The origin of floral structures through insect and other agencies

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Preface

The belief that we must look mainly to the environment as furnishing the influences which induce plants to vary in response to them — whereby adaptive morphological (including anatomical) structures are brought into existence— appears to be reviving. To illustrate the progress of this belief, I will give a few cases.

In 1795, GeofFroy Saint Hilaire "seems to have relied chiefly on the conditions of life, or the ' monde ambiant,' as the cause of change." *

In 1801, Lamarck " attributed something to the direct action of the physical conditions of life " as the means of modification, "something to the crossing of already existing forms, and much to use and disuse."

In 1831, Mr. Patrick Matthew (who, like Dr. W. C. Wells in 1818, anticipated Mr. Darwin in the theory of "natural selection") "seems to have attributed much influence to the direct action of the conditions of life."

* I quote from Mr. Darwin's "Historical Sketch" in bis Origin of Species, 6th ed., 1878.

VI PREFACE.

In 1844, the "Vestiges of Creation" appeared. The author suggests that " impulses " were imparted to the forms of life, on the one hand advancing them, and on the other hand tending to modify organic structures in accordance with external circumstances ; the effects thus produced by the conditions of life being gradual.

In 1852, Mr. Herbert Spencer " attributed the modifications [of species] to the change of circumstances."

In 1859, "The Origin of Species" appeared. Mr. Darwin did not at first seem to lay so much stress as his predecessors upon the action of the environment as a cause, for he says : " It is curious how largely my grandfather, Dr. Erasmus Darwin, anticipated the views and erroneous grounds of opinion of Lamarck." Again, in speaking of the constancy of some varieties, he says, " Such considerations incline me to lay less weight on the direct action of the surrounding conditions, than on a tendency to vary, due to causes of which we are quite ignorant." * He had, however, previously said, " Changed conditions of life are of the highest importance in causing variability. ... It is not probable that variability is an inherent and necessary contingent under all circumstances." f

With regard to my own opinion, having been early and greatly interested in Paley's "Natural Theology," as well as the "Vestiges" when Mr. Darwin's work

* Or. of Sp., p. 107. t I^id., p. 31. See also Desc. of Man, ii., p. 388.

PREFACE. Vll

appeared, the great difficulties I felt in accepting natural selection as any real origin of species lay, first, in the seeming impossibility of the histological minutige of the organs in adaptation having been selected together; and, secondly, in the idea that all those wonderful and "purposeful" structures which Paley thought could only have been " designed," could be the ultimate result of any number of accidental and apparently at first " purposeless " variations. In a broad sense natural selection seemed obviously true ; for Geology had revealed the fact that the world had been peopled over and over again by old forms dying out and new forms coming in ; so that although it might account for the extinction of the former, it did not seem to me capable to account for the origin of the latter. I, therefore, still looked to the environment as affording a better clue to the source of variations.*

In 1869, when watching a large humble-bee hanging on to the dependent stamens of Epilohiutn angustifolium, the idea first occurred to me that insects themselves might be the real cause of many peculiarities in the structure of flowers. The thought passed through my mind that the way the stamens hung down might perhaps have become an hereditary effect from the repeatedly applied weight of the bees.

In 1877, I advanced this idea as a speculation

* See Letter to Nature, vol. v., p. 123.

Vlll PREFACE.

when suggesting the origin of nectaries and irregularities of flowers in my paper on " Self-fertilisation of Flowers." *

In 1880, Mr. A. R. Wallace reviewed Dr. Aug. Weismann's " Studies in the Theory of Descent." f In this work the author says : " According to my view, transmutation by purely internal causes is not to be entertained. . . . The action of external inciting causes is alone able to produce modifications." Mr. Wallace adds that he had "arrived at almost exactly similar conclusions."

In 1881, when reviewing Paul Janet's work on " Final Causes/' ^ I took occasion to remark that " 1 regarded the environment as by far the most important "cause" of variations, in that it influences the organism, which, by its inherent but latent power to vary, responds to the external stimulus, and then varies accordingly."

In 1881, appeared the first really systematic treatise that I know of, by Dr. C. Semper, § which dealt with the orioin of variations in animals as beinor referable to the environment.

In 1884, Dr. A. de Bary's " Comparative Anatomy of the Vegetative Organs of the Phanerogams and Ferns,"

* Trans. Lin. Soc, 2nd ser., Bot., vol. i., p. 317. t Nature, xxii., p. 141. J Modern Revieiv, 1881, p. 53.

§ The Natural Conditions of Existence as they affect Animals," Intern. Sci. Ser., vol. xxxi.

PREFACE. IX

was published in English. In the Introduction, the author writes as if it were a perfectly well understood thing that species have arisen by adaptations to the influences of the environment.*

In 1886, Mr. Herbert Spencer contributed two articles on " The Factors of Organic Evolution " to the Nineteenth Century.'] In these he showed, from many passages in Mr. Darwin's works, especially "Animals and Plants under Domestication" and in his later volumes, that he became much more favourably inclined to the belief that the effects of the environment were accumulative, and that in the course of some generations the variations set up tended to cease and become fixed. Mr. Spencer particularly notes the change of view, as illustrated by the expression " little doubt " being replaced by " no doubt " in the following sentence : " I think there can be no doubt that use in our domestic animals has strengthened and enlarged certain parts, and disuse diminished them ; and that such modifications are inherited." % It may be added that in "The Cross and Self Fertilisation of Flowers" (1876), and in "Forms of Flowers" (1877), Mr. Darwin makes many observations upon the effects of the external conditions upon plants as influencing and modifying them in various ways. It is curious to note that the three influences upon which Lamarck laid

X "Use" and "disuse" in animals corresponds to what I have called " hypertrophy " and " atrophy " in plants, in this work.

X PREFACE.

emphasis are just those which Mr. Darwin himself latterly, though often indirectly perhaps, laid stress upon in his experiments, viz. crossing, use and disuse, and the physical conditions of life.

In 1886, also appeared an article in Nature, entitled, " Plants considered in Relation to their Environment." It was not signed, but the author alludes to the external conditions as bringing about all sorts of changes in the vegetative system. He stops short of discussing floral structures.

In 1886, Dr. Vines' " Physiology of Plants" appeared. After discussing various views and theories of reproduction, he observes, that " variability was first induced as the response of the organism to changes in the conditions of life." * . . . We conclude, then, that the production of varieties is the result of the influence of the conditions of life, t

In the last page of his work. Dr. Vines calls attention to Naegeli's view as follows : " Naegeli suggests, and his suggestion is worthy of serious consideration, that there is an inherent tendency to a higher organisation, so that each succeeding generation represents an advance, ... as in cases of what is termed saltatory evolution." Thus,

* Page 676. Dr. Vines here uses almost identically the same words as myself in 1881. I have just found that Mr. St. G. Mivart said much the same in 1870, Genesis of Species, p. 269. See also 0. Schmidt's Doctrine of Descent and Darwinism, p. 175.

t Page 679.

PREFACE. XI

while Mr. Darwin seems at last to have tacitly accepted Lamarck's ideas, at least to a considerable extent, we have here a return in 1887 to the views of the author of the " Vestiges " of 1884.

1888. I have attempted in the present work to return to 1795, and to revive the "Monde ambiant" of Geoffroy Saint Hilaire, as the primal cause of change. My object is to endeavour to refer every part of the structures of flowers to some one or more definite causes arising from the environment taken in its widest sense. To some extent the attempt must be regarded as speculative ; and, therefore, any deductive or d priori reasonings met with must be considered by the reader as being suggestive only.

Contents

CHAPTKR

PAOE

I. General Principles ... ... ••• ••• 1

Chapter I. General Principles

Introductory. — Mucli bas been written on the structure of flowers, and it migbt seem almost superfluous to attempt to say anything more on the subject ; but it is only within the last few yeare that a new literature has sprung up, in which the authors have described their observations and given their interpretations of the uses of floral mechanisms, more especially in connection with the processes of fertilisation.

Moreover, there is a considerable amount of scattered literature on special points which seems never to have been collated, so as to show the relative significance of the different classes of observations to which the authors have devoted themselves respectively. The consequence is, that, good as each in itself may be, it often requires the help of other classes of facts to enable one to fully elucidate any question to be discussed.

Now, the primary object of the first really scientific study of plants was their classification, and no longer with the sole view of ascertaining the real or imaginary medicinal uses of herbs ; as had been the case in Gerarde's time, when a botanist and a herbalist were one and the same.

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Systematic botanists, however, have hitherto invariably contented themselves with observing differences of structure only; and paid little or no attention to the "why" and the " wherefore " of the differences they seized upon as being more or less important for the purpose of distinguishing species. When, however, the desirability of a more thorough knowledge of the origin of parts of plants as interpreting morphological characters was felt, developmental history began to be studied ; a method strongly insisted upon by Schleiden, for example ; and the most elaborate result of this method of investigation is undoubtedly Payer's Traite d' Organog^nie Comparee de la Fleur, published in 1857: but if it be thought sufficient to limit the study of flowers to tracing their morphological development alone, one soon begins to see that it is far from being so, and, taken by itself, it may lead one into false interpretations, so that to the study of development must be added that of anatomy. To Ph. van Tieghem we are indebted for an elaborate treatise, entitled Becherches sur la Structure du Pistil et sur VAnatomee Comparee de la Fleur (1871), dealing with the more minute details of floral structures. This treatise, however, still leaves much to be desired.

Besides these methods, analogy and especially teratology furnish assistance of no mean value. Here we are especially indebted to Dr. M. T. Masters for his standard work on Teratology.^

Now, any one of these methods taken alone would be insufficient, and in many cases would be far from thoroughly accounting for particular points under consideration.

Hence to arrive at a complete interpretation of the origin of every sort of structure to be found in flowers, it can only

* A German edition, Tflanzen Teratologic, ed. Tammer, 1886, has numerous additions.

GENERAL PHINCIPLES.

be done by calling in the aid of each and all these methods to the very utmost extent possible.

Lastly, to attempt any theoretical exposition of the evolutionary history of flowers, considerable caution is required ; for the causes of variation are generally so obscure, the chances of seeing them in activity so small, and experimental methods of verification well-nigh impossible, that speculations on this subject cannot altogether escape the bounds of hypothesis so as to become demonstrable facts. Hence observations which I shall make later on, with reference to the origin of existing floral structures, will not profess to be anything more than theoretical, and at most only a " working hypothesis " for future investigations.

The Structure of a Typical Flower. — Before considering how the innumerable forms of flowers deviate from one another, it is advisable to assume some typical form or plan as a preliminary basis to start from, or to which all flowers, if possible, may be referred as a standard. It would be quite possible to adopt some kind of flower as it exists in nature, but as this would be arbitrary, it may be better to take an ideal type, and the diagram (Fig. 1) will answer the purpose, in which the outermost circle is supposed to represent a cross section of the five Sepals constituting the Calyx. The second circle is that of the five Petals of the Corolla. Tlie third stands for the Anthers of the five Stamens superposed to the sepals ; the fourth being those of five Stamens superposed to the petals. These two whorls of stamens together

Fig. 1.— Diagram of a typical flower.

constitute the Androecium. Lastly, there are represented two * whorls of Carpels forming the Gynoecium j or Pistil. The outermost wliorl of carpels is superposed to the sepals, the innermost to the petals.

There may be additional structures in flowers, such as disks, honey-glands, etc. ; but as these, when they occur on the floral-receptacle, are merely cellular protuberances and form no part of the floral whorls proper — not being folia?' in their origin — they may be omitted, especially as their position is by no means constantly the same in all flowers. J

The Principles op Yaeiation. — Having thas assumed an ideal type, we may at once consider the " Principles of Variation," as I propose to call them, in accordance with which the different members of flowers can be altered; so that by means of various combinations of these principles all the flowers in the Vegetable Kingdom can be brought under this one fundamental plan.

There are five principles which require special consideration. They are usually designated by the terms Number, Arrangement, Cohesion, Adhesion, and Form.

" Number " refers to the number of whorls and the number of parts in each whorl. If two or more whorls contain the same number of parts or be multiples of one another, they are said to be " symmetrical " or " isomerous." If they differ in the number of parts they are " unsymmetrical " or '' anisomerous."

"Arrangement" refers to the relative positions of the

* Why I assume two whorls for the pistil, instead of 07ie only, as is generally done, will be understood hereafter, I have since found that Robert Brown came to the same conclusion (Col. Works, i. 293).

t I adopt the spelling Gynoscium for the sake of uniformity ; it may be regarded as a shortened form of Gyncecoecium.

;J: I do not here allude to certain glandular structures, which may be the homologues of arrested organs.

GENERAL PRINCIPLES. 5

different whorls, as well as of those of the indivddual members of the whorls with regard to each other,

" Cohesion " signifies the union of parts of any, but of the same whorl. The original or ancestral condition of the parts composing every whorl is presumed, on the principles of evolution, to have been one of entire freedom ; so that the members w^ere as completely separate or free as, for example, they are in a Buttercup. Reversions to this condition of freedom may occur, and then the process is called " dialysis ; " as in the case of a polypetalous CamimnuJa occasionally cultivated as a garden plant.

" Adhesion " signifies the union of parts of different whorls ; as well as that between the ovary and the receptacular tube, constituting the so-called inferior ovary. I regard adhesion as representing a more advanced or a more highly differentiated state than that of cohesion. Reversions may occur by " solution," which brings about a freedom of parts normally united, as in the abnormal cases of Apples, double Saxifrage, members of the U'mbeUifer<T, etc., which have all their parts perfectly free, though with inferior ovaries under ordinary circumstances.

" Form " refers to the shape of the organs ; such as those of sepals and petals upon which generic characters are so often founded, the length of the filaments, and other peculiarities. If all the parts of any whorl be exactly alike, it is said to be " regular ; " if not, the w^horl wnll be " irregular."

The above five principles constitute the most important in accordance with which Nature has brought about the infinite diversity which exists in the Floral world. There are minor distinctions, hereafter to be considered, such as colours, scents, etc. ; but they are of less importance in investigating the causes at work which have evolved specific and generic differences amongst flowering plants.

There is another point which may be here noticed. That a flower-bud is a metamorphosed leaf -bud is now an accepted fact ; but an obvious difference between them consists in the arrested state of the axis of the former, constituting the floral receptacle ; and the question arises, how has this arrest been brought about ? Like all other peculiarities of structure to be described, I would attribute the arrest primarily to the altered nature of the foliar organs on becoming members of flowers. Thus, a Fir-cone and a Buttercup are arrested branches ; but when the parts of a flower are reduced in number, and instead of being in a continuous spiral are grouped in " compressed cycles," * I would then (hypothetically) attribute this further reduction of the axis, as well as other features hereafter to be described, to the irritation of insects in probing for juices, and causing nectaries to be formed, f It is the commonest thing for leaf - buds to be arrested, and sometimes metamorphosed as well, by insects puncturing and depositing their eggs in them. Such may be seen on the germinal shoots of Yews, Thyme, and in certain kinds of Oak-galls, etc. In all such cases the immediate effect is the total arrest of the axis, though the leaves may be but slightly altered, as in the Yew. How the various metamorphoses of leaves into petals, etc., has followed will be discussed later on.

It must not be forgotten, however, that the tendency to shorten the axis is primarily, in some cases, due to the altered structure of the foliar organs, as in Gymnosperms ; whereby they undertake the reproductive functions. At the same time, I think insects have had a good deal to do with it, in many other phanerogams, which have but few parts to their whorls.

Each of the above principles must now be considered in detail.

* See pp. 41, 42. f See p. 140, seqq.

CHAPTEE 11.

THE PRINCIPLE OF NUMBER.

Number — Genehal Observations. — The first principle of Variation to be considered is that of the number of parts composing the different whorls of flowers. There are good reasons for considering that six whorls, consisting of five, four, three, or two parts each, as the case may be, should be regarded as the theoretically complete number of verticils of any flower.

Anatomical investigations prove that the rule is for the pedicel to contain — at least, immediately below the flower, — if the latter be pentamerous, ten more or less distinct fibrovascular cords, five of which belong to the sepals and five to the petals; if it be hexamerous, there will be six cords, three for each whorl of the perianth. Each of these cords can give rise by branching, first, to a whorl of stamens and subsequently to a whorl of carpels, furnishing at least two marginal and one dorsal cord for each of the latter.

In many flowers bnth whorls of stamens are present, and the androecium is then isomerous with the entire perianth. More often one whorl is arrested, and then it may be either one ; but most usually it is the petaline. On the other hand, the calycine may not be developed as in Primroses, Rhamnus^ etc.

The absence of the petaline stamens is possibly attributable to the law of compensation, in consequence of the enhanced growth of the corolla, the petals thereby abstracting the nourishment that would be required by the stamens superposed to them.

That the number of staminal whorls should be two in verticillate flowers, i.e., equal to the perianth, is apparent from the fact that two whorls prevail in Monocotyledons and are not at all uncommon in Dicotyledons ; and when the petaline whorl alone exists, as in Primulacece and Myrsineoe, calycine staminodia are sometimes present which tend to restore the complete number, as in the genus Samolus in the former and in the tribe Theophrastece of the latter order.

The reduction of the number of carpels is very generally carried to a greater extent than that oi the stamens. Assuming two complete whorls of carpols as the primitive number, not only are both rarely to be found in the same flower, as in Butomus, but a portion only of one whorl is commoner than even a single entire whorl. Thus, two are characteristic of Cruciferce, Polygaleoe, and of most of the gamopetalous orders ; while one carpel only prevails in Leguminosoe and elsewhere.

That the absence of parts of, as well as of entire whorls of flowers as they now exist does not represent primitive conditions, is testified to by the frequent occurrence of various kinds of degradations, such as were alluded to above in the case of the staminodia of Samolus, etc. Thus, with regard to the calyx, it is a noticeable fact that when the inflorescence consists of a large number of flowers, especially if small and closely compacted, there is a strong tendency for the sepals to become partially arrested and remain rudimentary, or even not to be developed at all. This is particularly observable in some epigynous orders as Umhelliferce, Araliacece, Caprifoliacece, Rubiaceoe, Covipositce, etc.

THE PRINCIPLE OF NUMBEPt. 9

The degradation of the corolla is likewise very common. As its enhancement has been due to insect agency, so, conversely, its reduction in size, colour, etc., is presumably often the result of the neglect of insects. Consequently inconspicuousness becomes a characteristic feature of self-fertilising flowers. By increased degradation the corolla may disappear entirely, as in Sagina apetala, some cleistogamous flowers, and in the Incomjjleto' generally. Such degradation is also characteristic of wind-fertilised flowers.

As both calyx and corolla maybe degraded and disappear, so may the stamens and carpels, unisexual and neuter flowers beiug the result.

Further observations, however, will be made upon this subject when treating of the several whorls respectively, and especially when discussing the phenomenon of degeneracy.

The Oeigin of Different Numbers. The number of parts constituting the floral whorls is, without doubt, primarily due to phyllotaxis ; and therefore, to understand why certain numbers, such as fives, fours, and threes prevail, it is needful to give some preliminary remarks on the principles of leaf arrangement. It has long been observed that these are referable to two kinds — one in which two or more leaves are situated on the same node, when they are decussate,* that is to say, each pair or whorl of three or more leaves alternates in position with the whorl immediately above and below it. The second system is when only one leaf occurs at a node ; the leaves are then said to be alternate. The leaves are then arranged on a continuous spiral line, and can be represented by the fractions of the well-known series 4-, i, -|, f , tj, /y, etc. Of these fractions the denominator represents the number of

* Rare exceptions occur in species of Poiamogeton, in which alternate internodes between the distichously arranged leaves are suppressed, so that they become opposite, but are all in the same plane.

leaves in a " cycle," and tlie numerator the number of times a spiral line, passing through the position of the leaves, coils round the stem in forming a cycle ; thus, with the f arrangement, any leaf being taken as number 1, the sixth leaf will be first that falls in the same vertical line with number 1, the leaves 1 to 5 constituting the cycle. The portion of the spiral line which passes through the leaves 1 to 6 coils twice round the stem, and if projected on a plane forms two circles. The angular distance, measured from the centre of the stem or circles, between any t^70 successive leaves is always found by multiplying 360° by the fraction : thus f X 360" = 144'^.

The interpretation, therefore, of the prevailing numbers 3 and 5 in floral whorls is that they are, in most cases, cycles of the ^ or f types respectively ; while 4 is primarily due to the union of two pairs of opposite and decussate parts,

6, 8, 10 are merely the doubles of the preceding, and mostly represent two pairs of w^horls or cycles blended together, thus forming one whorl, or so closely approximated as scarcely recognizable as two ; though the rare number 8, in some cases, such as Nigella, and HeUeborus foetidus, may represent a cycle of the f type. Similarly, the still rarer numbers

7, 9, and 11 in flowers correspond to the absence of these numbers as denominators of any fractions of the above prevailing series.

With the exception of dimerous and tetramerous whorls, all the rest are presumably due to alternate arrangements. Now, opposite leaves present a more primitive type than alternate ; that this is so, is not only reasonable from the primordial condition of the cotyledons of Dicotyledons, but the transition from an opposite to an alternate condition maybe often witnessed en rapidly growing stems, such as of the Jerusalem Artichoke. Whenever this plant bears opposite leaves below, and alternate leaves above, it will be found that the arrangement of the latter is almost invariably represented by the f type. It is secured by developing internodes between the two opposite leaves of each pair, and by shifting their positions so as to acquire ultimately an angular divergence of 144°.*

The feature to be especially observed in the transitions from opposite to alternate arrangements is the order in which the opposite leaves separate so as to assume successive positions on the continuous spiral line passing through their insertions, when they have become alternate. This will be understood from the accompanying diagram, in which the numbers represent the order which the leaves will ultimately assume on the f tj^pe ; though they are placed as if still opposite and decussate. The numbers 1 and 2, 3 and 4, 5 and 6, etc., represent the successive pairs of opposite leaves, the arrows showing the direction of the spiral.

It will be at once observed that the numbers 6, 9, 14, and 22 are in the same row, and correspond to the divergences f, ^, -i\, /y. No. 17 falls into the 3 8 11 series ^-, and completes the second cycle of that type from No. 1.

It may be observed here, as occasion will arise for a fuller allusion to the ^'^" ^' significance of the fact, that, with the sole exception of the

* I have fully explained this in my paper, On the Variations of the Angular Divergences of the Leaves of Helianthus Tuberosus, Tran?. Lin. Soc, vol. xxvi., p. 647. See also On the Origin of the Prevailing Systems of Fhyllotaxisf I.e., 2nd series, vol. i. p. 37.

i

T2 THE STRUCTURE OF FLOWERS.

distichous or ^ type, every other arrangement always has three leaves in every projected circle.

It may be noticed that No. 4 not only does not occur in the row 1, 6, 9, etc., — a fact which corresponds with the rarity of a ternary arrangement occurring amongst flowers of Dicotyledons, — but in order to fall over No. 1 it would have to pass through 270°, that is from right to left, practically an impossibility ; so that when " threes " are met with in Dicotyledons we must look for some other interpretation than to refer them to the ^ type.

The numbers 7 and 11, as stated, are extremely rare in flowers, and this is in accordance with the fact that they belong to another series, viz. ^, ^, f , y\, y\, etc., which is rarely represented in nature. Examples, however, will be found in the leaves of Sedum reflexum, on some branches of Araucaria imhricata, and sometimes in the Jerusalem Artichoke. In the last case, it will be discovered that the heptastichous or ■f- type arises out of verticils of threes, in precisely the same way as the pentastichous or f type does from an opposite and decussate arrangement ; and as there are always four leaves in every projected circle, for every type of this series, excepting the first or ^-, it can only occur where the leaves are narrow or are short, or do not occupy too much space so as to overshadow one another.