The Various Contrivances by which Orchids are Fertilised by Insects/Chapter 2

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Fly and Spider Ophrys—Bee Ophrys, apparently adapted for perpetual self-fertilisation, but with paradoxical contrivances for intercrossing—Herminium monorchis, attachment of the pollinia to the front legs of insects—Peristylus viridis, fertilisation indirectly effected by nectar secreted from three parts of the labellum—Gymnadenia conopsea, and other species—Habenaria or Platanthera chlorantha and bifolia, their pollinia attached to the eyes of Lepidoptera—Other species of Habenaria—Bonatea—Disa—Summary on the powers of movement in the pollinia.

The genus Ophrys differs from Orchis chiefly in having separate pouch-formed rostella,[1] instead of the two being confluent.

In Ophrys muscifera, or the Fly Ophrys, the chief peculiarity is that the caudicle of the pollinium (B, fig. 5) is doubly bent. The nearly circular piece of membrane, to the under side of which the ball of viscid matter adheres, is of considerable size, and forms the summit of the rostellum. It is thus freely exposed to the air, instead of lying almost hidden at the base of the anther, as in Orchis, and thus kept damp. Nevertheless, when a pollinium is removed, the caudicle bends downwards in the course of about six minutes, and, therefore, at an unusually slow rate; the upper

Fig. 5.

On the Various Contrivances by Which British and Foreign Orchids are Fertilised by Insects, and on the Good Effects of Intercrossing - Fig 5.png

Ophrys muscifera, or Fly Ophrys.

a. anther. s. stigma.
r, r. rostella. l. labellum
A. Flower viewed in front: the two upper petals are almost cylindrical and hairy: the two rostella stand a little in advance of the bases of the anther-cells; but this is not shown from the foreshortening of the drawing.
B. One of the two pollinia removed from its anther-cell, and viewed laterally.

end still remaining curved. I formerly thought that it was incapable of any movement, but have been convinced by Mr. T. H. Farrer of my error. The ball of viscid matter is bathed in fluid within the pouch formed by the lower half of the rostellum, and this is necessary, as the viscid matter quickly sets hard when exposed to the air. The pouch is not elastic, and does not spring up when the pollinium is removed. Such elasticity would have been useless, as there is here a separate pouch for each viscid disc; whereas in Orchis, after one pollinium has been removed, the other has to be kept covered up and ready for action. Hence it appears that nature had been so economical as to save even superfluous elasticity.

The polinnia cannot, as I have often proved, be shaken out of the anther-cells. That insects of some kind visit the flowers, though not frequently, and remove the pollinia, is certain, as we shall immediately see. Twice I have found abundant pollen on the stigmas of flowers, in which both polinnia were still in their cells; and no doubt this might have been much oftener observed. The elongated labellum affords a good landing-place for insects: at its base, just beneath the stigma, there is a rather deep depression, representing the nectary in Orchis; but I could never see a trace of nectar within it; nor have I ever observed any insects approach these inconspicuous and scentless flowers, often as I have watched them. There is, however, on each side of the base of the labellum a small shining projection, having an almost metallic lustre, which appears curiously like a drop of fluid or nectar; and as these flowers are only visited occasionally by insects, Sprengel's view of the existence of sham-nectaries is far more probable in this case than in any other known to me. On several occasions I have detected minute punctures in these protuberances, but I was not able to decide whether they had been made by insects, or whether superficial cells had spontaneously burst. Similar shining protuberances are present on the labella of all the other species of Ophrys. The two rostella stand not far apart, and project over the stigma; and if any object is gently pushed against one of them, the pouch is depressed and the viscid ball, together with the pollinium adheres to it and is easily removed.

The structure of the flower leads me to believe that small insects (as we shall see in the case of Listera) crawl up the labellum to its base, and that in bending their heads downwards, so as to puncture and suck, or only to examine one of the small shining protuberances, they push against the pouch, and a pollinium is attached to their heads; they then fly to another flower, and there bending down in a similar manner, the attached and doubly-bent pollinium, after the movement of depression, strikes the sticky stigmatic surface, and leaves pollen on it. Under the next species we shall see reason for believing that the natural double curvature of the caudicle compensates for its slight power of movement, compared with that in all the species of Orchis.

Number of Flowers.
Both Pollinia or one removed by Insects. Both Pollinia in their Cells.
In 1858, 17 plants, bearing 57 flowers, growing near each other were examined 30 27
In 1858, 25 plants growing in another spot, and bearing 65 flowers 15 50
In 1860, 17 plants, bearing 61 flowers 28 33
In 1861, 4 plants from S. Kent, bearing 24 flowers (all the previous plants having grown in N. Kent) 15 9
Total 88 119

That insects visit the flowers of the Fly Ophrys and remove the pollinia, though not effectually or sufficiently, the following cases show. During several years before 1858 I occasionally examined some flowers, and found that only thirteen out of 102 had one or both pollinia removed. Although at the time I recorded in my notes that most of the flowers were partly withered, I now think that I must have included many young flowers, which might perhaps have been subsequently visited; so I prefer trusting to the following observations.

We here see that, out of 207 flowers examined, not half had been visited by insects. Of the eighty-eight flowers visited, thirty-one had only one pollinium removed. As the visits of insects are indispensable for the fertilisation of this Orchid, it is surprising (as in the case of Orchis fusca) that the flowers have not been rendered more attractive to insects. The number of seed-capsules produced is proportionably even less than the number of flowers visited by insects. The year 1861 was extraordinarily favourable to this species in this part of Kent, and I never saw such numbers in flower; accordingly I marked eleven plants, which bore forty-nine flowers, but these produced only seven capsules. Two of the plants each bore two capsules, and three other plants each bore one, so that no less than six plants did not produce a single capsule! What are we to conclude from these facts? Are the conditions of life unfavourable to this species, though during the year just alluded to it was so numerous in some places as to deserve to be called quite common? Could the plant nourish more seed; and would it be of any advantage to it to produce more seed? Why does it produce so many flowers, if it already produces a sufficiency of seeds? Something seems to be out of order in its mechanism or in its conditions. We shall presently see that Ophrys apifera or the Bee Ophrys presents a wonderful contrast in every flower producing a capsule.

Ophrys aranifera, or the Spider Ophrys.—I am indebted to Mr. Oxenden for some spikes of this rare species.Fig. 6. On the Various Contrivances by Which British and Foreign Orchids are Fertilised by Insects, and on the Good Effects of Intercrossing - Fig 6.pngOphrys aranifera.
A. Pollinium before the act of depression.
B. Pollinium after the act of depression.
Whilst the pollinia remain enclosed within their cells, the lower part of the caudicle projects up in a straight line from the viscid disc, and therefore has a very different form from the corresponding part of the caudicle of O. muscifera; but the upper part (A, fig. 6) is a little bent forward, that is, towards the labellum. The point of attachment of the caudicle to the disc is hidden within the bases of the anther-cells, and is thus kept damp; consequently, as soon as the pollinia are exposed to the air, the usual movement of depression takes place, and they sweep through an angle of about ninety degrees. By this movement they assume, supposing them to be attached to an insect's head, a position exactly adapted for striking the stigmatic surface, which is situated, relatively to the pouch-formed rostella, rather lower down in the flower than in the Fly Ophrys.

I examined fourteen flowers of the Spider Ophrys, several of which were partly withered; and in none were both pollinia, and in three alone was one pollinium removed. Hence this species, like the Fly Ophrys, is but little visited by insects in England. In parts of Italy it is even less visited, for Delpino states[2] that in Liguria hardly one flower out of 3000 sets a capsule, though near Florence rather more capsules are produced. The labellum does not secrete any nectar. The flowers, however, must be occasionally visited and fertilised by insects, for Delpino found[3] pollen-masses on the stigmas of some flowers which still retained both their own pollinia.

The anther-cells are remarkably open, so that with some plants which were sent me in a box, two pair of pollinia fell out, and stuck by their viscid discs to the petals. Here we have an instance of the first appearance of a trifling structure which is of not the least use to its possessor, but becomes when a little more developed, highly beneficial to a closely-allied species; for although the open state of the anther-cells is useless to the Spider Ophrys, it is of the highest importance, as we shall presently see, to the Bee Ophrys. The flexure of the upper end of the caudicle of the pollinium is of service to the Spider and Fly Ophrys, by aiding the pollen-masses, when carried by insects to another flower, to strike the stigma; but by an increase of this bend together with increased flexibility in the Bee Ophrys, the pollinia become adapted for the widely different purpose of self-fertilisation.

Ophrys arachnites.—This form, of which Mr. Oxenden sent me several living specimens,Fig. 7.Darwin - The various contrivances by which orchids are fertilized by insects (1877) - Fig 7.pngPollinium of Ophrys arachnite is considered by some botanists as only a variety of the Bee Ophrys, by others as a distinct species. The anther-cells do not stand so high above the stigma, and do not overhang it so much, as in the Bee Ophrys, and the pollen masses are more elongated. The caudicle is only two-thirds, or even only half as long as that of the Bee Ophrys, and is much more rigid; the upper part is naturally curved forward; the lower part undergoes the usual movement of depression, when the pollinia are removed from their cells. The pollen-masses never fall spontaneously out of their cells. This plant, therefore, differs in every important respect from O. apifera, and seems to be much more closely allied to O. aranifera.

Ophrys scolopax of Cavanilles.—This form inhabits the north of Italy and the south of France. Mr. Moggridge says[4] that at Mentone it never shows any tendency to fertilise itself, whilst at Cannes the pollen-masses naturally fall out of their cells and strike the stigma. He adds: "This material difference between the two is accomplished by a very slight bend in the anther-ceils, which are prolonged into a beak of variable length, in the case of the self-fertilising blossoms."

Ophrys apifera.—The Bee Ophrys differs widely from the great majority of Orchids in being excellently constructed for fertilising itself. The two pouch-formed rostella, the viscid discs, and the position of the stigma, are nearly the same as in the other species of Ophrys; but the distance of the two pouches from each other, and the shape of the pollen-masses are somewhat variable.[5] The caudicles of the pollinia are remarkably long, thin, and flexible, instead of being, as in all the other Ophreæ seen by me, rigid enough to stand upright. They are necessarily curved forward at their upper ends, owing to the shape of the anther-cells; and the pear-shaped pollen-masses lie embedded high above and directly over the stigma. The anther-cells naturally open soon after the flower is fully expanded, and the thick ends of the pollen-masses then fall out, the viscid discs still, remaining in their pouches. Slight as is the weight of the pollen-masses, yet the caudicles are so thin and quickly become so flexible, that in the course of a few hours they sink down, until they hang freely in the air

Fig. 8.

Darwin - The various contrivances by which orchids are fertilized by insects (1877) - Fig 8.png

Ophrys apifera, or Bee Ophrys.

l. l.a. anther.
l. l. labellum.
A. Side view of flower, with the upper sepal and the two upper petals removed. One pollinium, with its disc still in its pouch, is represented as just falling out of the anther-cell; and the other has fallen almost to its full extent, opposite to the hidden stigmatic surface.
B. Pollinium in the position in which it lies embedded.

(see lower pollen-mass in fig. A) exactly opposite to and in front of the stigmatic surface. In this position a breath of air, acting on the expanded petals, sets the flexible and elastic caudicles vibrating, and they almost immediately strike the viscid stigma, and, being there secured, impregnation is effected. To make sure that no other aid was requisite, though the experiment was superfluous, I covered up a plant under a net, so that the wind, but no insects, could pass in, and in a few days the pollinia became attached to the stigmas. But the pollinia of a spike kept in water in a still room remained free, suspended in front of the stigma, until the flowers withered.

Robert Brown first observed that the structure of the Bee Ophrys is adapted for self-fertilisation.[6] When we consider the unusual and perfectly-adapted length, as well as the remarkable flexibility of the caudicles; when we see that the anther-cells naturally open, and that the masses of pollen, from their weight, slowly fall down to the exact level of the stigmatic surface, and are there made to vibrate by the slightest breath of wind until the stigma is struck; it is impossible to doubt that these several points of structure and function, which occur in no other British Orchid, are specially adapted for self-fertilisation.

The result is what might have been anticipated. I have often noticed that the spikes of the Bee Ophrys apparently produced as many seed-capsules as flowers; and near Torquay I carefully examined many dozen plants, some time after the flowering season; and on all I found from one to four, and occasionally five, fine capsules, that is, as many capsules as there had been flowers. In extremely few cases, with the exception of a few deformities, generally on the summit of the spike, could a flower be found which had not produced a capsule. Let it be observed what a contrast this species presents with the Fly Ophrys, which requires insect aid for its fertilisation, and which from forty-nine flowers produced only seven capsules!

From what I had then seen of other Orchids, I was so much surprised at the self-fertilisation of this species, that I examined during many years, and asked others to examine, the state of the pollen-masses in many hundreds of flowers, collected in various parts of England. The particulars are not worth detailing; but I may give as an instance, that Mr. Farrer found in Surrey that not one flower out of 106 had lost both pollinia, and that only three had lost a single one. In the Isle of Wight, Mr. More examined 136 flowers, and of these the very unusual number of ten had lost both, and fourteen had lost one; but then he found that in eleven cases the caudicles had been gnawed through apparently by snails, the discs still remaining in their pouches; so that the pollinia had not been carried away by insects. In some few cases, also, in which I found the pollinia removed, the petals were marked with the slime of snails. Nor must we forget that a blow from a passing animal, and possibly heavy storms of wind might occasionally cause the loss of one or both pollinia.

During most years the pollen-masses of the many hundred flowers which were examined, adhered with the rarest exceptions to the stigma, with their discs still enclosed within the pouches. But in the year 1868, from some cause the nature of which I cannot conjecture, out of 116 flowers gathered in two localities in Kent, seventy-five retained both pollinia in their cells; ten had one pollinium, and only thirty-one had both adhering to the stigma. Long and often as I have watched plants of the Bee Ophrys, I have never seen one visited by any insect.[7] Robert Brown imagined that the flowers resembled bees in order to deter their visits, but this seems extremely improbable. The flowers with their pink sepals do not resemble any British bee, and it is probably true, as I have heard it said, that the plant received its name merely from the hairy labellum being somewhat like the abdomen of a humble-bee. We see how fanciful many of the names are,—one species being called the Lizard and another the Frog Orchis. The resemblance of O. muscifera to a fly is very much closer than that of O. apifera to a bee; and yet the fertilisation of the former absolutely depends on and is effected by the means of insects.

All the foregoing observations relate to England, but Mr. Moggridge made similar ones on the Bee Ophrys in Northern Italy and Southern France, as did Treviranus[8] in Germany, and. Dr. Hooker in Morocco. We may therefore conclude,—from the pollinia spontaneously falling on the stigma—from the co-related structure of all the parts for this purpose—and from almost all the flowers producing seed-capsules—that this plant has been specially adapted for self-fertilisation. But there is another side to the case.

When an object is pushed against one of the pouches of the rostellum, the lip is depressed, and the large viscid disc adheres firmly to it; and when the object is removed, so is the pollinium, but perhaps not quite so readily as in the other species of Ophrys. Even after the pollen-masses have naturally fallen out of their cells on to the stigma, their removal can sometimes be thus effected. As soon as the disc is drawn out of its pouch a movement of depression commences, by which the pollinium if attached to the front of an insect's head would be brought into a proper position for striking the stigma. When a pollen-mass is placed on the stigma and then withdrawn, the elastic threads by which the packets are tied together break, and leave several packets on the viscid surface. In all other Orchids the meaning of these several contrivances is unmistakably clear—namely, the downward movement of the lip of the rostellum when gently pushed—the viscidity of the disc—the depression of the caudicle as soon as the disc is exposed to the air—the rupturing of the elastic threads—and the conspicuousness of the flower. Are we to believe that these adaptations for cross-fertilisation in the Bee Ophrys are absolutely purposeless, as would certainly be the case if this species has always been and will always be self-fertilised? It is, however, just possible that insects, although they have never been seen to visit the flowers, may at rare intervals transport the pollinia from plant to plant, during such seasons as that of 1868, when the pollinia did not all fall out of the anther-cells so as to reach the stigmas. The whole case is perplexing in an unparalleled decree, for we have in the same flower elaborate contrivances for directly opposed objects.

That cross-fertilisation is beneficial to most Orchids, we may infer from the innumerable structures serving for this purpose which they present; and I have elsewhere shown in the case of many other groups of plants[9] that the benefits thus derived are of high importance. On the other hand, self-fertilisation is manifestly advantageous in as far as it ensures a full supply of seed; and we have seen with the other British species of Ophrys which cannot fertilise themselves, how small a proportion of their flowers produce capsules. Judging therefore from the structure of the flowers of O. apifera, it seems almost certain that at some former period they were adapted for cross-fertilisation, but that failing to produce a sufficiency of seed they became slightly modified so as to fertilise themselves. It is, however, remarkable on this view, that none of the parts in question show any tendency to abortion—that in the several and distant countries which the plant inhabits, the flowers are still conspicuous, the discs still viscid, and the caudicles still retain the power of movement when the discs are exposed to the air. The metallic points at the base of the labellum are however smaller than in the other species; and if these serve to attract insects, this difference is of some signification. As it can hardly be doubted that O. apifera was at first constructed so as to be regularly cross-fertilised, it may be asked will it ever revert to its former state; and if it does not so revert, will it become extinct? These questions cannot be answered, any more than in the case of those plants which are now propagated exclusively by buds, stolons, &c., but which produce flowers that rarely or never set any seed; and there is reason to believe that a sexual propagation is closely analogous to long-continued self-fertilisation.

Finally Mr. Moggridge has shown that in North Italy Ophrys apifera, aranifera, arachnites, and scolopax are connected by so many and such close intermediate links,[10] that all seem to form a single species in accordance with the belief of Linnæus, who grouped, them all together under the name of Ophrys insectifera. Mr. Moggridge further shows that in Italy O. aranifera flowers first, and O. apifera last, the intermediate forms at intermediate periods; and according to Mr. Oxenden, the same fact holds good to a certain extent in Kent. The three forms which inhabit England do not seem to blend into one another as in Italy, and I am assured by Mr. Oxenden, who has closely attended to these plants in their native homes, that O. aranifera and apifera always grow in distinct spots. The case therefore is an interesting one, as here we have forms which may be and generally have been ranked as true species, but which in North Italy have not as yet been fully differentiated. The case is all the more interesting, as the intermediate forms can hardly be due to the crossing of O. aranifera with apifera; this latter species being regularly self-fertilised and apparently never visited by insects. Whether we rank the several forms of Ophrys as closely allied species or as mere varieties of the same species, it is remarkable that they should differ in a character of such physiological importances as the flowers of some being plainly adapted for self-fertilisation, whilst the flowers of others are strictly adapted for cross-fertilisation, being utterly sterile if not visited by insects.

Herminium monorchis.—The Musk Orchis, which is a rare British plant, is generally spoken of as having naked glands or discs, but this is not strictly correct. The disc is of unusual size, nearly equalling the mass of pollen-grains: it is subtriangular, with one side protuberant, and somewhat resembles a distorted helmet in shape: it is formed of hard tissue with the base hollowed out, and viscid; the base resting on and being covered by a narrow strip of membrane, which is easily pushed away, and answers to the pouch in Orchis. The whole upper part of the helmet answers to the minute oval bit of membrane to which the caudicle of Orchis is attached and which in Ophrys is larger and convex. When the lower part of the helmet is moved by any pointed object, the point readily slips into its hollow base, and is there held so firmly by the viscid matter, that the whole helmet appears adapted to stick to some prominent part of an insect's body. The caudicle is short and very elastic; it is attached not to the apex of the helmet, but to the hinder end; if it had been attached to the apex, the point of attachment would have been freely exposed to the air and not kept damp; and then the pollinium when removed from its cell would not have been quickly depressed.

This movement is well marked, and serves to bring the end of the pollen-mass into a proper position for striking the stigma. The two viscid discs stand wide apart. There are two transverse stigmatic surfaces, meeting by their points in the middle; but the broad part of each lies directly beneath each disc. The labellum is remarkable from not differing much in shape from the two upper petals, and from not always occupying the same position in reference to the axis of the plant, owing to the ovarium being more or less twisted. This state of the labellum is intelligible, for as we shall see, it does not serve as a landing-place for insects. It is upturned, and together with the two other petals makes the whole flower in some degree tubular. At its base there is a hollow so deep as almost to deserve to be called a nectary; but I could not perceive any nectar, which, as I believe, remains enclosed in the intercellular spaces. The flowers are very small and inconspicuous, but emit a strong honey-like odour. They seem highly attractive to insects; in a spike with only seven flowers recently open, four had both pollinia, and one had a single pollinium removed.

When the first edition of this book appeared I did not know how the flowers were fertilised, but my son George has made out the whole process, which is extremely curious and differs from that in any other Orchid known to me. He saw various minute insects entering the flowers, and brought home no less than twenty-seven specimens with pollinia (generally with only one, but sometimes with two) attached to them. These insects consisted of minute Hymenoptera (of which Tetrastichus diaphantus was the commonest), of Diptera and Coleoptera, the latter being Malthodes brevicollis. The one indispensable point appears to be that the insect should be of very small size, the largest being only the 1/20 of an inch in length. The pollinia were always attached to the same place, namely, to the outer surface of the femur of one of the front legs, and generally to the projection formed by the articulation of the femur with the coxa. The cause of this peculiar mode of attachment is sufficiently clear: the middle part of the labellum stands so close to the anther and stigma, that insects always enter the flower at one corner, between the edge of the labellum and one of the upper petals; they also almost always crawl in with their backs turned directly Or obliquely towards the labellum. My son saw several which began to crawl into the flowers in a different position; but they came out and changed their position. Standing in either corner of the flower, with their backs turned towards the labellum, they insert their heads and fore legs into the short nectary, which is seated between the two widely separated viscid discs. I ascertained that they had occupied this position by finding three dead insects, permanently glued to the discs. Whilst sucking the nectar, which takes two or three minutes, the projecting joint of the femur stands under the large helmet-like viscid disc on either side; and when the insect retreats, the disc exactly fits on and is glued to the prominent joint, or to the surface of the femur. The movement of depression in the caudicle now takes place, and the mass of pollen-grains then projects just beyond the tibia; so that the insect, when entering another flower, can hardly fail to fertilise the stigma, which is situated directly beneath the disc on either side.

Fig. 9.

Darwin - The various contrivances by which orchids are fertilized by insects (1877) - Fig 9.png

Peristylus viridis, or Frog Orchis.

Front view of flower.

a. anther. n′ n′. lateral nectarics.
s. stigma. l. labellum
n. orifice of central nectary.

Peristylus viridis.—This plant, which bears the odd name of the Frog Orchis, has been placed by many botanists in the genus Habenaria or Platanthera; but as the discs are not naked, it is doubtful whether this classification can be correct. The rostella are small and widely separated from each other. The viscid matter on the under side of the disc forms an oval ball which is enclosed within a small pouch. The upper membrane to which the caudicle is attached is of large size relatively to the whole disc, and is freely exposed to the air. Hence probably it is that the pollinia when removed from their cases do not become depressed until, as Mr. T. H. Farrer has observed, twenty or thirty minutes have elapsed. Owing to this long interval, I formerly thought that they did not undergo any movement of depression. Supposing a pollinium to be attached to the head of an insect, and to have become depressed, it will stand at the proper angle, vertically, for striking the stigma. But from the lateral position of the anther-cells, notwithstanding that they converge a little towards their upper ends, it is difficult at first to see how the pollinia when removed by insects are afterwards placed on the stigma; for this is of small size and is situated in the middle of the flower between the two widely separated rostella.

The explanation is, I believe, as follows. The base of the elongated labellum forms a rather deep hollow in front of the stigma, and in this hollow, but some way in advance of the stigma, a minute slit-like orifice (n) leads into a short bilobed nectary. Hence an insect, in order to suck the nectar with which the nectary is filled, would have to bend down its head in front of the stigma. The labellum has a medial ridge, which would probably induce an insect first to alight on either side; but, apparently to make sure of this, besides the true nectary, there are two spots (n′ n′) which secrete drops of nectar on each side at the base of the labellum, bordered by prominent edges, directly beneath the two pouches. Now let us suppose an insect to alight on one side of the labellum so as first to lick up the exposed drop of nectar on this side; from the position of the pouch exactly over the drop, it would almost certainly get the pollinium of this side attached to its head. If it were now to go to the mouth of the true nectary, the pollinium attached to its head from not having as yet become depressed would not touch the stigma; that there would be no self-fertilisation. The insect would then probably suck the exposed drop of nectar on the other side of the labellum, and would perhaps get another pollinium attached to its head; it would thus be considerably delayed by having to visit the three nectaries. It would then visit other flowers on the same plant, and afterwards flowers on a distinct plant; and by this time, but not before, the pollinia will have undergone the movement of depression and will be in a proper position for effecting cross-fertilisation. It thus appears that the secretion of nectar at three separate points of the labellum,—the wide distance apart of the two rostella,—and the slow downward movement of the caudicle without any lateral movement—are all correlated for the same purpose of cross-fertilisation.

To what extent this Orchis is frequented by insects, and what the kinds are, I do not know, but several of the flowers on two spikes, sent me by the Rev. B. S. Maiden, had a single pollinium removed, and one flower had both removed.

We now come to two genera, namely, Gymnadenia and Habenaria or Platanthera, including four British species, which have uncovered viscid discs. The viscid matter, as before remarked, is of a somewhat different nature from that in Orchis, Ophrys, &c., and does not rapidly set hard. Their nectaries are stored with free nectar. With respect to the uncovered condition of the discs, the last species, or Peristylus viridis, is in an almost intermediate condition. The four following species compose a much broken series. In Gymnadenia conopsea the vicid discs are narrow and much elongated, and lie close together; in G. albida they are less elongated, but still approximate; in Habenaria bifolia they are oval and far apart; and, lastly, in H. clorantha they are circular and much farther apart.

Gymnadenia conopsea.—In general appearance this plant resembles pretty closely a true Orchis. The pollinia differ in having naked, narrow, strap-shaped

Fig. 10.

Darwin - The various contrivances by which orchids are fertilized by insects (1877) - Fig 10.png

Gymnadenia conopsea.

A. Pollinium, before the act of depression.
B. Pollinium, after the act of depression, but before it has closely clasped the disc.

discs, which are as long as the caudicles (fig. 10). When the pollinia are exposed to the air the caudicle is depressed in from thirty to sixty seconds; and as the posterior surface of the caudicle is slightly hollowed out, it closely clasps the upper membranous surface of the disc. The mechanism of this movement will be described in the last chapter. The elastic threads by which the packets of pollen are bound together are unusually weak, as is likewise the case with the two following species of Habenaria: this was well shown by the state of specimens which had been kept in spirits of wine. This weakness apparently stands in relation to the viscid matter of the discs not setting hard and dry as in Orchis; So that a moth with a pollinium attached to its proboscis might be enabled to visit several flowers without having the whole pollinium dragged off by the first stigma which was struck. The two strap-shaped discs lie close together, and form the arched roof of the entrance into the nectary. They are not protected, as in Orchis, by a lower lip or pouch, so that the structure of the rostellum is simpler. When we come to treat of the homologies of the rostellum we shall see that this difference is due to a small change, namely, to the lower and exterior cells of the rostellum resolving themselves into viscid matter; whereas in Orchis the exterior surface retains its early cellular or membranous condition.

As the two viscid discs form the roof of the mouth of the nectary, and are thus brought down near to the labellum, the two stigmas, instead of being confluent and standing beneath the rostellum, as in most of the species of Orchis, are lateral and separate. These stigmas consist of protuberant, almost horn-shaped, processes on each side of the nectary. That their surfaces are really stigmatic I ascertained by finding them deeply penetrated by a multitude of pollen-tubes. As in the case of Orchis pyramidalis, it is a pretty experiment to push a fine bristle straight into the narrow mouth of the nectary, and to observe how certainly the narrow elongated viscid discs, forming the roof, stick to the bristle. When the bristle is withdrawn, the pollinia adhering to its upper side are withdrawn; and as the discs form the sides of the arched roof, they adhere somewhat to the sides of the bristle. They then quickly become depressed so as to lie in the same line with the bristle,—one a little on one side, and the other on the other side; and if the bristle, held in the same relative position, be now inserted into the nectary of another flower, the two ends of the pollinia accurately strike the two protuberant stigmatic surfaces, situated on each side of the mouth of the nectary.

The flowers smell sweet, and the abundant nectar always contained in their nectaries seems highly attractive to Lepidoptera, for the pollinia are soon and effectually removed. For instance, in a spike with forty-five open flowers, forty-one had their pollinia removed, or had pollen left on their stigmas: in another spike with fifty-four flowers, thirty-seven had both pollinia, and fifteen had one pollinium, removed; so that only two flowers in the whole spike had neither pollinium removed.

My son George went at night to a bank where this species grows plentifully, and soon caught Plusia chrysitis with six pollinia, P. gamma with three, Anaitis plagiata with five, and Triphæna pronuba with seven pollinia attached to their proboscides. I may add that he also caught the first-named moth in my flower-garden, with the pollinia of this Orchis attached to its proboscis, but with all the pollen-grains removed, although the garden is a quarter of a mile distant from any spot where the plant grows. Many of the above moths had only a single pollinium attached, somewhat laterally to their proboscides; and this would happen in every case, unless the moth stood directly in front of the nectary and inserted it proboscis exactly between the two discs. But as the labellum is rather broad and flat, with no guiding ridges like those on the labellum of Orchis pyramidalis, there is nothing to compel moths to insert their proboscides symmetrically into the nectary, and there would be no advantage in their doing so.

Gymnadenia albida.—The structure of the flower of this species resembles in most respects that of the last; but, owing to the upturning of the labellum, it is rendered almost tubular. The naked elongated discs are minute and approximate. The stigmatic surfaces are partially lateral and divergent. The nectary is short, and full of nectar. Small as the flowers are, they seem highly attractive to insects: of the eighteen lower flowers on one spike, ten had both, and seven had one pollinium removed; on some older spikes all the pollinia had been removed, except from two or three of the uppermost flowers.

Gymnadenia odoratissima is an inhabitant of the Alps, and is said by Dr. H. Müller[11] to resemble in all the above characters G. conopsea. As the flowers, which are pale coloured and highly perfumed, are not visited by butterflies, he believes that they are fertilised exclusively by moths. The North American G. tridentata, described by Professor Asa Gray,[12] differs in an important manner from the foregoing species. The anther opens in the bud, and the pollen-grains, which in the British species are tied together by very weak threads, are here much more incoherent, and some invariably fall on the two stigmas and on the naked cellular tip of the rostellum; and this latter part, strange to say, is penetrated by the pollen-tubes. The flowers are thus self-fertilised. Nevertheless, as Professor Gray adds, "all the arrangements for the removal of the pollinia by insects, including the movement of depression, are as perfect as in the species which depend upon insect aid." Hence there can be little doubt that this species is occasionally cross-fertilised.

Fig. 11.

Darwin - The various contrivances by which orchids are fertilized by insects (1877) - Fig 11.png

Habenaria chlorantha, or Butterfly Orchis.

a a. anther-cells.
d. disc of pollinium.
s. stigma.
n. nectary.
n′. orrifice of nectary.
l. labellum.
A. Flower viewed in front, with all the sepals and petals removed except the labellum with its nectary, which is turned to one side.
B. A pollinium. (This has hardly a sufficiently elongated appearance.) The drum-like pedicel is hidden behind the disc.
C. Diagram, giving a section through the viscid disc, the drum-like pedicel, and the attached end of the caudicle. The viscid disc is formed of an upper membrane with a layer of viscid matter beneath.

Habenaria or Platanthera chlorantha.—The pollinia of the Large Butterfly Orchis differ considerably from those of any species hitherto mentioned. The two anther-cells are separated from each, other by a wide space of connective membrane, and the pollinia are enclosed in a backward sloping position (fig. 11). The viscid discs front each other, and stand in advance of the stigmatic surface. In consequence of their forward position, the caudicles and pollen-masses are much elongated. Each viscid disc is circular, and, in the early bud, consists of a mass of cells, of which the exterior layers (answering to the lip or pouch in Orchis) resolve themselves into adhesive matter. This matter has the property of remaining adhesive for at least twenty-four hours after the pollinium has been removed from its cell. The disc, externally covered with a thick layer of adhesive matter (see fig. C, which stands so that the layer of viscid matter is below) is produced on its opposite and embedded side into a short drum-like pedicel. This pedicel is continuous with the membranous portion of the disc and is formed of the same tissue. The caudicle of the pollinium is attached in a transverse direction to the embedded end of the pedicel, and its extremity is prolonged, as a bent rudimentary tail, just beyond the drum. The caudicle is thus united to the viscid disc in a very different manner, and in a plane at right angles, to what occurs in the other British Orchids. In the short drum-like pedicel, we have a small development of the long pedicel of the rostellum, which is so conspicuous in many Vandeæ, and which connects the viscid disc with the true caudicles of the pollinia.

The drum-like pedicel is of the highest importance, not only by rendering the viscid disc more prominent and more likely to stick to the face of an insect whilst inserting its proboscis into the nectary beneath the stigma, but on account of its power of contraction. The pollinia lie inclined backwards in their cells (see fig. A), above and some way on each side of the stigmatic surface; if attached in this position to the head of an insect, the insect might visit any number of flowers, and no pollen would be left on the stigma. But observe what takes place: in a few seconds after the inner end of the drum-like pedicel has been removed from its embedded position and exposed to the air, one side of the drum contracts, and this contraction draws the thick end of the pollinium inwards, so that the caudicle and the viscid surface of the disc are no longer parallel, as they were at first, and as they are represented in the section, fig. C. At the same time the drum rotates through nearly a quarter of a circle, and this moves the caudicle downwards, like the hand of a clock, depressing the thick end of the pollinium or mass of pollen-grains. Let us suppose the right-hand disc to be affixed to the right side of an insect's face, and by the time required for the insect to visit another flower on another plant, the pollen-bearing end of the pollinium will have moved downwards and inwards, and will now infallibly strike the viscid surface of the stigma, situated in the middle of the flower beneath and between the two anther-cells.

The little rudimentary tail of the caudicle projecting beyond the drum-like pedicel is an interesting point to those who believe in the modification of species; for it shows us that the disc has been carried a little inwards, and that primordially the two discs stood even still further in advance of the stigma than they do at present. We thus learn that the parent-form approached in this respect the structure of that extraordinary Orchid, the Bonatea speciosa of the Cape of Good Hope.

The remarkable length of the nectary, containing much free nectar, the white colour of the conspicuous flowers, and the strong sweet odour emitted by them at night, all show that this plant depends for its fertilisation on the larger nocturnal Lepidoptera. I have often found spikes with almost all the pollinia removed. From the lateral position and distance of the two viscid discs from each other, the same moth would generally remove only one pollinium at a time; and in a spike which had not as yet been much visited, three flowers had both pollinia, and eight flowers had only one pollinium removed. From the position of the discs it might have been anticipated that they would adhere to the side of the head or face of moths; and Mr. F. Bond sent me a specimen of Hadena dentina with one eye covered and blinded by a disc, and a specimen of Plusia v. aureum with a disc attached to the edge of the eye. Mr. Marshall[13] collected twenty specimens of Cucullia umbratica on an island in Derwentwater, separated by half-a-mile of water from any spot where H. chlorantha grew; nevertheless, seven of these moths had the pollinia of this Orchid affixed to their eyes. Although the discs are so adhesive that almost all the pollinia in a bunch of flowers which was carried in my hand and thus shaken were removed by adhering to the petals or sepals, yet it is certain that moths, probably the smaller species, often visit these flowers without removing the pollinia; for on examining the discs of a large number of pollinia whilst still in their cells I found minute Lepidopterous scales glued to them.

The cause of the flowers of various kinds of Orchids being constructed so that the pollinia are always affixed to the eyes or proboscides of Lepidoptera, and to the naked foreheads or proboscides of Hymenoptera, no doubt is that the viscid discs cannot adhere to a scaly or very hairy surface; the scales themselves being easily detached. Variations in the structure of the flower of an Orchid, unless they led to the viscid discs touching some part of the body of an insect where they would remain firmly attached, would be of no service, but an injury to the plant; and consequently such variations would not be preserved and perfected.

Habenaria bifolia, or Lesser Butterfly Orchis.—I am aware that this form and the last are considered by Mr. Bentham and by some other botanists as mere varieties of one another; for it is said that intermediate gradations in the position of the viscid discs occur. But we shall immediately see that the two forms differ in a large number of other characters, not to mention general aspect and the stations inhabited, with which we are not here concerned. Should these two forms be hereafter proved to graduate into each other, independently of hybridisation, it would be a remarkable case of variation; and I, for one, should be as much pleased as surprised at the fact, for these two forms certainly differ from one another more than do most species belonging to the same genus.

The viscid discs of the Lesser Butterfly Orchis are oval, and face each other. They stand far closer together than in the last species; so much so, that in the bud, when their surfaces are cellular, they almost touch. They are not placed so low down relatively to the mouth of the nectary. The viscid matter is of a somewhat different chemical nature, as shown by its much greater viscidity, if after having been long dried it is moistened, or after being kept in weak spirits of wine. The drum-like pedicel can hardly be said to be present, but is represented by a longitudinal ridge, truncated at the end where the caudicle is attached, and there is hardly a vestige of the rudimentary tail. In fig. 12 the discs of both species, of the proper proportionalFig. 12.Darwin - The various contrivances by which orchids are fertilized by insects (1877) - Fig 12.pngB. Disc and caudicle of H. chlorantha, seen from above, with the drum-like pedicel fore-shortened.
A.  Disc and caudicle of H. bifolia, seen from above.
sizes, are represented as seen vertically from above. The pollinia, after removal from their cells, undergo nearly the same movements as in the last species. In both forms the movement is well shown, by removing a pollinium by the thick end with a pair of pincers, and holding it under the microscope, when the plane of the viscid disc will be seen to move through an angle of at least forty-five degrees. The caudicles of the Lesser Butterfly Orchis are relatively very much shorter than in the other species; the little packets of pollen are shorter, whiter, and, in a mature flower, separate much more readily from one another. Lastly, the stigmatic surface is differently shaped, being more plainly tripartite, with two lateral prominences, situated beneath the viscid discs. These prominences contract the mouth of the nectary, making it subquadrangular. Hence I cannot doubt that the Larger and Lesser Butterfly Orchids are distinct species, masked by close external similarity.[14]

As soon as I had examined the present species, I felt convinced, from the position of the viscid discs, that it would be fertilised in a different manner from the Larger Butterfly Orchis; and now, owing to the kindness of Mr. F. Bond, I have examined two moths, namely, Agrotis segetum and Anaitis plagiata, one with three pollinia, and the other with five pollinia, attached, not to the eyes and side of the face as in the last species, but to the base of the proboscis. I may remark that the pollinia of these two species of Habenaria, when attached to moths, can be distinguished at a glance.

Professor Asa Gray has described[15] the structure of no less than ten American species of Platanthera. Most of them resemble in their manner of fertilisation the two British species; but some of the species, in which the viscid discs do not stand far apart, have curious contrivances, such as a channelled labellum, lateral shields, &c., compelling moths to insert their proboscides directly in front. P. hookeri, on the other hand, differs in a very interesting manner: the two viscid discs stand widely separated from each other; consequently a moth, unless of gigantic size, would be able to suck the copious nectar without touching either disc; but this risk is avoided in the following manner:—the central line of the stigma is prominent, and the labellum, instead of hanging down, as in most of the other species, is curved upwards, so that the front of the flower is made somewhat tubular and is divided into halves. Thus a moth is compelled to go to the one or other side, and its face will almost certainly be brought into contact with one of the discs. The drum of the pollinium, when removed, contracts in the same manner as I have described under P. chlorantha. Professor Gray has seen a butterfly (Nisoniades) from Canada with a pollinium of this species attached to each eye. In the case of P. flava, moths are compelled in a different manner to enter the nectary on one side. A narrow but strong protuberance, rising from the base of the labellum, projects upwards and backwards, so as almost to touch the column ; thus the moth, being forced to go to either side, is almost sure to withdraw one of the viscid discs. P. hyperborea and dilatata have been regarded by some botanists as varieties of the same species; and Professor Asa Gray says that he was formerly tempted to come to the same conclusion; but on closer examination he finds, besides other characters, a remarkable physiological difference, namely, that P. dilatata, like its congeners, requires insect aid and cannot fertilise itself; whilst in P. hyperborea the pollen-amasses commonly fall out of the anther-cells whilst the flower is very young or in bud, and thus the stigma is self-fertilised. Nevertheless, the various structures adapted for crossing are still present.[16]

The genus Bonatea is closely allied to Habenaria, and includes plants having an extraordinary structure. Bonatea speciosa is an inhabitant of the Cape of Good Hope, and has been carefully described by Mr. Trimen;[17] but it is impossible to explain its structure without drawings. It is remarkable from the manner in which the two stigmatic surfaces, as well as the two viscid discs, project far out in front of the flower, and from the complex nature of the labellum, which consists of seven, or probably of nine distinct parts all fused together. As in Platanthera flava, there is a process at the base of the labellum which compels moths to enter the flower on either side. The nectary, according to Mr. Trimen and Mr. J. Mansel Weale, does not contain free nectar; but the latter author believes that the tissue of which it is composed tastes sweet, so that moths probably penetrate it for the sake of the intercellular fluid. The pollinia are of astonishing length, and when removed from their cases hang down merely from the weight of the pollen-masses, and if attached to the head of an insect would be in a proper position for adhering to the stigma. Mr. Weale has likewise described some other South African species of Bonatea.[18] These differ from B. speciosa in having their nectaries full of nectar. He found a small butterfly, Pyrgus elmo, "perfectly embarrassed by the number of pollinia of this Bonatea attached to its sternum." But he does not specify whether the sternum was naked or covered with scales.

The South African genera Disa and Disperis are placed by Lindley in two sub-tribes of the Ophreæ. The superb flowers of Disa grandiflora have been described and figured by Mr. Trimen.[19] The posterior sepal, instead of the labellum, is developed into a large nectary. In order that insects may reach the copiously stored nectar, they must insert their proboscides on either side of the column; and in accordance with this fact the viscid discs are turned outwards in an extraordinary manner. The pollinia are crooked, and when removed bend downwards from their own weight, so that no movement is necessary for placing themselves in a proper position. Considering the large supply of nectar and that the flowers are very conspicuous, it is remarkable that they are rarely visited by insects. Mr. Trimen wrote to me in 1864 that he had lately examined seventy-eight flowers, and only twelve of these had one or both pollinia removed by insects, and only five had pollen on their stigmas. He does not know what insects occasionally fertilise the flowers; but Mrs. Barber has more than once seen a large fly, allied to Bombylius, with the pollinia of Disa polynoides attached to the base of its proboscis. Mr. Weale states[20] that D. macrantha differs from D. grandiflora and cornuta in producing plenty of seed, and is remarkable from often fertilising itself. This follows from "a very slight jerk, when the flower is fully expanded, sufficing to eject the pollinia from their widely open anther-cases, and to bring them into contact with the stigma. This in nature is not unseldom the case, as I have repeatedly found many flowers thus fertilised." He has, however, no doubt that the flowers are likewise cross-fertilised by nocturnal insects. He adds that D. grandiflora in being so seldom fertilised by insects offers a case like that of Ophrys muscifera; whilst D. macrantha in being often self-fertilised closely corresponds with Ophrys apifera; but this latter species seems to be invariably self-fertilised.

Lastly, Mr. Weale has described,[21] as far as he could make out, the manner in which a species of Disperis is fertilised by the aid of insects. It deserves notice that the labellum and two lateral sepals of this plant secrete nectar.

We have now finished with the Ophreæ; but before passing on to the following tribes, I will recapitulate the chief facts with respect to the movements of the pollinia, all due to the nicely regulated contraction of that small portion of membrane (together with the pedicel in the case of Habenaria) lying between the layer or ball of adhesive matter and the extremity of the caudicle. In a few cases, however, as with some of the species of Disa and Bonatea, the caudicles when removed from their cells do not undergo any movement ; the weight of the pollen-masses sufficing to depress them into a proper position. In most of the species of Orchis the stigma lies directly beneath the anther-cells, and the pollinia simply move vertically downwards. In Orchys pyramidalis there are two lateral and inferior stigmas, and the pollinia move downwards and outwards, diverging to the proper angle, so as to strike the two lateral stigmas. In Gymnadenia the pollinia move only downwards, but they are adapted for striking the lateral stigmas, by being attached to the upper lateral surfaces of the proboscides of Lepidoptera. In Nigritella they move upwards, but this depends merely on their being always affixed to the lower side of the proboscis. In Habenaria the stigmatic surface lies beneath and between the two widely-separated anther-cells, and the pollinia here converge, instead of diverging as in Orchis pyramidalis, and likewise move downwards. A poet might imagine that whilst the pollinia were borne through the air from flower to flower, adhering to an insect's body, they voluntarily and eagerly placed themselves in that exact position, in which alone they could hope to gain their wish and perpetuate their race.

  1. It is not correct to speak of two rostella, but the inaccuracy may be forgiven from its convenience. The rostellum strictly is a single organ, formed by the modification of the dorsal stigma and pistil; so that in Ophrys the two pouches, the two viscid discs, and the space between them together form the true rostellum. Again, in Orchis I have spoken of the pouch-formed organ as the rostellum, but strictly the rostellum includes the little crest or fold of membrane (see B in fig. 1) projecting, between the bases of the anther-cells. This folded crest (sometimes, converted into a solid ridge) corresponds with the smooth surface lying between the two pouches in Ophrys, and owes its protuberant and folded condition in Orchis to the two pouches having been brought together and rendered confluent. This modification will be more fully explained in a future chapter.
  2. 'Ult. Osserv. s. Dicogamia,' &c. Parte i. 1868–69, p. 177.
  3. 'Fecondazione nelle Piante Antocarpee,' 1867, p. 20.
  4. 'Journ. Linn. Soc.' vol. viii. 1865, p. 258.
  5. I once found a single flower on the summit of a spike, with the two rostella as completely and symmetrically confluent as in the genus Orchis, and with the two viscid discs likewise confluent, as in Orchis pyramidalis or hircina.
  6. 'Transact. Linn. Soc.' vol. xvi. p. 740. Brown erroneously believed that this peculiarity was common to the genus. As far as the four British species are concerned, it applies to this one alone.
  7. Mr. Gerard E. Smith, in his 'Catalogue of Plants of S. Kent,’ 1829, p. 25, says: "Mr. Price has frequently witnessed attacks made upon the Bee Orchis by a bee, similar to those of the troublesome Apis muscorum." What this sentence means I cannot conjecture.
  8. 'Bot. Zeitung,' 1863, p. 241. This botanist at first doubted my observations on Ophrys apifera and aranifera, but has since fully confirmed them.
  9. 'The Effects of Cross and Self-Fertilisation in the Vegetable Kingdom,' 1876.
  10. These forms are illustrated by beautiful coloured drawings in the 'Flora of Mentone,' pl. 43 to 45; and in his memoir in the 'Verhandlungen der Kaiserl. Leop. Car. Akad.' (Nov. Act.), tom. xxxv. 1869.
  11. 'Nature,' Dec. 31, 1874, p. 199.
  12. 'American Journal of Science,' vol, xxxiv. 1862, p. 426, and footnote p. 260; and vol. xxxvi. 1863, p. 293. In the latter paper he adds some remarks on 'G. flava and nivea.
  13. 'Nature,' Sept. 12, 1872, p. 393.
  14. According to Dr. H. Müller, Habenaria or Platanthera bifolia of English authors is the P. solstitialis of Boenninghausen; and he fully agrees with me that it must be ranked as specifically distinct from P. chlorantha. Dr. Müller states that this latter species is connected by a series of gradations with another form which in Germany is called P. bifolia. He gives a very full and interesting account of the variability of these three forms of Platanthera, and of their structure in relation to their manner of fertilisation: 'Verhandl. d. Nat. Verein. f. Pr. Rh. u. Westfal.' Jahrg. xxv. III. Folge, v. Bd. pp. 36–38.
  15. 'American Journal of Science,' vol. xxxiv. 1862, pp. 143, 250, and 424, and vol. xxxvi. 1863, p. 292.
  16. Mr. J. Mansel Weale has described ('Journ. Lin. Soc. Bot.' vol. xiii. 1871, p. 47) the method of fertilisation of two South African species of Habenaria: one of these is remarkable from the pollinia not undergoing any movement or change of position when removed from their cases.
  17. 'Journ. Linn. Soc. Bot.' vol. ix. 1865, p. 156.
  18. 'Journ. Linn. Soc. Bot.' vol. x. p. 470.
  19. 'Journ. Linn. Soc. Bot.' vol. vii. 1863, p. 144.
  20. 'Journ. Linn. Soc. Bot.' vol. xiii. 1871, p. 45.
  21. 'Journ. Linn. Soc. Bot.' vol. xiii. 1871, p. 42.