Darwin's Backyard

by James T. Costa

Flower of yellow sage (Salvia glutinosa). No. 1 shows a male-stage flower with the immature short stigma (st) and process at the base of the fertile anther (a2). No. 2 shows a female-stage flower, with an elongated and receptive stigma (st). A fused fertile + sterile stamen is shown in No. 3, showing the ripe anther (a1) and sterile anther reduced as a spur or process (a2). The stamen in No. 4 is poised to deposit pollen; when a visiting bee (dotted line) pushes on the spur, the fertile anther is tipped down by lever action. From Ray Lankester’s Science From an Easy Chair: A Second Series (New York, Henry Holt & Co., 1913), p. 4.

  3. Mountain laurel (Kalmia latifolia)

  The showy flowering shrub mountain laurel (Kalmia latifolia), a relative of rhododendron native to eastern North America and now widely planted, presents a nice example of spring-loaded stamens. Mountain laurel is prized for its showy clusters of pinkish-white flowers, each about the size of a nickel. Peer more closely and you’ll see that the flowers are beautifully sculpted bowls, the filament of each stamen gracefully arched back, the anthers tucked securely into little puckered compartments or pouches along the bowl’s edge.

  The flower is a pollen-showering trap waiting to spring on unwary bumblebees as they try to get to the nectaries. Their weight slightly deforms the bowl-shaped corolla, releasing stamens. They spring up, showering their pollen on the bee. You can simulate this and trip some stamens yourself by carefully deforming the shape of a flower by gently pushing on opposite sides of the inner edge of the corolla bowl.

  Mountain laurel (Kalmia latifolia) flower, with 9 reflexed and 1 sprung stamen. Drawing by Leslie C. Costa.

  4. Barberry (Berberis or Mahonia)

  A different form of catapulting stamens is found in the barberry genus Berberis, also classified as Mahonia by some authorities. Common ornamentals include the Mexican barberry (B. trifoliata), Oregon grape (B. aquifolium—Oregon’s state flower), common (European) barberry (B. vulgaris), and Japanese barberry (B. thunbergii). These plants produce clusters of small pale white or yellow six-petaled flowers. Be careful handing them: they often have small thorns along the stem, and in some species the leaves are stiff and armed with sharp points like hollies. The flowers can look doubled since the sepals are about as well developed as the petals. Alongside each petal stands a stamen, arrayed around the single central pistil, which often has a mushroom-shaped stigma. Barberry stamens are “irritable” (technically termed seismonastic)—sensitive to touch. Nectar organs are found at the base of each stamen. When an insect comes probing, contact causes the stamen to spring toward the pistil. After about 20 minutes the stamens are slowly retracted, ready to spring anew—an indication that the movement is caused by rapid change in internal (turgor) pressure in certain cells. It’s easy to trip the stamens yourself, even one at a time: just gently probe the filament (stalk) of the stamens with a toothpick or camel-hair brush tip and they will spring forward. You can time their refractory period: how long does it take for them to return to the “armed” position?

  Barberry (Berberis) flower cross-sections showing four of the six stamens and the central pistil. (Left) Open “armed” position of stamens. (Right) Tripped stamens have moved toward the central stigma. Drawing by Leslie C. Costa.

  5. Common foxglove (Digitalis purpurea)

  The uppermost flowers in a spike will be male-phase, while the lowermost flowers will be female. Select a flower and, with the craft knife or razor blade, carefully slice the flower longitudinally slightly off-center to leave the pistil in place, as pictured. Are stamens or pistils held over the gangway? Does that correspond to the flower’s position along the spike? The long style with the bifid (forked) stigma is positioned along the middle of the corolla tube (gangway) in the female stage, but in male-phase flowers it is held out of the way along the roof of the corolla tube. When the anthers mature they move to the gangway, where they can easily shower bees with pollen. Feel the inside lower surface of the flower. Darwin described how the floor the flower is carpeted with coarse hairs. One of Darwin’s correspondents suggested that the hairs might provide bees with a foothold as they clamber up the corolla tube.

  Cross-section of a foxglove flower (Digitalis), showing the position of the stamens and pistil along the upper part of the tubular flower and the bee “gangway” along the spotted lower part. Drawing by Leslie C. Costa.

  II. Exploring Flower Morphs

  One of Darwin’s greatest contributions to botany was his discovery of the significance of heterostyly—flower morphs bearing stamens and pistils of very different length. These morphs ensure outcrossing. Here we’ll observe heterostyly in some familiar plants—once you know what to look for, you will find that this phenomenon is far more common than you might have realized.

  A. Materials

  • Obtain one or more plants with dimorphic flowers (two morphs, long-styled pin and short-styled thrum): primrose (Primula spp.), lungwort (Pulmonaria spp.), forsythia (Forsythia spp.), and yellow Jessamine (Gelsemium sempervirens) are readily available from garden centers and nurseries.

  • Obtain one or more plants with trimorphic flowers (three morphs: long-, medium-, and short-styled): purple loosestrife (Lythrum salicaria) and the aquatic pickerelweed (Pontederia cordata).

  • Craft knife or razor blade

  • Forceps or tweezers

  • Ruler

  • Magnifying lens and/or dissecting microscope

  B. Procedure

  1. In each of these genera the flowers have a corolla tube, and since the stamens and pistil typically do not extend beyond the tube a careful dissection of the flowers will be necessary: gently cut along the corolla tube of one or more dimorphic flower with the knife or razor blade and peel back to expose the stamens and pistil within.

  2. Is your flower pin or thrum? If you have access to both, measure the length of the stamens and pistils in each morph and compare.

  Primrose (Primula) flower morphs: thrum (left) with short style and long anthers; pin (right) with a long style and short anthers. Drawing by Leslie C. Costa.

  3. Note that a given individual will have pin or thrum flowers, never both.

  4. Repeat, carefully cutting along the corolla tube of one or more trimorphic flower to expose the stamens and pistil within. Is your flower long styled, medium styled, or short styled?

  5. Carefully remove each stamen at the base with the forceps or knife and measure the length. Ideally, repeat with several flowers to increase the stamen sample size. What do you notice about the distribution of stamen lengths?

  See also:

  “Floral Dimorphism” at the Darwin Correspondence Project: www.darwinproject.ac.uk/learning/universities/getting-know-darwins-science/floral-dimorphism.

  7

  It Bears on Design

  It must have struck many as odd that the epochal work On the Origin of Species—a seismic book, quintessentially big picture with its bold expansive theory of species change and provocative philosophical implications—was followed 2½ years later by a slender volume meticulously detailing the pollination of orchids. Had Darwin gone mad? If so there was method to his madness, though it’s equally true that it wasn’t his original plan. In January 1860 he had been home a month from the hydropathic spa at Ilkley, Yorkshire, where he had taken refuge during the publication of the Origin. The battle lines were being drawn for and against his theory, and naturalists and clergy alike (often one and the same) were found on both sides of the question. Darwin’s intention now was to write a three-part series of volumes expanding on the key arguments of the Origin. He hoped to make good on his promise to “show that I have not been quite so rash as many suppose,”1 as he put it in a letter to Charles Lyell that spring. He had to get to work right away. And he did, except for the interruptions. Of course, the interruptions were in no small part of his own doing, and as we shall see, at one phase orchids were the main culprit.

  In the course of Darwin’s investigations into flower structure and pollination, a line of research begun in the 1840s, he s
tudied orchids off and on in the late 1850s and into 1860, performing experiments to look at fertilization success and seed set. Or tried to: an experiment book entry dated July 2, 1857, records an ill-fated experiment cross-pollinating bee orchids, ending with a hastily scrawled note in pencil, “All Killed by Cows.”2 He had better luck the following year. It was only a matter of time before he was drawn in more deeply by these beguiling plants, as a number of lovely species grew locally. In fact, one of his and Emma’s favorite retreats was a peaceful site teeming with these botanical beauties just a half-mile from his home, high on a hillside of wood and meadow overlooking the fertile Cudham Valley. “Orchis Bank” was the family’s private name for Downe Bank. Many years later Etty recalled the site fondly: “Just on the other side of the narrow steep little lane leading to the village of Cudham, perched high above the valley, was ‘Orchis Bank’ where bee, fly, musk and butterfly orchises grew. This was a grassy terrace under one of the shaws of old beeches, and with a quiet view across the valley, the shingled spire of Cudham church shewing above its old yews.”3

  Epipactis helleborine orchid growing at Orchis Bank, Kent, a favorite spot for picnics and botanical explorations by Darwin and family. The most widely distributed of the approximately 25 Epipactis species, this one is pollinated almost exclusively by vespid wasps. Photograph by the author.

  Now preserved by the Kent Wildlife Trust, Orchis Bank has a timeless beauty evocative of Darwin’s day—a verdant landscape dotted with wildflowers where it is easy to imagine Emma and Charles on a family picnic, some of the children exploring and others marauding, their governess in pursuit. In the spring of 1860 five children were home: the girls, Etty (17) and Bessy (13), and the three youngest boys, Franky (12), Lenny (10), and Horace (9). Darwin shared his botanical enthusiasms with them on those excursions, and encouraged a closer look at the weird and wonderful orchids to be found there: compact purple clusters of pyramidal orchid (Anacamptis pyramidalis); tall, pale helleborine (Epipactis helleborine), mysterious man orchid (Aceras anthromorpha) with its rust-colored and odd human-shaped lip; strange insect-mimicking fly and bee orchids (Ophrys insectifera and O. apifera); and more. Some nine orchid species are found at Downe Bank today, and more grew there in Darwin’s day—like the bizarre parasitic bird’s-nest orchid (Neottia nidus-avis), which Emma noted seeing only twice in the beech wood lining the bank. The orchids of Orchis Bank would soon become study subjects, but it was closer to home that Darwin made the startling discovery that got him thinking about orchids in a different way.

  The Rube-Goldbergest Flowers

  Orchids, as Darwin well knew from his Cambridge days studying botany with Henslow, were most unusual flowers. The often bizarre floral structures of this largest of plant families are such a departure from the typical, generalized, flower form that they have their own terminology: stigma, rostellum, column, labellum—the product of parts fused and elaborated to create intricate passageways and chambers, often subtended by a protruding or puckered lip. Orchid pollen is unusual too, packaged into paired sacs called pollinia (singular: pollinium) rather than being freely released by the stamens. This is a trait shared by only one other plant group, the milkweeds (Asclepiaceae), and it means that for each flower pollen transfer is all or nothing: the entire sac must be delivered. Such precious cargo is rarely entrusted to generalist couriers; a great many orchids have very specific insect pollinators whose anatomy fits the orchid like a key fits its lock. Many orchids can be pollinated by insects on the wing while others invite the unsuspecting insects inside, enticing them with intoxicating fragrances or oils in special chambers but then forcing the groggy insects to exit through one-way tunnels where the pollen packets are affixed. Others like the bee and fly orchids of Europe (Ophrys spp.) or hammer orchids of Australia (Drakea spp.) entice male insects with the lure of sex, mimicking sex pheromones or even the appearance of the female insect. Yes, of all the Rube Goldberg contrivances that flowering plants have evolved to achieve cross-fertilization, orchids must be the Rube Goldbergest of all.

  The exotic beauty and intricate structure of orchids make them irresistible, and not just to horticulturists. If roses are the flowers of love, orchids are the flowers of sex, and not necessarily of the most straightforward kind; more Rocky Horror Picture Show than Kiss Me Kate. It’s not just that the name “orchid” derives from orchis, Greek for testicle (for its paired ellipsoid tubers, a shape inevitably taken as a sign of aphrodisiacal properties). No, it’s the flowers that have long excited admiration and passion, with a whiff of the dangerous: what other flower could inspire frenzied collectors, brooding comic book characters, artists, and escort agencies? Only orchids could lie at the center of that Venn diagram.

  Long before orchids loomed large in Georgia O’Keefe’s art or inspired the dark superheroine Black Orchid of DC Comics, these plants drove Victorian collectors to a form of madness called “orchidelirium.” Chambers’ Journal of Popular Literature, Science, and Art for April 28, 1894, ran a story recounting the trials, tribulations, murder, and mayhem connected with “The Romance of Orchid-Collecting,” perhaps inspiring H. G. Wells to write his short story “The Flowering of the Strange Orchid” a few years later—a macabre tale of a mysterious tropical orchid that proves to possess a deadly combination of irresistible beauty, intoxicating perfume, and a thirst for human blood. This murderous orchid would have been the stuff of nightmares for Oxford artist and critic John Ruskin, who had died 5 years before Wells’s story appeared in 1905. In the 1870s and 1880s the perhaps by then slightly deranged Ruskin had already railed against orchids, a “strange” order, as he put it in his scheme of “moral botany” published as Proserpina: Studies of Wayside Flowers in 1875. Orchids seem more wayward than wayside to Ruskin. Of both orchids and the whole of Darwin’s investigations into the sex lives of plants, Ruskin declared that “with these obscene processes and prurient apparitions the gentle and happy scholar of flowers has nothing whatever to do. I am amazed and saddened . . . by finding how much that is abominable may be discovered by an ill-taught curiosity.”4

  Ruskin was railing against modernity, scientific inquiry being little more than “ill-taught curiosity” to him. It was true enough that the discovery of the evolutionary process by Darwin and Wallace led to new insights into the natural world at once exhilarating and frightening to many of their contemporaries. It’s difficult, perhaps, for a modern reader to realize that it was not so long ago that wildly different assumptions about the natural world prevailed: moralizing from nature was standard fare from Aesop onward. The lives and behavior of animals played out as so many parables, and plants presented similar lessons in a perfectly designed world. The beautiful and fragrant blossoms were for our benefit, and it was the height of absurdity if not perversity to hold that such things have a sex life. By the time of Linnaeus in the eighteenth century plant sexuality was becoming better understood by naturalists, even as some felt that botany was an unsuitable subject for young ladies to pursue as a result. But it is also true that even well into the nineteenth century the key role of insects in cross-pollination was not widely accepted, let alone the idea of flowers as sexual advertisements.

  In rebelling against the new botany, Ruskin came up with a newer botany in Proserpina, replacing Linnean binomials with ones of his own device based on traits reflecting the supposed virtues (or not) of each plant. Orchids were renamed order “Ophryds,” and most fell into the dubious suborder of “Contorta” (for their twisted petioles, but also for their twisted habit of growing mainly in “torn and irregular ground, under alternations of unwholesome heat and shade, and among swarms of nasty insects”5). It may not be coincidental that the orchid Ruskin used to illustrate the group as a whole was the one that Darwin first studied, and the first species illustrated in his 1862 orchid treatise: the early purple orchid, Orchis mascula in the Linnean system but renamed by Ruskin Contorta purpurea.

  Beautiful Contrivances

  Darwin was on his customary stroll about the
sandwalk one day in May 1860 when he noticed some early purple orchids in bloom. Ever the opportunistic experimentalist, he decided to perform an insect-exclusion experiment, covering some of them and leaving others exposed to visiting insects. In the course of these experiments Darwin poked and probed the purple flowers as an insect might. To his surprise he triggered the flower’s pollen release mechanism: retracting his probe, two tiny stalked yellow sacs, the pollinia, were firmly affixed. That’s when he first witnessed a decidedly odd thing: the stalked sacs came out of the flower standing straight up, sometimes singly and sometimes both, like diminutive horns, but within seconds they bent forward nearly ninety degrees, like taking a bow. I imagine Darwin sitting bolt upright and peering at his unexpected catch like a serene fisherman suddenly jolted into action when the line jerks. Was it a fluke, or a maybe a defect? He probed another flower and out the pollinia came, again first upright and then bowing forward and holding that position. He was familiar with the “irritability” found in some flowers, with their spring-loaded stamens, but this was another form of irritability altogether—two forms in fact. First the rostellum, a thin, flexible, cup-like membrane in which the pollinia are nestled, is spring-loaded: when ever-so-slightly touched as a probing insect might, the rostellum ruptures, freeing the pollinia with their stalks firmly attached to small sticky discs. The discs immediately contact that probing insect—or pencil—and in the few seconds it takes the insect to back out of the flower they are cemented firmly in place. Seconds more and the next wonderful expression of irritability is on display: certain precisely positioned cells found on the lower front surface of the stalks suddenly deflate, causing the stalks to collapse in that direction, rather like a felled tree tipping in the precise direction of a skillfully placed notch. Darwin immediately realized the significance of this trick: when the pollen-bearing insect visits another orchid flower, pollinia pointing upward would fail to contact the stigma and pollinate the flower. But by tipping forward at 90º, the pollen sac is ready for action: it will be rammed onto the stigma as the insect probes the new flower. The precision of the mechanism enthralled him: it was “a beautiful contrivance” that took plant cross-fertilization to a whole new level.