FORMS OF FLOWERS, PLANT MOVEMENT

Wood sorrels, shamrocks, and other species in the cosmopolitan genus Oxalis have features that led Darwin to study the plants on several levels, from heterostyly to leaf and fruit movement. In the early 1860s, when Darwin first became aware that the flowers of some species exhibit morphs with varied lengths of pistils and stamens (see p. 271), he queried his botanist friends for more cases. He surmised that the different morphs were erroneously interpreted as distinct species, something that the distinguished English botanist George Bentham confirmed in sending Darwin a list of Oxalis species varying in stamens and pistil length, many of which he and others suspected were actually morphs of each other.111

Ultimately, with the help of South African naturalist Roland Trimen and German botanist Friedrich Hildebrand, he was able to present data for thirteen Oxalis species from around the world in Forms of Flowers. Their work focused on trimorphic flowers that produce three distinct stamen and pistil length morphs, which practically cried out for experiments testing “legitimate” and “illegitimate” crosses. Darwin also pondered unusual “homostyled” Oxalis species such as the common European wood sorrel O. acetosella, with single-morph flowers, and specialized cleistogamous flowers that set seed in abundance despite never opening in bloom.

In 1863 Mr. Roland Trimen wrote to me from the Cape of Good Hope that he had there found species of Oxalis which presented three forms; and of these he enclosed drawings and dried specimens. Of one species he collected 43 flowers from distinct plants, and they consisted of 10 long-styled, 12 mid-styled, and 21 short-styled. Of another species he collected 13 flowers, consisting of 3 long-styled, 7 mid-styled, and 3 short-styled. In 1866 Prof. Hildebrand proved by an examination of the specimens in several herbaria that 20 species are certainly heterostyled and trimorphic, and 51 others almost certainly so. He also made some interesting observations on living plants belonging to one form alone; for at that time he did not possess the three forms of any living species. During the years 1864 to 1868, I occasionally experimented on Oxalis speciosa, but until now have never found time to publish the results. I may premise that in all the species seen by me, the stigmas of the five straight pistils of the long-styled form stand on a level with the anthers of the longest stamens in the two other forms. In the mid-styled form, the stigmas pass out between the filaments of the longest stamens and they stand rather nearer to the upper anthers than to the lower ones. In the short-styled form, the stigmas also pass out between the filaments nearly on a level with the tips of the sepals. The anthers in this latter form and in the mid-styled rise to the same height as the corresponding stigmas in the other two forms.

Oxalis speciosa.1—This species, which bears pink flowers, was introduced from the Cape of Good Hope. A sketch of the reproductive organs of the three forms [is shown]. The stigma of the long-styled form (with the papillae on its surface included) is twice as large as that of the short-styled, and that of the mid-styled intermediate in size.

Thirty-six flowers on the three forms legitimately fertilised yielded 30 capsules, these containing on an average 58.36 seeds. Ninety-five flowers illegitimately fertilised yielded 12 capsules, containing on an average 28.58 seeds. Therefore, the fertility of the six legitimate to that of the twelve illegitimate unions, as judged by the proportion of flowers which yielded capsules, is as 100 to 15, and judged by the average number of seeds per capsule as 100 to 49.

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Oxalis speciosa (with the petals removed). S, stigmas. The dotted lines with arrows show which pollen must be carried to the stigmas for legitimate fertilisation.

Darwin’s later research, conducted with his son Francis, involved various kinds of movement of stems, leaves, flowers, and fruit capsules. Nighttime folding of leaves, for example (for which they coined the term “nyctitropism”), was widely known, but there was no accepted explanation at the time. Linnaeus and others hinted at a protective function, but Darwin and son approached the question experimentally, testing several species including Oxalis acetosella and the Chilean O. carnosa, which fold their three leaves like a closed umbrella at night. In one series of experiments, they pinned or tied leaves open and exposed the plants to subfreezing temperatures outdoors to determine if folding protects from radiative heat loss and frost damage. It does. “I think we have proved that the sleep of plants is to lessen injury to leaves from radiation,” he wrote to Joseph Hooker at the Royal Botanic Gardens, Kew, “this has interested me much and has cost us great labour, as it has been a problem since the time of Linnaeus.” The revelation was not without cost, however, and he lamented to Hooker, “we have killed or badly injured a multitude of plants.”112

In other studies of leaves, shoots, and fruits, Darwin tracked movements using tracing paper on glass plates, marking patterns of growth and slow circumnutation, circular movements, hour by hour and day by day. He noted and defined movements such as “apogeotropism” (growth away from the earth), “hyponasty” (growth along a lower surface causing leaves and stems to bend upward), and “epinasty” (increased growth on the upper surface, causing downward bending).

We will now describe in detail the experiments which were tried. These were troublesome from our not being able to predict how much cold the leaves of the several species could endure. Many plants had every leaf killed, both those which were secured in a horizontal position and those which were allowed to sleep—that is, to rise up or sink down vertically. Others again had not a single leaf in the least injured, and these had to be re-exposed either for a longer time or to a lower temperature.

Oxalis acetosella.—A very large pot, thickly covered with between 300 and 400 leaves, had been kept all winter in the greenhouse. Seven leaves were pinned horizontally open and were exposed on March 16th for 2 h. to a clear sky, the temperature on the surrounding grass being -4° C. (24° to 25° F.). Next morning all seven leaves were found quite killed, so were many of the free ones which had previously gone to sleep, and about 100 of them, either dead or browned and injured were picked off. Some leaves showed that they had been slightly injured by not expanding during the whole of the next day, though they afterwards recovered. As all the leaves which were pinned open were killed, and only about a third or fourth of the others were either killed or injured, we had some little evidence that those which were prevented from assuming their vertically dependent position suffered most.

The following night (17th) was clear and almost equally cold (-3° to -4° C. on the grass), and the pot was again exposed, but this time for only 30 m. Eight leaves had been pinned out, and in the morning two of them were dead, whilst not a single other leaf on the many plants was even injured.

Considering these cases, there can be no doubt that the leaves of this Oxalis, when allowed to assume their normal vertically dependent position at night, suffer much less from frost than those which had their upper surfaces exposed to the zenith.

The difference in the amount of dew on the pinned-open leaflets and on those which had gone to sleep was generally conspicuous; the latter being sometimes absolutely dry, whilst the leaflets which had been horizontal were coated with large beads of dew. This shows how much cooler the leaflets fully exposed to the zenith must have become, than those which stood almost vertically, either upwards or downwards, during the night.

From the several cases above given, there can be no doubt that the position of the leaves at night affects their temperature through radiation to such a degree, that when exposed to a clear sky during a frost, it is a question of life and death. We may therefore admit as highly probable, seeing that their nocturnal position is so well adapted to lessen radiation, that the object gained by their often complicated sleep movements, is to lessen the degree to which they are chilled at night. It should be kept in mind that it is especially the upper surface which is thus protected, as it is never directed towards the zenith, and is often brought into close contact with the upper surface of an opposite leaf or leaflet.

In most of the species in this large genus the three leaflets sink vertically down at night; but as their sub-petioles are short, the blades could not assume this position from the want of space, unless they were in some manner rendered narrower; and this is effected by their becoming more or less folded (Figure below).

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Oxalis acetosella: A, leaf seen from vertically above; B, diagram of leaf asleep, also seen from vertically above.

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Passiflora caerulea. Bodycolor on vellum by Jan Withoos, Dutch Florilegium.

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