ORCHIDS, FORMS OF FLOWERS, POLLINATION, CROSS AND SELF-FERTILIZATION
Ophrys orchids, a genus with well over 100 terrestrial species, are the premier example of sexual deception in plants. These orchids deploy visual as well as chemical mimicry (sex pheromones) to entice male insects to attempt mating with the flower, termed pseudo-copulation. What the duped males get for their efforts is a packet of pollinia glued to their body, without the reward of either nectar or sex.104 The common names of two widespread European species, the fly orchid (Ophrys insectifera) and the bee orchid (O. apifera), reflect the insects they attract. Darwin found Ophrys apifera while vacationing at the seaside town of Torquay, and it presented a special puzzle—a tendency to self-fertilize in Britain, in the northern part of its range, with few insect visitors arriving in spite of its apparent “efforts” at attraction. His letters to colleagues noted his concerns. “No single point in natural history interests and perplexes me as much as the self-fertilization of the bee orchis,”105 he wrote to one correspondent, and to another he lamented that “all facts point clearly to eternal self-fertilisation; yet I cannot swallow the bitter pill” that Ophrys is self-fertilized.106 After an attempt at crowd-sourcing, with a letter published in the Gardeners’ Chronicle that presented his observations and encouraged readers to study the fertilization of the plants in locales where insects might be more abundant, Darwin concluded that, to avoid extinction, plants such as the bee orchid are capable of producing viable seeds by self-fertilisation in order to survive times when insect pollinators are scarce.
I should be extremely much obliged to any person living where the Bee or Fly Orchis is tolerably common, if he will have the kindness to make a few simple observations on their manner of fertilisation. … [In] the Bee Orchis (Ophrys apifera) … the pollen masses are furnished with sticky glands, but differently from in [other] Orchids, they naturally fall out of their pouches; and from being of the proper length, though still retained at the gland-end, they fall on the stigmatic surface, and the plant is thus self-fertilised. During several years I have examined many flowers, and never in a single instance found even one of the pollen-masses carried away by insects, or ever saw the flower’s own pollen-masses fail to fall on the stigma. Robert Brown consequently believed that the visits of insects would be injurious to the fertilisation of this Orchis; and rather fancifully imagined that the flower resembled a bee in order to deter their visits. We must admit that the natural falling out of the pollen-masses of this Orchis is a special contrivance for its self-fertilisation; and as far as my experience goes, a perfectly successful contrivance, for I have always found this plant self-fertilised; nevertheless a long course of observation has made me greatly doubt whether the flowers of any kind of plant are for a perpetuity of generations fertilised by their own pollen. And what are we to say with respect to the sticky glands of the Bee Orchis, the use and efficiency of which glands in all other British Orchids are so manifest? Are we to conclude that this one species is provided with these organs for no use? I cannot think so; but would rather infer that, during some years or in some other districts, insects do visit the Bee Orchis and occasionally transport pollen from one flower to another, and thus give it the advantage of an occasional cross. So with the Bee Orchis, though its self-fertilisation is specially provided for, it may not exist here under the most favourable conditions of life; and in other districts or during particular seasons it may be visited by insects, and in this case, as its pollen masses are furnished with sticky glands, it would almost certainly receive the benefit of an occasional cross impregnation. It is this curious apparent contradiction in the structure of the Bee Orchis—one part, namely the sticky glands, being adapted for fertilisation by insect agency—another part, namely the natural falling out of the pollen-masses, being adapted for self-fertilisation without insect agency—which makes me anxious to hear what happens to the pollen-masses of the Bee Orchis in other districts or parts of England.
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. The caudicles of the pollinia are remarkably long, thin, and flexible, instead of being, as in all the other Ophreae 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 (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. …
Ophrys apifera, or Bee Ophrys. 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. a. anther l. labellum
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! …
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 that the benefits thus derived are of high importance. On the other hand, self-fertilisation is mainfestly 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 deserves especial attention that the flowers of all the above-named self-fertile species still retain various structures which it is impossible to doubt are adapted for insuring cross-fertilisation, though they are now rarely or never brought into play. We may therefore conclude that all these plants are descended from species or varieties which were formerly fertilised by insect-aid. Moreover, several of the genera to which these self-fertile species belong, include other species, which are incapable of self-fertilisation.
Orchis mascula. Watercolor by Elizabeth Blackwell, A Curious Herbal.