Beauty and the seed

One of the real pleasures afforded in reading Charles Darwin’s correspondence is the discovery
of areas of research on which he never published, but which interested him deeply. We can gain
many insights about Darwin’s research methods by following these
‘letter
trails’ and observing how correspondence served as a
vital research tool for him.

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The duke of Argyll

One such story begins with the preparation of a new edition of
On the Origin of
Species (the fourth) in 1866. Darwin made substantive changes
to every new edition of Origin; often the changes were inspired by recent criticism
or new research. In 1865, George Douglas Campbell, the eighth duke of Argyll, had written an
article that appeared in parts in the magazine Good Words entitled the
‘Reign of law’. The article contained an argument about beauty in
nature.

The duke, who was best known for his interest in geology and ornithology, claimed:

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The Lamprolaima rhami hummingbird

Spangles of the emerald are no better in the battle of life than spangles of the ruby. A
crest of flame does not enable a Humming Bird to reach the curious recesses of an orchid better
than a crest of sapphire. … The evidence is indeed abundant, that ornament and
variety are provided for in nature for themselves and by themselves, separate from all other
use whatever. Any theory on the origin of species which is too narrow to hold this fact, must
be taken back for enlargement and repair.

Reign of Law, p. 231.

Campbell’s was only the latest statement of a common argument against Darwin’s theory, one he
had dealt with already in Origin but which he now felt compelled to expand on as he
prepared a fourth edition of the book.

Holly berries on the branch

Spindle-wood berries on the branch

Darwin began with the argument that
‘the idea of the beauty of any particular
object obviously depends on the mind of man, irrespective of any real quality in the admired
object; and that the idea is not an innate and unalterable element in the mind,’
and continued,
‘On the view of beautiful objects having been created for man’s
gratification, it ought to be shown that there was less beauty on the face of the earth before
man appeared than since he came on the stage. Were the beautiful volute and cone shells of the
Eocene epoch, and the gracefully sculptured ammonites of the Secondary period, created that man
might ages afterwards admire them in his cabinet?’
After mentioning sexual selection as another instance of beauty-with-a-purpose, Darwin turned to
the plant world and remarked:

that the gaily-coloured fruit of the spindle-wood tree and the scarlet berries of the holly
are beautiful objects, will be admitted by every one. But this beauty serves merely as a guide
to birds and beasts, that the fruit may be devoured and the seeds thus disseminated: I infer
that this is the case from having as yet found in every instance that seeds, which are embedded
within a fruit of any kind, that is within a fleshy or pulpy envelope, if it be coloured of any
brilliant tint, or merely rendered conspicuous by being coloured white or black, are always
disseminated by being first devoured.

Origin, 4th ed., p. 240.

… or are they?

Fritz Müller

Towards the end of September 1866 Darwin received a letter from Fritz Müller, a German
naturalist who had emigrated to Brazil in 1852, and who had begun to correspond with Darwin only
a year earlier. The letter is now incomplete; Darwin had pasted one fragment of it into his
experimental notebook for reference.

What interested Darwin so much was something that had been on his mind since writing that
‘in every instance’ seeds were surrounded by a fleshy pulp and
‘always disseminated by being first devoured’. Müller had noted that
seeds that fell to the ground as soon as the capsule opened were commonly dark-coloured, but
those that remained attached to the valve were brightly coloured – or had brightly
coloured surrounds – to attract attention.

Digital composite showing fragment of letter from Fritz Müller to Charles Darwin, 2 Aug
1866, where it was pasted into Darwin’s experimental notebook.

Seeds use to fall to the ground, as soon as the seed-capsules open and in this case they are
commonly dark-coloured; if on the contrary, they remain attached to the open valvæ,
in all the cases, I know, either the seeds themselves, or the arillus, or the interior of the
valvæ are brightly coloured so as to attract the attention, which may carry the seeds
to distant places. Thus the large valvæ of a Tabernaemontana are filled with a
bright red pulpa;—the black and shining seeds of a Paullinia are half-imbedded
into a white arillus and fixed to red valvæ,—and the seeds of a fine small
tree related to Acacia or Inga, which also for some time remain attached to the
valvæ, are black and white and visible at a great distance.—

Fritz Müller to Charles Darwin, 2 Aug 1866.
See the letter

Darwin immediately responded:

I have been much interested by what you say on seeds which adhere to the valves being
rendered conspicuous: you will see in the new Edit. of the origin why I have alluded to the
beauty & bright colours of fruit; after writing this, it troubled me that I
remembered to have seen brilliantly coloured seed, & your view occurred to me. There is
a species of Peony in which the inside of the pod is crimson & the seeds dark purple. I
had asked a friend to send me some of these seeds, to see if they were covered with any thing
which c^d prove attractive to birds. I rec^d some seeds the day after
receiving your letter; & I must own that the fleshy covering is so thin that I can
hardly believe it w^d lead birds to devour them; & so it was in an analogous
case with Passiflora gracilis. How is this in the cases mentioned by you? The whole case seems
to me rather a striking one.

Darwin, C. R. to Müller, J. F. T., 25 Sept [1866]
See
the letter

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Mauro Galetti: profile of an ecologist

src=”images/stories/ImagesNotManuscriptsNorPrintedMatter/PortraitsHumans/mauro_galetti/mauro_galetti_in_pantanal_200w.jpg”
title=”Prof. Mauro Galetti”
alt=”A smiling man with a short dark beard and moustache kneels for the camera. He is wearing rimless glasses, tan shirt, trousers and hat, and has a pair of binoculars slung around his neck.”
style=”float:right; margin: 0 0 10px 10px;”/>Like every kid, I always liked to be in the woods
and watch animals in the zoo. When I decided to start my career in biology in Brazil, I did not
really know what kind of job I would take, but I knew that to be successful in any career I
needed to do what I enjoyed most. While at university I started studying the behavior of howler
monkeys in a forest near my university. Twice a week I spent the whole morning studying what
they ate, where they moved, how they divided the space with other animals. This gave me
experience and time to watch other organisms in the forest, such as squirrels, birds, capuchin
monkeys and, of course, plants. As a zoologist, I never realized how complex and interesting
the strategies are that plants have evolved to attract animals for pollination or seed
dispersal. I started collecting all kind of fruits in this wood and described for each species
the strategy that they used for dispersal. Some fruits are dispersed by wind, a few by ants,
but most of them (in Brazil) are dispersed by birds or mammals. My second favorite place was
always the library of my university. After coming from the field, I spent one or two hours
reading the scientific journals and books. Knowing what the “top scientists” are studying and
why they are doing their research is a fundamental step for every student. Since most of the
journals or books were in English, it took me a long time to translate each paper, or each
book. This is certainly the largest barrier to doing science in non-English-speaking countries.
Now, describing fruit strategies is a kind of hobby and job, and I enjoy traveling to new
places to compare how plants disperse their fruits. This is relevant to understanding evolution
and ecology, and has been a major tool in speeding up the restoration of wild places.

In one of these places I came across an Ormosia tree, full of red and black seeds,
with no pulp. I knew from old naturalists, like Darwin, Ridley and van der Pijl, that some
fruits ‘tried’ to mislead birds and evolved colourful fruits but no
fleshy reward, the so-called mimetic seeds. I never took this idea for granted, and decided to
investigate on my own. So, I spent two years coming every month to this place to study this
species. First, I marked and mapped all Ormosia trees. I could find no more than eight
trees in a 2200 hectare region! They were very rare. In the meantime, I also found several
other species with the same strategy: Margaritaria nobilis, Rhynchosia
pyramidalis and Abrus precatorius. After marking all the Ormosia, I started
watching every morning, to see whether any bird would come to eat its mimetic fruits. After
many, many days, no success. In the same place I found some fruiting trees of Copaifera
langsdorffii, a leguminous tree, with a very similar fruit display, but with a pulp reward
for the dispersers. So, I started my experiments transplanting Copaifera arils to
Ormosia seeds and placed them on the ground to see whether wild birds would take them.
Later, I decided to try with captive birds. My findings show that it is hard to mislead a bird,
but naïve (captive-born) birds are easily misled by Ormosia seeds. Nowadays, I continue
studying the adaptations of fruits to dispersal, especially the ones dispersed by extinct
megafauna.

This letter must have crossed in the post with a follow-up one from Müller
(see the letter),
who had found more examples of the phenomenon including
‘a tree, probably belonging
to the Mimoseae, which after the opening of the seed-capsules presents a truly magnificent
aspect, being covered over and over with large and elegant curls of pale yellowish silk, (the
spirally contracted valves) beset with brilliant red pearls.’
By the time he received Darwin’s letter he had found yet more examples and speculated,

‘With Mimosa and Rhynchosia there is no fleshy hull but the seeds are
exceptionally hard and since gallinaceous birds often swallow small stones in order to promote
the breaking up of their food, I imagined that these hard and conspicuous seeds could well serve
the same purpose when swallowed by our Jacús (Penelope) or other birds.’
(see the letter) By
this time Darwin had already sent some of the seeds Müller had enclosed with his October letter
to his best friend, the botanist Joseph Dalton Hooker, for identification
(see the letter).

A selection of mimetic seeds

The selection of seeds in the adjacent photograph will give you some idea of the difficulties.

Darwin picked up on Müller’s suggestion and tried the experiment himself, but the results were
disappointing. He wrote to Hooker:

I enclose 3 seeds of the Mimoseous tree, of which the pods open & wind
spirally outwards & display a lining like yellow silk, studded with these crimson seeds,
& looking gorgeous. I gave two seeds to a confounded old cock, but his gizzard ground
them up; at least I c^d. not find them during 48^o in his excrement. Please
M^r. Deputy-Wriggler explain to me why these seeds & pods, hang long &
look gorgeous, if Birds only grind up the seeds, for I do not suppose they can be covered with
any pulp.— Can they be disseminated like acorns merely by birds accidentally dropping
them. The case is a sore puzzle to me.—

Darwin, C. R. to Hooker, J. D., 10 Dec [1866]
See
the letter

Hooker replied with his own speculations (14 December 1866):

The Scarlet seed is that of Adenanthera pavonina a native of India. I am well
acquainted with itself … I should suppose that it is to imitate a scarlet insect
& thus attract insectivorous birds, or frugiferous perchers, of weak digestions, that
the color is acquired. The plant is a very common Indian one, & it would be easy to
ascertain how far it is a prey to birds.

Hooker, J. D. to Darwin, C. R., 14 Dec 1866
See
the letter

Adenanthera Pavonina seeds in situ

Darwin was skeptical about the ‘weak gizzard’ explanation and
although he told Hooker
‘it is not worth enquiring in India about, though it is a
perplexing case, for I can hardly admit your wriggle of the seeds being devoured by birds with
weak gizzards:’
he did mention the case to a correspondent in India, John Scott, who duly experimented and
replied in September 1867 that his sulphur-crested cockatoo (the cockatoo Cacatua
sulphurea is native to Sulawesi and many of the surrounding islands, where Adenanthera
pavonina is also found) could
‘with little difficulty split
their hard testa, and eat with seeming gusto the embryonic parts only rejecting the coloured
covering.’
It was not surprising that a seed predator would be attracted but where was the benefit to the
plant? Scott noted that his cockatoo dropped about half the seeds he tried to eat, possibly
confirming Darwin’s suggestion of accidental dissemination. But at this point the investigation
was finally dropped – and we suppose remained a
‘sore
puzzle’ to Darwin.

Mauro Galetti collecting fruits in the Atlantic rainforests of Brazil

Luckily for us, modern researchers have taken up the puzzle and have been able to resolve some
of the questions Darwin posed. Brazilian ecologist, and former Cambridge PhD student, Mauro
Galetti of the
Conservation
Biology Laboratory
at Universidade Estadual Paulista in Rio Claro, Brazil, can bring us up to date on modern
research into ‘mimetic fruit’, as these seeds are now known.

Some plant species have evolved fruits with no nutritive rewards – they enjoy the
benefit of dispersal without the cost of pulp production. But how do they get away with it?
‘One strategy is to hide small fruits and seeds among leaves that are ingested by
large herbivores …. Another strategy is to display colourful seeds resembling fleshy
ornithochoric (i.e. bird-dispersed) fruits, so-called “mimetic
fruits”.’
(Galetti 2002, p. 177.)

Like Darwin, Galetti tested seeds on captive birds, and even used guans (the bird species
suggested by Fritz Müller) and toucans, but was also able to observe the behaviour of birds and
some mammals in the field. Seeds of Ormosia arborea were fed to both granivorous birds
with muscular gizzards like guans and frugivorous birds with non-muscular gizzards like toucans.
Naïve toucans (captive born) eat more Ormosia than wild captured toucans, a behaviour that might
explain how these seeds get dispersed. Afterwards the defecated or regurgitated seeds were
planted to observe germination. The surprise was that defacated seeds had much lower rates of
germination than those in the control group and so the hypothesis that the seeds might be used as
grit by galliform birds was rejected. Another possibility considered was that the seeds were
aposematic (colour serves as a warning to seed predators of poison). Although this was
provisionally rejected because agoutis (a kind of large rodent) prey on seeds, further study is
being done. The hypothesis which best fitted the group’s observations was that these seeds are
parasitic, that is they deceive naïve birds by mimicking similar-looking fleshy fruits. Galetti
listed dozen of species (many of them cited by Darwin and Müller), as mimetic fruits are found in
several plant families and this dispersal strategy has evolved independently several times.

References

• Campbell, George Douglas (duke of
  Argyll).
  Scottish statesman and author.
• Campbell, George Douglas. The reign of law. Good Words 1865: 126-133, 227-232.
• Cazetta, E., Schaefer, H, M., Galetti, M. 2008. Does
  attraction to frugivores or defense against pathogens shape fruit pulp composition?
  Oecologia 155: 277–86
• Darwin, Charles. 1866.
  
  On the origin of species by means of natural selection, or the
  preservation of favoured races in the struggle for life
  .
  London: John Murray.
• Hooker, Joseph Dalton. Botanist, and
  director of the Royal Botanic Gardens, Kew.
• Galetti, M. 2002.
  
  Seed dispersal of mimetic seeds: parasitism, mutualism,
  aposematism or exaptation?
  
  In Seed dispersal and frugivory: ecology, evolution and conservation, edited by D.
  Levey, et al. New York: CABI Publishing.
• Guimaraes Jr., P. R., Galetti, M., Jordano, P. 2008
  Seed Dispersal
  Anachronisms: Rethinking the Fruits Extinct Megafauna Ate,
  PLoS ONE 3(3): e1745.
  >(Alternative
  link)
• Müller, Johann Friedrich Theodor
  (Fritz).
  German naturalist . Studied mathematics and natural history, and then medicine, before
  emigrating to the German colony in Blumenau, Brazil, in 1852.
• Pijl, Leendert van der (1903–90). Dutch botanist. Wrote
  Principles of
  dispersal in higher plants (1969; 2nd ed. 1972, 3rd ed. 1982).
• Ridley, Henry Nicholas. English
  economic botanist. Wrote The dispersal of plants throughout the world (1930).
• Scott, John. Curator of the Calcutta
  botanic garden.