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 excludedab initio, since we are here concerned with larvæ, and not with reproductiveforms.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 theSphingidæwe 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, notonly in the small group of theSphingidæbut in the whole order Lepidoptera, we shall arrive at the followingresults:—
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 ofSesiidæ(the generaSesia,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 asHepialus Humuliat the roots of hop, andH. Lupulinusat those ofTriticum Repens, possess neither colour nor marking. These, like the foregoing, are yellowish-white, evidently because they are deprived of the influence oflight.142The larvæ ofcertain small moths, such asTortrix ArbutanaandPomonana, which live in fruit, and many case-bearingTineina, 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 ofNepticula. 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 youngSmerinthuscaterpillars 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 theSphingidæof 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 planton 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 theSatyrinæpossess larvæ conspicuously striped—a fact which is readily explicable, because all these caterpillars live on grasses. This is the case with the generaMelanargia,Erebia,Satyrus,Pararge,Epinephele, andCænonympha, 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 certainSphingidæ, 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 theSphingidæalso, 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 ofSatyrus, such asS. 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 theSphingidæ; 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 theSatyrinæ, most of the larvæ of thePierinæandHesperidæpossess longitudinal stripes, which are generally less strongly pronounced than in the former subfamily. Some of thePierinælive onCruciferæ, of which the narrow leaves and thin leaf- and flower-stalks present nothing but a linear arrangement; other species of this group, however, feed onLeguminosæ(Lathyrus,Lotus,Coronilla,Vicia), and some few on broad-leaved bushes (Rhamnus). This last fact may appear to beopposed to the theory; but light lateral stripes, such for example, as those possessed byGonepteryx 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 otherLeguminosæ, 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 theHesperidælarvæ, which partly feed on grasses but mostly on species ofLeguminosæ, 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 asChesias Spartiata, which lives on broom (Spartium Scoparium),its longitudinal stripes deceptively resembling the sharp edges of the stems of thisplant.143
3.Oblique striping.Can the lilac and white oblique stripes on the sides of a large green caterpillar, such as those ofSphinx Ligustri; or the red and white, or white, black, and red stripes ofSmerinthus TiliæandSphinx Drupiferarumrespectively, 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 ofjust 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. OcellatusonSalix; 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 manySphingidæ, 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 hasalready been shown with respect to theSphingidæ, in which the oblique stripes are only completely developed in the subfamiliesSmerinthinæandSphinginæ. The species ofSmerinthusall live on trees such as willows, poplars, lime, oak, &c., and all possess oblique stripes. The genusAnceryxalso belongs to theSphinginæ, 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 ofSphinx, 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, theSphinxcaterpillars being adapted to ordinary foliage. The species ofAnceryx, 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 theConiferæ.
Of theSphinginæliving 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 RusticaandCingulata;Dolba HylæusandAcherontia Atropos.
Besides among theSphinginæ, oblique stripes occur in the larvæ of certain butterflies, viz.Apatura Iris,Ilia, andClytie, 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. ofAglia TauandEndromis Versicolora, both of which also live on forest trees.
Oblique stripes also occasionally occur in the smaller caterpillars ofNoctuæ,Geometræ, and even in those of certainPyrales, 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 ofEriopus Pteridis. This little Noctuid lives onPteris 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 ofsoriof 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 theSphingidæare 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 possibilityof 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 ofSphinx Ligustrion 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 inSphinx Ligustrithese edges are lilac, and inS. Drupiferarum,S. Prini, andDolba Hylæusred, nor why they are black and green inMacrosila Rustica, and blue inAcherontia 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 theSphingidæmust 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 andeven during the night;i.e.in a light so faint that feeble colours would produce scarcely any effect. The bright blue ofAcherontia 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 ofChærocampaandSphinx, 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 byday.144An insect whichacquires 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 naturalselection, 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 ofSmerinthus, as has already been established, showing this with particular distinctness. InS. Tiliæthe course of development can be followed till the somewhat irregular red border is formed. In the species ofSphinxthis border has become completely linear. It is very possible that the ontogeny ofS. LigustriorDrupiferarumwould 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 theSphingidæ,viz.:—
4.Eye-spots and Ring-spots.—These markings, besides among theSphingidæ, are found only in a very few caterpillars, such as certain tropicalPapilionidæandNoctuæ. 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 theChærocampalarvæ and inPterogon 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 thisaccount, 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 generaChærocampaandPterogon; ring-spots by the genusDeilephila. In accordance with the data furnished by the above-given developmental histories, the origination of these markings in the two genera may be thusrepresented:—
In the genera named, eye-spots and ring-spots are formed by the transformation of single portions of the subdorsal line.
InChærocampathe 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.
InDeilephilawe learn from the development ofD. 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 transferredto the others as a secondary character. InChærocampathis transference is chiefly backwards, inDeilephilainvariably forwards.
We have now to inquire whether complete eye-spots—such as those of theChærocampalarvæ—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 theHeliconinæandDanainæamong 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 nativeChærocampalarvæ 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 possessthan 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 theSphingidæare known to behave themselves in different manners when attacked. Some species, such, for instance, asSphinx LigustriandSmerinthus 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 terrifytheir 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 ocellatedChærocampalarvæ 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 theinexperienced.145Now 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. 28represents the larva ofC. Porcellusin 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 ofChærocampaElpenor, 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 brownElpenorlarva 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 DomesticaandCœlebs) 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.
I often repeated this experiment, and always with the same result. Once it could be plainly seen that it was really fear and not mere curiosity that the birds showed towards the caterpillar. The latter was outside the trough amongst scattered grains of food, so that from one side it was concealed by the trough. A sparrow flew down obliquely from above, so that at first it could not see the caterpillar, close to which it alighted. The instant it caught sight of the insect, however, it turned in evident fright and flew away.
Of course these experiments do not prove that the larger insectivorous birds are also afraid of these caterpillars. Although I have not been able to experiment with such birds, I can certainly prove that even fowls have a strong dislike to these insects. I frequently placed a largeElpenorlarva in the poultry yard, where it was soon discovered, and a fowl would run hastily towards it, but would draw back its head just when about to give a blow with the bill, as soon as it saw the caterpillar closely. The bird would now run round the larva irresolutely in a circle—the insect in the meantime assuming its terrifying attitude—and stretching out its head would make ten or twenty attempts to deal a blow with its bill, drawing back again each time. All the cocks and hens acted in a similar manner, and it was often five or ten minutes before one particularly courageous bird would give the first peck, which would soon befollowed by a second and third, till the caterpillar, appearing palatable, would finally be swallowed.
These experiments were always made in the presence of several persons, in order to guard myself against too subjective an interpretation of the phenomena; but they all invariably considered the conduct of the birds to be as I have here representedit.146
If it be admitted that the ocelli of caterpillars are thus means of exciting terror, the difficulty of their occurring in protectively coloured species at once vanishes. They do not diminish the advantage of the adaptive colouring, because they do not make the caterpillars conspicuous, or at least any more easily visible at a distance, excepting when the insects have assumed their attitude of alarm. But these markings are of use when, in spite of protective colouring, the larva is attacked by an enemy. The eye-spots accordingly serve the caterpillar as a second means of defence, which is resorted to when the protective colouring has failed.
By this it must not be understood that the ocelli of theChærocampalarvæ invariably possess only this, and no other significance for the life of the insect. Every pattern can be conceived to renderits possessor in the highest degree conspicuous by strongly contrasted and brilliant colouring, so that it might be anticipated that perfect eye-spots in certain unpalatable species would lose their original meaning, and instead of serving for terrifying become mere signals of distastefulness. This is perhaps the case withChærocampa Tersa(Fig. 35), the numerous eye-spots of which make the insect easily visible. Without experimenting on this point, however, no certain conclusion can be ventured upon, and it may be equally possible that in this case the variegated ocelli with bright red nuclei resemble the blossoms of the food-plant (Spermacoce Hyssopifolia).147I here mention this possibility only in order to show how an inherited form of marking, even when as well-defined and complicated as in the present case, may, under certain circumstances, be turned in quite another direction by natural selection, for the benefit of its possessor. Just in the same manner one and the same organ, such, for instance, as the limb of a crustacean, may, in the course of phyletic development, perform very different functions—first serving for locomotion, then for respiration, then for reproduction or oviposition, and finally for the acquisition of food.
I now proceed to the consideration of the biological value of incomplete eye-spots, or, as I have termed them, ring-spots. Are these also means of terrifying, or are they only signals of distastefulness?
I must at the outset acknowledge that on this point I am able to offer but a very undecided explanation. The decision is only to be arrived at by experiments conducted with each separate species upon which one desires to pronounce judgment. It is not here legitimate to draw analogical inferences, and to apply one case to all, since it is not only possible, but very probable, that the biological significance of ring-spots changes in different species. Nothing but a large series of experiments could completely establish this. Unfortunately I have hitherto failed in obtaining materials for this purpose. I would have deferred the publication of this essay for a year, could I have foreseen with certainty that such materials would have been forthcoming in sufficient quantity during the following summer; but this unfortunately depends very much upon chance, and I believed that a preliminary conclusion would be preferable to uncertainty. Perhaps some entomologist to whom materials are more easily accessible, may, by continuing these experiments, accomplish this object.
The experiments hitherto made by other observers, are not sufficient for deciding the questionunder consideration.Weir,148as is well known, showed that certain brightly coloured and conspicuous larvæ were refused by insectivorous birds; andButler149proved the same for lizards and frogs. These experiments are unfortunately so briefly described, that in no case is the species experimented with mentioned by name, so that we do not know whether there were any Sphinx caterpillars amongthem.150I have likewise experimented in this direction with lizards, in order to convince myself of the truth of the statement that (1) there are caterpillars which are not eaten on account of their taste, and (2) that such larvæ possess bright colours. I obtained positive, and on the whole, very decided results. Thus, the common orange and blue striped caterpillars ofBombyx Neustriaenjoyed complete immunity from the attacks of lizards, whilst those of the nearly alliedEriogaster LanestrisandL. Piniwere devoured, although not exactly relished. That the hairiness is not the cause of their being unpalatable, is shown by the fact thatL. Piniis much more hairy thanB. Neustria. The very conspicuous yellow and black ringed caterpillar ofEuchelia Jacobæægave also most decided results. I frequently placed thisinsect in a cage withLacerta Viridis, but they would never even notice them, and I often saw the caterpillars crawl over the body, or even the head of the lizards, without being snapped at. On every occasion the larvæ remained for several days with the lizards without one being ever missed. The reptiles behaved in a precisely similar manner with respect to the moth ofE. Jacobææ, not one of which was ever touched by them. The yellow and black longitudinally striped caterpillars ofPygæra Bucephalawere also avoided, and so were the brightly coloured larvæ of the large cabbage white (Pieris Brassicæ), which when crushed give a disagreeable odour. This last property clearly shows why lizards reject this species as distasteful. Both caterpillar and butterfly possess a blood of a strong yellow colour and oily consistency, in which, however, I could not detect such a decided smell as is emitted by that of theHeliconinæandDanainæ.151
I next made the experiment of placing before a lizard a caterpillar as much as possible like that ofE. Jacobææ. Half grown larvæ ofBombyx Rubilikewise possess golden yellow (but narrower)transverse rings on a dark ground, and they are much more hairy than those ofE. Jacobææ. The lizard first applied its tongue to this caterpillar and then withdrew it, so that I believed it would also be avoided; nevertheless it was subsequently eaten. The caterpillars ofSaturnia Carpiniwere similarly devoured in spite of their bristly hairs, and likewise cuspidate larvæ (Dicranura Vinula), notwithstanding their extraordinary appearance and their forked caudalhorn.152These lizards were by no means epicures, but consumed large numbers of earth-worms, slugs, and great caterpillars, and once a specimen of the large and powerfully biting Orthopteron,Decticus Verucivorus. Creatures which possessed a strongly repugnant odour were, however, always rejected, this being the case with the strongly smelling beetle,Chrysomela Populi, as also with the stinking centipede,Iulus Terrestris, whilst the inodorousLithobius Forficatuswas greedily eaten. I will call particular attention to these last facts, because they favour the supposition that with rejected caterpillars a disgusting odour—although perhaps not always perceptible by us—is the cause of their being unpalatable.
Striking colours are of course only signals of distastefulness, and the experiment withBombyxRubishows that the lizards were from the first prejudiced against such larvæ, the prejudice only being overcome on actually trying the specimen offered. A subsequent observation which I made after arriving at this conclusion, is most noteworthy. After the lizard had learnt by experience that there might be not only distasteful caterpillars (E. Jacobææ), but also palatable ones banded with black and yellow (B. Rubi), it sometimes tasted theJacobæælarvæ, as if to convince itself that the insect was actually as it appeared to be, viz., unpalatable!
A striking appearance combined with a very perceptible and penetrating odour is occasionally to be met with, as in the caterpillar of the common Swallow-tail,Papilio Machaon. I have never seen a lizard make the slightest attempt to attack this species. I once placed two large specimens of this caterpillar in the lizard vivarium, where they remained for five days, and finally pupated unharmed on the side of the case.
I have recorded these experiments, although they do not thus far relate to Sphinx-caterpillars, with the markings of which we are here primarily concerned, because it appeared to me in the first place necessary to establish by my own experiments that signals of distastefulness did occur in caterpillars.
I now come to my unfortunately very meagre experience withDeilephilalarvæ, with only twospecies of which have I been able to experiment, viz.,D. GaliiandEuphorbiæ.
The first of these was constantly rejected. Two large caterpillars, one of the black and the other of the yellow variety, were left for twelve hours in the lizard vivarium, without being either examined or touched. It thus appears thatD. Galiiis a distasteful morsel to lizards; and the habits of the caterpillar are quite in accordance with this, since it does not conceal itself, but rests fully exposed by day on a stem, so that it can scarcely escape being detected. It is almost as conspicuous asD. Euphorbiæ.
I was much surprised to find, however, that this last species was not rejected by lizards. On placing a large caterpillar, six to seven centimeters long, in the vivarium, the lizard immediately commenced to watch it, and as soon as it began to crawl about, seized it by the head, and, after shaking it violently, commenced to swallow it. In spite of its vigorous twisting and turning, the insect gradually began to disappear, amidst repeated shakings; and in less than five minutes was completelyswallowed.153With regard to lizards, therefore, the prominent ring-spots of this larva are not effective as a means of alarm, nor are they considered as a sign of distastefulness.
Unfortunately I have not hitherto been able to make any experiments with birds. It would be rash to conclude from the experience with lizards that ring-spots were of no biological value. There is scarcely any one means of protection which can render its possessor secure againstallits foes. The venom of the most poisonous snakes does not protect them from the attack of the secretary bird (Serpentarius Secretarius) and serpent eagle (Spilornis Cheela); and the adder, as is well known, is devoured by hedgehogs without hesitation. It must therefore be admitted that many species which are protected by distastefulness, may possess certain foes against which this quality is of no avail. Thus, it cannot be said that brightly coloured caterpillars, which are not eaten by birds and lizards, are also spared by ichneumons. It is readily conceivable therefore, that the larva ofD. Euphorbiæmay not be unpalatable to lizards, because they swallow it whole; whilst it is perhaps distasteful to birds, because they must hack and tear in order to swallow it.
From these considerations it still appears most probable to me thatD. Euphorbiæ, and the nearly alliedD. DahliiandMauritanica, bear conspicuous ring-spots as signs of their being unpalatable to the majority of their foes. The fact that these species feed on poisonousEuphorbiaceæ, combined with their habit of exposing themselves openly by day, so as to be easily seen at a distance, mayperhaps give support to this view. As these insects are not protectively coloured, this habit would long ago have led to their extermination; instead of this, however, we find that in all situations favourable to their conditions of life they are among the commonest of theSphingidæ.
Thus,D. Euphorbiæoccurs in large numbers both in South and North Germany (Berlin); and Dr. Staudinger informs me that in Sardinia the larvæ ofD. Dahliiwere brought to him by baskets full.
But if the conspicuous ring-spots (combined of course with the other bright colours) may be regarded as signals of distastefulness in many species ofDeilephila, this by no means excludes the possibility that in some species these markings play another part, and are effective as a means of alarm. It even appears conceivable to me that in one and the same caterpillar they may play both parts against different foes, and it would certainly be of interest to confirm or refute this supposition by experiment.
In the light yellow variety of the caterpillar ofD. Galiithe ring-spots may serve as means of alarm, and still more so in that ofD. Nicæa, the resemblance of which to a snake has struck earlierobservers.154
In those species ofDeilephilawhich conceal themselves by day, the ring-spots cannot be considered as signals of distastefulness, and they must therefore have some other meaning. As examples of this class may be mentionedD. Vespertilio, which is protectively coloured both in the young and in the adult stages; and likewiseD. Hippophaës, in which this habit of concealment is associated with adaptive colouring. In the case of the first-named species, it appears possible that the numerous large ring-spots may serve to alarm small foes, but the truth of this supposition could only be decided by experiment. InD. Hippophaës, on the other hand, such an interpretation must be at once rejected, since most individuals possess but a single ring-spot, which shows no resemblance whatever to an eye.
I long sought in vain for the meaning of this ring-spot, the discovery of which would in this particular case be of the greatest value, because we have here obviously the commencement of the whole development of ring-spots before us—the initial stage from which the marking of all the other species ofDeilephilahas proceeded.
I believe that I have now found the correct answer to this riddle, but unfortunately at a period of the year when I am unable to prove itexperimentally. I consider that the ring-spots are crude imitations of the berries of the food-plant. The latter are orange-red, and exactly of the same colour as the spots; the agreement in colour between the latter and the berries is quite as close as that between the leaves and the general colouring of the caterpillar. I know of no species which more closely resembles the colour of the leaves of its food-plant, the dark upper side and light under side corresponding in the leaves and caterpillars. The colour of theHippophaeis not an ordinary green, but a grey-green, which shade also occurs, although certainly but rarely, in the larvæ. I may expressly state that I have repeatedly shown to people as many as six to eight of the large caterpillars on one buckthorn branch, without their being able at once to detect them. It is not therefore mere supposition, but a fact, that this species is protected by its general colouring. At first the orange-red spots appear rather to diminish this protection—at least when the insects are placed on young shoots bearing no berries. But since at the same time when the berries become red (end of July and the beginning of August) the caterpillars are in their last stage of development (i.e.possess red spots), it appears extremely probable that these spots are vague representations of the berries. For the same reason that these caterpillars have acquired the habit of feeding only at dusk and during themorning twilight, or at night, and of concealing themselves by day, it must be advantageous for them to have the surface of their large bodies not only divided by white stripes, but also interrupted in yet another manner. How could this be better effected than by two spots which, in colour and position, represent the grouping of the red berries on the branches? When feeding, the insect always rests with the hind segments on a branch, the front segments only being more or less raised and held parallel to the leaves; the red spots thus always appear on the stem, where the berries are likewise situated. It might indeed be almost supposed that the small progress which the formation of secondary ring-spots on the other segments has made up to the present time, is explicable by the fact that such berry-like spots on other portions of the caterpillar would be rather injurious than useful.
It may, however, be asked how an imitation of red berries, which are eaten by birds just as much as other berries, can be advantageous to a caterpillar, since by this means it would rather attract the attention of its enemies?
Two answers can be given to this. In the first place, the berries are so numerous on every plant that there is but a very small chance of the smaller and less conspicuous berry-spots catching the eye of a bird before the true berries; and, secondly, the latter, although beginning to turnred when the caterpillars are feeding, do not completely ripen till the autumn, when the leaves are shed, and the yellowish-red clusters of berries can be seen at a distance. The caterpillar, however, pupates long before this time.
I have considered this case in such detail because it appears to me of special importance. It is the only instance which teaches us that the rows of ring-spots of theDeilephilalarvæ proceed from one original pair—the only instance which permits of the whole course of development being traced to its origin. Were it possible to arrive at the causes of the formation of these spots, their original or primary significance would thereby be made clear.
I will now briefly summarise the results of the investigation of the biological value of theDeilephilaring-spots.
In the known species of the genus now existing these spots have different meanings.
In some species (certainly inGalii, and probably inEuphorbiæandMauritanica) the conspicuous ring-spots serve as signals of distastefulness for certain enemies (not for all).
In a second group of species they serve as a means of alarm, like the eye-spots of theChærocampalarvæ (Nicæa? light form ofGalii?).
Finally, in a third group, of which I can at present only citeHippophaës, they act as an adaptive resemblance to a portion of a plant,and enhance the efficacy of the protective colouring.
5.Subordinate Markings.—If, from the foregoing considerations, it appears that the three chief elements of the Sphinx-markings—longitudinal and oblique stripes, and spot formations—are not purely morphological characters, but have a very decided significance with respect to their possessors, there should be no difficulty in referring the whole of the markings of theSphingidæto the action of natural selection, supposing that these three kinds of marking were the only ones which actually occurred.
In various species, however, there appear other patterns, which I have comprised under the term “subordinate markings,” some of which I will select, for the purpose of showing the reasons which permit of their being thus designated.
I ascribe to this category, for example, that fine network of dark longitudinal streaks which often extends over the whole upper side of the caterpillar, and which is termed the “reticulation.” This character is found chiefly in the adult larvæ ofChærocampa, being most strongly pronounced in the brown varieties: it occurs also inDeilephila Vespertilio,Pterogon Œnotheræ, andSphinx Convolvuli. As far as I know, it is only associated with adaptive colours, and indeed occurs only in those caterpillars which rest periodically at thebase of their food-plants among the dead leaves and branches. I do not consider this reticulation to be a distinct imitation, but only as one of the various means of breaking up the large uniform surface of the caterpillar so as to make it present inequalities, and thus render it less conspicuous. There can be no doubt as to the dependence of this character upon natural selection.
There is, however, a second group of markings, which must be referred to another origin. To this group, for instance, belong those light dots inChærocampa PorcellusandElpenorwhich have been termed “dorsal spots.” I know of no other explanation for these than that they are the necessary results of other new formations, and depend on correlation (Darwin), or, as I may express it, they are the result of the action of the law governing the organization of these species.
As long as we are confined to the mere supposition that the character in question may be the outward expression of an innate law of growth, it is permissible to attempt to show that a quite similar formation in another species depends upon such a law.
Many of the dark specimens ofSphinx Convolvulishow whitish dots on segments six to eleven, one being situated on the front edge of each of these segments, at the height of the completely vanished subdorsal line (Fig. 52). These spots vary much in size, lightness, and sharpness ofdefinition. Now it might be difficult to attribute any biological significance to this character, but its origin becomes clear on examining light specimens in which the oblique white stripes are distinct on the sides and the subdorsal line is retained at least on the five or six anterior segments. It can then be seen that the spots are located at the points of intersection of the subdorsal and the oblique stripes (Fig. 16,Pl. III.), and they can accordingly be explained by the tendency to the deposition of light pigment being twice as great in these positions as in other portions of the two systems of light lines. Light spots are thus formed when the lines which cross at these points are partially or completely extinct throughout their remaining course.
A marking is therefore produced in this case by a purely innate law of growth—by the superposition of two ancient characters now rudimentary. Many other unimportant details of marking must be regarded as having been produced in a similar manner, although it may not be possible to prove this with respect to every minute spot and stripe. The majority of “subordinate markings” depend on the commingling of inherited, but now meaningless, characters with newly acquired ones.
It would be quite erroneous to attribute to natural selection only those characters which can be demonstrated to still possess a biological value in the species possessing them. They may beequally due to heredity. Thus, it is quite possible that the faint and inconspicuous ring-spots ofDeilephila Vespertilioare now valueless to the life of the species—they may be derived from an ancestral form, and have not been eliminated by natural selection simply because they are harmless. I only mention this as a hypothetical case.
In the case of markings of the second class,i.e.oblique stripes, a transference to later phyletic stages can be demonstrated, although the stripes thereby lose their original biological value. Thus, theChærocampalarvæ, when they were green throughout their whole life and adapted to the leaves, appear to have all possessed light oblique stripes in imitation of the leaf-ribs. All the species of the older type of colouring and marking, such asChærocampa Syriaca(Fig. 29) andDarapsa Chœrilus(Fig. 34), and also the light green young forms ofC. Elpenor(Fig. 20), andPorcellus(Figs. 25 and 26), show these oblique stripes. In these last species the foliage imitation is abandoned at a later stage, and a dark brown, or blackish-brown, ground-colour acquired. Nevertheless the oblique stripes do not disappear, but show themselves—in the fourth stage especially, and sometimes in the fifth—as distinct dirty yellow stripes, although not so sharply defined as in the earlier stages. These persistent stripes, in accordance with their small biological value, are very variable, since they are only useful in so far as they help to breakup the large surface presented by the caterpillar, and are of no value as imitations of surrounding objects.
The oblique stripes ofSphinx Convolvulioffer a precisely similar case; and it may be safely predicted that the young forms of this species would possess sharply defined light oblique stripes, since more or less distinct remnants of these markings occur in all the adult larvæ, and especially in the green form. The entire pattern of this caterpillar depends essentially on the commingling of characters persisting from an earlier period,i.e.of residues of the subdorsal and oblique stripes, both these markings being extraordinarily variable. The black reticulation was added to the ground-colour as a new means of adaptation, this character appearing only in the phyletically younger brown form, and being entirely absent, or only faintly indicated, in the older green variety.