Trevira.n.u.s has shown that this is the case in his review of my original paper "Botanische Zeitung" 1863 page 189.), and having observed this fact in L. flavum more than thirty years ago, I was led, after ascertaining the nature of heterostylism in Primula, to examine the first species of Linum which I met with, namely, the beautiful L. grandiflorum. This plant exists under two forms, occurring in about equal numbers, which differ little in structure, but greatly in function. The foliage, corolla, stamens, and pollen-grains (the latter examined both distended with water and dry) are alike in the two forms (Figure 3.4). The difference is confined to the pistil; in the short-styled form the styles and the stigmas are only about half the length of those in the long- styled. A more important distinction is, that the five stigmas in the short- styled form diverge greatly from one another, and pa.s.s out between the filaments of the stamens, and thus lie within the tube of the corolla. In the long-styled form the elongated stigmas stand nearly upright, and alternate with the anthers.
In this latter form the length of the stigmas varies considerably, their upper extremities projecting even a little above the anthers, or reaching up only to about their middle. Nevertheless, there is never the slightest difficulty in distinguishing between the two forms; for, besides the difference in the divergence of the stigmas, those of the short-styled form never reach even to the bases of the anthers. In this form the papillae on the stigmatic surfaces are shorter, darker-coloured, and more crowded together than in the long-styled form; but these differences seem due merely to the shortening of the stigma, for in the varieties of the long-styled form with shorter stigmas, the papillae are more crowded and darker-coloured than in those with the longer stigmas.
Considering the slight and variable differences between the two forms of this Linum, it is not surprising that hitherto they have been overlooked.
In 1861 I had eleven plants in my garden, eight of which were long-styled, and three short-styled. Two very fine long-styled plants grew in a bed a hundred yards off all the others, and separated from them by a screen of evergreens. I marked twelve flowers, and placed on their stigmas a little pollen from the short-styled plants. The pollen of the two forms is, as stated, identical in appearance; the stigmas of the long-styled flowers were already thickly covered with their own pollen--so thickly that I could not find one bare stigma, and it was late in the season, namely, September 15th. Altogether, it seemed almost childish to expect any result. Nevertheless from my experiments on Primula, I had faith, and did not hesitate to make the trial, but certainly did not antic.i.p.ate the full result which was obtained. The germens of these twelve flowers all swelled, and ultimately six fine capsules (the seed of which germinated on the following year) and two poor capsules were produced; only four capsules shanking off. These same two long-styled plants produced, in the course of the summer, a vast number of flowers, the stigmas of which were covered with their own pollen; but they all proved absolutely barren, and their germens did not even swell.
The nine other plants, six long-styled and three short-styled, grew not very far apart in my flower-garden. Four of these long-styled plants produced no seed- capsules; the fifth produced two; and the remaining one grew so close to a short-styled plant that their branches touched, and this produced twelve capsules, but they were poor ones. The case was different with the short-styled plants. The one which grew close to the long-styled plant produced ninety-four imperfectly fertilised capsules containing a mult.i.tude of bad seeds, with a moderate number of good ones. The two other short-styled plants growing together were small, being partly smothered by other plants; they did not stand very close to any long-styled plants, yet they yielded together nineteen capsules.
These facts seem to show that the short-styled plants are more fertile with their own pollen than are the long-styled, and we shall immediately see that this probably is the case. But I suspect that the difference in fertility between the two forms was in this instance in part due to a distinct cause. I repeatedly watched the flowers, and only once saw a humble-bee momentarily alight on one, and then fly away. If bees had visited the several plants, there cannot be a doubt that the four long-styled plants, which did not produce a single capsule, would have borne an abundance. But several times I saw small diptera sucking the flowers; and these insects, though not visiting the flowers with anything like the regularity of bees, would carry a little pollen from one form to the other, especially when growing near together; and the stigmas of the short-styled plants, diverging within the tube of the corolla, would be more likely than the upright stigmas of the long-styled plants, to receive a small quant.i.ty of pollen if brought to them by small insects. Moreover from the greater number of the long-styled than of the short-styled plants in the garden, the latter would be more likely to receive pollen from the long-styled, than the long-styled from the short-styled.
In 1862 I raised thirty-four plants of this Linum in a hot-bed; and these consisted of seventeen long-styled and seventeen short-styled forms. Seed sown later in the flower-garden yielded seventeen long-styled and twelve short-styled forms. These facts justify the statement that the two forms are produced in about equal numbers. The thirty-four plants of the first lot were kept under a net which excluded all insects, except such minute ones as Thrips. I fertilised fourteen long-styled flowers legitimately with pollen from the short-styled, and got eleven fine seed-capsules, which contained on an average 8.6 seeds per capsule, but only 5.6 appeared to be good. It may be well to state that ten seeds is the maximum production for a capsule, and that our climate cannot be very favourable to this North-African plant. On three occasions the stigmas of nearly a hundred flowers were fertilised illegitimately with their own-form pollen, taken from separate plants, so as to prevent any possible ill effects from close inter-breeding. Many other flowers were also produced, which, as before stated, must have received plenty of their own pollen; yet from all these flowers, borne by the seventeen long-styled plants, only three capsules were produced. One of these included no seed, and the other two together gave only five good seeds. It is probable that this miserable product of two half-fertile capsules from the seventeen plants, each of which must have produced at least fifty or sixty flowers, resulted from their fertilisation with pollen from the short-styled plants by the aid of Thrips; for I made a great mistake in keeping the two forms under the same net, with their branches often interlocking; and it is surprising that a greater number of flowers were not accidentally fertilised.
Twelve short-styled flowers were in this instance castrated, and afterwards fertilised legitimately with pollen from the long-styled form; and they produced seven fine capsules. These included on an average 7.6 seeds, but of apparently good seed only 4.3 per capsule. At three separate times nearly a hundred flowers were fertilised illegitimately with their own-form pollen, taken from separate plants; and numerous other flowers were produced, many of which must have received their own pollen. From all these flowers on the seventeen short-styled plants only fifteen capsules were produced, of which only eleven contained any good seed, on an average 4.2 per capsule. As remarked in the case of the long- styled plants, some even of these capsules were perhaps the product of a little pollen accidentally fallen from the adjoining flowers of the other form on to the stigmas, or transported by Thrips. Nevertheless the short-styled plants seem to be slightly more fertile with their own pollen than the long-styled, in the proportion of fifteen capsules to three; nor can this difference be accounted for by the short-styled stigmas being more liable to receive their own pollen than the long-styled, for the reverse is the case. The greater self-fertility of the short-styled flowers was likewise shown in 1861 by the plants in my flower- garden, which were left to themselves, and were but sparingly visited by insects.
On account of the probability of some of the flowers on the plants of both forms, which were covered under the same net, having been legitimately fertilised in an accidental manner, the relative fertility of the two legitimate and two illegitimate unions cannot be compared with certainty; but judging from the number of good seeds per capsule, the difference was at least in the ratio of 100 to 7, and probably much greater.
Hildebrand tested my results, but only on a single short-styled plant, by fertilising many flowers with their own-form pollen; and these did not produce any seed. This confirms my suspicion that some of the few capsules produced by the foregoing seventeen short-styled plants were the product of accidental legitimate fertilisation. Other flowers on the same plant were fertilised by Hildebrand with pollen from the long-styled form, and all produced fruit. (3/2.
"Botanische Zeitung" January 1, 1864 page 2.)
The absolute sterility (judging from the experiments of 1861) of the long-styled plants with their own-form pollen led me to examine into its apparent cause; and the results are so curious that they are worth giving in detail. The experiments were tried on plants grown in pots and brought successively into the house.
FIRST.
Pollen from a short-styled plant was placed on the five stigmas of a long-styled flower, and these, after thirty hours, were found deeply penetrated by a mult.i.tude of pollen-tubes, far too numerous to be counted; the stigmas had also become discoloured and twisted. I repeated this experiment on another flower, and in eighteen hours the stigmas were penetrated by a mult.i.tude of long pollen- tubes. This is what might have been expected, as the union is a legitimate one.
The converse experiment was likewise tried, and pollen from a long-styled flower was placed on the stigmas of a short-styled flower, and in twenty-four hours the stigmas were discoloured, twisted, and penetrated by numerous pollen-tubes; and this, again, is what might have been expected, as the union was a legitimate one.
SECONDLY.
Pollen from a long-styled flower was placed on all five stigmas of a long-styled flower on a separate plant: after nineteen hours the stigmas were dissected, and only a single pollen-grain had emitted a tube, and this was a very short one. To make sure that the pollen was good, I took in this case, and in most of the other cases, pollen either from the same anther or from the same flower, and proved it to be good by placing it on the stigma of a short-styled plant, and found numerous pollen-tubes emitted.
THIRDLY.
Repeated last experiment, and placed own-form pollen on all five stigmas of a long-styled flower; after nineteen hours and a half, not one single grain had emitted its tube.
FOURTHLY.
Repeated the experiment, with the same result after twenty-four hours.
FIFTHLY.
Repeated last experiment, and, after leaving pollen on for nineteen hours, put on an additional quant.i.ty of own-form pollen on all five stigmas. After an interval of three days, the stigmas were examined, and, instead of being discoloured and twisted, they were straight and fresh-coloured. Only one grain had emitted a quite short tube, which was drawn out of the stigmatic tissue without being ruptured.
The following experiments are more striking:--
SIXTHLY.
I placed own-form pollen on three of the stigmas of a long-styled flower, and pollen from a short-styled flower on the other two stigmas. After twenty-two hours these two stigmas were discoloured, slightly twisted, and penetrated by the tubes of numerous pollen-grains: the other three stigmas, covered with their own-form pollen, were fresh, and all the pollen-grains were loose; but I did not dissect the whole stigma.
SEVENTHLY.
Experiment repeated in the same manner, with the same result.
EIGHTHLY.
Experiment repeated, but the stigmas were carefully examined after an interval of only five hours and a half. The two stigmas with pollen from a short-styled flower were penetrated by innumerable tubes, which were as yet short, and the stigmas themselves were not at all discoloured. The three stigmas covered with their own-form pollen were not penetrated by a single pollen-tube.
NINTHLY.
Put pollen of a short-styled flower on a single long-styled stigma, and own-form pollen on the other four stigmas; after twenty-four hours the one stigma was somewhat discoloured and twisted, and penetrated by many long tubes: the other four stigmas were quite straight and fresh; but on dissecting them I found that three pollen-grains had protruded very short tubes into the tissue.
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 mult.i.tude 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 mult.i.tude 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 mult.i.tude 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, pa.s.s 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 circ.u.mference 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 coa.r.s.e net, through which the wind, when high, pa.s.sed; 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 s.e.x 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 quant.i.ty 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 h.o.m.ostyled 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 circ.u.mference, 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 pa.s.s 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 s.p.a.ce 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. Austriac.u.m 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.)