The excretion of a sweet fluid by glands seated outside of a flower is rarely utilised as a means for cross-fertilisation by the aid of insects; but this occurs with the bracteae of the Marcgraviaceae, as the late Dr. Cruger informed me from actual observation in the West Indies, and as Delpino infers with much acuteness from the relative position of the several parts of their flowers. (10/51. ‘Ult. Osservaz. Dicogamia’ 1868-69 page 188.) Mr. Farrer has also shown that the flowers of Coronilla are curiously modified, so that bees may fertilise them whilst sucking the fluid secreted from the outside of the calyx. (10/52. ‘Nature’ 1874 page 169.) It further appears probable from the observations of the Reverend W.A. Leighton, that the fluid so abundantly secreted by glands on the phyllodia of the Australian Acacia magnifica, which stand near the flowers, is connected with their fertilisation. (10/53. ‘Annals and Magazine of Natural History’ volume 16 1865 page 14. In my work on the ‘Fertilisation of Orchids’ and in a paper subsequently published in the ‘Annals and Magazine of Natural History’ it has been shown that although certain kinds of orchids possess a nectary, no nectar is actually secreted by it; but that insects penetrate the inner walls and suck the fluid contained in the intercellular spaces. I further suggested, in the case of some other orchids which do not secrete nectar, that insects gnawed the labellum; and this suggestion has since been proved true. Hermann Muller and Delpino have now shown that some other plants have thickened petals which are sucked or gnawed by insects, their fertilisation being thus aided. All the known facts on this head have been collected by Delpino in his ‘Ult. Osserv.’ part 2 fasc. 2 1875 pages 59-63.)
The amount of pollen produced by anemophilous plants, and the distance to which it is often transported by the wind, are both surprisingly great. Mr. Hassall found that the weight of pollen produced by a single plant of the Bulrush (Typha) was 144 grains. Bucketfuls of pollen, chiefly of Coniferae and Gramineae, have been swept off the decks of vessels near the North American shore; and Mr. Riley has seen the ground near St. Louis, in Missouri, covered with pollen, as if sprinkled with sulphur; and there was good reason to believe that this had been transported from the pine-forests at least 400 miles to the south. Kerner has seen the snow-fields on the higher Alps similarly dusted; and Mr. Blackley found numerous pollen-grains, in one instance 1200, adhering to sticky slides, which were sent up to a height of from 500 to 1000 feet by means of a kite, and then uncovered by a special mechanism. It is remarkable that in these experiments there were on an average nineteen times as many pollen-grains in the atmosphere at the higher than at the lower levels. (10/54. For Mr. Hassall’s observations see ‘Annals and Magazine of Natural History’ volume 8 1842 page 108. In the ‘North American Journal of Science’ January 1842, there is an account of the pollen swept off the decks of a vessel. Riley ‘Fifth Report on the Noxious Insects of Missouri’ 1873 page 86. Kerner ‘Die Schutzmittel des Pollens’ 1873 page 6. This author has also seen a lake in the Tyrol so covered with pollen, that the water no longer appeared blue. Mr. Blackley ‘Experimental Researches on Hay-fever’ 1873 pages 132, 141-152.) Considering these facts, it is not so surprising as it at first appears that all, or nearly all, the stigmas of anemophilous plants should receive pollen brought to them by mere chance by the wind. During the early part of summer every object is thus dusted with pollen; for instance, I examined for another purpose the labella of a large number of flowers of the Fly Ophrys (which is rarely visited by insects), and found on all very many pollen-grains of other plants, which had been caught by their velvety surfaces.
The extraordinary quantity and lightness of the pollen of anemophilous plants are no doubt both necessary, as their pollen has generally to be carried to the stigmas of other and often distant flowers; for, as we shall soon see, most anemophilous plants have their sexes separated. The fertilisation of these plants is generally aided by the stigmas being of large size or plumose; and in the case of the Coniferae, by the naked ovules secreting a drop of fluid, as shown by Delpino. Although the number of anemophilous species is small, as the author just quoted remarks, the number of individuals is large in comparison with that of entomophilous species. This holds good especially in cold and temperate regions, where insects are not so numerous as under a warmer climate, and where consequently entomophilous plants are less favourably situated. We see this in our forests of Coniferae and other trees, such as oaks, beeches, birches, ashes, etc.; and in the Gramineae, Cyperaceae, and Juncaceae, which clothe our meadows and swamps; all these trees and plants being fertilised by the wind. As a large quantity of pollen is wasted by anemophilous plants, it is surprising that so many vigorous species of this kind abounding with individuals should still exist in any part of the world; for if they had been rendered entomophilous, their pollen would have been transported by the aid of the senses and appetites of insects with incomparably greater safety than by the wind. That such a conversion is possible can hardly be doubted, from the remarks lately made on the existence of intermediate forms; and apparently it has been effected in the group of willows, as we may infer from the nature of their nearest allies. (10/55. Hermann Muller ‘Die Befruchtung’ etc. page 149.)
It seems at first sight a still more surprising fact that plants, after having been once rendered entomophilous, should ever again have become anemophilous; but this has occasionally though rarely occurred, for instance, with the common Poterium sanguisorba, as may be inferred from its belonging to the Rosaceae. Such cases are, however, intelligible, as almost all plants require to be occasionally intercrossed; and if any entomiphilous species ceased to be visited by insects, it would probably perish unless it were rendered anemophilous. A plant would be neglected by insects if nectar failed to be secreted, unless indeed a large supply of attractive pollen was present; and from what we have seen of the excretion of saccharine fluid from leaves and glands being largely governed in several cases by climatic influences, and from some few flowers which do not now secrete nectar still retaining coloured guiding-marks, the failure of the secretion cannot be considered as a very improbable event. The same result would follow to a certainty, if winged insects ceased to exist in any district, or became very rare. Now there is only a single plant in the great order of the Cruciferae, namely, Pringlea, which is anemophilous, and this plant is an inhabitant of Kerguelen Land, where there are hardly any winged insects, owing probably, as was suggested by me in the case of Madeira, to the risk which they run of being blown out to sea and destroyed. (10/56. The Reverend A.E. Eaton in ‘Proceedings of the Royal Society’ volume 23 1875 page 351.)
A remarkable fact with respect to anemophilous plants is that they are often diclinous, that is, they are either monoecious with their sexes separated on the same plant, or dioecious with their sexes on distinct plants. In the class Monoecia of Linnaeus, Delpino shows that the species of twenty-eight genera are anemophilous, and of seventeen genera entomophilous. (10/57. ‘Studi sopra un Lignaggio anemofilo delle Compositae’ 1871.) The larger proportion of entomophilous genera in this latter class is probably the indirect result of insects having the power of carrying pollen to another and sometimes distant plant much more securely than the wind. In the above two classes taken together there are thirty-eight anemophilous and thirty-six entomophilous genera; whereas in the great mass of hermaphrodite plants the proportion of anemophilous to entomophilous genera is extremely small. The cause of this remarkable difference may be attributed to anemophilous plants having retained in a greater degree than the entomophilous a primordial condition, in which the sexes were separated and their mutual fertilisation effected by means of the wind. That the earliest and lowest members of the vegetable kingdom had their sexes separated, as is still the case to a large extent, is the opinion of a high authority, Nageli. (10/58. ‘Entstehung und Begriff der Naturhist. Art’ 1865 page 22.) It is indeed difficult to avoid this conclusion, if we admit the view, which seems highly probable, that the conjugation of the Algae and of some of the simplest animals is the first step towards sexual reproduction; and if we further bear in mind that a greater and greater degree of differentiation between the cells which conjugate can be traced, thus leading apparently to the development of the two sexual forms. (10/59. See the interesting discussion on this whole subject by O. Butschli in his ‘Studien uber die ersten Entwickelungsvorgange der Eizelle; etc. 1876 pages 207-219. Also Engelmann “Ueber Entwickelung von Infusorien” ‘Morphol. Jahrbuch’ B. 1 page 573. Also Dr. A. Dodel “Die Kraushaar-Algae” ‘Pringsheims Jahrbuch f. Wiss. Bot.’ B. 10.) We have also seen that as plants became more highly developed and affixed to the ground, they would be compelled to be anemophilous in order to intercross. Therefore all plants which have not since been greatly modified, would tend still to be both diclinous and anemophilous; and we can thus understand the connection between these two states, although they appear at first sight quite disconnected. If this view is correct, plants must have been rendered hermaphrodites at a later though still very early period, and entomophilous at a yet later period, namely, after the development of winged insects. So that the relationship between hermaphroditism and fertilisation by means of insects is likewise to a certain extent intelligible.
Why the descendants of plants which were originally dioecious, and which therefore profited by always intercrossing with another individual, should have been converted into hermaphrodites, may perhaps be explained by the risk which they ran, especially as long as they were anemophilous, of not being always fertilised, and consequently of not leaving offspring. This latter evil, the greatest of all to any organism, would have been much lessened by their becoming hermaphrodites, though with the contingent disadvantage of frequent self-fertilisation. By what graduated steps an hermaphrodite condition was acquired we do not know. But we can see that if a lowly organised form, in which the two sexes were represented by somewhat different individuals, were to increase by budding either before or after conjugation, the two incipient sexes would be capable of appearing by buds on the same stock, as occasionally occurs with various characters at the present day. The organism would then be in a monoecious condition, and this is probably the first step towards hermaphroditism; for if very simple male and female flowers on the same stock, each consisting of a single stamen or pistil, were brought close together and surrounded by a common envelope, in nearly the same manner as with the florets of the Compositae, we should have an hermaphrodite flower.
There seems to be no limit to the changes which organisms undergo under changing conditions of life; and some hermaphrodite plants, descended as we must believe from aboriginally diclinous plants, have had their sexes again separated. That this has occurred, we may infer from the presence of rudimentary stamens in the flowers of some individuals, and of rudimentary pistils in the flowers of other individuals, for example in Lychnis dioica. But a conversion of this kind will not have occurred unless cross-fertilisation was already assured, generally by the agency of insects; but why the production of male and female flowers on distinct plants should have been advantageous to the species, cross-fertilisation having been previously assured, is far from obvious. A plant might indeed produce twice as many seeds as were necessary to keep up its numbers under new or changed conditions of life; and if it did not vary by bearing fewer flowers, and did vary in the state of its reproductive organs (as often occurs under cultivation), a wasteful expenditure of seeds and pollen would be saved by the flowers becoming diclinous.
A related point is worth notice. I remarked in my Origin of Species that in Britain a much larger proportion of trees and bushes than of herbaceous plants have their sexes separated; and so it is, according to Asa Gray and Hooker, in North America and New Zealand. (10/60. I find in the ‘London Catalogue of British Plants’ that there are thirty-two indigenous trees and bushes in Great Britain, classed under nine families; but to err on the safe side, I have counted only six species of willows. Of the thirty-two trees and bushes, nineteen, or more than half, have their sexes separated; and this is an enormous proportion compared with other British plants. New Zealand abounds with diclinous plants and trees; and Dr. Hooker calculates that out of about 756 phanerogamic plants inhabiting the islands, no less than 108 are trees, belonging to thirty-five families. Of these 108 trees, fifty-two, or very nearly half, have their sexes more or less separated. Of bushes there are 149, of which sixty-one have their sexes in the same state; whilst of the remaining 500 herbaceous plants only 121, or less than a fourth, have their sexes separated. Lastly, Professor Asa Gray informs me that in the United States there are 132 native trees (belonging to twenty-five families) of which ninety-five (belonging to seventeen families) “have their sexes more or less separated, for the greater part decidedly separated.”) It is, however, doubtful how far this rule holds good generally, and it certainly does not do so in Australia. But I have been assured that the flowers of the prevailing Australian trees, namely, the Myrtaceae, swarm with insects, and if they are dichogamous they would be practically diclinous. (10/61. With respect to the Proteaceae of Australia, Mr. Bentham ‘Journal of the Linnean Society Botany’ volume 13 1871 pages 58, 64, remarks on the various contrivances by which the stigma in the several genera is screened from the action of the pollen from the same flower. For instance, in Synaphea “the stigma is held by the eunuch (i.e., one of the stamens which is barren) safe from all pollution from her brother anthers, and is preserved intact for any pollen that may be inserted by insects and other agencies.”) As far as anemophilous plants are concerned, we know that they are apt to have their sexes separated, and we can see that it would be an unfavourable circumstance for them to bear their flowers very close to the ground, as their pollen is liable to be blown high up in the air (10/62. Kerner ‘Schutzmittel des Pollens’ 1873 page 4.); but as the culms of grasses give sufficient elevation, we cannot thus account for so many trees and bushes being diclinous. We may infer from our previous discussion that a tree bearing numerous hermaphrodite flowers would rarely intercross with another tree, except by means of the pollen of a distinct individual being prepotent over the plants’ own pollen. Now the separation of the sexes, whether the plant were anemophilous are entomophilous, would most effectually bar self-fertilisation, and this may be the cause of so many trees and bushes being diclinous. Or to put the case in another way, a plant would be better fitted for development into a tree, if the sexes were separated, than if it were hermaphrodite; for in the former case its numerous flowers would be less liable to continued self-fertilisation. But it should also be observed that the long life of a tree or bush permits of the separation of the sexes, with much less risk of evil from impregnation occasionally failing and seeds not being produced, than in the case of short-lived plants. Hence it probably is, as Lecoq has remarked, that annual plants are rarely dioecious.
Finally, we have seen reason to believe that the higher plants are descended from extremely low forms which conjugated, and that the conjugating individuals differed somewhat from one another,—the one representing the male and the other the female—so that plants were aboriginally dioecious. At a very early period such lowly organised dioecious plants probably gave rise by budding to monoecious plants with the two sexes borne by the same individual; and by a still closer union of the sexes to hermaphrodite plants, which are now much the commonest form. (10/63. There is a considerable amount of evidence that all the higher animals are the descendants of hermaphrodites; and it is a curious problem whether such hermaphroditism may not have been the result of the conjugation of two slightly different individuals, which represented the two incipient sexes. On this view, the higher animals may now owe their bilateral structure, with all their organs double at an early embryonic period, to the fusion or conjugation of two primordial individuals.) As soon as plants became affixed to the ground, their pollen must have been carried by some means from flower to flower, at first almost certainly by the wind, then by pollen-devouring, and afterwards by nectar-seeking insects. During subsequent ages some few entomophilous plants have been again rendered anemophilous, and some hermaphrodite plants have had their sexes again separated; and we can vaguely see the advantages of such recurrent changes under certain conditions.
Dioecious plants, however fertilised, have a great advantage over other plants in their cross-fertilisation being assured. But this advantage is gained in the case of anemophilous species at the expense of the production of an enormous superfluity of pollen, with some risk to them and to entomophilous species of their fertilisation occasionally failing. Half the individuals, moreover, namely, the males, produce no seed, and this might possibly be a disadvantage. Delpino remarks that dioecious plants cannot spread so easily as monoecious and hermaphrodite species, for a single individual which happened to reach some new site could not propagate its kind; but it may be doubted whether this is a serious evil. Monoecious plants can hardly fail to be to a large extent dioecious in function, owing to the lightness of their pollen and to the wind blowing laterally, with the great additional advantage of occasionally or often producing some self-fertilised seeds. When they are also dichogamous, they are necessarily dioecious in function. Lastly, hermaphrodite plants can generally produce at least some self-fertilised seeds, and they are at the same time capable, through the various means specified in this chapter, of cross-fertilisation. When their structure absolutely prevents self-fertilisation, they are in the same relative position to one another as monoecious and dioecious plants, with what may be an advantage, namely, that every flower is capable of yielding seeds.