The Various Contrivances by which Orchids are Fertilised by Insects/Chapter 4

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Epipactis palustris; curious shape of the labellum and its importance in the fructification of the flower—other species of Epipactis—Epipogium—Goodyera repens—Spiranthes autumnalis; perfect adaptation by which the pollen of a younger flower is carried to the stigma of an older flower on another plant—Listera ovata; sensitiveness of the rostellum; explosion of viscid matter; action of insects; perfect adaptation of the several organs—Listera cordata—Neottia nidus-avis; its fertilisation effected in the same manner as in Listera—Thelymitra, self-fertile.

We have now arrived at a third tribe, the Neotteæ of Lindley, which includes several British genera. These present many interesting points with respect to their structure and manner of fertilisation.

The Neotteæ have a free anther standing behind the stigma. Their pollen-grains are tied together by fine elastic threads, which partially cohere and project at the upper end of the pollen-mass, being there attached (with some exceptions) to the back of the rostellum. Consequently the pollen-masses have no true and distinct caudicles. In one genus alone (Goodyera) the pollen-grains are collected into packets as in Orchis. Epipactis and Goodyera agree pretty closely in their manner of fertilisation with the Neotteæ, but are more simply organised. Spiranthes comes under the same category, but has been differently modified in some respects.

Epipactis palustris.[1]—The lower part of the large

Fig. 15.

Darwin - The various contrivances by which orchids are fertilized by insects (1877) - Fig 15.png

Epipactis palustris.

a. anther, with the two open cells seen in the front view D.
a′. rudimentary anther, or auricle, referred to in a future chapter.
r. rostellum.
s. stigma.
l. labellum.
A. Side view of flower, with the lower sepals removed, in its natural position.
B. Side view of flower, with the distal portion of the labellum depressed, as if by the weight of an insect.
C. Side view of flower, somewhat enlarged, with all the sepals and petals removed, excepting the labellum, of which the near side has been cut away; the massive anther is seen to be of large size.
D. Front view of column, somewhat enlarged, with all the sepals and petals removed: the rostellum has sunk down a little in the specimen figured, and ought to have stood higher, so as to hide more of the anther-cells.
stigma is bilobed and projects in front of the column (see s in the side and front views, C, D, fig. 15). On its square summit a single, nearly globular rostellum is seated. The anterior face of the rostellum (r, C, D) projects a little beyond the surface of the upper part of the stigma, and this is of importance. In the early bud the rostellum consists of a friable mass of cells, with the exterior surface rough: these superficial cells undergo a great change during development, and become converted into a soft, smooth, highly elastic membrane or tissue, so excessively tender that it can be penetrated by a human hair; when thus penetrated, or when slightly rubbed, the surface becomes milky and in some degree viscid, so that the pollen-grains adhere to it. In some cases, though I observed this more plainly in Epipactis latifolia, the surface of the rostellum apparently becomes milky and viscid without having been touched. This exterior soft elastic membrane forms a cap to the rostellum, and is internally lined with a layer of much more adhesive matter, which, when exposed to the air, dries in from five to ten minutes. By a slight upward and backward push with any object, the whole cap, with its viscid lining, is removed with the greatest ease; a minute square stump, the basis of the rostellum, being alone left on the summit of the stigma.

In the bud-state the anther stands quite free behind the rostellum and stigma; it opens longitudinally whilst the flower is still unexpanded, and exposes the two oval pollen-masses, which now lie loose in their cells. The pollen consists of spherical granules, cohering in fours, but not affecting each other's shapes: and these compound grains are tied together by fine elastic threads. The threads are collected into bundles extending longitudinally along the middle line of the front of each pollinium, where it comes into contact with the back of the uppermost part of the rostellum. From the number of these threads this middle line looks brown, and each pollen-mass here shows a tendency to divide longitudinally into halves. In all these respects there is a close general resemblance to the pollinia of the Ophreæ.

The line where the parallel threads are the most numerous is the line of greatest strength; elsewhere the pollen-masses are extremely friable, so that large portions can easily be broken off. In the bud-state the rostellum is curved a little backwards, and is pressed against the recently-opened anther; and the above-mentioned slightly projecting bundles of threads become firmly attached to the posterior flap of the membranous cap of the rostellum. The point of attachment lies a little beneath the summit of the pollen-masses; but the exact point is somewhat variable, for I have met with specimens in which the attachment was one-fifth of the length of the pollen-masses from their summits. This variability is so far interesting, as it is a step leading to the structure of the Ophreæ, in which the confluent threads, or caudicles, always spring from the lower ends of the pollen-masses. After the pollinia are firmly attached by their threads to the back of the rostellum, the rostellum bends a little forwards, and this partly draws the pollinia out of the anther-cells. The upper end of the anther consists of a blunt, solid point, not including pollen; this blunt point projects slightly beyond the face of the rostellum, which circumstance, as we shall see, is important.

The flowers stand out (fig. A) almost horiozontally from the stem. The labellum is curiously shaped, as may be seen in the drawings: the distal half, which projects beyond the other petals and forms an excellent landing-place for insects, is joined to the basal half by a narrow hinge, and naturally (fig. A) is turned a little upwards, so that its edges pass within the edges of the basal portion. So flexible and elastic is the hinge that the weight of even a fly, as Mr. More informs me, depresses the distal portion; it is represented in fig. B in this state; but when the weight is removed it instantly springs up to its former position (fig. A), and with its curious medial ridges partly closes the entrance into the flower. The basal portion of the labellum forms a cup, which at the proper time is filled with nectar.

Now let us see how all the parts, which I have been obliged to describe in detail, act. When I first examined these flowers I was much perplexed: trying in the same manner as I should have done with a true Orchis, I slightly pushed the protuberant rostellum downwards, and it was easily ruptured; some of the viscid matter was withdrawn, but the pollinia remained in their cells. Reflecting on the structure of the flower, it occurred to me that an insect in entering one in order to suck the nectar, would depress the distal portion of the labellum, and consequently would not touch the rostellum; but that, when within the flower, it would be almost compelled, from the springing up of this distal half of the labellum, to rise a little upwards and back out parallel to the stigma. I then brushed the rostellum lightly upwards and backwards with the end of a feather and other such objects; and it was pretty to see how easily the membranous cap of the rostellum came off, and how well from its elasticity it fitted any object, whatever its shape might be, and how firmly it clung to the object owing to the viscidity of its under surface. Large masses of pollen, adhering by the elastic threads to the cap of the rostellum were at the same time withdrawn.

Nevertheless the pollen-masses were not removed nearly so cleanly as those which had been naturally removed by insects. I tried dozens of flowers, always with the same imperfect result. It then occurred to me, that an insect in backing out of the flower would naturally push with some part of its body against the blunt and projecting upper end of the anther, which overhangs the stigmatic surface. Accordingly I so held a brush that, whilst brushing upwards against the rostellum, I pushed against the blunt solid end of the anther (see fig. C); this at once eased the pollinia, and they were withdrawn in an entire state. At last I understood the mechanism of the flower.

The large anther stands above and behind the stigma, forming an angle with it (fig. C), so that the pollinia when withdrawn by an insect would adhere to its head or body in a position fitted to strike the sloping stigmatic surface as soon as another flower was visited. Hence we have not here, or in any of the Neotteæ, that movement of depression so common with the pollinia of the Ophreæ. When an insect with the pollinia attached to its back or head enters another flower, the easy depression of the distal portion of the labellum probably plays an important part; for the pollen-masses are extremely friable, and if they were struck against the tips of the petals much of the pollen would be lost; but as it is, an open gangway is offered, and the viscid stigma, with its lower protuberant part lying in front, is the first object against which the pollen-masses projecting forwards from the insect's head or back would naturally strike. I may add that in one large lot of flower-spikes, a great majority of the pollinia had been naturally and cleanly removed.

In order to ascertain whether I was right in believing that the distal hinged portion of the labellum was of importance in the fertilisation of the flowers, I asked Mr. More to remove this part from some young flowers, and to mark them. He tried the experiment on eleven flowers, three of which did not produce seed-capsules; but this may have been accidental. Of the eight capsules which were produced, two contained about as many seeds as those from unmutilated flowers on the same plant; but six capsules contained much fewer seeds. Most of the seeds were well-formed. These experiments, as far as they go, support the view that the distal part of the labellum is of importance in causing insects to enter and leave the flowers in the best manner for their fertilisation.

Since the appearance of the first edition of this book, my son William has observed for me this Epipactis in the Isle of Wight. Hive-bees seem to be the chief agents in fertilisation; for he saw them visit about a score of flowers, and many had pollen-masses attached to their foreheads, just above the mandibles. I had supposed that insects always crawled into the flowers; but hive-bees are too large to do this; they always clung, whilst sucking the nectar, to the distal and hinged half of the labellum, which was thus pressed downwards. Owing to this part being elastic and tending to spring up, the bees, as they left the flowers, seemed to fly rather upwards; and this favoured, in the manner previously explained, the complete withdrawal of the pollen-masses, quite as well as if the insects had crawled, in an upward direction, out of the flower. Perhaps the upward movement may not be so necessary in all cases as I had supposed; for, judging from the manner in which the pollen-masses were attached to the hive-bees, the back part of their heads could hardly fail to press against and lift up the blunt, solid, upper end of the anther, thus freeing the pollen-masses. Various other insects besides hive-bees visit the flowers. My son saw several large flies (Sarcophaga carnosa) haunting them; but they did not enter in so neat and regular a manner as the hive-bees; nevertheless two had pollen-masses attached to their foreheads. Several smaller flies (Cœlopa frigida) were also seen entering and leaving the flowers, with pollen-masses adhering rather irregularly to the dorsal surface of the thorax. Three or four distinct kinds of Hymenoptera (one of small size being Crabro brevis) likewise visited the flowers; and three of these Hymenoptera had pollen-masses attached to their backs. Other still more minute Diptera, Coleoptera, and ants were seen sucking the nectar; but these insects appeared to be too small to transport the pollen-masses. It is remarkable that some of the foregoing insects should visit the flowers; for Mr. F. Walker informs me that the Sarcophaga frequents decaying animal matter, and the Cœlopa haunts seaweed, occasionally settling on flowers. The Crabro also, as I hear from Mr. F. Smith, collects small beetles (Haticæ) for provisioning its nest. It is equally remarkable, seeing how many kinds of insects visit this Epipactis, that although my son watched hundreds of plants for some hours on three occasions, not a single humble-bee alighted on a flower, though many were flying about.

Epipactis latifolia.—This species agrees with the last in most respects. The rostellum, however, projects considerably further beyond the face of the stigma, and the blunt upper end of the anther less so. The viscid matter lining the elastic cap of the rostellum takes a longer time to get dry. The upper petals and sepals are more widely expanded than in E. palustris: the distal portion of the labellum is smaller, and is firmly united to the basal portion (fig. 16), so that it is not flexible and elastic; it apparently serves only as a landing-place for insects. The fertilisation of this species depends simply on an insect striking in an upward and backward direction the highly-protuberant rostellum, which it would be apt to do when retreating from the flower after having sucked the copious nectar

Fig. 16.

Darwin - The various contrivances by which orchids are fertilized by insects (1877) - Fig 16.png

Epipactis latifolia.

Flower viewed sideways, with all the sepals and petals removed, except the labellum.

a. anther. s. stigma.
r. rostellum. l. labellum

in the cup of the labellum. Apparently it is not at all necessary that the insect should push upwards the blunt upper end of the anther; at least I found that the pollinia could be removed easily by simply dragging off the cap of the rostellum in an upward or backward direction.

As some plants grew close to my house, I have been able to observe here and elsewhere their manner of fertilisation during several years. Although hive-bees and humble-bees of many kinds were constantly flying over the plants, I never saw a bee or any Dipterous insect visit the flowers; but in Germany Sprengel caught a fly with the pollinia of this plant attached to its back. On the other hand I have repeatedly observed the common wasp (Vespa sylvestris) sucking the nectar out of the open cup-shaped labellum. I thus saw the act of fertilisation effected by the pollen-masses being removed by the wasps, and afterwards carried attached to their foreheads to other flowers. Mr. Oxenden also informs me that a large bed of E. purpurata (which is considered by some botanists to be a distinct species, and by others a variety) was frequented by "swarms of wasps." It is very remarkable that the sweet nectar of this Epipactis should not be attractive to any kind of bee. If wasps were to become extinct in any district, so probably would the Epipactis latifolia.

To show how effectually the flowers are fertilised, I may add that during the wet and cold season of 1860 a friend in Sussex examined five spikes bearing eighty-five expanded flowers; of these, fifty-three had the pollinia removed, and thirty-two had them in place: but as many of the latter were immediately beneath the buds, a larger number would almost certainly have been afterwards remowed. In Devonshire I found a spike with nine open flowers, and the pollinia in all were removed with one exception, and in this case a fly, too small to remove the pollinia, had become glued to the rostellum, and had there miserably perished.

Dr. H. Müller has published[2] some interesting observations on the difference in structure and manner of fertilisation, as well as on the intermediate forms between Epipactis rubiginosa, microphylla, and viridiflora. The latter species is remarkable for the absence of a rostellum, and for being regularly self-fertilised. Self-fertilisation here follows from the incoherent pollen-grains in the lower part of the pollen-masses emitting, whilst still within the anther-cells, their tubes, which penetrate the stigma; and this occurs even in the bud. This species, however, is probably visited by insects, and occasionally crossed; for the labellum contains nectar. E. microphylla is intermediate in structure between E. latifolia, which is always fertilised by the aid of insects, and E. viridiflora, which does not necessarily require any such aid. The whole of this memoir by Dr. H. Müller deserves to be attentively studied.

Epipogium gmelini.—This plant, which has only once been found in Great Britain, has been fully described by Dr. Rohrbach in a special memoir.[3] The structure and manner of fertilisation is in many respects like that of Epipactis, to which genus the author believes the present one to be allied, though placed by Lindley amongst the Arethuseæ. Rohrbach saw the flowers visited by Bomhus lucorum, but it appears that only a few produce capsules.

Goodyera repens.[4]—This genus is rather closely related to Epipactis, in most of the characters with which we are concerned. The shield-like rostellum is almost square, and projects beyond the stigma; it is supported on each side by sloping sides rising from the upper edge of the stigma, in nearly the same manner as we shall presently see in Spiranthes. The surface of the protuberant part of the rostellum is rough, and when dry can be seen to be formed of cells; it is delicate, and, when slightly pricked, a little milky viscid fluid exudes; it is lined by a layer of very adhesive matter, which quickly sets hard when exposed to the air. The protuberant surface of the rostellum, when gently rubbed upwards, is easily removed, and carries with it a strip of membrane, to the hinder part of which the pollinia are attached. The sloping sides which support the rostellum are not removed at the same time, but remain projecting up like a fork and soon wither. The anther is borne on a broad elongated filament; and a membrane on both sides unites this filament to the edges of the stigma, forming an imperfect cup or clinandrum. The anther-cells open in the bud, and the pollen-masses become attached by their anterior faces, just beneath their summits, to the back of the rostellum. Ultimately the anther opens widely, leaving the pollinia almost naked, but partially protected within the membranous cup or clinandrum. Each pollinium is partially divided lengthways; the pollen-grains cohere in subtriangular packets, including a multitude of compound grains, each consisting of four grains; and these packets are tied together by strong elastic threads, which at their upper ends run together and form a single flattened brown elastic ribbon, of which the truncated extremity adheres to the back of the rostellum.

The surface of the orbicular stigma is remarkably viscid, which is necessary in order that the unusually strong threads connecting the packets of pollen should be ruptured. The labellum is partially divided into two portions; the terminal portion is reflexed, and the basal portion is cup-formed and filled with nectar. The passage between the rostellum and labellum is contracted whilst the flower is young; but when mature the column moves further back from the labellum, so as to allow of insects with the pollinia adhering to their proboscides, to enter the flowers more freely. In many of the specimens received, the pollinia had been removed, and the fork-shaped supporting sides of the rostellum were partially withered. Mr. R. B. Thomson informs me that in the north of Scotland he saw many humble-bees (Bombus pratorum) visiting the flowers with pollen-masses attached to their proboscides. This species grows also in the United States; and Professor Asa Gray[5] confirms my account of its structure and manner of fertilisation, which is likewise applicable to another and very distinct species, namely, Goodyera pubescens.

Goodyera is an interesting connecting link between several very distinct forms. In no other member of the Neotteæ observed by me is there so near an approach to the formation of a true caudicle;[6] and it is curious that in this genus alone the pollen-grains cohere in large packets, as in the Ophreæ. If the nascent caudicles had been attached to the lower ends of the pollinia, and they are attached a little beneath their summits, the pollinia would have been almost identical with those of a true Orchis. In the rostellum being supported by sloping sides, which wither when the viscid disc is removed,—in the existence of a membranous cup or clinandrum between the stigma and anther,—and in some other respects, we have a clear affinity with Spiranthes. In the anther having a broad filament we see a relation to Cephalanthera. In the structure of the rostellum, with the exception of the sloping sides, and in the shape of the labellum, Goodyera resembles Epipactis. Goodyera probably shows us the state of the organs in a group of Orchids, now mostly extinct, but the parents of many living descendants.

Spiranthes autumnalis.—This Orchid with its pretty name of Ladies'-tresses, presents some interesting peculiarities.[7] The rostellum is a long, thin, flat projection, joined by sloping shoulders to the summit of the stigma. In the middle of the rostellum a narrow vertical brown object (fig. 17, C) may be seen, bordered and covered by transparent membrane. This brown object I will call "the boat-formed disc." It forms the middle portion of the posterior surface of the rostellum, and consists of a narrow strip of the exterior membrane in a modified condition. When removed from its attachment, its summit (fig. E) is seen to be pointed, with the lower end rounded; it is slightly bowed, so as altogether to resemble a boat or canoe. It is rather more than 4/100 of an inch in length, and less than 1/100 in breadth. It is nearly rigid, and appears fibrous, but is really formed of elongated and thickened cells, partially confluent.

This boat, standing vertically up on its stern, is filled with thick, milky, extremely adhesive fluid, which, when exposed to the air, rapidly turns brown, and in about one minute sets quite hard. An object is well glued to the boat in four or five seconds, and when the cement is dry the attachment is wonderfully strong. The transparent sides of the rostellum consist of membrane, attached behind to the edges of the boat, and folded over in front, so as to form the anterior face of the rostellum. This folded membrane, therefore, covers, almost like a deck, the cargo of viscid matter within the boat.

Fig. 17.

Darwin - The various contrivances by which orchids are fertilized by insects (1877) - Fig 17.png

Spiranthes automnalis, or Ladies'-Tresses.

a. anther.
p. pollen-masses.
t. threads of the pollen-masses.
cl. margin of clinandrum,
r. rostellum.
s. stigma.
n. nectar receptacle.
A. Side view of flower in its natural position, with the two lower sepals alone removed. The labellum can be recognised by its fringed and reflexed lip.
B. Side view enlarged of a mature flower, with all the sepals and petals removed. The positions of the labellum and of the upper sepal are shown by the dotted lines.
C. Front view of the stigma, and of the rostellum with its embedded, central, boat-formed disc.
D. Front view of the stigma and of the rostellum after the disc has been removed.
E. Disc, removed from the rostellum, greatly enlarged, viewed posteriorly, with the attached elastic threads of the pollen-masses; the pollen-grains have been removed from the threads.

The anterior face of the rostellum is slightly furrowed in a longitudinal line over the middle of the boat, and is endowed with a remarkable kind of irritability; for, if the furrow be touched very gently by a needle, or if a bristle be laid along the furrow, it instantly splits along its whole length, and a little milky adhesive fluid exudes. This action is not mechanical, or due to simple violence. The fissure runs up the whole length of the rostellum, from the stigma beneath to the summit: at the summit the fissure bifurcates, and runs down the back of the rostellum on each side and round the stern of the boat-formed disc. Hence after this splitting action the boat-formed disc lies quite free, but embedded in a fork in the rostellum. The act of splitting apparently never takes place spontaneously. I covered a plant with a net, and after five of the flowers had fully expanded they were kept protected for a week: I then examined their rostella, and not one had split; whereas almost every flower on the surrounding and uncovered spikes, which would almost certainly have been visited and touched by insects, had their rostella fissured, though they had been open for only twenty-four hours. Exposure for two minutes to the vapour of a little chloroform causes the rostellum to split; and this we shall hereafter see is likewise the case with some other Orchids.

When a bristle is laid for two or three seconds in the furrow of the rostellum, and the membrane has consequently become fissured, the viscid matter within the boat-formed disc, which lies close to the surface and indeed slightly exudes, is almost sure to glue the disc longitudinally to the bristle, and both are withdrawn together. When the disc, with the pollinia attached to it, is withdrawn, the two sides of the rostellum (fig. D), which have been described by some botanists as two distinct foliaceous projections, are left sticking up like a fork. This is the common condition of the flowers after they have been open for a day or two, and have been visited by insects. The fork soon withers.

Whilst the flower is in bud, the back of the boat-formed disc is covered with a layer of large rounded cells, so that the disc does not strictly form the exterior surface of the back of the rostellum. These cells contain slightly viscid matter: they remain unaltered (as may be seen at fig. E) towards the upper end of the disc, but at the point where the pollinia are attached they disappear. Therefore I at one time concluded that the viscid matter contained in these cells, when they burst, serve to fasten the threads of the pollinia to the disc; but, as in several other genera, in which a similar attachment has to be effected, I could see no trace of such cells, this view may be erroneous.

The stigma lies beneath the rostellum, and projects with a sloping surface, as may be seen at B in the side-view: its lower margin is rounded and fringed with hairs. On each side a membrane (cl, B) extends from the edges of the stigma to the filament of the anther, thus forming a membranous cup or clinandrum, in which the lower ends of the pollen-masses lie safely protected.

Each pollinium consists of two leaves of pollen, quite disconnected at their lower and upper ends, but united for about half their length in the middle by elastic threads. A very slight modification would convert the two pollinia into four distinct masses, as occurs in the genus Malaxis and in many foreign Orchids. Each leaf consists of a double layer of pollen-grains, joined by fours together, and these united by elastic threads, which are more numerous along the edges of the leaves, and converge at the summit of the pollinium. The leaves are very brittle, and, when placed on the adhesive stigma, large pieces are easily broken off.

Long before the flower expands, the anther-cells, which are pressed against the back of the rostellum, open in their upper part, so that the included pollinia come into contact with the back of the boat-formed disc. The projecting threads then become firmly attached to rather above the middle part of the back of the disc. The anther-cells afterwards open lower down, and their membranous walls contract and become brown; so that by the time the flower is fully expanded the upper part of the pollinia lie quite naked, with their bases resting in a little cup formed by the withered anther-cell, and laterally protected by the clinandrum. As the pollinia thus lie loose, they are easily removed.

The tubular flowers are elegantly arranged in a spire round the spike, and project from it horizontally (fig. A). The labellum is channelled down the middle, and is furnished with a reflexed and fringed lip, on which bees alight; its basal internal angles are produced into two globular processes, which secrete an abundance of nectar. The nectar is collected (n, fig. B) in a small receptacle in the lower part of the labellum. Owing to the protuberance of the inferior margin of the stigma and of the two lateral inflexed nectaries, the orifice into the nectar-receptacle is much contracted. When the flower first opens the receptacle contains nectar, and at this period the front of the rostellum, which is slightly furrowed, lies close to the channelled labellum; consequently a passage is left, but so narrow that only a fine bristle can be passed down it. In a day or two the column moves a little farther from the labellum, and a wider passage is left for insects to deposit pollen on the stigmatic surface. On this slight movement of the column the fertilisation of the flower absolutely depends.[8]

With most Orchids the flowers remain open for some time before they are visited by insects; but with Spiranthes I have generally found the boat-formed discs removed very soon after their expansion. For example, in the two last spikes which I happened to examine there were numerous buds on the summit of one, with only the seven lowest flowers expanded, of which six had their discs and pollinia removed; the other spike had eight expanded flowers, and the pollinia of all were removed. We have seen that when the flowers first open they would be attractive to insects, for the receptacle already contains nectar; and at this period the rostellum lies so close to the channelled labellum that a bee could not pass down its proboscis without touching the medial furrow of the rostellum. This I know to be the case by repeated trials with a bristle.

We thus see how beautifully everything is contrived, that the pollinia should be withdrawn by insects visiting the flowers. They are already attached to the disc by their threads, and, from the early withering of the anther-cells, they hang loosely suspended but protected within the clinandrum. The touch of the proboscis causes the rostellum to split in front and behind, and frees the long, narrow, boat-formed disc, which is filled with extremely viscid matter, and is sure to adhere longitudinally to the proboscis. When the bee flies away, so surely will it carry away the pollinia. As the pollinia are attached parallel to the disc, they adhere parallel to the proboscis. When the flower first opens and is best adapted for the removal of the pollinia, the labellum lies so close to the rostellum, that the pollinia attached to the proboscis of an insect cannot possibly be forced into the passage so as to reach the stigma; they would be either upturned or broken off: but we have seen that after two or three days the column becomes more reflexed and moves from the labellum,—a wider passage being thus left. When I inserted the pollinia attached to a fine bristle into the nectar-receptacle of a flower in this condition (n, fig. B), it was pretty to see how surely the sheets of pollen were left adhering to the viscid stigma. It may be observed in the diagram, B, that owing to the projection of the stigma, the orifice into the nectar-receptacle (n) lies close to the lower side of the flower; insects would therefore insert their proboscides along this lower side, and an open space above is thus left for the attached pollinia to be carried down to the stigma, without being brushed off. The stigma evidently projects so that the ends of the pollinia may strike against it.

Hence, in Spiranthes, a recently expanded flower, which has its pollinia in the best state for removal, cannot be fertilised; and mature flowers will be fertilised by pollen from younger flowers, borne, as we shall presently see, on a separate plant. In conformity with this fact the stigmatic surfaces of the older flowers are far more viscid than those of the younger flowers. Nevertheless, a flower which in its early state had not been visited by insects would not necessarily, in its later and more expanded condition, have its pollen wasted; for insects, in inserting and withdrawing their proboscides, bow them forwards or upwards, and would thus often strike the furrow in the rostellum. I imitated this action with a bristle, and often succeeded in withdrawing the pollinia from old flowers. I was led to make this trial from having at first chosen old flowers for examination; and on passing a bristle, or fine culm of grass, straight down into the nectary, the pollinia were never withdrawn; but when it was bowed forward, I succeeded. Flowers which have not had their pollinia removed can be fertilised as easily as those which have lost them; and I have seen not a few cases of flowers with their pollinia still in place, with sheets of pollen on their stigmas.

At Torquay I watched for about half an hour a number of these flowers growing together, and saw three humble-bees of two kinds visit them. I caught one and examined its proboscis: on the superior lamina, some little way from the tip, two perfect pollinia were attached, and three other boat-formed discs without pollen; so that this bee had removed the pollinia from five flowers, and had probably left the pollen of three on the stigmas of other flowers. The next day I watched the same flowers for a quarter of an hour, and caught another humble-bee at work; one perfect pollinium and four boat-formed discs adhered to its proboscis, one on the top of the other, showing how exactly the same part of the rostellum had each time been touched.

The bees always alighted at the bottom of the spike, and, crawling spirally up it, sucked one flower after the other. I believe humble-bees generally act in this manner when visiting a dense spike of flowers, as it is the most convenient method; on the same principle that a woodpecker always climbs up a tree in search of insects. This seems an insignificant observation; but see the result. In the early morning, when the bee starts on her rounds, let us suppose that she alighted on the summit of a spike; she would certainly extract the pollinia from the uppermost and last opened flowers; but when visiting the next succeeding flower, of which the column in all probability would not as yet have moved from the labellum (for this is slowly and very gradually effected), the pollen-masses would be brushed off her proboscis and wasted. But nature suffers no such waste. The bee goes first to the lowest flower, and, crawling spirally up the spike, effects nothing on the first spike which she visits till she reaches the upper flowers, and then she withdraws the pollinia. She soon flies to another plant, and, alighting on the lowest and oldest flower, into which a wide passage will have been formed from the greater reflexion of the column, the pollinia strike the protuberant stigma. If the stigma of the lowest flower has already been fully fertilised, little or no pollen will be left on its dried surface; but on the next succeeding flower, of which the stigma is adhesive, large sheets of pollen will be left. Then as soon as the bee arrives near the summit of the spike she will withdraw fresh pollinia, will fly to the lower flowers on another plant, and fertilise them; and thus, as she goes her rounds and adds to her store of honey, she continually fertilises fresh flowers and perpetuates the race of our autumnal Spiranthes, which will yield honey to future generations of bees.

Spiranthes australis.—This species, an inhabitant of Australia, has been described and figured by Mr. Fitzgerald.[9] The flowers are arranged on the spike in the same manner as in S. autumnalis; and the labellum with two glands at its base closely resembles that of our species. It is therefore an extraordinary fact that Mr. Fitzgerald could not detect even in the bud any trace of a rostellum or of viscid matter. He states that the pollinia touch the upper edge of the stigma, and fertilise it at an early age. Protecting a plant from the access of insects by a bell-glass made no difference in its fertility; and Mr. Fitzgerald, though he examined many flowers, never noticed the slightest derangement of the pollinia, or any pollen on the surfaces of the stigmas. Here then we have a species which fertilises itself as regularly as does Ophrys apifera. It would, however, be desirable to ascertain whether insects ever visit the flowers, which it may be presumed secrete nectar, as glands are present; and any such insects should be examined, so as to make certain that pollen does not adhere to some part of their bodies.

Listera ovata, or Tway-blade.—This Orchid is one of the most remarkable in the whole order. The structure and action of the rostellum has been the subject of a valuable paper in the 'Philosophical Transactions,' by Dr. Hooker,[10] who has described minutely and of course correctly its curious structure; he did not, however, attend to the part which insects play in the fertilisation of the flowers. C. K Sprengel well knew the importance of insect-agency, but he misunderstood both the structure and the action of the rostellum.

The rostellum is of large size, thin, or foliaceous, convex in front and concave behind, with its sharp summit slightly hollowed out on each side; it arches over the stigmatic surface (fig. 18, A, r, s). Internally,

Fig. 18.

Darwin - The various contrivances by which orchids are fertilized by insects (1877) - Fig 18.png

Listera ovata, or Tway-blade. (Partly copied from Hooker.)

col. summit of column.
a. anther.
p. pollen.
r. rostellum.
s. stigma.
l. labellum.
n. nectar-secreting furrow.
A.Flower viewed laterally, with all the sepals and petals, except the labellum, removed.
B.Ditto, with the pollinia removed, and with the rostellum bent down after the ejection of the viscid matter.

it is divided by longitudinal septa into a series of loculi, which contain viscid matter and have the power of violently expelling it. These loculi show traces of their original cellular structure. I have met with this structure in no other genus except in the closely allied Neottia. The anther, situated behind the rostellum and protected by a broad expansion of the top of the column, opens in the bud. When the flower is fully expanded, the pollinia are left quite free, supported behind by the anther-cells, and lying in front against the concave back of the rostellum, with their upper pointed ends resting on its crest. Each pollinium is almost divided into two masses. The pollen-grains are attached together in the usual manner by a few elastic threads; but the threads are weak, and large masses of pollen can be broken off easily. After the flower has long remained open, the pollen becomes more friable. The labellum is much elongated, contracted at its base, and bent downwards, as represented in the drawing; the upper half above the bifurcation is furrowed along the middle; and the borders of this furrow secrete much nectar.

As soon as the flower opens, if the crest of the rostellum be touched ever so lightly, a large drop of viscid fluid is instantaneously expelled; and this, as Dr. Hooker has shown, is formed by the coalescence of two drops proceeding from two depressed spaces on each side of the centre. A good proof of this fact was afforded by some specimens kept in weak spirits of wine, which apparently had expelled the viscid matter slowly, and here two separate little spherical balls of hardened matter had been formed, attached to the two pollinia. The fluid is at first slightly opaque and milky; but on exposure to the air for less than a second, a film forms over it, and in two or three seconds the whole drop sets hard, soon assuming a purplish-brown tint. So exquisitely sensitive is the rostellum, that a touch from the thinnest human hair suffices to cause the explosion. It will take place under water. Exposure to the vapour of chloroform for about one minute also caused an explosion; but the vapour of sulphuric ether did not thus act, though one flower was exposed for five, and another for twenty minutes to a strong dose. The rostellum of these two flowers when afterwards touched exploded in the usual manner, so that sensitiveness had not been lost in either case. The viscid fluid when pressed between two plates of glass before it has set hard is seen to be structureless; but it has a reticulated appearance, perhaps caused by the presence of globules of a denser immersed in a thinner fluid. As the pointed tips of the pollinia lie on the crest of the rostellum, they are always caught by the exploded drop: I have never seen this once to fail. So rapid is the explosion and so viscid the fluid, that it is difficult to touch the rostellum with a needle, however quickly this may be done, without removing the pollinia. Hence, if a bunch of flowers be carried home in the hand, some of the sepals or petals will almost certainly touch the rostellum and withdraw the pollinia; and this gives the false appearance of their having been ejected to a distance.

After the anther-cells have opened and the naked pollinia have been left resting on the concave back of the rostellum, this latter organ curves a little forwards, and perhaps the anther also moves a little backwards. This movement is of much importance; if it did not occur, the tip of the anther, within which the pollinia are lodged, would be caught by the exploded viscid matter, and the pollinia would be for ever locked up and rendered useless. I once found an injured flower which had been pressed and had exploded before fully expanding, and the anther with the enclosed pollen-masses was permanently glued to the crest of the rostellum. The rostellum, which is naturally somewhat arched over the stigma, quickly bends forwards and downwards at the moment of the explosion, so as then to stand (fig. B) at right angles to the surface of the stigma. The pollinia, if not removed by the touching object which causes the explosion, become fixed to the rostellum, and by its movement are likewise drawn a little forward. If their lower ends are now freed by a needle from the anther-cells, they spring up; but they are not by this movement placed on the stigma. In the course of some hours, or of a day, the rostellum not only slowly recovers its original slightly-arched position, but becomes quite straight and parallel to the stigmatic surface. This backward movement of the rostellum is of service; for if after the explosion it had remained permanently projecting at right angles over the stigma, pollen could not readily have been deposited by insects on the viscid surface of the stigma. When the rostellum is touched so quickly that the pollinia are not removed, they are, as I have just said, drawn a little forward; but by the subsequent backward movement of the rostellum they are pushed back again into their original position.

From the account now given we may safely infer how the fertilisation of this Orchid is effected. Small insects alight on the labellum for the sake of the nectar copiously secreted by it; as they lick this they slowly crawl up its narrowed surface until their heads stand directly beneath the overarching crest of the rostellum; when they raise their heads they touch the crest; this then explodes, and the pollinia are instantly and firmly cemented to their heads. As soon as the insect flies away, it withdraws the pollinia, carries them to another flower, and there leaves masses of the friable pollen on the adhesive stigma.

In order to witness what I felt sure would take place, I watched for an hour a group of plants on three occasions; each time I saw numerous specimens of two small Hymenopterous insects, namely, a Hæmiteles and a Cryptus, flying about the plants and licking up the nectar; most of the flowers, which were visited over and over again, already had their pollinia removed, but at last I saw both these species crawl into younger flowers, and suddenly retreat with a pair of bright yellow pollinia sticking to their foreheads; I caught them, and found the point of attachment was to the inner edge of the eye; on the other eye of one specimen there was a ball of the hardened viscid matter, showing that it had previously removed another pair of pollinia, and in all probability had subsequently left them on the stigma of a flower. As these insects were captured, I did not witness the act of fertilisation; but Sprengel saw a Hymenopterous insect leave its pollen-mass on the stigma. My son watched another bed of this Orchid at some miles' distance, and brought me home the same Hymenopterous insects with attached pollinia, and he saw Diptera also visiting the flowers. He was struck with the number of spider-webs spread over these plants, as if the spiders were aware how attractive the Listera was to insects.

To show how delicate a touch suffices to cause the rostellum to explode, I may mention that I found an extremely minute Hymenopterous insect vainly struggling to escape, with its head cemented by the hardened viscid matter, to the crest of the rostellum and to the tips of the pollinia. The insect was not so large as one of the pollinia, and after causing the explosion had not strength enough to remove them; it was thus punished for attempting a work beyond its strength, and perished miserably.

In Spiranthes the young flowers, which have their pollinia in the best state for removal, cannot possibly be fertilised; they must remain in a virgin condition until they are a little older and the column has moved away from the labellum. Here the same end is gained by widely different means. The stigmas of the older flowers are more adhesive than those of the younger flowers. These latter have their pollinia ready for removal; but immediately after the rostellum has exploded, it curls forwards and downwards, thus protecting the stigma for a time; but it slowly becomes straight again, and now the mature stigma is left freely exposed, ready to be fertilised.

I wished to know whether the rostellum would explode, if never touched; but I have found it difficult to ascertain this point, as the flowers are highly attractive to insects, and it is scarcely possible to exclude very minute ones, the touch of which suffices to cause the explosion. Several plants were covered by a net and left till the surrounding plants had set their capsules; and the rostella in most of the covered-up flowers were found not to have exploded, though their stigmas were withered, and the pollen mouldy and incapable of removal. Some few of the very old flowers, however, when roughly touched, were still capable of a feeble explosion. Other flowers under the nets had exploded, and they had the tips of their pollinia fixed to the crest of the rostellum; but whether these had been touched by some minute insect, or had exploded spontaneously, it was impossible to determine. It should be observed, that although I looked carefully, not a grain of pollen could be found on the stigmas of any of these flowers, and their ovaria had not swollen. During a subsequent year, several plants were again covered by a net, and I found that the rostellum lost its power of explosion in about four days; the viscid matter having turned brown within the loculi of the rostellum. The weather at the time was unusually hot, and this probably hastened the process. After the four days the pollen had become very incoherent, and some had fallen on the two corners, and even over the whole surface of the stigma, which was penetrated by the pollen-tubes. But the scattering of the pollen was largely aided by, and perhaps wholly depended on, the presence of Thrips—insects so minute that they could not be excluded by any net, and which abounded on the flowers. This plant, therefore, is capable of occasional self-fertilisation, if the access of winged insects be prevented; but I have every reason to believe that this occurs very rarely in a state of nature.

That insects do their work of cross-fertilisation effectually is shown by the following cases. The seven upper flowers on a young spike with many unexpanded buds, still retained their pollinia, but these had been removed from the ten lower flowers; and there was pollen on the stigmas of six of them. In two spikes taken together, the twenty-seven lower flowers all had their pollinia removed, and had pollen on their stigmas; these were succeeded by five open flowers with the pollinia not removed and without any pollen on the stigmas; and these were succeeded by eighteen buds. Lastly, in an older spike with forty-four fully expanded flowers, the pollinia had been removed from every single one; and there was pollen, generally in large quantity, on all the stigmas which I examined.

I will recapitulate the several special adaptations for the fertilisation of this plant. The anther-cells open early, leaving the pollen-masses free, protected by the summit of the column, and with their tips resting on the concave crest of the rostellum. The rostellum then slowly curves over the stigmatic surface, so that its explosive crest stands at a little distance from the summit of the anther; and this is very necessary, otherwise the summit would be caught by the viscid matter, and the pollen for ever locked up. The curvature of the rostellum over the stigma and over the base of the labellum is excellently adapted to favour an insect striking the crest when it raises its head, after having crawled up the labellum and licked the last drop of nectar. The labellum, as C. K. Sprengel has remarked, becomes narrower where it joins the column beneath the rostellum, so that there is no risk of an insect going too much to either side. The crest of the rostellum is so exquisitely sensitive, that a touch from a very minute insect causes it to rupture at two points, and instantly two drops of viscid fluid are expelled, which coalesce. This viscid fluid sets hard in so wonderfully rapid a manner that it rarely fails to cement the tips of the pollinia, nicely laid on the crest of the rostellum, to the forehead of the touching insect. As soon as the rostellum has exploded it suddenly curves downwards so as to project at right angles over the stigma, protecting it from impregnation at an early age, in the same manner as the stigmas of the young flowers of Spiranthes are protected by the labellum clasping the column. But as the column of Spiranthes after a time moves from the labellum, leaving a free passage for the introduction of the pollinia, so here the rostellum moves backwards, and not only recovers its former arched position, but stands upright, leaving the stigmatic surface, now rendered more adhesive, perfectly free for pollen to be left on it. The pollen-masses, when once cemented to an insect's forehead, will remain attached to it, until they are brought into contact with the stigma of a mature flower; and then these encumbrances will be removed, by the rupturing of the weak elastic threads which tie the grains together; the flower being at the same time fertilised.

Listera cordata.—Professor Dickie of Aberdeen was so kind as to send me, but rather too late in the season, two sets of specimens. The flowers have essentially the same structure as in the last species. The loculi of the rostellum are very distinct. Two or three little hairy points project from the middle of the crest of the rostellum; but I do not know whether these have any functional importance. The labellum has two basal lobes (of which vestiges may be seen in L. ovata) which curve up on each side; and these would compel an insect to approach the rostellum straight in front. In two of the flowers the pollinia were firmly cemented to the crest of the rostellum; but in almost all the others the pollinia had been previously removed by insects.

In the following year Professor Dickie observed the flowers on living plants, and he informs me that, when the pollen is mature, the crest of the rostellum is directed towards the labellum, and that, as soon as touched, the viscid matter explodes, the pollinia becoming attached to the touching object; after the explosion, the rostellum bends downwards, thus protecting the virgin stigmatic surface; subsequently it rises up and exposes the stigma; so that here everything goes on as I have described under Listera ovata. The flowers are frequented by minute Diptera and Hymenoptera.

Neottia nidus-avis.—I made numerous observations on this plant, the Bird's-nest Orchis,[11] but they are not worth giving, as the action and structure of every part is almost identically the same as in Listera ovata and cordata. On the crest of the rostellum there are about six minute rough points, which seem particularly sensitive to a touch, causing the expulsion of the viscid matter. The exposure of the rostellum to the vapour of sulphuric ether for twenty minutes did not prevent this action, when it was touched. The labellum secretes plenty of nectar, which I mention merely as a caution, because during one cold and wet season I looked several times and could not see a drop, and was perplexed at the apparent absence of any attraction for insects; nevertheless, had I looked more perseveringly, perhaps I should have found some.

The flowers must be freely visited by insects, for all in one large spike had their pollinia removed. Another unusually fine spike, sent me by Mr. Oxenden from South Kent, had borne forty-one flowers, and it produced twenty-seven large seed-capsules, besides some smaller ones. Dr. H. Müller of Lippstadt informs me that he has seen Diptera sucking the nectar and removing the pollinia.

The pollen-masses resemble those of Listera, in consisting of compound grains tied together by a few weak threads; they differ in being much more incoherent; after a few days they swell and overhang the sides and summit of the rostellum; so that if the rostellum of a rather old flower be touched and an explosion caused, the pollen-masses are not so neatly caught by their tips as those of Listera. Thus a good deal of the friable pollen is often left behind in the anther-cells and is apparently wasted. Several plants were protected from the access of winged insects by a net, and after four days the rostella had almost lost their sensitiveness and power to explode. The pollen had become extremely incoherent, and in all the flowers much had fallen on the stigmas which were penetrated by the pollen-tubes. The spreading of the pollen seems to be in part caused by the presence of Thrips, many of which minute insects were crawling about the flowers, dusted all over with pollen. The covered-up plants produced plenty of capsules, but many of these were much smaller and contained fewer seeds than those produced by the adjoining uncovered plants.

If insects had been forced by the labellum being more upturned to brush against the anther and stigma, they would always have been smeared with the pollen as soon as it became friable; and they would thus have fertilised the flowers effectually without the aid of the explosive rostellum. This conclusion interested me, because, when previously examining Cephalanthera, with its aborted rostellum, its upturned labellum and friable pollen, I had speculated how a transition, with each gradation useful to the plant, could have been effected from the state of the pollen in the similarly constructed flowers of Epipactis, with their pollinia attached to a well-developed rostellum, to the present condition of Cephalanthera. Neottia nidus-avis shows us how such a transition might have been effected. This Orchid is at present mainly fertilised by means of the explosive rostellum, which acts effectually only as long as the pollen remains in mass; but we have seen that as the flower grows old the pollen swells and becomes friable, and is then apt to fall or be transported by minute crawling insects on to the stigma. By this means self-fertilisation is assured, should larger insects fail to visit the flowers. Moreover, the pollen in this state readily adheres to any object; so that by a slight change in the shape of the flower, which is already less open or more tubular than that of Listera, and by the pollen becoming friable at a still earlier age, its fertilisation would be rendered more and more easy without the aid of the explosive rostellum. Ultimately it would become a superfluity; and then, on the principle that every part which is not brought into action tends to disappear, from causes which I have elsewhere endeavoured to explain,[12] this would happen with the rostellum. We should then see a new species, in the condition of Cephalanthera as far as its means of fertilisation were concerned, but in general structure closely allied to Neottia and Listera.

Mr. Fitzgerald, in the introduction to his 'Australian Orchids,' says that Thelymitra carnea, one of the Neotteæ, invariably fertilises itself by means of the incoherent pollen falling on the stigma. Nevertheless a viscid rostellum, and other structures adapted for cross-fertilisation are present. The flowers seldom expand, and never until they have fertilised themselves; so that they seem tending towards a cleistogene condition. Thelymitra longifolia is likewise fertilised in the bud, according to Mr. Fitzgerald, but the flowers open for about an hour on fine days, and thus cross-fertilisation is at least possible. On the other hand, the species of the allied genus Diuris are said to be wholly dependent on insects for their fertilisation.

  1. I am much indebted to Mr. A. G. More, of Bembridge, in the Isle of Wight, for repeatedly sending me fresh specimens of this beautiful Orchis.
  2. 'Verhandl. d. Nat. Ver. f. Westfal.' Jahrg. xxv. III. Folge, v. Bd. pp. 7–36.
  3. 'Ueber den Blüthenbau von Epipogium,' &c. 1866; see also Irmisch, 'Beitrage zur Biologie der Orchideen,' 1853, p. 55.
  4. Specimens of this rare Highland Orchid were kindly sent me by the Rev. G. Gordon of Elgin.
  5. 'Amer. Journal of Science,' vol. xxxiv. 1862, p. 427. I formerly thought that with this plant and Spiranthes, it was the labellum which moved from the column to allow of the more free entrance of insects; but Professor Gray is convinced that it is the column which moves.
  6. In a foreign species, Goodyera discolor, sent me by Mr. Bateman, the pollinia approach in structure still more closely those of the the Ophreæ; for the pollinia extend into long caudicles, resembling in form those of an Orchis. The caudicle is here formed of a bundle of elastic threads, with very small and thin packets of pollen-grains attached to them and arranged like tiles one over the other. The two caudieles are united together near their bases, where they are attached to a disc of membrane lined with viscid matter. From the small size and extreme thinness of the basal packets of pollen, and from the strength of their attachment to the threads, I believe that they are in a functionless condition; if so, these prolongations of the pollinia are true caudicles.
  7. I am indebted to Dr. Battersby of Torquay, and to Mr. A. G. More of Bembridge, for sending me specimens. I subsequently examined many growing plants.
  8. Professor Asa Gray was so kind as to examine for me Spiranthes gracilis and cernua in the United States. He found the same general structure as in our S. autumnalis, and was struck with the narrowness of the passage into the flower. He has since confirmed ('Amer. Journ. of Science,' vol. xxxiv. p. 427) my account of the structure and action of all the parts in Spiranthes, with the exception that it is the column and not the labellum, as I formerly thought, which moves as the flowers become mature. He adds that the widening of the passage, which plays so important a part in the fertilisation of the flower, "is so striking that we wonder how we overlooked it."
  9. 'Australian Orchids,' part ii. 1876.
  10. 'Philosophical Transactions,' 1834, p. 259.
  11. This unnatural sickly-looking plant has generally been supposed to be parasitic on the roots of the trees under the shade of which it lives; but, according to Irmisoh ('Beiträge zur Biologie und Morphologie der Orchideen,' 1853, s. 25), this certainly is not the case.
  12. 'Variation of Animals and Plants under Domestication,' 2nd edit. vol. ii. p. 309.