Darwin's Backyard

by James T. Costa

  Venus flytrap, Dionaea muscipula. In this drawing of an open trap by George Darwin, the triangle of small trigger hairs is visible on the inner surface of the upper leaflet. The long, stiff spikes lining the edges of the lobes look lethal and some early observers thought they functioned to pierce prey. Their lethality stems, however, from their vise-like grip once the trap snaps shut. From Darwin (1875a), p. 287.

  “Astonishing production!” exulted colonial-era American naturalist William Bartram in 1791, contemporary of Erasmus though a generation younger. This was the plant, recall, that Bartram declared was endowed with “sensible faculties or attributes, similar to those that dignify animal nature; they are organical, living and self-moving bodies, for we see here, in this plant, motion and volition.”18 Darwin concurred, opening his discussion in Insectivorous Plants with the declaration that “This plant . . . is one of the most wonderful in the world.”19

  Remember that Darwin’s Drosera studies were initially a means to an end, and that end was to understand the Venus flytrap: “I began this work on Drosera in relation to gradation as throwing light on Dionaea,” he wrote in 1860 to Daniel Oliver at Kew. Oliver was able to oblige him with a few flytrap leaves for study, and eventually whole living plants, but not before Darwin had to beg, cajole, plead, implore . . . everything short of grovel:

  Is it [Dionaea] a very precious plant? Could a living plant be packed so as to come here by Railway & could I keep it alive for week or two in sitting room? If so, would you be so kind as to give me address of any nurseryman where I could purchase a plant. Or if there are several plants at Kew, would you read this note to Sir William [director of Kew at the time] & ask him whether he could lend me a plant, which should be returned (carriage free) to Kew; but I should require to gather & dissect some leaves. I want to compare structure of hairs of Dionæa & Drosera . . . I would just as soon purchase as borrow: I only mention Kew in case the plant is not to be easily purchased & in case of there being several plants at Kew. How I should like to see a fly caught by it!20

  It was a precious plant, a rarity that the gardeners of Kew were not very willing to share (hard to imagine today, when every garden center large and small offers them for sale, each neatly packaged in its own plastic hothouse). Darwin’s desperation is almost palpable—he was ecstatic when he finally got a few to study, so imagine how he would have reveled over them in their native environment of the coastal Carolina marshlands. Like the sundews, at a distance natural populations of this diminutive plant form an impressionistic red-tinged green wash, resolving on closer inspection into whorls of bilobed green leaves fringed with those evil-looking (but harmless) spikes, each leaf gaping wide to show its tempting scarlet throat—a lascivious trap set with a botanical come-hither look outdone only by the orchids.

  What made Venus flytrap especially wonderful to Darwin was not so much how its snap-trap leaves become a temporary stomach, fascinating and instructive though that was to him. (He tested their reaction to the same diversity of substances as with Drosera.) Rather, he was convinced it had a nervous system analogous to that of animals, something he investigated but could not quite convince himself of with the “reflex action” of the sundews. Darwin’s initial work done with the flytraps was put on hold along with his sundew experiments back in the early 1860s, but later that decade Asa Gray first drew Darwin’s attention to the work of another American naturalist, William Marriott Canby of Wilmington, Delaware. Canby, a businessman and philanthropist, was also an avid botanist and a regular correspondent with Gray on such matters. In 1867 Canby wrote to Gray: “The little Dionaea has become exceedingly interesting to me, & I have been making some experiments with a view to test its carniverous [sic] propensities.” He then went on to describe a host of observations and experiments on prey trapping and digestion, even testing their taste for various substances à la Darwin: “In one leaf I placed a piece of cheese. This was partly dissolved but it was evidently not the food nature intended, as the leaf after going through a considerable part of the operation of digestion, became sick and finally died.” Death by indigestion—a horrible end, even in a plant. Gray sent the letter to Darwin. The observations were scarcely new to him, however, and he had already made the same observations. He wrote back to Gray, “This letter fires me up to complete and publish on Drosera, Dionaea, etc., but when I shall get time I know not. I am working like a slave to complete my book,”21 he lamented. Darwin was still bogged down finishing Variation, which came out at last the following year. Turning his attention back to his “sagacious” plants in the early 1870s, he recalled Canby’s letter to Gray, and Canby’s declaration in that letter that he wished “someone would take hold of this who was fully able to elaborate it” and that he would “gladly aid all I can in furnishing specimens, &c.” In January 1873, 6 years on, Darwin again wrote Gray about this:

  You sent me a letter dated Wilmington July 9. ‘67 about Dionaea. It has no signature but you refer to it as written by Mr. Canlay or Canbay or Cawley. Will you be so kind as to write the name for me distinctly, for some people are so foolish as to say that your handwriting, like mine, is not very legible. The letter has interested me much in some respects & the gentleman seems very kind & willing to oblige.22

  (It was an understatement for Darwin to acknowledge that his handwriting was “not very legible”—even today few individuals are versed in the art of deciphering his notoriously illegible scrawl.) Gray supplied him with Canby’s address and Darwin soon wrote, but mistakenly thought that Canby lived close to the native habitat of the flytraps—an understandable error, with the plants naturally found around Wilmington, North Carolina, while by coincidence Canby lived in the more northerly Wilmington, Delaware. Canby set Darwin straight, and let him know that in some months’ time he hoped to travel to coastal North Carolina and would make observations for him.

  In the meantime Darwin subjected his flytraps to a battery of experiments, quickly noticing that the inner surface of each leaf lobe bears three slender filaments arrayed in a triangle. These proved to be the trigger hairs that produce the snap-action of the trap. Unbeknownst to Darwin, the clergyman and naturalist Moses Ashley Curtis (who unlike Canby did live in Wilmington, North Carolina) had correctly noted the function of these hairs decades earlier, in an 1834 paper. Curtis had also noted the digestive properties of the leaf, commenting in his paper on the plants’ mucilaginous fluid that seemed to dissolve insects.

  Darwin explored the sensitivity of the filaments (technically termed “trichomes”) by devising a probe: a piece of “very delicate human hair” (probably his own) was affixed to a handle and cut to 1 inch in length, a length “sufficiently rigid to support itself in a nearly horizontal line.” Carefully reaching in and touching the side of a filament lightly with his probe, he induced the lobes to abruptly snap shut. He could have done this with a needle or some such, but using the fine hair enabled him to show that the trigger hairs were sensitive to the lightest touch. Of course, the price of such sensitivity of the leaf might be needless closing—cases of mistaken identity, when blown debris happens to touch a filament, or wasted effort when insect prey minute enough to escape between the fringing bristles touch it off. Darwin tried to trip the trap by sprinkling water and other substances like flour on the lobes. He even tried blowing hard, simulating a gale. The traps remained unsprung. He correctly concluded that in the plant’s natural environment downpours and gales are common, and the plants adapted so as not to be fooled. Occasionally blown debris may set one off, but more often than not it is a prospective meal that springs the trap, and a noteworthy property of the trigger reduces the error rate: the filaments must be contacted by something solid, and a given filament must be contacted not once but twice within about 15 seconds to induce the trap to close. Reducing the error rate is important for the plant because the traps have the ability to snap shut only so many times. After all the leaves lose their ability to close, the plant can only rely on photosynthesis to live.

  The reas
on for this gets at the heart of an important difference between animal movement by muscle action and the movement of these plants: think of the pull of muscle attached to bone as a force generated from within the body. In contrast, movement of the flytrap leaf lobes stems from a force generated outside, on the leaf surface. More specifically, the pull results from changes in the curvature of the leaf surface, which in turn results from rapid shrinkage of the inner side of the leaf relative to the outer. But what is behind the spurt of growth of the leaf cells? Plant cell walls are usually fairly rigid, but Venus flytrap has a mechanism called “acid growth” that permits rapid cell expansion. Acidic chemical compounds are produced that relax the usually rigid cell walls, allowing the cells to grow or expand. Expansion on the outer side of the leaf makes that side larger in area than the other, so the leaf flexes in the opposite direction—the lobes close inward. The problem is that this is not reversible. Turgor pressure changes in the cells on the outer leaf surface result in the lobes slowly opening, and resetting the trap, but each time the trap snaps shut the acid growth process results in the cells getting slightly larger; after a while they reach their limit, and that leaf is no longer able to function.

  Darwin did not know these details, but he realized that each trap can be sprung a limited number of times. He looked closely at the mode of capture and was immediately struck by the speed and force with which the leaf lobes closed on prey. The lightning-fast closure is helped by the fact that the lobes are at right angles to one another, so each needs to move about 45º as opposed to the 90º arc needed if they were splayed out horizontally. The fringing bristles of each lobe interlace with one another, like the fingers of clasped hands, but he was careful to note that the bristles themselves did not move. Leaves that had been fooled into closing by probing the trigger hairs or feeding them indigestible substances took a day or more to reopen fully. Even when partially open (Darwin observed that of 10 leaves observed most were about two-thirds open after about 7 hours) they are capable, however, of closing again quickly. Another thing that a more casual eye might not notice is how the lobes initially form a concave space around trapped prey, like a stomach, and then slowly but surely become firmly appressed all around the prey until the trapped insect appears as a distinct bulge on either side of the leaf, like a meal within opaque green shrink-wrapping. At this point the lobes are so tightly shut that Darwin could only peer inside by forcefully driving a wedge between them. He had to be careful; with too much force they “are generally ruptured rather than yield.”

  The quick snap action of the leaves immediately reminded Darwin of reflexive motor impulses of animals. Here, perhaps, was a better candidate for a botanical nerve-pulse “reflex action” than sundews. His first breakthrough in pursuing the idea that the plant had a nervous system came in fall of 1872; as he described in an excited letter to Gray:

  The point which has interested me most is tracing the nerves!!! which follow the vascular bundles. By a prick with a sharp lancet at a certain point, I can paralyse ½ the leaf, so that a stimulus to the other half causes no movement. It is just like dividing the spinal marrow of a Frog:—no stimulus can be sent from the Brain or anterior part of spine to the hind legs; but if these latter are stimulated, they move by reflex actions. I find my old results about the astonishing sensitiveness of the nervous system (!?) of Drosera to various stimulants fully confirmed & extended.23

  Ever supportive, Gray replied: “it is wonderful—your finding the nervous system of Dionaea!!!” Pursuing this line of inquiry further required the assistance of a specialist. He collaborated again with John Burdon-Sanderson, his physiologist friend. In the summer of 1873 Burdon-Sanderson suggested experiments using a galvanometer to test for electrical activity in the leaves. Working with plants at Kew Gardens, it was not long before Burdon-Sanderson had flytraps wired up like a patient getting an ECG. He first found differences in electrical potential using parts of the leaf and stem, and then, most excitingly, discovered that when a fly stimulates a leaf, a striking change in the leaf’s electrical current results: the “leaf-current,” as he called it, showed an abrupt spike in electrical potential immediately before the lobes snapped to a close. He telegraphed Darwin with the news, and soon gave lectures on the phenomenon at the British Association and the Royal Society. “These currents are subject,” he declared, “to the same laws as those of muscle and nerve.”24 Darwin was so excited that he made a rare effort to get up to London to attend Burdon-Sanderson’s lecture at the Royal Institution that June.

  John Burdon-Sanderson’s test of the electrical properties of a Venus flytrap leaf using a modified Thomson galvanometer. From Burdon-­Sanderson (1874), p. 128.

  Darwin reported Burdon-Sanderson’s results along with his own flytrap experiments in Insectivorous Plants. He was able to show that the lobes can act independently by “paralyzing” one of the two lobes, and with the help of his son Frank he made detailed study of the cellular structure of the leaves. More than any other plant he had studied to date, Venus flytrap really did seem animal-like not only in its “behavior” and digestive abilities, but also in having a sort of nervous system. He shared Bartram’s wonder at these plants, endowed as Bartram said with “sensible faculties or attributes, similar to those that dignify animal nature”—plants with volition, even. Little wonder that Darwin declared these plants “one of the most wonderful in the world.”25

  An Aquatic Flytrap?

  A good many other carnivorous plant groups were experimented upon and discussed in Insectivorous Plants: other sundews, aquatic and terrestrial members of the bladderwort family, Lentibulariaceae: Utricularia, with its tiny underwater “suction traps,” and Pinguicula, the butterworts common on heathlands where they compete with sundews by trapping minute insects on their sticky flypaper-like leaves. The most striking one, though, turned out to be an aquatic relative of the Venus flytrap: the waterwheel plant, Aldrovanda vesiculosa, widely distributed from Europe to Africa and Australia. The botanist Giuseppe Monti named this plant Aldrovandia in 1747, in honor of the sixteenth-century Italian naturalist Ulisse Aldrovandi. Evidently Linnaeus made a typographical error when he recorded the name in his Species Plantarum of 1753, inadvertently dropping the “i.” The error stuck.

  Aldrovanda is a curious, rootless plant, with hinged leaves arranged in a whorl around a central, free-floating stem. The leaves are lobed somewhat like those of the Venus flytrap and also snap shut at the touch of trigger hairs, but do so far faster than Venus flytrap, in as little as a tenth of a second. Hooker sent some over from Kew in September of 1874.

  Darwin immediately noticed that the plant seemed to have snap-action leaves like Dionaea, but floated in water and caught minute free-swimming prey like Utricularia, the aquatic bladderwort. On closer investigation he found that Aldrovanda was even more similar to bladderwort than he thought. The inner surface of the leaf lobes has lots of minute filaments, each with four tiny arms. Darwin called them “quadrifid processes,” and soon determined that they played a digestive function, like the glands in Drosera and Dionaea, which secrete digestive enzymes and absorb the digested matter. Then he noticed that the lobe edges are lined with similar filaments, which apparently only absorb and do not secrete enzymes. Now, that was a novelty for a carnivorous plant. It suggested a rudimentary form of the kind of specialized function found in other carnivorous plants. As he put it in the conclusion of his chapter on Aldrovanda: “if this view is correct, we have the remarkable case of different parts of the same leaf serving for very different purposes—one part for true digestion, and another for the absorption of decayed animal matter.” If so, this would have broader evolutionary implications, he realized: “We can thus also understand how, by the gradual loss of either power, a plant might be gradually adapted for the one function to the exclusion of the other; and it will hereafter be shown that two genera, namely Pinguicula [butterworts] and Utricularia [bladderworts], belonging to the same family, have been adapted to two different functions.”2
6 In Aldrovanda Darwin thus saw the grand themes of gradual adaptation, divergence, and common descent that his theory of evolution by natural selection so nicely explained.

  The sensitivity to touch, movement, and digestive abilities of carnivorous sundews and flytraps may echo the animal world, but the mechanisms behind them are not just simpler versions of mechanisms better developed in animals. They are analogous rather than homologous; generally speaking, they are evolutionary convergences of similar solutions to the same problem. Darwin may have been hoping for a closer correspondence, but he conceded that phenomena like the “reflex action” of these plants were probably very different physiologically from those of the animal world. At another level, Darwin was right on the plant-animal relationship: the physiology and anatomical machinery behind movement and digesting food in these plants may differ from those of animals, yet there are enough similarities to point to commonalities in physiology, commonalities that point to common ancestry.