The Effects of Cross & Self-Fertilisation in the Vegetable Kingdom · Charles Darwin
CHAPTER XI.
THE HABITS OF INSECTS IN RELATION TO THE FERTILISATION OF FLOWERS. Insects visit the flowers of the same species as long as they can. Cause of this habit. Means by which bees recognise the flowers of the same species. Sudden secretion of nectar. Nectar of certain flowers unattractive to certain insects. Industry of bees, and the number of flowers visited within a short time. Perforation of the corolla by bees. Skill shown in the operation. Hive-bees profit by the holes made by humble-bees. Effects of habit. The motive for perforating flowers to save time. Flowers growing in crowded masses chiefly perforated. Bees and various other insects must be directed by instinct to search flowers for nectar and pollen, as they act in this manner without instruction as soon as they emerge from the pupa state. Their instincts, however, are not of a specialised nature, for they visit many exotic flowers as readily as the endemic kinds, and they often search for nectar in flowers which do not secrete any; and they may be seen attempting to suck it out of nectaries of such length that it cannot be reached by them. (11/1. See, on this subject Hermann Muller ‘Befruchtung’ etc. page 427; and Sir J. Lubbock’s ‘British Wild Flowers’ etc. page 20. Muller ‘Bienen Zeitung’ June 1876 page 119, assigns good reasons for his belief that bees and many other Hymenoptera have inherited from some early nectar-sucking progenitor greater skill in robbing flowers than that which is displayed by insects belonging to the other Orders.) All kinds of bees and certain other insects usually visit the flowers of the same species as long as they can, before going to another species. This fact was observed by Aristotle with respect to the hive-bee more than 2000 years ago, and was noticed by Dobbs in a paper published in 1736 in the Philosophical Transactions. It may be observed by any one, both with hive and humble-bees, in every flower-garden; not that the habit is invariably followed. Mr. Bennett watched for several hours many plants of Lamium album, L. purpureum, and another Labiate plant, Nepeta glechoma, all growing mingled together on a bank near some hives; and he found that each bee confined its visits to the same species. (11/2. ‘Nature’ 1874 June 4 page 92.) The pollen of these three plants differs in colour, so that he was able to test his observations by examining that which adhered to the bodies of the captured bees, and he found one kind on each bee.
Humble and hive-bees are good botanists, for they know that varieties may differ widely in the colour of their flowers and yet belong to the same species. I have repeatedly seen humble-bees flying straight from a plant of the ordinary red Dictamnus fraxinella to a white variety; from one to another very differently coloured variety of Delphinium consolida and of Primula veris; from a dark purple to a bright yellow variety of Viola tricolor; and with two species of Papaver, from one variety to another which differed much in colour; but in this latter case some of the bees flew indifferently to either species, although passing by other genera, and thus acted as if the two species were merely varieties. Hermann Muller also has seen hive-bees flying from flower to flower of Ranunculus bulbosus and arvensis, and of Trifolium fragiferum and repens; and even from blue hyacinths to blue violets. (11/3. ‘Bienen Zeitung’ July 1876 page 183.) Some species of Diptera or flies keep to the flowers of the same species with almost as much regularity as do bees; and when captured they are found covered with pollen. I have seen Rhingia rostrata acting in this manner with the flowers of Lychnis dioica, Ajuga reptans, and Vici sepium. Volucella plumosa and Empis cheiroptera flew straight from flower to flower of Myosotis sylvatica. Dolichopus nigripennis behaved in the same manner with Potentilla tormentilla; and other Diptera with Stellaria holostea, Helianthemum vulgare, Bellis perennis, Veronica hederaefolia and chamoedrys; but some flies visited indifferently the flowers of these two latter species. I have seen more than once a minute Thrips, with pollen adhering to its body, fly from one flower to another of the same kind; and one was observed by me crawling about within a convolvulus with four grains of pollen adhering to its head, which were deposited on the stigma.
Fabricius and Sprengel state that when flies have once entered the flowers of Aristolochia they never escape,--a statement which I could not believe, as in this case the insects would not aid in the cross-fertilisation of the plant; and this statement has now been shown by Hildebrand to be erroneous. As the spathes of Arum maculatum are furnished with filaments apparently adapted to prevent the exit of insects, they resemble in this respect the flowers of Aristolochia; and on examining several spathes, from thirty to sixty minute Diptera belonging to three species were found in some of them; and many of these insects were lying dead at the bottom, as if they had been permanently entrapped. In order to discover whether the living ones could escape and carry pollen to another plant, I tied in the spring of 1842 a fine muslin bag tightly round a spathe; and on returning in an hour’s time several little flies were crawling about on the inner surface of the bag. I then gathered a spathe and breathed hard into it; several flies soon crawled out, and all without exception were dusted with arum pollen. These flies quickly flew away, and I distinctly saw three of them fly to another plant about a yard off; they alighted on the inner or concave surface of the spathe, and suddenly flew down into the flower. I then opened this flower, and although not a single anther had burst, several grains of pollen were lying at the bottom, which must have been brought from another plant by one of these flies or by some other insect. In another flower little flies were crawling about, and I saw them leave pollen on the stigmas.
I do not know whether Lepidoptera generally keep to the flowers of the same species; but I once observed many minute moths (I believe Lampronia (Tinea) calthella) apparently eating the pollen of Mercurialis annua, and they had the whole front of their bodies covered with pollen. I then went to a female plant some yards off, and saw in the course of fifteen minutes three of these moths alight on the stigmas. Lepidoptera are probably often induced to frequent the flowers of the same species, whenever these are provided with a long and narrow nectary, as in this case other insects cannot suck the nectar, which will thus be preserved for those having an elongated proboscis. No doubt the Yucca moth visits only the flowers whence its name is derived, for a most wonderful instinct guides this moth to place pollen on the stigma, so that the ovules may be developed on which the larvae feed. (11/4. Described by Mr. Riley in the ‘American Naturalist’ volume 7 October 1873.)With respect to Coleoptera, I have seen Meligethes covered with pollen flying from flower to flower of the same species; and this must often occur, as, according to M. Brisout, “many of the species affect only one kind of plant.” (11/5. As quoted in ‘American Nat.’ May 1873 page 270.)
It must not be supposed from these several statements that insects strictly confine their visits to the same species. They often visit other species when only a few plants of the same kind grow near together. In a flower-garden containing some plants of Œnothera, the pollen of which can easily be recognised, I found not only single grains but masses of it within many flowers of Mimulus, Digitalis, Antirrhinum, and Linaria. Other kinds of pollen were likewise detected in these same flowers. A large number of the stigmas of a plant of Thyme, in which the anthers were completely aborted, were examined; and these stigmas, though scarcely larger than a split needle, were covered not only with pollen of Thyme brought from other plants by the bees, but with several other kinds of pollen.
That insects should visit the flowers of the same species as long as they can, is of great importance to the plant, as it favours the cross-fertilisation of distinct individuals of the same species; but no one will suppose that insects act in this manner for the good of the plant. The cause probably lies in insects being thus enabled to work quicker; they have just learnt how to stand in the best position on the flower, and how far and in what direction to insert their proboscides. (11/6. Since these remarks were written, I find that Hermann Muller has come to almost exactly the same conclusion with respect to the cause of insects frequenting as long as they can the flowers of the same species: ‘Bienen Zeitung’ July 1876 page 182.) They act on the same principle as does an artificer who has to make half-a-dozen engines, and who saves time by making consecutively each wheel and part for all of them. Insects, or at least bees, seem much influenced by habit in all their manifold operations; and we shall presently see that this holds good in their felonious practice of biting holes through the corolla.
It is a curious question how bees recognise the flowers of the same species. That the coloured corolla is the chief guide cannot be doubted. On a fine day, when hive-bees were incessantly visiting the little blue flowers of Lobelia erinus, I cut off all the petals of some, and only the lower striped petals of others, and these flowers were not once again sucked by the bees, although some actually crawled over them. The removal of the two little upper petals alone made no difference in their visits. Mr. J. Anderson likewise states that when he removed the corollas of the Calceolaria, bees never visited the flowers. (11/7. ‘Gardeners’ Chronicle’ 1853 page 534. Kurr cut off the nectaries from a large number of flowers of several species, and found that the greater number yielded seeds; but insects probably would not perceive the loss of the nectary until they had inserted their proboscides into the holes thus formed, and in doing so would fertilise the flowers. He also removed the whole corolla from a considerable number of flowers, and these likewise yielded seeds.
Flowers which are self-fertile would naturally produce seeds under these circumstances; but I am greatly surprised that Delphinium consolida, as well as another species of Delphinium, and Viola tricolor, should have produced a fair supply of seeds when thus treated; but it does not appear that he compared the number of the seeds thus produced with those yielded by unmutilated flowers left to the free access of insects: ‘Bedeutung der Nektarien’ 1833 pages 123-135.) On the other hand, in some large masses of Geranium phaeum which had escaped out of a garden, I observed the unusual fact of the flowers continuing to secrete an abundance of nectar after all the petals had fallen off; and the flowers in this state were still visited by humble-bees. But the bees might have learnt that these flowers with all their petals lost were still worth visiting, by finding nectar in those with only one or two lost. The colour alone of the corolla serves as an approximate guide: thus I watched for some time humble-bees which were visiting exclusively plants of the white-flowered Spiranthes autumnalis, growing on short turf at a considerable distance apart; and these bees often flew within a few inches of several other plants with white flowers, and then without further examination passed onwards in search of the Spiranthes. Again, many hive-bees which confined their visits to the common ling (Calluna vulgaris), repeatedly flew towards Erica tetralix, evidently attracted by the nearly similar tint of their flowers, and then instantly passed on in search of the Calluna.
That the colour of the flower is not the sole guide, is clearly shown by the six cases above given of bees which repeatedly passed in a direct line from one variety to another of the same species, although they bore very differently coloured flowers. I observed also bees flying in a straight line from one clump of a yellow-flowered Œnothera to every other clump of the same plant in the garden, without turning an inch from their course to plants of Eschscholtzia and others with yellow flowers which lay only a foot or two on either side. In these cases the bees knew the position of each plant in the garden perfectly well, as we may infer by the directness of their flight; so that they were guided by experience and memory. But how did they discover at first that the above varieties with differently coloured flowers belonged to the same species? Improbable as it may appear, they seem, at least sometimes, to recognise plants even from a distance by their general aspect, in the same manner as we should do. On three occasions I observed humble-bees flying in a perfectly straight line from a tall larkspur (Delphinium) which was in full flower to another plant of the same species at the distance of fifteen yards which had not as yet a single flower open, and on which the buds showed only a faint tinge of blue. Here neither odour nor the memory of former visits could have come into play, and the tinge of blue was so faint that it could hardly have served as a guide. (11/8. A fact mentioned by Hermann Muller ‘Die Befruchtung’ etc. page 347, shows that bees possess acute powers of vision and discrimination; for those engaged in collecting pollen from Primula elatior invariably passed by the flowers of the long-styled form, in which the anthers are seated low down in the tubular corolla. Yet the difference in aspect between the long-styled and short-styled forms is extremely slight.)
The conspicuousness of the corolla does not suffice to induce repeated visits from insects, unless nectar is at the same time secreted, together perhaps with some odour emitted. I watched for a fortnight many times daily a wall covered with Linaria cymbalaria in full flower, and never saw a bee even looking at one. There was then a very hot day, and suddenly many bees were industriously at work on the flowers. It appears that a certain degree of heat is necessary for the secretion of nectar; for I observed with Lobelia erinus that if the sun ceased to shine for only half an hour, the visits of the bees slackened and soon ceased. An analogous fact with respect to the sweet excretion from the stipules of Vicia sativa has been already given. As in the case of the Linaria, so with Pedicularis sylvatica, Polygala vulgaris, Viola tricolor, and some species of Trifolium, I have watched the flowers day after day without seeing a bee at work, and then suddenly all the flowers were visited by many bees. Now how did so many bees discover at once that the flowers were secreting nectar? I presume that it must have been by their odour; and that as soon as a few bees began to suck the flowers, others of the same and of different kinds observed the fact and profited by it. We shall presently see, when we treat of the perforation of the corolla, that bees are fully capable of profiting by the labour of other species. Memory also comes into play, for, as already remarked, bees know the position of each clump of flowers in a garden. I have repeatedly seen them passing round a corner, but otherwise in as straight a line as possible, from one plant of Fraxinella and of Linaria to another and distant one of the same species; although, owing to the intervention of other plants, the two were not in sight of each other.
It would appear that either the taste or the odour of the nectar of certain flowers is unattractive to hive or to humble-bees, or to both; for there seems no other reason why certain open flowers which secrete nectar are not visited by them. The small quantity of nectar secreted by some of these flowers can hardly be the cause of their neglect, as hive-bees search eagerly for the minute drops on the glands on the leaves of the Prunus laurocerasus. Even the bees from different hives sometimes visit different kinds of flowers, as is said to be the case by Mr. Grant with respect to the Polyanthus and Viola tricolor. (11/9. ‘Gardeners’ Chronicle’ 1844 page 374.) I have known humble-bees to visit the flowers of Lobelia fulgens in one garden and not in another at the distance of only a few miles. The cupful of nectar in the labellum of Epipactis latifolia is never touched by hive- or humble-bees, although I have seen them flying close by; and yet the nectar has a pleasant taste to us, and is habitually consumed by the common wasp.
As far as I have seen, wasps seek for nectar in this country only from the flowers of this Epipactis, Scrophularia aquatica, Symphoricarpus racemosa (11/10. The same fact apparently holds good in Italy, for Delpino says that the flowers of these three plants are alone visited by wasps: ‘Nettarii Estranuziali, Bulletino Entomologico’ anno 6.), and Tritoma; the two former plants being endemic, and the two latter exotic. As wasps are so fond of sugar and of any sweet fluid, and as they do not disdain the minute drops on the glands of Prunus laurocerasus, it is a strange fact that they do not suck the nectar of many open flowers, which they could do without the aid of a proboscis. Hive-bees visit the flowers of the Symphoricarpus and Tritoma, and this makes it all the stranger that they do not visit the flowers of the Epipactis, or, as far as I have seen, those of the Scrophularia aquatica; although they do visit the flowers of Scrophularia nodosa, at least in North America. (11/11. ‘Silliman’s American Journal of Science’ August 1871.)
The extraordinary industry of bees and the number of flowers which they visit within a short time, so that each flower is visited repeatedly, must greatly increase the chance of each receiving pollen from a distinct plant. When the nectar is in any way hidden, bees cannot tell without inserting their proboscides whether it has lately been exhausted by other bees, and this, as remarked in a former chapter, forces them to visit many more flowers than they otherwise would. But they endeavour to lose as little time as they can; thus in flowers having several nectaries, if they find one dry they do not try the others, but as I have often observed, pass on to another flower. They work so industriously and effectually, that even in the case of social plants, of which hundreds of thousands grow together, as with the several kinds of heath, every single flower is visited, of which evidence will presently be given. They lose no time and fly very quickly from plant to plant, but I do not know the rate at which hive-bees fly. Humble-bees fly at the rate of ten miles an hour, as I was able to ascertain in the case of the males from their curious habit of calling at certain fixed points, which made it easy to measure the time taken in passing from one place to another.
With respect to the number of flowers which bees visit in a given time, I observed that in exactly one minute a humble-bee visited twenty-four of the closed flowers of the Linaria cymbalaria; another bee visited in the same time twenty-two flowers of the Symphoricarpus racemosa; and another seventeen flowers on two plants of a Delphinium. In the course of fifteen minutes a single flower on the summit of a plant of Œnothera was visited eight times by several humble-bees, and I followed the last of these bees, whilst it visited in the course of a few additional minutes every plant of the same species in a large flower-garden. In nineteen minutes every flower on a small plant of Nemophila insignis was visited twice. In one minute six flowers of a Campanula were entered by a pollen-collecting hive-bee; and bees when thus employed work slower than when sucking nectar. Lastly, seven flower-stalks on a plant of Dictamnus fraxinella were observed on the 15th of June 1841 during ten minutes; they were visited by thirteen humble-bees each of which entered many flowers. On the 22nd the same flower-stalks were visited within the same time by eleven humble-bees. This plant bore altogether 280 flowers, and from the above data, taking into consideration how late in the evening humble-bees work, each flower must have been visited at least thirty times daily, and the same flower keeps open during several days. The frequency of the visits of bees is also sometimes shown by the manner in which the petals are scratched by their hooked tarsi; I have seen large beds of Mimulus, Stachys, and Lathyrus with the beauty of their flowers thus sadly defaced.
Text from Project Gutenberg, public domain in the United States.