PERFORATION OF THE COROLLA BY BEES.
I have already alluded to bees biting holes in flowers for the sake of obtaining the nectar. They often act in this manner, both with endemic and exotic species, in many parts of Europe, in the United States, and in the Himalaya; and therefore probably in all parts of the world. The plants, the fertilisation of which actually depends on insects entering the flowers, will fail to produce seed when their nectar is stolen from the outside; and even with those species which are capable of fertilising themselves without any aid, there can be no cross-fertilisation, and this, as we know, is a serious evil in most cases. The extent to which humble-bees carry on the practice of biting holes is surprising: a remarkable case was observed by me near Bournemouth, where there were formerly extensive heaths. I took a long walk, and every now and then gathered a twig of Erica tetralix, and when I had got a handful all the flowers were examined through a lens. This process was repeated many times; but though many hundreds were examined, I did not succeed in finding a single flower which had not been perforated. Humble-bees were at the time sucking the flowers through these perforations. On the following day a large number of flowers were examined on another heath with the same result, but here hive-bees were sucking through the holes. This case is all the more remarkable, as the innumerable holes had been made within a fortnight, for before that time I saw the bees everywhere sucking in the proper manner at the mouths of the corolla. In an extensive flower-garden some large beds of Salvia grahami, Stachys coccinea, and Pentstemon argutus (?) had every flower perforated, and many scores were examined. I have seen whole fields of red clover (Trifolium pratense) in the same state. Dr. Ogle found that 90 per cent of the flowers of Salvia glutinosa had been bitten. In the United States Mr. Bailey says it is difficult to find a blossom of the native Gerardia pedicularia without a hole in it; and Mr. Gentry, in speaking of the introduced Wistaria sinensis, says “that nearly every flower had been perforated.” (11/12. Dr. Ogle ‘Pop. Science Review’ July 1869 page 267. Bailey ‘American Naturalist’ November 1873 page 690. Gentry ibid May 1875 page 264.)
As far as I have seen, it is always humble-bees which first bite the holes, and they are well fitted for the work by possessing powerful mandibles; but hive-bees afterwards profit by the holes thus made. Dr. Hermann Muller, however, writes to me that hive-bees sometimes bite holes through the flowers of Erica tetralix. No insects except bees, with the single exception of wasps in the case of Tritoma, have sense enough, as far as I have observed, to profit by the holes already made. Even humble-bees do not always discover that it would be advantageous to them to perforate certain flowers. There is an abundant supply of nectar in the nectary of Tropaeolum tricolor, yet I have found this plant untouched in more than one garden, while the flowers of other plants had been extensively perforated; but a few years ago Sir J. Lubbock’s gardener assured me that he had seen humble-bees boring through the nectary of this Tropaeolum. Muller has observed humble-bees trying to suck at the mouths of the flowers of Primula elatior and of an Aquilegia, and, failing in their attempts, they made holes through the corolla; but they often bite holes, although they could with very little more trouble obtain the nectar in a legitimate manner by the mouth of the corolla.
Dr. W. Ogle has communicated to me a curious case. He gathered in Switzerland 100 flower-stems of the common blue variety of the monkshood (Aconitum napellus), and not a single flower was perforated; he then gathered 100 stems of a white variety growing close by, and every one of the open flowers had been perforated. (11/13. Dr. Ogle ‘Popular Science Review’ July 1869 page 267. Bailey ‘American Naturalist’ November 1873 page 690. Gentry ibid May 1875 page 264.) This surprising difference in the state of the flowers may be attributed with much probability to the blue variety being distasteful to bees, from the presence of the acrid matter which is so general in the Ranunculaceae, and to its absence in the white variety in correlation with the loss of the blue tint. According to Sprengel, this plant is strongly proterandrous (11/14. ‘Das Entdeckte’ etc. page 278.); it would therefore be more or less sterile unless bees carried pollen from the younger to the older flowers. Consequently the white variety, the flowers of which were always bitten instead of being properly entered by the bees, would fail to yield the full number of seeds and would be a comparatively rare plant, as Dr. Ogle informs me was the case.
Bees show much skill in their manner of working, for they always make their holes from the outside close to the spot where the nectar lies hidden within the corolla. All the flowers in a large bed of Stachys coccinea had either one or two slits made on the upper side of the corolla near the base. The flowers of a Mirabilis and of Salvia coccinea were perforated in the same manner; whilst those of Salvia grahami, in which the calyx is much elongated, had both the calyx and the corolla invariably perforated. The flowers of Pentstemon argutus are broader than those of the plants just named, and two holes alongside each other had here always been made just above the calyx. In these several cases the perforations were on the upper side, but in Antirrhinum majus one or two holes had been made on the lower side, close to the little protuberance which represents the nectary, and therefore directly in front of and close to the spot where the nectar is secreted.
But the most remarkable case of skill and judgment known to me, is that of the perforation of the flowers of Lathyrus sylvestris, as described by my son Francis. (11/15. ‘Nature’ January 8, 1874 page 189.) The nectar in this plant is enclosed within a tube, formed by the united stamens, which surround the pistil so closely that a bee is forced to insert its proboscis outside the tube; but two natural rounded passages or orifices are left in the tube near the base, in order that the nectar may be reached by the bees. Now my son found in sixteen out of twenty-four flowers on this plant, and in eleven out of sixteen of those on the cultivated everlasting pea, which is either a variety of the same species or a closely allied one, that the left passage was larger than the right one. And here comes the remarkable point,—the humble-bees bite holes through the standard-petal, and they always operated on the left side over the passage, which is generally the larger of the two. My son remarks: “It is difficult to say how the bees could have acquired this habit. Whether they discovered the inequality in the size of the nectar-holes in sucking the flowers in the proper way, and then utilised this knowledge in determining where to gnaw the hole; or whether they found out the best situation by biting through the standard at various points, and afterwards remembered its situation in visiting other flowers. But in either case they show a remarkable power of making use of what they have learnt by experience.” It seems probable that bees owe their skill in biting holes through flowers of all kinds to their having long practised the instinct of moulding cells and pots of wax, or of enlarging their old cocoons with tubes of wax; for they are thus compelled to work on the inside and outside of the same object.
In the early part of the summer of 1857 I was led to observe during some weeks several rows of the scarlet kidney-bean (Phaseolus multiflorus), whilst attending to the fertilisation of this plant, and daily saw humble- and hive-bees sucking at the mouths of the flowers. But one day I found several humble-bees employed in cutting holes in flower after flower; and on the next day every single hive-bee, without exception, instead of alighting on the left wing-petal and sucking the flower in the proper manner, flew straight without the least hesitation to the calyx, and sucked through the holes which had been made only the day before by the humble-bees; and they continued this habit for many following days. (11/16. ‘Gardeners’ Chronicle’ 1857 page 725.) Mr. Belt has communicated to me (July 28th, 1874) a similar case, with the sole difference that less than half of the flowers had been perforated by the humble-bees; nevertheless, all the hive-bees gave up sucking at the mouths of the flowers and visited exclusively the bitten ones. Now how did the hive-bees find out so quickly that holes had been made? Instinct seems to be out of the question, as the plant is an exotic. The holes cannot be seen by bees whilst standing on the wing-petals, where they had always previously alighted. From the ease with which bees were deceived when the petals of Lobelia erinus were cut off, it was clear that in this case they were not guided to the nectar by its smell; and it may be doubted whether they were attracted to the holes in the flowers of the Phaseolus by the odour emitted from them. Did they perceive the holes by the sense of touch in their proboscides, whilst sucking the flowers in the proper manner, and then reason that it would save them time to alight on the outside of the flowers and use the holes? This seems almost too abstruse an act of reason for bees; and it is more probable that they saw the humble-bees at work, and understanding what they were about, imitated them and took advantage of the shorter path to the nectar. Even with animals high in the scale, such as monkeys, we should be surprised at hearing that all the individuals of one species within the space of twenty-four hours understood an act performed by a distinct species, and profited by it.
I have repeatedly observed with various kinds of flowers that all the hive and humble-bees which were sucking through the perforations, flew to them, whether on the upper or under side of the corolla, without the least hesitation; and this shows how quickly all the individuals within the district had acquired the same knowledge. Yet habit comes into play to a certain extent, as in so many of the other operations of bees. Dr. Ogle, Messrs. Farrer and Belt have observed in the case of Phaseolus multiflorus that certain individuals went exclusively to the perforations, while others of the same species visited only the mouths of the flowers. (11/17. Dr. Ogle ‘Pop. Science Review’ April 1870 page 167. Mr. Farrer ‘Annals and Magazine of Natural History’ 4th series volume 2 1868 page 258. Mr. Belt in a letter to me.) I noticed in 1861 exactly the same fact with Trifolium pratense. So persistent is the force of habit, that when a bee which is visiting perforated flowers comes to one which has not been bitten, it does not go to the mouth, but instantly flies away in search of another bitten flower. Nevertheless, I once saw a humble-bee visiting the hybrid Rhododendron azaloides, and it entered the mouths of some flowers and cut holes into the others. Dr. Hermann Muller informs me that in the same district he has seen some individuals of Bombus mastrucatus boring through the calyx and corolla of Rhinanthus alecterolophus, and others through the corolla alone. Different species of bees may, however, sometimes be observed acting differently at the same time on the same plant. I have seen hive-bees sucking at the mouths of the flowers of the common bean; humble-bees of one kind sucking through holes bitten in the calyx, and humble-bees of another kind sucking the little drops of fluid excreted by the stipules. Mr. Beal of Michigan informs me that the flowers of the Missouri currant (Ribes aureum) abound with nectar, so that children often suck them; and he saw hive-bees sucking through holes made by a bird, the oriole, and at the same time humble-bees sucking in the proper manner at the mouths of the flowers. (11/18. The flowers of the Ribes are however sometimes perforated by humble-bees, and Mr. Bundy says that they were able to bite through and rob seven flowers of their honey in a minute: ‘American Naturalist’ 1876 page 238.) This statement about the oriole calls to mind what I have before said of certain species of humming-birds boring holes through the flowers of the Brugmansia, whilst other species entered by the mouth.
The motive which impels bees to gnaw holes through the corolla seems to be the saving of time, for they lose much time in climbing into and out of large flowers, and in forcing their heads into closed ones. They were able to visit nearly twice as many flowers, as far as I could judge, of a Stachys and Pentstemon by alighting on the upper surface of the corolla and sucking through the cut holes, than by entering in the proper way. Nevertheless each bee before it has had much practice, must lose some time in making each new perforation, especially when the perforation has to be made through both calyx and corolla. This action therefore implies foresight, of which faculty we have abundant evidence in their building operations; and may we not further believe that some trace of their social instinct, that is, of working for the good of other members of the community, may here likewise play a part?
Many years ago I was struck with the fact that humble-bees as a general rule perforate flowers only when these grow in large numbers near together. In a garden where there were some very large beds of Stachys coccinea and of Pentstemon argutus, every single flower was perforated, but I found two plants of the former species growing quite separate with their petals much scratched, showing that they had been frequently visited by bees, and yet not a single flower was perforated. I found also a separate plant of the Pentstemon, and saw bees entering the mouth of the corolla, and not a single flower had been perforated. In the following year (1842) I visited the same garden several times: on the 19th of July humble-bees were sucking the flowers of Stachys coccinea and Salvia grahami in the proper manner, and none of the corollas were perforated. On the 7th of August all the flowers were perforated, even those on some few plants of the Salvia which grew at a little distance from the great bed. On the 21st of August only a few flowers on the summits of the spikes of both species remained fresh, and not one of these was now bored. Again, in my own garden every plant in several rows of the common bean had many flowers perforated; but I found three plants in separate parts of the garden which had sprung up accidentally, and these had not a single flower perforated. General Strachey formerly saw many perforated flowers in a garden in the Himalaya, and he wrote to the owner to inquire whether this relation between the plants growing crowded and their perforation by the bees there held good, and was answered in the affirmative. Hence it follows that the red clover (Trifolium pratense) and the common bean when cultivated in great masses in fields,—that Erica tetralix growing in large numbers on heaths,—rows of the scarlet kidney-bean in the kitchen-garden,—and masses of any species in the flower-garden,—are all eminently liable to be perforated.
The explanation of this fact is not difficult. Flowers growing in large numbers afford a rich booty to the bees, and are conspicuous from a distance. They are consequently visited by crowds of these insects, and I once counted between twenty and thirty bees flying about a bed of Pentstemon. They are thus stimulated to work quickly by rivalry, and, what is much more important, they find a large proportion of the flowers, as suggested by my son, with their nectaries sucked dry. (11/19. ‘Nature’ January 8, 1874 page 189.) They thus waste much time in searching many empty flowers, and are led to bite the holes, so as to find out as quickly as possible whether there is any nectar present, and if so, to obtain it.
Flowers which are partially or wholly sterile unless visited by insects in the proper manner, such as those of most species of Salvia, of Trifolium pratense, Phaseolus multiflorus, etc., will fail more or less completely to produce seeds if the bees confine their visits to the perforations. The perforated flowers of those species, which are capable of fertilising themselves, will yield only self-fertilised seeds, and the seedlings will in consequence be less vigorous. Therefore all plants must suffer in some degree when bees obtain their nectar in a felonious manner by biting holes through the corolla; and many species, it might be thought, would thus be exterminated. But here, as is so general throughout nature, there is a tendency towards a restored equilibrium. If a plant suffers from being perforated, fewer individuals will be reared, and if its nectar is highly important to the bees, these in their turn will suffer and decrease in number; but, what is much more effective, as soon as the plant becomes somewhat rare so as not to grow in crowded masses, the bees will no longer be stimulated to gnaw holes in the flowers, but will enter them in a legitimate manner. More seed will then be produced, and the seedlings being the product of cross-fertilisation will be vigorous, so that the species will tend to increase in number, to be again checked, as soon as the plant again grows in crowded masses.