Charles Darwin's botanical studies provide a way to expose students to his work that followed the publication of On the Origin of Species. We can use stories from his plant investigations to illustrate key concepts in the life sciences and model how questions are asked and answered in science.
When the work of Charles Darwin is presented in an introductory class, the primary emphases are usually his voyage aboard the H.M.S. Beagle, particularly the time he spent exploring the Gal´´pagos Islands, and the book that eventually resulted from his thoughts that began on that voyage, On the Origin of Species (Darwin 1859). Although this book, in which he proposed that evolution occurs by the process of natural selection, is unquestionably a significant contribution to our understanding of the natural world, students are left with the impression that natural selection is the extent of Darwin's contributions to science and our understanding of nature. They never realize that he published several more books and papers on the various studies that he did at his home in Kent. Introducing students to these subsequent works provides them a broader and often different view of someone they thought they knew. Darwin's botanical studies, in particular, provide good examples of his later work. The botanical work was not only descriptive but investigative as well, supplying evidence to support the theory of natural selection. As Kohn (2005: pp. 39——40) put it, ““The best, most consistent, and most enduring web of evidence that Darwin ever developed in defense of his theory was botanical.””
If students in introductory classes encounter Darwin's botanical work, it is most likely the last investigations that he did on plant movements in collaboration with his son Francis (Darwin & Darwin, 1896). Their explorations of phototropism and gravitropism are generally the prelude to coverage of either plant movements or plant hormones. Often omitted are Darwin's studies on plant reproduction, especially pollination biology, and carnivorous plants (Darwin, 1862, 1900, 1986). In his books on these subjects, Darwin carefully described each of the specific plants he studied. This information is key because his experiments grew out of what he gleaned from close observations of organisms, often starting with field observations. Once he established the appearance of a specific organism in his reader's mind, he proceeded to describe his thoughts and actions as he probed that organism to discover the adaptive fitness of a particular feature. Darwin's writing models how questions are asked and answered in the sciences (see ““Science as Inquiry Standards”” in National Research Council, 1996). Furthermore, the areas he studied mesh well with our need to explain the basic attributes of living organisms to our students (Table 1; see ““Life Science Standards”” in National Research Council, 1996). Examples from Darwin's investigations with plants can increase and add variety to our collection of stories for covering these topics (Kreps Frisch & Saunders, 2008) and provide a historical perspective (see ““History and Nature of Science Standards”” in National Research Council, 1996). Additionally, we can emphasize the universality of these characteristics by using plant-based examples, helping us raise awareness of these often neglected organisms (Uno, 1994).
Many writers have noted that Darwin's botanical work alone —— even without his contribution of natural selection —— would have made him a significant Victorian scientist (Heslop-Harrison, 1958; Browne, 2002). In fact, when he was elected to the French Institute, it was in the Botanical Section in recognition of his discoveries with plants, not for his theory of natural selection (F. Darwin, 1899; Heslop-Harrison, 1958; Browne, 2002). Although he often protested that he was no botanist (F. Darwin, 1899; Darwin & Barlow, 1958; Heslop-Harrison, 1958), his botanical investigations led to some of his most significant and famous discoveries, such as revealing the adaptive advantage of one species producing different forms of flowers (Darwin, 1986), predicting the pollinator of an unusual orchid (Darwin, 1862; Kritsky, 1991), and concluding that plants use what we now call ““hormones”” to transmit information through their bodies (Darwin & Darwin, 1896).
Because the experiments included in The Power of Movement in Plants are often covered in introductory biology and botany classes, I will restrict this paper to Darwin's studies of pollination biology, sexual reproduction strategies of plants, and carnivorous plants. These studies were documented in three books that Darwin wrote on researches that grew out of field observations he made near his home (Browne, 2002; Kohn, 2005): On the Various Contrivances by Which British and Foreign Orchids Are Fertilised by Insects, and on the Good Effects of Intercrossing; The Different Forms of Flowers on Plants of the Same Species; and Insectivorous Plants.
The Biology of Pollination
The first book that Darwin wrote after On the Origin of Species was On the Various Contrivances by Which British and Foreign Orchids Are Fertilised by Insects, in which hereported the results of studies of how insects interact with orchid flowers to pick up and deliver pollen (Darwin, 1862). Orchids presented Darwin with a wide diversity of flower forms within a single taxonomic group in which he could learn how one group of organisms demonstrates diverse adaptations that accomplish the same objective, fertilization. Furthermore, the orchid is a good natural-history puzzle because in most orchids the pollen is not released as a dust composed of individual pollen grains for transfer by multiple insects. Instead, the pollen grains are released as aggregates called ““pollinia.”” A slender stalk connects a pollium to a sticky base that adheres the entire pollinium, containing thousands of pollen grains, to a pollinator. Darwin considered the adaptive advantage of this pollen delivery system in the last chapter of the book. A single orchid flower produces several thousand seeds and therefore needs to receive several thousand pollen grains. Pollinia are an efficient way to deliver this amount of pollen (Darwin, 1862).
In order for cross-pollination to occur, insects need access to the pollinia, and the collected pollinia need to be positioned on the insect properly for transfer to the stigma of a flower on another plant. Darwin (1862) described the variations of the pollination process that he found while exploring a wide variety of orchid species. These descriptions illustrate how two dissimilar organisms use distinct structures with specific functions to cooperate with each other (see ““Life Science Content Standards”” in National Research Council, 1996). For example, in his investigation of early purple orchid (Orchis mascula), he discovered the significance of the movement of pollinia after they become attached to an insect. Darwin observed that insects would land on the lowest flower petal and then make their way to the center of the flower, where the pollinia and stigma are located. He used the tip of a pencil to mimic the action of an insect as it reached its head into the center to obtain nectar. On withdrawing the pencil, a pollinium was stuck to it, with the stalk straight up. Darwin observed several pollinia that he removed in this fashion and found that the stalk would make a right-angle bend after about 30 seconds. He realized that if the stalk remained upright, the pollinium could not touch the stigma. If the stalk bent forward, the pollinium was correctly positioned to transfer pollen to the stigma. Darwin concluded that the 30-second delay in bending was sufficient to allow the insect time to leave the flower before the pollinium was in position to transfer pollen, thus avoiding self-pollination (Darwin, 1862).
Darwin's study of Mormodes ignea provides a good example of the importance of considering all observations of a subject before drawing conclusions (see ““Science as Inquiry Standards”” in National Research Council, 1996). This species belongs to a group of orchids that eject their pollinia when an insect enters the flower and presses a trigger. Darwin had found that the trigger was a structure located between the stigma and the pollinia. He assumed that insects would enter the lower part of the flower to reach the trigger. If they hit it while in that part of the flower, the ejected pollinia could not land on them. Darwin (1862:249) wrote, ““I had given up the case as hopeless, until, summing up my observations, the explanation presently to be given, and subsequently proved by repeated experiments to be correct, suddenly occurred to me.”” As he reviewed his observations, he realized that the landing petal, which was in a ““strange position”” that he had assumed was ““for no good purpose,”” was actually positioned to guide insects to the top of the flower to reach the trigger. If insects followed the guide to the trigger, they would be in place to receive the ejected pollinia.
Darwin began his orchid research with native British orchids. As time went by, he also looked at the flowers of exotic orchids that were sent to him by a variety of individuals from their greenhouses or from the Royal Botanic Gardens at Kew. In January 1862, he received some flowers of Angraecum sesquipedale (the Madagascar star orchid or Darwin's orchid), a native of Madagascar. Darwin's study of this orchid led to one of the more well-known stories about him. The nectar of this orchid is located at the base of an impressively long spur. Drawing on his theory of natural selection, Darwin predicted that a moth with a proboscis 10——11 inches long must exist, because only such a creature could both reach the nectar and be positioned while doing so to collect or deliver the pollinia (Darwin, 1862). In most accounts of this tale, the discovery of the moth, Xanthopan morgani praedicta (named in honor of Darwin's prediction), in 1903 in Madagascar by Rothschild and Jordan is the triumphant ending (Kritsky, 1991).
Another way to present the tale of the orchid and the predicted moth involves the co-discoverer of evolution by natural selection, Alfred Russel Wallace (Kritsky, 1991). In 1867, George Campbell, the Duke of Argyll, wrote The Reign of Law. In this book, he used Darwin's descriptions of the fit of orchids and their pollinators to serve as proof of the existence of God rather than of natural selection. Argyll also mocked Darwin's prediction about the pollinator of A. sesquipedale (Argyll, 1867). Wallace (1867) wrote a rebuttal, Creation by Law, defending both the prediction and the theory of natural selection on which it was based. The rebuttal, which was accompanied by an illustration of the hypothetical moth, earned Wallace Darwin's heartfelt gratitude (Marchant, 1975). This version of the tale of Darwin's orchid provides a lesson in the development of the theory of natural selection by showing the kind of challenges to the theory that were made in Darwin's day and how he and his colleagues responded to these challenges (see ““History and Nature of Science Standards”” in National Research Council, 1996).
Reproductive Strategies in Flowering Plants
One topic to be addressed when covering sexual reproduction in plants (see ““Life Science Standards”” in National Research Council, 1996) is how plants avoid self-fertilization. Darwin's interest in pollen transfer from a flower on one plant to a flower on a different plant went hand-in-hand with his conviction regarding the benefit of outcrossing over inbreeding. He ended the orchid book with ““Nature thus tells us, in the most emphatic manner, that she abhors perpetual self-fertilisation”” (Darwin, 1862: p. 359). Different species of flowering plants employ one or more strategies that promote outcrossing. Some species are self-incompatible and reject their own pollen. Others have flowers that release their pollen before the stigma is receptive, or vice versa. Still others have male (staminate) flowers on one plant and female (pistillate) flowers on another. In The Different Forms of Flowers on Plants of the Same Species, Darwin considered the role of flower structure in promoting outcrossing. In species that exhibit heterostyly, the flowers come in two forms, ““pin”” flowers with long styles (the portion of the pistil between the stigma and the ovary) and short stamens and ““thrum”” flowers with short styles and long stamens (Darwin, 1986).
Darwin's interest in the role of insect pollinators prompted him to consider where pollen would stick on an insect's body when it came to collect nectar. Pollen from a pin flower should be in one position on the insect and pollen from a thrum flower in another. He went out to his garden and caught three different insect species that were visiting the flowers of Primula veris (cowslip). He then examined the insects and the pollen they were carrying with a microscope. Because the pollen grains of the two flower types are different sizes, he could tell whether a patch of pollen was from a pin flower or a thrum flower. His prediction about pollen location was confirmed when he found pin pollen in one place and thrum pollen in another on each insect (Darwin, 1986).
Darwin then did four types of crosses with the two forms of 70 P. veris flowers: pollen from pin flowers onto the stigma of a pin flower, thrum pollen to thrum stigma, thrum pollen to pin stigma, and pin pollen to thrum stigma. Seed was produced in 31% of the crosses between same-form flowers. By contrast, 71% of the crosses between different-form flowers set seed (Darwin, 1986). Darwin concluded that because crosses between different flower forms produced more seed than crosses between like flower forms, ““the benefit which heterostyled dimorphic plants derive from the existence of the two forms is sufficiently obvious, namely, the intercrossing of distinct plants being thus ensured”” (Darwin, 1986: p. 30). When he reflected on this discovery in his autobiography, he wrote, ““I do not think anything in my scientific life has given me so much satisfaction as making out the meaning of the structure of these plants”” (Darwin & Barlow, 1958: p. 134).
Darwin closed The Different Forms of Flowers with a consideration of flowers that do not open to admit pollinators and thus self-fertilize. He considered some of the advantages of this strategy, including reduced pollen production due to increased pollination efficiency, less pollen lost to insects or weather, and smaller flowers (Darwin, 1986). He was concerned, however, about the deleterious effects of continued self-fertilization and noted in his autobiography that he wished he had paid more attention to adaptations for self-fertilization (Darwin & Barlow, 1958). He had come across one such adaptation while studying orchids. The flowers of the bee orchid, Ophrys apifera, have pollinia that hang freely instead of being tucked inside the flower. Darwin did an experiment to show that wind is sufficient to move the dangling pollinia into contact with the stigma; no insect agent is required. He covered a plant with a net to allow the wind to have access to the flowers while excluding insects. The flowers on this plant set seed; the flowers of a plant kept in a still room did not (Darwin, 1862). So convinced was Darwin that generations of inbreeding would eventually lead to the extinction of this species that he even remarked that he wished ““to live a few thousand years”” in order to see it (Darwin, 1896: p. 450).
Darwin's knowledge and appreciation of insects contributed to his extensive studies on pollination. He understood the structure of insects, had observed their behavior, knew their movement patterns, and could readily identify insects in the field (Remington & Remington, 1961). His familiarity with insects was also useful when he studied carnivorous plants. The leaves of these plants are adapted to absorb small molecules, which they obtain by luring, trapping, and/or digesting prey (Givnish et al., 1984). The adaptations provide many examples of structural and functional specialization in a single organ, the leaf (see ““Life Science Standards”” in National Research Council, 1996).
The first carnivorous plant that Darwin examined was the sundew (Drosera rotundifolia), which caught his attention in the summer of 1860 (Darwin & Barlow, 1958; Browne, 2002). The leaves of the sundew are covered with tall hairs that are tipped with sticky glands. On that day in 1860, Darwin randomly collected a dozen plants and proceeded to count the leaves that had captured insects. He concluded that ““as this plant is extremely common in some districts, the number of insects thus annually slaughtered must be prodigious”” (Darwin, 1900: p. 2). He continued that ““it was soon evident that Drosera was excellently adapted for the special purpose of catching insects, so that the subject seemed well worthy of investigation”” (C. Darwin, 1900: p. 2).
Over the next 15 years, Darwin would turn his attention to carnivorous plants when he needed a break from writing. The first 10 chapters of Insectivorous Plants (Darwin, 1900) present the sundew experiments designed to determine what types of substances triggered movement of the sticky trichomes to wrap around prey and stimulated secretion of the digestive fluid. He came to realize that only nitrogen-containing substances, such as high-protein foods like meat, egg white, milk, and peas, elicited the full carnivorous response.
Darwin also examined the nature of the digestive fluid secreted by the leaves. His observations provide an example of the effect of pH on enzyme activity in a natural system (see ““Life Science Standards”” in National Research Council, 1996). He tested the digestive fluid of the sundew with litmus paper and found it to be acidic. If he added alkali to the fluid, digestion stopped. If he then added acid, digestion resumed. Darwin observed that acid alone did not digest the substances. A ““ferment,”” which we would now call a ““protease”” (an enzyme that breaks down proteins to amino acids), was also required (Darwin, 1900).
Likening sundews to animals, Darwin tried various poisons that impair animals to see if they would block any part of the response in sundews. He was surprised to see that a solution of cobra venom actually stimulated it (Darwin, 1900). This response that stumped Darwin provides an opportunity to apply new knowledge to solve an old problem (see ““Science as Inquiry Standards”” in National Research Council, 1996). Now that we know that cobra venom is a protein, we can understand why applying it to a sundew leaf would trigger the carnivorous response.
In Insectivorous Plants, Darwin (1900) made reference numerous times to the pollen grains, leaf fragments, and seeds found on the sticky leaves of sundews and butterworts (Pinguicula). He tested to see if these substances were digested and absorbed and found that they were. He concluded that these plants get at least some of their resources from plant matter. Barry Rice (2007), who maintains an extensive Web site on carnivorous plants, is sometimes asked if there are any vegetarian carnivorous plants. His examples include butterworts that digest and absorb pollen grains that land on their leaves as well as a tropical pitcher plant (Nepenthes ampullaria) that collects leaf debris in its pitchers and various bladderworts (Utricularia), aquatic plants that sometimes catch algae and in some cases seem to maintain algae in their bladders in a mutualism.
Darwin also studied the Venus flytrap (Dionaea muscipula). His report on this plant stands out because it illustrates his thought process (see ““Science as Inquiry Standards”” in National Research Council, 1996) as he determined what adaptive value a feature might have for an individual organism. The leaf of the flytrap is edged with spine-like projections, and he was curious as to their usefulness. As he watched a leaf close around its prey, he observed that these spiny projections form bars like those of a cage. He surmised that small insects would be able to escape before the leaf closed completely and the plant committed resources to the full digestion and absorption process. Larger, more worthwhile prey would be unable to get out. He made an analogy to a fishing net with a large mesh that would allow small fish to escape while keeping large fish ensnared. He wanted to know if he was correct about Venus flytraps catching insects under natural conditions. Because the Venus flytrap is not native to England, he asked a North American naturalist for help in observing insects caught by plants growing in the wild in North Carolina. The naturalist mailed Darwin some closed leaves containing prey so that Darwin could see and measure the insects for himself. He concluded that his proposal about the function of the spiny projections on the edges of the leaves was correct (Darwin, 1900).
In the conclusion of Insectivorous Plants, Darwin put carnivory in the larger context of the methods by which plants obtain resources. The ““ordinary plants”” absorb minerals from the soil with their roots. Among the carnivores, he recognized two groups. Although both ensnare their prey and absorb the digested material, one group digests the prey directly, whereas the other relies on microbial flora to do the digestion. For completeness, he mentioned parasitic plants and mycotrophic plants, which rely on mycorrhizal fungi to pass them materials from a woody plant. This summary supports the recurring theme of all of Darwin's investigations, that a variety of adaptations are found among diverse organisms to accomplish the same task (Darwin, 1900).
Darwin's approach to studying a problem was that of a naturalist. He considered the needs of the whole organism in the context of its environment as he sought to understand the purpose of the adaptations he observed in specific plants. The stories presented here emphasize a specific organism in a specific situation. Although a student may not recall the details, anecdotes of this type increase engagement and comfort with the material (Kreps Frisch & Saunders, 2008). Also, just remembering that a story accompanied the explanation of a concept seems to help students recall information on exams (Kreps Frisch & Saunders, 2008).
Many authors have written of Darwin's botany, pointing out its importance as experimental work to provide evidence in support of his theory of natural selection (F. Darwin, 1899; Heslop-Harrison, 1958; Ornduff, 1984; Kohn, 2005). Darwin himself appreciated this point, for he wrote to T. H. Huxley in 1880 that ““plants are splendid for making one believe in Natural Selection, as will and consciousness are excluded”” (F. Darwin & Seward, 1903: p. 387). Particularly strong in this regard are the three studies that Darwin took up in the wake of the publication of On the Origin of Species: pollination, heterostyly, and carnivorous plants (Kohn, 2005), studies that originated as investigations of plants he saw while out for a walk.
I thank JaNae Kinikin for her tireless editing of multiple drafts of the manuscript.