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.
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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),
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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
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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.
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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
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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).
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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
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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]
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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).
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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).
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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.
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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
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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
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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
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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).
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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]
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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.
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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
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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. D., and A. M. Montalvo. 1990. Short- and long-term limitations to fruit production in tropical orchid. Ecology 71: 263–272.
Ackerman, J. D., and J. K. Zimmerman. 1994. Bottlenecks in the life
histories of orchids: Resources, pollination, population structure,
and seedling establishment. In A. Pridgeon [ed.], Proceedings of the
14th World Orchid Conference, Glasgow 1993, 125–129. HMSO
Publications, Glasgow.
Anonymous. 1880. What Mr. Darwin saw in his voyage round the world in
the ship “Beagle.” Harper & Brothers, New York, New York, USA.
Anonymous. 1922. Orchid mycorrhiza. Orchid Review 30: 78–81 [probably by G. Wilson].
Anonymous. 2008. Orchids. Darwin form orchids to variation. Website
http://en.wikipedia.org/wiki/Darwin_from_Orchids_to_Variation [accessed 15 December 2008].
Arditti, J. 1966. Orchids. Scientific American 214: 70–78.
Arditti, J. 1967. Factors affecting the germination of orchid seeds.
Botanical Review 33: 1–97.
Arditti, J. 1971. Orchids and the discovery of auxin. American Orchid
Society Bulletin 40: 211–214.
Arditti, J. 1975. Orchids, pollen poison, Pollenhormon and plant hormones. Orchid Review 83: 127–129.
Arditti, J. 1979. Aspects of the physiology of orchids. In H. W.
Woolhouse [ed.], Advances in botanical research, vol. 7, 421–655.
Academic Press, London, UK.
Arditti, J. 1984. An history of orchid hybridization, seed germination and tissue culture. Botanical Journal of the Linnean Society 89:
359–381.
Arditti, J. 1990. Lewis Knudson (1884–1956): His science, his times,
and his legacy. Lindleyana 5: 1–79.
Arditti, J. 1992. Fundamentals of orchid biology. John Wiley, New
York, New York, USA.
Arditti, J. 2005. Resupination. In H. Nair and J. Arditti [eds.],
Proceedings of the Seventeenth World Orchid Conference, Shah
Alam 2002. Natural History Publications (Borneo), Kota Kinabalu,
Sabah, Malaysia.
Arditti, J., and A. K. Abdul Ghani. 2000. Numerical and physical
properties of orchid seeds and their biological implications. 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. American Journal of
Botany 67: 347–360 .
Avadhani, P. N., H. Nair, J. Arditti, and C. S. Hew. 1994. Physiology of
orchid flowers. In J. Arditti [ed.], Orchid biology, reviews and perspectives,
vol. VI, 189–362. Cornell University Press, Ithaca, New York, USA.
Ayala, F. J. 1977. Philosophical issues. In T. Dobzhanski, F. J. Ayala,
G. L. Stebbins, and J. W. Valentine [eds.], Evolution. W. H. Freeman
and Co., San Francisco, California, USA.
Beekman, E. M. 1999. Rumphius: The Ambonese curiosity cabinet. Yale
University Press, New Haven, Connecticut, USA.
Beer, J. G. 1863. Beiträge zur morphologie und biologie der familie
der orchideen. Druck und Verlag von Carl Gerold’s Sohn, Vienna,
Austria.
Bernard, N. 1899. Sur la germination du Neottia nidus-avis. Comptes
Rendus Académie des Sciences, Paris 128: 1253–1255.
Boysen-Jensen, P. 1913. Uber die Leitung des phototropischen Reizes in
der Avenakoleoptile. Berichte der Deutsche Botanischge Gesselschaft
31: 559–566.
Breynius, J. 1678. 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. In: Burkhardt,
Frederick, and Smith, Sydney. 1994. A Calendar to the correspondence of Charles Darwin 1821–1882. ed 2. Cambridge University
Press, Cambridge.
Correvon, H. 1899. Album des orchidees de l’Europe centrale et septentrionale. Librarie Georg et Cie, Geneva, Switzerland.
Darwin, C. R. 1859. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. John
Murray, London.
Darwin, C. R. 1860a. Letter 3290–Darwin, C. R., to Hooker, J. D., 19 June
1860. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 13 (Suppl). Cambridge University Press,
Cambridge.
Darwin, C. R. 1860b. Letter 2838–Darwin, C. R., to Lyell, Charles,
20 June 1860. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 8. Cambridge University
Press, Cambridge, p 262.
Darwin, C. R. 1860c. Letter 2871–Darwin, C. R., to Hooker, J. D., 19 July
1860. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence of
Charles Darwin. Vol. 8. Cambridge University Press, Cambridge, p 292.
Darwin, C. R. 1860d. Letter 2892–Darwin, C. R., to Hooker, J. D., 7 Aug
1860. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence of
Charles Darwin. Vol. 8. Cambridge University Press, Cambridge, p 313.
Darwin, C. R. 1860e. Letter 2956–Darwin, C. R., to Oliver, Daniel,
20 Oct 1860. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 8. Cambridge University
Press, Cambridge, p 439.
Darwin, C. R. 1861a. Letter 3061–Darwin, C. R., to Gardeners’ Chronicle
[before 9 Feb 1861. Website http://www.darwinproject.ac.uk/darwinletters/calendar/entry-3061.html [accessed 15 December 2008].
Darwin, C. R. 1861b. Letter 3174–Darwin, C. R., to More, A. G., 2 June
1861. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence of
Charles Darwin. Vol. 9. Cambridge University Press, Cambridge, p 159.
2149
Darwin, C. R. 1861c. Letter 3190–Darwin, C. R., to Hooker, J. D., 19 June
1861. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 9. Cambridge University Press, Cambridge,
p 181.
Darwin, C. R. 1861d. Letter 3207–Darwin, C. R., to Hooker, J. D., 13 July
1861. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 9. Cambridge University Press, Cambridge,
p 201.
Darwin, C. R. 1861e. Letter 3220–Darwin, C. R., to Hooker, J. D., 27 July
1861. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 9. Cambridge University Press, Cambridge,
p 220.
Darwin, C. R. 1861f. Letter 3221–Darwin, C. R., to Hooker, J. D., 28
July–10 Aug 1861. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 9. Cambridge University
Press, Cambridge, p 222.
Darwin, C. R. 1861g. Letter 3238–Darwin, C. R., to Hooker, J. D., 30 Aug
1861. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 9. Cambridge University Press, Cambridge,
p 243.
Darwin, C. R. 1861h. Letter 3259–Darwin, C. R., to Murray, John
(b), 21 Sep 1861. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 9. Cambridge University
Press, Cambridge, p 272.
Darwin, C. R. 1861i. Letter 3262–Darwin, C. R., to More, A. G., 23 Sep
1861. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 9. Cambridge University Press, Cambridge,
p 275.
Darwin, C. R. 1861j. Letter 3263–Darwin, C. R., to Hooker, J. D., 24 Sep
1861. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 9. Cambridge University Press, Cambridge,
p 277.
Darwin, C. R. 1861k. Letter 3264–Darwin, C. R., to Murray, John
(b), 24 Sep 1861. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 9. Cambridge University
Press, Cambridge, p 278.
Darwin, C. R. 1861l. Letter 3273–Darwin, C. R., to More, A. G., 1 Oct
1861. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 9. Cambridge University Press, Cambridge,
p 291.
Darwin, C. R. 1861m. Letter 3274–Darwin, C. R., to Bates, H. W., 2 Oct
1861. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 9. Cambridge University Press, Cambridge,
p 292.
Darwin, C. R. 1861n. Letter 3275–Darwin, C. R., to Murray, John
(b), 3 Oct 1861. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 9. Cambridge University
Press, Cambridge, p 293.
Darwin, C. R. 1861o. Letter 3276a–Darwin, C. R., to Murray, John
(b), 5 Oct 1861. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 9. Cambridge University
Press, Cambridge, p 294.
Darwin, C. R. 1861p. Letter 3284–Darwin, C. R., to Darwin, W. E., 12 Oct
1861. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 9. Cambridge University Press, Cambridge,
p 302.
Darwin, C. R. 1861q. Letter 3289–Darwin, C. R., to Lindley, John 18 Oct
1861. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 9. Cambridge University Press, Cambridge,
p 308.
Darwin, C. R. 1861r. Letter 3291–Darwin, C. R., to Lyell, Charles 20 Oct
1861. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence of
Charles Darwin. Vol. 9. Cambridge University Press, Cambridge, p 309.
Darwin, C. R. 1861s. Letter 3301–Darwin, C. R., to Hooker, J. D., 27 Oct
1861. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 9. Cambridge University Press, Cambridge,
p 323.
Darwin, C. R. 1861t. Letter 3337–Darwin, C. R., to Hooker, J. D., 1 Dec
1861. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
2150
American Journal of Botany
of Charles Darwin. Vol. 9. Cambridge University Press, Cambridge,
p 361.
Darwin, C. R. 1862a. Letter 3442–Darwin, C. R., to Murray, John
(b), 9 Feb 1862. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 10. Cambridge University
Press, Cambridge, p 76.
Darwin, C. R. 1862b. Letter 3484–Darwin, C. R., to Hooker, J. D., 26 Mar
1862. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 10. Cambridge University Press, Cambridge,
p 135.
Darwin, C. R. 1862c. Letter 3501–Darwin, C. R., to Murray, John
(b), 9 Apr 1862. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 10. Cambridge University
Press, Cambridge, p 148.
Darwin, C. R. 1862d. Letter 3520–Darwin, C. R., to Darwin, W. E., 26 Apr
1862. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 10. Cambridge University Press, Cambridge,
p 170.
Darwin, C. R. 1862e. Letter 3531–Darwin, C. R., to Murray, John (b), 2 May
1862. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence of
Charles Darwin. Vol. 10. Cambridge University Press, Cambridge, p
177.
Darwin, C. R. 1862f. Letter 3560–Darwin, C. R., to More, A. G., 18 May
1862. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 10. Cambridge University Press, Cambridge,
p 209.
Darwin, C. R. 1862g. Letter 3570–Darwin, C. R., to Wallace, A.
R., 24 May 1862. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 10. Cambridge University
Press, Cambridge, p 218.
Darwin, C. R. 1862h. Letter 3560–Darwin, C. R., to Murray, John
(b), 24 Aug 1862. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 10. Cambridge University
Press, Cambridge, p 209.
Darwin, C. R. 1862i. On the various contrivances by which British and
foreign orchids are fertilised by insects and the good effects of intercrossing. John Murray, Albemarle Street, London. UK.
Darwin, C. R. 1863a. Letter 4061–Darwin, C. R., to Hooker, J. D., 26 Mar
1863. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence of
Charles Darwin. Vol. 11. Cambridge University Press, Cambridge, p 265.
Darwin, C. R. 1863b. Letter 4185–Darwin, C. R., to Scott, John, 25
& 28 May 1863. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 11. Cambridge University
Press, Cambridge, p 448.
Darwin, C. R. 1865a. Letter 4916–Darwin, C. R., to Müller, J. F.
T., 17 Oct 1865. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 13. Cambridge University
Press, Cambridge.
Darwin, C. R. 1865b. Letter 4949–Darwin, C. R., to Müller, J. F.
T., 9 Dec 1865. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 13. Cambridge University
Press, Cambridge.
Darwin, C. R. 1866a. Letter 5050–Darwin, C. R., to Müller, J. F. T.,
9 and 15 Apr 1866. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 14. Cambridge University
Press, Cambridge.
Darwin, C. R. 1866b. Letter 5216–Darwin, C. R., to Müller, J. F.
T., 25 Sep 1865. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 14. Cambridge University
Press, Cambridge.
Darwin, C. R. 1866c. Letter 5050–Darwin, C. R., to Müller, J. F. T., 26 Sep
1866. In: Burkhardt, Frederick, et al., eds. 2003. The Correspondence
of Charles Darwin. Vol. 14. Cambridge University Press, Cambridge.
Darwin, C. R. 1866d. Letter 5261–Darwin, C. R., to Müller, J. F. T.,
before 10 Dec 1866. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 14. Cambridge University
Press, Cambridge.
Darwin, C. R. 1866–1867. Letter 5331–Darwin, C. R., to Müller, J. F.
T., late Dec 1866 & 1 Jan 1867. In: Burkhardt, Frederick, et al., eds.
[Vol. 96
2003. The Correspondence of Charles Darwin. Vol. 14. Cambridge
University Press, Cambridge.
Darwin, C. R. 1867a. Letter 5509–Darwin, C. R., to Müller, J. F.
T., 22 Apr 1867. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 15. Cambridge University
Press, Cambridge.
Darwin, C. R. 1867b. Letter 5551–Darwin, C. R., to Müller, J. F. T.,
26 May 1867. In: Burkhardt, Frederick, et al., eds. 2003. The
Correspondence of Charles Darwin. Vol. 15. Cambridge University
Press, Cambridge.
Darwin, C. R. 1868. Letter 6230–Darwin, C. R., to Farrer, T. H., 7 June,
1868. In: ML 2: 373.
Darwin, C. R. 1869. Letter 6835–Darwin, C. R., to Müller, J. F. T., 18
July 1869. In: ML 2: 356.
Darwin, C. R. 1870. De la fécondation des orchidées par les insectes et
des bons résultats du croisement. C. Reinwald, Paris, France.
Darwin, C. R. 1876. Letter 10603–Darwin, C. R., to Cooke, R. F., &
(John Murray, Publishers), 16 Sept 1876. In: ML 3: 292.
Darwin, C. R. 1877a. On the various contrivances by which British
and foreign orchids are fertilised by insects, 2nd ed. John Murray,
Albemarle Street, London, UK.
Darwin, C. R. 1877b. On the various contrivances by which British and
foreign orchids are fertilised by insects, 2nd ed. D. Appleton, New
York, New York, USA.
Darwin, C. R. 1877c. Die verschiedenen Einrichtungen durch welche
Orchideen von Insecten befruchtet werden, Zweite durchgesehene
Auflage. E. Schweizerbart’sche Verlagshandlung (E. Koch), Stuttgart,
Germany.
Darwin, C. R. 1878. Letter 11698–Darwin, C. R., to Müller, H. L. H., 20
Sep 1878. In: ML 2: 419.
Darwin, C. R. 1880a. Letter 12485–Darwin, C. R., to Bentham, George,
16 Feb 1880. In: ML 2: 423.
Darwin, C. R. 1880b. The variation of animals and plants under domestication, vol. II. D. Appleton and Company, New York, New York, USA.
Darwin, C. R. 1890. The variations of animals and plants under domestication. D. Appleton and Company, New York, New York, USA
Darwin, C. R. 1891. De la fécondation des orchidées par les insectes et
des bons résultats du croisement. 2nd printing called “2nd edition.” C.
Reinwald, Paris, France.
Darwin, C. R. 1904. On the various contrivances by which British and
foreign orchids are fertilised by insects, 7th impression of the 2nd ed.
John Murray, Albemarle Street, London, UK.
Darwin, C. R., and F. Darwin. 1880. The power of movement in plants.
John Murray, Albemarle Street, London, UK.
Darwin, C. R., and F. Darwin. 1898. The power of movement in plants.
D. Apleton Company, New York, New York, USA.
Darwin, F. [ed.]. 1958. The autobiography of Charles Darwin and selected letters. Dover Publications, New York, New York, USA; also
available on the Gutenberg Project Website http://www.gutenberg.
org/files/2010/2010-h/2010-h.htm [accessed 05 January 2008].
Diem, K. [ed.]. 1962. Documenta Geigy. Geigy Pharmeceutical, Geigy
Chemical Company, Ardsley, New York, USA.
Dressler, R. L. 1961. The structure of the orchid flower. Missouri
Botanical Garden Bulletin 49: 60–69.
Dressler, R. L. 1981. The orchids: natural history and classification.
Harvard University Press, Cambridge, Massachusetts, USA.
Ernst, R., and J. Arditti. 1994. Resupination. In J. Arditti [ed.],
Orchid biology, reviews and perspectives, vol VI, 135–188. Cornell
University Press, Ithaca, New York, USA.
Fay, M. F., and M. W. Chase. 2009. Orchid biology: From Linnaeus via
Darwin to the 21st century. Annals of Botany 104: 359–364 .
Fitting, H. 1907. Die Leitung Tropistischer Reize in parallelotropen
Pflanzenteilen. Jahrbuch für Wissenschaftliche Botanik 44: 177–253.
Fitting, H. 1909a. Die Beeinflussung der Orchideenblüten durch die
Bestäubung und durch andere Umstände. Zeitschrift für Botanik 1:
1–86.
Fitting, H. 1909b. Die Beeinflussung der Orchideenblüten durch die
Bestäubung und durch andere Umstände. [abstract] Botanische
Jahrbuch für Systematik 43: 24.
December 2009]
Yam et al.—Darwin and his orchids
Fitting, H. 1909c. Entwicklungsphysiologische Probleme der Fruchtbildung.
Biologisches Centralblatt 19: 193–205, 225–239.
Fitting, H. 1910. Weitere entwicklungsphysiologische Untersuchungen
an Orchideenblüten. Zeitschrift für Botanik 2: 225–267.
Fitting, H. 1911. Untersuchungen über die vorzeitige Entblätterung von
Blüten. Jahrbuch für Wissenschaftliche Botanik 49: 187–266.
Fitting, H. 1912. Über eigenartige Farbänderungen von Blüten and
Blütenfarbstoffen. Zeitschrift für Botanik 4: 81–105.
Fitting, H. 1921. Das Verblühen der Blüten. Naturwissenschaften
9: 1–9.
Fitting, H. 1936. Die Hormone als physiologische Reizstoffe.
Biologisches Centralblatt 56: 69–86.
Gallier, R. 1849a. Orchids from seed. Gardeners’ Chronicle Number
[Number 42, 20 October; in those days, this journal, which was initiated in 1841, had no volume numbers; it listed only issue number and
date of publication]: 661.
Gallier, R. 1849b. Orchids from seed. Orchid Review 57: 171.
Garay, L. A. 1960. On the origin of the Orchidaceae. Botanical Museum
Leaflets, Harvard University 13: 57–96.
Gesner, C. 1751. Opera botanica (published by C. I. Trew and C. C.
Schmiedel). Seligmani, Norimbergae (Nurnberg), Germany.
Goebel, K. 1909. The biology of flowers. In A. C. Seward [ed.], Darwin
and modern science. Website http://www.stephenjaygould.org/library/
modern-science/ [accessed 18 February 2009].
Goebel, K. 1920. Die Entfaltungsbewegungen der Pflanzen und deren
teleologische Deutung. Verlag Gustav Fischer, Jena.
Goebel, K. 1924. Die Entfaltungsbewegungen der Pflanzen und deren
teleologische Deutung, 2nd ed. Verlag Gustav Fischer, Jena.
Harrison, C. R. 1977. Ultrastructural and histochemical changes during the germination of Cattleya aurantiaca (Orchidaceae). Botanical
Gazette (Chicago, Ill.) 138: 41–45.
Harrison, C. R., and J. Arditti. 1976. Post-pollination phenomena in
orchid flowers. VII. Phosphate transport. American Journal of Botany
63: 911–918.
Harrison, C. R., and J. Arditti. 1978. Physiological changes during the
germination of Cattleya aurantiaca (Orchidaceae). Botanical Gazette
(Chicago, Ill.) 139: 180–189.
Hildebrand, F. 1863a. Die Fruchbildung der Orchideen, ein beweiss fur
die doppelte wirkung des Pollens. Botanische Zeitung 21: 329–333;
337–345.
Hildebrand, F. 1863b. On the impregnation of orchids, as a proof of the
two different effects of the pollen. Annals and Magazine of Natural
History Series III 12: 169–174.
Hildebrand, F. 1865. Basdardirungsversuche an orchideen. Botanische
Zeitung 23: 245–249.
Jacquet, P. 2007. A translation of the writings of Noël Bernard. In K. M.
Cameron, J. Arditti, and T. Kull [eds.], Orchid biology, reviews and
perspectives vol. IX, 311–431. New York Botanical Garden Press,
New York, New York, USA.
Jennings, S. 1875. Orchids: And how to grow them in India and other
tropical climates. L. Reeve & Co., London, UK [facsimile CD edition
by www.biolib.de and www.BioLiteraturShop.de].
Klass, C. S. 1964. The extraction and identification of free auxin from orchid
pollinia. M.A. Thesis, Brooklyn College, Brooklyn, New York, USA.
Knudson, L. 1929. Physiological investigations on orchid seed germination. Proceedings of the International Congress of Plant Science 2:
1183–1189.
Koopowitz, H., and T. A. Marchant. 1998. Postpollination nectar reabsorption in the African epiphyte Aerangis verdickii (Orchidaceae).
American Journal of Botany 85: 508–512.
Kull, T. 1998. Fruit set and recruitment in populations of Cypripedium
calceolus L. in Estonia. Biological Journal of the Linnean Society.
Linnean Society of London 126: 27–38.
Kurzweil, H. 2005. The structure of orchid flowers. In H. Nair and J.
Arditti [eds], Proceedings of the 17th World Orchid Conference, Shah
Alam 2002, 105–110. Natural History Publications (Borneo), Kota
Kinabalu, Sabah, Malaysia.
Laibach, F. 1929. Untersuchungen über die Postfloration tropischer
Orchideen. Planta 9: 341–387.
2151
Laibach, F. 1932. Pollenhormon und Wuchstoff. Berichte der Deutschen
Botanischen Gesellschaft 50: 383–390.
Laibach, F. 1933a. Wuchstoffversuche mit lebenden Orchideenpollinien.
Berichte der Deutschen Botanischen Gesellschaft 51: 336–340.
Laibach, F. 1933b. Versuche mit Wuchstoffpaste. Berichte der Deutschen
Botanischen Gesellschaft 51: 386–392.
Laibach, F., and P. Kornmann. 1933. Zur Frage des Wuchstofftransportes
in der Haferkoleoptile. Planta 21: 396–418 .
Laibach, F., and E. Maschmann. 1933. Über den Wuchstoff der
Orchideenpollinien. Jahrbücher für Wissenschaftliche Botanik 78:
399–430.
Lee, J. 1774. An introduction to botany. Containing an explanation of
that science, extracted from the work of Dr. Linnaeus, 3rd ed. J. F. and
C. R. Rivington, London, UK.
Lennox, G. J. 1993. Darwin was a teleologist. Biology and Philosophy
8: 409–421.
Lindley, J. 1826. Orchidearum sceletos, reproduced in Linnaea 2:
527–532.
Lindley, J. 1830–1840. The genera and species of orchidaceous plants.
553 pages. Ridgways, London, UK.
Linnaeus, C. 1780. Philosophia botanica 2. D. Johannes Gottlieb
Gleditsch, Berolini (Berlin), Germany.
Mai, G. 1934. 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]
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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
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—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]