Darwin's Backyard

by James T. Costa

  Darwin summarized the direction and rate of movement of over 40 twiners in a long, five-page table; some rotated with the sun, some opposite the sun, some fast, some slow. The champion of this botanical track-race was Scyphanthus, an attractive vine from Chile, lapping in just an hour and 17 minutes. He later found two climbers that rotated even faster: tendrils of the purple-flowered Mexican vine Cobaea completed a circuit in about an hour and 15 minutes, and a passionflower, Passiflora gracilis, had tendril speeds averaging 1 hour and 1 minute. Now, that’s a vine you could set your watch by!

  Elliptical movement of the upper internodes of a common pea plant (Pisum sativum), as traced on a bell jar and transferred to paper with illumination coming from the direction of the bottom of the diagram. From Darwin (1865), p. 65, fig. 6.

  Darwin needed a way to graphically represent the movement of shoots and tendrils. Working with Frank, his first approach was to put a plant inside a large bell jar, a sort of terrarium of domed glass, and at regular time intervals mark the position of the upper stem seen through the glass with painted dots. The dots were then traced onto a flat sheet of paper, much as stars in the apparent curved “dome” of the night sky can be represented on a flat star map. The result showed the back-and-forth elliptical movement of the stem.

  The American geologist James D. Hague visited Down House in 1871, and described another experimental setup in an 1884 memoir of his visit:

  The work of the forenoon was the careful observation of a number of tender shoots that were growing in pots, each under a separate bell-glass, and all ranged on a table exposed to the morning sun. To the growing tip of each plant there had been attached by wax . . . one end of a straight piece of very finely drawn glass thread, in such a manner that its other end projected about two inches, horizontally or nearly so, from the point of attachment, where any revolutionary movement of the stem must be imparted to the glass thread, and cause it to turn like a radial arm from a central point. The ends of the glass thread were made conspicuous by little “blobs” of [paint], thus giving two easily distinguished points in one straight line. By marking then upon the outer surface of the bell-glass a third point in line with the two “blobs”, the subsequent departure of the outer “blob” from that line, caused by the turning of the stem of the plant, very soon became distinctly visible.10

  At some point in the late 1870s Charles and Frank realized that the bell jars weren’t ideal for their circumnutation studies—maybe owing to the curvature of the glass, or the limited size of the plants the jars could accommodate. Charles had an idea: why not try Emma’s and Etty’s plant case? Back in the early 1860s the Darwins became the proud owners of a Miss Maling’s Patent In-door Plant Case (a “handsome ornament for the Drawing Room or the Sitting Room”). Basically a large terrarium, about the size of a 50-gallon fish tank, Miss Maling’s ingenious design included slots in the base for pans of hot water, to be replaced twice daily in order to warm the case and “preserve many of the most tender Exotic Plants through the severest winter.” Darwin had originally bought the case for just that reason—as a hothouse for experiments—but it didn’t quite live up to its billing.

  Advertisement for Miss Maling’s Patent In-door Plant Case, an early terrarium. Darwin co-opted the family’s case for circumnutation studies. From the Gardeners’ Chronicle and Agricultural Gazette, January 17, 1863, p. 64.

  His frustration was one reason he resolved to build the greenhouse and hothouse, abandoning Miss Maling’s case to a delighted Etty. She and her mother kept it in the drawing room done up with hyacinths, azaleas, deutzias, and other plants. After Etty married Richard Litchfield in the summer of 1871, upkeep of the case fell to Emma. It was about this time that Darwin had the idea of using the top and side panes of the case for his circumnutation tracings—flat surfaces made tracing on them much easier than on the curved bell jars. Some of the species he documented were the very ones Emma most prized for the plant case, among them slender deutzia (Deutzia gracilis) and Indian azalea (Azalea indica), showy flowering shrubs from Japan. She surely didn’t mind having the case co-opted for the cause of science.

  Darwin’s circumnutation studies burgeoned and blossomed like the plants themselves, growing into a multitude of circumnutation tracings—roots and stolons, seedlings and leaves, flower stalks and tendrils. All of these entailed variations on the theme of his basic experimental design, described so well by Hague: the attachment of a fine glass needle with a small ball of wax affixed on the end to the structure being traced. The wax ball was viewed through a glass plate—the roof or side window of the plant case—using a fixed point of reference, and the position of the ball in the line of sight marked on the glass.

  It was tedious work, but in its way just what Frank needed to occupy his mind at a time of great sadness. Frank had studied medicine and physiology, and was married a few years after Etty, in 1874. He and his wife, Amy, had settled in the village of Downe, not far from Down House, and Frank would walk over almost daily to help his father with various experiments. Tragedy struck just 2 years later when Amy died in childbirth, though fortunately the baby survived. A devastated Frank and his newborn son Bernard moved back home with Charles and Emma. In his grief he threw himself into work and continued to help at Down House with all manner of experiments, especially plant movement, until his father’s death in 1882.

  For a while, the movement of plants became all-consuming for father and son, and one of their great insights was to realize that the gyratory movements Darwin had observed with climbing plants was actually a special case of a far more general tendency for nearly all plants and plant parts to revolve as they grow—roots, shoots, flowers, and leaves all are constantly but slowly, imperceptibly, tracing irregular and often narrow ellipses or ovals. Charles and Frank had hit upon a general principle of plant growth, one that if true could show how basic movements seemingly common to nearly all plants could be elaborated and modified in manifold ways. “Every growing part of every plant is continually circumnutating,” Darwin later wrote, “though often on a small scale. . . . In this universally present movement we have the basis or groundwork for the acquirement, according to the requirements of the plant, of the most diversified movements.”11 The uncanny power of movement in climbers was likely a special, derived case of movement found in plants generally, movement that may be simply a by-product of the growth process.

  Touchy Plants

  There is more to the climbing habit than circumnutation, and touch perception of all kinds in climbers fascinated Charles. Frank, too, became ensnared by the “irritability” of tendrils and other structures. Recall that in the eighteenth and nineteenth centuries one definition of the words “irritable” and “irritability” referred to being highly responsive to stimuli, a definition that botanists soon applied to the movement of plants in response to touch. Darwin’s climbers were plenty touchy, and he and Frank set about documenting when and under what circumstances. It’s plain enough that climbers sense the object that they move toward and grow upon, but are all parts of the growing shoot or tendril irritable? Will the plant respond to a fleeting touch as well as prolonged contact? Darwin’s approach was to lightly rub the petioles or internodes with a small stick and observe the response, or suspend a bit of string or thread for a very light touch. Unlike the lightning-fast action of plants like Venus flytrap, these climbers would respond in more usual “plant time”—taking hours. Darwin found that touch sensitivity resided in whatever organ was modified for climbing—petioles in the case of Clematis, for example, the last couple of internodes of the shoot for hops, and the entire tendril for grape vines. Of the many climbers he studied one of the most curious was the Mexican species Lophospermum (now Maurandya) scandens, a member of the plantain family, Plantaginaceae. This was a leaf-climber that used its petioles to grasp, but did so in an odd way: when the petiole bows and clasps a stick the adjacent internode is drawn to the stick too, and upon contacting the stick it also bends, trapping the stick between peti
ole and stem like pincers or forceps. Darwin tried 15 trials, each time rubbing the internodes two or three times and timing the result: most bent within 2 hours (all within 3), and then straightened themselves by the next day. He determined that all sides of the internodes were sensitive, and he was able to get them to bend first in one direction, then another. The response, he noted, was always toward the rubbed side.

  Another curious expression of touch perception was found in the crossvine, Bignonia capreolata, of the southeastern United States, a vine celebrated for its lovely large, red-orange hummingbird-pollinated flowers. Each tendril is multiply branched, and each branch is divided into bifid or trifid hooked ends, like tiny grappling irons. What made them remarkable, however, was more their behavior than their appearance. Darwin was puzzled at first to find the tendrils had little sensitivity and seemed almost indifferent to the sticks he offered for climbing. Then he noticed that the stem curved away from the light, toward the darkest side of the room. He tried to trick them into climbing a tube, simulating a stick but blackened within, and found that the plant soon “recoiled, with what I can only call disgust, from these objects, and straightened themselves.” In another experiment, Darwin placed a potted crossvine bearing six tendrils into a box open on one side only, and situated the opening to obliquely face a light source. Within two days he found that all of the tendrils were pointing toward the darkest corner of the box. This observation was all the more striking because the tendrils, being on different locations along the shoot, had to bend different degrees and directions to point that way. “Six wind-vanes could not have more truly shown the direction of the wind, than did these branched tendrils the course of the stream of light which entered the box,”12 he marveled.

  He began to connect the dots when he replaced the smooth slender stick with stouter posts, one with rough bark and one with fissures. The tiny tendril hooks soon found their niche, literally: “the points of the tendrils crawled into all the crevices in a beautiful manner.” Serendipitously, he discovered what the crossvine was really after: when a tendril seized on a bit of wool left within reach it dawned on him that the plant sought out fibrous, textured surfaces. He wrapped flax, moss, and wool around a smooth stick and voila!—the tendrils grasped and the vine climbed with abandon. What’s more, the little hooks at the end of the tendrils metamorphosed into tiny disks or balls that secreted an adhesive substance. Darwin had a hunch that this was related to the plant’s native habitat. He wrote to Gray in May 1864:

  Have you travelled south, & can you tell me, whether the trees, which Bignonia capreolata climbs, are covered with moss, or filamentous lichen or Tillandsia [Spanish moss]; I ask because its tendrils abhor a simple stick, do not much relish rough bark, but delight in wool or moss. They adhere in curious manner, by making little disks at end of each point, like the Ampelopsis [Virginia creeper]; when the disk sticks to bundle of fibres, these fibres grow between them & then unite, so that the fibres of wool end by being embedded in middle.13

  Gray replied that he had seen B. capreolata growing in the mountains of North Carolina and Tennessee. The vines, he said, climbed moist and shady trees, the trunks of which he didn’t doubt were “well furnished with Lichens and Mosses.” Gray remembered well: the southern Appalachian mountains are so wet that the vast deciduous forests of the region are distinctly green even when leafless in winter, so thick is the coating of epiphytic mosses, lichens, and ferns. The shade-seeking behavior of the tendrils thus makes sense: faced with a choice between light or shade, growing toward shade or shadow is more likely to pay off for young plants in terms of trees to climb, ultimately giving the vine access to light.

  Darwin was doubly delighted by his discovery: “It is a highly remarkable fact,” he declared, “that a leaf should become metamorphosed into a branched organ which turns from the light, and which can by its extremities either crawl like roots into crevices, or seize hold of minute projecting points.”14 This turning away from light belongs to a general class of plant movements called tropisms, from the Greek tropos, “turning.” Tropism refers to turning movements in response to environmental stimuli, of which there are several types: hydrotropism for moisture, thermotropism for temperature, and so on. Tropisms are further described as “positive” for movement toward and “negative” for movement away from the stimulus. So, “negative phototropism” describes the darkness-seeking behavior of Darwin’s Bignonia tendrils, an oddity in structures derived from light-loving leaves.

  Of Roots and Shoots

  Darwin came to suspect that insofar as all plant parts circumnutated, the rotary searching motion of climbers was an exaggerated expression. He embarked upon an investigation of circumnutation in a multitude of species and, crucially, at different stages of their growth. He found to his surprise that even the roots and shoots of seedlings gyrated. He was even more surprised, however, to find that in some cases an environmental stimulus overrode the gyration and influenced the direction of movement—certainly that was true of crossvine’s flight from light. For most plants attraction to light is the norm, of course. But just how is this accomplished? Is the entire plant light-sensitive, or are there specialized cells or organs, analogous to eyes, that see the light and direct the plant?

  Like the tendrils that John Horwood fancied could see, Darwin found that the growing tips of canary grass, Phalacris canariensis, also seemed to have eyes: “It can hardly fail to be of service to seedlings, by aiding them to find the shortest path from the buried seed to the light, on nearly the same principle that the eyes of most of the lower crawling animals are seated at the anterior ends of their bodies.”15 Grass shoots are encased in the seed leaf, the coleoptile. Father and son devised a series of experiments to show that the coleoptile has a distinct zone of sensitivity, one that signals other cells in the shoot about what direction to grow. Here is an example of their experimental approach:

  • As a control, they topped the coleoptile tips of nine seedlings with transparent glass caps and exposed them to a bright southwest window on a bright day for 8 hours. All seedlings strongly curved toward the light as expected, but the experiment also showed that the glass tubes did not prevent shoot movement.

  • They similarly enclosed 19 other coleoptiles in glass tubes, but these tubes were painted with black ink to block out the light. Five had to be rejected after the ink dried and cracked, permitting some light to get in. Of the remaining 14 seedlings, 7 remained upright and 7 were bowed, showing a light response. The Darwins suspected that the light response was due to leakage, or maybe reflected light from below the cap.

  • In an effort to better control the light exposure to the tips, they next fitted 24 seedlings with tiny tinfoil caps, like diminutive botanical sunglasses, covering the last 0.15–0.2 inch of the coleoptile. Three seedlings still detected light and bent, but of the remaining ones, 17 stayed upright, while 4 only slightly bent. To ensure that the lack of movement wasn’t due to injury from the caps themselves, they were removed and the plants fully exposed to light; all soon bowed toward the light, showing they were uninjured.

  • Since tinfoil caps between 0.15 inch and 0.2 inch long proved to be efficient in preventing the seedlings from bending toward light, they fitted another 8 coleoptiles with even smaller caps, just 0.06 to 0.12 inch long. Of these, only 1 bent markedly toward the light; the lack of response from all but this one showed that the sensitive zone was very close to the tip of the shoot.

  • Finally, the Darwins took another step toward localizing the zone of sensitivity by “bandaging” 8 shoots with strips of tinfoil about 0.2 inch wide, leaving the very tip of the coleoptile exposed. After 8 hours, the seedlings were curved toward the light. This was complemented with an experiment using the varnish-coated glass tubes again, only this time a tiny line or slit about 0.1–0.2 inch wide was etched into one side of the coating of each cap. While the lower half of 27 seedlings was left fully exposed to light, at the tips the only light exposure came from the etched slits. After 8 hours, hal
f (14) of the seedlings remained vertical, while the other 13 were bowed—and not simply toward the window, but rather in the direction of the etched slits. Clearly, just a tiny amount of light was often all that was needed to induce the light response, and this contained directional information too.

  Charles and Frank were certain that light exposure at the tip of the shoot somehow signaled the cells lower down to bend: the bowing that they observed took place not at the top of the shoot, but well below it. This means that the plant is capable of transmitting a signal from an area of stimulation—in this case the coleoptile—to elicit a response from cells elsewhere. It was a “striking fact,” Darwin declared. “These results seem to imply the presence of some matter in the upper part which is acted on by light, and which transmits its effects to the lower part. It has been shown that this transmission is independent of the bending of the upper sensitive part.”16

  Indeed, there is a means by which plants transmit the effects of stimulation: here Darwin anticipated the discovery of plant growth hormones. Nearly 50 years later, in 1928, Dutch botanist Fritz Went isolated the first plant hormone from canary grass, the very same species that the Darwins studied. He called the substance “auxin” from the Greek auxein—to grow or increase. Its chemical structure was determined by British plant physiologist Kenneth V. Thimann, and in 1937 he and Went coauthored a book entitled Phytohormones on the subject.

  Charles and Frank found a similar phenomenon with bean radicles. It was received wisdom that just as shoots and leaves grow toward light, so too do roots grow downward, toward the earth. If you pin or in some other way affix a germinated bean, say, so that the radicle is held out horizontally, it will soon bend downward. This was termed geotropism in Darwin’s day, but is more commonly known as gravitropism today. The conventional view of the time was that the growing radicle was pulled by gravity, it did not sense and respond to gravity per se. Or did it? Just as the Darwins showed with canary grass that the part of the growing shoot that is light-sensitive is not the same as the part that responds by bending toward light, they argued that there was more than met the eye with growing root radicles: the tip of the root is sensitive to gravity, they showed, and transmits a signal to cells farther up the radicle to induce the downward growth.