The Different Forms of Flowers on Plants of the Same Species

by Charles Darwin

TENTHLY.

Repeated the experiment, with the same result after twenty-four hours, excepting that only two own-form grains had penetrated the stigmatic tissue with their tubes to a very short depth. The one stigma, which was deeply penetrated by a multitude of tubes from the short-styled pollen, presented a conspicuous difference in being much curled, half-shrivelled, and discoloured, in comparison with the other four straight and bright pink stigmas.

I could add other experiments; but those now given amply suffice to show that the pollen-grains of a short-styled flower placed on the stigma of a long-styled flower emit a multitude of tubes after an interval of from five to six hours, and penetrate the tissue ultimately to a great depth; and that after twenty-four hours the stigmas thus penetrated change colour, become twisted, and appear half-withered. On the other hand, pollen-grains from a long-styled flower placed on its own stigmas, do not emit their tubes after an interval of a day, or even three days; or at most only three or four grains out of a multitude emit their tubes, and these apparently never penetrate the stigmatic tissue deeply, and the stigmas themselves do not soon become discoloured and twisted.

This seems to me a remarkable physiological fact. The pollen-grains of the two forms are undistinguishable under the microscope; the stigmas differ only in length, degree of divergence, and in the size, shade of colour, and approximation of their papillae, these latter differences being variable and apparently due merely to the degree of elongation of the stigma. Yet we plainly see that the two kinds of pollen and the two stigmas are widely dissimilar in their mutual reaction—the stigmas of each form being almost powerless on their own pollen, but causing, through some mysterious influence, apparently by simple contact (for I could detect no viscid secretion), the pollen-grains of the opposite form to protrude their tubes. It may be said that the two pollens and the two stigmas mutually recognise each other by some means. Taking fertility as the criterion of distinctness, it is no exaggeration to say that the pollen of the long-styled Linum grandiflorum (and conversely that of the other form) has been brought to a degree of differentiation, with respect to its action on the stigma of the same form, corresponding with that existing between the pollen and stigma of species belonging to distinct genera.

Linum perenne.

This species is conspicuously heterostyled, as has been noticed by several authors. The pistil in the long-styled form is nearly twice as long as that of the short-styled. In the latter the stigmas are smaller and, diverging to a greater degree, pass out low down between the filaments. I could detect no difference in the two forms in the size of the stigmatic papillae. In the long- styled form alone the stigmatic surfaces of the mature pistils twist round, so as to face the circumference of the flower; but to this point I shall presently return. Differently from what occurs in L. grandiflorum, the long-styled flowers have stamens hardly more than half the length of those in the short-styled. The size of the pollen-grains is rather variable; after some doubt, I have come to the conclusion that there is no uniform difference between the grains in the two forms. The long-stamens in the short-styled form project to some height above the corolla, and their filaments are coloured blue apparently from exposure to the light. The anthers of the longer stamens correspond in height with the lower part of the stigmas of the long-styled flowers; and the anthers of the shorter stamens of the latter correspond in the same manner in height with the stigmas of the short-styled flowers.

I raised from seed twenty-six plants, of which twelve proved to be long-styled and fourteen short-styled. They flowered well, but were not large plants. As I did not expect them to flower so soon, I did not transplant them, and they unfortunately grew with their branches closely interlocked. All the plants were covered under the same net, excepting one of each form. Of the flowers on the long-styled plants, twelve were illegitimately fertilised with their own-form pollen, taken in every case from a separate plant; and not one set a seed- capsule: twelve other flowers were legitimately fertilised with pollen from short-styled flowers; and they set nine capsules, each including on an average 7 good seeds, ten being the maximum number ever produced. Of the flowers on the short-styled plants, twelve were illegitimately fertilised with own-form pollen, and they yielded one capsule, including only 3 good seeds; twelve other flowers were legitimately fertilised with pollen from long-styled flowers, and these produced nine capsules, but one was bad; the eight good capsules contained on an average 8 good seeds each. Judging from the number of seeds per capsule, the fertility of the two legitimate to that of the two illegitimate unions is as 100 to 20.

The numerous flowers on the eleven long-styled plants under the net, which were not fertilised, produced only three capsules, including 8, 4, and 1 good seeds. Whether these three capsules were the product of accidental legitimate fertilisation, owing to the branches of the plants of the two forms interlocking, I will not pretend to decide. The single long-styled plant which was left uncovered, and grew close by the uncovered short-styled plant, produced five good pods; but it was a poor and small plant.

The flowers borne on the thirteen short-styled plants under the net, which were not fertilised, produced twelve capsules, containing on an average 5.6 seeds. As some of these capsules were very fine, and as five were borne on one twig, I suspect that some minute insect had accidentally got under the net and had brought pollen from the other form to the flowers which produced this little group of capsules. The one uncovered short-styled plant which grew close to the uncovered long-styled plant yielded twelve capsules.

From these facts we have some reason to believe, as in the case of L. grandiflorum, that the short-styled plants are in a slight degree more fertile with their own pollen than are the long-styled plants. Anyhow we have the clearest evidence, that the stigmas of each form require for full fertility that pollen from the stamens of corresponding height belonging to the opposite form should be brought to them.

Hildebrand, in the paper lately referred to, confirms my results. He placed a short-styled plant in his house, and fertilised about 20 flowers with their own pollen, and about 30 with pollen from another plant belonging to the same form, and these 50 flowers did not set a single capsule. On the other hand he fertilised about 30 flowers with pollen from the long-styled form, and these, with the exception of two, yielded capsules, containing good seeds.

It is a singular fact, in contrast with what occurred in the case of L. grandiflorum, that the pollen-grains of both forms of L. perenne, when placed on their own-form stigmas, emitted their tubes, though this action did not lead to the production of seeds. After an interval of eighteen hours, the tubes penetrated the stigmatic tissue, but to what depth I did not ascertain. In this case the impotence of the pollen-grains on their own stigmas must have been due either to the tubes not reaching the ovules, or to their not acting properly after reaching them.

The plants both of L. perenne and grandiflorum, grew, as already stated, with their branches interlocked, and with scores of flowers of the two forms close together; they were covered by a rather coarse net, through which the wind, when high, passed; and such minute insects as Thrips could not, of course, be excluded; yet we have seen that the utmost possible amount of accidental fertilisation on seventeen long-styled plants in the one case, and on eleven long-styled plants in the other, resulted in the production, in each case, of three poor capsules; so that when the proper insects are excluded, the wind does hardly anything in the way of carrying pollen from plant to plant. I allude to this fact because botanists in speaking of the fertilisation of various flowers, often refer to the wind or to insects as if the alternative were indifferent. This view, according to my experience, is entirely erroneous. When the wind is the agent in carrying pollen, either from one sex to the other, or from hermaphrodite to hermaphrodite, we can recognise structure as manifestly adapted to its action as to that of insects when these are the carriers. We see adaptation to the wind in the incoherence of the pollen,—in the inordinate quantity produced (as in the Coniferae, Spinage, etc.),—in the dangling anthers well fitted to shake out the pollen,—in the absence or small size of the perianth,—in the protrusion of the stigmas at the period of fertilisation,—in the flowers being produced before they are hidden by the leaves,—and in the stigmas being downy or plumose (as in the Gramineae, Docks, etc), so as to secure the chance-blown grains. In plants which are fertilised by the wind, the flowers do not secrete nectar, their pollen is too incoherent to be easily collected by insects, they have not bright-coloured corollas to serve as guides, and they are not, as far as I have seen, visited by insects. When insects are the agents of fertilisation (and this is incomparably the more frequent case with hermaphrodite plants), the wind plays no part, but we see an endless number of adaptations to ensure the safe transport of the pollen by the living workers. These adaptations are most easily recognised in irregular flowers; but they are present in regular flowers, of which those of Linum offer a good instance, as I will now endeavour to show.

I have already alluded to the rotation of each separate stigma in the long- styled form of Linum perenne. In both forms of the other heterostyled species and in the homostyled species of Linum which I have seen, the stigmatic surfaces face the centre of the flower, with the furrowed backs of the stigmas, to which the styles are attached, facing outwards. This is the case with the stigmas of the long-styled flowers of L. perenne whilst in bud. But by the time the flowers have expanded, the five stigmas twist round so as to face the circumference, owing to the torsion of that part of the style which lies beneath the stigma. I should state that the five stigmas do not always turn round completely, two or three sometimes facing only obliquely outwards. My observations were made during October; and it is not improbable that earlier in the season the torsion would have been more complete; for after two or three cold and wet days the movement was very imperfectly performed. The flowers should be examined shortly after their expansion, as their duration is brief; as soon as they begin to wither, the styles become spirally twisted all together, the original position of the parts being thus lost.

He who will compare the structure of the whole flower in both forms of L. perenne and grandiflorum, and, as I may add, of L. flavum, will not doubt about the meaning of this torsion of the styles in the one form alone of L. perenne, as well as the meaning of the divergence of the stigmas in the short-styled form of all three species. It is absolutely necessary as we know, that insects should carry pollen from the flowers of the one form reciprocally to those of the other. Insects are attracted by five drops of nectar, secreted exteriorly at the base of the stamens, so that to reach these drops they must insert their proboscides outside the ring of broad filaments, between them and the petals. In the short-styled form of the above three species, the stigmas face the axis of the flower; and had the styles retained their original upright and central position, not only would the stigmas have presented their backs to the insects which sucked the flowers, but their front and fertile surfaces would have been separated from the entering insects by the ring of broad filaments, and would never have received any pollen. As it is, the styles diverge and pass out between the filaments. After this movement the short stigmas lie within the tube of the corolla; and their papillous surfaces being now turned upwards are necessarily brushed by every entering insect, and thus receive the required pollen.

In the long-styled form of L. grandiflorum, the almost parallel or slightly diverging anthers and stigmas project a little above the tube of the somewhat concave flower; and they stand directly over the open space leading to the drops of nectar. Consequently when insects visit the flowers of either form (for the stamens in this species occupy the same position in both forms), they will get their foreheads or proboscides well dusted with the coherent pollen. As soon as they visit the flowers of the long-styled form they will necessarily leave pollen on the proper surface of the elongated stigmas; and when they visit the short-styled flowers, they will leave pollen on the upturned stigmatic surfaces. Thus the stigmas of both forms will receive indifferently the pollen of both forms; but we know that the pollen alone of the opposite form causes fertilisation.

(Figure 3.5. Long-styled form of L. perenne var. Austriacum in its early condition before the stigmas have rotated. The petals and calyx have been removed on the near side. (3/3. I neglected to get drawings made from fresh flowers of the two forms. But Mr. Fitch has made the above sketch of a long- styled flower from dried specimens and from published engravings. His well-known skill ensures accuracy in the proportional size of the parts.)

In the case of L. perenne, affairs are arranged more perfectly; for the stamens in the two forms stand at different heights, so that pollen from the anthers of the longer stamens will adhere to one part of an insect’s body, and will afterwards be brushed off by the rough stigmas of the longer pistils; whilst pollen from the anthers of the shorter stamens will adhere to a different part of the insect’s body, and will afterwards be brushed off by the stigmas of the shorter pistils; and this is what is required for the legitimate fertilisation of both forms. The corolla of L. perenne is more expanded than that of L. grandiflorum, and the stigmas of the long-styled form do not diverge greatly from one another; nor do the stamens of either form. Hence insects, especially rather small ones, will not insert their proboscides between the stigmas of the long-styled form, nor between the anthers of either form (Figure 3.5), but will strike against them, at nearly right angles, with the backs of their head or thorax. Now, in the long-styled flowers, if each stigma did not rotate on its axis, insects in visiting them would strike their heads against the backs of the stigmas; as it is, they strike against that surface which is covered with papillae, with their heads already charged with pollen from the stamens of corresponding height borne by the flowers of the other form, and legitimate fertilisation is thus ensured.

Thus we can understand the meaning of the torsion of the styles in the long- styled flowers alone, as well as their divergence in the short-styled flowers.

One other point is worth notice. In botanical works many flowers are said to be fertilised in the bud. This statement generally rests, as far as I can discover, on the anthers opening in the bud; no evidence being adduced that the stigma is at this period mature, or that it is not subsequently acted on by pollen brought from other flowers. In the case of Cephalanthera grandiflora I have shown that precocious and partial self-fertilisation, with subsequent full fertilisation, is the regular course of events. (3/4. ‘Fertilisation of Orchids’ page 108; 2nd edition 1877 page 84.) The belief that the flowers of many plants are fertilised in the bud, that is, are perpetually self-fertilised, is a most effectual bar to understanding their real structure. I am, however, far from wishing to assert that some flowers, during certain seasons, are not fertilised in the bud; for I have reason to believe that this is the case. A good observer, resting his belief on the usual kind of evidence, states that in Linum Austriacum (which is heterostyled, and is considered by Planchon as a variety of L. perenne) the anthers open the evening before the expansion of the flowers, and that the stigmas are then almost always fertilised. (3/5. H. Lecoq ‘Etudes sur la Geogr. Bot.’ 1856 tome 5 page 325.) Now we know positively that, so far from Linum perenne being fertilised by its own pollen in the bud, its own pollen is as powerless on the stigma as so much inorganic dust.

Linum flavum.

The pistil of the long-styled form of this species is nearly twice as long as that of the short-styled; the stigmas are longer and the papillae coarser. In the short-styled form the stigmas diverge and pass out between the filaments, as in the previous species. The stamens in the two forms differ in length; and, what is singular, the anthers of the longer stamens are not so long as those of the other form; so that in the short-styled form both the stigmas and the anthers are shorter than in the long-styled form. The pollen-grains of the two forms do not differ in size. As this species is propagated by cuttings, generally all the plants in the same garden belong to the same form. I have inquired, but have never heard of its seeding in this country. Certainly my own plants never produced a single seed as long as I possessed only one of the two forms. After considerable search I procured both forms, but from want of time only a few experiments were made. Two plants of the two forms were planted some way apart in my garden, and were not covered by nets. Three flowers on the long- styled plant were legitimately fertilised with pollen from the short-styled plant, and one of them set a fine capsule. No other capsules were produced by this plant. Three flowers on the short-styled plant were legitimately fertilised with pollen from the long-styled, and all three produced capsules, containing respectively no less than 8, 9, and 10 seeds. Three other flowers on this plant, which had not been artificially fertilised, produced capsules containing 5, 1, and 5 seeds; and it is quite possible that pollen may have been brought to them by insects from the long-styled plant growing in the same garden. Nevertheless, as they did not yield half the number of seeds compared with the other flowers on the same plant which had been artificially and legitimately fertilised, and as the short-styled plants of the two previous species apparently evince some slight capacity for fertilisation with their own-form pollen, these three capsules may have been the product of self-fertilisation.

Besides the three species now described, the yellow-flowered L. corymbiferum is certainly heterostyled, as is, according to Planchon, L. salsoloides. (3/6. Hooker’s ‘London Journal of Botany’ 1848 volume 7 page 174.) This botanist is the only one who seems to have inferred that heterostylism might have some important functional bearing. Dr. Alefeld, who has made a special study of the genus, says that about half of the sixty-five species known to him are heterostyled. (3/7. ‘Botanische Zeitung’ September 18, 1863 page 281.) This is the case with L. trigynum, which differs so much from the other species that it has been formed by him into a distinct genus. (3/8. It is not improbable that the allied genus, Hugonia, is heterostyled, for one species is said by Planchon (Hooker’s ‘London Journal of Botany’ 1848 volume 7 page 525) to be provided with “staminibus exsertis;” another with “stylis staminibus longioribus,” and another has “stamina 5, majora, stylos longe superantia.”) According to the same author, none of the species which inhabit America and the Cape of Good Hope are heterostyled.

I have examined only three homostyled species, namely, L. usitatissimum, angustifolium, and catharticum. I raised 111 plants of a variety of the first- named species, and these, when protected under a net, all produced plenty of seed. The flowers, according to H. Muller, are frequented by bees and moths. (3/9. ‘Die Befruchtung der Blumen’ etc. page 168.) With respect to L. catharticum, the same author shows that the flowers are so constructed that they can freely fertilise themselves; but if visited by insects they might be cross- fertilised. He has, however, only once seen the flowers thus visited during the day; but it may be suspected that they are frequented during the night by small moths for the sake of the five minute drops of nectar secreted. Lastly, L. Lewisii is said by Planchon to bear on the same plant flowers with stamens and pistils of the same height, and others with the pistils either longer or shorter than the stamens. This case formerly appeared to me an extraordinary one; but I am now inclined to believe that it is one merely of great variability. (3/10. Planchon in Hooker’s ‘London Journal of Botany’ 1848 volume 7 page 175. See on this subject Asa Gray in ‘American Journal of Science’ volume 36 September 1863 page 284.)