidence of auxin function, see Gar W. Rothwell and Simcha Lev-Yadun, “Evidence of Polar Auxin Flow in 375 Million-Year-Old Fossil Wood,” AJB 92 (2005): 903–6. The excellent progress we have made in using physical and chemical foundations to understand plant biology is seen in two recent University of Chicago Press titles: Steven Vogel, The Life of a Leaf (Chicago: University of Chicago Press, 2012); and Karl J. Niklas and Hanns-Christof Spatz, Plant Physics (Chicago: University of Chicago Press, 2012). For examples of mathematical rules in plant and leaf development, see Darcy A. W. Thompson, On Growth and Form, 2nd ed. (Cambridge: Cambridge University Press, 1942); P. Prusinkiewicz and L. Lindenmayer, The Algorithmic Beauty of Plants (New York: Springer Verlag,1990); and Györgi Doczi, The Power of Limits: Proportional Harmonies in Nature, Art and Architecture (Boulder, CO: Shambala, 1981). For criticisms of the general solutions to complex problems, see Stuart Kaufmann, At Home in the Universe: The Search for the Laws of Self-Organization and Complexity (New York: Oxford University Press, 1996). For the problem of emergence: Marcelo Gleiser, A Tear at the Edge of Creation: A Radical New Vision for Life in an Imperfect Universe (New York: Free Press, 2010). For our impatience for answers to complex questions: V. S. Ramachandran, The Tell-Tale Brain (New York: Norton, 2011). For an appreciation about how the brain’s structure might influence preferences for aesthetic solutions: Roland Fischer, “A Cartography of the Ecstatic and Meditative States,” Science 174 (1971): 897–904. For leaf senescence and death, including senescence during leaf expansion, see Susheng Gan, ed., Senescence Processes in Plants, Annual Plant Reviews, vol. 26 (Oxford: Blackwell Publishing, 2008); Howard Thomas, Lin Huang, Mike Thomas, and Helen Ougham, “Evolution of Plant Senescence,” BMC Evolutionary Biology 9 (2009): 163, doi:10.1186/1471-2148-9-163; H. L. Arunika and A. N. Gunawardena, “Programmed Cell Death and Tissue Remodeling in Plants,” JEB 59 (2008): 445– 51; H. L. Arunika, A. N. Gunawardena, John S. Greenwood, and Nancy G. Dengler, “Programmed Cell Death Remodels Lace Plant Leaf Shape during Development,” PC 16 (2004): 60–73; Christina E. N. Lord, H. L. Arunika, and A. N. Gunawar-

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dena, “The Lace Plant: A Novel Model System to Study Plant Proteases during Developmental Programmed Cell Death in Vivo,” PPL 145 (2012): 114–20; and H. L. Arunika, A. N. Gunawardena, Kathy Sault, Petra Donnelly, John S. Greenwood, and Nancy G. Dengler, “Programmed Cell Death and Leaf Morphogenesis in Monstera obliqua (Araceae),” Planta 221 (2005): 607–18. The scientific names of plants in this chapter, mentioned in order by common name: edible fig = Ficus carica (L.) Moraceae; borage = Borago officinalis L. (Boraginaceae); grape vine = Vitis vinifera L. (Vitaceae); common bean = Phaseolus vulgaris L. (Fabaceae); mallow = Malva parviflora L. (Malvaceae); copper leaf = Acalypha amentacea Roxb. var. “heterophylla” (Euphorbiaceae); thale cress = Arabidopsis thaliana (L.) Heynh. (Brassicaceae); kale = Brassica oleracea L. (Brassicaceae); spike moss = Selaginella sp. (Selaginellaceae, Lycophyta); Guarea = Guarea cf. guidonia (L.) Sleumer (Meliaceae); Old World climbing fern = Lygodium microphyllum (Cav.) R. Br. (Schizeaceae); Angiopteris = Angiopteris evecta (Forster f.) Hoffm. (Marattiaceae); wild coffee = Psychotria nervosa Sw. (Rubiaceae); Arabian coffee = Coffea arabica L. (Rubiaceae); traveler’s palm = Ravenala madagascariensis Sonn. (Strelitziaceae); screwpine = Pandanus cf. utilis Bory (Pandanaceae); sunflower = Helianthus annuus L. (Asteraceae); dinner plate plant = Aeonium urbicum (C.Sm. ex Hornem.) Webb & Berthel. (Crassulaceae); European fan palm = Chamaerops humilis L. (Arecaceae); Amborella tree = Amborella trichopoda Baill. (Amborellaceae); snapdragon = Antirrhinum majus L. (Scrophulariaceae); Monophyllaea = Monophyllaea cf. horsefieldii R. Br. (Gesneriaceae); bryophyllum = Kalenchoe cf. delagoensis Ecklon & Zeyher (Crassulaceae); cat’s claw vine = Dolichandra unguis- cati (L.) L. Lowman (Bignoniaceae); Swiss cheese vine = Monstera cf. obliqua Miq. (Araceae); lace plant = Aponogeton Madagascariensis (Mirbel) Bruggen (Aponogetonaceae).

Chapter Seven: Architecture The quotes of poetry at the beginning of the chapter are from Kathleen Raine, “Envoi,” Collected Poems of Kathleen Raine (Ipswich, Suffolk, UK: Golgonooza Press, 2008); and Linda Pastan, “Vertical,” Ploughshares 33 (2007/2008): 152. For the definition of “architecture,” I used the New Oxford Dictionary of English (Oxford: Oxford University Press, 2001). For information on Leonardo da Vinci, I used Wikipedia (http://en.wikipedia .org/wiki/Leonardo_da_Vinci); William A. Emboden, Leonardo da Vinci on Plants and Gardens (Portland, OR: Dioscorides Press, 1985); Leonardo da Vinci, The Notebooks of Leonardo da Vinci, arranged and introduced by Jean Paul Richter (New York, Dover, 1970); and Leonardo da Vinci, The Notebooks of Leonardo da Vinci, vol. 1 (New York: Reynal & Hitchcock, 1939), arranged, translated, and introduced by Edward MacCurdy. For Owen Jones: his biography in Wikipedia, http://en.wikipedia.org/wiki/Owen_Jones_ (architect), and his masterful book, The Grammar of Ornament (1856; reprint, New York: Van Nostrand Reinhold, 1982). For Joseph Paxton and the Crystal Palace, I relied on excellent Wikipedia articles: http://en.wikipedia.org/wiki/Joseph_Paxton and http://en .wikipedia.org/wiki/The_Crystal_Palace. For the two contemporary examples of archi-

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tectural projects based on leaf structure, see www.inhabitat.com/brazilian-leaf-house -by-mareines-and-patalano/, for the Brazilian house; and www.vincent.callebaut.org /page1-img-lilypad.html, for the utopian floating cities.

For the life and work of Antoni Gaudí, I consulted his Wikipedia biography (http://en.wikipedia.org/wiki/Antoni_Gaudi); Juan José Lahuerta, Antoni Gaudí, 1853– 1926: Architecture Ideology and Politics (Milan: Electo, 1992); and Joan Bergós, Gaudí: The Man and His Work (Boston: Little, Brown & Company, 1999). For Louis Sullivan, I consulted his Wikipedia biography (https://en.wikipedia.org/wiki/Louis _Sullivan) and two critical works: Robert Twombley, Louis Sullivan: His Life and Work (Chicago: University of Chicago Press, 1986); and Lauren S. Weingareden, Louis H. Sullivan and a 19th-Century Poetics of Naturalized Architecture (Burlington, VT: Ashgate, 2009). The Sullivan quote on design and nature is from his book Kindergarten Chats (Revised 1918) and Other Writings (New York: George Wittenborn, 1947). For John Ruskin, I consulted his Wikipedia biography (https://en.wikipedia.org/wiki/John _Ruskin) and Kristine Ottesen Garrigan, Ruskin on Architecture: His Thought and Influence (Madison: University of Wisconsin Press, 1973). My FIU colleague Gray Read helped me with the architectural history. My biographical knowledge of Francis Hallé is grounded in a 37-year friendship and a short biography written for my translation of his book: Francis Hallé, In Praise of Plants (Portland, OR: Timber Press, 2008). The article by E. J. H. Corner that influenced Hallé: “The Durian Theory or the Origin of the Modern Tree,” AB 13, n.s. (1949): 367– 414. Hallé’s original system was described with Roelof A. A. Oldeman, Essai sur l’architecture et la dynamique de croissance des arbres tropicaux (Paris: Masson, 1971), translated by Benjamin C. Stone as Essay on the Architecture and Growth of Tropical Trees (Kuala Lumpur: University of Malaya Press, 1973), but it became more widely appreciated from Francis Hallé, Roelof A. A. Oldeman, and P. Barry Tomlinson, Tropical Trees and Forests: An Architectural Analysis (Berlin: Springer-Verlag, 1978). For the view of a plant as a population of meristems, see J. White, “The Plant as a Metapopulation,” ARES 10 (1979): 109– 45; Diddahally R. Govindaraju, David B. Wagner, Graydon P. Smith, and Bruce P. Dancik, “Chloroplast DNA Variation within Individual Trees of a Pinus banksiana–Pinus conforta Sympatric Region,” Canadian Journal of Forest Research 18 (1988): 1347– 50; and Brett P. Olds, Patrick J. Mulrooney, and Ken N. Paige, “Somatic Mosaicism in Populus trichocarpa Leads to Evolutionary Change,” the Preliminary Program for 97th ESA Annual Meeting (August 5–10, 2012). For the architecture of herbs, I used Adrian D. Bell, Plant Form: An Illustrated Guide to Flowering Plant Morphology, new ed. (Portland, OR: Timber Press, 2008); Adrian D. Bell, “Computerized Vegetative Mobility in Rhizomatous Plants,” in Automata, Languages and Development, A. Lindenmayer and G. Rosenberg (Amsterdam: North HoIland, 1976), 3–14; and Adrian D. Bell and P. Barry Tomlinson, “Adaptive Architecture in Rhizomatous Plants,” BotJLS 80 (1980): 125–60. For coral architecture: P. M. Dauget, “Applications of Tree Architectural Models to Coral Reef Growth Forms,” Marine Biology 111 (1991): 157–65; and Paulina Kaniewska, Ken-

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neth R. N. Anthony, and Ove Hoegh-Guldberg, “Variation in Colony Geometry Modulates Internal Light Levels in Branching Corals, Acropora humilis and Stylophora pistillata,” Marine Biology 155 (2008): 649–60. For information about Henry Horn and his contributions to tree architecture: Henry S. Horn, The Adaptive Geometry of Trees (Princeton, NJ: Princeton University Press, 1971); Eric R. Pianka and Henry S. Horn, “Ecology’s Legacy from Robert MacArthur,” in Ecological Paradigms Lost: Routes of Theory Change, ed. Kim Cuddington and Beatrix E. Beisner (New York: Elsevier Academic Press, 2005); and I obtained further biographical information through e-mail correspondence with Horn. The following reviews cover the extensive literature on tree architecture summarized in this chapter: P. de Reffye, C. Edelin, J. Francon, M. Jaeger, and C. Puech, “Plant Models Faithful to Botanical Structure and Development,” Computer Graphics 22 (1988): 151–58; Jack B. Fisher, “How Predictive Are Computer Simulations of Tree Architecture?” IJPS 153 (1992): S137–S146; R. Sievanen, E. Nikinmaa, P. Nygren, H. Ozier-Lafontaine, J. Perttunen, and H. Hakula, “Components of FunctionalStructural Tree Models,” Annales of Forest Science 57 (2000): 399– 412; Christophe Godin, “Representing and Encoding Plant Architecture: A Review,” Annales of Forest Science 57 (2000): 413– 38; F. J. Sterck, F. Schieving, A. Lemmens, and T.L. Pons, “Performance of Trees in Forest Canopies: Explorations with a Bottom-Up Functional-Structural Plant Growth Model,” NP 166 (2005): 827–43; C. Turnbull, Plant Architecture and Its Manipulation, Annual Plant Reviews, vol. 17 (Oxford: Blackwell Publishing, 2005); M. T. Allen, P. Prusinkiewicz, and T. M. DeJong, “Using L-Systems for Modeling Source-Sink Interactions, Architecture and Physiology of Growing Trees: The L-PEACH Model,” NP 166 (2005): 869–80; T. Fourcaud, X. P. Zhang, A. Stokes, H. Lambers, and C. Korner, “Plant Growth Modeling and Applications: The Increasing Importance of Plant Architecture in Growth Models,” AB 101 (2008): 1053– 63; Przemysław Prusinkiewicz and Adam Runions, “Computational Models of Plant Development and Form,” NP 193 (2012): 549– 69; and Yan Guo, Thierry Fourcaud, Marc Jaeger, Xiaopeng Zhang, and Baoguo Li, “Plant Growth and Architectural Modelling and Its Applications,” AB 107 (2011): 723–727. For documentation of the architectural analysis of the pagoda tree: Jack B. Fisher, “A Quantitative Study of Terminalia Branching,” in Tropical Trees as Living Systems, ed. P. B. Tomlinson and Martin H. Zimmerman (New York: Cambridge University Press, 1978), 285–320; Jack B. Fisher and Hisao Honda, “Computer Simulation of Branching Pattern and Geometry in Terminalia (Combretaceae), a Tropical Tree,” Botanical Gazette 138 (1977): 377– 84; Jack B. Fisher and Hisao Honda, “Branch Geometry and Effective Leaf Area: A Study of Terminalia Branching Pattern. I. Theoretical Trees,” AJB 66 (1979): 633–44; and Jack B. Fisher and Hisao Honda, “Branch Geometry and Effective Leaf Area: A Study of TerminaliaBranching Pattern. II. Survey of Real Trees,” AJB 66 (1979): 645–55. Three widely cited articles beautifully described how adjustment of branch- length angle and length- optimized light capture by the flat branches: Hisao Honda and Jack B.

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Fisher, “Tree Branch Angle: Maximizing Effective Leaf Area,” Science 199 (1978): 888– 90; Hisao Honda and Jack B. Fisher, “Ratio of Tree Branch Length: The Equitable Distribution of Leaf Clusters on Branches,” PNAS 76 (1978): 3875–79; and P. B. Tomlinson, “Tree Architecture,” American Scientist 71 (1983): 141–49.For the costs and benefits of tree architecture, see Robert W. Pearcy, Hiroyuki Muraoka, and Fernando Valladares, “Crown Architecture in Sun and Shade Environments: Assessing Function and Trade-offs with a Three-Dimensional Simulation Model,” NP 166 (2005): 791–800. For the plasticity and crown characteristics within a single architectural model, see Jack B. Fisher and David E. Hibbs, “Plasticity of Tree Architecture: Specific and Ecological Variations Found in Aubreville’s Model,” AJB 69 (1982): 690–702. For effects of leaf angle on light penetration: Juan M. Posada, Martin J. Lechowicz, and Kaoru Kitajima, “Optimal Photosynthetic Use of Light by Tropical Tree Crowns Achieved by Adjustment of Individual Leaf Angles and Nitrogen Content,” AB 103 (2009): 795–805. For a discussion of reiteration, see Hallé, Oldeman, and Tomlinson, cited above. For scaling from crown to canopy, there is much to learn, but important contributions nonetheless: Boris Zeide, “Unit of the Tree Crown,” Ecology 74 (1993): 1598– 602; Heather Fish, Victor J. Lieffers, Uldis Silins, and Ronald J. Hall, “Crown Shyness in Lodgepole Pine Stands of Varying Stand Height, Density, and Site Index in the Upper Foothills of Alberta,” Canadian Journal of Forest Research 36 (2006): 2104–11; M. Rudnicki, U. Silins, V.J. Lieffers, and G. Josi, “Measure of Simultaneous Tree Sways and Estimation of Crown Interactions among a Group of Trees,” Trees— Structure and Function 15 (2001): 83–90; Francis E. Putz, G. G. Parker, and R. M. Archibald, “Mechanical Abrasion and Intercrown Spacing,” American Midland Naturalist 112 (1984): 24–28; Drew Purves and Stephen Pacala, “Predictive Models of Forest Dynamics,” Science 320 (2008): 1452–355; Drew W. Purves, J. W. Lichstein, and Stephen W. Pacala, “Crown Plasticity and Competition for Canopy Space: A New Spatially Implicit Model Parameterized for 250 North American Tree Species,” PLoS ONE 2 (2007): e870, doi:10.1371/journal.pone.0000870; Charles D. Canham, Michael J. Papaik, Maria Uriarte, William H. McWilliams, and Jennifer C. Jenkins, “Neighborhood Analyses of Canopy Tree Competition Along Environmental Gradients in New England Forests,” Ecological Applications 16 (2006): 540–54; Stanley R. Herwitz, Robert E. Slye, and Stephen M. Turton, “Long- Term Survivorship and Crown Area Dynamics of Tropical Rain Forest Canopy Trees,” Ecology 81 (2000): 585–97; Xavier Morin, “Species Richness Promotes Canopy Packing: A Promising Step towards a Better Understanding of the Mechanisms Driving the Diversity Effects on Forest Functioning,” FE 29 (2015): 993–94; and James R. Kellner and Gregory P. Asner, “Winners and Losers in the Competition for Space in Tropical Forest Canopies,” EL 17 (2014): 556–62. For comprehensive discussions of plant biomechanics, see Karl, J. Niklas, Plant Biomechanics: An Engineering Approach to Plant Form and Function (Chicago: University of Chicago Press, 1992); and Karl J. Niklas and Hanns-Christof Spatz, Plant Physics (Chicago: University of Chicago Press, 2012). For leaf biomechanics: Karl J. Niklas,

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“A Mechanical Perspective on Foliage Leaf Form and Function,” NP 143 (1999): 19–31. For background on the discussion about the biomechanics of architecture in understory plants, see Arielle M. Cooley, Alexandra Reich, and Philip Rundel, “Leaf Support Biomechanics of Neotropical Understory Herbs,” AJB 91 (2004): 573– 81; Robin L. Chazdon, “The Costs of Leaf Support in Understory Palms: Economy versus Safety,” AM 127 (1986): 9–30; Thomas J. Givnish, “Biomechanical Constraints on Canopy Geometry in Forest Herbs,” in On the Economy of Plant Form and Function, ed. T. J. Givnish (Cambridge: Cambridge University Press, 1986), 525–83; Zygmunt Hejnowicz and Wilhelm Barthlott, “Structural and Mechanical Peculiarities of the Petioles of Giant Leaves of Amorphophallus (Araceae),” AJB 92 (2005): 391–403; Karl J. Niklas, “Biomechanical Responses of Chamaedorea and Spathiphyllum Petioles to Tissue Dehydration,” AB 67 (1991): 67–76; and P. Barry Tomlinson, James Horn, and Jack Fisher, The Anatomy of Palms (New York: Oxford University Press, 2011). For the comparison of the panicled aster and the Canada goldenrod, see B. Schmid and F. A. Bazzaz, “Crown Construction, Leaf Dynamics, and Carbon Gain in Two Perennials with Contrasting Architecture,” Ecological Monographs 64 (1994): 177–203. For rhubarb petioles: D. Pasini, “On the Biological Shape of the Polygonaceae Rheum Petiole,” International Journal of Design and Nature and Ecodynamics 3 (2008): 39–64. For the agronomic importance of plant architecture, see E. Costes, P. É. Lauri, and J. L. Regnard, “Analyzing Fruit Tree Architecture: Implications for Tree Management and Fruit Production,” Horticultural Reviews 32 (2006): 1–61; J. Vos, F. B. Evers, G. H. Buck- Sorlin, B. Andrieu, M. Chelle, and P. H. B. de Visser, “Functional-Structural Plant Modelling: A New Versatile Tool in Crop Science,” JEB 61 (2010): 2101–15. For the ending discussion on Leonardo da Vinci’s description of branching, put on a scientific basis, see Kosei Sone, Alata Antonio Suzuki, Shin- Ichi Miyazawa, Ko Noguchi, and Ichiro Terashima, “Maintenance Mechanisms of the Pipe Model Relationship and Leonardo da Vinci’s Rule in the Branching Architecture of Acer rufinerva Trees,” Journal of Plant Research 122 (2009): 41– 52; and Christophe Eloy, “Leonardo’s Rule, Self-Similarity, and Wind-Induced Stresses in Trees,” PRL 107 (2011), doi: http://dx.doi.org/10.1103/PhysRevLett.107.258101. Scientific names of plants mentioned in order in chapter: elm = Ulmus glabra Hudson (Ulmaceae); cherry tree = Prunus cerasus L. (Rosaceae); walnut = Juglans regia L. (Juglandaceae); Amazon lily = Victoria amazonica (Poeppig) Sowerby (Nymphaeaceae); water lily = Nymphaea odorata Aiton (Nymphaeaceae); rubber tree = Hevea brasiliensis (A.Juss.) Muell. Arg. (Euphorbiaceae); sumac = Rhus typhina L. (Anacardiaceae); frangipani = Plumeria rubra L. (Apocynaceae); poinciana = Delonix regia (Hook.) Raf. (Fabaceae); red-osier dogwood = Cornus sericea L. (Cornaceae); American beech = Fagus grandifolia Ehrh. (Fagaceae); red oak = Quercus rubra L. (Fagaceae); red maple = Acer rubrum L. (Sapindaceae); Indian almond, pagoda tree = Terminalia catappa L. (Combretaceae); May apple = Podophyllum peltatum L. (Berberi-

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daceae); Amorphophallus = Amorphophallus paeonifolius (Dennst.) Nicolson (Araceae); peacock begonia = Begonia pavonina Ridl. (Begoniaceae); rhubarb = Rheum raponticum L. (Polygonaceae); Canada goldenrod = Solidago Canadensis L. (Asteraceae); panicled aster = Symphyotrichum lanceolatum (Willd.) G. L. Nesom (Asteraceae); apple = Malus pumila Mill. (Rosaceae).

Chapter Eight: Shapes and Edges The quotes at the beginning of the chapter are from Henry David Thoreau, “A Week on the Concord and Merrimack Rivers,” in The Portable Thoreau (New York: Viking Press, 1964); and dialogue from Tom Stoppard’s play Arcadia (London: Faber & Faber, 1993). Volkmar Vareschi’s descriptions of Venezuelan vegetation are in Vegetations-ökologie der Tropen (Stuttgart: Verlag Eugen Ulmer, 1980). For Humboldt on plant distributions with Aimé Bonpland, Essay on the Geography of Plants, trans. Sylvie Romanowski (Chicago: University of Chicago Press, 2009). Theophrastus described leaf shapes in his Inquiry into Plants, trans. Sir Arthur Hort (New York: G. P. Putnam & Sons, 1916). For a thorough discussion of the school of physiological anatomy, see Eugene Cittadino, Nature as Laboratory: Darwinian Plant Ecology in the German Empire, 1880–1900 (Cambridge: Cambridge University Press, 1990). I also consulted Gottfried Haberlandt, Physiological Plant Anatomy, trans. Montagu Drummond (London: Macmillan and Company, 1914); Alfred F. W. Schimper, Plant-Geography upon a Physiological Basis, trans. William R. Fisher (New York: University of Oxford Press, 1903); and E. Stahl, “Über Bunte Laubblätter: Ein Beitrag zur pflanzenbiologie II,” Annales du Jardin Botanique de Buitenzorg 13 (1896): 137–216.

For the discussion on the molecular biology of leaf shape and margin development, I used the following articles: Mary Byrne, Marja Timmermans, Catherine Kidner, and Rob Martienssen, “Development of Leaf Shape,” COPB 4 (2001): 38–43; Daniel Koenig and Neelima Sinha, “Evolution of Leaf Shape: A Pattern Emerges,” Current Topics in Developmental Biology 91 (2010): 169–83; Nancy Dengler and Julie Kang, “Vascular Patterning and Leaf Shape,” COPB 4 (2001): 50–56; E. Kawamura, G. Horiguchi, and H. Tsukaya, “Mechanisms of Leaf Tooth Formation in Arabidopsis,” Plant Journal 62 (2010): 429–41; Enrico Scarpella, Michalis Barkoulas, and Miltos Tsiantis, “Control of Leaf and Vein Development by Auxin,” Cold Spring Harbor Perspectives in Biology 2 (2010): a001511; Adrienne B. Nicotra et al., “The Evolution and Functional Significance of Leaf Shape in the Angiosperms,” FPB 38 (2011): 535–52; and Maya Bar and Naomi Ori, “Compound Leaf Development in Model Plant Species,” COPB 23 (2015): 61–69. For plasticity of leaf shape within species induced by environmental factors, I used A. H. Di Benedetto and D. H. Cogliatti, “Effects of Light Intensity and Quality on the Obligate Shade Plant Aglaonema commutatum: I. Leaf Size and Leaf Shape,” Journal of Horticultural Science 65 (1990): 689–98; Daniel Buisson and David W. Lee, “The Developmental Responses of Papaya Leaves to Simulated Canopy Shade,” AJB 80 (1993): 947–52; Cynthia S. Jones, “Does Shade Prolong Juvenile Development? A Morphological Analysis of Leaf Shape Changes in Cucurbita argyrosperma subsp. sororia (Cucurbitaceae),” AJB 82 (1995): 346– 59; David W. Lee, “Simulat-

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ing Forest Shade to Study the Developmental Ecology of Tropical Plants: Juvenile Growth in Three Vines,” JTE 4 (1988): 281–92; David W. Lee et al., “Effects of Irradiance and Spectral Quality on the Development of two Hopea Species,” Oecologia 110 (1997): 1– 9; David W. Lee et al., “Effects of Irradiance and Spectral Quality on Leaf Structure and Function in Seedlings of Two Southeast Asian Hopea Species,” AJB 87 (2000): 447– 55; and Maciej Zwieniecki, C. Kevin Boyce, and Noel Michele Holbrook, “Hydraulic Limitations Imposed by Crown Placement Determine Final Size and Shape of Quercus rubra L. Leaves,” PCE 27 (2004): 357– 65; and Dana L. Royer, Laura A. Meyerson, Kevin M. Robertson, and Jonathan M. Adams, “Phenotypic Plasticity of Leaf Shape Along a Temperature Gradient in Acer rubrum,” PLoS ONE 4 (2009): e7653, doi:10.1371/journal.pone.0007653. For genetically controlled changes in leaf shape within an individual: Cynthia S. Jones and M. A. Watson, “Heteroblasty and Preformation in Mayapple, Podophyllum peltatum (Berberidaceae): Developmental Flexibility and Morphological Constraint,” AJB 88 (2001): 1340–58; Cynthia S. Jones, “An Essay on Juvenility, Phase Change and Heteroblasty in Seed Plants,” IJPS 160 (1999): S105–S111; and David W. Lee and Jennifer H. Richards, “Heteroblastic Development in Vines,” in The Biology of Vines, ed. H. A. Mooney and F. H. Putz (New York: Cambridge University Press, 1991), 205–43. For anisophylly: Nancy G. Dengler, “Anisophylly and Dorsiventral Shoot Symmetry,” IJPS 160 (1999): S67–S80. For general information on leaf morphology and the evolutionary record, I used Thomas N. Taylor, Edith L. Taylor, and Michael Krings, Paleobotany. The Biology and Evolution of Fossil Plants, 2nd ed. (New York: Elsevier, 2009). For information on leaf shapes in evolution: W. I. Crepet, D. C. Nixon, and M. A. Gandolfo, “Fossil Evidence and Phylogeny: The Age of Major Angiosperm Clades Based on Mesofossil and Macrofossil Evidence from Cretaceous Deposits,” AJB 91 (2004): 1666–82; J. A. Doyle, “Systematic Value and Evolution of Leaf Architecture Across the Angiosperms in Light of Molecular Phylogenetic Analyses,” Courier ForschungeInstitut Senckenberg 258 (2007): 21– 37; and K. J. Johnson and B. Ellis, “A Tropical Rainforest in Colorado 1.4 million Years after the Cretaceous-Tertiary Boundary,” Science 296 (2002): 2379–83. For leaf fossils in the Eocene floras of the Northwest, see R. J. Burnham, “Palaeoecological and Floristic Heterogeneity in the PlantFossil Record— an Analysis Based on the Eocene of Washington,” U.S. Geological Survey Bulletin 2085B (1994): 1–25; J. A. Wolfe and W. Wehr, “Middle Eocene Dicotyledonous Plants from Republic, Northeastern Washington,” U. S. Geological Survey Bulletin 1597 (1987): 1–25; Melanie B. DeVore and Kathleen B. Pigg, “Floristic Composition and Comparison of Middle Eocene to Late Eocene Late Oligocene Floras in North America,” Bulletin of Geosciences 85 (2010): 111–34; and Richard M. Dillhoff, Estella B. Leopold, and Steven R. Manchester, “The McAbee Flora of British Columbia and Its Relation to the Early-Middle Eocene Okanagan Highlands Flora of the Pacific Northwest,” Canadian Journal of Earth Sciences 42 (2005): 151–66. I examined certain plants in detail. For maples: David D. Ackerly and Michael

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J. Donoghue, “Leaf Size, Sapling Allometry, and Corner’s Rules: Phylogeny and Correlated Evolution in Maples (Acer),” AN 152 (1998): 767–91; M. C. Boulter, J. N. Benfield, H. C. Fisher, D. A. Gee, and M. Lhotak, “The Evolution and Global Migration of the Aceraceae,” PTRSB 351 (1996): 589–609; and G. W. Grimm, T. Denk, and V. Hemleben, “Evolutionary History and Systematics of Acer Section Acer— a Case Study of Low-Level Phylogenetics,” PSE 267 (2007): 215–53. For oaks: Paul S. Manos, Jeff J. Doyle and Kevin C. Nixon, “Phylogeny, Biogeography, and Processes of Molecular Differentiation in Quercus Subgenus Quercus (Fagaceae),” Molecular Phylogenetics and Evolution 12 (1999): 333–49; Paul S. Manos, ZheKun Zhou, and Charles H. Cannon, “Systematics of Fagaceae: Phylogenetic Tests of Reproductive Trait Evolution,” IJPS 162 (2001): 1361–379. For violets: Harvey Ballard Jr., Kenneth Sytsma, Robert R. Kowal, “Shrinking the Violets: Phylogenetic Relationships and Infrageneric Groups in Viola (Violaceae) Based on Internal Transcribed Spacer DNA Sequences,” SB 23 (1999): 439–58; G. A. Wahlert, T. Marcussen, J. de Paula-Souza, M. Feng, and H. E. Ballard Jr., “A Phylogeny of the Violaceae (Malpighiales) Inferred from Plastid DNA Sequences: Implications for Generic Diversity and Intrafamilial Taxonomy,” SB 39 (2014): 239–52; and Thomas J. Givnish, “Biomechanical Constraints on Crown Geometry in Forest Herbs,” in On the Economy of Plant Form and Function, ed. Thomas J. Givnish (Cambridge: Cambridge University Press, 1986), 525– 83. For geraniums: C. S. Jones, F. T. Bakker, C. D. Schlichting, and A. B. Nicotra, “Leaf Shape Evolution in the South African Genus Pelargonium L’Hér. (Geraniaceae),” Evolution 63 (2009): 479– 97; F. T. A. Bakker, P. Culham, T. Hettiarachi, T. Touloumenidou, and M. Gibby, “Phylogeny of Pelargonium (Geraniaceae) Based on DNA Sequences from Three Genomes,” Taxon 53 (2004): 17–28. For the interesting story of leaf margins and climate (and palaeoclimates), I consulted the following: I. W. Bailey and E. W. Sinnott, “A Botanical Index of Cretaceous and Tertiary Climates,” Science 46 (1915): 831–34; Irving W. Bailey and Edmund W. Sinnott, “The Climatic Distribution of Certain Types of Angiosperm Leaves,” AJB 3 (1916): 24–39; Robyn J. Burnham, Nigel C. A. Pitman, Kirk R. Johnson, and Peter Wilf, “Habitat-Related Error in Estimating Temperatures from Leaf Margins in a Humid Tropical Forest,” AJB 88 (2001): 1096–102; Robyn J. Burnham and Gayle S. Tonkovich, “Climate, Leaves, and the Legacy of Two Giants,” NP 190 (2011): 514–17; Dana L. Royer, Robert M. Kooyman, Stefan A. Little, and Peter Wilf, “Ecology of Leaf Teeth: A Multi-Site Analysis from an Australian Subtropical Rainforest,” AJB 96 (2009): 738–50; Dana L. Royer, P. Wilf, D. A. Janesko, E. A. Kowalski, and D. L. Dilcher, “Correlations of Climate and Plant Ecology to Leaf Size and Shape: Potential Proxies for the Fossil Record,” AJB 92 (2005): 1141–51; Dana L. Royer, D. J. Peppe, E. A. Wheeler, and Ü. Niinemets, “Roles of Climate and Functional Traits in Controlling Toothed vs. Untoothed Leaf Margins,” AJB 99 (2012): 915– 22; Peter Wilf, “When Are Leaves Good Thermometers? A New Case for Leaf Margin Analysis,” Paleobiology

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23 (1997): 373–90; J. A. Wolfe, “Paleoclimate Estimates from Tertiary Leaf Assemblages,” Annual Review of Earth and Planetary Sciences 23 (1995): 119–42; and Jian Yang et al., “Leaf Form–Climate Relationships on the Global Stage: An Ensemble of Characters,” GEB 10 (2015): 1113–25. For the role of fluid dynamics and boundary layers influencing leaf shape, see the books by Steven Vogel, The Life of a Leaf (Chicago: University of Chicago Press, 2012); and Karl Niklas and Hanns-Christof Spatz, Plant Physics (Chicago: University of Chicago Press, 2012). I used the following reviews on the subject of leaf shape and function: David Parkhurst and O. L. Loucks, “Optimal Leaf Size in Relation to Environment,” JE 60 (1972): 505–37; S. E. Taylor, “Optimal Leaf Form,” in Perspectives of Biophysical Ecology, David M. Gates and R. B. Schmere (New York: Springer-Verlag, 1975), 143–49; Thomas J. Givnish and Geerat J. Vermeij, “Sizes and Shapes of Liane Leaves,” AN 110 (1976): 743–78; Thomas J. Givnish, “On the Adaptive Significance of Leaf Form,” in Topics in Plant Population Biology, O. T. Solbrig, S. Jain, G. B. Johnson, and P. H. Raven (New York: Columbia University Press, 1979), 375–407; Thomas J. Givnish, “Comparative Studies of Leaf Form: Assessing the Relative Roles of Selective Pressures and Phylogenetic Constraints,” NP 106 (suppl., 1987): 1131–60; and V. K. Brown and J. H. Lawton, “Herbivory and the Evolution of Leaf Size and Shape,” PTRSB 333 (1991): 265–72. The following papers provide experimental support for different aspects of leaf function. Temperature: Douglas E. Gottschlich and Alan P. Smith, “Convective Heat Transfer Characteristics of Toothed Leaves,” Oecologia 53 (1982): 418–20; and Jessica Gurevitch and P. H. Schuepp, “Boundary Layer Properties of Highly Dissected Leaves: An Investigation Using an Electrochemical Fluid Tunnel,” PCE 13 (1990): 783–92. Photosynthesis: A. B. Nicotra, M. J. Cosgrove, A. Cowling, C. D. Schlichting, and C. S. Jones, “Leaf Shape Linked to Photosynthetic Rates and Temperature Optima in South African Pelargonium Species,” Oecologia 154 (2008): 625– 35; William F. Curtis, “Photosynthetic Potential of Sun and Shade Viola Species,” CJB 62 (1984): 1273–78; and Dana L. Royer and P. Wilf, “Why Do Toothed Leaves Correlate with Cold Climates? Gas Exchange at Leaf Margins Provides New Insights into a Classic Paleotemperature Proxy,” IJPS 167 (2006): 11–18. Guttation: Taylor S. Feild, T. L. Sage, C. Czerniak, and W. J. D. Iles, “Hydathodal Leaf Teeth of Chloranthus japonicus (Chloranthaceae) Prevent Guttation- Induced Flooding of the Mesophyll,” PCE 23 (2005): 1179–90. Drip tips: Christopher T. Ivey and N. DeSilva, “A Test of the Function of Drip Tips,” Biotropica 33 (2001): 188–91; R. Lucking and A. Bernecker-Lucking, “Drip-Tips Do Not Impair the Development of Epiphyllous Rain-Forest Lichen Communities,” JTE 21 (2005): 171–77; and Ana C. M. Malhado et al., “Drip-Tips Are Associated with Intensity of Precipitation in the Amazon Rain Forest,” Biotropica 44 (2012): 728–37. Aerodynamics: S. E. Taylor and O. J. Sexton, “Some Implications of Leaf Tearing in Musaceae,” Ecology 53: 143–49; Steven Vogel, “Drag and Reconfiguration of Broad Leaves in High Winds,” JEB 40 (1989): 941–48; Karl J. Niklas, “The Elastic Moduli and

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Mechanics of Populus tremuloides (Salicaceae) Petioles in Bending and Torsion,” AJB 78 (1991): 989–96; and Steven J. Vogel, “Convective Cooling at Low Airspeeds and the Shapes of Broad Leaves,” JEB 21 (1970): 91–101. There is quite a bit of information available about leaf sizes and shapes in different environments, especially for tropical rainforests. For recent studies: A. C. M. Malhado et al., “Spatial Trends in Leaf Size of Amazonian Rainforest Trees,” BG 6 (2009): 1563–76; A. C. M. Malhado et al., “Spatial Distribution and Functional Significance of Leaf Lamina Shape in Amazonian Forest Trees,” BG 6 (2009): 1577–90; A. N. Sringeswara, M. B. Shivanna, and Balakrishna Gowda, “Role of Ecological Factors on Leaf Size Spectra in an Evergreen Forest, Western Ghats, India— an Ecological Hotspot,” International Journal of Science and Nature 1 (2010): 61–66. I used recent studies of leaf function and evolution in Viburnum as an example: David W. Chatelet, Wendy L. Clemens, Lauren Sack, Michael J. Donoghue, and Erika J. Edwards, “The Evolution of Photosynthetic Anatomy in Viburnum (Adoxaceae),” IJPS 174 (2014): 1277–91; Michael J. Donoghue et al., “Evolution of Leaf Form Correlates with Tropical- Temperate Transitions in Viburnum (Adoxaceae),” PRSB 279 (2012), doi:10.1098/rspb.2012.1110; Wendy L. Clement, Monica Arakaki, P. W. Sweeney, Erika J. Edwards, and Michael J. Donoghue, “A Chloroplast Tree for Viburnum and Its Implications for Phylogenetic Classification and Character Evolution,” AJB 101 (2014): 1029–49; and Elizabeth L. Spriggs et al., “Temperate Radiations and Dying Embers of a Tropical Past: The Diversification of Viburnum,” NP 207 (2015): 340–54. For the odd leaves of Gunnera: D. Q. Fuller and L. J. Hickey, “Systematics and Leaf Architecture of the Gunneraceae,” BR 71 (2005): 295–353. For my discussion on the functions of compound leaves: Thomas J. Givnish, “On the Adaptive Significance of Compound Leaves, with Particular Reference to Tropical Trees,” in Tropical Trees as Living Systems, ed. P. Barry Tomlinson and Martin H. Zimmerman (New York: Cambridge University Press, 1978), 351–80; Lawrence G. Stowe and Jeffrey L. Brown, “A Geographic Perspective on the Ecology of Compound Leaves,” Evolution 35 (1981): 818–21; Ü. Niinemets, “Are Compound-Leaved Woody Species Inherently Shade-Intolerant? An Analysis of Species Ecological Requirements and Foliar Support Costs,” PE 134 (1998): 1–11; A. T. Moles and M. Westoby, “Do Small Leaves Expand Faster than Large Leaves, and Do Shorter Expansion Times Reduce Herbivore Damage?” Oikos 90 (2000): 517–24; A. C. M. Malhado et al., “Are Compound Leaves an Adaptation to Seasonal Drought or to Rapid Growth? Evidence from the Amazon Rain Forest,” Global Ecology and Biogeography 19 (2010): 852–62; Laura Warman, Angela T. Moles, and Will Edwards, “Not So Simple After All: Searching for Ecological Advantages of Compound Leaves,” Oikos 120 (2011): 813–21; Lonnie Aarson, “Reducing Size to Increase Number: A Hypothesis for Compound Leaves,” Ideas in Ecology and Evolution 5 (2012): 1–5. For descriptions of the geometry of leaves, I started with the writings of D’Arcy Wentworth Thompson and his early influences: D’Arcy Wentworth Thompson, On Growth and Form (Cambridge: Cambridge University Press, 1961); R. Melville,

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“The Accurate Definition of Leaf Shapes by Rectangular Coordinates,” AB 1 (1937): 673–79; and Denis Barabé, Stéphane Daigle, and Luc Brouillet, “On the Interpretation of the Asymmetrical Leaf of Begonia by D’Arcy Thompson,” Acta Biotheoretica 40 (1992): 329–32. I’ve added more recent work in chronological order: R. J. Jensen, “Detecting Shape Variation in Oak Leaf Morphology: A Comparison of Rotational-Fit Methods,” AJB 77 (1990): 1279–93; Przemysław Prusinkiewicz and Aristid Lindenmayer, The Algorithmic Beauty of Plants (New York: Springer Verlag, 1990); Tom W. Ray, “Landmark Eigenshape Analysis: Homologous Contours: Leaf Shape in Syngonium (Araceae),” AJB 70 (1992): 69–76; R. J. Bird and F. Hoyle, “On the Shapes of Leaves,” JM 219 (1994): 225–41; Karl J. Niklas, “Simulation of Organic Shape: The Roles of Phenomenology and Mechanism,” JM 219 (1994): 243– 46; Eran Sharon, Michael Marder, and Harry L. Swinney, “Leaves, Flowers and Garbage Bags: Making Waves,” American Scientist 92 (1994): 254–61; Tracy McLellan and John A. Endler, “The Relative Success of Some Methods for Measuring and Describing the Shape of Complex Objects,” Systematic Biology 47 (1998): 264–81; R. Moraczewski, “Analyzing Leaf Margins with the Use of a Shape Feature Description Language,” CJB 76 (1998): 552–60; Wojciech Borkowski, “Fractal Dimension Based Features Are Useful Descriptors of Leaf Complexity and Shape,” Canadian Journal of Forest Research 29 (1999): 1301–10; Yodthong Rodkaew et al., “Modeling Leaf Shapes Using L-systems and Genetic Algorithms” International conference NICOGRAPH (April 2002): 73–78; Johan Gielis, “A Generic Geometric Transformation That Unifies a Wide Range of Natural and Abstract Shapes,” AJB 90 (2003): 333–38; Qinglan Xia, “The Formation of a Tree Leaf,” ESAIM: Control, Optimisation and Calculus of Variations 13 (2007): 359–77; Haiyi Liang and L. Mahadevan, “The Shape of a Long Leaf,” PNAS 106 (2009): 22049–54; Przemysław Prusinkiewicz and Pierre Barbier de Reuille, “Constraints of Space in Plant Development,” JEB 61 (2010): 2117–29; David A. Young, “Growth Algorithm Model of Leaf Shape,” 2010, arXiv.org/abs/1004.4388; and Simcha Lev-Yadun, “Fern Leaves and Cauliflower Curds Are Not Fractals,” PSB 7 (2012): 533–34. For the controls of leaf asymmetry, including fluctuating asymmetry: Tracy McLellan, “Geographic Variation and Plasticity of Leaf Shape and Size in Begonia dregei and B. homonyma (Begoniaceae),” BotJLS 132 (2000): 79–95; and Vincenzo Viscosi et al., “Leaf Shape and Size Differentiation in White Oaks: Assessment of Allometric Relationships among Three Sympatric Species and Their Hybrids,” IJPS 173 (2012): 875–84. For fluctuating asymmetry in leaf shape: S. V. Dongen, “Fluctuating Asymmetry and Developmental Instability in Evolutionary Biology: Past, Present and Future,” JEVB 19 (2006): 1727–43; Sara M. Handy, Kim McBreen, and Mitchell B. Cruzan, “Patterns of Fitness and Fluctuating Asymmetry Across a Broad Hybrid Zone,” IJPS 165 (2004): 973–81; and Helen T. Murphy and Jon Lovett-Doust, “Landscape-Level Effects on Developmental Instability: Fluctuating Asymmetry Across the Range of Honey Locust, Gleditsia triacanthos (Fabaceae),” IJPS 165 (2004): 795–803. For leaf shape recognition and the development of software for more general

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use, see David P. A. Corney, H. Lilian Tang, Jonathan Y. Clark, Yin Hu, and Jing Jin, “Automating Digital Leaf Measurement: The Tooth, the Whole Tooth, and Nothing but the Tooth,” PLoS ONE 7 (2012): e42112, doi:10.1371/journal.pone.0042112; Kue-Bum Lee and Kwang-Seok Hong, “Advanced Leaf Recognition Based on Leaf Contour and Centroid for Plant Classification,” Lecture Notes in Electrical Engineering 214 (2013): 109–16; Jyotismita Chaki and Ranjan Parekh, “Plant Leaf Recognition Using Shape Based Features and Neural Network Classifiers,” International Journal of Advanced Computer Science and Applications 2 (2011): 41–47; and Max Bylesjö et al., “LAMINA: A Tool for Rapid Quantification of Leaf Size and Shape Parameters,” BMC Plant Biology 8 (2008), doi:10.1186/1471- 2229-8-82. See the following websites (although I expect this field will evolve quickly and some may not work): http://www.light-speed.de/ (Leaf Recognition v. 10, a neural network-based recognition system for leaf shapes); flavia.sourceforge.net (a leaf-recognition algorithm for plant classification using probabilistic neural networks); and leafsnap.com (an electronic field guide for tree and plant species). The scientific names of the plants mentioned in the chapter, in order: red oak = Quercus rubra L. (Fagaceae); red maple = Acer rubrum L. (Sapindaceae); papaya = Carica papaya L. (Caricaceae); Selaginella = Selaginella cf. willdenowii (Desv.) Bak. (Selaginellaceae); sassafras = Sassafras albidum (Nutt.) Nees (Lauraceae); ginkgo = Ginkgo biloba L. (Ginkgoaceae); plane tree = Platanus occidentalis L. (Platanaceae); black gum = Nyssa sylvatica Marsh. (Cornaceae); sabal palm = Sabal palmetto (Walter) Schultes & Schultes f. (Arecaceae); Matonia = Matonia pectinata R. Br. (Matoniaceae); English oak = Quercus robur L.; sugar maple = Acer saccharum L. (Sapindaceae); geranium = Geranium sp. (Geraniaceae); violet = Viola sp. (Violaceae); viburnum = Viburnum cf. dentatum L. (Adoxaceae); gunnera = Gunnera insignis (Oerst.) Oerst.

Chapter Nine: Surfaces For reference to poem by Shinsui, see Yoel Hoffmann, Japanese Death Poems: Written by Zen Monks and Haiku Poets on the Verge of Death (North Clarendon, VT: Tuttle Publishing, 1994). I was made aware of the lyrics to the song by Allan Sherman from a review by Beverly Glover: “Differentiation in Plant Epidermal Cells,” JEB 51 (2000): 497–505. For biographical information about George de Mestral, I used an article in Wikipedia, https://en.wikipedia.org/wiki/George_de_Mestral, and the Velcro Corporation website: www.velcro.com. For general descriptions of biomimicry and bioinspiration: Bharat Bhushan, “Biomimetics: Lessons from Nature— an Overview,” PTRSA 367 (2009): 1445–86; and Yoseph Bar-Cohen, ed., Biomimetics: Nature-Based Innovation (Boca Raton, FL: CRC Press, 2012).

For general descriptions of leaf epidermis, see Brian Gunning and M. W. Steer, Plant Cell Biology: Structure and Function of Plant Cells (Boston: Jones and Bartlett, 1996); Al¸ison M. Smith et al., Plant Biology (New York: Garland Science, 2010); Lincoln Taiz and Eduardo Zeiger, Plant Physiology, 4th ed. (Sunderland, MA: Sinauer Associates, 2006); and Sigal Savaldi-Goldstein, Charles Peto, and Joanne Chory, “The Epidermis Both Drives and Restricts Plant Shoot Growth,” Nature 446 (2007):

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199–202. For the thickening of cell walls and directions of cellulose microfibrils, see D. Cosgrove, “Growth of the Plant Cell Wall,” Nature Reviews Molecular Cell Biology 6 (2005): 850–61; U. Kutschera, “The Growing of the Outer Epidermal Wall: Design and Physiological Role of a Composite Structure,” AB 101 (2008): 615–21; Clive Lloyd and Jordi Chan, “The Parallel Lives of Microtubules and Cellulose Microfibrils,” COPB 11 (2008): 641–46; A. C. Neville and S. Levy, “The Helicoidal Concept in Plant Cell Ultrastructure and Morphogenesis,” in The Biochemistry of Plant Cell Walls, ed. C. T. Brett and J. R. Hillman (Cambridge: Cambridge University Press, 1985), 91–124; and Chris Somerville, “Cellulose Synthesis in Higher Plants,” Annual Review of Cell and Developmental Biology 22 (2006): 53–78. For the control of the epidermal outer cell wall shape, see J. L. Atwood and N. H. Williams, “Surface Features of the Adaxial Epidermis in the Conduplicate- Leaved Cypripedioideae (Orchidaceae),” BotJLS 78 (1979): 141–56; Beverley J. Glover, Maria Perez-Rodriguez, and Cathie Martin, “Development of Several Epidermal Cell Types Can Be Specified by the Same MYB- Related Plant Transcription Factor,” Development 125 (1998): 3497–508; C. Martin, K. Bhatt, and K. Baumann, “Shaping in Plant Cells,” COPB 4 (2001): 540–49; K. Noda, Beverly J. Glover, P. Linstead, and C. Martin, “Flower Color Intensity Depends on Specialized Cell Shape Controlled by a Myb-Related Transcription Factor,” Nature 369 (1994): 661–64; Heather M. Whitney, L. Chittka, T. J. A. Bruce, and B. J. Glover, “Conical Epidermal Cells Allow Bees to Grip Flowers and Increase Foraging Efficiency,” CB 19 (2009): 948–53; and Heather M. Whitney, Rosa Poetes, Ullrich Steiner, Lars Chittka, and Beverley J. Glover, “Determining the Contribution of Epidermal Cell Shape to Petal Wettability Using Isogenic Antirrhinum Lines,” PlosONE 6 (2011): e17576, doi:10.1371/journal.pone.0017576. For background on the cuticle, including the chemistry of cutin and epicuticular waxes, see Bob B. Buchanan, Wilhelm Gruissem, and Russell L. Jones, Biochemistry & Molecular Biology of Plants (Rockville, MD: American Society of Plant Physiologists, 2000); G. Kerstiens, ed., Plant Cuticles: An Integrated Functional Approach (Oxford: BIOS Scientific, 1996); Lacey Samuels, Ljerka Kunst, and Reinhard Jetter, “Sealing Plant Surfaces: Cuticular Wax Formation by Epidermal Cells,” ARPB 59 (2008): 683–707; G. Kerstiens, “Signaling Across the Divide: A Wider Perspective of Cuticular Structure-Function Relationships,” TPS 1 (1996): 125–29; J. T. Martin and Barry E. Juniper, The Cuticles of Plants (New York: St. Martin’s Press, 1970), old but good; Yusuke Onoda, Lora Richards, and Mark Westoby, “The Importance of Leaf Cuticle for Carbon Economy and Mechanical Strength,” NP 196 (2012): 441–47; P. J. Peeters, “Ecophysiology of Cuticular Transpiration: Comparative Investigation of Cuticular Water Permeability of Plant Species from Different Habitats,” BiolJLS 77 (2002): 43–65; and L. Schreiber and M. Riederer, “Ecophysiology of Cuticular Transpiration: Comparative Investigation of Cuticular Water Permeability of Plant Species from Different Habitats,” Oecologia 107 (1996): 426–32. For general descriptions of structures at the leaf surface, see Kevin J. Carpenter, “Specialized structures in the leaf epidermis of basal angiosperms: morphology, dis-

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tribution, and homology,” AJB 93 (2006): 665-681; H.J. Hewson, Plant Indumentum: A Handbook of Terminology (Canberra: Australian Government Publishing Service, 1988); H.P. Wilkinson, “The plant surface (mainly leaf ),” in C.R. Metcalfe and L. Chalk, eds., Anatomy of the Dicotyledons, vol. 1, 2nd ed. (Oxford: Clarendon Press, 1979), pp. 97-165. For fossil cuticles: Richard Barclay, Jennifer McElwain, David Dilcher, and Bradley Sageman, “The cuticle database: developing an interactive tool for taxonomic and palaeo-environmental study of the fossil cuticle record,” Courier Forschungsinstitut Senckenberg 258 (2007): 39-55. There is considerable interest in the formation of patterns of stomata at the leaf surface: Leila Kheibarshekan Asl et al., “Model-Based Analysis of Arabidopsis Leaf Epidermal Cells Reveals Distinct Division and Expansion Patterns for Pavement and Guard Cells,” PP 156 (2011): 2172–83; Lynn Jo Pillitteri and Keiko U. Torii, “Mechanisms of Stomatal Development,” ARPB 63 (2012): 591–614; Min Tang, Yu- Xi Hu, Jin Xing Lin, and Xiao- Bai Jin, “Developmental Mechanism and Distribution Pattern of Stomatal Clusters in Begonia peltata,” Acta Botanica Sinica 44 (2012): 384–90; Anne Vatén and Dominique C. Bergmann, “Mechanisms of Stomatal Development: An Evolutionary View,” EvoDevo 3 (2012): 11; Jie Le et al., “Auxin Transport and Activity Regulate Stomatal Patterning and Development,” Nature Communications 5 (2014), doi:10.1038/ncomms4090; Graham J. Dow, Joseph A. Berry, and Dominique C. Bergmann, “The Physiological Importance of Developmental Mechanisms That Enforce Proper Stomatal Spacing in Arabidopsis thaliana,” NP 201 (2014): 1205–17; Peter J. Franks and Stuart Casson, “Connecting Stomatal Development and Physiology,” NP 201 (2014): 1079– 82; Paula J. Rudall, Jason Hilton, and Richard M. Bateman, “Several Developmental and Morphogenetic Factors Govern the Evolution of Stomatal Patterning in Land Plants,” NP 200 (2013): 598–614; and Graham J. Dow, Dominique C. Bergmann, and Joseph A. Berry, “An Integrated Model of Stomatal Development and Leaf Physiology,” NP 201 (2014): 1218–26. For the relation of stomatal patterns to function: Peter J. Franks, Paul L. Drake, and David J. Beerling, “Plasticity in Maximum Stomatal Conductance Constrained by Negative Correlation between Stomatal Size and Density: An Analysis Using Eucalyptus globulus,” PCE 32 (2009): 1737– 48; Paul L. Drake, Ray H. Froend, and Peter J. Franks, “Smaller, Faster Stomata: Scaling of Stomatal Size, Rate of Response, and Stomatal Conductance,” JEB 64 (2013): 495–505; John A. Raven, “Speedy Small Stomata?” JEB 65 (2014): 1415–24; Jin Suk Lee et al., “Competitive Binding of Antagonistic Peptides Fine-Tunes Stomatal Patterning,” Nature 522 (2015): 439–43; Peter Lehmann and Dani Or, “Effects of Stomata Clustering on Leaf Gas Exchange,” NP 207 (2015): 1015–25; Peter J. Franks, Timothy W. Doheny-Adams, Zoe J. Britton-Harper, and Julie E. Gray, “Increasing Water-Use Efficiency Directly through Genetic Manipulation of Stomatal Density,” NP 207 (2015): 188–95; and Scott A. M. McAdam, Frances C. Sussmilch, and Timothy J. Brodribb, “Stomatal Responses to Vapour Pressure Deficit Are Regulated by High Speed Gene Expression in Angiosperms,” PCE 39 (2016): 485–91.

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There is a lot of information on trichomes from different perspectives. For general descriptions, see Daniel H. Benzing, Bromeliaceae: Profile of an Adaptive Radiation (New York: Cambridge University Press, 2000); Christopher P. Bickford, “Ecophysiology of Leaf Trichomes,” FE (2016): 807–14; Francoise Favi, Charles L. Cantrell, Tadesse Mebrahtu, and Mark E. Kraemer, “Leaf Peltate Glandular Trichomes of Vernonia galamensis ssp. galamensis var. ethiopica Gilbert: Development, Ultrastructure and Chemical Composition,” IJPS 169 (2008): 605–14; and W. L. Theobald, J. L. Krahulik, and R. C. Rollins, “Trichome Description and Classification,” in Anatomy of the Dicotyledons, vol. 1, 2nd ed., ed. C. R. Metcalfe and L. Chalk (Oxford: Clarendon Press, 1979), 40–53. For the development of trichomes and patterns, see Markus Grebe, “The Patterning of Epidermal Hairs in Arabidopsis— Updated,” COPB 15 (2012): 31– 37; and Thomas Payne, John Clement, David Arnold, and Alan Lloyd, “Heterologous MYB Genes Distinct from GL1 Enhance Trichome Production When Overexpressed in Nicotiana tabacum,” Development 126 (1999): 671–82. For the environmental effects of trichomes: Jim Ehleringer, O. Björkman, and H. A. Mooney, “Leaf Pubescence: Effects on Absorptance and Photosynthesis in a Desert Shrub,” Science 192 (1976): 376–77; Benno M. Eller, “Leaf Pubescence: The Significance of Lower Surface Hairs for the Spectral Properties of the Upper Surface,” JEB 28 (1977): 1054–59; David W. Lee and J. Brian. Lowry, “Plant Speciation on Tropical Mountains: Leptospermum (Myrtaceae) on Mount Kinabalu, Borneo,” BotJLS 80 (1980): 223–42; and Y. Manetas, “The Importance of Being Hairy: The Adverse Effects of Hair Removal on Stem Photosynthesis of Verbascum speciosum Are Due to Solar UV-B Radiation,” NP 158 (2003): 503–8. The defensive effects of trichomes are highlighted by these articles, which also survey the literature: Christer Björkman, Peter Dalin, and Karin Ahrné, “Leaf Trichome Responses to Herbivory in Willows: Induction, Relaxation and Costs,” NP 179 (2008): 176–84; Peter Dalin, Jon Ågren, Christer Björkman, Piritta Huttunen, and Katri Kärkkäinen, “Leaf Trichome Formation and Plant Resistance to Herbivory,” in Induced Plant Resistance to Herbivory, ed. A. Schaller (Berlin: Springer Science+Business Media B.V., 2008); L. Seelman, A. Auer, D. Hoffmann, and P. Schausberger, “Leaf Pubescence Mediates Intra- Guild Predation between Predatory Mites,” Oikos 116 (2007): 807–17; and P. L. Valverde, J. Fornoni, and J. Núnez-Farfán, “Defensive Role of Leaf Trichomes in Resistance to Herbivorous Insects in Datura stramonium,” JEVB 14 (2001): 424–32. For the use of trichomes in trapping bedbugs, see Michael F. Potter, “The History of Bedbug Management— with Lessons from the Past,” American Entomologist 57 (2011): 13–25; Megan W. Szyndler, Kenneth F. Haynes, Michael F. Potter, Robert M. Corn, and Catherine Loudon, “Entrapment of Bed Bugs by Leaf Trichomes Inspires Microfabrication of Biomimetic Surfaces,” JRSI 10 (2013), doi.org/10.1098/rsif.2013.0174; Eric W. Riddicka and Alvin M. Simmons, “Do Plant Trichomes Cause More Harm Than Good to Predatory Insects?” Pest Management Science 70 (2014), doi10.1002/ps3772/ pdf; Robert W. Sutherst, Raymond J. Jones, and Herbert J. Schnitzerling, “Tropical Legumes of the Genus Stylosanthes Immobilize and Kill Cattle Ticks,” Nature 295

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(1982): 320–21; Thomas Eisner, Maria Eisner, and E. Richard Hoebeke, “When Defense Backfires: Detrimental Effect of a Plant’s Protective Trichomes on an Insect Beneficial to the Plant,” PNAS 95 (1998): 4410– 14; and Geerat J. Vermeij, “Plants That Lead: Do Some Surface Features Direct Enemy Traffic on Leaves and Stems?” BiolJLS 116 (2015): 288–94. For leaf surfaces and biomimicry, we start with hooked hairs in bedstraw, G. Bauer, M.-C. Klein, S. N. Gorb. T. Speck, D. Voigt, and F. Gallenmüller, “Always on the Bright Side: The Climbing Mechanism of Galium aparine,” PRSB 278 (2011): 2233–39. Most work has been on water repellency, the “lotus effect”: W. Barthlott and C. Neinhuis, “Purity of the Sacred Lotus, or Escape from Contamination in Biological Surfaces,” Planta 202 (1997): 1–8; B. Bushan, ed., “Biomimetics I: Functional Biosurfaces,” PTRSA 367 (2009): 1631–813; Lin Feng et al., “Petal Effect: A Superhydrophobic State with High Adhesive Force,” Langmuir 24 (2008): 4114– 19; Kerstin Koch, Bharat Bhushan, and Wilhelm Barthlott, “Diversity of Structure, Morphology and Wetting of Plant Surfaces,” Soft Matter 4 (2008): 1943–63; K. Koch and W. Barthlott, “Superhydrophobic and Superhydrophilic Plant Surfaces: An Inspiration for Biomimetic Materials,” PTRSA 367 (2009): 1487–509; K. Koch, B. Bhushan, and W. Barthlott, “Multifunctional Surface Structures of Plants: An Inspiration for Biomimetics,” Progress in Materials Science 54 (2009): 137– 78; C. Neinhuis and W. Barthlott, “Characterization and Distribution of WaterRepellent, Self-Cleaning Plant Surfaces,” AB 79 (1997): 667–77; and W. E. Ward, “The Lotus Symbol: Its Meaning in Buddhist Art and Philosophy,” Journal of Aesthetics and Art Criticism 11 (1952): 135– 46. For the Salvinia effect: Wilhelm Barthlott et al., “The Salvinia Paradox: Superhydrophobic Surfaces with Hydrophilic Pins for Air-Retention under Water,” Advanced Materials 22 (2010): 2325–28; Pieter Verboven, Olle Pedersen, Quang Tri Ho, Bart M. Nicolai, and Timothy D. Colmer, “The Mechanism of Improved Aeration Due to Gas Films on Leaves of Submerged Rice,” PCE 37 (2014): 2433–52; and Anders Winkel et al., “Leaf Gas Films, Underwater Photosynthesis and Plant Species Distributions in a Flood Gradient,” PCE 39 (2016): 1537–48. For effects of leaf surface wetting on function, see M. Ishibashi and I. Terashima, “Effects of Continuous Leaf Wetness on Photosynthesis: Adverse Aspects of Rainfall,” PCE 18 (1995): 431–38; William K. Smith and T. M. McClean, “Adaptive Relationship between Leaf Water Repellency, Stomatal Distribution, and Gas Exchange,” AJB 76 (1989): 463– 69; A. Egri, A. Horváth, G. Kriska and G. Horváth, “Optics of Sunlit Water Drops on Leaves: Conditions under Which Sunburn Is Possible,” NP 185 (2010): 979–87; and C. A. Brewer, William K. Smith, and Thomas C. Vogelmann, “Functional Interaction between Leaf Trichomes, Leaf Wettability and the Optical Properties of Water Droplets,” PCE 14 (1991): 955–62. For the interesting research on pitcher plants and slippery surfaces, I consulted Tak-Sing Wong et al., “Bioinspired Self- Repairing Slippery Surfaces with PressureStable Omniphobicity,” Nature 477 (2011): 443– 47; Vincent Bonhomme et al., “Slippery or Sticky? Functional Diversity in the Trapping Strategy of Nepenthes Car-

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nivorous Plants,” NP 191 (2011): 545–54; Alexander K. Epstein, Tak-Sing Wong, Rebecca A. Belisle, Emily Marie Boggs, and Joanna Aizenberga, “Liquid-Infused Structured Surfaces with Exceptional Anti-Biofouling Performance,” PNAS 109 (2012): 13182– 87; Michael Nosonovsky, “Slippery When Wetted,” Nature 477 (2011): 412–13; Michael Riedel, Anna Eichner, Harald Meimberg, and Reinhard Jetter, “Chemical Composition of Epicuticular Wax Crystals on the Slippery Zone in Pitchers of Five Nepenthes Species and Hybrids,” Planta 225 (2007): 1517–34; and Holger F. Bohn and Walter Federle, “Insect Aquaplaning: Nepenthes Pitcher Plants Capture Prey with the Peristome, a Fully Wettable Water-Lubricated Anisotropic Surface,” PNAS 101 (2004): 14138–43. For recent developments on SLIPS: Elie Dolgin, “Fabrics of Life,” Nature 519 (215): S10–11; and Kenneth Chang, “Solving a Sticky Problem,” NYT, March 24, 2015, D4. For applications of leaf surfaces that attract water, see Stefan Vogel and Ute Müller-Dobliesb, “Desert Geophytes under Dew and Fog: The “Curly-Whirlies” of Namaqualand (South Africa),” Flora 206 (2011): 3–31; Thomas Norgaard, Martin Ebner, and Marie Dacke, “Animal or Plant: Which Is the Better Water Collector?” PLoS One 7 (2011), doi: e34603.10.1371/journal.pone.0034603; Philip W. Rundel et al., “Tillandsia landbeckii in the Coastal Atacama Desert of Northern Chile,” Revista Chilena de Historia Natural 70 (1997): 341–49; and Claudio Latorre et al., “Establishment and Formation of Fog-Dependent Tillandsia landbeckii Dunes in the Atacama Desert: Evidence from Radiocarbon and Stable Isotopes,” Journal of Geophysical Research: BG 116 (2011), doi: 10.1029/2010JG001521. For surface optical properties, see the example of edelweiss hairs: J. P. Vigneron et al., “Optical Structure and Function of the White Filamentary Hair Covering the Edelweiss Bracts,” PR E 71 (2005): 011906, 1–8. For the optical properties of leaf surfaces, see Richard E. Bone, David W. Lee, and John. N. Norman, “Epidermal Cells Functioning as Lenses in Leaves of Tropical Rainforest Shade Plants,” Applied Optics 24 (1985): 1408–12; Craig R. Broderson and Thomas C. Vogelmann, “Do Epidermal Lens Cells Facilitate the Absorptance of Diffuse Light?” AJB 94 (1997): 1061– 66; David W. Lee, Nature’s Palette: The Science of Plant Color (Chicago: University of Chicago Press, 2007); David W. Lee, “Biomimicry of the Ultimate Optical Device— the Plant,” in Biomimetics: Nature-Based Innovation, ed. Yoseph BarCohen (Boca Raton, FL: CRC Press, 2012), 307–30; John H. McClendon, “The Micro-Optics of Leaves: 1. Patterns of Reflection from the Epidermis,” AJB 71 (1984): 1391–97; E. E. Pfündel, G. Agati, and Z. G. Cerovic, “Optical Properties of Plant Surfaces,” in Biology of the Plant Cuticle, ed. M. Riederer and C. Müller (Oxford: Blackwell, 2006), 216–49; and Greg Strout et al., “Silica Nanoparticles Aid in Structural Leaf Colouration in the Malaysian Tropical Rainforest Understory Herb, Mapania caudata,” AB 112 (2013): 1141–48. For the biomimicry of such surfaces: J.-F. Revol, H. Bradford, J. Giasson, R. H. Marchessault, and D. G. Gray, “Helicoidal Self-Ordering of Cellulose Microfibrils in Aqueous Suspension,” International Journal of Biological Macromolecules 14 (1992): 170–72; E. D. Cranston and Derrick. G. Gray, “Morphological and Optical Characterization of Polyelectrolyte Multilay-

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ers Incorporating Nanocrystalline Cellulose,” Biomacromolecules 7 (2006): 2522– 30; Aditi Risbud, Akhlesh Lakhtakia, and Michael H. Bartl, “Toward Bioreplicated Texturing of Solar-Cell Surfaces,” in Encyclopedia of Nanotechnology, ed. Bharat Bhushan (Berlin: SpringerReference, 2012), 2755–62; and A. J. Schulte, “Biomimetic Replicas: Transfer of Complex Architectures with Different Optical Properties from Plant Surfaces onto Technical Materials,” Acta Biomaterialia 5 (2009): 1848–54. For examples of bicycle reflectors in leaves, see review by Lee, “Biomimicry of the Ultimate Optical Device— the Plant” above; Alan P. Smith, “Ecology of Leaf Color Polymorphism in a Tropical Forest Species: Habitat Segregation and Herbivory,” Oecologia 69 (1986): 283–87; and Y. Zhang, T. Hayashi, M. Hosokawa, S. Yazawa, and Y. Li, “Metallic Luster and the Optical Mechanism Generated from the Leaf Surface of Begonia rex Putz.,” Scientia Horticulturae 121 (2009): 213–17. Scientific names of plants mentioned in the text, in order: cocklebur = Xanthium strumarium L. (Asteraceae); carnauba palm = Copernica prunifera (Mill.) H. Moore (Arecaceae); stinging nettle = Urtica dioica L. (Urticaceae); sagebrush = Artemisia tridentata Nutt. (Asteraceae); Espeletia = Espeletia sp. (Asteraceae); dwarf Leptospermum = Leptospermum recurvum Hook. f. (Myrtaceae); snow lotus = Saussurea sp. (Asteraceae); mullein = Verbascum thapsus L. (Scrophulariaceae); edelweiss = Leontopodium nivale (Ten.) Hand-Mazz. susbsp. alpinum (Cass.) Greuter (Asteraceae); bedstraw = Galium aparine L. (Rubiaceae); common bean = Phaseolus vulgaris L. (Fabaceae); Stylosanthes = Stylosanthes humilis Kunth (Fabaceae); sacred lotus = Nelumbo nucifera Gaertn. (Nymphaeaceae); American pitcher plant = Sarracenia cf. purpurea L. (Sarraceniaceae); Asian pitcher plant = Nepenthes cf. rajah Hook. f. (Nepenthaceae); curlywhirly = Dipcadi panousei Saugave & Veilex (Asparagaceae); Chilean fog tillandsia = Tillandsia landbeckii Philippi (Bromeliaceae); understory sedge, Mapania = Mapania caudata Kük. (Cyperaceae); silver begonia = Begonia maculata Raddi (Begoniaceae).

Chapter Ten: Veins For the poetry quotes at the beginning of the chapter, see Rabindranath Tagore, “Stream of Life,” in Gitanjali (New York: Dover, 2011); and W. S. de Piero, “Only in Things,” in Nitro Nights (Port Townsend, WA: Copper Canyon Press, 2011).

For general articles on vein development, see H. Candela, A. MartinezLaborda, and J. L. Micol, “Venation Pattern Formation in Arabidopsis thaliana Leaves,” DB 205 (1999): 205–16; Julie Kang and Nancy Dengler, “Vein Pattern Development in Adult Leaves of Arabidopsis thaliana,” IJPS 165 (2004): 231–42; Anne-Gaëlle Rolland-Lagan, “Vein Patterning in Growing Leaves: Axes and Polarities,” Current Opinion in Genetics & Development 18 (2008): 348–53; Anne-Gaëlle Rolland-Lagan, Mira Amin, and Malgosia Pakulska, “Quantifying Leaf Venation Patterns: TwoDimensional Maps,” Plant Journal 57 (2009): 195–205; and Megan G. Sawchuk and Enrico Scarpella, “Control of Vein Patterning by Intracellular Auxin Transport,” PSB 8 (2013): e27205. For the early connections between plant and human anatomy, see biographical citations for Grew and Malpighi in chapter 6; and Marianna Karamanou and

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George Androutsos, “Completing the Puzzle of Blood Circulation: The Discovery of Capillaries,” Italian Journal of Anatomy and Embryology 115 (2010): 175–79. See the following for discussions of blood vessel development: Peter Carmeliet and Rakesh K. Jain, “Molecular Mechanisms and Clinical Applications of Angiogenesis,” Nature 473 (2011): 298–307; Mary J. C. Hendrix, Elisabeth A. Seftor, Angela R. Hess, and Richard E. B. Seftor, “Vasculogenic Mimicry and Tumour-Cell Plasticity: Lessons from Melanoma,” Nature Reviews 3 (2003): 411–21; Bin Li et al., “VEGF and PlGF Promote Adult Vasculogenesis by Enhancing EPC Recruitment and Vessel Formation at the Site of Tumor Neovascularization,” FASEB Journal 20 (2006): E664–776; and Rulong Shen et al., “Precancerous Stem Cells Can Serve as Tumor Vasculogenic Progenitors,” PLoS ONE 3 (2008), e1652.doi:10.1371/journal.pone.0001652. For general descriptions of the anatomy and function of leaf veins, see Peter H. Raven, Ray F. Evert, and Susan E. Eichhorn, Biology of Plants, 8th ed. (New York: W. H. Freeman, 2013); Alison M. Smith et al., Plant Biology (New York: Garland Science, 2010); Lincoln Taiz and Eduardo Zeiger, Plant Physiology, 4th ed. (Sunderland, MA: Sinauer Associates, 2006); and Lawren Sack and N. Michele Holbrook, “Leaf Hydraulics,” ARPB 57 (2006): 361–81. For the history of the understanding of transport and translocation: Harry F. Clements, “Translocation of Solutes in Plants,” Northwest Science 8, no. 4 (1934): 9– 21; Martin H. Zimmermann, “Long Distance Transport,” PP 54 (1974): 472–79; and Robert E. Hungate, “The Cohesion Theory of Transpiration,” PP 9 (1934): 783–94. For how veins can create compartments in leaves: Andrea Nardini, Emmanuelle Gortan, Matteo Ramani, and Sebastiano Salleo, “Heterogeneity of Gas Exchange Rates Over the Leaf Surface in Tobacco: An Effect of Hydraulic Architecture?” PCE 31 (2008): 804– 12. For the balance between veins and stomata: Madeline R. Carins Murphy, Gregory J. Jordan, and Timothy J. Brodribb, “Acclimation to Humidity Modifies the Link between Leaf Size and the Density of Veins and Stomata,” PCE 37 (2014): 124–31; Paul L. Drake, Charles A. Price, Pieter Poot, and Erik J. Veneklaas, “Isometric Partitioning of Hydraulic Conductance between Leaves and Stems: Balancing Safety and Efficiency in Different Growth Forms and Habitats,” PCE 38 (2015): 1628– 36; Markus Nolf, Danielle Creek, Remko Duursma, Joseph Holtum, Stefan Mayr, and Brendan Choat, “Stem and Leaf Hydraulic Properties Are Finely Coordinated in Three Tropical Rain Forest Tree Species,” PCE 38 (2015): 2652–61. About the importance of Martin Zimmerman, although I never met him, I have listened carefully to stories by Barry Tomlinson, Missy Holbrook, and Jennifer Richards, and also add some external biographical material here: John W. Einset, “Listening to Thirsty Plants,” Arnoldia 46 (1986): 42–45. For the discussion of veins and whole tree water transport, I used two trees as examples, the sugar maple and the Australian mountain ash, from the following articles: Andrew W. J. Burton, Kurt S. Pregitzer, and David D. Reed, “Leaf Area and Foliar Biomass Relationships in Northern Hardwood Forests Located on

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an 800 km Acid Deposition Gradient,” Forest Science 37 (1991): 1041–59; Todd E. Dawson, “Determining Water Use by Trees and Forests from Isotopic, Energy Balance and Transpiration Analyses: The Roles of Tree Size and Hydraulic Lift,” TP 16 (1996): 263–72; Jennifer M. Nagel et al., “Energy Investment in Leaves of Red Maple and Co-Occurring Oaks within a Forested Watershed,” TP 22 (2002): 859–67; Gabriel F. Tucker, James P. Lassoie, and Timothy J. Fahey, “Crown Architecture of Stand-Grown Sugar Maple (Acer saccharum Marsh.) in the Adirondack Mountains,” TP 13 (1993): 297–310; R. A. Vertessy, R. G. Benyon, S. K. O’Sullivan, and P. R. Gribben, “Relationships between Stem Diameter, Sapwood Area, Leaf Area and Transpiration in a Young Mountain Ash Forest,” TP 15 (1995): 559–67; R. A. Vertessy, T. J. Hatton, P. Reece, S. K. O’Sullivan, and R. G. Benyon, “Estimating Stand Water Use of Large Mountain Ash Trees and Validation of the Sap Flow Measurement Technique,” TP 17 (1997): 747–56; and Stan D. Wullschleger, F. C. Meinzer, and R. A. Vertessy, “A Review of Whole-Plant Water Use Studies in Trees,” TP 18 (1998): 499–512. For vein density, I consulted the supplementary data of Lawren Sack et al., “Developmentally Based Scaling of Leaf Venation Architecture Explains Global Ecological Patterns,” Nature Communications 3 (2012): 1–10. For the discussion of hydraulic lift: Martyn M. Caldwell, Todd E. Dawson, and James H. Richards, “Hydraulic Lift: Consequences of Water Efflux from the Roots of Plants,” Oecologia 113 (1998): 151– 61. The general discussion of pressure (water potential) and transport, see L. Taiz and E. Zeiger, Plant Physiology, 4th ed. (Sunderland, MA: Sinauer Associates, 2006). I’ve used the example of the world’s tallest tree for the most extreme negative pressure pulling water up the trunks and through leaf veins, for which there is some interesting recent research and speculation: P. Becker, F. C. Meinzer, and S. D. Wullschleger, “Hydraulic Limitation of Tree Height: A Critique,” FE 14 (2000): 4–11; Jean-Christophe Domec et al., “Maximum Height in a Conifer Is Associated with Conflicting Requirements for Xylem Design,” PNAS 105 (2008): 12069–74; George W. Koch, Stephen C. Sillett, Gregory M. Jennings, and Stephen D. Davis, “The Limits to Tree Height,” Nature 428 (2004): 851–54; George W. Koch and Stephen C. Sillett, “A Response to Limitations within ‘the Limits to Tree Height,’ ” AJB 96 (2009): 542– 44; Karl J. Niklas and Hanns- Christof Spatz, “Growth and Hydraulic (Not Mechanical) Constraints Govern the Scaling of Tree Height and Mass,” PNAS 101 (2004): 15661–63; Michael G. Ryan and Barbara J. Yoder, “Hydraulic Limits to Tree Height and Tree Growth,” BioScience 47 (1997): 235–42; Kaare H. Jensen and Maciej A. Zwieniecki. “Physical Limits to Leaf Size in Tall Trees,” PRL 110 (2013), doi:018104; and H. Roaki Ishii, Wakana Azuma, Keiko Kuroda, and Stephen C. Sillett, “Pushing the Limits to Tree Height: Could Foliar Water Storage Compensate for Hydraulic Constraints in Sequoia sempervirens?” FE 28 (2014): 1087–93; The authority for vein patterns in general is Beth Ellis et al., Manual of Leaf Architecture (Ithaca, NY: Cornell University Press, 2009). For the evolution of vein

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patterns: Athena D. McKown, Hervé Cochard, and Lawren Sack, “Decoding Leaf Hydraulics with a Spatially Explicit Model: Principles of Venation Architecture and Implications for Its Evolution,” AN 175 (2010): 447– 60; Ronald Melville, “Leaf Venation Patterns and the Origin of the Angiosperms,” Nature 224 (1969): 121–25; Anita Roth-Nebelsick, Dieter Uhl, Volker Mosbrugger, and Hans Kerp, “Evolution and Function of Leaf Venation Architecture: A Review,” AB 87 (2001): 553–66. The interesting evolution of net venation among monocots was studied by Thomas J. Givnish et al., “Repeated Evolution of Net Venation and Fleshy Fruits among Monocots in Shaded Habitats Confirms a priori Predictions: Evidence from an ndhF Phylogeny,” PRSB 272 (2005): 1481–90. Comparisons between streams, and then with leaves, sparked much quantitative research on vein patterns: Robert E. Horton, “Erosional Development of Streams and Their Drainage Basins: Hydro- Physical Approach to Quantitative Morphology,” Geological Society of America Bulletin 56 (1945): 275–370; Arthur N. Strahler, “Quantitative Analysis of Watershed Geomorphology,” Transactions of the American Geophysical Union 38 (1957): 913–20; Luna B. Leopold, “Trees and Streams: The Efficiency of Branching Patterns,” JTB 31 (1971): 339– 54; Jon D. Pelletier and Donald L. Turcotte, “Shapes of River Networks and Leaves: Are They Statistically Similar?” PTRSB 355 (2000): 307–11; Sean D. Willett, Scott W. McCoy, J. Taylor Perron, Liran Goren, and Chia-Yu Chen, “Dynamic Reorganization of River Basins,” Science 343 (2014), doi:1248765; Benjamin Blonder, Tina W. Wey, Anna Dornhaus, Richard James, and Andrew Sih, “Temporal Dynamics and Network Analysis,” Methods in Ecology and Evolution 3 (2012): 958–72; S. B. Bohn, S. Andreotti, J. Couady, J. Mantzinger, and Y. Couder, “Constitutive Property of the Local Organization of Leaf Venation Networks,” PR E 65 (2002): 1–12; Francis Corson. “Fluctuations and Redundancy in Optimal Transport Networks,” PRL 104 (2010): 048703; P. Dimitriov and S. W. Zucker, “A Constant Production Hypothesis Guides Leaf Venation Patterning,” PNAS 103 (2006): 9363–68; Peter Sheridan Dodds, “Optimal Form of Branching Supply and Collection Networks,” PRL 104 (2010): 048702; Maria F. Laguna, Steffen Bohn, and Eduardo A. Jagla, “The Role of Elastic Stresses on Leaf Venation Morphogenesis,” PLoS Computer Biology 4 (2008): e1000055, doi:10.1371/journal.pcbi.1000055; Benoit Mandelbrot, The Fractal Geometry of Nature (New York: W. H. Freeman, 1983); Adam Runions, Martin Fuhrer, Brendan Lane, Pavol Federl, Anne-Gaëlle Rolland-Lagan, and Przemysław Prusinkiewicz, “Modeling and Visualization of Leaf Venation Patterns,” ACM Transactions on Graphics 24 (2005): 702– 11; and D. L. Turcotte, J. D. Pelletier, and W. I. Newman, “Networks with Side Branching in Biology,” JTB 193 (1998): 466–81. For the constructal theory, see Adrian Bejan and J. Peder Zane, Design in Nature: How the Constructal Law Governs Evolution in Biology, Physics, Technology, and Social Organization (New York: Doubleday, 2012). For what may be exceptions to this theory: Eleni Katifori, J. Gergely, J. Szöllösi, and Marcelo O. Magnasco, “Damage and Fluctuations Induce Loops in Optimal Transport Networks,” PRL 104 (2010): 048704;

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Eleni Katifori and Marcelo O. Magnasco, “Quantifying Loopy Network Architectures,” PLoS ONE 7 (2012): e37994, doi:10.1371/journal.pone.0037994; and Lawren Sack, E. M. Dietrich, C. M. Streeter, D. Sánchez-Gómez, and N. Michele Holbrook, “Leaf Palmate Venation and Vascular Redundancy Confer Tolerance of Hydraulic Disruption,” PNAS 105 (2008): 1567–72. The abundance of recent excellent research on leaf veins has focused on several topics reviewed at the end of the chapter. For the importance of leaf vein density on angiosperm evolution and climate: C. Kevin Boyce, Tim J. Brodribb, Taylor S. Feild, and Maciej A. Zwieniecki, “Angiosperm Leaf Vein Evolution Was Physiologically and Environmentally Transformative,” PRSB 276 (2009): 1771–76; C. Kevin Boyce, Jung-Eun Lee, Taylor S. Feild, Tim J. Brodribb, and Maciej A. Zwieniecki, “Angiosperms Helped Put the Rain in the Rainforests: The Impact of Plant Physiological Evolution on Tropical Biodiversity,” Annals of the Missouri Botanical Garden 97 (2010): 527–40; C. Kevin Boyce and Maciej A. Zwieniecki, “Leaf Fossil Record Suggests Limited Influence of Atmospheric CO2 on Terrestrial Productivity Prior to Angiosperm Evolution,” PNAS 109 (2012): 10403– 8; Tim J. Brodribb, N. Michele Holbrook, Maciej A. Zwieniecki, and Beatriz Palma, “Leaf Hydraulic Capacity in Ferns, Conifers and Angiosperms: Impacts on Photosynthetic Maxima,” NP 165 (2005): 839–46; Tim J. Brodribb, Taylor S. Feild, and Lawren Sack, “Viewing Leaf Structure and Evolution from a Hydraulic Perspective,” FPB 37 (2010): 488–98; Taylor S. Feild et al., “Fossil Evidence for Cretaceous Escalation in Angiosperm Leaf Vein Evolution,” PNAS 108 (2011): 8363–66; Lawren Sack and Christine Scoffoni, “Leaf Venation: Structure, Function, Development, Evolution, Ecology and Applications in the Past, Present and Future,” NP 198 (2013): 983–1000; Charles A. Price, Scott Wing, and Joshua S. Weitz, “Scaling and Structure of Dicotyledonous Leaf Venation Networks,” EL 15 (2012): 87–95; Lauren E. Sack and K. Frole, “Leaf Structural Diversity Is Related to Hydraulic Capacity in Tropical Rainforest Trees,” Ecology 87 (2006): 483–91; Ramona L. Walls, “Angiosperm Leaf Vein Patterns Are Linked to Leaf Functions in a Global-Scale Data Set,” AJB 98 (2011): 244–53; Ian J. Wright, Daniel S. Falster, Melinda Pickup, and Mark Westoby, “Cross-Species Patterns in the Coordination between Leaf and Stem Traits, and Their Implications for Plant Hydraulics,” PPl 127 (2006): 445– 56; Lawren Sack, Melvin T. Tyree, and N. Michele Holbrook, “Leaf Hydraulic Architecture Correlates with Regeneration Irradiance in Tropical Rainforest Trees,” NP 167 (2005): 403–13; and Benjamin Blonder, Dana L. Royer, Kirk R. Johnson, Ian Miller, and Brian J. Enquist, “Plant Ecological Boundaries Extend Beyond the Cretaceous-Paleogene Boundary,” PloS Biology 12 (2014): e1001949, doi:10.1371/ Journal.Pbio1001949. For leaf venation’s relationship to the leaf economic spectrum (as in chapter 5): Benjamin Blonder, Cyrille Violle, Lisa Patrick Bentley, and Brian J. Enquist, “Venation Networks and the Origin of the Leaf Economics Spectrum,” EL 14 (2011): 91–100.

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Plants mentioned in this chapter by common name, in order: ground pine = Lycopodium sp. (Lycopodiaceae); Arabidopsis = Arabidopsis thaliana (L.) Heynh. (Brassicaceae); carrot, Queen Anne’s lace = Daucus carota L. (Apiaceae); sugar maple = Acer saccharum L. (Sapindaceae); coastal redwood = Sequoia sempervirens (D. Don) Endl. (Cupressaceae); mountain ash (Australia); Eucalyptus regnans F. Muell. (Myrtaceae); spike moss = Selaginella sp. (Selaginellaceae); high bush blueberry = Vaccinium corymbosum L. (Ericaceae); red maple = Acer rubrum L. (Sapindaceae); ti plant = Cordyline fruticosa (L.) Goeppert (Asparagaceae); peepul, bodhi = Ficus religiosa L. (Moraceae); velvet leaved clerodendron = Clerodendron quadrilocare (Blanco) Merr. (Verbenaceae); Swiss chard = Beta vulgaris L. (Chenopodiaceae).

Chapter Eleven: Color The poetry quotes at the beginning of the chapter are from D. H. Lawrence, Amores: Poems (1916) (New York: Bartleby.com, 1999); and Siegfried Sassoon, Collected Poems, 1908– 1956 (London: Faber & Faber, 1986). I wrote a book about plant color, extensively referenced, that covers the literature on leaf color up through 2006: David Lee, Nature’s Palette: The Science of Plant Color (Chicago: University of Chicago Press, 2007). I have added references that are extremely important, or that have appeared after the publication of that book. Particularly useful for the present discussion are chapters 3, 4, 6, and 11.

For additional information on leaf optical properties, particularly how chloroplast movement can affect leaf color, see Thomas Vogelmann, “Plant Tissue Optics,” ARPPPMB 44 (1993): 231–51; and Martina Königer and Nicole Bollinger, “Chloroplast Movement Behavior Varies Widely among Species and Does Not Correlate with High Light Stress Tolerance,” Planta 236 (2012): 411–26. For a recent article on betalain pigments, Samuel F. Brockington, Rachel H. Walker, Beverley J. Glover, Pamela S. Soltis, and Douglas E. Soltis, “Complex Pigment Evolution in the Caryophyllales,” NP 190 (2011): 854– 64. The coevolutionary significance of leaf color was discussed extensively in Nature’s Palette; for additional articles, mostly since that publication, see Delbert Wiens, “Mimicry in Plants,” Evolutionary Biology 11 (1978): 365–78; Ulf Soltau, Stefan Dötterl, and Sigrid Liede-Schumann, “Leaf Variegation in Caladium steudneriifolium (Araceae): a Case of Mimicry?” Evolutionary Ecology 23 (2009): 503– 12; Simcha Lev-Yadun and Gidi Ne’eman, “When May Green Plants Be Aposematic?” BiolJLS 81 (2004): 413–16; Simcha Lev-Yadun, “Defensive Coloration in Plants: A Review of Current Ideas about Anti-Herbivore Coloration Strategies,” Floriculture, Ornamental and Plant Biotechnology 4 (2006): 292–99; Simcha Lev-Yadun and Kevin S. Gould, “Role of Anthocyanins in Plant Defence,” in Life’s Color Solutions: The Biosynthesis, Function and Applications of Anthocyanins, ed. Kevin S. Gould, K. M. Davies, and Chris Winefield (Berlin: Springer-Verlag, 2008), 21–48; Tamar Keasar, Adi Sadeh, Yoram Gerchman, and Avi Shmida, “The Signaling Function of an Extra-Floral Display: What Selects for Signal Development?” Oikos 118 (2009): 1752–59; Nik Fadzly, J. Cameron, H. M. Schaefer, and Kevin C. Burns, “Ontogenetic Colour Changes in an Insular Tree

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Species: Signalling to Extinct Browsing Birds?” NP 184 (2009): 495–501; and Nik Fadzly and Kevin C. Burns, “Hiding from the Ghost of Herbivory Past: Evidence for Crypsis in an Insular Tree Species,” IJPS 171 (2010): 828–33. For recent articles on color and leaf function: J.-H. B. Hatier, Michael J. Clearwater, and Kevin S, Gould, “The Functional Significance of Black- Pigmented Leaves: Photosynthesis, Photoprotection and Productivity in Ophiopogon planiscapus ‘Nigrescens,’ ” PLoS ONE 8 (2013): e67850, doi:10.1371/journal.pone.0067850; and Nancy Y. Kiang, “The Color of Plants on Other Worlds,” Scientific American 298 (2008): 48–55. For foliage in the spring: Simcha Lev-Yadun, Kazuo Yamazaki, Jarmo K. Holopainen, and Aki Sinkkonen, “Spring versus Autumn Leaf Colours: Evidence for Different Selective Agents and Evolution in Various Species and Floras,” Flora 207 (2012): 80– 85; and Nicole M. Hughes, “Winter Leaf Reddening in ‘Evergreen’ Species,” NP 190 (2011): 573–81. The following articles appeared previous to 2009, were cited in Nature’s Palette, and were particularly important in this chapter: Taylor S. Feild, Noel Michele Holbrook, and David W. Lee, “Why Leaves Turn Red in Autumn: The Role of Anthocyanins in Senescing Leaves of Red-Osier Dogwood,” PP 127 (2001): 566– 74; Kevin. S. Gould, J. McKelvie, and Kenneth R. Markham, “Do Anthocyanins Function as Antioxidants in Leaves? Imaging of H2O2 in Red and Green Leaves after Mechanical Injury,” PCE 24 (2002): 1261–69; David. W. Lee, John O’Keefe, N. Michele Holbrook, and Taylor S. Feild, “Pigment Dynamics and Autumn Leaf Senescence in a New England Deciduous Forest, Eastern USA,” ER 18 (2003): 677–94; and William A. Hoch, Eric L. Singsaas, and Brent H. McCown, “Resorption Protection: Anthocyanins Facilitate Nutrient Recovery in Autumn by Shielding Leaves from Potentially Damaging Light Levels,” PP 133 (2003): 1296–305. The following articles were published since 2009 and have informed the discussion on the function of autumn leaf color: Marco Archetti et al., “Unraveling the Evolution of Autumn Colours: An Interdisciplinary Approach,” TREE 24 (2009): 166–72— the review from the Oxford workshop; Marco Archetti, “Loss of Autumn Colors under Domestication: A Byproduct of Selection for Fruit Flavor?” PSB 4 (2009): 856–58; Marco Archetti, “Evidence from the Domestication of Apple for the Maintenance of Autumn Colours by Co-evolution,” PRSB 276 (2009): 2575– 80; Luke J. Cooney et al., “ Red Leaf Margins Indicate Increased Polygodial Content and Function as Visual Signals to Reduce Herbivory in Pseudowintera colorata,” NP 194 (2012): 488–97; Thomas F. Döring, Marco Archetti, and Jim Hardie, “Autumn Leaves Seen through Herbivore Eyes,” PRSB 276 (2009): 121–27; Johanna Keskitalo, Gustaf Bergquist, Per Gardeström, and Stefan Jansson, “A Cellular Timetable of Autumn Senescence,” PP 139 (2005): 1635–48; Simcha Lev-Yadun and Jarmo K. Holopainen, “Why Red-Dominated Autumn Leaves in America and Yellow-Dominated Autumn Leaves in Northern Europe?” NP 183 (2009): 506– 12; Simcha Lev-Yadun and Jarmo K. Holopainen, “How Red Is the Red Autumn Leaf Herring and Did It Lose Its Red Color?” PSB 6 (2011): 1879–80; Aki Sinkkonen et al., “Genotypic Variation in Yellow Autumn Leaf Colours Explains Aphid

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Load in Silver Birch,” NP 195 (2012): 461– 69; Simcha Lev- Yadun and Tamar Keasar, “Prerequisites for Evolution: Variation and Selection in Yellow Autumn Birch Leaves,” NP 195 (2012): 282–84; C. C. Ramirez, B. Lavandero, and Marco Archetti, “Coevolution and the Adaptive Value of Autumn Tree Colours: Colour Preference and Growth Rates of a Southern Beech Aphid,” JEVB 21 (2008): 49– 56; M. J. Tallis et al., “The Transcriptome of Populus in Elevated CO2 Reveals Increased Anthocyanin Biosynthesis during Delayed Autumnal Senescence,” NP 186 (2010): 415–28; T. C. R. White, “Catching a Red Herring: Autumn Colours and Aphids,” Oikos 118 (2009): 1610–12; Kazuo Yamazaki, “Autumn Leaf Colouration: A New Hypothesis Involving Plant-Ant Mutualism via Aphids,” Naturwissenschaften 95 (2008): 671–76; Yong-Jiang Zhang, Qiu-Yun Yang, David W. Lee, Guillermo Goldstein, and Kun-Fang Cao, “Extended Leaf Senescence Promotes Carbon Gain and Nutrient Resorption: Importance of Maintaining Winter Photosynthesis in Subtropical Forests,” Oecologia 173 (2013): 721–30; and Andy Moy, Sherry Le, and Amy Verhoeven, “Different Strategies for Photoprotection during Autumn Senescence in Maple and Oak,” PPl 155 (2015): 205–16. These articles concern the significance of leaf color and physiology affecting the timing of leaf fall, and the length of the leaf life-span, including the effects of global climate change: Jason D. Fridley, “Extended Leaf Phenology and the Autumn Niche in Deciduous Forest Invasions,” Nature 485 (2012 ): 359–64; Paul G. Schaberg, P. F. Murakami, M. Heitz, and G. J. Hawley, “Association of Red Coloration with Senescence of Sugar Maple Leaves in Autumn,” Trees 22 (2008): 573– 78; Irene Garenne et al., “Strong Contribution of Autumn Phenology to Changes in Satellite- Derived Growing Season Length Estimates across Europe (1982– 2011),” GCB 20 (2014): 3457–70; Su-Jong Jeong and David Medvigy, “Macroscale Prediction of Autumn Leaf Coloration throughout the Continental United State,” GEB 23 (2014): 1245–54; Marco Archetti, Andrew D. Richardson, John O’Keefe, and Nicolas Delpierre, “Predicting Climate Change Impacts on the Amount and Duration of Autumn Colors in a New England Forest,” PLoS One 8 (2013): e57373, doi:10.1371/journalpone.0057373; and Amanda S. Gallinat, Richard B. Primack, and David L. Wagner, “Autumn, the Neglected Season in Climate Change Research,” TREE 30 (2015): 169–176. Common names listed in order of appearance, with scientific equivalents: juneberry = Amelanchier arborea (Michaux f.) Fern. (Rosaceae); red maple = Acer rubrum L. (Sapindaceae); black cherry = Prunus serotina Ehrh. (Rosaceae); sumac = Rhus coppalina L. (Anacardiaceae); beech = Fagus grandifolia Ehrh. (Fagaceae); ash = Fraxinus americana L. (Oleaceae); trout lily = Erythronium americanum Ker-Gawler (Liliaceae); white-streaked clover = Trifolium pratense L. (Fabaceae); Japanese maple = Acer palmatum Thunb. (Sapindaceae); European ash = Fraxinus excelsior L. (Oleaceae); scarlet oak = Quercus coccinea Muenchh. (Fagaceae); white oak = Quercus alba L. (Fagaceae); red oak = Quercus rubra L. (Fagaceae); spruce = Picea mariana (Mill.) Britton, Sterns & Pogg. (Pinaceae); hemlock = Tsuga canadensis (L.) Carr. (Pinaceae); croton, Codaieum = Codaieum variegatum (L.) Blume (Euphorbiaceae); black false eranthemum

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= Pseuderanthemum carruthersii (Seem.) Guillaumin (Acanthaceae); wild caladium = Caladium steudneriifolium Engl. (Araceae); silver birch = Betula pendula Roth (Betulaceae); horopito = Pseudowintera colorata (Raoul) Dandy (Winteraceae); sugar maple = Acer saccharum L. (Sapindaceae); sassafras = Sassafras albidum (Nutt.) Nees (Lauraceae); sourwood = Oxydendron arboretum (L.) DC (Ericaceae); American chestnut = Castanea dentata (Marshall) Borkh. (Fagaceae); American elm = Ulmus americana L. (Ulmaceae).

Chapter Twelve: Food At the beginning of the chapter, for the spinach poem by Kenn Nesbitt, see his book Aliens Have Landed at Our School (Minnetonka, MN: Meadowbrook Press, 2006); and for the quote by Michael Pollan, In Defense of Food: An Eater’s Manifesto (New York: Penguin, 2009).

The nutritional information on leaves is provided by the USDA National Nutrient Database for Standard Reference, http://ndb.nal.usda.gov/. I also used the Wikipedia article on spinach, https://en.wikipedia.org/wiki/Spinach. For the historical role of leaves in human diet: Thure E. Cerling et al., “Stable Isotope-Based Diet Reconstructions of Turkana Basin Hominins,” PNAS 110 (2013): 10501–6; Cathie Martin, Yang Zhang, Chiara Tonelli, and Katia Petroni, “Plants, Diet, and Health,” ARPB 64 (2013): 19– 46; Matt Sponheimer et al., “Isotopic Evidence of Early Hominin Diets,” PNAS 110 (2013): 10513–18; and Ainara Sistiaga, Carolina Mallol, Bertila Galvan, and Roger Everett Summons, “The Neanderthal Meal: A New Perspective Using Faecal Biomarkers,” PLoS One 9 (2014): e101045, doi:10.1371/ journal.pone.0101045. For general reviews on the physiology of leaves and their high nutrient value: Lincoln Taiz and Eduardo Zeiger, Plant Physiology, 4th ed. (Sunderland, MA: Sinauer Associates, 2006); Bob Buchanan, Wilhelm Gruissem, and Russell Jones, eds., The Biochemistry and Molecular Biology of Plants (New York: John Wiley, 2002). For the nutritional value of pigments: Norman I. Krinsky, John T. Landrum, and Richard A. Bone, “Biologic Mechanisms of the Protective Role of Lutein and Zeaxanthin in the Eye,” Annual Review of Nutrition 23 (2003): 171–201; Johannes von Lintig, “Colors with Functions: Elucidating the Biochemical and Molecular Basis of Carotenoid Metabolism,” Annual Review of Nutrition 30 (2010): 35– 56; and Mario G. Ferruzzia and Joshua Blakeslee, “Digestion, Absorption, and Cancer Preventative Activity of Dietary Chlorophyll Derivatives,” Nutrition Research 27 (2007): 1–12. For general reviews on herbivory, including some historically important studies: M. R. Berenbaum, “The Chemistry of Defense: Theory and Practice,” PNAS 92 (1995): 2–8; Phylis D. Coley, John P. Bryant, and F. Stuart Chapin III, “Resource Availability and Plant Antiherbivore Defense,” Science 230 (1985): 895–99; Paul R. Ehrlich and Peter H. Raven, “Butterflies and Plants: A Study in Coevolution,” Evolution 18 (1964): 586– 608; G. S. Fraenkel, “The Raison d’être of Secondary Plant Substances,” Science 129 (1959): 1466–70; Daniel H. Janzen, “Coevolution of Mutualisms between Ants and Acacias in Central America,” Evolution 20 (1966):

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249–75; Marc T. J. Johnson, “Evolutionary Ecology of Plant Defenses against Herbivores,” FE 25 (2011): 305–11; H. A. Mooney and S. L. Gulmon, “Constraints on Leaf Structure and Function in Reference to Herbivory,” BioScience 32 (1982): 198– 206; Tobias Lortzing et al., “Extrafloral Nectar Secretion from Wounds of Solanum dulcamara,” Nature Plants 2 (2016), http://dx.doi.org/10.1038/nplants.2016.56; and Glen R. Iason, Marcel Dicke, and Susan E. Hartley, eds., The Ecology of Plant Secondary Metabolites (Cambridge: Cambridge University Press, 2012). For the evolutionary history of herbivory on leaves: Thomas N. Taylor, Edith L. Taylor, and Michael Krings, Paleobotany: The Biology and Evolution of Fossil Plants, 2nd ed. (Amsterdam: Academic Press, 2009); and Sandra R. Schachat et al., “Plant-Insect Interactions from Early Permian (Kungurian) Colwell Creek Pond, North-Central Texas: The Early Spread of Herbivory in Riparian Environments,” IJPS 175 (2014): 855–90. For camouflage and leaf defenses against herbivory: David W. Lee, Nature’s Palette: The Science of Plant Color (Chicago: University of Chicago Press, 2007)— chapter 6, on leaf color in particular. For the remarkable recent research on changing leaf shape: Ernesto Gianoll and Fernando Carrasco-Urra, “Leaf Mimicry in a Climbing Plant Protects against Herbivory,” CB 24 (2014): 984–87. For articles on types of chemical defenses and theories of strategy: Anurag A. Agrawal, “Macroevolution of Plant Defense Strategies,” TREE 22 (2006): 103–9; Anurag A. Agrawal, “Current Trends in the Evolutionary Ecology of Plant Defence,” FE 25 (2011): 420–32; Arjen Biere, Hamida B. Marak, and Jos M. M. van Damme, “Plant Chemical Defense against Herbivores and Pathogens: Generalized Defense or Trade-offs?” Oecologia 140 (2004): 430–41; Daneel Ferreira, Georg G. Gross, Herbert Kolodziej, and Takashi Yoshida, “Tannins and Related Polyphenols: Fascinating Natural Products with Diverse Implications for Biological Systems, Ecology, Industrial Applications and Health Protection,” Phytochemistry 66 (2005): 2124–26; Paul V. A. Fine et al., “The Growth-Defense Trade-off and Habitat Specialization by Plants in Amazonian Forests,” Ecology 87 (2006): S150– 62; Douglas J. Futuymaa and Anurag A. Agrawal, “Macroevolution and the Biological Diversity of Plants and Herbivores,” PNAS 106 (2009): 18054–61; Maria Heinrich, Ian T. Baldwin, and Jianqiang Wu, “Protein Kinases in Plant Growth and Defense,” Journal of Endocytobiosis and Cell Research 22 (2012): 48–51; Richard A. Lankau, “Specialist and Generalist Herbivores Exert Opposing Selection on a Chemical Defense,” NP 175 (2007): 176–84; and Juha-Pekka Salminen and Maarit Karonen, “Chemical Ecology of Tannins and Other Phenolics: We Need a Change in Approach,” FE 25 (2011): 325–38. For the distribution of defenses and their influence by the physical environment: Titta Kotilainena et al., “Seasonal Fluctuations in Leaf Phenolic Composition under UV Manipulations Reflect Contrasting Strategies of Alder and Birch Trees,” PPl 140 (2010): 297–309; Angela T. Moles, Stephen P. Bonser, Alistair G. B. Poore, Ian R. Wallis, and William J. Foley, “Assessing the Evidence for Latitudinal Gradients in Plant Defense and Herbivory,” FE 25 (2011): 380–88; Angela T. Moles et al., “Putting Plant Resistance Traits on the Map: A

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Test of the Idea That Plants Are Better Defended at Lower Latitudes,” NP 191 (2011): 777–88; and Angela T. Moles et al., “Correlations between Physical and Chemical Defences in Plants: Tradeoffs, Syndromes, or Just Many Different Ways to Skin a Herbivorous Cat?” NP 198 (2013): 252– 63. For canopy raft research: Kelsey R. Downum, David W. Lee, Francis Hallé, Martin Quirke, and Gary N. Towers, “Plant Secondary Compounds in the Canopy and Understorey of a Tropical Rainforest in Gabon,” JTE 17 (2001): 477–81. For shade effects on defense allocation: Carlos Ballaré, “Light Regulation of Plant Defense,” ARPB 65 (2914): 335–63. For articles on latexes and resins: Judith X. Becerra, “Squirt-Gun Defense in Bursera and the Chrysomelid Counterploy,” Ecology 75 (1994): 1991– 96; David E. Dussourd, “Do Canal- Cutting Behaviours Facilitate Host- Range Expansion by Insect Herbivores?” BiolJLS 96 (2009): 715–31; and William F. Pickard, “Laticifers and Secretory Ducts: Two Other Tube Systems in Plants,” NP 177 (2007): 877–88. For insecticidal chemicals in tomato trichomes: W. G. Williams, George G. Kennedy, Robert T. Yamamoto, J. D. Thacker, and Jon Bordner, “2-Tridecanone: A Naturally Occurring Insecticide from the Wild Tomato Lycopersicon hirsutum f. glabratum,” Science 207 (1980): 888–89; and G. F. Antonius, D. L. Dahlmen, and L. M. Hawkins, “Insecticidal and Acaricidal Performance of Methyl Ketones in Wild Tomato Leaves,” Bulletin of Environmental Contamination and Toxicology 71 (2003): 400–407. For inducible defenses in general, I consulted Gen-Ichiro Arimura, Rika Ozawa, and Massimo E. Maffei, “Recent Advances in Plant Early Signaling in Response to Herbivory,” International Journal of Molecular Sciences 12 (2011): 3723– 39; Christopher J. Frost et al., “Within- Plant Signaling via Volatiles Overcomes Vascular Constraints on Systemic Signaling and Primes Response against Herbivores,” EL 10 (2007): 490– 98; Richard Karban, “The Ecology and Evolution of Induced Resistance against Herbivores,” FE 25 (2011): 339–47; Stefan Meldau, Matthias Erb, and Ian T. Baldwin, “Defence on Demand: Mechanisms Behind Optimal Defence Patterns,” AB 110 (2012): 1503–14; Nawaporn Onkokesung et al., “Jasmonic Acid and Ethylene Modulate Local Responses to Wounding and Simulated Herbivory in Nicotiana attenuata Leaves,” PP 153 (2010): 785–98; Meredith C. Schuman, Kathleen Barthel, and Ian T. Baldwin, “Herbivory- Induced Volatiles Function as Defenses Increasing Fitness of the Native Plant Nicotiana attenuata in Nature,” eLife 1 (2012): e00007, doi:10.7554/eLife.00007; J. Q. Wu and I. T. Baldwin, “Herbivory-Induced Signaling in Plants: Perception and Action,” PCE 32 (2009): 1161– 74; Pavan Kumar, Sagar S. Pandit, Anke Steppuhn, and Ian T. Baldwin, “Natural History- Driven, Plant-Mediated RNAi- Based Study Reveals CYP6B46’s Role in a Nicotine-Mediated Antipredator Herbivore Defense,” PNAS 111 (2014): 1245–52; C. Wasternack and B. Hause, “Jasmonates: Biosynthesis, Perception, Signal Transduction and Action in Plant Stress Response, Growth and Development: An Update to the 2007 Review in Annals of Botany,” AB 111 (2013): 1021–58; and Elizabeth Rowen and Ian Kaplan, “Eco-Evolutionary Factors Drive Induced Plant Volatiles: A Meta-Analysis,” NP 210 (2016): 284–94.

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For signaling between individuals, species, and generations: Sergio Rasmann et al., “Herbivory in the Previous Generation Primes Plants for Enhanced Insect Resistance,” PP 158 (2012): 854–63; Liza M. Holeski, Georg Jander, and Anurag A. Agrawal, “Transgenerational Defense Induction and Epigenetic Inheritance in Plants,” TREE 27 (2012): 618–26; Richard Karban, Plant Sensing and Communication (Chicago: University of Chicago Press, 2015); and Richard Karban, Louie H. Yang, and Kyle F. Edwards, “Volatile Communication between Plants That Affects Herbivory: A Meta-Analysis,” EL 17 (2014): 44–52. The following articles describe responses to the hornworms, including tomatoes and tobacco, although this interaction is covered in some of the previous articles: Taiz and Zeiger, cited above; and Rayko Halitschke, Ursula Schittko, Georg Pohnert, Wilhelm Boland, and Ian T. Baldwin, “Molecular Interactions between the Specialist Herbivore Manduca sexta (Lepidoptera, Sphingidae) and Its Natural Host Nicotiana attenuata. III. Fatty Acid-Amino Acid Conjugates in Herbivore Oral Secretions Are Necessary and Sufficient for Herbivore-Specific Plant Responses,” PP 125 (2001): 711– 17. For more general information, I used two Wikipedia articles on tomato and tobacco hornworm: http://en.wikipedia.org/wiki/Tomato and http://en.wikipedia.org/wiki/Manduca_sexta. For general descriptions of plant VOCs: Natalia Dudareva, Antje Klempien, Joëlle K. Muhlemann, and Ian Kaplan, “Biosynthesis, Function and Metabolic Engineering of Plant Volatile Organic Compounds,” NP 198 (2013): 16–32; A. Kessler and I. T. Baldwin, “Defensive Function of Herbivore-Induced Plant Volatile Emissions in Nature,” Science 291 (2001): 2141–44; Erin Pichersky, Joseph P. Noel, and Natalia Dudareva, “Biosynthesis of Plant Volatiles: Nature’s Diversity and Ingenuity,” Science 311 (2006): 808–11; Stephen A. Goff and Harry J. Klee, “Plant Volatile Compounds: Sensory Cures for Health and Nutritional Value?” Science 311 (2006): 815–19; Silke Allmann and Ian T. Baldwin, “Insects Betray Themselves in Nature to Predators by Rapid Isomerization of Green Leaf Volatiles,” Science 329 (2010): 1075–78; and Martin Heil, “Herbivore- Induced Plant Volatiles: Targets, Perception and Unanswered Questions,” NP 204 (2014): 297– 306. For whitefly resistance: Qi Su, Kerry M. Oliver, Wen Xie, Qingjun Wu, Shaoli Wang, and Youjun Zhang, “The Whitefly-Associated Facultative Symbiont Hamiltonella defensa Suppresses Induced Plant Defences in Tomato,” FE 29 (2015): 1007–18. For the interactions that include the herbivores and their predators, see the following (with particular emphasis on the hornworm): Martin Heil, “Indirect Defence via Tritrophic Interactions,” NP 178 (2008): 41–61; Nina E. Fatouros et al., “Plant Volatiles Induced by Herbivore Egg Deposition Affect Insects of Different Trophic Levels,” PLoS ONE 7 (2012): e43607, doi:10.1371/journal.pone.0043607; Rayka Halitschke, Johan A. Stenberg, Danny Kessler, André Kessler, and Ian T. Baldwin, “Shared Signals—‘Alarm Calls’ from Plants Increase Apparency to Herbivores and Their Enemies in Nature,” EL 11 (2008): 24–34; M. R. Kant, K. Ament, M. W. Sabelis, M. A. Haring, and R. C. Schuurink, “Differential Timing of Spider Mite-Induced Direct and Indirect Defenses in Tomato Plants,” PP 135 (2004):

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483–95; André Kessler and Martin Heil, “The Multiple Faces of Indirect Defences and Their Agents of Natural Selection,” FE 25 (2011): 348–57; Justin B. Runyon, Mark C. Mescher, and Consuelo M. De Moraes, “Volatile Chemical Cues Guide Host Location and Host Selection by Parasitic Plants,” Science 313 (2006): 1964– 67; and Martin Heil, “Herbivore-Induced Plant Volatiles: Targets, Perception and Unanswered Questions,” NP 204 (2014): 297–306. Where insect sounds induce chemical responses: H. M. Appel and R. B. Cocraft, “Plants Respond to Leaf Vibrations Caused by Insect Herbivore Chewing,” Oecologia 175 (2014): 1257–66. Where volatile chemical messages are transformed into the defense: Koichi Sugimoto et al., “Intake and Transformation to a Glycoside of (Z)-3-hexenol from Infested Neighbors Reveals a Mode of Plant Odor Reception and Defense,” PNAS 111 (2014): 7144–49. Where additional trophic levels are involved, affecting parasitoids: Jeltje M. Stam et al., “Plant Interactions with Multiple Insect Herbivores: From Community to Genes,” ARPB 65 (2014): 689–713. For examples of plants recruiting animals, particularly insects, for their defense, see the previously cited article by Janzen, and Suzanne Koptur, “Experimental Evidence for Defense of Inga (Mimosoideae) Saplings by Ants,” Ecology 65 (1984): 1787–93; Suzanne Koptur, “Alternative Defenses against Herbivores in Inga (Fabaceae: Mimosoideae) over an Elevational Gradient,” Ecology 66 (1985): 1639– 50; Alain DeJean, Champlain Djiêto-Lordon, and Jérôme Orivel, “The Plant Ant Tetraponera aethiops (Pseudomyrmecinae) Protects Its Host Myrmecophyte Barteria fistulosa (Passifloraceae) through Aggressiveness and Predation,” BiolJLS 93 (2008): 63–69; Jacob R. Goheen and Todd M. Palmer, “Defensive Plant Ants Stabilize Megaherbivore-Driven Landscape Change in an African Savanna,” CB 20 (2010): 1766–72; and Victor Rico-Gray and Paulo S. Oliveira, The Ecology and Evolution of Ant-Plant Interactions (Chicago: University of Chicago Press, 2007). For communication between trees via the production of volatile chemicals: Nawaporn Onkokesung et al., “Jasmonic Acid and Ethylene Modulate Local Responses to Wounding and Simulated Herbivory in Nicotiana attenuata Leaves,” PP 153 (2010): 785–98; Wouter van Hoven, “Mortalities in Kudu (Tragelaphus strepsiceros) Populations Related to Chemical Defence in Trees,” Journal of African Zoology 105 (1991): 141–45; Wouter van Hoven and D. Furstenburg, “The Use of Purified Condensed Tannin as a Reference in Determining Its Influence on Rumen Fermentation,” Comparative Biochemistry and Physiology l0lA (1992): 381–85; Caroline C. von Dahl and Ian T. Baldwin, “Deciphering the Role of Ethylene in Plant- Herbivore Interactions,” Journal of Plant Growth Regulation 26 (2007): 201–9; and Bruce Adie, José Manuel Chico, Ignacio Rubio-Somoza, and Roberto Solano, “Modulation of Plant Defenses by Ethylene,” Journal of Plant Growth Regulation 26 (2007): 160–77. For the relationships of these complex signaling pathways to the controversial topics of plant neurobiology and intelligence, I used the following articles: Jyotasana Gulati, Sang-Gyu Kim, Ian T. Baldwin, and Emmanuel Gaquerel, “Deciphering Herbivory-Induced Gene-to-Metabolite Dynamics in Nicotiana attenuata Tissues Using a Multifactorial Approach,” PP 162 (2013): 1042–59; Jörg Fromm

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and Silke Lautner, “Electrical Signals and Their Physiological Significance in Plants,” PCE 30 (2007): 249– 57; Daniel Charnozitz, What a Plant Knows: A Field Guide to the Senses (New York: Scientific American/Farrar, Straus and Giroux, 2012); Eric D. Brenner et al., “Plant Neurobiology: An Integrated View of Plant Signaling,” TPS 11 (2006): 413–19; Amedeo Alpi et al., “Plant Neurobiology: No Brain, No Gain?” TPS 12 (2007): 135–36; Eric D. Brenner, Rainer Stahlberg, Stefano Mancuso, František Baluska, and Elizabeth Van Volkenburgh , “Response to Alpi et al.: Plant Neurobiology: The Gain Is More Than the Name,” TPS 12 (2007): 285–86; Anthony Trewavas, “What Is Plant Behavior?” PCE 32 (2009): 606–16; Anthony Trewavas, “Plant Intelligence,” Naturwissenschaften 92 (2005): 401–13 (on stomatal control and the diffuse intelligence systems of plants); and Anthony Trewavas, “Green Plants as Intelligent Organisms,” TPS 10 (2005): 414–19. The scientific names of plants mentioned in order in the text: spinach = Spinachia oleracea L. (Chenopodiaceae); New Zealand spinach = Tetragonia tetragonioides (Pallas) Kunze (Aizoaceae); Malabar spinach = Basella alba L. (Basellaceae); water spinach = Ipomoea aquatica Forrsk. (Convolvulaceae); African spinach = Celosia argentea L. (Amaranthaceae); Swiss Chard = Beta vulgaris L. (Chenopodiaceae); kale = Brassica oleracea L. (Brassicaceae); tea = Camellia sinensis (L.) Kuntze (Theaceae); tobacco = Nicotiana tabacum L. (Solanaceae); coca = Erythroxylum coca Lam. (Erythroxylaceae); ayahuasca = Banisteriopsis caapi (Griseb.) Morton (Malpighiaceae); foxglove = Digitalis purpurea L. (Plantaginaceae); oleander = Nerium oleander L. (Apocynaceae); cabbage = Brassica oleracea L. (Brassicaceae); Brussel sprouts = Brassica oleracea L. (Brassicaceae); mustard greens = Brassica juncea (L.) Vassilii Czernajew (Brassicaceae); boquillo = Boquila trifoliolata (DC.) Decne. (Lardizabalaceae); Brazilian rubber tree = Hevea brasiliensis (A. Juss.) Muell. Arg. (Euphorbiaceae); tomato = Solanum lycopersicum L. (Solanaceae); potato = Solanum tuberosum L. (Solanaceae); hook thorn = Senegalia caffra (Thunb.) P.J.H. Hurter & Mabb. (Fabaceae); bullhorn acacia = Vachellia cornigera (L.) Seigler & Ebinger; bittersweet nightshade = Solanum dulcamera L. (Solanaceae); inga = Inga densiflora Benth. and I. punctata Willd. (Fabaceae); Barteria = Barteria fistulosa Mast. (Passifloraceae); vanilla = Vanilla planifolia Jackson (Orchidaceae); cloves = Syzygium aromaticum (L.) Merr. & Perry (Myrtaceae); all- spice = Pimenta dioica (L.) Merr. (Myrtaceae); thyme = Thymus vulgaris L. (Menthaceae); cinnamon = Cinnamomum verum J. Presl (Lauraceae); rosemary = Rosmarindus officinalis L. (Menthaceae); oregano = Origanum vulgare L. (Menthaceae); bay leaf = Laurus nobilis L. (Lauraceae); tarragon = Artemisia dracunculus L. (Asteraceae); coriander = Coriandrum sativum L. (Apiaceae); lavender = Lavandula angustifolia Mill. (Menthaceae); rue = Ruta graveolens L. (Rutaceae); sage = Salvia officinalis L. (Menthaceae); Chinese cabbage, bok choy = Brassica rapa L. (Brassicaceae); collard greens = Brassica oleracea L. (Brassicaceae).

Chapter Thirteen: Homes The opening quotes are from James Dickey, The Selected Poems (Middletown, CT: Wesleyan University Press, 1998), and Paul Shepard, Man in the Landscape (New York: Knopf,

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1967). For James Nelson and “Treehouse Masters,” see an article by Stephen Kurutz in the New York Times, “Houses for Dreamers (and Kids),” May 29, 2013; and the Animal Planet homepage http://www.animalplanet.com/tv-shows/treehouse-masters/.

For nest-building activities among the primates, see Susan M. Cheyne, Dominic Rowland, Andrea Höing, and Simon J. Husson, “How Orangutans Choose Where to Sleep: Comparison of Nest-Site Variables,” Asian Primates Journal 3 (2013): 13–17; Barbara Fruth and Gottfried Hohmann, “Nest Building Behavior in the Great Apes: The Great Leap Forward?” in W. C. McGrew, L. F. Marchant, and T. Nishida, eds., Great Ape Societies (Cambridge: Cambridge University Press, 1996), 225–40; Mbangin Mulavwa et al., “Nest Groups of Wild Bonobos at Wamba: Selection of Vegetation and Tree Species and Relationships between Nest Group Size and Party Size,” American Journal of Primatology 72 (2010): 575–86; A. R. Brownlow, A. J. Plumptre, V. Reynolds, and R. Ward, “Sources of Variation in the Nesting Behavior of Chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda,” American Journal of Primatology 55 (2001): 49–55; A. E. Russon, D. P. Handayani, P. Kuncoro, and A. Ferisa, “Orangutan Leaf-Carrying for Nest-Building: Toward Unraveling Cultural Processes,” Animal Cognition 10 (2007): 189–202; and Kathelijne Koops, William C. McGrew, Tetsuro Matsuzawa, and Leslie A. Knapp, “Terrestrial Nest-Building by Wild Chimpanzees (Pan troglodytes): Implications for the Tree-to-Ground Sleep Transition in Early Hominins,” American Journal of Physical Anthropology 148 (2012): 351–61. I used my own recollections to describe the homes of the Temuan and Warli, and checked with John Dransfield on the identity of the palm in the Temuan house. For a general description of bat roosts, see J. D. Altringham, T. McOwat, and L. Hammond, Bats: Biology and Behaviour (Oxford: Oxford University Press, 1996); and Thomas H. Kunz and L. F. Lumsden, “Ecology of Cavity and Foliage Roosting Bats,” in Bat Ecology, ed. Thomas Kunz and Brock Fenton (Chicago: University of Chicago Press, 2003), 3– 89. For articles on the use of leaves in tent- making: K. Stoner, “Leaf Selection by the Tent-Making Bat Artibeus watsoni in Asterogyne mauritiana Palms in Southwestern Costa Rica,” JTE 16 (2000): 151–57; and Thomas H. Kunz, Marty S. Fujita, Anne P. Brooke, and Gary F. McCracken, “Convergence in Tent Architecture and Tent-Making Behavior among Neotropical Paleotropical Bats,” Journal of Mammalian Evolution 2 (1994): 57–78. For tent-making in the white Honduran fruit bat: A. P. Brooke, “Tent Selection, Roosting Ecology and Social Organization of the Tent-Making Bat, Ectophylla alba, in Costa Rica,” Journal of Zoology 221 (1990): 11–19; B. Rodríguez-Herrera, R. A. Medellín, and M. Gamba-Rios, “Roosting Requirements of White Tent-Making Bat Ectophylla alba (Chiroptera: Phyllostomidae),” Acta Chiropterologica 10 (2008): 89–95; R. M. Timm and J. Mortimer, “Selection of Roost Sites by Honduran White Bats, Ectophylla alba (Chiroptera: Phyllostomatidae),” Ecology 57 (1976): 385–89; and Gloriana Chaverri and Erin H. Gillam, “Sound Amplification by Means of a Horn-like Roosting Structure in Stix’s Disc-Winged Bat,” PRSB 280 (2013), doi:20132362. The following articles document my discussion of weaver ants: N. Azuma, K.

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Ogata, T. Kikuchi, and S. Higashi, “Phylogeography of Asian Weaver Ants, Oecophylla smaragdina,” ER 21 (2006): 126–36; M. Chapuisat and L. Keller, “Division of Labour Influences the Rate of Ageing in Weaver Ant Workers,” PRSB 269 (2002): 909–13; W. Federle, W. Baumgartner, and B. Hölldober, “Biomechanics of Ant Adhesive Pads: Frictional Forces Are Rate- and Temperature-Dependent,” Journal of Experimental Biology 207 (2004): 67–74; B. Hölldober and E. O. Wilson, “Weaver Ants— Social Establishment and Maintenance of Territory,” Science 195 (1977): 900– 902; A. Lioni, C. Sauwens, G. Theraulaz, and J. L. Deneubourg, “Chain Formation in Oecophylla longinoda,” Journal of Insect Behavior 14 (2001): 679–96; R. K. Peng, K. Christian, and K. Gibb, “Locating Queen Ant Nests in the Green Ant, Oecophylla smaragdina (Hymenoptera, Formicidae),” Insectes Sociaux 45 (1998): 477– 80; and J. W. S. Bradshaw, R. Baker, and P. E. Howse, “Chemical Composition of the Poison Apparatus Secretions of the African Weaver Ant, Oecophylla longinoda, and Their Role in Behaviour,” Physiological Entomology 4 (1979): 39–46. Concerning phytotelmata, see the following general reviews: Bassett Maguire Jr., “Phytotelmata: Biota and Community Structure Determination in Plant-Held Waters,” ARES 2 (1971): 439–64; and R. L. Kitching, “Food Webs in Phytotelmata: ‘Bottom-Up’ and ‘Top-Down’ Explanations for Community Structure,” Annual Review of Entomology 46 (2001): 729–60. For tank bromeliads: Peter Armbruster, Robert A. Hutchinson, and Peter Cotgreave, “Factors Influencing Community Structure in a South American Tank Bromeliad Fauna,” Oikos 96 (2002): 225–34; Michael Balke, “Ancient Associations of Aquatic Beetles and Tank Bromeliads in the Neotropical Forest Canopy,” PNAS 105 (2008): 6356–61; David H. Benzing, Karen Henderson, Bruce Kessel, and JoAnne Sulak, “The Absorptive Capacities of Bromeliad Trichomes,” AJB 63 (1976): 1009–14; David H. Benzing, “Foliar Specializations for Animal-Assisted Nutrition in Bromeliaceae,” in Insects and Plant Surfaces, ed. B. E. Juniper and S. E. Southwood (London: Edward Arnold, 1986), 235–56; J. H. Frank and L. P. Lounibos, “Insects and Allies Associated with Bromeliads: A Review,” Terrestrial Arthropod Reviews 1 (2008): 125–53; Mason J. Ryan and Deborah S. Barry, “Competitive Interactions in Phytotelmata— Breeding Pools of Two Poison-Dart Frogs (Anura: Dendrobatidae) in Costa Rica,” Journal of Herpetology 45 (2011): 438–43; Barbara A. Richardson, “The Bromeliad Microcosm and the Assessment of Diversity in a Neotropical Forest,” Biotropica 31 (1999): 321–36, and Scott Zona and Maarten J. M. Christenhusz, “Litter-Trapping Plants: FilterFeeders of the Plant Kingdom,” BJLS 179 (2015): 554–86. Ant gardens as sites for air plants are described in S. E. Kleinfeldt, “AntGardens: The Interaction of Codonathe crassifolius (Gesneriaceae) and Crematogaster longispina (Formicideae),” Ecology 59 (1978): 449– 56; S. E. Kleinfeldt, “AntGardens,” in Insects and Plant Surfaces, ed. B. E. Juniper and S. E. Southwood (London: Edward Arnold, 1986), 283–94; Céline Leroy, Bruno Corbara, Alain Dejean, and Régis Céréghino, “Ants Mediate Foliar Structure and Nitrogen Acquisition in a Tank-Bromeliad,” NP 183 (2009): 1124–33. For the relationship between tanks and carnivory, see Victor A. Albert, Ste-

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phen E. Williams, and Mark W. Chase, “Carnivorous Plants: Phylogeny and Structural Evolution,” Science 257 (1992): 1491–495; Barry E. Juniper, “The Path to Carnivory,” in Insects and Plant Surfaces, ed. B. E. Juniper and S. E. Southwood (London: Edward Arnold, 1986), 96–217; and Thomas J. Givnish, E. L. Burkhardt, R. E. Happel, and J. D. Weintraub, “Carnivory in the Bromeliad Brocchinia reducta: With a Cost/Benefit Model for the General Restriction of Carnivorous Plants to Sunny, Moist, Nutrient-Poor Habitats,” AN 124 (1984): 479–97. For articles on aspects of epiphyll biology, see T. F. Preece and C. H. Dickinson, eds., Ecology of Leaf Surface Micro- Organisms (New York: Academic Press, 1971)— old but good. For microbes: Steven E. Lindow and Maria T. Brandl, “Microbiology of the Phyllosphere,” Applied and Environmental Microbiology 69 (2003): 1875– 83; Robert R. Junker and Dorothea Tholl, “Volatile Organic Compound Mediated Interactions at the Plant-Microbe Interface,” Journal of Chemical Ecology 39 (2013): 810–25; Nathanaël Delmotte et al., “Community Proteogenomics Reveals Insights into the Physiology of Phyllosphere Bacteria,” PNAS 106 (2009): 16428–33; and T. L. W. Carver and S. J. Gurr, “Filamentous Fungi on Plant Surfaces,” APR 23 (2006): 368–92. For larger organisms: Phyllis D. Coley, Thomas A. Kursar, and Jose-Luis Machado, “Colonization of Tropical Rain Forest Leaves by Epiphylls: Effects of Site and Host Plant Leaf Lifetime,” Ecology 74 (1993): 619–23; Phyllis D. Coley and Thomas A. Kursar, “Causes and Consequences of Epiphyll Colonization,” in Tropical Forest Plant Ecophysiology, ed. Stephen S. Mulkey, Robin L. Chazdon, and Alan P. Smith (New York: Chapman and Hall, 1996), 337–62; Linda L. Kinkel, “Microbial Population Dynamics on Leaves,” Annual Review of Phytopathology 35 (1997): 327–47; Julian Monge-Najera and Mario A. Blanco, “The Influence of Leaf Characteristics on Epiphyllic Cover: A Test of Hypotheses with Artificial Leaves,” Tropical Bryology 11 (1995): 5–9; Sylvain Pincebourde and H. Arthur Woods, “Climate Uncertainty on Leaf Surfaces: The Biophysics of Leaf Microclimates and Their Consequences for Leaf-Dwelling Organisms,” FE 26 (2012): 844–53; and Barbara Bentley and Edward J. Carpenter, “Direct Transfer of Newly- Fixed Nitrogen from Free-Living Epiphyllous Free-Living Microorganisms to Their Host Plant,” Oecologia 63 (1984): 52–56. For a general review on leaf mining insects, see H. A. Hespenheide, “Bionomics of Leaf-Mining Insects,” Annual Review of Entomology 36 (1991): 535–60. For detailed articles informing my discussions, see Leo J. Hickey and Ronald W. Hodges, “Lepidopteran Leaf Miners from the Early Eocene Wind River Formation of Northwestern Wyoming,” Science 189 (1975): 718– 20; Yoshiko Ayabe and Takatoshi Ueno, “Complex Feeding Tracks of the Sessile Herbivorous Insect Ophiomyia maura as a Function of the Defense against Insect Parasitoids,” PLoS One 7 (2012): e32594, doi:10.1371/journal.pone.0032594; Shinji Sugiura and Kazuo Yamazaki, “Host Plant, Oviposition Behavior and Larval Ecology of a Sawfly Leafminer, Profenusa japonica (Hymenoptera: Tenthredinidae),” Entomological Science 6 (2003): 247– 51; and Kazuo Yamazaki, “Leaf Mines as Visual Defensive Signals to Herbivores,” Oikos 119 (2010): 796–801.

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For articles on insect galls, I used K. C. Larson and T. G. Whitham, “Manipulation of Food Resources by a Gall-Forming Aphid: The Physiology of Sink-Source Interactions,” Oecologia 88 (1991): 15–21; A. E. Weis and A. Kapelinski, “Variable Selection on Eurosta’s Gall Size. II. A Path Analysis of the Ecological Factors Behind Selection,” Evolution 48 (1994): 734– 45; Raham Stone and Karsten Schönrogge, “The Adaptive Significance of Insect Gall Morphology,” TREE 18 (2008): 512–522; and Carolyn Class and Warren T. Johnson, “Galls on Plants,” Cornell University Cooperative Extension Bulletin, 2012, http://www.cornell.edu/cals/entomology /extension/idl/idlfactsheetlist/cfm. For general discussions of interactions between plants and ants, see Martin Heil and Doyle McKey, “Protective Ant-Plant Interactions as Model Systems in Ecological and Evolutionary Research,” AREES 34 (2003): 425– 53; Camilla R. Huxley, “Symbiosis between Ants and Epiphytes,” Biological Reviews 55 (1980): 321– 40; Camilla R. Huxley, “Evolution of Benevolent Ant-Plant Relationships,” in Insects and Plant Surfaces, ed. B. E. Juniper and S. E. Southwood (London: Edward Arnold, 1986), 257–92; and Victor Rico-Gray and Paulo S. Oliveira, The Ecology and Evolution of Ant-Plant Interactions (Chicago: University of Chicago Press, 2007). For general reviews of mite domatia, see David Evans Walter, “Living on Leaves: Mites, Tomenta, and Leaf Domatia,” Annual Review of Entomology 41 (1996): 101– 14; and D. J. O’Dowd and M. F. Willson, “Association between Mites and Leaf Domatia,” TREE 6 (1991): 179– 82. See the following for detailed descriptions: Anurag A. Agrawal, “Do Leaf Domatia Mediate a Plant-Mite Mutualism? An Experimental Test on Predators and Herbivores,” Ecological Entomology 22 (1997): 371–76; Anurag A. Agrawal, Richard Karban, and Ramana G. Colfer, “How Leaf Domatia and Induced Plant Resistance Affect Herbivores, Natural Enemies and Plant Performance,” Oikos 89 (2000): 70–80; Andrew P. Norton, Greg EnglishLoeb, David Gadoury, and Robert C. Seem, “Mycophagous Mites and Foliar Pathogens: Leaf Domatia Mediate Tritrophic Interactions in Grapes,” Ecology 81(2000): 490–99; Andrew P. Norton, Greg English-Loeb, and Edward Belden, “Host Plant Manipulation of Natural Enemies: Leaf Domatia Protect Beneficial Mites from Insect Predators,” Oecologia 126 (2001): 535–42; Robert W. Pemberton and Charles E. Turner, “Occurrence of Predatory and Fungivorous Mites in Leaf Domatia,” AJB 76 (1989): 105–12; Lora A. Richards and Phyllis D. Coley, “Domatia Morphology and Mite Occupancy of Psychotria horizontalis (Rubiaceae) across the Isthmus of Panama,” Arthropod-Plant Interactions XX (2011), doi:10.1007/s11829-011-9161-4; Gustavo Q. Romero and Woodruff W. Benson, “Leaf Domatia Mediate Mutualism between Mites and a Tropical Tree,” Oecologia 140 (2004): 609–16; Gustavo Q. Romero and Woodruff W. Benson, “Biotic Interactions of Mites, Plants and Leaf Domatia,” COPB 8 (2005): 436–40; Patricia M. Tilney, Abraham E. van Wyk, and Chris F. van der Merwe, “Structural Evidence in Plectroniella armata (Rubiaceae) for Possible Material Exchange between Domatia and Mites,” PLoS ONE 7 (2012): e39984, doi:10.1371/journal.pone.0039984. For the complex diversity of domatia and mites in the camphor tree, see

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Sachiko Nishida, Akiyo Naiki, and Takayoshi Nishida, “Morphological Variation in Leaf Domatia Enables Coexistence of Antagonistic Mites in Cinnamomum camphora,” CJB 83 (2005): 93–101; Sachiko Nishida, Hirokazu Tsukaya, Hidetoshi Nagamasu, and Masumi Nozaki, “A Comparative Study on the Anatomy and Development of Different Shapes of Domatia in Cinnamomum camphora (Lauraceae),” AB 97 (2006): 601–10; and Norio Yamamura, “Conditions under Which Plants Help Herbivores and Benefit from Predators through Apparent Competition,” Ecology 88 (2007): 1593–99. For articles on ants and domatia, consult Camilla R. Huxley, “The Ant-Plants Myrmecodia and Hydnophytum (Rubiaceae), and the Relationships between Their Morphology, Ant Occupants, Physiology and Ecology,” NP 80 (1978): 231–68; Guillaume Chomicki and Susanne S. Renner “Phylogenetics and Molecular Clocks Reveal the Repeated Evolution of Ant-Plants after the Late Miocene in Africa and the Early Miocene in Australasia and the Neotropics,” NP 207 (2015): 411– 24; Céline Leroy, Alain Jauneau , Angélique Quilichini, Alain Dejean, and Jérôme Orivel. “Comparative Structure and Ontogeny of the Foliar Domatia in Three Neotropical Myrmecophytes,” AJB 97 (2010): 557– 65; John T. Longino, “Geographic Variation and Community Structure in an Ant-Plant Mutualism: Azteca and Cecropia in Costa Rica,” Biotropica 21 (1989): 126–32; J. T. Longino, “Azteca Ants in Cecropia Trees: Taxonomy, Colony Structure and Behavior,” in Ant-Plant Interactions, ed. Camilla R. Huxley and David F. Cutler (Oxford: Oxford University Press, 1961), 271–88; G. Q. Romero and T. J. Izzo, “Leaf Damage Induces Ant Recruitment in the Amazonian Ant- Plant Hirtella myrmecophila,” JTE 20 (2004): 675– 82; and C. L. Sagers, S. M. Ginger, and R. E. Evans, “Carbon and Nitrogen Isotopes Trace Nutrient Exchange in an Ant-Plant Mutualism,” Oecologia 123 (2000): 582–86. For Ant-Plant Interactions in Dischidia, see R. E. Holttum, Plant Life in Malaya (London: Longmans, Green, 1954); Tatyana Livshultz, Tran The Bach, Somchanh Bounphanmy, and Daniel Schott, “Dischidia (Apocynaceae, Asclepiadoideae) in Laos and Vietnam,” Blumea 59 (1995): 113– 34; Kathleen. K. Treseder, Diane D. Davidson, and Jim R. Ehleringer, “Absorption of Ant-Provided Carbon Dioxide and Nitrogen by a Tropical Epiphyte,” Nature 375 (1995): 137–39; Livia Wanntorp, Alexander Kocyan, Ruurd van Donkelaar, and Suzanne S. Renner, “Towards a Monophyletic Hoya (Marsenieae, Apocynaceae): Inferences from the Chloroplast trnL Region and the rbcL-atpB Spacer,” Systematic Botany 31 (2006): 586–96; J. S. Weir and R. Kiew, “A Reassessment of the Relations in Malaysia between Ants (Crematogaster) on Trees (Leptospermum and Dacrydium) and Epiphytes of the Genus Dischidia (Asclepiadaceae) including ‘Ant-Plants,’ ” BiolJLS 27 (1986): 113–32. For ants and Tococa, see Gustavo Alvarez, Inge Armbrecht, Elizabeth Jiminéz, Heidi Armbrecht, and Patricia Uloa- Chacĕn, “Ant- Plant Association in Two Tococa Species from a Primary Rainforest of Colombian Choco (Hymenoptera: Formicidae),” Sociobiology 38 (2001): 585–602; M. X. A. Bizerril and E. M. Vieira, “Azteca Ants as Antiherbivore Agents of Tococa formicaria (Melastomataceae)

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in Brazilian Cerrado,” Studies in Neotropical Fauna and Environment 37 (2002): 145– 49; M. Cabrera and K. Jaffe, “A Trophic Mutualism between the Myrmecophytic Melastomataceae Tococa guianensis Aublet and an Azteca Ant Species,” Ecotropicos 7 (1994): 1–10; Céline Leroy, Alain Jauneau , Angélique Quilichini, Alain Dejean, and Jérôme Orivel, “Comparative Structure and Ontogeny of the Foliar Domatia in Three Neotropical Myrmecophytes,” AJB 97 (2010): 557–65; Fabian A. Michelangeli, “Ant Protection against Herbivory in Three Species of Tococa (Melastomataceae) Occupying Different Environments,” Biotropica 35 (2003): 181–88; Fabian A. Michelangeli, “Neotropical Myrmecophilous Melastomataceae: An Annotated List and Key,” Proceedings of the California Academy of Sciences 61 (Series 4, 2010): 409– 49; Susanne S. Renner and Robert E. Ricklefs, “Herbicidal Activity of DomatiaInhabiting Ants in Patches of Tococa guianensis and Clidemia heterophylla,” Biotropica 30 (1998): 324–27; E. Svoma and W. Morawetz, “Drusenhare, Emergenzen und Blattdomatien bei der Ameisenpflanze Tococa occidentalis (Melastomataceae),” Botanische Jahrbuecher fuer Systematik Pflanzengeschichte und Pflanzengeographie 114 (1992): 185–200. For discussions and research on the importance in plant-animal interactions in agriculture, see J. D. Major, “The Influence of Ants and Ant Manipulation on the Cocoa Farm Fauna,” JAE 13 (1976): 157–75; Victor Rico-Gray and Paulo S. Oliveira, The Ecology and Evolution of Ant-Plant Interactions (Chicago: University of Chicago Press, 2007); Paul van Mele and Nguyen Thi Thu Cue, Ants as Friends: Improving Your Tree Crops with Weaver Ants (Egham, UK: CABI, 2007). For a general appreciation of plant/animal coevolution and some elegant examples, particularly in association with fungi, see Martin Heil, “Indirect defense via Tritrophic Interactions,” NP 178 (2008): 41– 61; Alain Dejean, P. J. Solano, J. Ayroles, B. Corbara, and J. Orivel, “Arboreal Ants Build Traps to Capture Prey,” Nature 434 (2005): 973; Emmanuel Deffosez et al., “Ant-Plants and Fungi: A New Three- Way Symbiosis,” NP 182 (2009): 942– 49; Emmanuel Deffosez et. al., “Plant-Ants Feed Their Host Plant, but Above All a Fungal Symbiont to Recycle Nitrogen,” PRSB 278 (2011): 1419– 26; Rumsais Blatrix et al., “Plant- Ants Use Symbiotic Fungi as a Food Source: New Insight into the Nutritional Ecology of Ant-Plant Interactions,” PRSB 279 (2012), doi:rspb20121403; and Rumsaïs Blatrix et al., “Repeated Evolution of Fungal Cultivar Specificity in Independently Evolved Ant-Plant-Fungus Symbioses,” PLOS One 8 (2013): e68101, doi:10.1371/journal. pone.0068101. The latter work came from the laboratory of Doyle McKey at the Université Montpellier, in France. For the pitcher plant-ant mutualism: Vincent Bazile et al., “A Carnivorous Plant Fed by Its Ant Symbiont: A Unique MultiFaceted Nutritional Mutualism,” PLoS One 7 (2012): 36179, doi:10.1371/journal. pone.oo36179; and Michael G. Schöner, Caroline R. Schöner, Ralph Simon, Sébastien J. Puechmaille, Liaw Lin Ji, and Gerald Kerth, “Bats Are Acoustically Attracted to Mutualistic Carnivorous Plants,” CB 25 (2015): 1–6. For quote by René Daumal at the end: Mount Analogue (New York: Penguin Books, 1974). For the scientific names of plants mentioned by order of appearance in the

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chapter: weeping willow = Salix babylonia L. (Salicaceae); Johannnesteijsmania = Johannesteijsmania altifrons (Reichb. F. & Zoll.) H. Moore (Arecaceae); wattle, karvi = Strobilanthes callosus Nees (Acanthaceae); teak = Tectona grandis L.f. (Verbenaceae); carnivorous bromeliad = Brocchinia reducta Bak. (Bromeliaceae); southern catopsis = Catopsis berteroniana (Schult. & Schult.f.) Mez (Bromeliaceae); North American pitcher plant = Sarracenia cf. flava L. (Sarraceniaceae); Asian pitcher plant = Nepenthes cf. raja Hook.f. (Nepenthaceae); camphor = Cinnamomum camphora (L.) J. Presl (Lauraceae); avocado = Persea americana Presl. (Lauraceae); bullhorn acacia = Vachellia cornigera (L.) Seigler & Ebinge (Fabaceae); barteria = Barteria fistulosa Mast (Passifloraceae); Dischidia, ant plant = Dischidia astephana Scort. ex King & Gamble (Apocynaceae); Leptospermum, gelam bukit = Leptospermum flavescens Sm. (Myrtaceae); urn vine = Dischidia major (Vahl) Merr. (Apocynaceae); snakewood, cecropia = Cecropia peltata L. (Urticaceae); macaranga, kenda = Macaranga cf. peltata (Roxb.) muell. (Euphorbiaceae); Hirtella = Hirtella physophora Mart. & Zucc. (Chrysobalanaceae).

Chapter Fourteen: Movements The two quotes at the beginning of the chapter are from Percy Bysshe Shelley, The Sensitive Plant (London: Haskell House Publishers, 1972), and Christina Lovin, “In the Garden of Carnivorous Plants,” Diner 6 (2006): 80. For Charles Darwin’s observations on leaf movement in the semaphore plant, in work published with his son Francis: The Power of Movement in Plants (London: John Murray, 1880).

For the history of leaf movements and its relationship to the scale of nature, I consulted Theophrastus, Enquiry into Plants, vol. I, part 4.7.2, trans. A. Hort (London: Heinemann, MCMXVI); Charles Bonnet, J. Wandelaar, and J.V.D. Schley, Recherches sur l’Usage des Feuilles dan les Plantes (Göttingen: E. Luzac, 1754); Craig W. Whippo and Roger P. Hangarter, “The ‘Sensational’ Power of Movement in Plants: A Darwinian System for Studying the Evolution of Behavior,” AJB 96 (2009): 2115–212; James T. Costa, “On Charles Darwin’s Reading of William Bartram’s Travels,” Chinquapin 17 (2009): 1–4; Mark W. Chase, Maarten J. M. Christenhusz, Dawn Sanders, and Michael F. Fay, “Murderous Plants: Victorian Gothic, Darwin and Modern Insights into Vegetable Carnivory,” BotJLS 161 (2009): 329–56; and Charles Webster, “The Recognition of Plant Sensitivity by English Botanists in the Seventeenth Century,” Isis 57 (1966): 5–23. For the introduction of the Venus flytrap to England: Richard Mabey, The Cabaret of Plants (New York: W. W. Norton, 2016), chap. 16. From E. Charles Nelson, Aphrodite’s Mousetrap: A Biography of Venus’s Flytrap (Martlesham, Suffolk, UK: Boethius Press, 1990). The quote by Annie Proulx, “The Sagebrush Kid,” in Just the Way It Is (New York: Scribners, 2008), is from Darwin’s other books on plant motion: Insectivorous Plants (London: John Murray, 1875) and The Movements and Habits of Climbing Plants (London: John Murray, 1865). For extravagant examples of carnivory, see Laurence Gaume and Yoël Forterre, “A Viscoelastic Deadly Fluid in Carnivorous Pitcher Plants,” PLoS One 2 (2007): e1185, doi:10.1371/journal.pone.0001185; Lijin Chin, Jonathan A. Moran, and

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Charles Clarke, “Trap Geometry in Three Giant Montane Pitcher Plant Species from Borneo Is a Function of Tree Shrew Body Size,” NP 186 (2010): 461–70; and A. S. Robinson, A. S. Fleischmann, S. R. McPherson, V. B. Heinrich, E. P. Gironella, and C. Q. Peña, “A Spectacular New Species of Nepenthes L. (Nepenthaceae) Pitcher Plant from Central Palawan, Philippines,” BotJLS 159 (2009): 195–202. For research on action potentials and leaf movements, see the historical article by John Burdon-Sanderson, “Note on the Electrical Phenomena Which Accompany Stimulation of the Leaf of Dionaea muscipula Ellis,” Philosophical Proceedings of the Royal Society of London 21 (1873): 495–96; plus the article on Burdon-Sanderson in Wikipedia: https://en.wikipedia.org/wiki/John_Burdon-Sanderson. For general reviews on action potentials in plants, see Eric Davies, “New Functions for Electrical Signals in Plants,” NP 161 (2004): 607–12; Jörg Fromm and Silke Lautner, “Electrical Signals and Their Physiological Significance in Plants,” PCE 30 (2007): 249–57; Rainer Hedrick, “The Physiology of Ion Channels and Electrogenic Pumps in Higher Plants,” ARPP 40 (1989): 539–59; Barbara Pickard, “Action Potentials in Higher Plants,” BR 39 (1973): 172–201; S. S. Pyatygin, V. A. Opritov, and V. A. Vodeneev, “Signaling Role of Action Potential in Higher Plants,” Russian Journal of Plant Physiology 55 (2008): 285– 91; Ruth L. Satter and Arthur W. Galston, “Mechanisms of Control of Leaf Movements,” ARPP 32 (1981): 83–110; Norbert Uehlein and Ralf Kaldenhoff, “Aquaporins and Plant Leaf Movements,” AB 101 (2008): 1–4; and Alexander Gallé, Silke Lautner, Jaume Flexas, and Jörg Fromm, “Environmental Stimuli and Physiological Responses: The Current View on Electrical Signaling,” EEB 114 (2015): 15– 21. For the importance of Chandra Bose in the history of this research, see his book The Nervous Mechanism of Plants (Calcutta: Longmans, Green and Company, 1926); and his biography in Wikipedia: http://en.wikipedia.org/wiki/Jagadish_Chandra_Bose. For recent work on similar signaling membrane receptors in plants and animals: Seyed A. R. Mousavi1, Adeline Chauvin, François Pascaud, Stephan Kellenberger, and Edward E. Farmer, “glutamate receptor-like Genes Mediate Leaf- to-Leaf Wound Signaling,” Nature 500 (2913): 422–29; Simon Michael and Hillel Fromm, “Closing the Loop on the GABA Shunt in Plants: Are GABA Metabolism and Signaling Entwined?” Frontiers in Plant Science 6 (2015): 419; and Sunita A. Ramesh et al., “GABA Signalling Modulates Plant Growth by Directly Regulating the Activity of Plant- Specific Anion Transporters,” Nature Communications 6 (2015): 7379. A recent review described the leaf movements of the semaphore plant in detail: Anders Johnsson, Vijay K. Sharma, and Wolfgang Engelmann, “The Telegraph Plant: Codariocalyx motorius (formerly also Desmodium gyrans),” in Plant Electrophysiology, ed. Alexander G. Volkov (Heidelberg: Springer Verlag, 2012), 85–124. For daily leaf movements, including “sleep” movements, I used the following articles. For ecological function: C. Arena, L. Vitale, and A. Virzo De Santo, “Paraheliotropism in Robinia pseudoacacia L.: An Efficient Strategy to Optimise Photosynthetic Performance under Natural Environmental Conditions,” Plant Biology 10 (2008): 194–201; Jim Ehleringer and Irwin Forseth, “Solar Tracking by Plants,”

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Science 210 (1980): 1094–98; Jim Ehleringer and S. D. Hammond, “Solar Tracking and Photosynthesis in Cotton Leaves,” Agricultural and Forest Meteorology 39 (1987): 25–35; J. T. Enright, “Sleep Movements in Leaves: In Defense of Darwin’s Interpretation,” Oecologia 54 (1982): 253– 59; Irwin N. Forseth and Jim R. Ehleringer, “Ecophysiology of Two Solar Tracking Desert Winter Annuals. IV. Effects of Leaf Orientation on Calculated Daily Carbon Gain and Water Use Efficiency,” Oecologia 58 (1983): 10–18; Claudio Pastenes, Paula Pimentel, and Jacob Lillo, “Leaf Movements and Photoinhibition in Relation to Water Stress in Field-Grown Beans,” JEB 56 (2005): 425–33; Mahmoud Raeini-Sarjaz, “Circadian Rhythm Leaf Movement of Phaseolus vulgaris and the Role of Calcium Ions,” PSB 6 (2011): 962– 67; Raymond B. Russell, Thomas T. Lei, and Erik T. Nilsen, “Freezing Induced Leaf Movements and Their Potential Implications to Early Spring Carbon Gain: Rhododendron maximum as Exemplar,” FE 23 (2009): 463– 71; and C. R. Schwintzer, “Energy Budgets and Temperatures of Nyctinastic Leaves on Freezing Nights,” PP 48 (1971): 203–7. For mechanisms behind leaf movements: Sarah L. Cronlund and Irwin N. Forseth, “Heliotropic Leaf Movement Response to H+/ATPase Activation, H+/ATPase Inhibition, and K+Channel Inhibition in Vivo,” AJB 82 (1995): 1507–13; P. M. Fleurat-Lessard and R. Satter, “Relationships between Structure and Motility of Albizzia Motor Organs: Changes in Ultrastructure of Cortical Cells during Dark-Induced Closure,” Protoplasma 128 (1985): 72–79; and Nava Moran, “Rhythmic Leaf Movements: Physiological and Molecular Aspects,” in Rhythms in Plants: Phenomenology, Mechanisms and Adaptive Significance, ed. S. Mancuso and S. Shabvala (Berlin: Springer-Verlag, 2007), 3–38. For the location of sensing: Judy Gougler Schmalstig, “Light Perception for Sun-Tracking Is on the Lamina in Crotalaria pallida (Fabaceae),” AJB 84 (1997): 308–14; Thomas C. Vogelmann, “Site of Light Perception and Motor Cells in a Sun Tracking Lupin (Lupinus succulentus),” PPl 62 (1984): 335–40; Thomas C. Vogelmann and L. O. Björn, “Response to Directional Light by Leaves of a Sun-Tracking Lupin (Lupinus succulentus),” PPl 59 (1983): 533– 38; and Chuanen Zhou et al., “Identification and Characterization of Petiolulelike Pulvinus Mutants with Abolished Nyctinastic Leaf Movement in the Model Legume Medicago truncatula,” NP 196 (2012), doi:10.1111/j.1469-8137.2012.04268.x. For circadian rhythms and leaf movements: C. Robertson McClung, “Plant Circadian Rhythms,” PC 18 (2006): 792– 803; R. H. Racusen and Ruth L. Satter, “Rhythmic and Phytochrome-Regulated Changes in Transmembrane Potential in Samanea Pulvini,” Nature 255 (1975): 408–10; Alison M. Smith et al., Plant Biology (New York: Garland Science, 2010); and Lincoln Taiz and Eduardo Zeiger, Plant Physiology, 4th ed. (Sunderland, MA: Sinauer Associates, 2006). For the odd idea of mimicry for the semaphore plant movements, see Simcha Lev-Yadun, “The Enigmatic Fast Leaflet Rotation in Desmodium motorium: Butterfly Mimicry for Defense?” PSB 8 (2013), doi:10.4161/psb.24473. For lunar effects on leaf movements: Peter W. Barlow, “Leaf Movements and Their Relationship with the Lunisolar Gravitational Force,” AB 116 (2015): 149–87. I consulted the following articles for rapid leaf movements in general: E. Was-

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sim Chehab, Elizabeth Eich, and Janet Braam, “Thigmomorphogenesis: A Complex Plant Response to Mechano-Stimulation,” JEB 60 (2009): 43–56; Livia Camilla, Trevisan Scorza, and Marcelo Carnier Dornelas, “Plants on the Move: Toward Common Mechanisms Governing Mechanically- Induced Plant Movements,” PSB 6 (2011): 1979–86; and Yoël Forterre, “Slow, Fast and Furious: Understanding the Physics of Plant Movements,” JEB 65 (2013): 4745– 60. In the sensitive plant, the following articles describe rapid movements: P. B. Applewhite and F. T. Gardner, “Rapid Leaf Closure of Mimosa in Response to Light,” Nature 233 (1971): 279–80; P. M. Fleurat-Lessard, “Structural and Ultrastructural Features of Cortical Cells in Motor Organs of Sensitive Plants,” Biological Reviews 63 (1988): 1–22; H. Toriyama and M. J. Jaffe, “Migration of Calcium and Its Role in the Regulation of Seismonasty in the Motor Cell of Mimosa pudica L.,” PP 49 (1972): 72–81; and K. Umrath and G. Kastberger, “Action Potentials of the High-Speed Conduction in Mimosa pudica and Neptunia plena,” Phyton 23 (1983): 65–78. For slow responses, modulated by growth regulators: Joachim Fisahnn, Oliver Herde, Lothar Willmitzer, and Hugo Peña-Cortés, “Analysis of the Transient Increase in Cytosolic Ca2+ during the Action Potential of Higher Plants with High Temporal Resolution: Requirement of Ca2+ Transients for the Induction of Jasmonic Acid Biosynthesis and PINII Gene Expression,” PCP 45 (2004): 456–59; P. M. Fleurat-Lessard and J.-L. Bonnemain, “Structural and Ultrastructural Characteristics of the Vascular Apparatus of the Sensitive Plant (Mimosa pudica L.),” Protoplasma 94 (1978): 127–43; E. Farmer and C.A. Ryan, “Interplant Communication: Airborne Methyl Jasmonate Induces Synthesis of Proteinase Inhibitors in Plant Leaves,” PNAS 87 (1990): 7713–16; Joanna K. Polko, Laurentius A. C. J. Voesenek, Anton J. M. Peeters, and Ronald Pierik, “Petiole Hyponasty: An Ethylene- Driven, Adaptive Response to Changes in the Environment,” AoB PLANTS (2011): plr031, doi:10.1093/aobpla/ plr031; S. Tsarumi and Y. Asahi, “Identification of Jasmonic Acid in Mimosa pudica and Its Inhibitory Effect on Auxin- and Light-Induced Opening of the Pulvinules,” PPl 64 (1985): 207– 11; Minoru Ueda and Yoko Nakamura, “Chemical Basis of Leaf Movement,” PCP 48 (2007): 900–907. For my discussion of leaf movements in carnivorous trapping plants, I consulted the following works for general information on carnivory: Wilhelm Barthlott, Stefan Porembski, Rüdiger Seine, and Inge Theisen, The Curious World of Carnivorous Plants (Portland, OR: Timber Press, 2007); Barry E. Juniper, Richard J. Robins, and Daniel M. Joel, Carnivorous Plants (London: Academic Press, 1989); Jim D. Karagatzides and Aaron M. Ellison, “Construction Costs, Payback Times, and the Leaf Economics of Carnivorous Plants,” AJB 96 (2009): 1612–19; Elzbieta Król1 et al., “Quite a Few Reasons for Calling Carnivores ‘the Most Wonderful Plants in the World,’ ” AB 109 (2012): 47–64; and Wolf-Ekkehard Lönnig and Heinz-Albert Becker, “Carnivorous Plants,” Nature Encyclopedia of the Life Sciences, www.els.net, 1–7. For general discussions on the trapping movements in plants: D. M. Joel, “Glandular Structures in Carnivorous Plants: Their Role in Mutual Exploitation of Insects,” in Insects and the Plant Surface, ed. B. E. Juniper and T. R. E.

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Southwood (London: Edward Arnold, 1986), 219–34; Thiago Paes de Barros De Luccia, “Mimosa pudica, Dionaea muscipula and Anesthetics,” PSB 7 (2012): 1163–67; and Simon Poppinga, Siegfried R. H. Hartmeyer, Tom Masselter, Irmgard Hartmeyer, and Thomas Speck, “Trap Diversity and Evolution in the Family Droseraceae,” PSB 8 (2013): 7, e24685. For discussions on the mechanisms of trap function in sundews: M. Bopp and I. Weber, “Studies on the Hormonal Regulation of the Leaf Blade Movement of Drosera capensis L.,” PPl 53 (1981): 491–96; Yoko Nakamura, Michael Reichelt, Veronika E. Mayer, and Axel Mithöfer, “Jasmonates Trigger Prey- Induced Formation of ‘Outer Stomach’ in Carnivorous Sundew Plants,” PRSB 280 (2013), doi:20130228; Simon Poppinga et al., “Catapulting Tentacles in a Sticky Carnivorous Plant,” PLoS ONE 7 (2012), doi:e45735; H. W. J. Ragetli, M. Wintraub, and E. Lo, “Characteristics of Drosera Tentacles: I. Anatomical and Cytological Detail,” CJB 50 (1972): 159–68; and Stephen E. Williams, “Comparative Physiology of the Droseraceae Sensu Stricto— How Do Tentacles Bend and Traps Close?” Proceedings of the Fourth ICPC (2002): 77–81. For the extensive literature on trap closure in the Venus flytrap, see B. Buchen, D. Henzel, and A. Sievers, “Polarity in Mechanoreceptor Cells of Trigger Hairs of Dionaea muscipula Ellis,” Planta 158 (1983): 458–68; Jacques Dumais and Yoël Forterre, “ ‘Vegetable Dynamicks’: The Role of Water in Plant Movements,” Annual Review of Fluid Mechanics 44 (2012): 453–78; Wayne R. Fagerberg, “Changes in Trap Tissue Relationships during Closure/Reopening in Venus’s Flytrap (Dionaea muscipula Ellis): A Possible Model to Explain Trap Morphological Changes,” Fourth IPCP Conference Proceedings (2002): 83–89; Yoël Forterre, Jan M. Skotheim, Jacques Dumais and L. Mahadevan, “How the Venus Flytrap Snaps,” Nature 433 (2005): 421– 25; D. Hodick and A. Sievers, “The Action Potential of Dionaea muscipula Ellis,” Planta 174 (1988): 8–18; F. T. Licthner and S. E. Williams, “Prey Capture and Factors Controlling Trap Narrowing in Dionaea (Droseraceae),” AJB 64 (1977): 881–86; D. Hodick and A. Sievers, “On the Mechanism of Trap Closure of Venus Flytrap (Dionaea muscipula Ellis),” Planta 179 (1989): 32–42; M. J. Jaffe, “The Role of ATP in Mechanically Stimulated Rapid Closure of the Venus’s Flytrap,” PP 51 (1973): 17– 18; Andrej Pavlovic, L’udmila Slováková, Camilla Pandolfin, and Stefano Mancuso, “On the Mechanism Underlying Photosynthetic Limitation upon Trigger Hair Irritation in the Carnivorous Plant Venus Flytrap (Dionaea muscipula Ellis),” JEB 62 (2011): 1991–2000; Alexander G. Volkov, Tejumade Adesina, Vladislav S. Markin, and Emil Jovanov, “Kinetics and Mechanism of Dionaea muscipula Trap Closing,” PP 146 (2008): 694–702; Alexander G. Volkov, Tejumade Adesina, and Emil Jovanov, “Charge Induced Closing of Dionaea muscipula Ellis Trap,” Bioelectrochemistry 74 (2008): 16–21; and Jennifer Böhm et al., “The Venus Flytrap Dionaea muscipula Counts Prey-Induced Action Potentials to Induce Sodium Uptake,” CB 26 (2016): 1–10. For interest in traps as inspirations for new devices: Ingo Burgert and Peter Fratzl, “Actuation Systems in Plants as Prototypes for Inspired Devices,” PTRSA

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367 (2009): 1541–57; Minoru Taya, “Bio-Inspired Design of Intelligent Materials,” in Symposium on Electromotive Polymers and Devices, ed. E. Y. Bar-Cohen (Bellingham, WA: SPIE Proceedings, March 2–6, 2003); Ruoting Yang, Scott C. Lenaghan, Mingjun Zhang, and Lijin Xia, “A Mathematical Model on the Closing and Opening Mechanism for Venus Flytrap,” PSB 5 (2010): 968–78; and Minjiun Zhang et al., “Nanofibers and Nanoparticles from the Insect-Capturing Adhesive of the Sundew (Drosera) for Cell Attachment,” Journal of Nanobiotechnology 8 (2010): 20. For articles on the evolution of traps, see Victor A. Albert, Stephen E. Williams, and Mark W. Chase, “Carnivorous Plants: Phylogeny and Structural Evolution,” Science 257 (1992): 1491–95; Kenneth M. Cameron, Kenneth J. Wurdack, and Richard W. Jobson, “Molecular Evidence for the Common Origin of Snap-Traps among Carnivorous Plants,” AJB 89 (2002): 1503–9; Aaron M. Ellison et al., “The Evolutionary Ecology of Carnivorous Plants,” AER 33 (2003): 2– 74; Aaron M. Ellison and Nicholas J. Gotelli, “Energetics and the Evolution of Carnivorous Plants— Darwin’s ‘Most Wonderful Plants in the World,’ ” JEB 60 (2009): 19– 42; and Barry E. Juniper, “The Path to Carnivory,” in Insects and Plant Surfaces, ed. B. E. Juniper and S. E. Southwood (London: Edward Arnold, 1986), 96–217. For proto-carnivory, as the transition to full carnivory in plants: George G. Spomer, “Evidence of Protocarnivorous Capabilities in Geranium viscosissimum and Potentilla arguta and Other Sticky Plants,” IJPS 160 (1999): 98–101; T. R. Radhamani, L. Sudarshana, and Rani Krishnan, “Defense and Carnivory: Dual Role of Bracts in Passiflora foetida,” Journal of Bioscience 20 (1995): 657–64; Thomas C. Gibson and Donald M. Waller, “Evolving Darwin’s ‘Most Wonderful’ Plant: Ecological Steps to a SnapTrap,” NP 183 (2009): 575–87; and a Wikipedia article: https://en.wikipedia.org /wiki/Protocarnivorous_plant. The scientific names are provided for the common names listed in order of appearance: banana = Musa acuminata Colla (Musaceae); semaphore or dancing plant = Codariocalyx motorius (Houtt.) Ohashi (Fabaceae); sensitive plant = Mimosa pudica L. (Fabaceae); Venus flytrap = Dionaea muscipula Ellis (Droseraceae); sagebrush = Artemisia tridentata L. (Asteraceae); giant pitcher plant = Nepenthes rajah Hook. f. (Nepenthaceae); life plant = Biophytum sensitivum (L.) DC (Oxalidaceae); tamarind tree = Tamarindus indica L. (Fabaceae); common bean = Phaseolus vulgaris L. (Fabaceae); tomato = Solanum lycopersicum L. (Solanaceae); Arabidopsis = Arabidopsis thaliana (L.) Heynh (Brassicaceae); bladderwort = Utricularia cf. vulgaris L. (Lentibulariaceae); sundew = Drosera cf. rotundifolia L. (Droseraceae); waterwheel plant = Aldrovandra vesiculosa L. (Droseraceae); North American pitcher plant = Sarracenia sp. (Sarraceniaceae.); Asian pitcher plant = Nepenthes sp. (Nepenthaceae); plumbago, or lead plant = Plumbago auriculata Lam. (Plumbaginaceae); sticky geranium = Geranium viscosissimum Fischer & C. Meyer (Geraniaceae); gooseberry, current = Ribes cf. sanguineum Pursh (Grossulariaceae).

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Chapter Fifteen: Seeing Leaves The lines by William Wordsworth are from “Lines Written a Few Miles above Tintern Abbey,” in Wordsworth: Poems (New York: Everyman’s Library, 1995). The quote by Mary Oliver is from New and Selected Poems, vol. 2 (Boston: Beacon Press, 2005).

On the value of wilderness exploration in fostering a love for nature, see Peter H. Kahn Jr. and Patricia H. Hasbach, eds., The Rediscovery of the Wild (Cambridge, MA: MIT Press, 2013). The following articles are on experiences in nature as sacred and motivational: Stanley T. Asah, David N. Bengston, and Lynne M. Westphal, “The Influence of Childhood: Operational Pathways to Adulthood Participation in Nature-Based Activities,” ENVB 44 (2012): 545–69; Louise Chawla, “Ecstatic Places,” Children’s Environments Quarterly 7 (1990): 18– 23; Louise Chawla, “Childhood Experiences Associated with Care for the Natural World,” Children, Youth & Environments 17 (2007): 144– 70; Judith Chen- Hsuan Cheng and Martha C. Monroe, “Connection to Nature: Children’s Affective Attitude toward Nature,” ENVB 44 (2012): 31– 49; P. Kahn and S. Kellert, Children and Nature: Psychological, Sociocultural and Evolutionary Investigations (Cambridge, MA: MIT Press, 2000); Ilias Kamitsis and Andrew J. P. Francis, “Spirituality Mediates the Relationship between Engagement with Nature and Psychological Wellbeing,” JEP 36 (2013): 136–43; Daniel Levi and Sara Kocher, “Perception of Sacredness at Heritage Religious Sites,” ENVB 45 (2013): 912– 30; S. Mazumdar and S. Mazumdar, “Religion and Place Attachment: A Study of Sacred Places,” JEP 24 (2004): 385–97; D. Seamon, “Emotional Experience of the Environment,” American Behavioral Scientist 27 (1984): 757–70; and Kim-Pong Tam, “Dispositional Empathy with Nature,” JEP 35 (2013): 92–104. The idea of “It and We and I” was explored by Ken Wilber in The Marriage of Sense and Soul: Integrating Science and Religion (New York: Harmony Books, 1999). On the grieving of natural scientists: Lynn Alvin Brant, “Grieving for Nature,” BioScience 42 (1992): 739–40. I reviewed the literature on the effects of nature on human welfare up through 2006 in Nature’s Palette: The Science of Plant Color (Chicago: University of Chicago Press, 2007), and am adding here additional and more recent articles on different benefits. Direct medical benefits: Terry Hartig and Clare Cooper Marcus, “Healing Gardens— Places for Nature in Health Care,” Lancet 368 (2006): S36– S37; Eeva Karjalainen, Tytti Sarjala, and Hannu Raitio, “Promoting Human Health through Forests: Overview and Major Challenges,” Environmental Health and Preventative Medicine 15 (2010): 1–8; Karin Laumann, Tommy Gärling, and Kjell Morten Stormark, “Selective Attention and Heart Rate Responses to Natural and Urban Environments,” JEP 23 (2003): 125– 34; R. Mitchell and F. Popham, “Effect of Exposure to Natural Environment on Health Inequalities: An Observational Population Study,” Lancet 9650 (2008): 1655– 60; Yuko Mizumo- Matsumoto, Syogi Kobashi, Yutaka Kobata, Osumo Ishakawa, and Fjusayo Asono, “Horticultural Therapy Has Beneficial Effects on Brain Functions in Cerebrovascular Diseases,”

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IC MED 2 (2008): 169– 82; T. Nelson and K. Hansen, “Do Green Areas Affect Health? Results from a Danish Survey on the Use of Green Areas and Health Indicators,” in Danish Centre for Forest, Landscape and Planning (Copenhagen: University of Copenhagen, 2006); Eeva Karjalainen, Tytti Sarjala, and Hannu Raitio, “Promoting Human Health through Forests: Overview and Major Challenges,” Environmental Health and Preventative Medicine 15 (2010): 1–8; B.-S. Kweon, R. S. Ulrich, V. D. Waler, and L. G. Tassinary, “Anger and Stress: The Role of Landscape Posters in an Office Setting,” EB 40 (2008): 355–81; R. S. Ulrich, R. F. Simons, and M. A. Miles, “Effects of Environmental Simulations and Television on Blood Donor Stress,” Journal of Architectural and Planning Research 20 (2003): 38–47; and Matthew Wichrowski, Jonathan Whiteson, Francois Haas, Ana Mola, and Mariano Rey, “Effects of Horticultural Therapy on Mood and Heart Rate in Patients Participating in an Inpatient Cardiopulmonary Rehabilitation Program,” Journal of Cardiopulmonary Rehabilitation 25 (2005): 270–74. Psychosocial benefits: Marc G. Berman, John Jonides, and Stephen Kaplan, “The Cognitive Benefits of Interacting with Nature,” Psychological Science 19 (2008): 1207–12; Linda Buzzell and Craig Chalquist, eds., Ecotherapy: Healing with Nature in Mind (San Francisco: Sierra Club Books, 2009); Geoffrey H. Donovan and Jeffrey P. Prestemon, “The Effect of Trees on Crime in Portland, Oregon,” EB 44 (2012): 3–30; Silvia Collado, Henk Staats, and José A. Corraliza, “Experiencing Nature in Children’s Summer Camps: Affective, Cognitive and Behavioral Consequences,” JEP 33 (2013): 37–44; Rachel Kaplan and Stephen Kaplan, “Well-Being, Reasonableness, and the Natural Environment,” Applied Psychology: Health and Well- Being 3 (2011): 304– 21; Ian Alcock et al., “Longitudinal Effects on Mental Health of Moving to Greener and Less Green Urban Areas,” Environmental Science and Technology 48 (2014): 1247– 55; Andrea Faber Taylor and Frances E. Kuo, “Children with Attention Deficits Concentrate Better after a Walk in the Park,” Journal of Attention Disorders 12 (2009): 402– 9; Andrea Faber Taylor and Frances E. (Ming) Kuo, “Could Exposure to Everyday Green Spaces Help Treat ADHD? Evidence from Children’s Play Settings,” Applied Psychology: Health and Well-Being 3 (2011): 281–303; Esther M. Sternberg, Healing Spaces: The Science of Place and Well- Being (Cambridge, MA: Harvard University Press, 2009); and Catharine Ward Thompson and Peter A. Aspinall, “Natural Environments and Their Impact on Activity, Health, and Quality of Life,” Applied Psychology: Health and Well- Being 3 (2011): 230– 60. Prison environments: J. Farbstein, M. Farling, and R. E. Wener, Effects of a Simulated Nature View on Cognitive and Psycho-Physiological Responses of Correctional Officers in a Jail Intake Area (Washington, DC: National Institute of Corrections, 2009); J. S. Rice and L. L. Remy, “Impact of Horticultural Therapy on Psychosocial Functioning among Urban Jail Inmates,” Journal of Offender Rehabilitation 26 (1998): 169– 91; Richard E. Wener, The Environmental Psychology of Prisons and Jails (New York: Cambridge University Press, 2012). For childhood experiences in nature, see citations provided under therapeutic effects of nature and the following: I. Altman and J. Wohlwill, eds., Children and

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the Environment (New York: Plenum Press, 1978); Louise Chawla, In the First Country of Places: Nature, Poetry, and Childhood Memory (Albany: State University of New York Press, 1994); Richard Louv, The Nature Principle. Human Restoration and the End of NatureDeficit Disorder (Chapel Hill, NC: Algonquin Books, 2011). For the quote on children’s experience in nature: Carl Jung, Memories, Dream, Reflections (London: Fontana Press, 1967); for additional works on Jung and nature: Meredith Sabini, ed., The Earth Has a Soul: Jung on Nature, Technology, and Modern Life (Berkeley, CA: North Atlantic Books, 2002); and Polly Young- Eisendrath and Terence Dawson, eds., The Cambridge Companion to Jung, 2nd ed. (Cambridge: Cambridge University Press, 2008). Paul Shepard’s quote is from Coming Home to the Pleistocene (Washington, DC: Island Press, 1998). For Jane Goodall’s quote: Reason for Hope: A Spiritual Journey (with Phillip Berman) (New York: Warner Books, 1999). Nalini Nadkarni’s experiences with children and adolescents (and the quote) are from Between Earth and Sky: Our Intimate Connection to Trees (Berkeley: University of California Press, 2008). For summaries of research on forest bathing: Eeva Karjalainen, Tytti Sarjala, and Hannu Raitio, “Promoting Human Health through Forests: Overview and Major Challenges,” Environmental Health and Preventative Medicine 15 (2010): 1– 8; Qing Li et al., “Effect of Forest Bathing Trips on Human Immune Function,” Environmental Health and Preventative Medicine 15 (2010): 9–17; Bum Jin Park, Yuko Tsunetsugu, Tamami Kasetani, Takahide Kagawa, and Yoshifumi Miyazaki, “The Physiological Effects of Shinrin-yoku (Taking in the Forest Atmosphere or Forest Bathing): Evidence from Field Experiments in 24 Forests across Japan,” Environmental Health and Preventative Medicine 15 (2010): 18–26; and Won Sop Shin, Poung Sik Yeoun, Rhi Wha Yoo, and Chang Seob Shin, “Forest Experience and Psychological Health Benefits: The State of the Art and Future Prospect in Korea,” Health and Preventative Medicine 15 (2010): 38–47. For the direct effects on brain physiology, using EEG and fMRI: Peter Aspinall, Panagiotis Mavros, Richard Coyne, and Jenny Roe, “The Urban Brain: Analysing Outdoor Physical Activity with Mobile EEG,” British Journal of Sports Medicine 47 (2013), doi:10.1136/bjsports-2012-091877; Michael D. Hunter et al., “The State of Tranquility: Subjective Perception Is Shaped by Contextual Modulation of Auditory Connectivity,” NeuroImage 53 (2010): 611–18; and Florian Lederbogen, “City Living and Urban Upbringing Affect Neural Social Stress Processing in Humans,” Nature 474 (2011): 498– 501. Such research was based on epidemiological differences in mental illness between rural and urban areas: Christopher Dye, “Health and Urban Living,” Science 319 (2008): 766– 68; Daniel P. Kennedy and Ralph Adolphs, “Stress and the City,” Nature 474 (2011): 452–53; J. Peen, R. A. Schoevers, A. T. Beekman, and J. Dekker, “The Current Status of Urban-Rural Differences in Psychiatric Disorders,” Acta Psychiatrica Scandinavica 121 (2010): 84–93; Gregory N. Bratman, Gretchen C. Daily, Benjamin J. Levy, and James J. Gross, “The Benefits of Nature Experience: Improved Affect and Cognition,” Landscape and Urban Planning 138 (2015): 41–50; Gregory N. Bratman, J. Paul Hamilton, Kevin S. Hahn,

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Gretchen C. Daily, and James J. Gross, “Nature Experience Reduces Rumination and Subgenual Prefrontal Cortex Activation,” PNAS 112 (2015): 8567–72. For biophilia and evolutionary psychology, see the original book: Edmund O. Wilson, Biophilia (Cambridge, MA: Harvard University Press, 1986), and supporting works: Herman Pontzer, “Overview of Hominin Evolution,” Nature Education Knowledge 3 (2012): 8; a Wikipedia article, http://en.wikipedia.org/wiki/Timeline _of_evolutionary_history of_life, and Stephen R. Kellert and Edward O. Wilson, eds., The Biophilia Hypothesis (Washington, DC: Island Press, 1993). For the triune hypothesis of brain evolution: http://en.wikipedia.org/wiki/Triune_brain. I discuss neurobiological evidence consistent with the potential for biophilia and an evolutionary influence on nature perception in the areas of phobias, facial recognition, color perception, and scene perception. For references on phobias: Fredrik Åhs et al., “Disentangling the Web of Fear: Amygdala Reactivity and Functional Connectivity in Spider and Snake Phobia,” Psychiatry Research: Neuroimaging 172 (2009): 103– 8; Judy S. DeLoache and Vanessa LoBue, “The Narrow Fellow in the Grass: Human Infants Associate Snakes and Fear,” Developmental Science 12: (2009): 201–7; Antje B. M. Gerdes, Gabriele Uhl, and Georg W. Alpers, “Spiders Are Special: Fear and Disgust Evoked by Pictures of Arthropods.” Evolution and Human Behavior 30 (2009): 66–73; Lynne A. Isbell, “Snakes as Agents of Evolutionary Change in Primate Brains,” Journal of Human Evolution 51 (2006): 1–35; Quan Van Le et al., “Pulvinar Neurons Reveal Neurobiological Evidence of Past Selection for Rapid Detection of Snakes,” PNAS 95 (2013), doi:10.1073/pnas.1312648110; and Arne Öhman and Susan Mineka, “The Malicious Serpent: Snakes as a Prototypical Stimulus for an Evolved Module of Fear,” Current Directions in Psychological Science 12 (2003): 5–9. For the recognition of faces, particularly threatening ones, these articles are important: Fredrik Åhs, Caroline F. Davis, Adam X. Gorka, and Ahmad R. Hariri, “Feature-Based Representations of Emotional Facial Expressions in the Human Amygdala,” Social Cognitive and Affective Neuroscience 8 (2013), doi:10.1093/scan/nst112; Christine L. Larson, Joel Aronoff, Issidoros C. Sarinopoulos, and David C. Zhu, “Recognizing Threat: A Simple Geometric Shape Activates Neural Circuitry for Threat Detection,” Journal of Cognitive Neuroscience 21 (2008): 1523–35; Christine L. Larson, Joel Aronoff, and Elizabeth L. Steuer, “Simple Geometric Shapes Are Implicitly Associated with Affective Value,” Motivation and Emotion 36 (2012): 404–13; Nikolaas N. Oosterhof and Alexander Todorov, “The Functional Basis of Face Valuation,” PNAS 105 (2008): 11087–92; Robert W. Shannon, Christopher J. Patrick, Noah C. Venables, and Sheng He, “ ‘Faceness’ and Affectivity: Evidence for Genetic Contributions to Distinct Components of Electrocortical Response to Human Faces,” NeuroImage 83 (2013): 609–15; Alexander Toet and Susanne Tak, “Look Out, There Is a Triangle Behind You! The Effect of Primitive Geometric Shapes on Perceived Facial Dominance,” i-Perception 4 (2013): 53–56; Mathias Weymar, Andreas Löw, Arne Öhman, and Alfons O. Hamm, “The Face Is More than Its Parts” Brain Dynamics of Enhanced Spatial Attention to Schematic Threat,” Neuroimage 58 (2011): 946–54.

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For references on innate color values, see those from chapters 3 and 12 in David W. Lee, Nature’s Palette, cited above, plus the following articles: A. J. Elliot, M. A. Maier, A. C. Moller, R. Friedman, and J. Meinhardt, “Color and Psychological Functioning: The Effect of Red on Performance Attainment,” Journal of Experimental Psychology: General 136 (2007): 154–68; Anya C. Hurlbert and Yazhu Ling, “Biological Components of Sex Differences in Color Preference,” CB 17 (2004): R623–25; Ravi Mehta and Rui (Juliet) Zhu, “Blue or Red? Exploring the Effect of Color on Cognitive Task Performances,” Science 323 (2009): 1226–29; Stephen E. Palmer and Karen B. Schloss, “An Ecological Valence Theory of Human Color Preference,” PNAS 107 (2010): 8877–82; Terry Regierl and Paul Kay, “Language, Thought, and Color: Whorf Was Half Right,” Trends in Cognitive Sciences 13 (2009): 439–46; Guillaume Thierry, Panos Athanasopoulos, Alison Wiggett, Bejamin Dering, and Jan-Rouke Kuipers, “Unconscious Effects of Language-Specific Terminology on Preattentive Color Perception,” PNAS 106 (2009): 4067–70; Iris Zemach, Susan Chang, and Davida Y. Teller, “Infant Color Vision: Prediction of Infants’ Spontaneous Color Preferences,” Vision Research 47 (2007): 1368– 81; and D. Dreiskaemper, B. Strauss, N. Hagemann, and D. Busch, “Influence of Red Jersey Color on Physical Parameters in Combat Sports,” Journal of Sports and Exercise Psychology 35 (2013): 44–49. For the neuroesthetics of landscapes, see Irving Biederman and Edward A. Vessel, “Perceptual Pleasure and the Brain,” American Scientist 94 (2006): 249–55; D. D. Dilks, J. B. Julian, A. M. Paunov, and N. Kanwisher, “The Occipital Place Area Is Causally and Selectively Involved in Scene Perception,” Journal of Neuroscience 33 (2013): 1331–36; Russell A. Epstein and Joshua B. Julian, “Scene Areas in Humans and Macaques,” Neuron 79 (2013): 615–17; Russell A. Epstein and Sean P. Macevoy, “Making a Scene in the Brain,” in Vision in 3D Environments, ed. L. R. Harris and M. R. M. Jenkin (Cambridge: Cambridge University Press, 2011); Gwang-Won Kim et al., “Functional Neuroanatomy Associated with Natural and Urban Scenic Views in the Human Brain: 3.0T Functional MR Imaging,” Korean Journal of Radiology 11 (2010): 507–13; Shahin Nasr, Kathryn J. Devaney, and Roger B. H. Tootell, “Spatial Encoding and Underlying Circuitry in Scene-Selective Cortex,” NeuroImage 83 (2013): 892–900; Ana Torralbo et al., “Good Exemplars of Natural Scene Categories Elicit Clearer Patterns than Bad Exemplars but Not Greater BOLD Activity,” PLoS ONE 8 (2013): e58594, doi:10.1371/journal.pone.0058594; Dirk B. Walther, Barry Chai, Eamon Caddigan, Diane M. Beck, and Li Fei-Feib, “Simple Line Drawings Suffice for Functional MRI Decoding of Natural Scene Categories,” PNAS 108 (2011): 9661–66; Xiaomin Yue, Edward A. Vessel, and Irving Biederman, “The Neural Basis of Scene Preferences,” NeuroReport 18 (2007): 525–29. For a philosophical context for our relationship to nature, see the book by Wilber, quoted above, and for the discussion on philosophy and human perception, I used the biographies in the Stanford Encyclopedia of Philosophy (www.plato.stanford.edu) for John Locke, Martin Heidegger, and Maurice Merleau-Ponty. I also consulted

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the following books and articles: David Abram, The Spell of the Sensuous: Perception and Language in a More-than-Human World (New York: Vintage, 1987); Lawrence W. Howe, “Heidegger’s Discussion of ‘The Thing’: A Theme for Deep Ecology,” Between the Species (Spring 1993): 93–97; Richard L. Lanigan, “Communication Science and Merleau-Ponty’s Critique of the Objectivist Illusion,” in Hugh J. Silverman, Algis Mickunas, Theodore Kisiel, and Alphonso Lingis, eds., The Horizons of Continental Philosophy. Essays on Husserl, Heidegger, and Merleau-Ponty (Boston: Klewer Academic Publishers, 1988), 206–26; Martin Heidegger, The Question Concerning Technology and Other Essays (New York: Garland, 1977); Maurice Merleau-Ponty, The Primacy of Perception (Evanston, IL: Northwestern University Press, 1964); Maurice Merleau-Ponty, The Visible and the Invisible, from Basic Writings (London: Routledge, 2004); and William J. Richardson, Heidegger: Through Phenomenology to Thought, 4th ed. (New York: Fordham University Press, 2003). Merleau-Ponty’s quote concerning the leaf is from Themes from the Lectures at the Collège de France, 1952–1960, trans. John O’Neill (Evanston, IL: Northwestern University Press, 1970). For Arne Næss, the founding philosopher of deep ecology, see his biography on Wikipedia (http://en.wikipedia.org/wiki/Arne_Naess) and his book Ecology, Community and Lifestyle: An Outline of an Ecosophy (Cambridge: Cambridge University Press, 1989). For other writings on deep ecology: Derrick Jensen, Dreams (New York: Seven Stories Press, 2011); Peter H. Kahn, The Human Relationship with Nature (Cambridge, MA: MIT Press, 1999); Peter H. Kahn Jr. and Patricia H. Hasbach, eds., Ecopsychology: Science, Totems, and the Technological Species (Cambridge, MA: MIT Press, 2012); Theodore Roszak, The Voice of the Earth (Boston: Phares Press, 2002); John Seed, Joanna Macy, Patricia Fleming, and Arne Næss, Thinking Like a Mountain (Philadelphia: New Society, 1988). For the environmental sensibility of traditional people, I used several articles in the edited book The Biophilia Hypothesis, as well as Abram’s book, cited above, and my own experiences with the Warli and the Temuan. Location of the Christmas spirit in the brain: Anders Hougaard et al., “Evidence of a Christmas Spirit Network in the Brain: Functional MRI Study,” British Medical Journal 351 (2015): h6266. For the effects of wilderness experiences: R. Bedard, L. Rosen, and T. VachaHaase, “Wilderness Therapy Programs for Juvenile Delinquents: A MetaAnalysis,” Journal of Therapeutic Wilderness Camping 3 (2003): 7–13; and R. Fuller, K. Irvine, P. Devine-Wright, P. Warren, and K. Gaston, “Psychological Effects of Green Space Increase with Biodiversity,” Biological Letters 3 (2007): 390–94. For the influence of meditation on brain activity: Steven Steinhubl et al., “Cardiovascular and Nervous System Changes during Meditation,” FHN 9 (2015): 145; Tim Gard, Maxime Taquet, Rohan Dixit, Britta K. Hölzel, Bradford C. Dickerson, and Sara W. Lazar, “Greater Widespread Functional Connectivity of the Caudate in Older Adults Who Practice Kripalu Yoga and Vipassana Meditation than in Controls,” FHN 9 (2015): 137; and Catherine E. Kerr, Matthew D. Sacchet, Sara W. Lazar, Christopher I. Moore, and Stephanie R. Jones, “Mindfulness Starts with

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the Body: Somatosensory Attention and Top-Down Modulation of Cortical Alpha Rhythms in Mindfulness Meditation,” FHN 7 (2013): 12. On the importance of design as a fundamental expression of human nature and the possibility of altering nature by design: Martin H. Krieger, What’s Wrong with Plastic Trees? Artifice and Authenticity in Design (Westport, CT: Praeger, 2000); Martin H. Krieger, “What’s Wrong with Plastic Trees?” Science 179 (1973): 446–55; and Bethany Ojalehto, Sandra R. Waxman, and Douglas L. Medin, “Teleological Reasoning about Nature: Intentional Design or Relational Perspectives?” Trends in Cognitive Sciences 17 (2013): 166–71. On the practice and ethics of faking nature (also discussed by Krieger above): Robert Elliot, Faking Nature: The Ethics of Environmental Restoration (Florence, KY: Routledge, 1997); Eric Katz, “The Ethical Significance of Human Intervention in Nature,” Restoration and Management Notes 9 (1991): 90–96; Theodore Roosevelt, “Nature Fakers,” in Roosevelt’s Writings, ed. Maurice Garton Fulton (New York: Macmillan, 1920); and Joshua J. Lawler et al., “The Theory Behind, and the Challenges of, Conserving Nature’s Stage in a Time of Rapid Change,” Conservation Biology 29 (2015): 618–29. On the esthetics of exotic forests: Emma Marris, Rambunctious Garden: Saving Nature in a Post-Wild World (New York: Bloomsbury, 2011). For the interface between technology and nature: Peter H. Kahn Jr. et al., “A Plasma Display Window? The Shifting Baseline Problem in a Technologically Mediated Natural World,” JEP 28 (2008): 192–99; Peter H. Kahn, Rachel L. Severson, and Jolina H. Ruckert, “The Human Relation with Nature and Technological Nature,” Current Directions in Psychological Science 18 (2009): 27–42; Peter H. Kahn Jr., Technological Nature: Adaptation and the Future of Human Life (Cambridge, MA: MIT Press, 2011); and O. Pergans and P. Zaradic, “Is Love of Nature in the U.S. Becoming Love of Electronic Media? 16-Year Downtrend in National Park Visits Explained by Watching Movies, Playing Video Games, Internet Use, and Oil Prices,” Journal of Environmental Management 80 (2006): 387–93. For information about Tom Defanti, see http://www.calit2.net/people/staff_detail.php?id=67. For virtual reality: Margaret Sullivan, “The Tricky Terrain of Virtual Reality,” NYT, November 14, 2015; Michael Cipley, “Virtual Reality ‘Wild’ Trek, with Reese Witherspoon,” NYT December 14, 2014. For Patrick Blanc: http://www.murvegetalpatrickblanc.com/. For reSTART: www.netaddictionrecovery.com/our-mission/partners.html. For some insights on creativity and nature, see Ruth Ann Atchley, David L. Strayer, and Paul Atchley, “Creativity in the Wild: Improving Creative Reasoning through Immersion in Natural Settings,” PLoS ONE 7 (2012): eS1474, doi:10.1371/ journalpone0051474; and Janetta Mitchell McCoy and Gary W. Evans, “The Potential Role of the Physical Environment in Fostering Creativity,” Creativity Research Journal 14 (2002): 409–26. For the multisensory nature of garden aesthetics: Stephanie Ross, What Gardens Mean (Chicago: University of Chicago Press, 1998). For beauty and science: Frank Wilczek, A Beautiful Question: Finding Nature’s Deep Design (New York: Penguin, 2015); and Crispin Sartwell, “Beauty,” in Stanford Encyclopedia of Philosophy, http://plato.stanford.edu/entries/beauty/.

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Common names of plants include, in order: mango = Mangifera indica L. (Anacardiaceae); European beech = Fagus sylvatica L. (Fagaceae); agallocha, agarwood = Aquilaria malaccensis Lam. (Thymeliaceae); durian = Durio zibethinus Murray (Malvaceae); Douglas fir = Pseudotsuga menziesii (Mirb.) Franco (Pinaceae); western red cedar = Thuja plicata Donn. ex D. Don (Cupressaceae).

illustr at ion n ot e s Unless directly credited (and all with locations and dates), the photographs used in this book were taken by the author. In a few cases, these are from Kodachrome transparencies taken over the decades, but mostly they are digital images taken with a Canon PowerShot SX200, particularly useful for extreme close- ups. Microscope photographs were taken with a Nikon Coolpix 4500 on a camera adapter. I frequently consulted David J. Mabberley, The Plant Book, 3rd ed. (Cambridge: Cambridge University Press, 2007), for plant names and authorities. I received generous support from many photographers, but particularly was helped by Brian Gunning, now Emeritus Professor at Australian National University, who “wrote the book” on plant cell structure and whose photographs were used in several places in the book. Citations used in credits may use abbreviations listed at the beginning of chapter notes, p. 347. Several words were used frequently in these notes for describing the illustrations, and I am substituting the following abbreviations for brevity:

FIU

Florida International University, Miami, FL

FTBG

Fairchild Tropical Botanic Garden, Miami, FL

HF

Harvard Forest, Petersham, MA

HOT

Francis Hallé, Roelof A. A. Oldeman, and P. Barry Tomlinson, Tropical Trees and Forests: An Architectural Analysis (Berlin: Springer-Verlag, 1978).

LM

light microscope photograph

LS

longitudinal (radial or tangential) section

MBG

Montgomery Botanical Center, Miami, FL

MIA

streets and yards of Miami, FL

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MPL

Library, Faculté de la Medicine, Université Montpellier

PD

paradermal section

SEM

scanning electron microscope photograph

TEM

transmission electron microscope photograph

TS

transverse tissue section

UM

University of Miami

Chapter One: Green Men

1.1 Left, at St. John’s College, Oxford, April 2008. Right, photographed at the National Museum of Denmark, in Copenhagen, courtesy of Wikimedia Commons. 1.2 Language tree redrawn from Thomas V. Gamkrelidze and Vjacˇeslav V. Ivanov, Indo-European and the Indo-Europeans: I. A Reconstruction and Historical Analysis of a ProtoLanguage and a Proto-Culture (New York: Mouton de Gruyter, 1995). 1.3 Left, Acanthus mollis L. (Acanthaceae), photographed at Old Royal Naval College, Greenwich, London, April 2015. Center, Butea monosperma (Lam.) Kuntze (Fabaceae), IA, February 2012. Right, Trifolium repens L. (Fabaceae) Philadelphia lawn, May 2013. 1.4 Photographed in Padua, Italy, April 1978. 1.5 Photographed in library of the Université Montpellier, Faculté de la Medecine, March 1978. 1.6 Courtesy of Wikimedia Commons. 1.7 Courtesy of the Metropolitan Museum of Art, New York City. 1.8 Courtesy of Wikimedia Commons. 1.9 Left, postcard courtesy of Archives, History Miami. Right, Coral Gables, FL, March 2009. 1.10 Left, display at Pinecrest Garden, MIA, December 2014. Right, photo provided by and courtesy of Norma Koch.

Chapter Two: Leaf History

2.1 Left, NASA/CXC/SAO. Right, Stromatalites are approximately 0.5 m across. 2.2 Phleum pretense L. (Poaceae), TEM, cell 40 μm in diameter. Courtesy of Brian Gunning and published in Plant Cell Biology on DVD, Information for Students and a Resource for Teachers (Heidelberg: Springer Verlag, 2009), www.springer.com /978-3-642-03690-3. 2.3. Tree of life inspired by diagram from Priscilla Spears, A Tour of the Flowering Plants (St. Louis, MO: Missouri Botanical Garden Press, 2006). 2.4 Left, Dawsonia longifolia (Bruch & Schimp.) Zanten (Polytrichaceae) photographed in cloud forest at 2,500 m on Mount Kinabalu, Sabah, May 1973. Right, Scapania bolanderi Aust. (Scapaniaceae), near Skagit River, Whatcom County, WA, March 2014.

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2.6 Left, Cooksonia cf. hemisphaerica W. H. Lang (Rhyniophyta), about 3 cm high. Right, Psilotum nudum (L.) P. Beauv (Psilotaceae), MIA, May 2014; stems are 2–3 mm thick. 2.7 Top, Sawdonia ornata (Dawson) F. M. Huber (Zosterophyllopsida), reconstruction from Henry N. Andrews, “Paleobotany, 1947–1972,” Annals of the Missouri Botanical Garden 61 (1974): 179–202, courtesy of the Missouri Botanical Garden Press. Bottom, Baragwanathia longifolia Lang & Cookson (Lycophyta); both images produced by the Victoria Museum in Australia and made available by Wikimedia. 2.8 Left, Lycopodium obscurum L. (Lycophyta, Lycopodiaceae); Loch Sheldrake Park, Sullivan County, NY, October 2013, 15 cm high. Right, Selaginella Willdenowii (Desv. ex Poir.) Baker (Lycophyta, Selaginellaceae); FTBG, August 2012, leaves are ca. 4 mm long. 2.9 Left, tree 7 m high, redrawn and colored; courtesy of Brad Seymour and the New York State Museum, Albany. Center, redrawn and colored from M. Hirmer, Handbuch der Paleobotanik. Bd. 1. Thallophyta – Bryophyta – Pteridophyta (Munich: R. Oldenbourg, 1927). Right, redrawn from Charles B. Beck, “Reconstruction of Archeopteris and Further Consideration of Its Phylogenetic Position,” AJB 44 (1962): 350–82. 2.11 Polystichum falcatum (L. f.) Diels (Dryopteridaceae), TS LM. 2.12 Left, Umbilicaria cf. mammulata (Ach.) Tuck. (Umbilicariaceae), Massachusetts, October 1998, thallus diameter ~7 cm. Right, Peltigera apthosa (L.) Willd. (Peltigeraceae), Skagit River, Whatcom County, WA, March 2013, photograph 8 cm across. 2.13 Top left, Elysia clarki, courtesy of Patrick Krug. See Michael Midlebrooks, Sydney K. Pierce, and Susan S. Bell, “Foraging Behavior under Starvation Conditions Is Altered via Photosynthesis in the Marine Gastropod, Elysia clarki,” PLoS ONE 6 (2011): e22162, doi:10.1371. Bottom left, Tridacna gigas L., from Komodo National Park, Indonesia, October 2006; photograph by Nick Hobgood. Right, Diana Reef, Pulau Batanta, Indonesia, May 2013. 2.14 Left, illustration from Francis Hallé, In Praise of Plants, trans. and preface by David W. Lee (Portland, OR: Timber Press, 2002).

Chapter Three: Green Machinery

3.1 Left and center, courtesy of Wikipedia. Right, from Vegetable Staticks, photographed MPL, March 1977. 3.2 Left, portrait by Ellen Sharples, Wikimedia. Right, from Experiments and Observations on Different Kinds of Air, vol. 2, MPL, April 1977. 3.3 Left, Wikimedia. Right, from “Untersuchungen über die Chlorophyllkörper und die Ihnen Homologen Gebilde,” Jahrbücher für Wissenschaftliche Botanik 16 (1885): 1–247; plate provided by Brian Gunning. 3.4 From David Lee, Nature’s Palette (Chicago: University of Chicago Press, 2007). 3.5 Left, spinach leaf thickness, 300 μm. Right, chloroplast length, 6 μm. Electron

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micrograph supplied by Professor James Barber and produced by Dr. Denis Greenwood, both of Imperial College London, through Brian Gunning (see fig. 2.3 above). 3.6 Reproduced with the permission by the American Society for Photobiology, from Holly Gorton (2010) Biological Action Spectra, Photobiological Sciences Online (ed. K. C. Smith), American Society for Photobiology, http:// www.photobiology.info/. 3.7 Chemical structures from Wikimedia. 3.8 Redrawn from Alison Smith et al., Plant Biology (New York: Garland Science, 2010), figs. 4.12, 4.16, and 4.19. 3.9 Chemical structures from Wikimedia. 3.10 Fig. 2 in Shelly Lumba et al., “A Mesoscale Abscisic Acid Hormone Interactome Reveals a Dynamic Signaling Landscape in Arabidopsis,” Developmental Cell 29 (2014): 360–72. 3.12 Efficiencies were documented in the articles cited in the chapter notes. 3.13 Hopea odorata Roxb. (Dipterocarpaceae), shade leaf was grown at 3% full sun; see David W. Lee et al., “Effects of Irradiance and Spectral Quality on Leaf Structure and Function in Seedlings of Two Southeast Asian Hopea (Dipterocarpaceae) Species,” AJB 87 (2000): 447–55. Height of images is 170 µm. 3.14 Left, Ruellia makoyana Hort. Makoy ex Closon (Acanthaceae), LM TS, thickness is 106 μm. Center, Nerium oleander L. (Apocynaceae), LM TS, thickness is 450 μm. Right, Saccharum officinale L. (Poaceae), thickness is 330 µm. 3.15 Left, Lithops optica (Marloth) N.E.Br. (Aizoaceae), Wikimedia. Right, sections are ~2 cm across.

Chapter Four: Nature’s Fabric

4.2 From Humboldt’s Essai sur la Géographie des Plantes: Accompagné d’une Tableau Physique des Régiones Équinoxiales (Paris: Levrault, Scholl et Compagnie, 1805), MPL. 4.3 Redrawn and condensed from Paul Richards, A Tropical Rainforest: An Ecological Study (Cambridge: Cambridge University Press, 1996), from data by Lord Medway, “Phenology of a Tropical Rain Forest in Malaya,” Biological Journal of the Linnean Society 4 (1972): 117– 46. Species diagrams from top to bottom: Cynometra malaccensis Meeuwen (Fabaceae), Garcinia sp. (Clusiaceae), Shorea dasyphylla Foxw. (Dipterocarpaceae), Erythroxylum cuneatum (Miq.) Kurz. (Erythroxylaceae), and Ficus sumatrana Miq. (Moraceae). 4.4 This is a pre-industrial biome map based on the LPX dynamic global vegetation model, prepared by Maria Martin Calvo of the Imperial College of London and assisted by Colin Prentice. 4.5 Used in David Lee, Nature’s Palette: The Science of Plant Color (Chicago: University of Chicago Press, 2007), fig. 2.10; and adapted from J. P. Kerr, G. W. Thurtell, and C. B. Tanner, “An Integrating Pyrometer for Climatological Observation Stations and Meso-Scale Networks,” Journal of Applied Meteorology 6 (1967): 688–94.

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4.6 From Working Group I, Intergovernmental Panel on Climate Change, Climate Change 2013: The Physical Science Basis (Fifth Assessment Report) (Cambridge: Cambridge University Press, 2013), from fig. 2.11, from M. Wild et al., “The Global Energy Balance from a Surface Perspective,” Climate Dynamics 40 (2013): 3107–34. 4.7 Redrawn from fig. 1, Taikan Oki and Shinjiro Kanae, “Global Hydrological Cycles and World Water Resources,” Science 313 (2006): 1068–72. 4.8 Both photographed July 1991. 4.9 For full citation, see chapter 5 from reference in fig. 4.6, above. 4.11 D. L. Royer, R. A. Berner, I. P. Montanez, N. J. Tabor, and D. J. Beerling, “CO2 as a Primary Driver of Phanerozoic Climate Change,” GSA Today 14, no. 3 (2004): 4–10, redrawn from figs. 2 & 4 with extinction events added.

Chapter Five: Leaf Economics

5.1 Portrait by Alexander Roslin, 1775, from Wikimedia. 5.2 Left, from Sri Lanka, 1960s, unknown photographer. Right, Wikimedia. 5.3 Left, Hans Willawaert, June 2007, from Wikimedia. Center and right, alpha tree in the Schulman Grove, Ancient Bristlecone Forest, Inyo National Forest, CA, August 1977. 5.4 Fig. 2a, field data from six biomes, in Peter B. Reich, Michael B. Walters, and David S. Ellsworth, “From Tropics to Tundra: Global Convergence in Plant Functioning,” PNAS 94 (1997): 13730–34. Permission of the National Academy of Sciences. 5.5 Left and right, FTBG, June 2013. Duckweed = Lemna minor L. (Araceae) and water fern = Azolla filiculoides Lam. (Pteridophyta, Azollaceae). 5.6 Left, FTBG, March 2011. Center and right, MBC, June 2003. 5.7 Camellia sinensis (L.) Kuntze (Theaceae).

Chapter Six: Metamorphosis

6.1 Left and right, courtesy of Wikimedia. 6.2 Photographed at MPL, March 1977. 6.3 Photographed at MPL, March 1977. 6.4 Photographed at MPL, March 1977 6.5 Center, Angiopteris evecta (Forster f.) Hoffm. (Davalliaceae), FTBG, May 2014. Left, Psychotria nervosa Sw. (Rubiaceae), MIA, June 2014. Right, Coffea Arabica L. (Rubiaceae), FTBG, January 2014. 6.6. Nehemiah Grew, Anatomy of Plants, MPL, March 1977. 6.7 Top left, diagram redrawn from fig. 25.4 in Peter H. Raven, Ray F. Evert, and Susan E. Eichhorn, Biology of Plants, 7th ed. (San Francisco: W. H. Freeman, 2005). Top right, Ricinus communis L. (Euphorbiaceae), LM, LS. Middle right, Artobotrys hexapetala (L. f.) Bandhari (Annonaceae). Bottom, Apium graveolens L. (Apiaceae), MIA, July 2015. 6.8 Acalypha amentacea Roxb. subsp. wilkesiana (Muell. Arg.) Fosb. (Euphorbiaceae), MIA, May 2012.

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6.9 Top left, Wikimedia. Bottom left, permission of Beth Krizak. Right, Zhongyuan Liu, Liguo Jia, Yanfei Mao, and Yuke He, “Classification and Quantification of Leaf Curvature,” JEB 61 (2010): 2757–67, fig. 2, open access. 6.10 Features in this diagram were derived from Brad T. Townsley and Neelima R. Sinha, “A New Development: Evolving Concepts in Leaf Ontogeny,” ARPB 63 (2012): 535–62, as well as a 2012 education module published in The Plant Cell. 6.11 Top, Chisocheton cf. sarawakanus (C.DC.) Harms (Meliaceae), see Jack B. Fisher, “Indeterminate Leaves of Chisocheton (Meliaceae): Survey of Structure and Development,” BotJLS 139 (2002): 207–21. Bottom, Lygodium microphyllum (Cav.) R. Br. (Lygodiaceae). 6.12 Left, Monophyllaea horsefieldii R. Brown (Gesneriaceae), leaf 25 cm long. Right, Bryophyllum daigremontianum (Raym.-Hamet & H. Perrier) A. Berger (Crassulaceae), plantlets 2 mm long. 6.13 Left, Monstera tenuis K. Koch (Araceae), height of photo 6 m, Las Selva Biological Station, April 1985. Right, Dolichandra unguis-cati (L.) L. Lohmann (Bignoniaceae): top, Wikimedia; middle and bottom, MIA, July 2014. 6.14 Left, Pandanus tectorius Parkinson (Pandanaceae), FTBG, June 2013. Center, Dypsis decaryii (Jum.) H. Beentje & J. Dransf. (Arecaceae), FTBG, July 2013. Right, Ravenala madagascariensis Sonn. (Strelitziaceae), MIA, July 2013. 6.15 Left, Helianthus annuus L. (Asteraceae). Center, Aeonium tabuliforme Webb & Berthel. (Crassulaceaea). Right, Brassica oleracea L. (Brassicaceae). 6.16 Top left and top right, Wikimedia. Bottom left, the Hubble Heritage (STScI / AURA)-ESA / Hubble Collaboration. 6.17 Left, Goethe in the Roman Campagna (1786) by Johann Heinrich Wilhelm Tischbein, Wikimedia. Right, Pierre Jean François Turpin, 1837, Wikimedia. 6.18 Top, influenced by fig. 5.78, in Alison M. Smith et al., Plant Biology (New York: Taylor and Francis, 2010). Bottom right, for explanation of mutant: Detlef Weigel and Elliot M. Meyerowitz, “The ABCs of Floral Homeotic Genes,” Cell 78 (1994): 203–9. 6.19 Left, from Darcy A. W. Thompson, On Growth and Form, 2nd ed. (Cambridge: Cambridge University Press, 1945), figs. 500 & 501 (p. 1045). Right, Przemysław Prusinkiewicz and Pierre Barbier de Reuille, “Constraints of Space in Plant Development,” JEB 61 (2010): 2117–29, fig. 7G, permission of Oxford University Press. 6.20 Left, Monstera deliciosa Liebm. (Araceae), FTBG, March 2014. Right, Aponogeton madagascariensis (Mirbel) Bruggen (Aponogetonaceae).

Chapter Seven: Architecture

7.1 Left, by Francisco Melzi, after 1510, from Wikipedia. Right, from Leonardo da Vinci, The Literary Works of Leonardo da Vinci, trans. Jean Paul Richter (London: S. Low, Marston, Searle & Rivington, 1883), vol. 1, plate 27, available from http:// www.sacred-texts.com.

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7.2 Victoria amazonica (Poeppig) Sowerby (Nymphaeaceae). Left, courtesy of Bok Tower Gardens; right, FTBG, June 2014, 12 cm across image. 7.3 Courtesy of www.copyrightexpired.com. 7.5 Both photographs courtesy of Wikipedia. 7.6 Left, Seattle Art Museum, June 2014. Right, purchased copyright from Canstockphoto.com. 7.7 Left, Melaleuca styphelioides Sm. (Myrtaceae), MIA, March 2003. Right, Fagus grandifolia Ehrh. (Fagaceae), HF, October 2004. 7.8 Left, redrawn from HOT, pp. 25, 88. 7.9 Left, HOT, 91. Right, Terminalia catappa L. (Combretaceae), MIA, January 1993. 7.10. Right, HOT, 85; Wodyetia bifurcata Irvine (Arecaceae). Left, HOT, 84; Corypha umbraculifera L. (Arecaceae). 7.11 Left, HOT, 97. Right, Delonix regia (Boj. ex Hook.) Raf. (Fabaceae), MIA, May 2010. 7.12 Top left, redrawn from Adrian D. Bell and P. Barry Tomlinson, “Adaptive Architecture in Rhizomatous Plants,” BotJLS 80 (1980): 125–60. Top right, redrawn from same article, 135. Bottom left and center, Medeola virginiana L. (Liliaceae), HF, October 2004. Bottom right, Alpinia zerumbet (Pers.) B. L. Burtt and R. M. Smith (Zingiberaceae), FTBG, July 2014. 7.13 Center, Fagus grandifolia L. (Fagaceae), HF, October 2004. Right, Cornus florida L. 7.14 Left, with permission of AB: Feng Wang et al., “A Stochastic Model of Tree Architecture and Biomass Partitioning: Application to Mongolian Scots Pines,” AB 107 (2011): 781–92, fig. 6G. Center, permission of JEB, Przemysław Prusinkiewicz and Pierre Barbier de Reuille, “Constraints of Space in Plant Development,” JEB 61 (2010): 2117–29, fig. 11. Right, P. Prusinkiewicz and W. Remphrey, “Characterization of Architectural Tree Models Using L-Systems and Petri Nets,” in L’arbre: The Tree 2000, ed. M. Labrecque (IQ Collectif, Canada, 2001, open library), 177–86, fig. 20. 7.15 Top left, see fig. 7.12, MIA, March 2014. Top right, permission of the AJB: Jack B. Fisher and Hisao Honda, “Branch Geometry and Effective Leaf Area: A Study of Terminalia- Branching Pattern. II. Survey of Real Trees,” AJB 66 (1979): 645–55, fig. 12. Bottom left, permission of the IJPS: Jack B. Fisher and Hisao Honda, “Computer Simulation of Branching Pattern and Geometry in Terminalia (Combretaceae), a Tropical Tree,” Botanical Gazette 138 (1977): 377– 84, fig. 7A. Bottom right, permission of PNAS: Hisao Honda and Jack B. Fisher, “Ratio of Tree Branch Length: The Equitable Distribution of Leaf Clusters on Branches,” PNAS 76 (1978): 3875–79, fig. 4A. 7.16 Redrawn from P. B. Tomlinson, “Tree Architecture,” American Scientist 71 (1983): 141–49. 7.17 Left, Pinus pinea L. (Pinaceae), near MPL, March 1977. Right, rainforest canopy, Madagascar, courtesy of Francis Hallé. 7.18 Left, MIA, intersection of State #826 and #836, June 2014. Center, Thrinax excelsa Lodd. ex Mart. (Arecaceae), LM TS, midrib thickness 1.2 mm. Right, Me-

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demia argun (Mart.) H. Wendl. (Arecaceae), LM TS, blade thickness 0.6 mm. Courtesy of Jack Fisher and Barry Tomlinson; see also P. Barry Tomlinson, James Horne, and Jack B. Fisher, The Anatomy of Palms (Oxford: Oxford University Press, 2011). 7.19 Left, Wikimedia. Center and right, Costus scaber Ruiz & Pav. (Costaceae); center, courtesy of Wikimedia; and right, LM TS, ca. 900 μm thick. 7.20 Left, Symphyotrichum lanceolatum (Willd.) G.L.Nesom (Asteraceae), Wikimedia. Center, drawing of two species, fig. 1, B. Schmid and F. A. Bazzaz, “Crown Construction, Leaf Dynamics, and Carbon Gain in Two Perennials with Contrasting Architecture,” EM 64 (1994): 177–203, courtesy of the Ecological Society of America. Right, Solidago Canadensis L. (Asteraceae), Wikimedia. 7.21 Apple orchards. Left, Floyd County, VA, October 2008. Right, Pheasant Orchards, Soap Lake, WA, June 2014.

Chapter Eight: Shapes and Edges

8.1 Volkmar Vareschi, Vegetations-ökologie der Tropen (Stuttgart: Verlag Eugen Ulmer, 1980), fig. 52 (p. 114) and fig. 57 (p. 121), © Eugen Ulmer KG, Stuttgart. 8.2 Information for these diagrams was taken from Elisabetta Di Giacomo, Maria Adelaide Iannelli, and Giovanna Frugis, “TALE and Shape: How to Make a Leaf Different,” Plants 2 (2013): 317– 42; and Daniel Koenig and Neelima Sinha, “Evolution of Leaf Shape: A Pattern Emerges,” Current Topics in Developmental Biology 91 (2010): 169–83. 8.3 From Daniel Buisson and David W. Lee, “The Developmental Responses of Papaya Leaves to Simulated Canopy Shade,” AJB 80 (1993): 947–52. 8.4 Left, Sassafras albidum L. (Lauraceae), Minnewaska State Park, October 2011. Bottom right, Selaginella willdenowii (Desv.) Bak. (Selaginellaceae), FTBG, July 2012, lateral leaves ca. 3.3 mm long. Top right, Ranunculus aquatilis L. (Ranunculaceae), Baca National Wildlife Refuge, CO, September 2015. 8.5 Top left, Ginkgo huttoni (Sternberg) Heer (Ginkgoaceae), Wikipedia. Top center, Ginkgo biloba L. (Ginkgoaceae), Ephrata, WA, June 2011. Right, G. biloba, November 2005. Bottom left, Laccopteris elegans Presl. (Matoniaceae), Wikimedia. Bottom center, Matonia pectinata R. Br. (Matoniaceae), October 2005. 8.6 Top and middle photographs, the Burke Museum of Natural History and Culture, Seattle, WA: www.burkemuseum.org/paleontology/stonerose. Bottom left, Sabal palmetto (Walt.) Lodd ex Schultes (Arecaceae), MIA, January 2014. Bottom right, Sabal campbellii J. S. Newberry, Wikimedia. 8.7 Top left, Quercus aliena Blume, Morris Arboretum, Philadelphia, November 2013. Top right, Q. alba L., Prince William Forest, VA, May 2014. Bottom left, Q. rubra L., Catskills, NY, June 2011. Bottom right, Q.imbricaria Michx., Spring Grove Cemetery, Cincinnati, OH, July 2011. 8.8 Left, Acer saccharum Marshall (Sapindaceae), South Fallsburg, NY, June 2011. Center, A. negundo L., Morris Arboretum, Philadelphia, November 2013. Right, A. laurinum Hassk., Sam Kathern National Park, Thailand.

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8.9 Left, Viola soraria Wild (Violaceae), Horsham, PA, April 2014. Center, V. trinervata (T.J. Howell) T.J. Howell ex Gray, Sagebrush Flats, Grant County, WA, March 2010. Right, V. arborescens L., southern Europe, Wikimedia. 8.10 Left, Pelargonium fulgidum (L.) L’Hér (Geraniaceae). Center, P. laxum G. Don, both collected from South Africa and grown at the University of Connecticut Greenhouses by Cindi Jones, December 2004. Right, Leavenworth, WA, July 2014. 8.11 Left, Posidonia oceanica (L.) Delile (Posidoniaceae); right, Rhyncholacis penicillata Matthiesen (Podostemaceae), Venezuela. Both photographs from Wikimedia. 8.12 Right, Populus tremuloides Michx., Slumgulion Pass, CO, September 2013. 8.13 Left, Gunnera manicata Linden (Gunneraceae), Lyme Regis, UK, April 2015, ~70 cm across. Right, Potentilla chiloensis (L.) Mabb. (Rosaceae), Wikimedia, ~ 5 cm across. 8.14. Left, Viburnum acerifolium L. (Adoxaceae), HF October 2004. Center, V. lantanoides Michx., Catskills, NY, May 2014. Right, V. cassinoides L., HF October 2004. 8.15 Top left, D’Arcy Wentworth Thompson, On Growth and Form (citation in notes, 6.19), see fig. 504, p. 1047; permission of Cambridge University Press. Top center and right, from Przemysław Prusinkiewicz and Aristid Lindenmayer, The Algorithmic Beauty of Plants (New York: Springer Verlag, 1990), both images courtesy of Wikimedia. Bottom left, Lactuca sativa L. (Asteraceae), Norman Brothers Produce, MIA, July 2014; bottom right, Brassica oleracea L. (Brassicaceae), home garden, MIA, March 2015. 8.16 Left, Thompson, On Growth and Form, see fig. 8.15 above, fig. 499, p. 1042, permission of Cambridge University Press. Center, Elatostema rugosum A. Cunn. (Urticaceae), Waitakare Range, New Zealand, June 1998. Right, Begonia pavonina Ridl. (Begoniaceae), Bukit Lanjang F.R., Malaysia, October 2005.

Chapter Nine: Surfaces

9.1 Left, fruit of Glycorrhiza glabra Pursh. (Fabaceae), Crestone, CO, September 2013. 9.2 Left, Redrawn from Smith et al., Plant Biology (see fig. 6.18 above for citation). 9.3 Left, Ficus elastica L. (Moraceae) photographed in MPL, March 1978. Center, Selaginella willdenowii (Desvaux ex Poiret) Baker (Selaginellaceae), photographed at FIU, April 1984. Right, Hoffmania ghiesbreghtii (Lemaire) Hemsley (Rubiaceae), photographed at FIU, April 1984. Distance across images is ~1 mm. 9.4 Left, Gnetum gnemon L. (Gnetaceae), leaf LM TS, height of image ~150 μm. Center, Xyris tortilis Wand. (Xyridaceae). TEM TS, vertical distance 0.9 μm, from Maria das Graças Sajo and Silvia Rodrigues Machado, “Submicroscopical Features of Leaves of Xyris Species,” Brazilian Archives of Biology and Technology 44 (2001): 405–10, fig. 5, permission of first author. Right, Brassica oleracea L. (Brassicaceae), SEM, 12 μm across, permission of Virginia Berg. 9.5 Left, structure of cutin, permission granted by the American Oil Chemists’ Society (AOCS) and the Lipid Library. Right, a wax (cetyl palmitate), courtesy of Wikimedia.

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9.6 Copernicia prunifera (Mill.) H.Moore (Arecaceae), MBC March 2013, pinna width is 4 cm. 9.7 Top left, Tradescantia pallida (Rose) D. Hunt. (Commelinaceae), PD, ~ 800 μm across. Top right, Cycas revoluta Thunb. (Cycadaceae), PD, ~500 μm across. Bottom left, Begonia foliosa Kunth. (Begoniaceae), PD, 1 mm across. Bottom right, fossil cuticle of Dioonopsis macrophylla (Potbury) Erdei (Zamiaceae) from the California Eocene: Boglárka Erdei, Steven R. Manchester, and Zlatko Kvacˇek, “Dioonopsis Horiuchi et Kimura Leaves from the Eocene of Western North America: A Cycad Shared with the Paleogene of Japan.” IJPS 173 (2012): 81–95, permission of Boglárka Erdei. 9.8 Top left, Heritiera littoralis Dryand. (Malvaceae) from FTBG, ~1 mm across. Top right, Pleopeltis polypodioides (L.) E.G.Andrews & Windham (Polypodiaceae), FIU, 700 mm across. Bottom left, Eucalyptus zygophylla Blakely (Myrtaceae), SEM, seen in Gunning, Plant Cell Biology (fig. 2.2 above for full citation). Bottom right, Salvia officinalis L. (Lamiaceae), 2 mm across, Crestone, CO, August 2015. 9.9 Urtica dioica L. (Urticaceae), Wikimedia. 9.10 Left, Verbascum thapsus L. (Scrophulariaceae), Crestone, CO, September 2013, 1.5 m high. Center, 2 mm across. Top right, Leontopodium alpinum Cass. (Asteraceae), courtesy of Wikimedia. Lower right, trichome details, from J. P. Vigneron et al., “Optical Structure and Function of the White Filamentary Hair Covering the Edelweiss Bracts,” PRE 71 (2005): 011906, 1–8, fig. 4, permission of American Physical Society. 9.11 Bedstraw, Galium aparine L. (Rubiaceae). Top right, Bowman Hill Wildflower Preserve, PA, May 2014; top left, courtesy of Thomas Speck and Friederike Gallenmüller. Bottom right, bractless blazing star = Mentzelia inada (Pursh) Torr. & A. Gray (Loasaceae); all from Crestone, CO, August 2015; trichomes are ~0.4 mm long. 9.12 See M. W. Szyndler, K. F. Haynes, M. F. Potter, R. M. Corn. And C. Loudon, “Entrapment of Bed Bugs by Leaf Trichomes Inspires Microfabrication of Biomimetic Surfaces,” JRSI 10 (2013): 20130174. 9.13 Top left and top center, Nelumbo nucifera Gaertn. (Nelumbonaceae), the Kampong, Miami, FL, August 2011. Top right and middle right, SEM. Bottom left and right, Salvinia sp. (Salviniaceae), lower right, SEM. All images courtesy of Wilhelm Barthlott. 9.14 Top left, Nepenthes balcalrata Hook.f. (Nepenthaceae), courtesy of Wikimedia. Top center and right, from Holger F. Bohn and Walter Federle, “Insect Aquaplaning: Nepenthes Pitcher Plants Capture Prey with the Peristome, a Fully Wettable Water-Lubricated Anisotropic Surface,” PNAS 101 (2004): 14138–43, fig. 1A & B, permission of PNAS, dimensions across images from left, 10 cm, 550 µm, and 370 µm. Bottom left, Sarracenia flava L. (Sarraceniaceae), HF, September 2004, trap lip 3 cm wide. Bottom right, FIU, July 2014, distance across = ~5 mm. 9.15 Top left, Gethyllis sp. (Amaryllidaceae), permission of Etwin Aslander. Top right, Dipcadi panousei Sauvage & Veilex (Asparagaceae), photographed in southwest

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Morocco by Annie Garcin, available with permission of Plant Biodiversity of Southwestern Morocco, www.teline.fr. Bottom, Tillandsia landbeckii Philippi (Bromeliaceae), photographs from the Atacama Desert of Chile were provided by Claudio Latorre. 9.16 Scindapsus pictus Hassk. (Araceae). All photographs from MPL, July 1978. Lens diagram is from Richard E. Bone, David W. Lee, and John N. Norman, “Epidermal Cells Functioning as Lenses in Leaves of Tropical Rainforest Shade Plants,” Applied Optics 24 (1985): 1408–12. Leaves are ~7 cm long, epidermal cells ~70 µm in diameter. 9.17 Mapania caudata Kük (Cyperaceae). Left, FIU Wertheim Conservatory, June 2009. Center left, Forest Research Institute of Malaysia, Kepong, November 11, 2005, leaves ~1 cm wide. Center, TEM by Greg Strout, see Greg Strout et al., “Silica Nanoparticles Aid in Structural Leaf Colouration in the Malaysian Tropical Rainforest Understory Herb, Mapania caudate,” AB 112 (2013): 1141–48. Center right, helicoidal diagram from David Lee, Nature’s Palette (Chicago: University of Chicago Press, 2007), fig. 10.6. Right, Scott Russell, from Mapania article. 9.18 Begonia maculata Raddi (Begoniaceae). Left, courtesy of Scott Zona. Center left, 1.5 cm across. Center right, LM TS, leaf ~400 μm thick. Right, leaf surface, image 1 mm across, FIU, February 2007.

Chapter Ten: Veins

10.1 Top left, NASA Landsat. Top right, Beta vulgaris subsp. Cicla (L.) W.D.J. Koch, image 5 cm across, MIA, July 2013. Bottom left, see J. Taylor Perron, James W. Kirchner, and William E. Dietrich, “Formation of Evenly Spaced Ridges and Valleys,” Nature 460 (2009): 502–4. Bottom right, Coccoloba rugosa desf. (Polygonaceae), Gifford Arboretum, UM, July 2013, 7 cm across image. 10.2 Left, Adiantum formosum R. Br. (Pteridaceae), FTBG, February 2013, image 15 mm across. Right, Passiflora coccinea Aubl. (Passifloraceae), Kampong, MIA, April 2012, 10 mm across. 10.3 Terminalia catappa L. (Combretaceae). Left, senescent leaf detail, MIA, January 2014, 3.5 cm across. Center, LM TS, FIU, April 1984, leaf thickness 280 μm. Right, LM, longitudinal section of vein, FIU, June 2014, image 300 μm across. 10.4 Permission of Gray Herbarium Library, Harvard University. 10.5 Acer saccharum L. (Sapindaceae). Left, photographed October 2012. Right, HF, October 2004. 10.6 Left, August 1979. Top and bottom right, courtesy of George Koch. 10.7 Elaeis guineensis Jacq. (Arecaceae), cleared PD leaf section, image width 9 mm. 10.8 Acer rubrum L. (Sapindaceae), images were scanned at high resolution in a flatbed scanner, August 2013. 10.9 Ficus religiosa L. (Moraceae), leaf skeletonized in India. Leaf blade 8 cm long, detail 1 cm wide. 10.10 Redrawn from Benoit B. Mandelbrot, The Fractal Geometry of Nature (San Francisco: W. H. Freeman, 1982), Pl. 164.

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Chapter Eleven: Color

11.1 Left, April 2010. Top right, Amelanchier arborea (F. Michx.) Fernald (Rosaceae). Middle right, Acer rubrum L. (Sapindaceae). Bottom right, Fagus grandifolia Ehrh. (Fagaceae). Plants were photographed at Pennypack Creek, PA, April 2014. 11.2 Left, Caladium bicolor Vent. (Araceae), FTBG, March 2014. Right, Episcea cupreata (Hook.) Hanst. (Gesneriaceae), FTBG, February 2011. 11.3 Left, Fagus sylvatica L. (Fagaceae), Wikimedia. Right, Acer palmatum Thunb. (Sapindaceae), Ephrata, WA, August 2001. 11.4 All photographs taken at Waterrock Knob, NC, October 2012. Top right, Oxydendrum arboretum (L.) DC (Ericaceae); bottom right, Quercus palustris Muenchh. (Fagaceae). 11.5 Left, Mesua ferrea L. (Clusiaceae), MIA, February 2004. Right, Elaeocarpus angustifolius Blume (Elaeocarpaceae), FTBG, September 2010. 11.6 Left, Breynia disticha Forst. & Forst. F. (Euphorbiaceae), the Kampong, MIA, June 2013. 11.7 Codaieum variegatum (L.) Blume (Euphorbiaceae), MIA, January 2011. 11.8 All diagrams and structures from David Lee, Nature’s Palette: The Science of Plant Color (Chicago: University of Chicago Press, 2007), figs. 3.3, 3.8, 3.16. 11.9 Pseuderanthemum carruthersii (Seem.) Guillaumin var. atropurpurea Fosberg (Acanthaceae), FTBG, February 2013. 11.10 Philodendron scandens (Schott) G.S.Bunting var. oxycardium Schott. (Araceae). Top left, MIA, January 2015. Bottom left, Fuchsia sp. (Loganiaceae), courtesy Brian Gunning, see fig. 2.2 above. Right, Barro Colorado Island, Panama, May 1987.

Chapter Twelve: Food

12.2 Both photos from FIU, April 2014. Left, Ficus microcarpa L.f. (Moraceae). Right, Boswellia sacra Flueckiger (Burseraceae). 12.3 Le Radeau des Cimes expedition, the Forest of the Bees, central Gabon, February 1999. For more information: http://www.radeau-des-cimes.org/. 12.4 Top left, Wikimedia. Top right, leaf margin, image ~4 mm across, FIU, April 2014. Bottom left, photographed by Daniel Schwen, Urbana, IL, September 2010. Bottom right, photographed by Max Wahrnhaftig, December 2005; both photographs courtesy of Wikimedia. 12.5 Wikimedia. 12.6 Top left, Vachellia cornigera (L.) Seigler & Ebinger (Fabaceae), permission of Judy Gallagher. Bottom left, Inga sp. (Fabaceae), Gamboa, Panama; see www .alexanderwild.com/Ants/Taxonomic-List-of-Ant-Genera/Ectatomma/i-kzg qnXr. Right, Barteria fistulosa (Passifloraceae), Forest of the Bees, central Gabon, February 1999. 12.7 Left, photographed April 1977; right, photographed April 1988.

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Chapter Thirteen: Homes

13.1 This bird’s nest play area is part of the children’s garden at the Morris Arboretum, in Philadelphia, October 2013. 13.2 Left, photographed by Kathelijne Koops, at Bousou, Guinea, West Africa, July 2006. Right, Near village of Gayagota, Thane District, Maharashtra, India, July 1984. 13.3 Left, Ulu Kenaboi, West Malaysia, April 1975. Right, Gayagota village, Thane District, Maharashtra, April 1984. 13.4 Wikimedia. 13.5 Both photos from Tasik Bera, West Malaysia, November 2005. 13.6 Neoregelia carolinae (Beer) L.B. Smith (Bromeliaceae), FTBG, February 2006. 13.7 Left, near Saül, January 1978. Right, Berthusen Memorial Park, Lynwood, WA, March 2014. 13.8 Left, galls are about 3 mm in diameter on this oak leaf, courtesy of BeenTree, Wikimedia. Right, courtesy of Jorge Pena and Rita Duncan. 13.9 Top left and center, Persea Americana Mill. (Lauraceae), MIA, July 2014. Top right, Coprosma repens A. Rich. (Rubiaceae), SEM. Bottom left, Schinus terebinthifolius Raddi (Anacardiaceae), 2.5 cm across image. Bottom right, SEM. 13.10 Left, Dischidia astephana Scort. ex King & Gamble (Apocynaceae), Gunung Ulu Kali October 2005, image 6 cm across. Center and right, Dischidia major (Vahl) Merr. (Apocynaceae). 13.11 Tococa guianensis Aubl. (Melastomataceae), Bocos del Toro, Panama, June 2003. 13.12 Hirtella physophora Mart. & Zucc. (Chysobalanaceae).

Chapter Fourteen: Movements

14.1 Codariocalys motorius (Houtt.) H. Ohashi (Fabaceae), XTBG, Menglun Township, Mengla County, Yunnan Province, October 2005. 14.2 Left, Robert Hooke, Micrographia (London: James Allefry, 1665), fig. 2, p. 114. Center, engraving, 1779, Wikimedia. Right, illustration from Charles Bonnet, J. Wandelaar, and J. V. D. Schley, Recherches sur l’usage des feuilles dan les plantes (Göttingen: E. Luzac, 1754). 14.3 All images from Wikimedia. 14.4 Left, Wikimedia. Right, Jagadish Chunder Bose, The Nervous Mechanism of Plants (London: Longmans, Green & Co., 1926), fig. 16, p. 58. 14.5 Left, permission of Lisa Sells, http://www.zenthroughalens.com/2012/01/aphis -nerii-and-i.html. Center, adapted from diagram by Freddy Tjallingii, EPG Systems, www.epgsystems.eu. Right, LM TS, Jennifer Richards and Rita Graham. 14.6 Leucaena leucocephala (Lam.) de Wit (Fabaceae), MIA, October 2013. 14.7 Wikimedia. 14.8 Top left, Utricularia foliosa L. (Lentibulariaceae), Everglades National Park, FL, July 1997. Top right, U. foliosa traps, ENP, courtesy of Jennifer Richards. Bottom left, Aldrovanda vesiculosa L. (Droseraceae), Wikimedia. 14.9 Top left, Drosera rotundifolia L. (Droseraceae) Jardin Têt d’Or, Lyon, France, No-

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vember 1977. Top right, D. rotundifolia, Bay of Fundy National Park, Canada, July 1972. Bottom, Drosera filiformis Raf.: left, Sunbelle Exotics, Boca Raton, FL, October 2013; center, leaf detail, FIU, November 2013; right, trichome detail, FIU, November 2013. 14.10 Dionaea muscipula Sol. ex J. Ellis (Droseraceae). Top left, Jardin Têt d’Or, Lyon, France, November 1977. Top right, Sunbelle Exotics, Boca Raton, FL, October 2013. Bottom left, Wikimedia. Bottom right, FIU, October 2013. 14.11 Plumbago zeylanica L. (Plumbaginaceae), MIA, October 2013, hairs ~1 mm long.

Chapter Fifteen: Seeing Leaves

15.1 Left, MIA, October 2001. Right, now Pinecrest Gardens, MIA, June 2013. 15.2 Left, McNeil Island Historical Society, www.mcneilisland.net. Right, Al Black mural appeared in Gary Monroe, The Highwayman Murals: Al Black’s Concrete Dreams (Gainesville: University Press of Florida, 2009). 15.3 Permission of Nalini Nadkarni. 15.4 Figure in J. V. Haxby, M. I. Gobbini, M. L. Furey, A. Ishai, J. L. Schouten, and P. Pietrini, “Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex,” Science 293 (2001): 2425–30. 15.5 Left, Ulu Kenaboi, West Malaysia, April 1975. Right, at the base of Mondagni Peak, Tansa Valley, April 1985. 15.6 Left, Alpine Lakes Wilderness Area, August 2008. Right, Shaun Lee, August 2007. 15.7 Permission of reSTART. See their website at www.netaddictionrecovery.com/. 15.8 Permission of New York Botanical Garden, taken at the garden for Patrick’s green wall designs for their annual orchid show, photo by Ivo M. Vermeulen in 2012. 15.9 Permission of Francis Hallé. 15.10 Permission by Julie Hedrick, http://juliehedrick.com/. Into the Forest, 2011, oil on canvas, 206 × 255 cm. See her work at Nora Haime Gallery, www .nohrahaimegallery.com. 15.11 Pink Flowers, cibachrome, 30 × 40 inches, 2001. Taken in parents’ backyard (see p. 307), permission of the artist.

Appendix A: Leaf Terminology

A.1 Celtis laevigata Willd. (Ulmaceae), UM, February 2003. A.2 Top left, Echinocereus viridiflorus Engelm. (Cactaceae), Tohono Chul Gardens, Tucson, AZ, March 2013. Top right, Sarracenia purpurea L. (Sarraceniaceae), HF, October 2004. Bottom left, Dolichandra unguis-cati (L.) L. Lohmann (Bignoniaceae), MIA, January 2014. Bottom right, Allium sativum L. (Alliaceae), MIA, January 2014. A.3 Top left, Quercus virginiana L. (Fagaceae), MIA, February 2009. Top center, Cordyline fruticosa (L.) Goeppert (Asparagaceae), MIA, April 2011. Top right, Cocos nucifera L. (Arecaceae), MIA, January 2014. Bottom left, Licuala grandis H. Wendl. (Areca-

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ceae), MIA, January 2014. Bottom center, Caryota mitis Lour. (Arecaceae), FTBG, January 2014. Bottom right, Sabal palmetto (Walt.) Lodd. ex Schultes (Arecaceae), MIA, January 2014. A.4 Left, Ravenala madagascariensis Sonn. (Strelitziaceae), MIA, January 2014. Left center, Casuarina equisetifolia L. ex J.R. & G. Forst. (Casuarinaceae), MIA, August 2010. Right center, Platycladus orientalis (L.) Franco (Cupressaceae), MIA, February 2003. Right, Pinus elliotii Engelm. (Pinaceae), FIU, January 2003. A.5 Left, Acer rubrum L. (Sapindaceae), HF, September 2004. Center, Euphorbia punicea Swartz. (Euphorbiaceae), FTBG, January 2014. Right, Nelumbo nucifera L. (Nelumbonaceae), Zoo Miami, FL, July 2012. A.6 Top left, Fagus grandifolia L. (Fagaceae) Minnewaska State Park, NY, June 2011. Top center, Coffea Arabica L. (Rubiaceae), FTBG, January 2014. Top right, Nerium oleander L. (Apocynaceae), FIU, February 2014. Bottom left, Lagerstroemia indica L. (Lythraceae), MIA, January 2014. Bottom right, Manilkara zapota (L.) P. Royen (Sapotaceae), FTBG, January 2014. A.7 Top left, Tilia Americana L. (Malvaceae), Spring Grove Cemetery, Cincinnati, OH, July 2011. Top center, Juglans nigra L. (Juglandaceae), Cincinnati, OH, July 2011. Top right, Schinus terebinthifolius Raddi. (Anacardiaceae), MIA, January 2014. Bottom left, Bulnesia arborea (Jacq.) Engl. (Zygophyllaceae), FTBG, January 2014. Bottom right, Aesculus glabra Willd. (Sapindaceae), Spring Grove Cemetery, Cincinnati, OH, July 2011. A.8 Left, Peltophorum pterocarpum (DC) K. Heyne (Fabaceae), MIA, January 2014. Right, Amorphophallus paeonifolius (Dennst.) Nicolson (Araceae), MIA, June 2014. A.9 Top left, Bucida buceras L. (Combretaceae), MIA, June 2002. Top right, Thevetia peruviana (Pers.) Schumann (Apocynaceae), Bocos Del Toro, Panama, June 2003. Bottom left, Mangifera indica L. (Apocynaceae), MIA, June 2002. Bottom center, Cinnamomum zeylanicum L. (Lauraceae), FIU, June 2003. Bottom right, Rhus toxidodendron L. (Anacardiaceae), MIA, March 2003. A.10 Left, Trema micranthum (L.) Blume (Ulmaceae), FIU, August 2003. Right, Begonia egregia N. E. Britt. (Begoniaceae), FTBG, February 2013. A.11 Left, Carica papaya L. (Caricaceae), MIA, January 2014. Center, Quercus alba L. (Fagaceae), Prince William Forest, VA, May 2014. Right, Bauhinia purpurea L. (Fabaceae), MIA, January 2014. A.12 Left, Liquidambar styraciflua L. (Hamamelidaceae), Cape May, NJ, June 2011. Right, Sassafras albidum (Nutt.) Nees (Lauraceae), Minnewaska State Park, NY, June 2011. A.13 Top left, Crossopetalum ilicifolium (Poir.) Kuntze (Celastraceae), MIA, March 2005. Top center, Achmea sp. (Bromeliaceae), FTBG, January 2014. Top right, Alnus rubra Bong. (Betulaceae), Whatcom County, WA, August 2007. Bottom left, Ricinus communis L. (Euphorbiaceae), FIU, February 2013. Bottom center, Quercus prinus L. (Fagaceae), Minnewaska State Park, NY, June 2011. Bottom right, Hydrocotyle umbellata L. (Apiaceae), MIA, February 2013.

· 441 ·

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A.14 Left, Cocculus laurifolius DC (Menispermaceae), UM, August 2002. Center, Pimenta dioica (L.) Merr. (Myrtaceae), FTBG, January 2014. Right, Mimusops elengii L. (Sapotaceae), FTBG, September 2002. A.15 Top left, Eugenia foetida Pers. (Myrtaceae), MIA, June 2004. Top center, Ficus religiosa L. (Moraceae), MIA, April 2006. Top right, Agave sp. (Agavaceae), FTBG, January 2014. Bottom left, Tectona grandis L. (Verbenaceae), FIU, June 2005. Bottom center, Noronhia emarginata Stadtm. (Oleaceae), MIA, September 2003. Bottom right, Liriodendron tulipifera L. (Magnoliaceae) New Paltz, NY, June 2011. A.16 Top left, Hypelate trifoliata Sw. (Sapindaceae), FTBG, August 2003. Top center, Mammea americana L. (Clusiaceae), FTBG, May 2005. Top right, Callicarpa americana L. (Verbenaceae), FTBG, August 2003. Bottom left, Dombeya wallichii (Lindl.) Benth. (Malvaceae), FTBG, January 2014. Bottom center, Populus tremuloides Michaux (Betulaceae), Crestone, CO, October 2014. Bottom right, Sagittaria montevidensis Cham. & Schltdl. (Alismataceae), FTBG, February 2010. A.17 Top left, Clusia rosea L. (Clusiaceae), FIU, June 2002. Top center, Guettarda scabra (L.) Vent. (Rubiaceae), FTBG, April 2005. Top right, Hoffmannia ghiesbreghtii (Lem.) Hemsl. (Rubiaceae), FTBG, March 2004. Bottom left, Psychotria punctata Vatke (Rubiaceae), FTBG, October 2003. Bottom center, Oplopanax horridus (Sm.) Miq. (Araliaceae), Whatcom County, WA, September 2011. Bottom right, Artemisia tridentata Nutt. (Asteraceae), Ephrata, WA, August 2011. A.18 Top left, Urtica dioica L. (Urticaceae), Whatcom County, WA, June 2010. Top right, Avicennia germinans (L.) L. (Verbenaceae), FTBG, May 2004. Bottom left, Suriana maritima L. (Surianaceae), FTBG, January 2003. Bottom right, Iris sp. (Iridaceae), MIA, February 2008. A.19 Top left, Ficus aurea Nutt. (Moraceae), MIA, January 2014. Top center, Ficus citrifolia Mill. (Moraceae), MIA, July 1988. Top right, Laguncularia racemosa (L.) Gaertn. f. (Combretaceae), MIA, January 2014. Bottom left, Delonix regia (Boj. ex Hook.) Raf. (Fabaceae), MIA, January 2014. Bottom right, Wodyetia bifurcata Irvine (Arecaceae), MIA, January 2014. A.20 Top left, Acacia koa A. Gray (Fabaceae), Kauai, HI, February 2008. Top right, Citrus aurantiifolia (Christm.) Swingle (Rutaceae), MIA, March 2003. Bottom from left to right: Anthurium sp. (Araceae); Licuala grandis H. Wendl (Arecaceae); Curcuma zedoaria (Christm.) Roscoe (Zingiberaceae); Filicium decipiens (Wight. & Arn.) Thw. (Sapindaceae); Thunbergia grandiflora (Rottler) Roxb. (Verbenaceae); Zamia furfuracea L. f. (Zamiaceae). Photographed MIA, May 2014. A.21 Top left, Ficus elastica L. (Moraceae), MIA, July 2002. Top right, Morinda citrifolia L. (Rubiaceae), FTBG, January 2014. Bottom left, Vachellia cornigera (L.) Seigler & Ebinger (Fabaceae), FTBG, May 2006. Bottom right, Smilax rotundifolia L. (Smilacaceae), MIA, Tropical Park Pinelands Preserve, March 2014. A.22 Top left, Artocarpus altilis (Parkinson) Fosb. (Moraceae), Bocos Del Toro, Panama, June 2003. Top center left, Cnidosculus chayamansa McVaugh (Euphorbiaceae), MIA, August 2002. Top center right, Adiantum capillus-veneris L.; (Pteridaceae), FIU, Jan-

I L L U S T R AT I O N N O T E S

· 442 ·

uary 2014. Bottom left, Tibouchina urvilleana Cogn. (Melastomataceae), FIU, July 2003. Bottom center, Bauhinia purpurea L. (Fabaceae), MIA, January 2014. Bottom right, Ficus religiosa L. (Moraceae), MIA, January 2014. A.23 Left, Gigantochloa atroviolacea Widjaja (Poaceae), MIA, April 2005. Left center, Anthurium warocqueanum J. Moore (Araceae), FTBG, February 2013. Right center, Maianthemum canadense Desf. (Asparagaceae), Hurleyville, NY, May 2009. Right, Musa acuminata Colla (Musaceae), FTBG, January 2014.

inde x Note: Page numbers in italics indicate a figure. ABC model, 128–29, 129 Abram, David: The Spell of the Sensuous, 298 abscisic acid (ABA), 132, 186 abscission zone, 34 acacia, 244; bull thorn, 247 acanthus, shrub, 6, 7 action potential, 274 Adams, John, 48 Addams Family, The, 271 adenosine triphosphate (ATP), 55, 57, 95, 205 ADHD, 289 adultery tree and ant, 247 aflatoxin, 238 aging, 228 air, “fixed,” 47–48; plant, 188, 199 Alexander the Great, 11, 12; soldiers, 189 algae, 27, 39; brown, 24; green, 27, 41, 47; red, 24 alkaloids, 239 Al-Khidr, 8, 12 all is leaf, 127–28 all is number, 108 Alpine Lakes Wilderness, Cascades, Washington, 287, 301 Alstroemeria, 126 Altai Mountains, 6 Alzheimer’s, 289 amaranth, 225 Amborella trichopoda, 128, 130 Amorphophallus, 153 amylose, 58 Anderson, Jan, 57 · 443 ·

Anderson, William, 1 angiogenesis, 203 angiosperms, 34 anthocyanins, 222, 224 anthropic principle, 22 ants, weaver, 256; attine, 266; and plants, 247 aphid, stylid, 275–76, 276 Appalachians, autumn foliage, 220 apple orchard, architecture, 156 aquaporins, 279 aquifer, 79 Arabidopsis (A. thaliana), 117, 128–29, 129; leaf rosettes, 153; vein development, 203 Archaeobacteria, 25 Archeopteris, 32 Archetti, Marco, 229 archetypes, 297–98 architectural models, 140–46; Aubréville, 143, 145, 148, 150; Corner, 144; Holttum, 144; Leeuwenberg, 142; quantitative, 148; Rauh, 142, 145; Troll, 145 architecture, etymology, 134 Arcimboldo, Giuseppe, 20 Aristotle, 12, 44, 108 aroid, form, 15 Arrhenius, Svante, 82 Art Basel, Miami, 305–6 Arthur, King, 3 Asia, central, 6 Aspects of Nature (Humboldt), 15

INDEX

· 444 ·

assimilation, 50 aster, panicled, 155–56, 156 asteroid, impact, 34 Atacama Desert, Chile, 196 Australia, Western, 23; mountain gum, 209 autotrophic, 38 auxin, 132, 161, 185, 202, 282 ayahuasca, 239 bacteria, 24; denitrifying, 81; purple sulfur, 23, 225 bacteriochlorophyll, 225 Bailey, Irving, 169 bamboo, 9; form, 15 banana, 12; form, 15 banyan, 7, 12; latex, 240 Baragwanathia, 30, 30–31 Barbieri, Alejandro, 119 barley, 6 Barnes, Charles, 50 Bartram, William and John, 271 Bassham, James, 55 bat: flying fox, 255; Honduran white fruit, 255; Spix’s disk-winged, 255 Bates, Marston; The Forest and the Sea, 17 Bazile, Vincent, 266 beam (engineering), 153, 157 bean, common: hooked trichomes, 192 bedbugs, 191–92, 192 bedstraw, surface hooks, 190–91, 191 beech: American, 142, 147; buds, 218; European, 220; Stonerose, 166 Bejan, Adrian, 213 Beltian body, 247 Benson, Andrew, 55 Berry, Wendell, 66 betalains, 223 bidi (cigarette), 105 biodiversity, collapse, 287 bioinspiration, 63, 180, 284 biomechanics, 152 biomes, 72 biomimicry, 63, 180, 190–95

biophilia, 294, 299 biosphere, 76 Birmingham, UK, 46 Black, Joseph, 46 Black, Sharon, 107 Blackman, Frederick Frost, 53 Blanc, Patrick: vegetable walls, 303–4, 304 blueberries, 228 Bluetooth, Harald, 3 bodhi, tree, 7 Bohm, David, 131 Bohn, Holger, 195 Bonnet, Charles, 46, 270–71, 271; Recherches sur l’usage des feuilles dans les plants, 46, 271 Bonpland, Aimé, 12, 14, 77 boreal forest, 74 Bose, Jagadish Chandra, 274–75, 275 Boston Marathon, 6 boundary layer, 103, 169, 171, 173 Boussingault, Jean-Baptiste, 77 Box, Eugene, 70 box elder, 168 Boyce, Kevin, 208 bractless blazing star, 191 brain: evolution, 294; “reptilian,” 294 branching: capture efficiency, 149; dichotomous, 143; monopodial, 142, 145; sympodial, 143, 145 bridge (engineering), 154 Broadribb, Tim, 208 Brocchinia reducta, 258 bromeliad, tank, 257 broome bloodwood, stellate hairs, 187 bryophytes, 28 Buddha, 7 Buisson, Daniel, 162 Buitenzorg (Bogor), Java, 50, 69 buttercup, aquatic, 164 cabbage leaf, epicuticular wax, 183 cacti, 223 caffeine, 95, 96, 239

· 445 ·

caladium, variegation, 228 Callebaut, Vincent, 137 Calvin, Melvin, 55 camouflage, 238; color, 227 cancer, colon, 238 canopy raft expedition, Gabon, 241 Canterbury Quadrangle, 1, 2 cantilevers (engineering), 153 carbon, 82; cycle, 82 carbon dioxide, 23, 29, 75, 86; concentrations, 85 cardiotonic glycosides, 239 carotene, 237 carotenoids, 222, 224 catchments, 80 cat’s claw vine, 122 Catskill Mountains, 218 Caucasus, 6 cauliflower, 151 Cavender-Bares, Jeanine, 208 Caventou, Joseph Bienaimé, 50 cavitation, 206, 209 cecropia, 266 cell, pressure (turgor), 154, 277; eukaryotic, 24; expansion, 181; guard, 181; lens-shaped, 183; theory, 114; walls, 38, 181 cellulose, 58, 59, 181; wall growth, 181 Celt, 4, 6, 7 Center for Tropical Forest Science (CTFS), 100 chard, Swiss, 237 chemiosmotic theory, 57 chemistry, origin, 46; pneumatic, 45 cherry, tree, 135 chicle, tree, 150 Children in Nature Network, 291 Chimborazo, Mount, Ecuador, 14, 68; vegetation, 87 Chisocheton, 120 chlorophyll, 50, 67; a and b, 222, 224; structure, 51 chloroplast, 24, 26, 50; grana, 57; stroma, 57; thylakoid, 52; ultrastructure, 52

INDEX

Christian, 7, 12; era, 10 Christmas wreath, 20 Church, Frederic: The Heart of the Andes, 16 circadian rhythms, 278 circular polarization, 197–98, 198 circulation, blood, 200 citron, 8 citrus leaf miner, 260 cladoxylid, tree, 32 climate change, 287 clover, three-leaved, 7 cloves, 12 coastal redwood, California, 206, 210 cocaine, 239 Coen, Enrico, 128–29 coffee, leaves, 95–96, 96 Cole, Thomas, 16 Coleridge, Samuel, 90 Colorado beetle, 242 colors, primary, 221; aposematic, 227; autumn, temperate forest, 229, 233; emotional effect, 295; interactions, 222; subtractive, 221 Columbia Plateau, 73 columns (engineering), 153 Concord, MA, 71 conifer, needles and scales, 201; forest, 73 Conrad, Joseph: Lord Jim, 17 consciousness, 292; and nature, 296– 300 Cooksonia, 29 copperleaf, mutant, 116 corals, 40; architecture, 145; bleaching, 39 Corinthian column, 7 Corner, E. J. H., 140; Corner’s rule, 103 cortisol, 293 Costus scaber, 154 cotton, 12 cotyledons, 111 Couder, Yves, 125 Cruikshank, William, 49 cryptochrome, 278 Crystal Palace, 17, 137 curly-whirlies, Namibia, 196

INDEX

· 446 ·

cuticle, 34, 183–85, 169 cutin, structure, 184 cyanidin-3-glucoside (C3G), 228 cyanobacteria, 24, 27, 37, 39 cyanogenic glucosides, 239 cytoskeleton, 182 Darwin, Charles, 17, 23, 64, 92, 124, 273, 273–74, 278, 280; expression of emotions, 296; and Wallace, 160 Darwin, Erasmus, 21, 46, 49 Darwin, Francis, 124, 270, 273 Daumal, Rene: Mount Analogue, 267–68 DeFanti, Tom, 303 deforestation: Malaysia and Indonesia, 84; oil palm plantation, 84 Delaware Valley, 218 desert: cold desert, 73; Great Basin, 73; hot desert, 72; South Africa, 64 design and artifice, 302 dessicationists, 77 diatoms, 26 Dickey, James, 251 Diffloth, Gérard, 9 digestive glands and enzymes, 280–85 digestive tract, 36 digital technology, screens, 302 dinner plate plant, 124 dinoflagellates, 39 Dioum, Baba, xii, 287 Di Piero, W. S., 200 Dischidia: D. major, 264; D. nummularifolia, 264 Dixon, Henry Horatio, 205 Dobzhansky, Theodosius, 21 dogwood, red-osier, 147 domatia, 261–66; ants, 263–66; avocado, mite, 262; Brazilian pepper, mite, 262; coastal coprosma, mite, 262; Dischidia, 263–64; Hirtella physophora, 266; Macaranga, 266; mites 261–62; Tococa guianensis (Melastomataceae), 265 Douady, Stéphane, 125 Downun, Kelsey, 241 Drosera (sundews), 280

Droseraceae, 284 druid, 4 duckweed, 102 durian, 234, 299 Eagle and Child Pub, 2, 231 East India Company (EIC), 76 ebony, 12 ecology, deep, 288, 297; etymology, 91 economics, etymology, 91 edelweiss, 189–90; Edelweiss Pirates, 190; UV-reflectance, 195 Edwards, Erika, 173 Egyptians, 44 Einstein, Albert, 64 electricity, 46 electrodes, 274 electroencephalography (EEG), 293 elements (earth, water, air, fire, ether), 44 elm, 135 Eloy, Christophe, 156 embryo, 111 emergence, 22, 300 Emerson, Robert, 54 endosymbiosis, 24, 25, 52 Engelmann, Theodor Wilhelm, 52 English, Middle, 10 Enrique, Klaus, 20 ents, 9, 42 epidermis, 34, 181; surface, 182 epiphylls, 258–59, 259 espalier, 156 esthetics and beauty, 306 ethylene, 132, 245–46 evapotranspiration (ET), 79 Everglades National Park, 301 evolution and development (evo-devo), 119 evolutionary psychology, 294, 297 Ewers, Frank, 208 extinction, 85 facial recognition, 295 fakery, 301

· 447 ·

Fan, Tongxiang, 63 Federle, Walter, 195 Feild, Taylor, 208, 230 fern, arborescent form, 15; filmy, 101; water, 102 Fertile Crescent, 8 Fibonacci series, 125 fir, Stonerose, 166 Fisher, Jack, 148, 150 Fisher, Naomi, 306–7, 307 fitness, 150 Flagler, Henry, 18 flatulence, 85 flavonoids, 239 Florida International University, 288 flow system, 213–14 fluctuating asymmetry, 163 fluid dynamics, 169 foraminifera, 39 forcing, 75 Foreigner’s Laboratory, Buitenzorg, 50, 160 forest bathing (shinrin-yoku), 293 Forster, Georg, 15, 68 Fountain of Youth, 12, 18 fractals, 176 frangipani, 144 frankincense, resin, 240 Franklin, Benjamin, 46 Fraxinus, 6 Frazer, Sir James: The Golden Bough, 4 freckle pelt lichen, 38 Freud, Sigmund, 298 Friedrich, Paul, 5 fructose, 58 functional magnetic resonance (fMRI), 293–94, 294 functional types, plant, 71 fungi, 29 Gaia, 88 galls, dyes, 261 Gandalf, 9 gardens: Buitenzorg, 50, 160; Calcutta,

INDEX

11; Chatsworth, 136; Fairchild Tropical Botanic Garden, Miami, 288; Garden of Eden, 10, 18; Garden of Paradise, 10, 12; Padua, 11; Pamplemousse, 11; Peradeniya, 11 garrigue, 250 gases, greenhouse, 75, 81, 85 Gaudí, Antoni, 138–39, 139, Sagrada Familia and Park Güell, 138 Gede, volcano, Java, 160 genes, developmental: AN3, 118; ANT, 118, 119; ARP, 119; ASSYMETRIC LEAVES1, 118; CUC2, 161; KANADI, 118, 119, 129; KNOX, 119; KNOX1, 118, 161; LFY, 161; MIXTA, 183; PIN, 161, 202; RAB, 119; SPCH, 185; YABBY, 118, 119, 129 Genesis, book of, 10 geography, plant, 68 geraniol, 167 geranium (Pelargonium), 167, 172 germen, 111 Gilgamesh, Epic of, 3, 8 Ginkgo, 164–65; 165; at Stonerose, 166 Gioia, Dana, ix Givnish, Tom, 90, 101, 171, 174 global warming and autumn colors, 232 Glossopteris, Antarctica, 86 glucose, 55, 58; as currency, 94 Gnetum gnemon, epidermal cells, 183 Goethe, Johann Wolfgang von, 11, 14, 107, 127; The Metamorphosis of Plants, 127, 130 golden angle, ratio and mean, 125 goldenrod, Canada, 155–56, 156 Gombak, West Malaysia, 70, 80, 83 Goodall, Jane, 290 great apes, nests, 252–53 Great Chain of Being, 274 Greeks, 6, 44, 45 Green Knight, 4 Grew, Nehemiah, 50, 91, 109, 203; leaf geometry, 175

INDEX

· 448 ·

ground pine, 31, 201 Gundestrup Cauldron, 2, 2–3 Gunnera, 81, 173, 175 Haas, Philip, 19 Haberlandt, Gottlieb: Physiological Plant Anatomy, 160 Haeckel, Ernst, 91 Hales, Stephen, 43, 45, 64; Vegetable Staticks, 43 Hallé, Francis, 40, 42, 140, 241; Il était une forét, 304–5, 305 Hamilton, William, 229 Hangartner, Roger, 273 Harvard Forest, 90, 162, 207 Harvey, William, 45, 23, 203; circulation, 110 Hass, Robert, 21 Hatra, Temple of, 3 Heade, Martin Johnson, 16 Hedrick, Julie, 306 Helmont, Jan Baptista van, 45, 79 hermetic, 108 heteroblasty, 122, 162 heterotrophic, 38 hex-vic, 246 Himalayas, 7 Hindu, 7 histamine, 189 hobblebush, 174 Hoch, William, 230 Hoffmania, surface, 182 Hofmeister, Wilhelm, 124 Holbrook, Missy, 208, 230 holly, 6; wild, 105 Holopainen, Jarmo, 232 hominines, 236 Honda, Hisao, 149, 150 Hooke, Robert, 109, 270 Hooker, Joseph, 273 Horn, Henry: Adaptive Geometry of Trees, 146–48, 172 hornworms, 242–43, 243 Horton, Robert, 212

Houton, Wouter van, 244 Hoyle, Sir Fred, 177 Hubble, Edwin, 22 Hudson, W. H.: Green Mansions, 17 Humboldt, Friedrich Wilhelm Heinrich Alexander von, 1, 12, 14, 17, 64, 72, 77, 88: charismatic leaves, 172; Cosmos, 15; forms of vegetation, 19; functional types, 68; and Goethe, 128; tropical nature, 287; Venezuela, 159 humidity: absolute, 78; relative, 78 Hunter, Michael, 293 Hurricane Andrew, 289 Huwawa (Humbaba), 3 hydathodes, 173 hydraulic lift, 209 hydrogen, ions, 57 hydrogen sulfide, 86 hygrometer, 79 Igorot, 18 immunity, 241 India, 44 Indian almond, 143, 148 Indian cucumber, 146 Indian rubber tree, surface, 182 Indo-Aryans, 7 Indo-European Language, 5; tree, 5, 25 infrared radiation (heat), 171 Inga nectaries and ants, 247 Ingen-Housz, Jan, 48 intelligent design, 64, 248 interactions, plant-animal, 240 interactome, 59 interference, 197 Irish, old, 7 ironwood, young foliage, 221 irritability, 271 Islam, 8, 10, 12 isoprene, 86 jackfruit, 12 Jackson, Peter, 9 Jacquet, Luc, 304–5, 305

· 449 ·

Jain, 7 Janzen, Daniel, 247 jasmonic acid, 244, 279, 282 Jefferson, Thomas, 48 Jewish, 8 Johannesteijsmania altifrons, 254 Johnson, Lyndon, 82 Jolly Green Giant, 20 Joly, John, 205 Jones, Owen: The Grammar of Ornament, 136–37 juneberry, 218 Jung, Carl, 289–90, 298 Kahn, Peter, 302 kale, 104; leaf margin, 176; ornamental, 124 Kamen, Martin, 54 Keeling, Charles David: CO2 curve, 83– 84, 84 Keillor, Garrison, 20 Kemp, Edward, 49 Kenworthy, J. B., 79 Kermit the Frog, 20 kilocalorie, 36 Kinabalu, Mount (Borneo), 274 Koch, George, 210 Koch, Norma, 19 Koptur, Suzanne, 247–48 Krieger, Martin: What’s Wrong with Plastic Trees, 302 kudu, lesser, 244 Laibach, Friedrich, 117 Large Hadron Collider (LHC), 100 latex and resin, 239–40 Laud, William, 2 laurel, 6 lavender, 73 Lavoisier, Antoine: Traité elémentaire de chimie, 48 Lawrence, D. H., 217 Lawrence, Ernest, 54; Lawrence Laboratory, 55

INDEX

lead plant (Plumbago), sticky hairs, 284, 284–85 leaf aerodynamics, streamlining, 169; trembling aspen, 171, 171–72 leaf anatomy, 62; Begonia maculata, 198; holly fern, 35; Indian almond, 204; merewan tree, 62 leaf color: black, 225; iridescent blue, 197, 223; red, 219; variegation, function, 199 leaf development: expansion, angiopteris, 113; expansion, robusta coffee, 113; expansion, wild coffee, 113; geometry, 113; primordia, 114, 120, 125, 161; senescence, 131–32 leaf ecology: drip tips, 174; leaf area index (LAI), 67; litter, 86; phenology, 87 leaf economics: construction costs, 93; economics spectrum, 98–99, 99; as factory, 94; life span, 99; longevity, 96; payback time, 95; size, 101 leaf edges: and climate, 169; teeth & photosynthesis, 173 leaf evolution: megaphyll, 32, 120; microphyll, 130 leaf morphology: blade, 202; compound, 161, 171; evergreen or deciduous, 100; simple and compound, 121, 174 leaf movement, 276–80; sleeping, 271, 277; sun-tracking, 271 leaf nutrition and defense; defensive structures, 238; herbivory, 238–39; miners, 242, 259; nutrients, 236; trichomes, 188; vitamins, 236 leaf optics, 63, 226; fiber-optic guides, 199; light absorption, 170; pathlengthening effect, 63; sieving effect, 63; surface lenses, 197 leaf shape: asymmetry, 177; geometry, 131; lobes, 161; mathematics, 175–77, 176; outlines, 159 leaf traits, 98, 313–30 Lee, Shaun, 288, 301, 306–7 Leeuwenhoek, Antonie van, 50

INDEX

· 450 ·

Leonardo da Vinci, 79, 156; Treatise on Painting, trees, 134–35, 135; veins, 212 Leonardo of Pisa (Fibonacci), 125 lettuce, 104; leaf margin, 176 Lewis, C. S.: The Chronicles of Narnia, 2 lichens, 37; leaf, 38 life, tree of, 26 life plant, leaf movements, 278 light: penumbral, 147; red to far-red (R:FR), 162–63, 163; secondary compounds, 241 lignin, 28, 183 lily, trout, 219; Victoria, 102, 136 Lindenmayer, Aristid, 176 Linnaeus, Carolus (Carl von Linné), 90–92, 92, 127; Oeconomia Naturae, 91 Little Shop of Horrors, 271 liverworts, 28, 31 living stones, 64 llanos, Venezuela, 72 Locke, John, 296 looking-glass mangrove, scales, 187 lotus, sacred, 9, 192–93, 193; effect, 192–93 Louv, Richard, 290–91 Lovelock, James, 88 Lovin, Christina, 269 L-systems, 148, 176 lulav, 8 Lunar Society, 46 lutein, 237 lycopene, 222 lycopsids, 31 Lygodium, 120 macaranga, 266 MacArthur, Robert, 146, 172 magnesium, chlorophyll, 237 maidenhair fern, veins, 202 Malaysia, 9; market, 234–35 Malpighi, Marcello, 109, 203 Mandelbrot, Benoit, 176–77 Mapania caudata, 198 maple: Japanese, 220; laurel, 168; red, 20;

red, fruits, 218; Stonerose, 166; sugar, 16, 168, 209 Mareines and Patalano (architects), 138 Margulis, Lynn, 24, 88 Marsham, Robert, 71 Masters, Michael, 117 Matonia, fern, 164–65, 165 Matthiessen, Peter: The Cloud Forest, 17 Mauna Kea, Hawaii, 83 May apple, 153 McQuade, Molly, 190 “Meaning of the Garden” course, 252, 289 meditation, 300 Mediterranean, 6; scrub, 73 Medusa, 3 Mereschkowsky, Konstantin, 24 Merleau-Ponty, Maurice: phenomenalism, 297 Merlin, 4 Mestral, George de, 179 metamorphosis, etymology, 108 metapopulation, 141 methane, 81, 84 methyl jasmonate, 246 Meyerowitz, Eliot, 117, 128 Miami, Miami-Dade County, 18, 36; humidity, 78 Miccosukee, 105 Michelangelo, Fabian, 265 midrib, 202 mimosa, form, 15 mindfulness, 300 mistletoe, 6, 20 Mitchell, Peter, 57 mitochondria, 27 Monophyllaea, 103 Monstera: leaves, 42; M. tenuis, 122 morphogenetic field hypothesis, 124 mosses, 28, 30 Muhammed, prophet, 8 mullein, 189–90 Münch, Ernst, 205 Munnar, South India, 104

· 451 ·

mutants, 116–17 mycorrhizae, 245 myrtle, 8 Nadkarni, Nalini, 291 National Ecological Observatory Network (NEON), 100 National Museum of Natural History, 29 National Phenology Network, 71 natural selection, 64, 131, 160 nature, artificial, 302; loss of, 287 Nelson, Pete, 251 neocortex, 294 Neolithic, 8 Nepenthes bicalcarata, 194 neptune grass, Mediterranean, 170 Nesbitt, Kenn, 234 nest, chimpanzee, 254 net primary production (NPP), 82–83 neuroesthetics, 306 neurohormones: GABA (gamma butyric acid), 276; glutamate, 276; L-dopa, 276; serotonin, 276 neurons, 274 Neurontin (gabapentin), 276 Newton, Isaac, 46; mechanics, 152 nicotinamide adenine dinucleotide phosphate (NADP), 57 nicotine, 239 Niklas, Karl, 153, 163, 177 nitrogen, 87; cycle, 81; resorption, 81, 230 nitrous oxide, 81 Nocera, Dan, 61 nomenclature, binomial system, 91 normalized difference vegetation index (NDVI), 67 oak, live, 100; English, 165; oriental white, 167; red, 162, 167; scarlet, 220; shingle, 167 Obi-Wan Kenobi, 9 Occam, William of, 130; Occam’s razor, 130 Ogham alphabet, 4, 6

INDEX

O’Keefe, John, 230 Oldeman, Roelof, 143, 150 Old Testament, 23 Oliver, Mary, 286 Olympics, 6 organelles, 24 Orians, Gordon, 146 Origin of Species (Darwin), 160 Orinoco River, 14 osmosis, 182, 205 Oxford University, 2 oxygen, 48; concentration, 86 ozone, 27, 86 paku merah, 9 Palasa, tree, 7 palisade cells, 35, 161 palm: African oil, venation, 211; African raffia, 101; argun, leaf anatomy, 154; carnauba, wax, 184–54, 154; coconut, 126–27; date, 8, 12; European fan, 128; foxtail, 144; giant-leaved caryota, 102; sabal, 105, 164, 166; talipot, 101, 102, 144; thatch, 154; traveler’s, 123; triangle, 123 Palm Sunday, 8 Pangaea, 86 papaya, 162–63 paperbark, prickly, 142 parastichies, 125 Paris Agreement, 88 Parker, Judith Evans, 19 Parkinson, John: Paradise in Sole Paradisus Terrestris, 12–13, 13 Parrot Jungle, 288 Pastan, Linda, 133 Paxton, Joseph, 136 peepal, leaf, 7, 213 Pelargonium (geranium): P. fulgidum, 168; P. laxum, 168; P. peltatum hybrid, 168 Pelletier, Pierre-Joseph, 50 Penning de Vries, Fritz, 94 peony, mutant, 116 PEP carboxylase, 63

INDEX

· 452 ·

pepper, 12 Perseus, 3 petagram, 83 petiole, 34; biomechanics, 155 phenology, 70, 221 pheromones, 247 phloem, 28, 38 phlogiston, 44, 48 phobias, 294–95 phosphoglyceric acid (PGA), 55 photon, 60 photoprotection, 230 photosynthesis, 24, 29, 38, 39, 68, 162; action spectrum, 53; C3, 73; C4, 63; CAM metabolism, 64, 72, 87; dark reaction, 53; efficiency, 36, 60–61; grasses, 72; light compensation point, 60; light-harvesting complexes, 57; light reaction, 53; light saturation point, 60; metabolism, 87; naming, 50; photoinhibition, 61, 225; photosystem I and II, 54, 57; Z-scheme, 56 phylloquinone, 237 phyllotaxis, 123–24 Physical Table of the Andes and Neighboring Regions (Humboldt), 159 physiognomy, 68; etymology, 68 physiological anatomists, 196 physiological plant anatomy, 160 phytochrome, 278 phytotelmata, 257 pigment, antioxidant, 228 pine: bristlecone, 97; lodgepole, 126 pipe model, 156 pitch apple, 64 pitcher plants, 194; Asian, and ant, 26; giant, 273 plane tree, American, 218 plant: carnivorous, 258, 280–85; flavor and fragrance, 249; functional types, 69–70; intelligence, 248; respiration, 82; vascular, 32; water harvesting, 195 plasmodesmata, 275

plasticity, 62 plates, continental, 86 Plato, “Allegory of the Cave,” 108 Pliny, Natural History, 4 plumule, 110–11, 111 pneumatic trough, 46–47, 47 Podostemaceae, Venezuela, 170 poinciana tree, 145 pokeberry, 225 Pollan, Michael, 44, 234 Ponce de Leon, 12, 18 Poorter, Hendrik, 94 Pope, Alexander, 66 Power of Movement in Plants, The (Darwin), 270 prayer plant, leaf movements, 278 Prentice, Colin, 72 pressure: atmospheric, 209; gradient hypothesis, 205 Priestley, Joseph, 45–47, 47, 64 Pringle, John, 48, 76 printing press, 12 prison, nature murals, 289 Protista, 25 Proto-Indo-European (PIE), 5, 8; arboreal units, 6; tree flora, 6 Proulx, Annie, 271 pseuderanthemum, 225 psychoanalysis, 298 pulvinus, 276 Pythagoras of Samos, 108 python, Burmese, 36, 73 Qur’an, 8 radiant energy, flows, 75 radioisotopes, 54; carbon 14 (14C), 54 radiolarians, 39 Raine, Kathleen, 133 Rainforest Action Network, 288 raisin, wild, 174 Ramachandran, V. S., 296–97 Rancho Grande, Venezuela, 159, 172 rap music, 291

· 453 ·

Raunkiaer, Christen, 69 reactive oxygen species (ROS), 228 reality, virtual, 303 Reich, Peter, 99 reiteration, 150–51, 151 respiration, 24; dark, 95 reSTART, 303 restoration, ecological, 301–2 Resurrection fern, scales, 187 retinoic acid, 237 rhizomes, 146 ribulose bisphosphate (RuBP), 55, 57 ribulose bisphosphate carboxylase (RuBisCO), 58, 61 rice, 12 Richards, Jennifer, 208 Ricklefs, Robert, 91 river basin, 80 Robin Hood, 20 rock tripe (lichen), 38 Romans, 6 roots, 31 rosemary, 73 Rosenberg, David, 10 Ross, Robin, 43 rowan (oak), 6 Roxburgh, William, 76 Royal Palm Hotel, 19 Royal Society of London, 46, 76, 110, 274 Ruben, Samuel, 54 rudraksha, old foliage, 221 Ruskin, John, 136 Ryman, Geoff, 42 Sachiko, Nishida, 262 Sack, Lauren, 208 sage, 73; glandular hairs, 187 Salvinia, 192 salvinia effect, 193 Sanderson,John Burden, 273, 273–74 Sanskrit, 7 Sarracenia flava, 194 sassafras, 163–64, 164; Stonerose, 166 Sassoon, Siegfried, 217

INDEX

satin pothos, epidermal lenses, 197 Saussure, Nicolas-Theodore de, 49 savanna, 72 Sawdonia, 30 scarlet passion flower, veins, 202 scene detection, 295 Schimper, Andreas, 24, 50, 69; PlantGeography upon a Physiological Basis, 160 Schultz, Jack, 249 Schumacher, E. F., 101 scientific method, 292 screw pine, 123 sea-level rise, 88 Selaginella (peacock fern), 9, 163–64, 164; surface, 182 self, the, 298 Semalai (Malaysia), 9 semaphore plant, 270, 276 Seminole, 105 Semitic, 8 Senebrier, Jean, 49 sensation and perception, 296 sensitive plant, 270–71, 274; electrical signal, 279; leaf movements, 279 Sharp, William, 203 sheep, vegetable, 189 Shelley, Percy Bysshe, 269 shell ginger, 146 Shepard, Paul, 251, 290, 298 Shiva, Lord, 7 shoot apical meristem (SAM), 93, 115, 123, 141, 161; castor bean, 115; celery, 115; green champa, 115 sieve cells, 205 sieve tube elements, 205, 275 sieving effect, 226 signaling, electric, 274 silica nano-particles, 198 silk spangle gall, 260 Sinnott, Edmund, 169 sinuses, 162 Sir Gawain and the Green Knight, 3 slippery liquid-infused porous structures (SLIPS), 195

INDEX

· 454 ·

sloth, three-toed, 40 slugs, sea, 39–40, 40 Smith, Adam: The Wealth of Nations, 92 snapdragon, 128 Snargaluff (Harry Potter and the Half-Blood Prince), 271 snowbush, white leaves, 222 Society of Plant Signaling and Behavior, 249 soil, 33 solar radiation, spectral distribution, 74 sourwood, 220 Sperry, John, 208 spices and herbs, 250 spider mites, 242 spinach (Spinacia oleracea), 225–36; leaf, 52; names, 235 spiral: dinner plate leaf, 126; galaxy M74, 126; logarithmic, 126 spongy cells, 35 Stapledon, Olaf, 41 Star Wars trilogy, 9 Stevens, Anthony, 298 stinging nettle, hypodermal hairs, 188 St. John’s College, Oxford 1, 231 stomates (stomata), 31, 35, 62, 173, 209; density, 79, 87, 169; function, 185; guard cells, 119, 185 Stonerose, WA, 164, 212 Stoppard, Tom, 158 Strahler, Arthur, 212 Strasburger, Eduard, 117 stromatolite, 22, 22–23 sucrose, 58, 204 Sukkot (Feast of the Tabernacles), 8 sulfur dioxide, 86 Sullivan, Louis, 139 Sumeria, 8 sundew, 274; round and filamentous leaved, 282; tentacle action potential, 282 sunflower, 124 super-hydrophobic, 192 supernova, 22

superorganism, 91 Swiss cheese vine, 132 system, hydraulic, 280 “Tableau of Nature” (Humboldt), 68– 69, 69 Tagore, Rabindranath, 200 taiga, 74 tanks, 257–58 tannins, 240, 244 tea, plantation, 104 temperate deciduous broadleaf trees, 69 temperate deciduous forest, 73 temperature, history, 85 Temuan, Malaysia, 253, 254, 298–99, 299 tendu, 105 terebinth, 12 terminalia, branching, 149 tetrapyrrole, 238 thale cress, 117 thatching, roof, 105 Theophrastus, 12, 44, 76, 160; Enquiry into Plants, 12, 108 theophylline, 239 therapy, digital: tree house, 303; wilderness, 306–7 Thompson, D’Arcy Wentworth, 175 Thoreau, Henry David, 70, 158 thyme, 73 tiger, 9 Tillandsia landbeckii, 196 Tokyo Dome, inflated root, 154 Tolkien, J. R. R., 2, 8, 42; The Lord of the Rings, 2, 8 tomatoes, enemies and defenses, 242– 44, 243 Tomlinson, Barry, 143, 208 Tomlinson, H. M.: The Sea and the Jungle, 17 tool kit, 118 Torah, 8 torsion, 155 tracheids, 28, 204; and vessel elements, 216 translocation, 28, 205

· 455 ·

transpiration, 46, 68, 77, 81; heat, 81 transpiration-cohesion hypothesis, 205 transport, 28, 205; electron, 56 tree: cacti, 69; crown packing, 152; crown shyness, 151–52, 152; species composition and autumn color, 232 Treebeard, 9, 20 tree house, Morris Arboretum, Philadelphia, 252 Treehouse Masters, 251 trees, pioneer, 173 Treseder, Kathleen, 265 Treub, Melchior, 160 Trewavas, Anthony, 249 tribology, 194 Tridacna, clam, 40 trigger hairs, 280–85 tropical deciduous forests, 70, 72 tropical rainforest, 72, 216; canopy, 291; profile diagram, 159 tundra, 74 Turing, Alan, 124 Tyree, Mel, 208 Ulrich, Roger, 293 Unitarian Church, 48 Ur, 8 Urpflanze, 127, 127–28 Ussher, James, 23 Utricularia (bladderworts), 280–81, 281 UV protection, 27 Valencia, Lake, Venezuela, 64, 67 Vareschi, Volkmar, 158, 172, 174 variegation, function, 219 vascular endothelial growth factor (VEGF), 203 Vedic culture, 3, 23 vegetable sheep, 12 vegetable vendor, Thailand, 235 vein: branching, 201; density, 215; development, 162, 202; dicots, 210; evolution, 214–15; fractal, 213, 215; monocots, 210; reticulate, 201

INDEX

Velcro, 179 Venezuela, 64 Venus flytrap, 270–71, 280, 283, 283–84; digestive enzymes, 284; trap closure, 284; trigger hairs, 284 vertebrates, evolution, 294 vessel elements, 28, 204 Viburnum, 173; maple-leaved, 174 Vigneron, Jean-Pol, 195 violet, sagebrush, 168; common blue, 168; tree, 168 Virgil, Aeneid, 4 Virgin Mary, 3 volatile organic compounds (VOC), 86, 243 volcanisnm, 34 volicitin, 244 Voyage of the Beagle, The (Darwin), 17 Wallace, Alfred Russel, 17, 64; The Malay Archipelago, 17 Wallin, Ivan, 24 Warburg, Otto, 53 Warli, Maharashtra, India, 254, 298–99, 299 warming, global, 85 wasp, parasitoid, 243, 260 watch, as designed machine, 91 water: cycle, 78; erosion, runoff, 77; molds, 26, yield, 77 watershed, 79 waterwheel plant, 280–81, 281 wax, structure, 184 Weeks, Michelle and Trent, 280 Weinberg, Steven, 22 Welwitschia mirabilis, 97 Went, Fritz, 124 Westoby, Mark, 99 whisk fern, 29 Wilber, Ken, 292 Willdenow, Carl Ludwig, 68 Williams, Kimberlyn, 94 Williams, Walter Jon, 42 Willis, Thomas, 296

INDEX

· 456 ·

Willstätter, Richard, 51 Wilson, E. O., 294 window plant, 132 Wordsworth, William, 286 World Fairs, 17; Centennial International Exhibition in Philadelphia (1876), 17; Exposition Universelle in Paris (1889), 17; Great Exhibition in London (1851), 17; Louisiana Purchase Exposition in St. Louis (1904), 17; World’s Columbian Exposition in Chicago (1893), 17 Wright, Frank Lloyd, 138 Wright, Ian, 99

Xishuangbanna Tropical Botanical Garden (China), 269 xylem, 28, 33, 35, 204, 280 Xyris, leaf epidermal cuticle, 183 yerba maté, 105 Yggdrasil, 4 Yoda, 9, 37 Zane, J. Peder, 213 Zimmerman, Martin, 207 zooxanthellae, 39, 145 Zwieniecki, Maciej, 162, 208