24: 307-308 (August 4, 1881)
Two Kinds of Stamens with Different Functions in the Same Flower
Hermann Müller

The following extract from a letter lately received from my brother Fritz Müller (of Blumenau, Prov. St. Catharina, Brazil) contains so new and curious an observation that it will probably interest the botanical readers of this journal.

A species of Heeria (Melastomaceae) which is not indigenous here begins in my garden now to open its beautiful red flowers remarkable for having two kinds of differently coloured anthers. The four petals spread in a perpendicular plane; the yellow anthers (a1) of the four shorter filaments, closely pressed together, project from the middle of the flower ; their bright yellow strikingly contrasts with the violet-shining light red of the corolla; the longer anthers (a2) are red, like the filaments, and the very long connective (c), which is lengthened beyond the point of insertion into a fork (f), with two yellowish points; these points stand close beneath the yellow anthers, whilst the apical apertures of the red anthers (a2) are placed far below them near the stigma; also the style and the stigma (st) are coloured so very like the corolla, that from some distance neither they nor the longer stamens can be seen at all. Any large bee (like Xylocopa, Centris, or Bombus), when working on the smaller anthers in order to collect pollen, would, by moving the connective fork of the larger ones, press the apertures of the latter against the ventral side of its abdomen and powder it with pollen. Until now I have only seen a little fly (Syrphidae) and Trigona ruficrus visiting this flower, both too small to fertilise it. The fly takes only notice of the yellow anthers; the Trigonas, too, always sit down first on these; but most of them (the more experienced specimens?) turn then round, and go to the larger anthers, which offer a more copious pollen-store, and work on them with their mandibles or eat them up entirely. Even if larger bees acted in the same manner as Trigona ruficrus, they would have powdered the ventral side of their abdomen before going to plunder the latter. The pollen of both kinds of anthers is white."

Flower of Heeria spec., longitudinally dissected. s, sepals; p, petals; a1, one of the conspicuous yellow anthers which attract the insects; a2 one of the inconspicuous red anthers, which powder the insects with pollen; c, connective of this anther; f, fork of this connective; st, stigma.

Nature 26: 386 (August 24, 1882)
Two Kinds of Stamens with Different Functions in the same Flower
Henry O. Forbes
Wai, Amboina, May

In Nature, vol. xxiv. p. 307 is a very interesting letter on this subject, in which while the functions performed by the two kinds of stamens are very clearly indicated, the modus operandi of fertilisation, it appears to me, is less clearly expressed. I have witnessed in many instances the visitation by various species of large Hymenoptera, such as Xylocopa and Bombus, of species especially of the genus Melastoma, possessing stamens in all points corresponding to that occurring in the Heeria described in the letter referred to and what takes place seems to be as follows. The large bees evidently make for the yellow platform offered by the short stamens, perhaps because they do not perceive the pistil and long stamens owing to their projection against the broad petaled corolla of the same colour in the background, and invariably receive the pistil between their legs, their feet settling on the fork of the connective, the instant effect of which is to collect the whole of the long stamens into a bunch, and to depress their anthers downwards and away from the body of the visiting bee, while the pistil remains in constant contact with its ventral side. At the moment of the bee's departure the hooks on the bee's feet by pulling on the connective fork raise the anthers of the long stamens, so as to bring the tips of the collected bunch into contact with its sides and abdomen. Dr. Muller's statement "by moving the connective fork of the larger ones" is somewhat ambiguous; for it is movement only in one direction that is of avail in raising the anthers of the larger stamens, pressure at the connective hook of course tends to depress the anthers and keep them apart from the bee's abdomen while a very slight backward pull at once raises the anther.

In various observations and discussions arising out of this letter, both Dr. Burck (the assistant director of the Botanical Gardens in Buitenzorg) and myself were able to observe a fact of considerable importance that there was, at any rate in those species examined by us, a great difference in the pollen of the two kinds of anthers. The pollen from the short stamens was large and three-cornered, while that of the longer ones was very much smaller and of a more oval shape; and while both forms were found on the pistil, only the pollen from the long stamens seemed to be fertile. We could not detect any of the short stamened pollen with tubes ejected.


Nature 27: 30 (Nov. 9, 1882)
Two Kinds of Stamens with Different Functions in the Same Flower
Lippstadt, October 25
Hermann Müller

It may be worth mentioning that cases strongly analogous to those described in NATURE (vol. xxiv. p. 307, and vol. xxvi. p. 386, are also to be observed among the Monocotyledons in the family of Commelynaceae, and that these cases offer some graduations.

In Tradescantia virginica, L., the flowers, as is generally known, are turned upwards and quite regular, the leafy organs of each whorl (3 sepals, 3 petals, 3 outer, 3 inner stamens, 3 united carpels) being alike and equal in size. As Delpino has clearly shown (Ulteriori osservazioni, parte ii. fascic. 2, p. 297) these flowers are adapted to Apidae, which in order to collect pollen take hold of the articulated hairs of the filaments. In some other species here to be considered the adaptation to pollen-collecting bees has remained, but the flowers have turned laterally, and thus not only has their form become irregular (bi-laterally symmetrical or zygomorphous), but also the function of the stamens has gradually changed.

In Tinnantia undata, Schlecht. (Fig. 1), sepals and petals are still almost unaltered in form and size, only stamens and pistil have become markedly irregular. The broad roundish petals, which are light purple, spread in a perpendicular plane. The 3 upper stamens, with shorter filaments projecting from the middle of the flower, are highly conspicuous by a diverging tuft of bright yellow articulated hairs, which on the last third of the light-purple filaments surround the golden yellow anthers like a cone of golden rays. At the tips of these filaments golden yellow pollen-grains are presented by the whole front side of the three upper anthers.

Fig. 1.—Front view of the flower of Tinnantia undata, Schlecht. Fig. 2.— Front view of the androeceum and gynoecium of Commelyna coelestis, Willd. s, s, s', sepals; p, p, p’ petals; a, a, a', outer whorl of anthers; a, a, a’, inner whorl of anthers, ov ovary; gr, style ("Griffel"); st, stigma.

The three lower stamens are much longer, directed obliquely downwards and forwards, with only their tips bending upwards, a little overtopped by the pistil, which has the same direction and incurvation. These parts, like the same parts in the described Melastomaceae, will hardly be perceived by an advancing insect, "owing to their projection against the broad-petalled corolla of the same colour in the background," for not only the style and the filaments, but also the hairs on the base on the two lateral lower filaments are of the same purple colour as the petal, and even the bluish lower anthers with their yellowish pollen are but feebly conspicuous. Any one of the Apidae or Syrphidae of suitable size, however, when making for the upper yellow stamens in order to collect their pollen (I have only once observed the honey-bee doing so), will involuntarily repose on the projecting part, and at first bring the stigma and then the two lateral of the lower anthers into contact with the under-side of its abdomen, and thus regularly effect cross fertilisation.

Here, then, as in Heeria, &c, the anthers have differentiated into upper ones, which attract insects and afford food to them, and lower ones which attach their pollen to the visitors, and cause it to be transported by them to the stigma of the next visited flowers. Also differentiation in the pollen of the two kinds of anthers in our Tinnantia has begun to take place, but contrary to Melastoma, the pollen-grains of the short stamens here are smaller than those of the longer ones. I measured numerous pollen-grains of two individuals in a moistened state (where they are of elliptical form), and found in the one stem the pollen-grains of the short stamens (in 1-1000 m.m.) 62-75 long, 31-38 broad, those of the longer ones 68-94 long, 38-44 broad; in the other stem, those of the short stamens 53-69 long, 28-37 broad; those of the longer ones 59-78 long, 31-40 broad. Both kinds of pollen proved to be quite fertile.

Commelyna coelestis, Willd. (Fig. 2) possesses in general the same contrivances for cross-fertilisation, but has gone a step further in differentiation. Its upper sepal is plainly smaller, its lower petal plainly larger than the two other ones; its upper anthers (a, a' a) have differentiated in themselves; two small lateral portions of each of them (po) produce a little pollen and four cross-like diverging flaps (fl), which are much larger, attract insects by their bright yellow colour strikingly contrasting with the azure corolla, and perhaps at the same time serve as food to the visitors. The articulated hairs of the filaments thus having lost not only their original function (which they have in all stamens of Tradescantia) as supports for the feet of pollen-collecting bees, but also their secondary function (which they have in the upper stamens of Tinnantia) of attracting insects, have disappeared altogether. The middlemost of the lower anthers, which in Tinnantia is nearly useless from its position behind the style here, has erected and become much larger than the two lateral ones, so as to be eminently useful.

The pollen-production of the upper anthers appears to be vanishing, not only from the diminution of the quantity of produced pollen, but also from the great variability of the size of the pollen grains. For whilst the pollen grains of the two lateral lower anthers only differ in length from 75 to 90, in breadth from 45 to 68, and those of the middlemost lower anther in length from 56 to 82, in breadth from 37 to 56, those of the three upper anthers fluctuate from 50 to 87 length, and from 31 to 56 breadth.

In Commelyna communis, differentiation has gone still further; the upper sepal and the lower petal are relatively very small; the upper filaments, like the upper petals, are blue-coloured; the lower filaments, like the pistil and the lower petal, are colourless. The upper anthers, as far as I have seen (without microscope) produce no more pollen.

The examination of other species and genera of Commelynaceae probably would show a longer scale of gradations.


Nature 27: 364-365 (February 15, 1883)
Two Kinds of Stamens with Different Functions in the Same Flower
FRITZ MÜLLER
Blumenau, Santa Cattarina, Brazil, December 27, 1882

To the Melastomacese and Commelynaceae mentioned in NATURE (vol. xxiv. p. 307, vol. xxvi. p. 386, and vol. xxvii. p. 30), may be added the genera Mollia (Tiliaceae), Lagerstroemia (Lythraceae), and Heteranthera (Pontederaceae), for having differently coloured anthers. In several species of Mollia, according to Darwin ("Forms of Flowers," p. 168, footnote), the longer stamens of the five outer cohorts have green pollen, whilst the shorter stamens of the five inner cohorts have yellow pollen; the stigma stands close beneath the uppermost anthers. In a Lagerstroemia in my garden the six outer stamens have green pollen, and are much longer than the numerous inner ones, which have bright yellow pollen; the stigma stands on a level with the outer anthers. I have repeatedly seen bees alighting on, and gathering the pollen of the inner anthers without noticing the outer ones.

In Heteranthera reniformis there is one long stamen (belonging to the outer whorl) having pale bluish pollen, and two short stamens (of the inner whorl) with bright yellow pollen. The stigma stands generally on a level with the anther of the long stamen. When the white flower opens, pistil and long stamen diverge, the pistil bending (almost without exception) to the right, and the stamen to the left; at the withering of the flower, they again approach each other, so that the stigma may be fertilised by the pollen of the long stamen. Visiting insects are attracted yet more to the yellow anthers of the two short stamens by their being placed close to a yellow spot, surrounded by a violet border, at the base of the upper petal.

Thus it may be safely assumed that in all these flowers, as well as in the above-mentioned Melastomaceae and Commelynaceae, fertilisation is almost exclusively effected by the pollen of the longer stamens, whilst the shorter stamens serve only to attract pollen-gathering or pollen-eating insects. It is far from surprising that the pollen of these latter stamens, though often produced in large quantity, should tend to degeneration. Darwin long ago came to this conclusion with respect to some Melastomaceae with differently-coloured anthers, of which he had raised seedlings from pollen both of the longer and shorter stamens ("There is reason to believe that the shorter stamens are tending to abortion." "Cross- and Self-Fertilisation," p. 298, footnote). The Lagerstroemia in my garden being self-sterile, I fertilised some flowers with green, and others with yellow pollen of a different variety (or species?) growing in other gardens; both produced fruits with apparently good seeds, but only some of those from the green pollen have germinated.

As in all the flowers above-named, with differently-coloured anthers, the dull colour of those of the longer stamens evidently serves to make them less visible to insects, may not the green colour of the anthers of the long stamens of the mid-styled and short-styled flowers of Lythrum salicaria also protect them against the attacks of pollinivorous insects, to which, from protruding far from the corolla, they would be more exposed than those of the shorter stamens?

Even without being differently coloured, the stamens of the same flower may be divided into different sets with different functions. Thus in a species of Cassia the visiting humble-bees gather the pollen of the four intermediate stamens (the three upper ones being pollenless), which are short and straight, whilst the three lower ones are very long and curved in such a way that their pollen is deposited on the back of the humble-bees. The pistil is of the same length and curved in the same way as the longer stamens. Another very striking instance has been carefully described by Prof. J. E. Todd of Tabor (Iowa) in a plant of a very different family, viz. Solanum rostratum, (American Naturalist, April, 1882, p. 281): one stamen and the pistil are very long and strangely curved; four stamens are short and straight, and serve only to furnish pollen to the visiting insects; all the anthers, as I am informed by Prof. Todd, are of the same dull yellow colour.

FIG. 1.—Flower-spike of Heteranthera reniformis (natural size). FIG. 2.—Upper end of the flower-tube, seen from behind. a', the one anther of the outer whorl, with pate bluish pollen; a, the two anthers of the inner whorl, with bright yellow pollen; st, stigma.