Weismann August
Studies in the Theory of Descent, Volume I
V. Biological Value of Special Markings
The following questions now present themselves: Have the markings of caterpillars any biological value, or are they in a measure only sports of nature? Can they be considered as partially or entirely the result of natural selection, or has this agency had no share in their production?
The problem here offers itself more distinctly than in any other group of living forms, because it presents an alternative without a third possibility. In other words, if it is not possible to show that larval markings have a distinct biological significance, there remains only for their explanation the assumption of a phyletic force, since the direct action of the environment is insufficient to account for such regularity of development throughout a series of forms. The explanation by sexual selection is excluded ab initio, since we are here concerned with larvæ, and not with reproductive forms.141
The biological significance of marking – if such significance it possess – will be most easily investigated by examining whether species with similar markings have any conditions of life in common which would permit of any possible inference as to the significance of the markings.
Among the Sphingidæ we find four chief forms of marking; (1) complete absence of all marking; (2) longitudinal stripes; either a simple subdorsal or this together with a spiracular and dorsal line; (3) oblique stripes; (4) eye-spots and ring-spots, single, paired, or in complete rows.
Now if we consider in which species these four kinds of marking are of general occurrence, not only in the small group of the Sphingidæ but in the whole order Lepidoptera, we shall arrive at the following results: —
1. Complete absence of marking, so common in the larvæ of other insects, such as the Coleoptera, is but seldom found among Lepidopterous caterpillars.
To this category belong all the species of Sesiidæ (the genera Sesia, Trochilia, Sciapteron, Bembecia, &c.), the larvæ of which, without exception, are of a whitish or yellowish colour, and live partly in the wood of trees and shrubs and partly in the shoots of herbaceous plants. Subterranean larvæ also, living at the roots of plants, such as Hepialus Humuli at the roots of hop, and H. Lupulinus at those of Triticum Repens, possess neither colour nor marking. These, like the foregoing, are yellowish-white, evidently because they are deprived of the influence of light.142 The larvæ of certain small moths, such as Tortrix Arbutana and Pomonana, which live in fruit, and many case-bearing Tineina, are likewise without marking and devoid of bright colour, being generally whitish. Many of the small caterpillars which feed exteriorly are also – so far as my experience extends – without definite markings, these being among the most minute, such as the greenish leaf-mining species of Nepticula. It is among the larger species that we first meet with longitudinal and oblique stripes. Eye-spots do not occur in any of these larvæ, a circumstance of the greatest importance for the biological significance of this character, as will be shown subsequently. The small size of the caterpillars cannot be the sole cause of the absence of such eye-spots, since in young Smerinthus caterpillars one centimeter long, the oblique stripes are beautifully developed, and the larvæ of many of the smaller moths considerably exceed this size. The surface of these caterpillars therefore, i. e., the field on which markings are displayed, is not absolutely too small for the development of such a character.
Besides the larvæ of the Micro-lepidoptera and of those species living in the dark, there is also a complete absence of marking in the young stages of many caterpillars. Thus, all the Sphingidæ of which I have been able to observe the development, show no markings immediately after emergence from the egg; in many they appear very soon, even before the first moult, and, in other species, after this period.
2. The second category of markings, longitudinal stripes, is very widely distributed among the most diverse families. This character is found among the larvæ of butterflies, Sphingidæ, Noctuæ, Micro-lepidoptera, &c., but in all these groups it is absent in many species. This last fact is opposed to the view that this character is purely morphological, and leads to the supposition that it may have a biological value, being of service for the preservation of the individual, and therefore of the species.
I find that such marking is of service, stripes extending longitudinally along the upper surface of the caterpillar generally making the latter less conspicuous. This, of course, does not hold good under all circumstances, since there are many species with very striking colours which possess longitudinal stripes. Let us consider, however, a case of adaptive colouring, such as a green caterpillar, which, on this account only, is difficult to see, since it accords with the colour of the plant on which it lives. If it is a small caterpillar, i. e., if its length and thickness do not considerably exceed that of the parts of its food-plant, it can scarcely be better concealed – stripes would hardly confer any special advantage unless the parts of the plant were also striped. But the case is quite different if the caterpillar is considerably larger than the parts of the plant (leaves, stalks, &c.). The most perfect adaptive colouring would not now prevent it from standing out conspicuously as a larger body, among the surrounding parts of the plants. It must be distinctly advantageous therefore to such a caterpillar to be striped, since these markings to a certain extent divide the large body into several longitudinal portions – they no longer permit it to be seen as a whole, and thus act more effectively than mere assimilative colouring in causing it to escape detection. This protection would be the more efficacious if the stripes resembled the parts of the plant in colour and size, such, for instance, as the lines of light and shadow produced by stalks or by long and sharp-edged leaves.
If this view be correct, we should expect longitudinal stripes to be absent in the smallest caterpillars, and to be present more especially in those species which live on plants with their parts similarly disposed, i. e., on plants with numerous thin, closely-growing stalks and grass-like leaves, or on plants with needle-shaped leaves.
It has already been mentioned that the smallest species are devoid of longitudinal striping. The larvæ of the Micro-lepidoptera show no such marking, even when they do not live in the dark, but feed either on the surface or in superficial galleries of the leaves (Nepticula, &c.), in which they must be exposed to almost as much light as when living on the surface. The fact that the subdorsal line sometimes appears in very young Sphinx-larvæ is explained, as has already been shown, by the gradual backward transference of adaptational characters acquired in the last stage of development.
It can easily be demonstrated that longitudinally striped caterpillars mostly live on plants, of which the general appearance gives the impression of a striped arrangement. We have only to consider in connection with their mode of life, any large group of adaptively coloured species marked in this manner. Thus, among the butterflies, nearly all the Satyrinæ possess larvæ conspicuously striped – a fact which is readily explicable, because all these caterpillars live on grasses. This is the case with the genera Melanargia, Erebia, Satyrus, Pararge, Epinephele, and Cænonympha, no species of which, so far as the larvæ are known, is without longitudinal stripes, and all of which feed on grasses. It is interesting that here also, as in certain Sphingidæ, some species are brown, i. e., adapted to the soil, whilst the majority are green, and are therefore adapted to living grass. Just as in the case of the Sphingidæ also, the brown species conceal themselves by day on the earth, whilst some of the green species have likewise acquired this habit. I have already shown how this habit originates from the increasing size of the growing larva, which would otherwise become too conspicuous, in spite of adaptive colour and marking. A beautiful confirmation of this view is found in the circumstance that only the largest species of Satyrus, such as S. Proserpinus, Hermione, Phædrus, &c., possess brown caterpillars. I should not be surprised if a more exact investigation of these species, which have hitherto been but seldom observed, revealed in some cases a dimorphism similar to that of the Sphingidæ; and I believe that I may venture to predict that the young stages of all these brown larvæ – at present quite unknown – are, as in the last-named group, green.
Besides the Satyrinæ, most of the larvæ of the Pierinæ and Hesperidæ possess longitudinal stripes, which are generally less strongly pronounced than in the former subfamily. Some of the Pierinæ live on Cruciferæ, of which the narrow leaves and thin leaf- and flower-stalks present nothing but a linear arrangement; other species of this group, however, feed on Leguminosæ (Lathyrus, Lotus, Coronilla, Vicia), and some few on broad-leaved bushes (Rhamnus). This last fact may appear to be opposed to the theory; but light lateral stripes, such for example, as those possessed by Gonepteryx Rhamni, can never be disadvantageous, and may be of use, even on large leaves, so that if we consider them as an inherited character, there is no reason for natural selection to eliminate them. In the case of caterpillars living on vetch, clover, and other Leguminosæ, it must not be forgotten that, although their food-plants do not present any longitudinal arrangement of parts, they always grow among grasses, the species feeding on such plants always resting between grass stems, and very frequently on the grass itself, so that they can have no better protective marking than longitudinal stripes. The striping of the Hesperidæ larvæ, which partly feed on grasses but mostly on species of Leguminosæ, can be explained in a similar manner.
It is not here my intention to go through all the groups of Lepidoptera in this manner. The instances adduced are quite sufficient to prove that longitudinal stripes occur wherever we should expect to find them, and that they really possess the biological significance which I have ascribed to them. That these markings are occasionally converted into an adaptive imitation of certain special parts of a plant, is shown by the larvæ of many moths, such for example as Chesias Spartiata, which lives on broom (Spartium Scoparium), its longitudinal stripes deceptively resembling the sharp edges of the stems of this plant.143
3. Oblique striping. Can the lilac and white oblique stripes on the sides of a large green caterpillar, such as those of Sphinx Ligustri; or the red and white, or white, black, and red stripes of Smerinthus Tiliæ and Sphinx Drupiferarum respectively, be of any possible use? Have we not here just one of those cases which clearly prove that such a character is purely morphological, and worthless for the preservation of the individual? Does not Nature occasionally sport with purposeless forms and colours; or, as it has often been poetically expressed, does she not here give play to the wealth of her phantasy?
At first sight this indeed appears to be the case. We might almost doubt the adaptive importance of the green ground-colour on finding coloured stripes added thereto, and thus – as one might suppose – abolishing the beneficial action of this ground-colour, by making the insect strikingly conspicuous. But this view would be decidedly incorrect, since oblique stripes are of just the same importance as longitudinal stripes. The former serve to render the caterpillar difficult of detection, by making it resemble, as far as possible, a leaf; they are imitations of the leaf-veins.
Nobody who is in the habit of searching for caterpillars will doubt that, in cases where the oblique stripes are simply white or greenish-white, it is extremely difficult to see the insect on its food-plant, e. g. S. Ocellatus on Salix; not only because it possesses the colour of the leaves, but no less because its large body does not present an unbroken green surface, which would bring it into strong contrast with the leaves, and thus arrest the attention. In the case of the species named, the coloured area of the body is divided by oblique parallel stripes, just in the same manner as a willow leaf. In such instances of course we have not presented to us any special imitation of a leaf with all its details – there is not a perfect resemblance of the insect to a leaf, but only an arrangement of lines and interspaces which does not greatly differ from the division of a leaf by its ribs.
That this view is correct is shown by the occurrence of this form of marking. It is on the whole rare, being found, besides in many Sphingidæ, in isolated cases in various families, but is always confined to those larvæ which live on ribbed leaves, and never occurring in species which feed on grasses or on trees with needle-shaped leaves. This has already been shown with respect to the Sphingidæ, in which the oblique stripes are only completely developed in the subfamilies Smerinthinæ and Sphinginæ. The species of Smerinthus all live on trees such as willows, poplars, lime, oak, &c., and all possess oblique stripes. The genus Anceryx also belongs to the Sphinginæ, and these caterpillars, as far as known, live on trees with needle-shaped leaves. The moths of this last genus are very closely allied to the species of Sphinx, not only in form and colour, but also in many details of marking. The larvæ are however different, this distinction arising entirely from their adaptation to needle-shaped leaves, the Sphinx caterpillars being adapted to ordinary foliage. The species of Anceryx, as has been already shown, are brown mixed with green, and never possess even a trace of the oblique stripes, but have a latticed marking, consisting of many interrupted lines, which very effectively serves to conceal them among the needles and brown bark of the Coniferæ.
Of the Sphinginæ living on plants with ordinary foliage, not a single species is without oblique stripes. I am acquainted with ten species of caterpillars and their respective food-plants, viz. Sphinx Carolina, Convolvuli, Quinquemaculata, Prini, Drupiferarum, Ligustri; Macrosila Rustica and Cingulata; Dolba Hylæus and Acherontia Atropos.
Besides among the Sphinginæ, oblique stripes occur in the larvæ of certain butterflies, viz. Apatura Iris, Ilia, and Clytie, all of which live on forest trees (aspen and willows), and are excellently adapted to the leaves by their green colour. In addition to these, I am acquainted with the larvæ of some few moths, viz. of Aglia Tau and Endromis Versicolora, both of which also live on forest trees.
Oblique stripes also occasionally occur in the smaller caterpillars of Noctuæ, Geometræ, and even in those of certain Pyrales, in all of which they are shorter and differently arranged. In these cases also, my theory of adaptation holds good, but it would take us too far if I attempted to go more closely into them. I will here only mention the extraordinary adaptation shown by the caterpillar of Eriopus Pteridis. This little Noctuid lives on Pteris Aquilina; it possesses the same green colour as this fern, and has double oblique white stripes crossing at a sharp angle on each segment, these resembling the lines of sori of the fern-frond so closely, that the insect is very difficult to perceive.
After all these illustrations it can no longer remain doubtful that the oblique stripes of the Sphingidæ are adaptive. But how are the coloured edges bordering these stripes in so many species to be explained?
I must confess that I long doubted the possibility of being able to ascribe any biological value to this character, which appeared to me only conspicuous, and not protective. Cases may actually occur in which the brightly coloured edges of the oblique stripes make the caterpillar conspicuous – just in the same manner as any marking may bring about a conspicuous appearance by presenting a striking contrast of colour. I am acquainted with no such instance, however. As a rule, in all well-adapted caterpillars, considering their colour in its totality, this is certainly not the case. The coloured edges, on the contrary, enhance the deceptive appearance by representing the oblique shadows cast by the ribs on the under-side of the leaf; all these caterpillars rest underneath the leaves, and never on the upper surface.
This explanation may, perhaps, at first sight appear far-fetched, but if the experiment be made of observing a caterpillar of Sphinx Ligustri on its food-plant, not immediately before one’s eyes in a room, but at a distance as under natural conditions, it will be found that the violet edges do not stand out brightly, but show a colour very similar to that of the shadows playing about the leaves. The coloured edges, in fact, produce a more effective breaking up of the large green surface of the caterpillar’s body, than whitish stripes alone. Of course if the insect was placed on a bare twig in the sun, it would be easily visible at a distance; the larva never rests in such a position, however, but always in the deep shadow of the leaves, in which situation the coloured edges produce their peculiar effect. It may be objected that the oblique white stripes, standing simply on a dark green ground-colour, would produce the same effect, and that my explanation therefore leaves the bright colouring of these edges still unaccounted for. I certainly cannot say why in Sphinx Ligustri these edges are lilac, and in S. Drupiferarum, S. Prini, and Dolba Hylæus red, nor why they are black and green in Macrosila Rustica, and blue in Acherontia Atropos. If we knew exactly on what plants these caterpillars fed originally, we might perhaps indulge in comparing with an artistic eye the shadows playing about their leaves, seeing in one case more red, and in another more blue or violet. The coloured stripes of the Sphingidæ must be regarded as the single strokes of a great master on the countenance of a human portrait. Looked into closely, we see red, blue, or even green spots and strokes; but all these colours, conspicuous when close, disappear on retreating, a general effect of colour being then produced, which cannot be precisely described by words.
Quite in accordance with this explanation, we see caterpillars with the brightest coloured stripes concealing themselves in the earth by day, and betaking themselves to their food-plants only in the dusk of the evening or dawn of morning and even during the night; i. e. in a light so faint that feeble colours would produce scarcely any effect. The bright blue of Acherontia Atropos, for example, would give the impression of oblique shadows without any distinctive colour.
It is precisely the case of this last caterpillar, which formerly appeared to me to present insurmountable difficulties to the explanation of the coloured stripes by adaptation, and I believed that this insect would have to be classed with those species which are brightly coloured because they are distasteful, and are avoided by birds. But although we have no experiments on this point, I must reject this view. Unfortunately, we know scarcely anything of the ontogeny of this caterpillar; but we know at least that the young larvæ (stage four) are greener than the more purely yellow ones of the fifth stage (which, however, are also frequently green), and we know further that some adults are of a dark brownish-grey, without any striking colours. From analogy with the dimorphism of the species of Chærocampa and Sphinx, fully considered previously, it must therefore be concluded that in this case also, a new process of adaptation has commenced – that the caterpillar is becoming adapted to the soil in and on which it conceals itself by day.144 An insect which acquires undoubted protective colours cannot, however, be classed with those which possess an immunity from hostile attacks.
That the coloured edges are correctly explained as imitations of the oblique shadows of the leaf-ribs, may also be proved from another point of view. Let us assume, for the sake of argument, that these coloured stripes are not adaptive, and that they have not been produced by natural selection, but by a hypothetical phyletic force. We should then expect to see them appear at some period in the course of the phyletic development – perhaps at first only in solitary individuals, then in several, and finally in all; but we certainly could not expect that at first single, irregular, coloured spots should arise in the neighbourhood of the oblique white stripes – that these spots should then multiply, and fusing together, should adhere to the white stripes, so as to form an irregular spot-like edge, which finally becomes formed into a straight, uniformly broad stripe. The phyletic development of the coloured edges takes place, however, in such a manner, the species of Smerinthus, as has already been established, showing this with particular distinctness. In S. Tiliæ the course of development can be followed till the somewhat irregular red border is formed. In the species of Sphinx this border has become completely linear. It is very possible that the ontogeny of S. Ligustri or Drupiferarum would reveal the whole process, although it may also be possible that owing to the contraction of the development, much of the phylogeny is already lost.
I have now arrived at the consideration of the last kind of marking which occurs in the Sphingidæ, viz.: —
4. Eye-spots and Ring-spots.– These markings, besides among the Sphingidæ, are found only in a very few caterpillars, such as certain tropical Papilionidæ and Noctuæ. I know nothing of the conditions of life and habits of these species, however, and without such knowledge it is impossible to arrive at a complete explanation.
With Darwin, I take an eye-spot to be “a spot within a ring of another colour, like the pupil within the iris,” but to this central spot “concentric zones” maybe added. In the Chærocampa larvæ and in Pterogon Œnotheræ, in which complete ocelli occur, there are always three zones – a central spot, the pupil, or, as I have called it, the “nucleus;” then a light zone, the “mirror;” and, surrounding this again, a dark zone (generally black), the “ground-area.”
As ring-spots I will consider those ocelli which are without the nucleus (pupil), and which are not therefore, strictly speaking, deceptive imitations of an eye, but present a conspicuous light spot surrounded by a dark zone.
Between these two kinds of markings there is, however, no sharp boundary, and morphologically they can scarcely be separated. Species with ring-spots sometimes have nuclei, and ocellated larvæ in some cases possess only a pale spot instead of a dark pupil. I deal here with the two kinds separately, because it happens that they appear in two distinct genera, in each of which they have their special developmental history. Ring-spots originate in a different position, and in another manner than eye-spots; but it must not, on this account, be assumed without further inquiry, that they are called into existence by the same causes; they must rather be investigated separately, from their origin.
Eye-spots are possessed by the genera Chærocampa and Pterogon; ring-spots by the genus Deilephila. In accordance with the data furnished by the above-given developmental histories, the origination of these markings in the two genera may be thus represented: —
In the genera named, eye-spots and ring-spots are formed by the transformation of single portions of the subdorsal line.
In Chærocampa the primary ocelli originate on the fourth and fifth segments by the detachment of a curved portion of the subdorsal, this fragment becoming the “mirror,” and acquiring a dark encircling zone (“ground-area”). The nucleus (pupil) is added subsequently.
In Deilephila we learn from the development of D. Hippophaës, that the primary annulus arises on the segment bearing the caudal horn (the eleventh) by the deposition of a red spot on the white subdorsal line, which is somewhat enlarged in this region. The formation of a dark “ground-area” subsequently occurs, and with this, at first the partial, and then the complete, detachment of the mirror-spot from the subdorsal line takes place.
In both genera the spots arise at first locally on one or two segments, from which they are transferred to the others as a secondary character. In Chærocampa this transference is chiefly backwards, in Deilephila invariably forwards.
We have now to inquire whether complete eye-spots – such as those of the Chærocampa larvæ – have any significance at all, and whether they are of biological importance. It is clear at starting, that these spots do not belong to that class of markings which make their possessors more difficult of detection; they have rather the opposite effect.
We might thus be disposed to class ocellated caterpillars with those “brightly coloured” species which, like the Heliconinæ and Danainæ among butterflies, possess a disgusting taste, and which to a certain extent bear the signal of their distastefulness in their brilliant colours. But even if I had not found by experiment that our native Chærocampa larvæ were devoured by birds and lizards, and that they are not therefore distasteful to these insect persecutors, from the circumstance that these caterpillars are all protectively coloured, it could have been inferred that they do not belong to this category. It has been found that all adaptively coloured caterpillars are eaten, and one and the same species cannot possibly be at the same time inconspicuously (adaptively) and conspicuously coloured; the one condition excludes the other.
What other significance can eye-spots possess than that of making the insects conspicuous? Had we to deal with sexually mature forms, we should, in the first place, think of the action of sexual selection, and should regard these spots as objects of taste, like the ocelli on the feathers of the peacock and argus-pheasant. But we are here concerned with larvæ, and sexual selection is thus excluded.
The eye-spots must therefore possess some other significance, or else they are of no importance at all to the life of the insect, and are purely “morphological characters;” in which case, supposing this could be proved, they would owe their existence exclusively to forces innate in the organism itself – a view which very closely approaches the admission of a phyletic vital force.
I am of opinion, however, that eye-spots certainly possess a biological value as a means of terrifying – they belong to that numerous class of characters which occur in the most diverse groups of animals, and which serve the purpose of making their possessors appear as alarming as possible.
The caterpillars of the Sphingidæ are known to behave themselves in different manners when attacked. Some species, such, for instance, as Sphinx Ligustri and Smerinthus Ocellatus, on the approach of danger assume the so-called Sphinx attitude; if they are then actually seized, they dash themselves madly to right and left, by this means not only attempting to get free, but also to terrify their persecutor. This habit frequently succeeds with men, and more especially with women and children; perhaps more easily in these cases than with their experienced foes, birds.
The ocellated Chærocampa larvæ behave differently. They remain quiet on being attacked, and do not put on a Sphinx-like attitude, but only withdraw the head and three small front segments into the large fourth segment, which thus becomes much swollen, and is on this account taken for the head of the insect by the inexperienced.145 Now the large eye-spots are situated on the fourth segment, and it does not require much imagination to see in such a caterpillar an alarming monster with fiery eyes, especially if we consider the size which it must appear to an enemy such as a lizard or small bird. Fig. 28 represents the larva of C. Porcellus in an attitude of defence, although but imperfectly, since the front segments can be still more withdrawn.
These facts and considerations do not, however, amount to scientific demonstration, and I therefore made a series of experiments, in order to determine whether these caterpillars did actually frighten small birds. The first experiment proved but little satisfactory. A jay, which had been domesticated for years, to which I threw a caterpillar of Chærocampa Elpenor, did not give the insect any time for manœuvring, but killed it immediately by a strong blow with its bill. This bird had been tame for years, and was in the habit of pecking at everything thrown to him. Perhaps a wild jay (Garrulus Glandarius) would have treated the insect differently, but it is hardly possible that such a large and courageous bird would have much respect for our native caterpillars. I now turned to wild birds. A large brown Elpenor larva was placed in the food-trough of an open fowl-house from which the fowls had been removed. A flock of sparrows and chaffinches (Fringilla Domestica and Cœlebs) soon flew down from the neighbouring trees, and alighted near the trough to pick up stray food in their usual manner. One bird soon flew on to the edge of the trough, and was just about to hop into it when it caught sight of the caterpillar, and stood jerking its head from side to side, but did not venture to enter. Another bird soon came, and behaved in a precisely similar manner; then a third, and a fourth; others settled on the perch over the trough, and a flock of ten or twelve were finally perched around. They all stretched their heads and looked into the trough, but none flew into it.
I now made the reverse experiment, by removing the caterpillar and allowing the birds again to assemble, when they hopped briskly into the trough.
