CROSS AND SELF-FERTILIZATION, PLANT MOVEMENT
Clovers of the world are commonly trifoliate, bearing compound leaves of three leaflets (hence the Latin trifolium) and heads of small densely clustered flowers of red, purple, white, or yellow. A common and seemingly unremarkable genus of field and lawn, several of the 300 or more Trifolium species are grown worldwide for fodder, hay, and silage, as well as pasture improvement thanks to their nitrogen-fixing roots. Their nectar-rich flowers have also made them a favorite of beekeepers. Darwin encouraged clovers in his meadows and gardens for another reason: he saw in them evolutionary dramas.
It started with cross-pollination studies. He was sure that bees, especially “humble-bees” (bumblebees) were vital to the cross-pollination of many flowering plants, but he needed data to back up his hunch. Turning to patches of red clover (T. pratense) in the meadow just behind his house, he performed a classic exclusion experiment, netting some patches to keep bees out while leaving others open, then counting the seeds produced by flowers in each group. It was, as he excitedly reported to Joseph Hooker, a success. “100 Head of Trifolium pratense protected from Bees did not produce one single seed; another Hundred visited by Humble-bees produced nearly 3000 seeds!”138 It got him thinking: if bees declined in the area, what would happen to the flowers? Further, what species might affect the bees? And what species might affect the species that affect the bees? This led to the classic passage in Origin quoted in this chapter, which is, perhaps, the first description of a chain of ecological interconnectedness, connecting cats in an area to its flower populations through the intermediaries of mice and bumblebees.139
I am tempted to give one more instance showing how plants and animals, most remote in the scale of nature, are bound together by a web of complex relations. … From experiments which I have tried, I have found that the visits of bees, if not indispensable, are at least highly beneficial to the fertilisation of our clovers; but humble-bees alone visit the common red clover (Trifolium pratense), as other bees cannot reach the nectar. Hence I have very little doubt, that if the whole genus of humble-bees became extinct or very rare in England, the heartsease and red clover would become very rare, or wholly disappear. The number of humble-bees in any district depends in a great degree on the number of field-mice, which destroy their combs and nests; and Mr. H. Newman, who has long attended to the habits of humble-bees, believes that “more than two thirds of them are thus destroyed all over England.” Now the number of mice is largely dependent, as every one knows, on the number of cats; and Mr. Newman says, “Near villages and small towns I have found the nests of humble-bees more numerous than elsewhere, which I attribute to the number of cats that destroy the mice.” Hence it is quite credible that the presence of a feline animal in large numbers in a district might determine, through the intervention first of mice and then of bees, the frequency of certain flowers in that district! …
Let us now turn to the nectar-feeding insects in our imaginary case: we may suppose the plant of which we have been slowly increasing the nectar by continued selection, to be a common plant; and that certain insects depended in main part on its nectar for food. I could give many facts, showing how anxious bees are to save time; for instance, their habit of cutting holes and sucking the nectar at the bases of certain flowers, which they can, with a very little more trouble, enter by the mouth. Bearing such facts in mind, I can see no reason to doubt that an accidental deviation in the size and form of the body, or in the curvature and length of the proboscis, &c., far too slight to be appreciated by us, might profit a bee or other insect, so that an individual so characterised would be able to obtain its food more quickly, and so have a better chance of living and leaving descendants. Its descendants would probably inherit a tendency to a similar slight deviation of structure. The tubes of the corollas of the common red and incarnate clovers (Trifolium pratense and incarnatum) do not on a hasty glance appear to differ in length; yet the hive-bee can easily suck the nectar out of the incarnate clover, but not out of the common red clover, which is visited by humble-bees alone; so that whole fields of the red clover offer in vain an abundant supply of precious nectar to the hive-bee. Thus it might be a great advantage to the hive-bee to have a slightly longer or differently constructed proboscis. On the other hand, I have found by experiment that the fertility of clover greatly depends on bees visiting and moving parts of the corolla, so as to push the pollen on to the stigmatic surface. Hence, again, if humble-bees were to become rare in any country, it might be a great advantage to the red clover to have a shorter or more deeply divided tube to its corolla, so that the hive-bee could visit its flowers. Thus I can understand how a flower and a bee might slowly become, either simultaneously or one after the other, modified and adapted in the most perfect manner to each other, by the continued preservation of individuals presenting mutual and slightly favourable deviations of structure.140
Things were a bit more complicated than Darwin realized, however. He believed that bumblebees alone pollinated red clover, as a honeybee, with its shorter proboscis, could not reach the nectar.
Trifolium repens (Leguminosae).—Several plants were protected from insects, and the seeds from ten flower-heads on these plants, and from ten heads on other plants growing outside the net (which I saw visited by bees), were counted; and the seeds from the latter plants were very nearly ten times as numerous as those from the protected plants. The experiment was repeated on the following year; and twenty protected heads now yielded only a single aborted seed, whilst twenty heads on the plants outside the net (which I saw visited by bees) yielded 2290 seeds, as calculated by weighing all the seed, and counting the number in a weight of two grains.
T. pratense.—One hundred flower-heads on plants protected by a net did not produce a single seed, whilst 100 heads on plants growing outside, which were visited by bees, yielded 68 grains weight of seeds; and as eighty seeds weighed two grains, the 100 heads must have yielded 2,720 seeds. I have often watched this plant, and have never seen hive-bees sucking the flowers, except from the outside through holes bitten by humble-bees, or deep down between the flowers, as if in search of some secretion from the calyx … It is at least certain that humble-bees are the chief fertilisers of the common red clover.
A vicar friend, Charles Hardy, corrected Darwin on this point, relating evidence of a red clover field teeming with honeybees (though he acknowledged that it was second-growth, after mowing, and the flowers seemed smaller).141 Darwin added Hardy’s observation to the third edition of Origin, but this also led him down a rabbit-hole (all good science has them). Watching honeybees visiting red clover, he noticed that some were nectar robbers, getting nectar from the base of the flower through holes chewed through the corolla, while others went into the flower in the usual way. He suddenly thought these behaviors could reflect separate foraging castes of bees, with long and short probosces. As he was on holiday in Southampton with his family when this occurred to him, he couldn’t find a clover field to test the idea, so he wrote an urgent letter to his neighbor John Lubbock, asking him to look out for these modes of foraging in his local bees, urging, “Now if you see this, do for Heaven sake catch me some of each and put in spirits and keep them separate.” But by the next day, he’d succeeded in finding a field and realized the idea was wrong, writing as follow up, “I beg a million pardons … it is all an illusion (but almost excusable) about the Bees. I do so hope that you have not wasted any time for my stupid blunder.” He closed with tongue-in-cheek self-flagellation: “I hate myself I hate clover and I hate Bees.”142
Darwin’s later interests in Trifolium extended to plant movement, with analyses of the nyctitropic (sleep) movement of leaves and circular (circumnutation) motion of cotyledons and flower stems. One of the most remarkable to him was the geotropic (gravity-sensitive) motion of T. subterraneum, the burrowing clover. This species is unique among clovers in that it buries its flowers after fertilization—the seeds develop underground, a phenomenon called geocarpy. “There seems much odd about whole case,” Darwin commented to his son Francis as he tried to figure out how the plant buried its own seeds.143 He eventually succeeded and reported how circumnutation of T. subterraneum peduncles continues even after the flower heads touch the ground, slowing “planting” their own seeds.
The Burying of Seed-capsules: Trifolium subterraneum.—The flower-heads of this plant are remarkable from producing only 3 or 4 perfect flowers, which are situated exteriorly. All the other many flowers abort, and are modified into rigid points, with a bundle of vessels running up their centres. After a time 5 long, elastic, claw-like projections, which represent the divisions of the calyx, are developed on their summits. As soon as the perfect flowers wither they bend downwards, supposing the peduncle to stand upright, and they then closely surround its upper part. This movement is due to epinasty, as is likewise the case with the flowers of T. repens. The imperfect central flowers ultimately follow, one after the other, the same course. Whilst the perfect flowers are thus bending down, the whole peduncle curves downwards and increases much in length, until the flower-head reaches the ground. … In whatever position the branches may be placed, the upper part of the peduncle at first bends vertically upwards through heliotropism; but as soon as the flowers begin to wither the downward curvature of the whole peduncle commences. As this latter movement occurred in complete darkness, and with peduncles arising from upright and from dependent branches, it cannot be due to apheliotropism or to epinasty, but must be attributed to geotropism.
After the heads have buried themselves, the central aborted flowers increase considerably in length and rigidity, and become bleached. They gradually curve, one after the other, upwards or towards the peduncle, in the same manner as did the perfect flowers at first. In thus moving, the long claws on their summits carry with them some earth. Hence a flower-head which has been buried for a sufficient time, forms a rather large ball, consisting of the aborted flowers, separated from one another by earth, and surrounding the little pods (the product of the perfect flowers) which lie close round the upper part of the peduncle. The calyces of the perfect and imperfect flowers are clothed with simple and multicellular hairs, which have the power of absorption; for when placed in a weak solution of carbonate of ammonia (2 gr. to 1 oz. of water) their protoplasmic contents immediately became aggregated and afterwards displayed the usual slow movements. This clover generally grows in dry soil, but whether the power of absorption by the hairs on the buried flower-heads is of any importance to them we do not know. Only a few of the flower-heads, which from their position are not able to reach the ground and bury themselves, yield seeds; whereas the buried ones never failed, as far as we observed, to produce as many seeds as there had been perfect flowers.
We will now consider the movements of the peduncle whilst curving down to the ground. We have seen that an upright young flower-head circumnutated conspicuously; and that this movement continued after the peduncle had begun to bend downwards. The same peduncle was observed when inclined at an angle of 19° above the horizon, and it circumnutated during two days. … During the first day the peduncle clearly circumnutated, for it moved 4 times down and 3 times up; and on each succeeding day, as it sank downwards, the same movement continued. …
Any one who will observe a flower-head burying itself, will be convinced that the rocking movement, due to the continued circumnutation of the peduncle, plays an important part in the act. Considering that the flower-heads are very light, that the peduncles are long, thin, and flexible, and that they arise from flexible branches, it is incredible that an object as blunt as one of these flower-heads could penetrate the ground by means of the growing force of the peduncle, unless it were aided by the rocking movement. After a flower-head has penetrated the ground to a small depth, another and efficient agency comes into play; the central rigid aborted flowers, each terminating in five long claws, curve up towards the peduncle; and in doing so can hardly fail to drag the head down to a greater depth, aided as this action is by the circumnutating movement, which continues after the flower-head has completely buried itself. The aborted flowers thus act something like the hands of the mole, which force the earth backwards and the body forwards.
Tropaeolum majus. Water and bodycolor on vellum by English School artist, Album of Garden Flowers.