American Journal of Botany 96(12): 2128–2154. 2009. “THE ORCHIDS HAVE BEEN A SPLENDID SPORT”—AN ALTERNATIVE LOOK AT CHARLES DARWIN’S CONTRIBUTION TO ORCHID BIOLOGY1 Tim Wing Yam,2,5 Joseph Arditti,3,5 and Kenneth M. Cameron4,5 2 Singapore Botanic Gardens, Cluny Road, Singapore, Republic of Singapore; 3 Department of Developmental and Cell Biology, University of California, Irvine, USA; and 4 Wisconsin State Herbarium & Department of Botany, University of Wisconsin, Madison, Wisconsin 53706 USA Charles Darwin’s work with orchids and his thoughts about them are of great interest and not a little pride for those who are interested in these plants, but they are generally less well known than some of his other studies and ideas. Much has been published on what led to his other books and views. However, there is a paucity of information in the general literature on how Darwin’s orchid book came about. This review will describe how The Various Contrivances by Which Orchids Are Fertilised by Insects came into being and will discuss the taxonomy of the orchids he studied. It also will concentrate on some of the less well-known aspects of Darwin’s work and observations on orchids—namely, rostellum, seeds and their germination, pollination effects, and resupination— and their influence on subsequent investigators, plant physiology, and orchid science. Key words: discovery of auxin; Fritz Müller; John Murray; pollination effects; orchid flowers; orchid seeds; resupination; rostellum. According to an easily accessible essay on the World Wide Web (Anonymous, 2008), “for July and August 1861 [Darwin and his wife] took their daughter Henrietta to the seaside village of Torquay. Darwin was diverted by spending hours considering the variety of wild orchids to be found along the shore. On returning home he looked for them near Downe [sic],6 and found a beautiful spot teeming with orchids….” This is worth citing as an example of incorrect information, posted on an easily accessible source, which could become an urban legend. Actually, Darwin (Fig. 1F, 2A, B, G) finished the manuscript, which became The Various Contrivances by Which Orchids Are Fertilised by Insects (TVC), “a few days” before 24 September 1861, when he wrote to his friend Joseph Dalton Hooker (J.D.H.; 1817–1911; Fig. 2C), director of The Royal Botanic Gardens, Kew, from 1865 until 1885. “When I finished a few days ago my Orchis paper, which turns out 140 1 folio pages!!7 and8 thought of the expense of woodcuts, I said to myself I will offer the Lin. Socy9 to withdraw it and publish it as a pamphlet. It then flashed on me that perhaps Murray would publish it…” (Darwin, 1861a). Darwin, whose unhurried and painstaking working habits are well known, could not have carried out as much research as he did and handwritten a 140-page paper in about a month and a half. In fact, he collected the information “during 20 years” (Darwin, 1861b), having started his work on orchids in the summer of 1838 or 1839 (footnote 2 in Darwin, 1861c). In his autobiography, Darwin wrote the following: On May 15th, 1862, my little book on the ‘Fertilisation of Orchids,’ which cost me ten months’ work, was published; most of the facts had been slowly accumulated during several previous years. During the summer of 1839, and, I believe, during the previous summer, I was led to attend to the cross-fertilisation of flowers by the aid of insects, from having come to the conclusion in my speculations on the origin of species, that crossing played an important part in keeping specific forms constant. I attended to the subject more or less during every subsequent summer; and my interest in it was greatly enhanced by having procured and read in November 1841, through the advice of Robert Brown, a copy of C. K. Sprengel’s [1750–1816; Fig. 3B] wonderful book,10 ‘Das entdeckte Geheimniss der Natur’ [Fig. 3A]. For some years before 1862 I had specially attended to the fertilisation of our British orchids; and it seemed to me the best plan is to prepare as complete a treatise on this group of plants as Manuscript received 3 May 2009; revision accepted 14 September 2009. Darwin’s (Fig. 1A–E) book and work on orchids deal mainly with pollination but also touch on several other aspects of this family. The pollination aspect of his orchid research has received the lion’s share of attention (Fay and Chase, Annals of Botany 2009; 104: 359-364). Other parts have received limited consideration. Therefore and because the other aspects are less well known, we chose to concentrate on them. Dedication by J.A.: For Dr. Wolfgang and Mrs. Heidi Zierau, University of Muenster, Germany, Jonathan’s and my friends for a quarter of a century. 5 Author for correspondence (YAM_Tim_Wing@nparks.gov.sg). Dr. Yam is sometimes in the field. If a quick reply is required, please also contact the other authors (jarditti@uci.edu [Professor Emeritus] or kmcameron@wisc.edu). 6 Darwin’s residence was named Down (Fig. 2D). The town near which it is located is Downe. 7 It is necessary to keep in mind that in those days these were handwritten pages. 8 Darwin used a symbol for “and.” doi:10.3732/ajb.0900122 9 Darwin used this abbreviation for “Society.” Sprengel was rector at Spandau, where he became so devoted to botany that he neglected his duties and was removed from the parish (Singer, 1959). He moved to Berlin and led a solitary and impoverished life. His book (Sprengel, 1793), described as a “work of genius” long after his death (Singer, 1959), was not received well during his lifetime. This depressed him to the point of abandoning botany for philology. 2128 10 December 2009] Yam et al.—Darwin and his orchids 2129 Fig. 1. The Various Contrivances by Which Orchids Are Fertilised by Insects. (A, B) First edition book and front page. (C) British second edition (courtesy Jeffrey Makala, C. Warren Irvin, Jr., Collection of Charles Darwin and Darwiniana, Thomas Cooper Library, University of South Carolina, and Sandra and Philip Murphy). (D) American second edition book and (E) the title page from a later printing by John Murray in London. (F) Charles Darwin, 1809–1882 (Anonymous, 1880). (G) John Murray, Darwin’s publisher (courtesy John R. Murray VII, 50 Albemarle Street, London W1S 4BD). well as I could, rather than to utilize the great mass of matter which I had slowly collected with respect to other plants (Darwin, 1958). Darwin “was probably attracted to the study of Orchids by the fact that several kinds are common near Down” [Fig. 2D] (Darwin, 1958). He devoted “a good deal of his attention” to orchids in 1860 and part of the summer and all of the autumn of 1861 (Darwin, 1958). According to his son Francis, Darwin “evidently considered himself idle for ‘wasting time’ on Orchids” (Darwin, 1958) because he wrote, “I feel quite guilty in trespassing on [variation under domestication] and not sticking to varieties of the confounded cocks, hens and ducks” (Darwin, 1862b; Darwin, 1958). He also “resolutely against my inclination [emphasis as in the original], put them [the orchids] away a month ago…for I am convinced that I ought to work on Variation & not [busy] myself with interludes” (Darwin, 1860e). But, he did “trespass” and went back to the “interlude” despite considering himself “rather idle, that I have been indulging in some extraneous work, and am going to publish a little work on the Fertilization of Orchids by Insects” (Darwin, 1861m) probably because the orchid pleased him (Darwin, 1880a) and : • “you cannot conceive how the Orchids have delighted me” (Darwin [to J. D. Hooker], 1861e), • of his request of J. D. Hooker to “Have pity on me & let me write once again on Orchids for I am in transport of admiration” (Darwin, 1860a), • for him, “the orchids are more play than real work” (Darwin, 1861g), • “the orchids have been a splendid sport” (Darwin, 1862b), 2130 American Journal of Botany [Vol. 96 Fig. 2. Charles Darwin (G), his handwriting (A), signature (B), home, Down House (D), and correspondents (A, B, D, G; from http://en.wikipedia.org/ wiki/Charles_Darwin; home, from Oscar Boleman at http://en.wikipedia.org/wiki/Down_House). (C) Joseph Dalton Hooker, 1817–1911 (courtesy Dan Weinstock, M.D., Geneva, New York). (E) Johann Friedrich Theodor “Fritz” Müller, 1821–1897, as he might have looked while studying and/or collecting orchids in Brazilian forests (Möller, 1921). (F) Sir Charles Lyell, 1797–1875 (Wikipedia [http://en.wikipedia.org/wiki/Charles_Lyell]). • “Orchids have interested me more than almost anything in my life” (Darwin, 1861q),11 • to Darwin, the orchids were “wonderful creatures” (Darwin, 1880a), • he could not “fancy anything more perfect than the many curious contrivances” of orchids (Darwin, 1861c), • in a comparison to woodpeckers, he stated: “Talk of adaptation in woodpeckers–some of the Orchids beat it” (Darwin, 1860b), • “the contrivances of Orchids beat, I think, any animal” (Darwin, 1861d), 11 This seems to have changed slightly later in Darwin’s life because in 1878 he wrote Herman Müller, “nothing in my life has ever interested me more than the fertilization of such plants as Primula and Lythrum [neither an orchid], or again Anacamptis or Listera [both orchids]” (Darwin, 1878). • “the beauty of the adaptations of parts seems to me unparalleled” (Darwin, 1861f), • he found perfection in the many contrivances in orchids (Darwin, 1861h), • orchids were his “hobby horse” (Darwin, 1861i), • he was “sillily & very idly interested in them” (Darwin, 1860d), and • not the least, “this subject is a passion with me” (Darwin, 1861b). What Darwin started in July and August 1861 was the writing of a manuscript he initially envisioned as a paper to be published in one of the Linnean Society journals (footnote 1 in Darwin, 1861c) and eventually offered to John Murray as TVC. At present, TVC is considered to be a classic, but Darwin had his doubts about it and was concerned about being fair to his December 2009] Yam et al.—Darwin and his orchids 2131 Fig. 3. Scientists who influenced, interacted with, and/or corresponded with Charles Darwin. (A, B) Conrad Sprengel (Tilanus, 1925) and his book. (C) Johann Friedrich Theodor “Fritz” Müller, 1821–1897, dressed formally (Möller, 1921). (D) Robert Brown, 1773–1858 (http://en.wikipedia.org/wiki/ Robert_Brown_%28botanist%29). (E) John Scott, 1838–1880 (originally accessed at http://www.denholmvillage.co.uk/photos/scott.jpg). publisher. He wrote to J.D.H., “It is a risk and Heaven knows whether it will not be a dead failure; but I have not deceived Murray [Fig. 1G] and told that it would interest those alone who cared much for Natural History….It will make a very little book” (Darwin, 1861j). His letter to John Murray III is interesting because in it Darwin discusses his doubts and provides insights into his approach to publishing and his business acumen: My dear Sir Will you have the kindness to give me your opinion, which I shall implicitly follow.—I have just finished a very long paper intended for Linn. Socy. (the title is enclosed) & yesterday for the first time it occurred to me that possibly [emphasis here and elsewhere in this letter as in the original] it might be worth publishing separately, which would save me trouble & delay.—The facts are new & have been collected during 20 yr & strike me as curious. Like a Bridge-water Treatise12 the chief object is to show the perfection of the many contrivances in Orchids. The subject of propagation is interesting to most people, & is treated in my paper so that any woman13 could read it. Parts are dry 12 “The Bridgewater Treatises is the collective name given to eight works on natural theology published between 1833 and 1836 under the terms of a bequest made to the Royal Society of London by Francis Henry Egerton, 8th Earl of Bridgewater. According to Egerton’s stipulations, each author was to write and publish a treatise ‘On the power, wisdom and goodness of God, as manifested in the creation’. Several of the volumes became classic works in the apologetic writings of natural theology . . .” (footnote in Darwin, 1861d). 13 This was written in 1861, when views about equality of genders were not the same as at present. 2132 American Journal of Botany [Vol. 96 & purely scientific: but I think my paper would interest a good many of such persons who care for Nat. History, but no others. In a few days an artist is coming here to make from 20–30 small woodcuts. experiment with fear and trembling,—not for my own sake, but for yours….. As far as I can calculate the paper contains about 29 000 words; in small page with rather open type, about 205 words to page, I calculate the matter would make 131 page[s], but with division into chapter[s] say at most 135 pages [the book had 365 pages]. So it would be a very little Book, & I believe you think very little books objectionable. I have myself great doubts on the subject…but the subject seems to me curious & interesting. I think this little volume will do good to the Origin, as it will show that I have worked hard at details, & it will, perhaps, serve [to] illustrate how natural History may be worked under the belief of the modification of Species.— I beg you not to be guided in the least to oblige me, but as far as you can judge, please give me your opinion.—If I were to publish separately, I would agree to any terms, such as half risk & half profit, or what you liked; but I would not publish on my sole risk, for to be frank, I have been told that no Publisher whatever, under such circumstances cares for success of a Book.—I would pay myself for all drawing on the wood, but not for cutting.—I shd. send rough M.S to be printed on Slips & would pay for extra corrections.—I shd require & pay for 30 or 40 copies.—But if this little Book were to fail, it occurs to me that it might injure sales of my future larger Books.—In fact I am utterly in doubt.—Please give me your impression. My dear Sir | Yours sincerely | C. Darwin (Darwin, 1861h) John Murray III thought more of the book than did Darwin: My Dear Sir I have considered attentively your very obliging & considerate note touching the publication of a little Vol. originally intended for Linnæan-Transactions—on the Fertilization of Brit. Orchids by Insects. I have no hesitation in offering to print & publish the work including Illustrations at my own sole cost & risque giving you one half of the profits of every Edition. On hearing from you I will insert the announcement on my next Quarterly List. I am | My Dear Sir | Yours very sincerely | John Murray (Murray, 1861) Darwin was grateful, ready to accept the offer, and willing to cooperate, but he still harbored doubts and was concerned for Murray’s bottom line: My dear Sir, I am very much obliged for your note & very liberal offer. I have some qualms and fears. All that I can feel sure of is that the M. S. contains many new & curious facts & I am sure the Essay would have interested me & will interest those who feel lively interest in the wonders of nature: but how far the Public will care for such minute details, I cannot at all tell. It is a bold experiment, & at worst, cannot entail much loss: as a certain amount of sale will, I think, be pretty certain. A large sale is out of the question. As far as I can judge generally the points which interest me, I find interest others; but I make the With hearty thanks | Yours very sincerely | Ch. Darwin P.S. | Do you think of a little Book with Cloth Back or Pamphlet in paper? I ask because if former, shd. you like an Orchis in Gold . . . I could get Mr Sowerby to draw one—for the woodcut, which I shall use will hardly do. Please let me have one line, if you wish for an ornament.— (Darwin, 1861k) There was additional correspondence. One letter dealt with the size of the book and an ornament (Darwin, 1861n). Another was concerned with page formatting and spelling: “I think it very good idea to match the Origin; but then I must beg you to have large type & lines wider apart, otherwise the Book will look ridiculously small; but of that hereafter. The advertisement reads well; I always spell Fertilisation & not Fertilization I will attend to outside ornament” (Darwin, 1861o). Darwin also expressed hope and concern but kept complaining: …I am half-dead with working with Mr Sowerby [according to Emma Darwin’s diary, George Bentham Sowerby, Jr., came to Down House on 07 October to prepare illustrations] at the Orchid drawings. It has been the devil’s own job (Darwin, 1861p) ….Mr Sowerby left this afternoon & comes back on Tuesday night, when I shall have 5 or 6 more very hard days’ work [Sowerby stayed until 12 October 1861, and came back to finish the job on 15 October 1861; he was paid £10 16s—about $16.50 at the rate of exchange in early 2009]. The drawings will be pretty successful; but I feel sure that my little book will be too difficult & too uniform for the Public & I almost wish I had never thought of separate publication. So I must chance it now (Darwin, 1861h). He also had second thoughts about converting his paper into a book and wrote to Charles Lyell (Fig. 2F): “I have been working terribly hard lately (for me) at Orchids. The subject is, I fear, too complex for the Public & I fear I have made a great mistake in not keeping to my first intention of sending it to Linnean Socy.; but it is now too late & I must make the best of a bad job” (Darwin, 1861r). Darwin was still fretting even when the manuscript was nearly complete (Darwin, 1862a): “I will send up to you by a servant tomorrow (Monday) the M.S of my Orchid Book, excepting the last Ch. which can be fully completed before I get first proofs. For Heavens sake be careful of the M.S. for I have no copy of three of the Chapters.—Inside the parcel you will see letter of Instructions to Messrs. Clowes [William Clowes & Sons were the printers of the book]; please read & modify as you think fit.—Urge Messrs. Clowes to print quickly, as I am incapable of changing my work & want to get on with my other Books. Now I have finished the Orchids, I can say with confidence that the M.S. contains many new & very curious facts & conclusions.—I have done my best to make the facts striking & clear. I think they will interest enthusiasts in Nat. History; but I fear will be too December 2009] Yam et al.—Darwin and his orchids difficult for general public. In short, I know not in the least, whether the Book will sell. If it prove a dead failure, I shall hold myself to a large extent responsible for having tempted you to publish with your eyes shut.—Perhaps there may be enough enthusiasts to prevent a dead failure.” Completion of the manuscript did not bring an end to Darwin’s fretting. When Murray printed 1500 copies, he wrote to him, “You are a bold man to print 1500 copies, & I hope to Heaven you will not repent it” (Darwin, 1862b). There seems to have been no end for his concerns and of what can even be described as meddling: My dear Sir I returned this morning to the Printers last page of Index. This last page is 365 so that the Book will not be quite so big as we feared [Darwin initially thought that the book would have 135 pages “at most”]. I hope you will reconsider the price: 10s seems to me high [the book was eventually priced at 9s]. About lettering the back of volume; I can think only of “Fertilisation of Orchids: Darwin,”; but this, I fear is too long [the wording on the spine is: Fertilisation (line 1) Of (line 2) Orchids (line 3) Darwin (line 4)]. Please let me hear on this head. I have got rather to think that Red Cloth would look too gaudy for a grave volume [the binding was plum-colored cloth]. You will, of course, settle what Reviewers to send to; but I may mention that the Editor of London Review would be inclined to be favorable. Also the Editors of the old “Cottage Gardener”, now called “Journal of Horticulture” are very civil to me, & I have contributed little articles for them; so that if the[y] keep any Reviewers, they would wish to review me favourably, & this Journal has very large circulation among men who cultivate Orchids. Lastly, will you be so very kind as to distribute by Post & otherwise the long enclosed list (which please keep safely): I fear the copies for Foreigners will cause you some trouble; but I beg you kindly to do the best for me.—I hope you will give me a few copies, as heretofore.—God knows whether my little book will succeed at all, but I am frightened when I think what a large Edition is published. My dear Sir | Yours very sincerely | Ch. Darwin (Darwin, 1862e) The book (Fig. 1A–B) was published on 15 May 1862 (Darwin, 1862f, i). Murray printed 1500 copies (Darwin, 1862c). By then Darwin was ready to “repent of the nine months spent on Orchids” and was “fearfully sick of” them (Darwin, 1862b). He thought that the book was not “worth . . . the 10 months it cost” him (Darwin, 1862g) and even wrote his son William Erasmus Darwin (1839–1914) on 26 April 1862, “To day, thank Heavens, I finished my accursed little orchid-Book” (Darwin, 1862d). Earlier, in a letter to Charles Lyell, he wrote that it was a mistake to not keep to his “first intention of sending it to [the] Linnean Society (Darwin, 1861r). TVC sold well for a short period—768 copies by 24 August 1862 (Darwin, 1862h), but sales slowed after that. In 1866 there were still 600 unsold copies, but Murray’s deficit was reduced to £30 (Murray, 1866). TVC sold out in 1874, and Murray settled the account in July of that year (Murray, 1874). 2133 A second edition (Fig. 1C–E) was published in 1877 (Cooke and Murray, 1877; Darwin, 1877a). This edition was also published in the United States (Darwin, 1876, 1877b). TVC was translated into French (Darwin, 1870) and German (Darwin, 1877c). The second edition went through at least seven printings by the early part of the 20th century (Darwin, 1904). A second printing of the French edition (Darwin, 1891) is identical to the first but still called “deuxième édition.” That TVC came into being is due in no small measure to Darwin’s publisher, John Murray III (Fig. 1G), who was part of a publishing dynasty that still exists at present, even as part of the Hodder Headline conglomerate. John Murray I (1745–1793), a Royal Marines officer who gave up his commission in 1768 (Murray, 1919), bought the well-established bookseller, William Sandby, and established the firm as “John Murray (successor to Mr. Sandby), Bookseller and Stationer at No. 32 . . . Fleet Street.” He published about 1000 titles, and his authors included Isaac D’Israeli (1766–1848), father of Benjamin D’Israeli (1804–1881), 1st Earl of Beaconsfield, the British Prime Minister who bought the Suez Canal for Britain (with money borrowed from Lionel de Rothschild). John Murray II (J.M.II; 1778–1843), John Murray’s son with his second wife, Hester Weems (sister of his first wife, Nancy), inherited the company in 1793 at the age of 14 and bought out his father’s partner in 1803. J.M.II became a successful publisher to authors such as Jane Austen, Lord Byron, Michael Faraday, Thomas Malthus, and Walter Scott. John Murray III (J.M.III; 1808–1892), was sent to study at Edinburgh University in 1817 at the age of 18 (Murray, 1919). There he took classes in geology, mineralogy (both of which were his favorites), political economy, chemistry, French, German, mathematics, and riding. He also did a lot of partying and met a number of interesting individuals including “‘a Mr. Audubon’ the distinguished American naturalist” (Murray, 1919). His journey home from Edinburgh was circuitous, which is indicative of his love for travel, a passion he engaged in from 1829 until 1884. He arrived in London in 1827 and joined his father’s firm, which he inherited in 1843. His travels convinced him of the need for travel books, and in 1836 he initiated the red-bound Murray Handbooks for Travelers series, which was a commercial success. On inheriting the firm in 1843, J.M.III found it to be a leading publisher in London but a company that was not very sound financially. He remedied the situation after many years of hard work (Murray, 1919). J.M.III was conservative, old fashioned, and a churchman. Therefore, publication of Darwin’s Origin of Species probably presented a problem for him. He showed it to the Rev. Whitwell Elwin (1816–1900), a man of strong opinions and the autocratic editor of the Quarterly Review, who suggested a book on pigeons instead. J.M.III also showed the manuscript to his friend George Pollock, who recommended publication. To his credit, J.M.III, a man of courage, published the book despite his devotion to his church. He published Darwin’s other books after that and seems to have been an encouraging, accommodating, generous, and patient publisher. The following episode, recounted by his son Sir John Murray IV (J.M.IV; 1851–1928), tells much about J.M.III and Charles Darwin. Charles Darwin was one of the most courteous and modest of authors. I was present when he called, in 1887, with a MS. in his hands and said, “Here is a work which has occupied me for many years and interested me much. I 2134 American Journal of Botany fear the subject of it will not attract the public, but will you publish it for me?” My father [J.M.III] replied, “It always gives me pleasure and hope to hear an author speak of his work thus. What is the subject?” “Earthworms,” said Darwin. The book was published, and six editions were called for in less than a year (Murray, 1919). J.M.IV continued with the firm and was Queen Victoria’s publisher. His successors, Sir John Murray V (1884–1967), John Murray VI (1909–1993), and John Murray VII (b. 1941), also managed the firm until it was sold to Hodder Headline in 2002. TAXONOMY OF DARWIN’S ORCHIDS The first edition of Darwin’s book on the fertilization of orchids by insects was published in 1862. It consists of 365 pages, including 34 illustrations, which are divided into seven chapters. At least 63 different orchid genera are considered in that edition. They are grouped into the major tribes of Orchidaceae as circumscribed by Lindley (1826 and 1830–1840). Most of the discussion focuses on various terrestrial orchids native to temperate Europe (e.g., Orchis, Spiranthes, Epipactis, Goodyera, Cypripedium), as would be expected, but Chapters V and VI are devoted mostly to Old and New World tropical species that were being cultivated in English glasshouses in the day. These include Cattleya, Dendrobium, Angraecum, and Catasetum, among others. With the second edition in 1877 came a significant increase in attention to foreign orchids and a slight reorganization of the book’s chapters to emphasize the contemporary classification used as a guiding framework for the text. The total number of orchid genera treated was expanded to approximately 85 (a 35% increase over the first edition), four additional illustrations were included, and the chapters were further divided from seven into nine. Listed in order, these were headed with the names of Lindley’s seven orchid tribes: I. Ophreæ; II. Ophreæ continued; III. Arethuseæ; IV. Neotteæ; V. Malaxeæ and Epidendreæ; VI. Vandeæ; VII. Vandeæ continued, Catasetidæ; VIII. Cypripedeæ and Homologies of the Flowers of Orchids; IX. Gradation of Organs, etc., and Concluding Remarks. Only one infra-tribal orchid lineage was emphasized—a clade of orchids that today are recognized as subtribe Catasetinae. Darwin erroneously referred to this group as a subfamily at the start of Chapter VII, perhaps to emphasize his unique fascination with these plants. Within the text he stated, “I have reserved for separate description one subfamily of the Vandeae, namely, Catasetidæ, which must, I think, be considered as the most remarkable of all Orchids” (p. 178). Before considering further the role of taxonomy within Darwin’s book, it is worth reviewing the state of orchid classification at that time. In 1827, Lindley published in Latin his short Orchidearum sceletos, in which the family Orchidaceae (excluding the family Apostasiaceae) was divided into eight tribes: Neottieæ, Arethuseæ, Gastrodieæ, Ophrydeæ, Vandeæ, Epidendreæ, Malaxideæ, and Cypripedieæ. Subsequently, from 1830 to 1840, Lindley published in English his revised and greatly expanded The Genera and Species of Orchidaceaous Plants, in which only seven tribes were treated but with some of these divided further into “sections” and “divisions.” For example, Malaxideae was divided into sections Pleurothalleae [Vol. 96 and Dendrobieae. Curiously, he did not divide tribe Vandeae further, so Darwin’s use of the name “Catasetidae” was apparently meant to be informal only; the modern subtribal name “Catasetinae” is attributed to Schlechter. Only 1980 species of orchid were known at the time, but Lindley was the first to admit that this number was far too low. He estimated that the world’s orchids might total as many as 6000 species. Darwin must have had a copy of Lindley’s book in his personal library. We can make this assumption because he begins Chapter I with, “Throughout the following volume I have followed, as far as I conveniently could, the arrangement of the Orchideæ given by Lindley” (p. 6). Darwin also personally thanked Dr. Lindley for sending fresh and dried specimens and for kindly helping him in “various ways” (p. 129). The same expression of gratitude was included in the first edition. It is not surprising that Darwin chose to organize his orchid book using the classification system of the day. First, it offers a logical means of dividing the book into discreet chapters, but more importantly, Darwin felt that taxonomy and classification had something to offer in terms of revealing patterns of evolution by natural selection—a topic that was still fresh in his mind, since the orchid book was his first to be published after The Origin of Species (Darwin, 1859). Classification is the subject of Chapter 13 in The Origin, the final chapter before making a recapitulation and drawing conclusions about his new theory. Within that chapter, Darwin argued the following: Naturalists, as we have seen, try to arrange the species, genera, and families in each class, on what is called the Natural System. But what is meant by this system? Some authors look at it merely as a scheme for arranging together those living objects which are most alike, and for separating those which are most unlike; . . . But many naturalists think that something more is meant by the Natural System; they believe that it reveals the plan of the Creator; but unless it be specified whether order in time or space, or both, or what else is meant by the plan of the Creator, it seems to me that nothing is thus added to our knowledge . . . I believe that something more is included, and that propinquity of descent—the only known cause of the similarity of organic beings—is the bond, hidden as it is by various degrees of modification, which is partially revealed to us by our classifications.” (Darwin, 1859, p. 413) Later, within the same chapter (p. 424), Darwin states that “every naturalist has in fact brought descent into his classification.” He uses an example from Orchidaceae to make his point: “As soon as three Orchidean forms (Monochanthus, Myanthus, and Catasetum), which had previously been ranked as three distinct genera, were known to be sometimes produced on the same spike, they were immediately included as a single species.” We can assume, therefore, that some of Darwin’s conclusions about orchids as presented in TVC were based not so much on his own observations as a scientist, but on his assumption that the orchid taxonomists (i.e., John Lindley) had some insight into the phylogeny of these plants as reflected in their system of classification. For example, in Chapter III. Arethuseæ, Darwin makes the observation that Cephalanthera “appears to me like a degraded Epipactis, a member of the Neotteae, to be described in the next chapter” (p. 80). He says this because both genera lack a rostellum and coherent pollinia. Had Lindley classified the two genera within the same tribe, one suspects that Darwin might have considered them as being December 2009] 2135 Yam et al.—Darwin and his orchids of common descent, and their shared reproductive features as plesiomorphic rather than secondarily “degraded.” Molecular phylogenetic studies show that Cephalanthera and Epipactis, together with Listera, indeed do share a common ancestor and that they are members of a grade of orchids sister to all Epidendroideae. Darwin did not consider himself a systematist, however, and so took it on good faith—as most people today still do—that the experts’ classifications must be correct! Either that or else Darwin was simply too polite to challenge Lindley publicly. There is at least one other instance in the book where Darwin graciously chose to ignore Lindley’s taxonomy. In Chapter IX he compares the flowers of Cypripedium with Apostasia, stating that the latter may not be considered an orchid by Lindley but is “ranked by Brown in the Orchidean order” (p. 248). Appendix 1 presents a list of orchid genera and species discussed in the second edition of Darwin’s book. A good deal of the nomenclature is now out of date. For example, Zootrophion atropurpureum (Lindl.) Luer was known to Darwin as Masdevallia fenestrata Lind. ex Hook. Nevertheless, it is remarkable to consider the diversity of taxa with which he was familiar, including members of all five currently recognized orchid subfamilies: apostasioid, vanilloid, cypripedioid, orchidoid, and epidendroid orchids. He had access to some of the orchids from Africa (e.g., Disa) and Australia (e.g., Pterostylis), known for their peculiar pollination biology, and was familiar with the floral morphology of at least some of the major neotropical genera. ROSTELLUM It was inevitable that Darwin would notice the rostellum (Figs. 1F–I, 5A, E–G) once he started to examine the structure of orchid flowers (Fig. 4). He observed correctly that (1) “pollen masses [Fig. 4E–G, I, K] are never retained on the rostellum except by accident” (Darwin, 1860c), (2) “viscous matter (at least the greater part) does not come out of the rostellum,” in some species (Darwin, 1860d), (3) Vanda (Fig. 4) pollinaria (Fig. 4E–G, I, K) are attached to the rostellum (Darwin, 1904), (4) there are variation and gradations in the structure of the Fig. 4. Orchid flower structure using Vanda Miss Joaquim, a natural hybrid and the National Flower of Singapore, as an example. (A) Intact flower magnified 1.13× (diameter, 74 mm). (B) Exploded flower magnified 87.7×. (C) Ventral view of gynostemium (column) magnified 3.6×. (D) Side view (approximately 45°) of ventral side of gynostemium. (E) Ventral side of gynostemium after removal of anther cap. (F) Side view of gynostemium after removal of anther cap and pollinarium. (G) Side view of longitudinal section of gynostemium. (H) Tip of gynostemium with anther cap in place. (I) Tip of gynostemium after removal of anther cap. (J) Tip of gynostemium removal of anther cap and pollinarium. (K) Pollinarium. Figure abbreviations: ac, anther cap (width at widest point, 4 mm); ds, dorsal sepal (width at widest point, 28.5 mm); gy, gynostemium (column; width at widest point, 5 mm); la, labellum (lip; width at widest point, 42 mm); lp, lateral petal (width at widest point, 39 mm); ls, lateral sepal (width at widest point, 29 mm); ov, ovary (diameter, 2 mm); pd, pedicel; po, pollinia (width of single pollinium, 1 mm); ro, rostellum; s, stigma (width, 3 mm); vi, viscidium (width at widest point, 4 mm). Vanda is used as an example here because there is a drawing of its gynostemium and rostellum in Darwin’s book on orchids (photographs by Dr. Tim Wing Yam, Singapore Botanic Gardens). 2136 [Vol. 96 American Journal of Botany rostellum in the species he observed (Darwin, 1904), and (5) in Catasetum the structure of the rostellum is “most singular” (Darwin, 1904). These observations led him to be willing to “give a good deal to know what the rostellum is, of which I have traced so many curious modifications” and to a view in one of his letters to J. D. Hooker, “I suppose it cannot be one of the stigmas; there seems to be a great tendency of two lateral stigmas to appear” (Darwin, 1861f). He changed his position on this in TVC (Darwin, 1904): “The rostellum strictly is a single organ, formed by the modification of the dorsal stigma and pistil . . .” (p. 45), “ . . . in . . .the Orchideae there are three confluent pistils; of these the dorsal one forms the rostellum . . .” (p. 149), and “There is every reason to believe that the whole of this upper stigma and not merely part, has been converted into the rostellum; for there are plenty of cases of two stigmas, but not one of three stigmatic surfaces being present in these Orchids which have a rostellum” (p. 248). This view coincides with Robert Brown’s (Fig. 3D) observation that “Orchideae have in reality three stigmata . . . two of which are . . . furnished with styles” (Fig. 4C–G), whereas the third, anterior lobe . . . manifestly differs from the other two. To this lobe . . . the pollen masses become attached . . .” (Brown, 1833). Darwin’s tracing of vascular bundles seems to have confirmed Brown’s observations (Darwin, 1861s). The concept of the third stigma becoming the rostellum was also supported by others (Vermeulen, 1959; Garay, 1960). More recent studies have shown that Brown’s and Darwin’s observations and conclusions are incorrect. The genera Coeloglossum, Dactylorchis, Galeorchis, Himantoglossum, Ophrys, Orchis, and Platanthera, among others (Vermeulen, 1955, 1959, 1966; Dressler, 1961, 1981; van der Pijl and Dodson, 1966; Arditti, 1992; Kurzweil, 2005), have three stigmas, and there is considerable diversity in the degree of rostellum formation within the family (Dressler, 1981; Kurzweil, 2005). Three primary evolutionary steps in rostellum formation have been defined (Dressler, 1981; Kurzweil, 2005): 3. A fully developed rostellum exists with a defined viscidium (sticky gland) that is attached to the pollinarium. This occurs in Cymbidium (Fig. 5A) and Vanda (Figs. 4, 5), for example. In Disa the rostellum can be three lobed. 1. A well-defined rostellum does not occur. An example of this is Cephalanthera. 2. A rostellum exists that is structurally different from the rest of the median stigmatic lobe but lacks a viscidium. Sobralia is an example of this. Orchid seeds (Fig. 6A, C–F) are unlike those of any other plant (Arditti, 1992; Arditti and Abdul Ghani, 2000; Yam et al., 2007): Darwin’s interest in the rostellum was structural and developmental and was from homology, pollination, gradation, and evolution points of view. He was not—and given what was known about the physiology of orchid flowers at the time, could not have been— aware of the physiological role of the rostellum, which became clear relatively recently (see Avadhani et al., 1994, for a review). This role is that of a sensor or “transducer” of the mechanical effects of pollen removal (Arditti and Flick, 1974; Strauss, 1976; Arditti, 1992; Strauss and Arditti, 1984). The rostellum is wounded by removal of the pollen (Fig. 5C). This triggers ethylene evolution (Fig. 5B), which brings about senescence of emasculated flowers. Energy for the production of ethylene is provided by the many mitochondria that are present in the rostellum (Fig. 5D). Vascular strands (Fig. 5D), which extend through the rostellum (Darwin, 1904; Strauss, 1976; Strauss and Arditti, 1984), bring in substrates. The energy used to produce ethylene and import substrates is compensated for by the hydrolysis of structural and reserve substances of floral segments and utilization of their components. Darwin did point out the evolutionary implications of the rostellum with a short discussion: “If the homologies of Orchids had not been pretty well made out, those who believe in the separate creation of each organism might have advanced this as an excellent instance of a perfectly new organ having been specially created, and which could not have been developed by successive modifications of any preexisting part. But, as Robert Brown long ago remarked, it is not a new organ . . . ” (Darwin, 1904). Thus, even a peculiarity of plants, in which Darwin described his interest as merely a hobby, was used by him to support the theory of evolution. SEED Fig. 5. The rostellum: its structure and function. (A, B) Cymbidium rostellum: its position, gross morphology, and ethylene evolution after application of naphthaleneacetic acid to the stigma. 1. Intact gynostemium (column); 2. gynostemium with anther cap removed; 3. pollinarium (pollinia, stype and viscidium) attached to rostellum; 4. rostellum. (C) Outer edge of the rostellum where the viscid disk was attached (three arrows on the right). Removal of the viscidium causes a wound that brings about ethylene evolution. (D) Rostellum cell with numerous mitochondria (C, D, G, from a dissertation by Dr. Michael S. Strauss, University of California, Irvine). (E) General diagram of the upper portion of a gynostemium showing the positions of the rostellum and viscidium (courtesy Dr. Hubert Kurzweil, Singapore Botanic Gardens). (F) Rostellum of the Vandae. “1. Filament bearing the anther . . . 2. Upper pistil, with the upper part modified into the rostellum. 3. The two lower confluent pistils, bearing the two confluent strigmas” (Darwin, 1904). (G) Gynostemium (column) of Phalaenopsis without the anther cap, showing pollinia and rostellum (right, arrow), pollinarium (bottom left) and anther cap (upper left). Explanation of symbols: A or a, anther cap; cw, cell wall; m, mitochondrion; p, pollinium; Po, pollinia; r, rostellum; s, stigma; t, tip of gynostemium; V or v, viscidium (A, G) and vacuole (D). December 2009] Yam et al.—Darwin and his orchids 2137 Fig. 6. Orchid seeds. (A) Scanning electron microscope photographs of testa cells. a, b. Calypso bulbosa from Colorado magnified 163× and 421×, respectively (Arditti et al., 1980); b, c. Paphiopedilum Susan Tucker × Paphiopedilum parishii magnified 199× and 476×, respectively (Arditti et al., 1979). (B) Floatation time in air by seeds vs. weight and air space inside the testa. Floatation time increases with larger air volume in the testa and with lower weight (Arditti and Abdul Ghani, 2000). (C) Paintings of orchid seeds; all seeds are magnified 52× (Beer, 1863). (D) Line drawing of Stanhopea oculata seed magnified 96× (Burgeff, 1936). (E) Opening (arrow) at the suspensor end of a testa of Paphiopedilum Susan Tucker × Paphiopedilum parishii magnified 771×. It is wide enough to allow the entry of fungal hyphae and water (Arditti et al., 1979). (F) Seeds of American orchids. a, b. Cypripedium calceolus var. parviflorum magnified 68× and 349×, respectively (Arditti et al., 1979); c. Calypso bulbosa from California magnified 523× (Arditti et al., 1980); d, e. Cypripedium reginae magnified 34× and 2842×, respectively; arrow points to opening at the suspensor end (Arditti et al., 1979). • Orchid seeds are produced in very large numbers ranging from 376 to 4 000 000 fruit−1 and up to 74 000 000 plant−1. • They can weigh 0.39 µg to 1.79 mg seed−1. • They vary in width from 0.1 to 0.72 mm and in length from 0.28 to 10.09 mm. • The seeds have free air space inside the testa, which can be 16% to 90% of the total volume (i.e., embryo volume is smaller than seed volume). • They include embryos that cannot metabolize significant amounts of their own food reserves (fat globules and starch grains). • Orchid seeds require penetration by a mycorrhizal fungus for germination. • They originate from ovules, which develop after pollination (Fig. 7). In fact, the pollen provides a stimulus (auxin) for the proliferation of cells in the placental ridges, the formation of archespores, the development of megapsores, and the production of the embryo sac. The interval between pollination and fertilization can be as long as 300 d in Vanda suavis, between pollination and embryo formation may extend to 32 wk in Cattleya gigas, and between pollination and seed maturation is 16.5 mo in Acampe reinschiana (Yam et al., 2007). 2138 American Journal of Botany [Vol. 96 Fig. 7. Ovary, ovule, seed, and seedling development in orchids as they were illustrated in Darwin’s time using Cattleya mossiae as an example unless indicated otherwise (Veitch and Sons, 1887–1894). (A) Ovary and gynostemium (column). (B) Longitudinal section of ovary and gynostemium (column). (C) Swelling of the ovary (1) at the time of pollination and (2) 2 wk and (3) 1 mo after that (in cross sections magnified 2.5×). (D) Ovary cross sections at (1) 55, (2) 72, and (3) 90 d after pollination, magnified 0.98×. (E) Cross section of ovary magnified 10.4×. (F) Gynostemium (column) in cross section magnified 10.6×. (G) Pollinia and pollen tubes magnified 200×. (H) A mass of pollen tubes magnified 200×. (I) 1–5. Development of “rudimentary ovules.” (No magnification factor was provided in the original illustrations.) (J) “Rudimentary ovules: one month after pollination.” (No magnification factor is provided in the original illustration.) (K) Ovules 5 mo after pollination magnified 62×. (L) Ovules and pollen tubes 90 d after pollination magnified 169×. (M) f–i. Development of fertilized ovule to mature seed magnified 100×. (N) Seedling development in Cattleya. In those days, seeds were germinated symbiotically even if the growers were not aware of this fact. The (1) seed and (2) protocorm are “greatly enlarged” in the original illustration; the rest are “natural size” in the original (Veitch and Sons, 1887–1894). Having read Friedrich Hildebrand’s (1835–1915) papers on double fertilization and hybridization in orchids (Hildebrand, 1863a, b, 1865), Darwin noted that ovules of Acropera were “wretched rudimentary” (Darwin, 1861t) and was aware “that with some orchids the ovules are not mature & are not fertilized until months after the pollen tubes have penetrated the column” (Darwin, 1866b), but he did “not know what to think” about it (Darwin, 1866–1867). It is surprising that the fact that this constitutes conservation of energy (because a structure that may not be used does not develop) seems to have escaped him. His interest in this aspect of orchids ended with musings. Perhaps he would have been more interested in the subject had he known that the substance (auxin from pollen) that brings about the bending and movement of Phalaris cotyledons in response to light (Darwin and Darwin, 1880, 1898) also (1) causes cell masses on placental ridges in orchid ovaries to start proliferating and eventually form ovules and (2) brings about (through initiation of ethylene evolution) the death of perianth segments in most orchids and greening in a few species of Zygopetalum, Huntleya, and Phalaenopsis (Avadhani et al., 1994) after pol- December 2009] Table 1. 2139 Yam et al.—Darwin and his orchids Darwin’s counts and estimates of orchid seeds and populations (Darwin, 1904). Seeds per Species Acropera Cephalanthera grandiflora Maxilaria Orchis maculata 1st generation (“parents”) Capsule Plant 371 250 74 000 000 6020 24 080 1 756 440 10 538 640 6200 186 300 2nd generation (“children”) 3rd generation (“grandchildren”) 4th generation (“great grandchildren”) lination (for a review, see Arditti, 1992). Of course, he had no way of knowing that. Darwin’s interest in orchid seeds was in their production, numbers, dispersion, and germination (Darwin, 1863a, 1866a, c, d, 1904; Müller, 1866a, 1868). He was surprised by Fritz Müller’s (Fig. 2E, 3C) assertion (Darwin, 1866c) that few flowers of orchids native to Brazil produce capsules. The reason for this is probably that in those days the paucity of pollinators in some tropical areas and the low fruit set caused by complex pollination mechanisms were not yet known. Darwin’s interest in the number of seeds per capsule, per plant, and per area (Table 1; Darwin, 1866d; Müller, 1866a, 1868) was more extensive perhaps because of his view that “what checks the unlimited multiplication of the Orchideae throughout the world is not known. The minute seeds within their light coats [a more appropriate wording would have been “the minute embryos within their light coats”] are well fitted for wide dissemination” (Fig. 6B) with seedlings of Epipactis latifolia “appearing at the distance of between eight and ten miles from any place where it grew. Notwithstanding the astonishing number of seeds produced by Orchids, it is notorious that they are sparingly distributed . . . if their seed or seedlings were not largely destroyed, any one [orchid] would immediately cover the whole land” (Darwin, 1904). This puzzlement by Darwin is surprising. His own studies and The Origin of Species should have taught him that any organism, no matter how prolific, is subject to limits. Further, his assumption that their “seeds or seedlings [are] largely destroyed” is incorrect. Most of the seeds never germinate. He had the correct reason for the limited distribution of orchids within his grasp (see below) but somehow missed it. In Darwin’s view, “the production of an almost infinite number of seeds or eggs, is undoubtedly a sign of lowness of organization” (Darwin, 1904). Production of so many seeds may seem primitive and risky because evolution does not forgive waste of energy and resources. Darwin must have thought of that, but he seems to have ignored the fact that orchids are very successful from the evolutionary point of view. The survival benefits of producing many small seeds outweigh the cost of producing them. This is neither “lowness” nor a primitive character (Arditti and Abdul Ghani, 2000). In addition, there are Acre Comments Count per capsule and estimate per plant are by Darwin. Count per capsule and estimate per plant are by Darwin. Count per capsule is by Fritz Müller. Calculation per plant assumes six fruits plant–1. 32 460 912 000 Count per capsule and estimates per plant, acre, and generation are by Darwin. The terms “children” and “grandchildren” are by Darwin. Assuming 174 240 plants acre–1. Darwin provided no information. Plants will cover a space slightly exceeding the island of Anglesea; current spelling, Anglesey (714 km2). “Clothe with one uniform green carpet the entire surface of the land throughout the globe.” The globe is 148 940 000 km2. adaptations in orchids that make up for energy used to produce the seeds. One example is fruit set in Cypripedium calceolus, which seems to be practically cost free on the annual ramet level. Ramets that produce fruits retain their leaves for a longer period and thereby compensate for annual energy in terms of carbon use on the ramet level due to the longer vegetation period (Kull, 1998). However, longer leaf life cannot compensate for other factors (mineral shortages, for example) that may limit fruit set and/or seed production. Thus it appears that the input by individual plants notwithstanding, the resources devoted by Cypripedium calceolus to the production of numerous small seeds may be minimal, if any, and a good investment. Seed production costs may be higher in orchids other than Cypripedium (Ackerman and Zimmerman, 1994). Evolution of food deceit (Ackerman, 1986) may reduce energy investment in seed production, but it does not eliminate it. Plants expend resources to produce the mechanisms of deception and floral structures and pigments. Nectar production also requires expenditures of resources. Aerangis verdickii plants are estimated to devote 684 J plant−1 season−1 to produce nectar (Koopowitz and Marchant, 1998). Much of that is wasted because as many as 67% of the flowers are robbed of their nectar by ants (but the ants offer protection against grazers). Altogether, nectar is a “significant expense” to this orchid (Koopowitz and Marchant, 1998). Production of fragrances also requires a considerable expenditure of resources. One examples is Gongora. The flowers are fragrance-reward blossoms. When the flowers first open, the hypochile is packed with starch to the point of looking like a potato if stained with iodine. The starch is gone after 2–3 d (M. Whitten, University of Florida, personal communication). It is probably used to provide energy for scent production. Aborted fruits and those lost to predation (Ackerman and Montalvo, 1990) can also be considered as resources devoted to seed production. Unused nectar may be reabsorbed by Aerangis verdickii after pollination (Koopowitz and Marchant, 1998). In most orchids, flowers senesce rapidly after pollination. This terminates the use of resources, and because perianth segments are broken down, smaller molecules (sugars, amino acids, phosphate) are transported into the gynostemium and ovary where they are 2140 American Journal of Botany reutilized (for a review, see Avadhani et al., 1994). These postpollination phenomena make microspermy possible because they reduce its cost to the plants. Thus the evolution of microspermy in at least some orchids clearly represents a derived character of adaptive value rather than a plesiomorphic (i.e., primitive) one. Another point to consider is that orchid embryos are very small. Some of them consist of only a few cells. Most have no endosperm (Weiss, 1916; Burgeff, 1936; Arditti, 1967, 1979, 1992; Arditti and Ernst, 1984). Their food reserves are lipids (Anonymous, 1922; Poddubnaya-Arnoldi and Zinger, 1961) in the form of oil droplets and starch grains, which occur inside cells at levels that are not high in absolute terms (Knudson, 1929). Therefore, orchids probably do not invest as many resources in seed production as the number of seeds may suggest. Actually, the total resources devoted by orchids to seed production may be similar or perhaps even less than those other plants invest in bigger, but fewer seeds that contain more reserves. This point becomes clear when seeds of coconut trees (coconuts) are compared with orchid seeds. Coconut seeds are suitable for such a comparison because relatively few large, lipid-rich seeds are produced by the trees. Seeds of Cycnoches ventricosum var. chlorochilon weigh 3.6 μg each. With capsules containing 4 000 000 seeds, the total seed weight is 14.4 g fruit−1. If the Cycnoches seeds contain as much lipid energy as fresh coconut solid endosperm (1470 kJ 100 g−1), the total is still a minuscule 212 kJ 14.4 g−1 or 0.000419618 kJ seed−1. This assumption can be made because orchid seeds, like coconuts, are fatty in nature (Harrison, 1977; Harrison and Arditti, 1978; Arditti and Ernst, 1984) and may contain as much as 32% lipids (Knudson, 1929; Arditti, 1967, 1979, 1992) vs. 34% for coconuts. Coconut endosperm (the white “meat” inside the nuts, which becomes copra) contains 34% fat (vs. 32% for orchids) and 212 kJ 14.4 g−1 (Diem, 1962). A nut purchased at random in a food store (Arditti and Abdul Ghani, 2000) contained 380 g “meat” and therefore 5586 kJ of energy (26 times the energy in a Cycnoches capsule) and 120 g of liquid endosperm (“coconut water,” which is often erroneously called “coconut milk”). The liquid endosperm also contains energy as well as vitamins, hormones, amino acids, and other substances. Therefore, the total energy content of a single coconut, excluding the shell and outer husk, may be as high as 6000 kJ (vs. 0.000419618 kJ Cycnoches) seed−1. This is equal to the energy content of 113 207 547 Cycnoches seeds (as many as would be contained in 28.3 capsules). Coconut trees can produce as many as 75 coconuts tree−1. About 25 nuts tree−1 is the average (Arditti and Abdul Ghani, 2000). Given this average, the production of 4 000 000 seeds (i.e., coconuts) will require 160 000 trees. That many nuts will contain 24 000 000 000 J in their “water” and “meat” (vs. 212 J for the same number of Cycnoches seeds). Even if a single Cycnoches seed and only one coconut produced a flowering-sized plant, the energy cost per mature offspring is lower for orchids. Such conservation of energy is not “lowness” of character. The number of eggs, embryo sacs, and seeds being produced are not the only points that must be considered. Other important considerations are as follows: Energy expended by the plant in producing eggs, embryo sacs, and seeds— It is reasonable to assume that orchids expend as much energy in producing eggs and ovules as do other plants. However, they devote energy to the production of an embryo sac only after being pollinated (for a review, see Arditti, 1992). [Vol. 96 This can be viewed as an advanced character, since it conserves energy. Success as a family— Orchid is a successful family despite the unique specialization of their pollination and seed germination. Survival advantages conferred on a species by the production of many seeds— When it comes to seeds, orchids are minimalistic in all but the number. Their seeds are small and balloon-like (for reviews, see Arditti and Abdul Ghani, 2000; Yam et al., 2002a) and contain only limited food reserves (for reviews, see Arditti, 1992; Yam et al., 2002b). However, the seeds are also not equipped with the metabolic machinery required for the utilization of the starch and lipids they do contain (Harrison, 1977; Harrison and Arditti, 1978). During the early stages of germination they depend on fungi for nutrients. Pollination mechanisms— In principle the life cycle of orchids is not different from that of other plants. However, there are differences in the details of pollination mechanisms and seed germination. The pollination mechanisms may involve profligate use of resources, such as the production of scents and maintenance of structures and pigmentation, which attract pollinators, but these cease almost immediately after a flower is pollinated (Avadhani et al., 1994; Yam et al., 2009). Therefore, total expenditure of energy for the purpose of attracting pollinators by orchids is probably not excessive. It may in fact be penurious. Seed germination— Germination of orchid seeds is unusual because of their requirement for penetration by (in some instances, highly specific) mycorrhizal fungi. (“Penetration” is preferred to the often-used “infection,” which should be avoided because of its pathogenic implications.) These fungi provide nutrients, vitamins, hormones (Harrison, 1977; Harrison and Arditti, 1978; Arditti and Ernst, 1984; Arditti, 1992; Yam et al., 2002a), and perhaps also elicitor-type molecules and genetic information (Arditti et al., 1990). Darwin had limited or no information about the first and last of these aspects (and neither do we at present about some of them!), but he was aware of the others. Therefore, it is surprising that he did not have second thoughts about the “lowness” of orchids. Perhaps the reason is that the most important factor and the one that underlies all of these aspects—conservation of energy—was largely beyond the technology and the thinking of his day and therefore was unavailable to him. Orchid seeds (Darwin, 1861l) and seed germination were of interest to Darwin even if he was not well informed about what orchid growers and breeders of the day were doing. On 26 May 1867 he wrote to Fritz Müller in Brazil that the seeds of crossed orchids do not germinate and that “one single man in Europe has found out how to make these seeds germinate, & he keeps it a secret in his trade of nurseryman. He also made some strange crosses between distinct genera, & these hybrids have flowered. Dr Hooker tells me that they have in vain tried at Calcutta to make seeds of hybrids germinate, yet American orchids growing at the Bot. Garden there have spontaneously sown themselves and grown on adjoining trees” (Darwin, 1867b). Actually, the first person to germinate orchid seeds under horticultural conditions was David Moore (1807–1879; Fig. 8A) at the Glasnevin Botanical Gardens in Ireland in 1849 (Moore, 1849, 1850). His report was quickly followed by two additional accounts, both by British gardeners, of orchids being germi- December 2009] Yam et al.—Darwin and his orchids 2141 Fig. 8. Individuals associated with early orchid breeding and seed germination. (A) David Moore, 1807–1879 (courtesy Glasnevin Botanical Garden). (B) John Dominy, 1816–1891 (http://commons.wikimedia.org/wiki/File:John_Dominy.jpg). (C, D) John Harris (1782–1855) and the Royal Devon and Exeter Hospital, where he worked, as it looked ca 1850 (courtesy Frank Hadfield, Administrator at the Royal Devon and Exeter Hospital in 1979). (E) Noël Bernard, 1874–1911 (courtesy N. Bernard’s son, the late Prof. Francis Bernard, and his wife Michelle in 1989). nated by growers (Cole, 1849; Gallier, 1849a, b; for reviews, see Arditti, 1984; Yam et al., 2002a; Yam and Arditti, 2009). The first orchid hybrid was produced by John Dominy (1816– 1891; Fig. 8B) of the Veitch establishment at the advice of John Harris (1782–1855; Fig. 8C, D), a surgeon. Its seeds were germinated using methods similar to those described by Cole, Gallier, and Moore. In 1853 Dominy crossed Calanthe masuca and Calanthe furcata, and the first plant of this hybrid flowered in 1856. The first Cattleya and Paphiopedilum hybrids flowered in 1856 and 1869, respectively (for a review, see Arditti, 1984). Dominy produced several first bigeneric hybrids (“strange crosses between distinct genera”) starting in 1861. Priority claims by French orchid growers cannot be substantiated. In fact, the literature suggests that they have no basis in fact (Arditti, 1984; Yam et al., 2002a; Yam and Arditti, 2009). Orchids were being germinated in Calcutta during that period using methods similar to those used by British growers: “The seed should be scattered lightly on the surface of living moss, or partially decayed wood, where it is not likely to be disturbed—about the roots of the parent plant is a very good place” (Jennings, 1875). According to John Scott (1838–1880; Fg. 3E), superintendent of the Calcutta Botanic Gardens, seeds sown “take from six weeks upwards to three months in germinating” (Jennings, 1875). Had the efforts to germinate the seeds been “in vain,” Scott would not have known how long it takes them to germinate. Darwin had “a passion to grow the seeds” of orchids (Darwin, 1863a). He had “some planted in sphagnum” and wanted to try to germinate orchid seeds on other substrates: “Do any tropical lichens or mosses or European withstand heat [and] grow on any tree in Hothouse at Kew; if so for love of Heaven favor my madness & have some scrapped off & sent to me. I am like a gambler, & love a wild experiment. It gives me great pleasure to fancy that I see radicles of orchid-seed penetrating the sphagnum; I know I shall not & therefore shall not be disappointed” (Darwin, 1863b). Had he been able to germinate orchid seeds, Darwin would have been disappointed anyway because radicles are not part of the process. Having not seen orchid seedlings, he had no way of knowing that. Despite Darwin not being well informed about orchid seed germination, having not seen the process, and having “not a fact to go on,” he had “a notion (no, I have a firm conviction) that they [i.e., the germinating seeds] are parasites in early youth on cryptogams!!” (Darwin, 1863b). In those days, the term “cryptogams” included fungi whose involvement in orchid seed germination was discovered by the French botanist Noël Bernard (1874–1911; Fig. 8E) in 1899 (Bernard, 1899; for reviews, see Arditti 1984, 1990; Yam et al., 2002a; Yam and Arditti, 2009; for a translation of Bernard, 1899, see Jacquet, 2007). Darwin 2142 American Journal of Botany was right and 36 yr ahead of his time. He gave no reason for his “firm conviction.” Could it be that the smallness of orchid seeds led Darwin to assume that they had limited or no food reserves and had to obtain nutrients from another organism? “POISONOUS” POLLEN—PREAMBLE TO PLANT HORMONES Darwin observed the pollination of orchids by insects and studied the flowers after they were pollinated either by a natural vector or manually with their own pollen or that of other species. He also solicited and exchanged information on orchids in general and pollination and its effects in particular with botanists in the tropics and elsewhere (Darwin, 1863b, 1865a, b, 1866a–d, 1867a, b, 1868, 1869; Scott, 1863; Müller, 1866b, 1867b, c, 1868, 1877). None of Darwin’s correspondents was more interesting, impressive, and perhaps eccentric than Johann Friendrich Thedor “Fritz” Müller, MD (1822 [Germany]–1897 [Brazil]) who was an early convert to the theory of evolution (W.F.H.B., 1897; Möller, 1921; Arditti, 1971, 1975, 1979; Avadhani et al., 1994; Yam et al., 2009). Müller questioned religion early, became an atheist in 1846, and refused to take the medical oath in Germany because the words “so help me God” were part of it. He also supported the 1848 Prussian revolution and was more liberal that the German regime of his day would tolerate. As a result, he had to leave Germany (W.F.H.B, 1897) in 1852. He moved to Brazil and wrote about his many observations in an extensive correspondence with scientists in Germany and with Charles Darwin as well as in journals. As a very early believer in the theory of evolution, Müller wrote Für Darwin in 1864.14 In this book, he used Brazilian crustaceans to support Darwin’s views. He corresponded extensively with Charles Darwin about orchids and patiently answered many of his questions. Among the topics covered by his letters was the effect of orchid pollen on flowers (Müller, 1867a,15 c, 1886b; Darwin, 1904; for a review, see Avadhani et al., 1994). Darwin described these effects in The Variation of Animals and Plants Under Domestication, Volume 2, as being “injurious and poisonous” (Darwin, 1880b, 1890). His authority resulted in the acceptance as a theory of the idea that orchid pollen is poisonous. What Darwin could not have known is that a substance that plays a role in the death of orchid flowers is also involved in the movement of plants in general and phototropism (which he studied with his son Francis) in particular (Darwin and Darwin, 1880, 1898; Went and Thimann, 1937; Arditti, 1971, 1975, 1979, 1992; Avadhani et al., 1994; Yam et al., 2009). One person who became interested in the “theory that [was] very common in the older German literature on pollination biology, namely that the pollinia of many exotic orchids act like a poison during cross-pollination” in 1970 was Hans Fitting 14 It was translated into English as Facts and Arguments for Darwin by William Sweetland Dallas in 1867 and is currently available online for downloading free of charge at http://www.bookrags.com/ Facts_and_Arguments_for_Darwin. 15 The full text of this letter is not posted online; it is available in Volume 15, pp. 3–8, of the collected Darwin correspondence. We thank Shelley Innes, Darwin Correspondence Project, Cambridge University, for a copies of this letter and one dated 2 February 1867 (Volume 15, pp. 61–64, of the collected Darwin correspondence). [Vol. 96 (1877–1970; Fig. 9A). He also read Müller’s letter to Darwin of 1 January 1867, which “elaborates on the toxicity of the orchid pollinia,”16 and he secured a travel grant to visit the Bogor Botanical Gardens in Indonesia (now Kebun Raya Indonesia) to carry out research on “poisonous pollen” theory. Fitting seems to have enjoyed his stay in Bogor, where he carried out many experiments with orchid flowers, pollen from orchids, and other plants and pollination effects from September or November 1907 until June 1908. Seventy-nine experiments were numbered (these were simple, consisting of a single part, or complex and multipart) and a large quantity had no numbers. (For details of his experiments and an extensive list of citations, see Yam et al., 2009.) His papers (Fitting 1909a–c, 1910, 1911, 1912, 1921, 1936) were very long because he described his experiments in excruciating (almost numbing) detail. He pollinated flowers (by crossing geitonogamously, by selfing, and xenogamously) and reported that in most cases pollination shortened the life span of the flowers and caused swelling of the gynostemium (column) and ovary a short time after the application of pollen to the stigma. Fitting also emasculated orchid flowers and observed that emasculation caused senescence of floral segments, which are slower to develop after pollination. Wilting of the perianth, senescence, and shortened life span of flowers also occurred after wounding or damaging the stigma in any way. Fitting killed pollinia by steaming and by submerging them in chloroform or boiling water and then determined their effects on flowers. Pollinia that were submerged in chloroform for 30 min brought about phenomena that were the same and as rapid as those caused by living pollen. The intensity of the phenomena was reduced in flowers pollinated with pollen that was soaked in chloroform for 60 min. Pollen killed by steeping in boiling water did not induce postpollination phenomena. Pollinia killed by steaming were as effective as live pollen. All of Fittings’ initial work involved pollinating blossoms with pollen of the same species. In his subsequent studies he investigated the effects of cross species and determined that the effects of intra- and inter-pollination were the same. Specifically, he found no differences in the effects on orchid flowers, regardless of whether the flowers were pollinated with pollen from (1) their own gynostemium (self pollinated), (2) another flower of the same species (intraspecific pollination), (3) flowers of other orchid species (interspecific pollination), or (4) other orchid genera (intergeneric pollination). After that he investigated whether pollen of non-Orchidaceous plants and orchid pollinia produced the same effects. He found that non-Orchidaceous pollen brought about wilting and senescence of orchid flowers, but it did not cause swelling of the gynostemium and stigmatic closure (both are auxin effects). Fitting placed the pollen in stigmas in his initial experiments. In another series of experiments, he placed living and dead sections of pollinia inside gynostemia. Swelling of gynostemia and ovaries, stigmatic closure, and wilting of the flowers were induced by both living and dead pollinia, regardless of where they were placed. A pollinium section placed below the rostellum also caused postpollination phenomena. 16 The quotes are from a letter by Prof. Hans Fitting (H.F.) to Joseph Arditti (J.A.) dated 10 November 1969. It was translated by Dr. Hubert Kurzweil (H.K.) of the Singapore Botanic Gardens. The full text of this and other letters to J.A. (all translated by H.K.) and a detailed account of H.F.’s work with orchids are available in Yam et al., 2009. The original letters are in the library of the Singapore Botanic Gardens. December 2009] Yam et al.—Darwin and his orchids 2143 Fig. 9. Early investigators of auxin. (A) Johannes Theodor Gustav Ernst “Hans” Fitting, 1877-1970 (photograph courtesy Mrs. Sigrid Fitting; signature from a letter by Fitting to J.A.). (B) Friedrich Laibach, 1885-1967 (courtesy Dr. Elliott M. Meyerowitz, California Institute of Technology; enlarged from a group photograph, which is the reason for the fuzziness and pixilation; no other likeness could be found). (C) Frits Warmolt Went, 1903-1990 (photograph and signature courtesy Dr. F. W. Went in 1988). On his return to Germany, Fitting repeated some of his experiments with flowers of Cattleya and other orchids that exhibit easily observable postpollination phenomena. After that, Fitting lost interest in orchids. He mentioned orchids in several papers but never worked with them again. Except for one paper from Japan (Morita, 1918), a short period of work (eight papers) in Germany by Friedrich Laibach (1885–1967; Fig. 9B) and his associates (Laibach, 1929, 1932, 1933a, b; Laibach and Kornmann, 1933; Laibach and Maschmann, 1933; Maschmann and Laibach, 1933; Mai, 1934), and several references in the first book on plant hormones (Went and Thimann, 1937), Fitting’s work on orchids lay almost forgotten until one of us (J.A.) became interested in postpollination phenomena of orchids (for a review, see Avadhani et al., 1994). Postpollination phenomena in orchid flowers are expressed in the (1) perianth (dorsal and lateral sepals, median and lateral petals; the median petal is the labellum), which move (for example, hyponasty in Phalaenopsis), senesce (in many orchids, Cattleya, for instance), and change color and structure and/or function (turn green and become fleshy in Zygopetalum and some Phalaenopsis species); (2) gynostemium, which swells (Cymbidium is an example); (3) stigma, which closes (Cattleya and Cymbidium); and (4) ovary, which swells while the ovules develop internally (Cattleya). Fitting observed and described all these phenomena and tried to find out whether one phenomenon can be induced without the others, especially 1–3 above. He was also interested in the effects of pollen on ovary swelling (phenomenon 4 above). To study these effects, he pollinated flowers with living and dead pollen and determined that (1) swelling of ovaries in some flowers can be brought about by pollinia but not in others, and (2) pollen tubes may be required for ovaries to swell. These conclusions were not entirely accurate (for a review, see Avadhani et al., 1994). Fitting’s experiments with Cattleya, Odontoglossum, Zygopetalum, and European orchid flowers on his return from Bogor were designed to characterize the active principle in orchid pollen. They were physiological and chemical in nature, ahead of their time, and modern. He apparently read widely and seems to have been familiar with literature on subjects other than plants because he knew of a suggestion by the British physiologist Ernest Starling (1866–1927) that substances he called “hormones” affect development in animals. He concluded correctly that “the active substances in pollinia are hormones” (Fitting, 1910). He assumed the existence of one hormone in orchid pollen and named it “Pollenhormon.” More recent research has shown that Fitting was only partially right. Orchid pollen contains more than one hormone. It contains very high concentrations of auxin and some 1-aminocyclopropane-1-carboxylic avid (ACC). Some evidence also exists that orchid pollen contains gibberellins and cytokinins (for a review, see Avadhani et al., 1994). Thus, Darwin’s acceptance and promotion of the Müller’s poisonous pollen idea led to Fitting’s research and the first suggestion that plants produce hormones. The first hormone identified in orchid pollen was auxin (Laibach, 1929, 1932, 1933a, b; Laibach and Kornmann, 1933; Laibach and Maschmann, 1933; Maschmann and Laibach, 1933; Mai, 1934). This identification was carried out after Frits W. Went discovered it in 1926 (Went, 1926, 1990; Went and Thimann, 1937). It is instructive to relate Fitting’s findings to our current knowledge about the induction of postpollination phenomena and floral senescence in orchid flowers (Avadhani et al., 1994). Ethylene evolution— Pollination, emasculation, and wounding of orchid flowers induce ethylene evolution, which causes senescence of floral segments and a number of other postpollination phenomena. In the case of pollination with living or dead pollinia, auxin (Fig. 5B) and the ethylene precursor ACC, which diffuse from the pollen initiate ethylene evolution (Nair et al., 1991; Avadhani et al., 1994). This is unrelated to pollen tube growth, ovule development, and fertilization except that substances from senesceing floral segments are transported to areas where they are used (Harrison and Arditti, 1976; for a review, see Avadhani et al., 1994). 2144 American Journal of Botany Solvents and solubility— Indole-3-acetic acid (IAA) and ACC are not soluble or are sparingly soluble in chloroform. This near insolubility may explain the different effects of pollinia that were soaked in chloroform for 30 or 60 min. Therefore, Fitting’s choice of killing agent was fortunate. He gave no reasons for using chloroform. However, since auxin was not known at the time, it is clear that he did not select chloroform on the basis of its solvent characteristics and the solubility of substances in the pollen. If Fitting had used ethanol (a solvent that is more easily available and, because of that, a more obvious choice), his result would have been different. Killing the pollinia with ethanol would have extracted both the auxin and ACC and would have caused the dead pollen to become ineffective. The solubility of auxin in hot water is limited, but the killing (i.e., exposure) period used by Fitting was probably long enough to extract sufficient auxin from the pollen to render the dead pollinia inert. His result would have been different had he soaked the pollinia in cold water. Altogether, ethanol and cold water, rather than chloroform and boiling water, would have altered Fitting’s findings and consequently would have changed the course of his experiments as well as his conclusions. Non-Orchidaceous pollen— Fitting found that pollen from plants other than orchids (Fitting, 1909a, b) causes floral wilting and senescence (all effects of ethylene) but not swelling of the gynostemium and stigmatic closure (both brought about by auxin). This suggests that non-Orchidaceous pollen contains sufficient auxin and/or ACC to initiate ethylene evolution but not enough to cause auxin effects. Considering that orchid pollinia contain very high auxin levels (Table 2; Müller, 1953; Klass, 1964; Stead, 1992; for a review, see Avadhani et al., 1994), perhaps higher than in the pollen of other plants, this is not surprising. Ethylene evolution by the rostellum— The rostellum (which in Cymbidium flowers [Fig. 5A] weighs a mere 20 μg) is a major site of ethylene evolution (Fig. 5B) in orchid flowers (Chadwick et al., 1986; see Avadhani et al., 1994, for a review). Production of the gas can be induced by both pollination and auxin (Chadwick et al., 1986). Rostella of Cymbidium start to produce ethylene (0.5 nmoles g−1 h−1) 4 hours after being treated with 25 μg naphthalene acetic acid (NAA). Maximum ethylene evolution (10 nmoles g−1 h−1) occurs 20 hours after treatment (Chadwick et al., 1986). Therefore, it is clear why a pollinium section (i.e., a source of auxin) placed below it by Fitting caused some postpollination phenomena (Fitting, 1909a). What becomes evident in the light of current knowledge is that the pollen is not “poisonous.” Rather, it induces ovule development and causes the senescence and death of floral segments that are no longer necessary. This is energy conservation. Transport and reutilization of substances from the senescing Table 2. Auxin content in orchid pollen Species Cattleya Enid Lomboglossum bictonense Oncidium splendidum Tropical orchids, mixture of pollinia Indoleacetic acid content (µg g–1) Reference 100 (0.11%, w/w) 113 (0.113%, w/w) 26 (0.026%, w/w) 100 (0.11%, w/w) Klass, 1964 Stead, 1992 Stead, 1992 Müller, 1953 [Vol. 96 segments into the ovary also conserve energy. Conservation of energy and resources in flowers elaborate and expensive (in terms of energy) to maintain is a necessary adaptation because “the final end of the whole flower, with all its parts, is the production of seed; and these are produced by orchid in vast profusion” (Darwin, 1904). And, the “production of seed . . . in vast profusion,” even if they contain limited reserve, requires energy and resources. In a conversation with F. W. Went, the discoverer of auxin (Fig. 9C), J.A.17 asked whether he knew of Fitting’s work. Specifically, he asked whether Went made a connection between Pollenhormon and Fitting’s research and auxin and his own work with Avena coleoptiles, which led to the discovery of auxin. Went replied that he had met Fitting several times, including once when he came to visit Prof. F. A. F. C. Went (F. W. Went’s father) in Utrecht, and that he did not connect the hormone in orchid pollen with the one in Avena coleoptiles. This is easy to understand because there is no obvious connection between the bending of coleoptiles and the swelling of gynostemia or the wilting of flowers, especially in the very early days of plant hormone research. The connection was established only after auxin was discovered and its effects were studied extensively. Went isolated auxin from Avena coleoptiles because several investigators followed up on Darwin and his son’s work on photropism (Darwin and Darwin, 1898). One of these investigators was Fitting, who made incisions on either the dark or the light side of the coleoptile to determine the translocation site of the signal (Fitting, 1907). He obtained inconclusive results because the signal could move across or around the incision. The coincidence is interesting, but it is obvious that Fitting did not connect the signal with his Pollenhormon. Conclusive evidence that basipetal transport of auxin in the dark side was obtained by inserting sections in impervious material rather than making incisions (Boysen-Jensen, 1913). These findings were confirmed by excising coleoptile tips in the dark, exposing only the tips to illumination, and placing them on only one side or the other of a decapitated coleoptile. Results showed that curvature occurred away from the side on which the tip was placed (Paal, 1918). Finally, in 1926, Went, still a graduate student, reported on the isolation of a plant growth substance by placing coleoptile tips on agar blocks for a time, removing them, and putting them on decapitated Avena coleoptiles. This caused the decapitated coleoptiles to resume growth (Went, 1926, 1928). Research on the poisonous pollen theory suggests that it is possible that auxin may have been discovered in work with orchid pollinia, but it would have been more difficult than with Avena coleoptiles because pollen of orchids (1) contains more than one hormone, (2) cannot be obtained easily in sufficient quantities, and (3) is harder to work with than Avena (Avadhani et al., 1994). 17 Went was J.A.’s house guest in 1988 when he came to present a lecture at the University of California, Irvine. He was an early riser who did not eat breakfast. The conversation took place at about 5 a.m., in J.A.’s library among orchid books and copies of papers by Went’s father (one of which he was seeing for the first time) on the control of flowering of the ephemeral orchid Dendrobium crumenatum in Indonesia in the 1890s. This conversation also led to a very interesting memoir by Went about his discovery of auxin and his work with orchids (Went, 1990). December 2009] Yam et al.—Darwin and his orchids 2145 Fig. 10. Early illustration and students of resupination. (A) Marcello Malpighi, 1628–1694 (a), Palma Christi (b, A–E), and Orchis maculata (c). Arrows point to spirals on the ovaries formed by resupination (a, b, Malpighi, 1675–1679; c, Correvon, 1899). (B) a. Carolus Linnaeus, 1707–1788, and (b) inflorescence and (c) single flower of Neottia nidus avis. Arrow points to spirals on the ovary formed by resupination (a, from http://en.wikipedia. org/wiki/Linnaeus; b, c, Correvon, 1899). (C) a. Conrad Gesner, 1516–1565, and (b–e) photographically and computer enlarged and enhanced (which explains the fuzziness and pixilation) flowers of Platanthera bifolia (a, from http://en.wikipedia.org/wiki/Conrad_Gesner; b–d, Zoller, Steinmann and Schmid, 1972–1980; e, Correvon, 1899). (D) a. Georgius Everhardus Rumphius, 1627–1702, (b) fruit of Grammatophyllum scriptum with spirals (arrow) that have almost disappeared because of deresupination;and (c) flower with spirals that are more pronounced (Rumphius, 1741–1750; the photographs are of a copy of Herbarium Amboinensis in the Singapore Botanic Gardens Library; we thank librarians Christina Soh Jeng Har and Zakiah Agil for access to this rare book and for allowing us to photograph the relevant pages). RESUPINATION—“WHEN THE UPPER LIP . . . LOOKS TOWARD THE GROUND, AND THE UNDER LIP TOWARD HEAVEN” This quote from James Lee (1715–1795; Lee, 1774) is a translation from Carolus Linnaeus’s (1707–1788; Fig. 10B) definition of “resupination” (a term he was the first to use): “florum resupination, cum carollae labium superius terram, inferius coelum spectat” (Linnaeus, 1780; for reviews, see Ernst and Arditti, 1994; Arditti, 2005). The process itself was illustrated much earlier by Conrad Gesner (1516–1565; Fig. 10C) between 1540 and his death in Europe (Gesner, 1751; Zoller et al., 1972–1980; for reviews, see Wehner et al., 2002; Arditti, 2005), Georgius Everhardus Rumphius (1627–1702; Fig. 10D) between 1653 and his death in 1702 in Ambon, Indonesia (Rumphius, 1741–1750; Beekman, 1999; Wehner et al., 2002; Arditti, 2005), and Marcello Malpighi (1628–1694; Fig. 10A) in Europe (Malpighi, 1675–1679; for reviews, see Ernst and Arditti, 1994; Wehner et al., 2002; Arditti, 2005). Linnaeus and Lee described resupination (Fig. 10–12), and the earlier observers noticed and illustrated it, but none of them assigned a function to it. 2146 American Journal of Botany [Vol. 96 Fig. 11. Different levels of resupination in European orchids. (A) Fully resupinate flowers of Calypso bulbosa with the labellum (l) lowermost. This species is circumglobal at northern latitudes. (B) Pouch (p) is lowermost in the fully resupinate flowers of Cypripedium calceolus. This species is found in the United States and Europe. (C) Epipactis palustris showing (1) two unresupinate buds, (2) a bud in the process of resupination, (3, 4) two partially resupinate flowers with their labella (l) pointing sideways, and (5) pollinated flowers in various stages of postpollination deresupination and movement. (D) Labella point upward in unresupinate flowers of Epipogium aphyllum flowers shown (1, 2) individually and (3, 4) on a plant. (E) Malaxis paludosa flowers shown (1, 2) individually and (3) on a plant resupinate 360°, resulting in their labella being uppermost, their dorsal sepals (ds) positioned lowermost, and tight spirals appearing on their ovaries (o). (F) 1. Partially and (2) fully resupinate flowers of Ophrys aranifera. (G) 1–3. Flowers resupinate to some extent in (4) Spiranthes autumnalis plants, but some of the positioning of the labellum in the lowermost location is caused by (5) twisting of the inflorescence. Spiraling can be seen both (1) on the inside and (1–3) on the outside of the ovary of this species (Correvon, 1899, with numbers and letters added). Darwin observed resupination, but if he was aware of the earlier literature he did not cite it. He also did not use the term “resupination”: “In most of the Orchideae, the upper sepal and the two upper petals . . . and all the sepals are reflexed . . . apparently to allow insects to freely visit the flower. The position of the labellum is the more remarkable, because it has been purposely acquired, as shown by the ovarium being spirally twisted. In all Orchids the labellum is properly directed upwards, but assumes its usual position on the lower side of the flower by the twisting of the ovarium; but in Malaxis the twisting has been carried so far that the flower occupies the position that it would have held if the ovarium had not been at all twisted, and which the ripe ovarium afterwards assumes, by a process of gradual untwisting” (Darwin, 1904, p. 131). And, “In many Orchids the ovarium (but sometimes the foot-stalk) becomes for a period twisted, causing the labellum to assume the position of a lower December 2009] Yam et al.—Darwin and his orchids 2147 Fig. 12. Resupination. (A) Dendrobium inflorescences, flowers resupinate to the extent necessary to position the labellum lowermost (Williams and Williams, 1894). (B) Extent of resupination as affected by the angle of the inflorescence. (C) Resupination by different flowers on the same inflorescence. (D) Resupination by a single untreated flower. (E) Resupination following removal of the gynstemium (column). (F) Resupination after emasculation. (B–E, Dr. Joseph Arditti’s laboratory, University of California, Irvine.) petal, so that insects can easily visit the flower; but from slow changes in the form or position of the petals, or from new sorts of insects visiting the flowers, it might be advantageous to the plant that the labellum should resume the normal position on the upper side of the flower, as is actually the case with Malaxis paludosa and some species of Catasetum, &c. This change, it is obvious, might be simply affected by the continued selection of varieties which had their ovaria less and less twisted; but if the plant only afforded varieties with the ovarium more twisted, the same could be attained by the selection of such variations, until the flower was turned completely round on its axis. This seems to have actually occurred with Malaxis paludosa, for the label- lum has acquired its present upward position by the ovarium being twisted twice as much as is usual” (Darwin, 1904, pp. 284, 28518). Darwin is correct in that most species resupinate until “the labellum [assumes] the position of a lower petal,” some do not, and the labellum is “on the upper side of the flower” (Fig. 11), and a few have the labellum uppermost because they turn “round completely” (for reviews, see Ernst and Arditti, 1994; Arditti, 2005). The following have been learned since Darwin’s time: 18 This is the 7th impression of the 2nd edition. It was written before Darwin’s death but published after it. 2148 [Vol. 96 American Journal of Botany • The torsion is usually approximately 180°, but the actual extent of turning is that which is necessary to place the labellum lowermost and depends on the position of the bud (Fig. 12A-12C). • Most of the torsion occurs shortly before and after anthesis (Fig. 12C). • In some species, buds alternate in turning clockwise and counterclockwise. • The untwisting described by Darwin is not limited to Malaxis. Flowers of several species deresupinate after pollination. • A few species resupinate 360°. • Some orchid species do not resupinate at all. • Resupination is a gravitropic phenomenon regulated by auxin, the same hormone that plays a role in the “poisonous” effects of pollen (Darwin, 1890) and also regulates phototropism in Avena and some of other plant movements studied by Darwin and his son (Darwin and Darwin, 1880). In resupinating flowers, turning is regulated by auxin, which seems to move basipetally from the pollinia (Fig. 12D–F). As with “poisonous pollen” and phototropism, auxin could have been discovered in research on resupination had anyone chosen to pursue it. However, it would have been more challenging because it is more difficult to work with resupinating orchid flower buds than with Avena coleoptiles.The general tone of Darwin’s descriptions of the twisting of the ovary (i.e., resupination) (Darwin, 1904, pp. 13, 284, 285) is teleological. Statements such as the following fit a definition of teleology that states that “an object or behavior is said to be teleological . . . when it gives evidence of design or appears to be directed toward certain ends” (Ayala, 1977): • “ . . . sepals are reflexed . . . apparently to allow insects to freely to visit. . . ,” • “The position of the labellum is the more remarkable, because it has been purposely acquired,” and • “labellum to assume the position of a lower petal, so that insects can easily visit the flower.” Karl Immanuel Eberhard Ritter19 von Goebel (1855–1932) called attention to Darwin’s teleological tendencies a century ago (Goebel, 1909, 1920, 1924). However, one current view is that “the evolutionary origin of living beings is teleological only in the indeterminate sense” (Ayala, 1977). This was interpreted (Ernst and Arditti, 1994) to mean that “traits come into existence and become established in populations because they serve a useful purpose. Resupination is such a trait. Besides, Darwin may well have been a teleologist” (Lennox, 1993). At this time, about 150 yr since Darwin became interested in orchids, it is hard to determine what drew him to them. It could have been their very presence near his home because “several kinds are common near Down” (Darwin, 1958). Or it may have been because, “If nature ever showed her playfulness in the formation of plants this is visible in the most striking way among the orchids . . . They take on the form of little birds, of lizards, of insects. They look like a man, like a woman. Sometimes like an austere sinister fighter, sometimes like a clown who excites our laughter. They represent the image of a lazy tortoise, a melancholy toad, an agile ever-chattering monkey. Nature has formed orchids in such a way that, unless they make us laugh, they surely excite our greatest admiration” (Breynius, 1678, translated by Oakes Ames and quoted by Arditti, 1966). Re19 Ritter means “knight” and is/was a title of nobility in German-speaking countries. gardless of what attracted Darwin at first—curiosity, admiration, an interesting image, or simply plants he looked at while taking a walk—he soon changed from a merely curious to an engrossed naturalist. His primary interest may have been the contrivances associated with pollination, but he also became intrigued by other features of these remarkable plants. By doing so, he showed that one can look at orchids both with great admiration and as plants that can be the subject of scientific studies. LITERATURE CITED Unless indicated otherwise, the J. Murray listed below is John Murray III (1808–1892), Darwin’s publisher. R. F. Cooke was a partner in the John Murray publishing firm. Online items were printed, but not necessarily read, on the day they were accessed. Ackerman, J. D. 1986. Mechanism and evolution in of food-deceptive pollination systems in orchids. Lindleyana 1: 108–113. Ackerman, J. 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The New Phytologist 145: 367–421. Arditti, J., and R. Ernst. 1984. Physiology of germinating orchid seeds. In J. Arditti [ed.], Orchid biology, reviews and perspectives, vol. III, 177–222. Cornell University Press, Ithaca, New York, USA. Arditti, J., R. Ernst, T. W. Yam, and C. Glabe. 1990. The contribution of orchid mycorrhizal fungi to seed germination: A speculative review. Lindleyana 5: 249–255. Arditti, J., and B. H. Flick. 1974. Postpollination phenomena in orchid flowers. V. Participation by the rostellum and gynostemium tip. American Journal of Botany 61: 643–651. Arditti, J., J. D. Michaud, and P. L. Healey. 1979. Morphometry of orchid seeds. I. Native California and related species of Cypripedium. American Journal of Botany 69: 1129–1139. December 2009] Yam et al.—Darwin and his orchids Arditti, J., J. D. Michaud, and P. L. Healey. 1980. Morphometry of orchid seeds. I. Native California and related species of Calypso, Cephalanthera, Corallorhiza, and Epipactid. 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Exoticarum aliarumque minus cognitaruna plantarum. Sumptibus Auctoris [published by the author], Gedani [an old name for Gdansk, Poland, or Danzig, Germany; in this case it probably refers to Germany because Breynius was German]. Brown, R. 1833. Observations on the organs and mode of fecundation in Orchideae and Asclepiadeae. Transactions of the Linnean Society of London. Botany 16: 685–720. Burgeff, H. 1936. Samenkeimung der Orchideen und entwicklung ihrer Keimpflanzen. Vberlag von Gustav Fischer, Jena, Germany. Chadwick, A. V., L. P. Nyman, and J. Arditti. 1986. Sites of ethylene evolution in orchid flowers. Lindleyana 1: 164–168. Cole, J. 1849. Orchids from seed. Gardeners’ Chronicle [Number 37, 15 September; in those days, this journal, which was initiated in 1841, had no volume numbers; it listed only issue number and date of publication]: 582. Cooke, R. F., and J. Murray. 1877. Letter 10771–Cooke, R. F., & John Murray, Publishers, to Darwin, C. R., 5 Jan 1877. 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Korrelationsuntersuchungen an entspreiteten Blattstielen mittels lebender Orchideenpollinien als Wuchstoffquelle. Jahrbücher für Wissenschaftliche Botanik 79: 681–713. Malpighi, M. 1675–1679. Anatome plantarum. De Floribus. Royal Society, London, UK. Maschmann, E., and F. Laibach. 1933. Über Wuchstoffe. Biochemische Zeitung 255: 446–452. Möller, A. [ed.], 1921. Fritz Müller, Werke, Briefe, Leben, 3rd ed. Gustav Fischer Verlag, Jena, Germany. Moore, D. 1849. On growing orchids from seeds. Gardeners’ Chronicle 9 [Number 35, 1 September; in those days, this journal, which was initiated in 1841, had no volume numbers; it listed only issue number and date of publication]: 549. Moore, D. 1850. Multiplication des orchidées de graine. Journal d’Horticulture Pratique de la Belgique 7: 234. Morita, K. 1918. Influences de la pollinisation et d’autres actions extéreurs sur la fleur du Cymbidium virens Lindl. Botanical Magazine (Tokyo) 32: 39–52. Müller, F. 1868. Ueber Befruchtungserscheinungen bei Orchideen. Botanische Zeitschrift 26: 630–632. Müller, F. 1886. Biologische Beobachtung an brasilianischen Orchideen. Verhandlungen der Botanischer Verein der Provinz Brandenburg 28: IV. Müller, J. F. T. 1866a. Letter 5226–Müller, J. F. T., to Darwin, C. R., 1 & 3 Oct 1866. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence of Charles Darwin. Vol. 14. Cambridge University Press, Cambridge. Müller, J. F. T. 1866b. Letter 5292a–Müller, J. F. T., to Darwin, C. R., 1 Dec 1866. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence of Charles Darwin. Vol. 14. Cambridge University Press, Cambridge. Müller, J. F. T. 1867a. Letter 5344a–Müller, J. F. T., to Darwin, C. R., 1 Jan 1867. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence of Charles Darwin. Vol. 15. Cambridge University Press, Cambridge Müller, J. F. T. 1867b. Letter 5429–Müller, J. F. T., to Darwin, C. R., 4 Mar 1867. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence of Charles Darwin. Vol. 15. Cambridge University Press, Cambridge Müller, J. F. T. 1867c. Letter 5480–Müller, J. F. T., to Darwin, C. R., 1 Apr 1867. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence of Charles Darwin. Vol. 15. Cambridge University Press, Cambridge Müller, J. F. T. 1877. Letter 10911–Müller, J. F. T., to Darwin, C. R., 25 Mar 1877. In: Burkhardt, Frederick, and Smith, Sydney. 1994. A Calendar to the correspondence of Charles Darwin 1821–1882. ed 2. Cambridge University Press, Cambridge. Müller, R. 1953. Zur quantitativen Bestimmung von Indolyl-essigsäure mittels Papierchromatographie ubd Papierelectrophorse. Beiträge zur Biologie der Pflanze 30: 1–32. 2152 American Journal of Botany Murray, J. 1861. Letter 3261–Murray, John (b), to Darwin, C. R., 23 Sep 1861. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence of Charles Darwin. Vol. 9. Cambridge University Press, Cambridge, p 276. Murray, J. 1866. Letter 5417–Murray, John (b), to Darwin, C. R., 24 Feb 1866. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence of Charles Darwin. Vol. 14. Cambridge University Press, Cambridge. Murray, J. 1874. Letter 9574–Murray, John (b), to Darwin, C. R., 29 July 1874. In: Burkhardt, Frederick, and Smith, Sydney. 1994. A Calendar to the correspondence of Charles Darwin 1821–1882. ed 2. Cambridge University Press, Cambridge. Murray, J. IV. 1919. John Murray III 1808–1892 a brief memoir. John Murray, Albemarle Street, W., London, UK. Nair, H., Z. M. Idris, and J. Arditti. 1991. Effects of 1-aminocyclopropane-1-carboxylic acid on ethylene evolution and senescence of Dendrobium (Orchidaceae) flowers. Lindleyana 6: 49–58. Paal, A. 1918. Uber phototropische Reizleitung. Jahrbuch für Wissenschaftliche Botanik 58: 406–458. Poddubnaya-Arnoldi, V. A., and N. V. Zinger. 1961. Application of biochemical technique to the study of embryonic processes in some orchids. Recent Advances in Botany 8: 711–714. Rumphius, G. E. 1741–1750. Herbarium amboinense [published by Joannes Burmannus]. Apud Franciscum Changuion, Joannem Catiffe and Hermannum Uytwerf, Amterdam, Netherlands. Scott, J. 1863. Letter 4202–Scott, John, to Darwin, C. R., 3 June 1863. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence of Charles Darwin. Vol. 11. Cambridge University Press, Cambridge, p 473. Singer, C. 1959. A history of biology to about the year 1900. AbelardSchuman, London. Sprengel, C. K. 1793. Das endeckte Geheimnis der Natur in Bau und in der Befruchtung der Blumen. Friedrich Vieweg dem Aeltern, Berlin, Germany (Reprint, 1972 by J. Cramer, 3301 Lehre, Germany). Stead, A. D. 1992. Pollination-induced flower senescence: A review. Plant Growth Regulation 11: 13–20. Strauss, M. S. 1976. The physiology of pollination induced phenomena in the Orchidaceae. Ph.D. dissertation, University of California, Irvine, California, USA. Strauss, M. S., and J. Arditti. 1984. Postpollination effects in orchid flowers. XII. Effects of pollination, emasculation, and auxin treatment on flowers of Cattleya Porcia ‘Cannizaro’ and the rostellum of Phalaenopsis. Botanical Gazette (Chicago, Ill.) 145: 43–49. Tilanus, C. B. 1925. Surgery a hundred years ago. Geofrey Bles, London, UK. Van Der Pijl, L., and C. H. Dodson. 1966. Orchid flowers, their pollination and evolution. University of Miami Press, Coral Gables, Florida, USA. Veitch, J., and Sons. 1887–1894. A manual of Orchidaceous plants, vol. I. Epidendreae. Royal Exotic Nursery, 514 King’s Road, Chelsea, S.W., UK. (Reprint 1963, A. Asher & Co., Amsterdam). Vermeulen, P. 1955. The rostellum of the Ophrydeae. American Orchid Society Bulletin 24: 239–245. Vermeulen, P. 1959. The different structures of the rostellum in Ophrydeae and Neottieae. Acta Botanica Neerlandica 8: 338–355. [Vol. 96 Vermeulen, P. 1966. The system of the orchidales. Acta Botanica Neerlandica 15: 224–253. W. F. H. B. 1897. Fritz Müller. Nature 56: 546–548. Wehner, U., W. Zierau, and J. Arditti. 2002. Plinius Germanicus and Plinius Indicus: Sixteenth and seventeenth century descriptions and illustrations of orchid “trash baskets,” resupination, seeds, floral segments and flower senescence in the European botanical literature. In T. Kull and J. Arditti [eds.], Orchid biology, reviews and perspectives, vol. VII, 37–140. Kluwer Academic Publishers, Boston, Massachusetts, USA. Weiss, F. E. 1916. Presidential address. Annual Report and Transactions, Manchester Microscopical Society [no volume number]: 32–43. Went, F. W. 1926. On growth accelerating substances in the coleoptile of Avena sativa. Proceedings of the Koenigliche Akademie der Wetenschappen 30: 10–19. Went, F. W. 1928. Wuchsstoff und Wachstum. Reueil des. Travaux Botaniques Neerlandais 24: 1–116. Went, F. W. 1990. Orchids in my life. In J. Arditti [ed.], Orchid biology, reviews and perspectives, vol V, 21–36. Timber Press, Portland, Oregon, USA. Went, F. W., and K. V. Thimann. 1937. Phytohormones. Macmillan, New York, New York, USA. Williams, B. S., and H. Williams. 1894. The orchid grower’s manual. Victoria and Paradise Nurseries, London, UK. Yam, T. W., and J. Arditti. 2009. History of orchid propagation: A mirror of the history of biotechnology. Plant Biotechnology Reports 3: 1–56. Yam, T. W., Y. N. Chow, P. N. Avadhani, C. S. Hew, J. Arditti, and H. Kurzweil. 2009. Pollination effects on orchid flowers and the first suggestion by Professor Hans Fitting (1877–1970) that plants produce hormones. In T. Kull, J. Arditti, and S. K. Wong [eds.], Orchid biology, reviews and perspectives, vol. X, 37–140. Springer Verlag, Boston, Massachusetts, USA. Yam, T. W., A. K. A. Ghani, S. Ichihashi, A. Thame, A. N. Rao, P. N. Avadhani, H. Nair et al. 2007. Time from pollination to fruit ripening, seed germination, and germination. In K. M. Cameron, J. Arditti, and T. Kull [eds.], Orchid biology, reviews and perspectives, vol. IX, 433–506. New York Botanical Garden Press, Bronx, New York, USA. Yam, T. W., H. Nair, C. S. Hew, and J. Arditti. 2002a. Orchid seeds and their germination: An historical account. In T. Kull and J. Arditti [eds.], Orchid biology, reviews and perspectives, vol. VII, 387–504. Kluwer Academic Publishers, Boston, Massachusetts, USA. Yam, T. W., E. C. Yeung, X.-L. Ye, S.-Y. Zee, and J. Arditti. 2002b. Orchid embryos. In T. Kull and J. Arditti [eds.], Orchid biology, reviews and perspectives, vol. VII, 287–385. Kluwer Academic Publishers, Boston, Massachusetts, USA. Zoller, H., M. Steinmann, and M. Schmid. 1972–1980. Conradi Gesneri Historia Plantarum faksimileausgabe. Bernard Rosenthal, San Francisco, California, USA. Reprints, copies or originals of most of the papers cited here (other than Darwin’s) as well as the correspondence referred to in the text are now in the library of the Singapore Botanic Gardens (SBG). They are part of a collection of orchid literature donated to SBG by Professor Joseph Arditti and his son Jonathan O. Arditti. December 2009] 2153 Yam et al.—Darwin and his orchids Appendix 1. Genera and species of Orchidaceae referenced in Darwin, C. R. 1877a. The Various Contrivances by Which Orchids Are Fertilised by Insects. 2nd ed. John Murray, London, UK. Page numbers are provided on the basis of this edition, and spellings are reproduced exactly as they appear within the index of the book. Names within brackets are those accepted currently by Govaerts, R. (2009). World Checklist of Orchidaceae. The Board of Trustees of the Royal Botanic Gardens, Kew. Published on the Internet; http://www.kew.org/wcsp/ accessed 2 August 2009. Aceras anthropophora, 26, 258 [Orchis anthropophora] —longibracteata, 26 [Barlia robertiana] Acianthus exsertus, 90 —fornicatus, 90, 280 —sinclairii, 90, 280 Acontia luctuosa, 31 [Acronia luctuosa = Pleurothallis luctuosa] Acropera, 154, 156, 276 [Gongora] —loddigesii, 166 [Gongora galeata] —luteola, 166, 239 [Gongora galeata] Aerides, 156, 265 —cornutum, 265 [Aerides odorata] —odorata, 158 —virens, 156 [Aerides odorata] Angræcum, 251 —distichum, 154 —eburneum, 155 —sesquipedale, 154, 162, 265, 282 Apostasia, 248 Barkeria, 146 Bolbophyllum, 274, 276 [Bulbophyllum] —barbigerum, 138 —cocoinum, 137 —cupreum, 137, 265 —rhizophoræ, 137 [Bulbophyllum falcatum var. velutinum] Cœlogyne cristata, 146 —truncata, 169 Coryanthes, 90, 173, 232, 265 Goodyera, 239, 260 —fieldingii, 175 —macrantha, 175 —speciosa, 174 —triloba, 281 [?] —discolor, 105 [Ludisia discolor] Cycnoches egertonianum, 224 Gymnadenia, 251 —ventricosum, 220–224 —albida, 43, 68 [Pseudorchis albida] —conopsea, 32, 40, 43, 65, 238, 239, 255, 271, 272 —odoratissima, 68 —tridentata, 68, 291 [Platanthera clavellata] Cymbidium giganteum, 155, 252, 260, 263 [Cymbidium iridiodes] Cypripedium, 226, 229, 262, 275 —acaule, 229 —barbatum, 239 [Paphiopedilum barbatum] —calceolus, 229–231, 282 —candidum, 235 —pubescens, 229, 230 [Cypripedium parviflorum var. pubescens] —purpuratum, 239 [Pahiopedilum purpuratum] Cyrtostylis, 90 Dendrobium, 287 —bigibbum, 142 —chrysanthum, 138–142, 265 —cretaceum, 142, 291 [Dendrobium polyanthum] —formosum, 142 —speciosum, 281 —tortile, 142 Goodyera pubescens, 105 —repens, 103, 105 Habenaria bifolia, 40, 43, 78, 251 [Platanthera bifolia] Habenaria chlorantha, 43, 69, 239, 244, 251 [Habenaria viridiflora] Herminium monorchis, 59, 61, 255 Lælia, 146 —cinnabarina, 148 [Sophronitis cinnabarina] Leptotes, 146 Liparis pendula, 239, 241 [Stichorkis viridiflora] Listera, 251, 287 [Neottia] —cordata, 124 [Neottia cordata] —ovata, 115–124, 276 [Neottia ovata] Disa, 265 Lycaste skinnerii, 155, 260 Malaxis, 251, 276 Bonatea speciosa, 71, 76, 244, 264, 361 —cornuta, 78 —grandiflora, 77, 281 [Disa uniflora] —macrantha, 78, 290 [Disa cornuta] Brassia, 156 Disperis, 265 Caladenia dimorpha, 89 Epidendrum cochleatum, 249 [Prosthechea cochleata] Calæna, 89 [Caleana] Calanthe dominii, 161 [Calanthe × dominii] —masuca, 161, 267, 269 [Calanthe sylvatica] —veratrifolia, 280 [Calanthe triplicata] —vestita, 162 Catasetum, 256, 270 —callosum, 192, 195 —luridum, 191 —mentosum, 206 —planiceps, 193 —saccatum, 180–185, 239 —tabulare, 192 —tridentatum, 191, 196, 197, 239, 256, 269 [Catasetum macrocarpum] —floribundum, 146, 249 [Epidendrum paniculatum] —glaucum, 146 [Dichaea glauca] Epipactis, 239, 251 —latifolia, 100, 101, 259, 282, 287 [Epipactis helleborine] —microphylla, 102 —palustris, 93–100, 275 —purpurata, 102 —rubiginosa, 102 [Epipactis atrorubens] —viridiflora, 102, 291 [Epipactis purpurata] Epipogium gmelini, 103 [Epipodium aphyllum] Cattleya, 143–148, 239, 265 Eulophia viridis, 156, 269 [? Eulophia viridiflora = Eulophia epidendraea] —crispa, 147 [Sophronitis crispa] Evelyna, 265 [Elleanthus] Cephalanthera, 277 —carivata, 146, 239, 241 [Elleanthus caravata] —ensifolia, 86 [Cephalanthera longifolia] —grandiflora, 80–86, 239, 242, 249, 259, 269, 277, 287, 290 [Cephalanthera longifolia] Galeandra funkii, 155 [Galeandra baueri] Chysis, 146 Cirrhæa, 171 Glossodia, 237 Gongora, 276 —atro-purpurea, 169 —maculata, 168 —paludosa, 32, 129–135, 239, 241, 258, 284 [Hammarbya paludosa] Masdevallia, 241, 274, 276 —fenestrata, 135, 136, 142 [Zootrophion fenestrata] Maxillaria, 156, 278 —ornithorhyncha, 157, 159 [?] Megaclinium falcatum, 138 [Bulbophyllum falcatum] Microstylus rhedii, 132, 135 [Malaxis resupinata] Miltonia clowesii, 154, 155 Monachanthus viridis, 196, 197, 198, 201 [Catasetum cernuum] Mormodes ignea, 208–219, 249, 276, 283 —luxata, 219 Myanthus barbatus, 192, 199, 203, 205 [Catasetum barbatum] Neotinia intacta, 27, 291 [Neotinea maculata] Neottia nidus-avis, 125, 258, 290 Nigritella angustifolia, 27 [Gymnadenia nigra] Notylia, 171 Odontoglossum, 156 Oncidium, 153, 156, 158, 239, 251, 266 2154 American Journal of Botany —unguiculatum, 252 Phalanopsis, 153, 159, 276 Selenipedium palmifolium, 232 Ophrys apifera, 52, 54–58, 259, 279, 291 —amabilis, 159 —grandiflora, 159, 269 [Phalaenopsis amabilis] Serapias cordigera, 27 —arachnites, 51 [Ophrys apifera] —aranifera, 50, 280 [Ophrys sphegodes] —muscifera, 32, 45, 49, 280 [Ophrys insectifera] —scolopax, 52, 292 Orchis fusca, 15, 25, 35, 37, 39, 273 [Orchis purpurea] —hircina, 25, 39, 273 [Himantoglossum hircinum] —latifolia, 15, 35, 37, 255 [Dactylorhiza incarnata] —maculata, 15, 32, 34, 35, 37, 39, 255, 277, 278 [Dactylorhiza maculata] Orchis mascula, 6, 273, 278 —militaris, 36, 37 —morio, 15, 33, 37, 39, 128, 278 [Anacamptis morio] —pyramidalis, 16, 21, 34, 37, 38, 39, 254, 256, 260, 261, 264, 272, 273 —ustulata, 25 [Neotinea ustulata] Ornithocephalus, 160 Peristylus viridis, 43, 63, 255 [Coeloglossum viride] Phaius, 146 —grandifolius, 280 [Phaius tankervilleae] Platanthera, 75 —chlorantha, 69 —dilatata, 77 [Piperia dilatata] —flava, 76, 77 —hookeri, 75 —hyperborea, 76, 291 Pleurothallis ligulata, 135 [Stelis ligulata] Sobralia macrantha, 91 Sophronitis, 146 Spiranthes australis, 114, 275, 291 [Spiranthes sinensis] —autumnalis, 106–114, 239 —cernua, 111 —gracilis, 111 [Chlorosa gracilis] —prolifera, 135 [Acianthera prolifera] Stanhopea, 155, 276 Pogonia ophioglossoides, 86 —devoniensis, 171 [Stanhopea hernandezii] —oculata, 171 Pterostylis, 232 —longiflora, 87, 89 [? Pterostylis longifolia] —trullifolia, 86, 88, 280 Rodriguezia secunda, 159 [Rodrigueza lanceolata] Stelis, 274 —racemiflora, 135 [Stelis quadrifida] Thelymitra, 291 —suaveolens, 156, 159 [Gomesa foliosa] —carnea, 127, 280 —longiflora, 127 [? Thelymitra longifolia] Saccolabium, 153, 156 Uropedium, 240 [Phragmipedium] Sarcanthus, 276 [Cleisostoma] Vanilla aromatica, 90 [Vanilla planifolia] —parishii, 142 [Cleisostoma parishii] —teretifolius, 154, 156, 268 [Cleisostoma simondii] Warrea, 155, 270 Zygopetalum mackai, 155 [Zygopetalum maculatum]