Chapter XXXII: Part III: The Metamorphoses of Insects (3)

“It is principally,” adds Riley, “by the leverage obtained by the
hooking of the sustainers in the retaining membrane, which acts as a
swimming fulcrum, that the chrysalis is prevented from falling after
the cremaster is withdrawn from the larval skin. It is also
principally by this same means that it is enabled to reach the silk
with the cremastral hook-pads.”

“Dissected immediately after suspension, the last abdominal segment
of the larva is found to be bathed, especially between the legs and
around the rectum, in an abundance of translucent, membranous
material.”

“An hour or more after suspension the end of the forming chrysalis
begins to separate from the larval skin, except at the tip of the
cremaster (Fig. 597, _b_). Gradually the skin of the legs and of the
whole subjoint (10th segment) stretches, and with the stretching,
the cremaster elongates, the rectal piece recedes more and more from
the larval rectum, and the sustentor ridges diverge more and more
from the cremaster, carrying with them, on the sustainers, a part of
the soft membrane.” The rectal ligament will sustain at least 10 or
12 times the weight of the chrysalis. That of Apatura seems to rely
almost entirely on the rectal ligament, assisted by the partial
holding of the delicate larval skin.

FORMATION OF THE PUPA AND IMAGO IN THE HOLOMETABOLOUS INSECTS (THE
DIPTERA EXCEPTED)

We have seen that in the incomplete metamorphosis, although there may be as many as five, and possibly seven moults, and in Chloëon as many as 20, and in _Cicada septemdecim_ perhaps 25 or 30, there is but a slight change of form from one stage to another, and no period of inactivity. And this gradual outer transformation is so far as yet known paralleled by that of the internal organs, the slight successive changes of which do not differ from those observed in the growth of ametabolous insects. With the growth of the internal organs there probably goes on a series of gradual regenerative processes, and Korschelt and Heider state that we may venture to assume that each changed cell or group of cells which have become exhausted by the exercise of the functions of life are reabsorbed and become restored through the vital powers of the tissues, so that as the result there goes on a constant, gradual regeneration of the organs.

While the Hemiptera have only an incomplete metamorphosis, the males of the Coccidæ are, as shown by O. Schmidt, remarkable for passing through a complete or holometabolous development, with four stages, three of which are pupal and inactive. Hence, as Schmidt observes, there is here a hypermetamorphosis, like that of the Meloidæ, Stylopidæ, etc.

Shortly before the end of the larval stage of the male appear the imaginal buds of the eyes, legs, and wings. In the 2d or 1st pupal stage there is an atrophy of the antennæ and legs. On the other hand, at this stage the female completes its metamorphosis.

The rudiments of the wings arise on the edge of the dorsal and ventral side of the 2d thoracic segment, and this, we would remark, is significant as showing a mode of origin of the wings intermediate between that of the manometamorphic and holometamorphic insects. (See pp. 137–142.) While Schmidt could not ascertain the exact structure of the imaginal buds, he says “in general the process of formation of the extremities is exactly as Weismann has described in Corethra.” The two later pupal stages are “as in other metabolic insects.” (See p. 690, Fig. 637.)

Thus far the internal changes in the metamorphosis of the Coleoptera have not been thoroughly studied. They are less complete than in the other holometabolous insects, the differences between the larva and imago being much less marked than in the more specialized orders, and so far as known all the larval organs pass, though not without some great changes, directly into the imaginal ones, the only apparent exception being the mid-intestine, which, as stated by Kowalevsky, undergoes a complete transformation during metamorphosis. The following account, then, refers almost wholly to the Lepidoptera, Hymenoptera, and Diptera.

_a._ The Lepidoptera

The first observations on the complete metamorphosis of insects which were in any way exact were those of Malpighi, in 1667, and of Swammerdam, in 1733. While the observations of Swammerdam, as far as they extended, were correct, his conclusions were extraordinary. They were, however, accepted by Réaumur and by Bonnet, and generally held until the time of Herold in 1815, and lingered on for some years after. The rather famous theory of incasement (“_emboîtement_”) propounded by Swammerdam was that the form of the larva, pupa, and imago preëxisted in the egg, and even in the ovary; and that the insects in these stages were distinct animals, contained one inside the other, like a nest of boxes, or a series of envelopes one within the other, or, to use his own words: “_Animal in animali, seu papilio intra erucam reconditus._”

This theory Swammerdam extended to the whole animal kingdom. It was based on the fact that by throwing the caterpillar, when about to pupate, in boiling water, and then stripping off the skin, the immature form of the butterfly with its appendages was disclosed. Malpighi had previously observed the same fact in the silkworm, perceiving that before pupation the antennæ are concealed in the head of the larva, where they occupy the place previously taken by the mandibular muscles; also that the legs of the moth grew in those of the larva, and that the wings developed from the sides of the worm.

Even Réaumur (1734) remarked: “Les parties du papillon cachées sous le fourreau de chenille sont d’autant plus faciles à trouver que la transformation est plus proche. Elles y sont neanmoins de tout temps.” He also believed in the simultaneous existence of two distinct beings in the insect. “Il serait très curieux de connaître toutes les communications intimes qui sont entre la chenille et le papillon.... La chenille hache, broye, digere les aliments qu’elle distribué au papillon; comme les mères préparent ceux qui sont portés aux fœtus. Notre chenille en un mot est destineé à nourrir et à defendre le papillon qu’elle renferme.” (T. i, 8^e Mémoire, p. 363.)

Lyonet (1760), even, did not expose the error of this view that the larva enveloped the pupa and imago, and, as Gonin says, it was undoubtedly because he did not use for his dissections of the caterpillar of Cossus any specimens about to pupate. Yet he detected the wing-germs and those of the legs, stating that he presumed the bodies he saw to be the rudiments of the legs of the moth (p. 450).

Herold, in his work on the development of the butterfly (1815), was the first to object to this erroneous theory, showing that the wings did not become visible until the very end of larval life; that as the larval organs disappear, they are transformed or are replaced by entirely new organs, which is not reconcilable with a simple putting off of the outer envelope. The whole secret of metamorphosis, in Herold’s opinion, consisted in this fact, that the butterfly in the larva state increases and accumulates a supply of fat until it has reached the volume of the perfect state; then it begins the chrysalis period, during which the organs are developed and take their definite form.[112] (Abstract mostly from Gonin.) Still the old ideas prevailed, and even Lacordaire, in his Introduction à l’Entomologie published in 1834, held on to Swammerdam’s theory, declaring that “a caterpillar is not a simple animal, but compound,” and he actually goes so far as to say that “a caterpillar, at first scarcely as large as a bit of thread, contains its own teguments threefold and even eightfold in number, besides the case of a chrysalis, and a complete butterfly, all lying one inside the other.” This view, however, we find is not original with Lacordaire, but was borrowed from Kirby and Spence without acknowledgment. These authors, in their Introduction to Entomology (1828), combated Herold’s views and stoutly maintained the old opinions of Swammerdam. They based their opinions on the fact, then known, that certain parts of the imago occur in the caterpillar. On the other hand, Herold denied that the successive skins of the pupa and imago existed as germs, holding that they are formed successively from the “_rete mucosum_,” which we suppose to be the hypodermis of later authors. In a slight degree the Swammerdam-Kirby and Spence doctrine was correct, as the imago does arise from germs, _i.e._ the imaginal disks of Weismann, while this was not discovered by Herold, though they do at the outset arise from the hypodermis, his _rete mucosum_. Thus there was a grain of truth in the Swammerdam-Kirby and Spence doctrine, and also a mixture of truth and error in the opinions of Herold.

The real nature of the internal changes wrought during the process of metamorphosis was first revealed by Weismann in 1864. His discovery of the germs of the imago (imaginal buds) of the Diptera, and his theory of _histolysis_, or of the complete destruction of the larval organs by a gradual process, was the result of the application of modern methods of embryology and histology, although his observations were first made on the extremely modified type of the Muscidæ or flies, and, at first, he did not extend his view to include all the holometabolous insects. Now, thanks to his successors in this field, Ganin, Dewitz, Kowalevsky, Van Rees, Bugnion, Gonin, and others, we see that metamorphosis is, after all, only an extension of embryonic life, the moults and great changes being similar to those undergone by the embryo, and that metamorphosis and alternation of generations are but terms in a single series. Moreover, the metamorphoses of insects are of the same general nature as those of certain worms, of the echinoderms, and the frog, the different stages of larva, pupa, and imago being adaptational and secondary.

While the changes in form from the larva to the pupa are apparently sudden, the internal histogenetic steps which lead to them are gradual. In the Lepidoptera a few days (usually from one to three) before assuming the pupa stage, the caterpillar becomes restless and ceases to take food. Its excrements are now hard, dry, and, according to Gonin, are “stained carmine red by the secretions of the urinary tubes.” Under the microscope we find that they are almost exclusively composed of fragments of the intestinal epithelium. These red dejections were noticed by Réaumur, and afterwards by Herold, and they are sure indications of the approach of the transformations. It now wanders about, and, if it is a spinner, spins its cocoon, and then lies quietly at rest while the changes are going on within its body. Meanwhile, it lives on the stores of fat in the fat-body, and this supply enables it to survive the pupal period.

The amount of fat is sometimes very great. Newport removed from the
larva of _Cossus ligniperda_ 42 grains of fat, being more than
one-fourth of the whole weight of the insect, he adds that the
supply is soon nearly exhausted during the rapid development of the
reproductive organs, “since, when these have become perfected, the
quantity that remains is very inconsiderable.”

Although the larval skin of a lepidopterous insect is suddenly cast off, the pupa quickly emerging front it, yet there are several intermediate stages, all graduating into each other. If a caterpillar of a Clisiocampa, which, as we have observed, is much shortened and thickened a day or two before changing to a pupa, is hardened in alcohol and the larval skin is stripped off, the semipupa (pro-nymph, pro-pupa of different authors) is found to be in different stages of development, and the changes of the mouth-parts are interesting, though not yet sufficiently studied.

Newport attributes the great enlargement and changes in the shape of the thoracic segments of the larva of _Vanessa urticæ_ at this time, to the contraction or shortening of the muscles of the interior of those segments, “which are repeatedly slowly extended and shortened, as if the insect were in the act of laborious respiration.” This, he adds, generally takes place at short intervals during the two hours immediately preceding the change to the pupa, and increases in frequency as that period approaches. He thus describes the mode of moulting the larval skin: “When the period has arrived, the skin bursts along the dorsal part of the 3d segment, or mesothorax, and is extended along the 2d and 4th, while the coverings of the head separate into three pieces. The insect then exerts itself to the utmost to extend the fissure along the segment of the abdomen, and, in the meantime, pressing its body through the opening, gradually withdraws its antennæ and legs, while the skin, by successive contortions of the abdomen, is slipped backwards, and forced towards the extremity of the body, just as a person would slip off his glove or his stocking. The efforts of the insect to get entirely rid of it are then very great; it twirls itself in every direction in order to burst the skin, and, when it has exerted itself in this manner for some time, twirls itself swiftly, first in one direction, then in the opposite, until at last the skin is broken through and falls to the ground, or is forced to some distance from it. The new pupa then hangs for a few seconds at rest, but its change is not yet complete. The legs and antennæ, which when withdrawn from the old skin were disposed along the under surface of the body, are yet separate, and do not adhere together as they do a short time afterwards. The wings are also separate and very small. In a few seconds the pupa makes several slow, but powerful, respiratory efforts; during which the abdominal segments become more contracted along their under surface, and the wings are much enlarged and extended along the lateral inferior surface of the body, while a very transparent fluid, which facilitated the slipping off of the skin, is now diffused among the limbs, and when the pupa becomes quiet dries, and unites the whole into one compact covering.”

=The changes in the head and mouth-parts.=—The changes of form from the active mandibulate caterpillar to the quiescent pupa, and then to the adult butterfly, are, as we have seen, in direct adaptation to their changed habits and surroundings, and they differ greatly in details in insects of different orders. In many Lepidoptera and certain Diptera the pupa and imago are without the mandibles of the larva, and, instead, the 1st maxillæ in the former order, and the 2d maxillæ in the latter, are highly developed and specialized. The changes in the shape of the head, with the antennæ, the latter rudimentary in the larvæ of the two orders named, are noteworthy, and will be referred to under those orders. The same may be said of the thorax with the legs and wings, and the abdomen with the ovipositor. Every part of the body undergoes a profound change, though in the Coleoptera, Trichoptera, and the more generalized and primitive Diptera, each segment and appendage of the larva are directly transformed into the corresponding parts of the pupa, and subsequently of the imago. We shall see, however, beyond, that this general statement does not apply to the Hymenoptera, in which there is a process of cephalization or transfer of parts headward, peculiar to that order.

FIG. 598.—Internal organs of _Sphinx ligustri_: 1, head; 2–4,
thoracic, 5–13, abdominal segments; _V_, fore-, _M_, mid-, _E_,
hind-intestine; _gs_, brain; _gi_, infraœsophageal ganglion; _n_,
ventral ganglion; _vm_, urinary tubes; _c_, heart; _G_, testis; _o_,
œsophagus; _a_, anus; _m_, alary muscles of the heart.
]

FIG. 599.—Pupa of the same.
]

FIG. 600.—Imago of the same.—This and Figs. 598 and 599 after Newport,
from Gegenbaur.
]

FIG. 601.—Nervous system of the larva of _Sphinx ligustri_.
]

FIG. 602.—Nervous system of the pupa of _Sphinx ligustri_, soon after
pupation.—This and Fig. 601, after Newport.
]

=The change in the internal organs.=—These were especially, as regards the nervous system, first carefully examined and illustrated by that great English entomotomist, Newport, and those of the reproductive organs by Herold as early as 1815. A glance at the figures (598–604), reproduced from Newport’s article Insecta, will show the changes wrought especially in the digestive and nervous systems of Sphinx and Vanessa, his account of the alterations in the muscles having already been quoted. As the pupal form is much nearer to that of the imago than of the larva, so the digestive canal is seen to be nearly as much differentiated in the pupa as in the imago, though the reservoir (“sucking-stomach”) of the imago is not indicated in the pupa. These changes are such as occur in an insect which is enormously voracious as a larva, and which often, passing through a period of complete inactivity, taking no food at all, finally becomes an insect which needs to suck in only a minimum quantity of water or nectar, and which practically abstains from all food. The head and genital glands also, as well as the urinary vessels, are nearly the same. On the other hand, the salivary glands have undergone, in the imago, a thoroughgoing reduction.

The changes undergone by the nervous system of _Sphinx ligustri_ and _Vanessa urticæ_ have been described by Newport with fulness of detail. An abstract of his observations on _Vanessa urticæ_, which undergoes its changes in June in 14 days, and in August in eight days, we will now give, in part verbatim, the subject being rendered much clearer by his figures, which are reproduced.

During the last larval stage, certain changes have already taken
place in different parts of the cord, which shows that they had been
a long time in progress. Besides the lateral approximation of the
cords, the first change consists in a union of the 11th and 12th
ganglia, the latter one being carried forwards; these two ganglia
being entirely separate before the 3d moult.

Two hours after the larva of _Vanessa urticæ_ has suspended itself
in order to pupate, the brain is not yet enlarged, but the
subœsophageal ganglion is nearly twice its original size and the
ganglia behind are nearer together. “A little while before the old
larval skin is thrown off there is great excitement throughout the
body of the insect.” About half an hour (Fig. 603, 2) before this
occurs the alary nerves and the cerebral, 2d, 3d, 4th, and 5th
ganglia are slightly enlarged, and the 1st subœsophageal ganglion
very considerably. Immediately after the insect has entered the pupa
state (Fig. 603, 3), all the ganglia are brought closer together.
One hour after (Fig. 603, 4) pupation the cerebral ganglia are found
to be more closely united, the 4th and 5th ganglia are nearer, and
the distance between the remaining ganglia is also reduced.

Seven hours after pupation there is a greater enlargement of the
cerebral ganglia, optic nerves, and ganglia and cords of the future
thoracic segments.

At 12 hours (Fig. 603, 5) the 5th pair of ganglia has almost
completely coalesced with the cord and the 4th; at 18 hours (Fig.
603, 6) the whole of the ganglia, cords, and nerves have become more
enlarged, especially those of the wings, while the 4th and 5th
ganglia of the cords have now so completely united as to appear like
an irregular elongated mass. At 24 hours (Fig. 604, 7) the 4th and
5th ganglia are completely united, the 5th being larger than the
4th. At 36 hours (Fig. 604, 8) the optic nerves have attained a size
almost equal to that of the brain. The 1st subœsophageal ganglion
now forms, with the cerebral ones, a complete ring around the
œsophagus, the crura having almost disappeared. The 6th ganglion has
now disappeared, but the nerves arising from it remain. At 48 hours
(Fig. 604, 9) the cord is straight instead of being sinuous, and the
7th ganglion has disappeared, while the thoracic ganglia are greatly
enlarged. At the end of 58 hours the 2d and 3d thoracic ganglia have
united, and the double ganglion thus formed is only separated from
the large thoracic mass composed of the 4th, 5th, and part of the
6th ganglia, by the short but greatly enlarged cords which pass on
each side of the central attachment of the muscles. “The optic and
antennal nerves have nearly attained their full development, and
those numerous and most intricate plexus of nerves in the three
thoracic segments of the larva form only a few trunks, which can
hardly be recognized as the same structures. The arrangement of the
whole nervous system is now nearly as it exists in the perfect
insect. The whole of these important changes are thus seen to take
place within the first three days after the insect has undergone its
metamorphosis; and they precede those of the alimentary canal,
generative system, and other organs, which are still very far from
being completed, and indeed, as compared with the nervous system,
have made but little progress.” (Art. Insecta, pp. 962–965.)

FIG. 603.—Changes in the nervous system of _Vanessa urticæ_, during
and after pupation.—After Newport.
]

FIG. 604.—Changes in the nervous system of _Vanessa urticæ_, from 24
to 58 hours after pupation.—After Newport.
]

The initial steps and many of the subsequent internal changes escaped the notice of Newport and others of his time, and it was not until the epoch-making work of Weismann on the ultimate processes of transformation of Corethra and of Musca, that we had an adequate knowledge of the subject.

Weismann (1864) was the first to show for the Muscidæ and Corethra that the appendages, wings, and other parts of the imago originate in separate, minute, cellular masses called imaginal disks, buds, or folds (histoblasts of Künckel). These imaginal buds, which arise from the hypodermis, being masses of indifferent cells, are usually present in the very young larva, and even in the later embryonic stages. It has been shown that such imaginal buds exist for each part of the body, not only for the appendages and wings (p. 126), but for the different sections of the digestive canal. During the semipupal stage these buds enlarge, grow, and at the same time there is a corresponding destruction of the larval organs. The process of destruction is due to the activity of the blood corpuscles or leucocytes (phagocytes), the larval organs thus broken up forming a creamy mass, the buds from which the new organs are to arise resisting the attacks of the virulent leucocytes, which attach themselves to the weakened tissue and engulf the pigments (see p. 422). The two processes of destruction of the larval organs (histolysis) and the building up of the imaginal organs (histogenesis) go hand in hand, so that the connection of the organs in question in most cases remains entirely continuous; while the last steps in the destruction of the larval organs only take place after the organs of the imago have assumed their definite shape and size. Other observers have corroborated and confirmed his statements and observations, Gonin extending them to the Lepidoptera and Bugnion to the Hymenoptera.

It is a pity that the observations, such as were set on foot by Weismann, were not first made on the Trichoptera and Lepidoptera, which are much more primitive and unmodified forms than the Diptera, but mistakes of this nature have frequently happened in the history of science.

FIG. 605.—Full grown larva of _Pieris brassicæ_ opened along the
dorsal line: _d_, digestive canal; _s_, silk-gland; _g_, brain; _st
I_, prothoracic stigma; _st IV_, 1st abdominal stigma; _a_, _a′_,
germs (buds) of fore and hind wings; _p_, bud of thoracic
segment;—those of the 3d pair are concealed under the silk-glands;
_I_-_III_, thoracic rings.—After Gonin.
]

The latest and most detailed researches are those of J. Gonin on the metamorphoses of _Pieris brassicæ_, made under the direction of Professor E. Bugnion. They fill an important gap in our knowledge, and show that the Lepidoptera transform in nearly the same manner as described by Weismann in Corethra. We give the following condensed account of Gonin’s observations.

On opening a caterpillar entering on the semipupa state (Fig. 605), the relative position of the germs (imaginal buds or folds) of the wings and of the legs are seen.

FIG. 606.—Section through thorax of a tineid larva on sycamore,
passing through the 1st pair of wings (_w_): _ht_, heart; _i_,
œsophagus; _s_, salivary gland; _ut_, urinary tube; _nc_, nervous
cord; _m_, recti muscles; a part of the fat-body overlies the heart.
_A_, right wing-germ enlarged.
]

FIG. 607.—Section of the same specimen as in Fig. 606, but cut through
the 2d pair of wings (_w_): _i_, mid-intestine; h, heart; _fb_,
fat-body; _l_, leg; _n_, nervous cord.
]

These imaginal buds in a more advanced stage are seen in our sections of a tineid larva (Figs. 606, 607).

The number of 12 imaginal buds found by Weismann in the thorax of Muscidæ does not occur in Lepidoptera, since, as in the Hymenoptera (Bugnion), the dorsal buds of the prothoracic segment are wanting. Gonin finds in Pieris that the ventral buds of the three thoracic segments are each represented by several distinct folds attached to the femoro-tibial bud and to the tarsal joints.

The imaginal buds serve in some cases for the formation of new organs (wings, legs of insects with apodous larvæ); in others for the growth and the transformation of organs already existing (legs, antennæ, 1st and 2d maxillæ of Lepidoptera).

As to the peripodal sac or hypodermic envelope which contains the
imaginal bud, a portion persists and is regenerated, while the other
part becomes useless and is detached under the form of débris, as
shown by Weismann, Viallanes, and Van Rees in the Muscidæ. On this
point Gonin disagrees with Dewitz, who stated that the walls of the
wing-sacs are not destroyed, but are only gradually withdrawn at the
time of pupation, in order to allow the orifice to distend and let
the wing pass out to the exterior.

The portion of the sac which persists (basal portion, peripheral pad
of Bugnion, or annular zone of Künckel) serves at first to attach
the appendage, while forming, to the hypodermis of the larva, then
afterwards to more or less completely regenerate the adjoining
portion of the integument. In this way the hypodermis of the thorax
is partially, that of the head is almost entirely, replaced by the
imaginal epithelium which proliferates at the base of the
appendages,[113] while that of the abdominal segments persists, at
least in a modified way, and only undergoes (at the end of the pupal
period) transformations as regards the appearance of the scales and
pigment.

=The wings.=—The imaginal buds of the wings do not participate in the larval moults. Gonin has observed, contrary to Dewitz, that their surface only forms a cuticle towards the end of the last larval stage.

The network of fine tracheæ of the wing-bud is drawn out at the time of pupation with the internal cuticle of the large tracheæ. The permanent tracheæ of the wing have already appeared at the time of the 3d moult under the form of large rectilinear trunks, the position of which corresponds afterwards to that of the veins, but they are not filled with air until the time of pupation. There are from eight to ten of these tracheæ in each wing (Fig. 159), and they give rise in the pupa to a new system of fine tracheæ (tracheoles) which replaces that of the larva. (For further details the reader is referred to pp. 126–137.)

=Development of the feet and the cephalic appendages.=[114]—In the apodous larvæ of Diptera and Hymenoptera the rudiments of the legs are, like those of the wings, developed within hypodermal sacs; at times they remain there up to the end of larval life, but sometimes they appear early at the surface. This origin of the legs, thanks to Weismann, Künckel, and Van Rees, is well known in the Diptera; in the Hymenoptera it has been proved to be the case with ants by Dewitz, and in Encyrtus by Bugnion. As for the Lepidoptera our knowledge that the legs of the imago arise from the six thoracic legs of the caterpillar, up to the date of Gonin’s paper has not been in advance of that of Malpighi and Swammerdam.

Réaumur, moreover, was supposed to have furnished the proof, having
from his experiments concluded that “if the legs of the pupa appear
longer and larger than those of the caterpillar wherein they were
contained, it is because they were folded and squeezed.” (8^e Mém.,
p. 365.)

This explanation of Réaumur’s has been generally accepted. Graber
(Die Insekten, p. 506) accepted it, after examining microscopic
sections of the legs, and Künckel averred that “Réaumur, having, in
certain caterpillars, completely cut off one of the thoracic legs,
had concluded that the butterfly which came from it lacked the
corresponding member.” (Rech. sur l’org. et dév. des volucelles, p.
160.)

Newport, it is true, denied this disappearance of the legs, but did
not wish to put himself in opposition to received ideas, and
supposed that the member cut off was partly reformed in the imago.

Künckel believes that he has found a better solution in his theory
of histoblasts or imaginal buds; in his opinion, “Réaumur and
Newport are both right,” but “when Réaumur cut off a caterpillar’s
leg, he at the same time removed the histoblast, the rudiment of the
leg of the butterfly. When Newport repeated this experiment, he
simply mutilated the histoblast without completely destroying it: in
the first case, the adult insect was born with one leg less; in the
second case, it appeared with an atrophied foot.”

“So ingenious an explanation,” says Gonin, “is not necessary.” To
prove that the experiments of the two savants are not contradictory,
it would have been sufficient to cite, as Künckel did not do, the
exact words of Réaumur, for he having cut from a caterpillar “more
than half of three of the thoracic legs on the same side,” says he
found that the chrysalis had “the three limbs on one side _shorter_
than the corresponding ones on the other side.” The same operation
repeated on a somewhat younger caterpillar again showed in the
chrysalis three maimed limbs, “so that they could not be said to be
entirely absent. These results are like those of Newport; the
interpretation only was faulty, as we shall attempt to prove.”

The real relations of the adult legs to the larval legs are thus shown by Gonin.

“If we carefully strip off the skin of a caterpillar near the time of pupation (Fig. 608), we see that the extremity only of the legs of the imago is drawn out of the larval legs; the other parts are pressed against each side of the thorax: near the ventral line a small pad represents the coxa and the trochanter; the femur and the tibia are distinctly recognizable, but soldered to each other and only separated by a slight furrow; they form by their union a very acute knee or bend. The femur is movable on the pad-like coxa, the tibia continues without precise limits with the extremity concealed in the larval legs. The three divisions of the latter do not appear to have any relation with the live joints of the perfect state. Under the microscope the rudiment appears very strongly plaited at the level of the tarsus, much less so in the other regions. A large trachea penetrates into the femur with some capillaries; reaching the knee it bends into the tibia at a sharp curve, but does not become truly sinuous in approaching the extremity. It is then the tarsus especially which is susceptible of elongation; it may, on being withdrawn, give rise to the illusion that the whole organ is disengaged from the larval leg.

“This disposition is, we believe, not known. It gives the key to the experiments of Réaumur and of Newport.

“Even when we cut off the limb of the caterpillar at its base, we only remove the tarsus of the imago; the femur and the tibia remain intact. From an evident homology Réaumur has erroneously concluded that there is an identity. His opinion, classical up to this day, that the limb of the butterfly is entirely contained in the leg of the caterpillar, has been found to be inexact and should be abandoned.”

=Embryonic cells and the phagocytes.=—Up to the last larval stage the legs do not offer, says Gonin, any vestige of an imaginal germ, but they contain a great number of embryonic cells (Fig. 145, _ec_). They are almost always collected around a nerve or trachea; sometimes they are independent, and sometimes retained in the peritoneal sheath, seeming to arise by proliferation from this sheath. Some thus contribute to the lengthening of the tracheal branches or nerves, and the others, becoming detached, form leucocytes or phagocytes. They are very numerous in the legs, at the beginning of the 4th stage, but are disseminated some days later throughout the whole cavity of the body. At the time of histolysis they attack the larval tissues and increase in volume at their expense; in return they serve for the nutrition of the imaginal parts and exercise no destructive action on them. Van Rees agrees with Kowalevsky in comparing these attacks of the embryonic cells, sometimes victorious and sometimes impotent, to the war which the leucocytes wage against both the attenuated and the virulent bacteria.

=Formation of the femur and of the tibia, transformation of the tarsus.=—Capillary tracheæ appear in the leg at the same time as in the wing. They arise from the end of a tracheal trunk near the base of the limb on the dorsal and convex side. After the 3d moult the hypodermis thickens near this place; in a few days a pad is formed there and then a large imaginal bud with a circular invagination. These buds were noticed by Lyonet, who supposed them to be “les principes des jambes de la phalène.” Nerves and a tracheal branch penetrate into the femoro-tibial bud and form a small bay or constriction which marks the point of junction of the femur with the tibia, and the body-cavity remains in direct communication with the end of the limb.

FIG. 608.—Feet of the Pieris butterfly withdrawing from those of the
larva.
]

FIG. 609.—Imaginal feet of Pieris uncovered with great care to
preserve the position which they had in the larva: _ta_, tarsus;
_t_, tibia; _g_, knee; _f_, femur; _h_, coxa.
]

The tarsus undergoes a series of changes; the surface is folded in a very complicated way; at the level of each articulation, but only in the internal and concave region of the leg, is developed a deep fold; on one side there is a hypodermic thickening, on the other a simple leaf of the envelope, which afterwards joins at its base with the parietal hypodermis, and then two leaves are destroyed with the large cells of the setæ. The internal part and end of the tarsus are then reconstituted with the elimination of the débris, while the external and convex region undergoes direct regeneration.

The coxa and trochanter are derived from the base of the larval leg, and only the 1st pair are well separated from the base of the thorax. One or two days before pupation the femoro-tibial bud, after having, until now, preserved its antero-posterior direction, is placed transversely as regards the larva, then becoming directed obliquely forward. This rotatory movement of the coxa may be attributed to the great extension of the fore wings, which push before them the two first pairs of legs. The last pair in their turn are simply covered by the hind wings and are but slightly displaced. This new position of the legs is that of the imago: the knee of the 1st pair is situated in front of the tarsus; that of the 2d a little outward; that of the 3d pair is directed backward. (Gonin.)

=The antennæ.=—These appendages also have the same relation with those of the caterpillar as in the case of the legs, the larval appendages being only the point of departure of the imaginal growth. Weismann has observed in Corethra how at the approach of each moult an invagination like the finger of a glove allows the antenna to elongate from its base. The process, says Gonin, is identical in the caterpillar of Pieris. At the last moult the invagination is so pronounced that it is not effaced with the renewal of the chitinous integument. Several days later it again begins to grow larger. As the imaginal bud gradually sinks into the cavity of the head, it presses back the hypodermic wall and thus forms an envelope around it. Its base, widely opened, gives admission to the nerves, besides capillaries and sometimes a large trachea.

FIG. 610.—Larva in same stage as Fig. 613; side view of head and
thorax: _a_, _a′_, wings, with the folds on the surface, and the
sinuous track of the tracheal bundles; _st I_, prothoracic stigma;
_p_, _p′_, ends of the legs.
]

As soon as it reaches the posterior region of the head, the antenna in lengthening becomes folded and describes the great curves which led Réaumur to compare it to a ram’s horn (Fig. 613). The leaf of the envelope thickens in the interior and all around the base of the organ. Its ultimate rôle is closely like that of the two other hypodermic formations. It is at the outset this layer of cells which in the larva supports the ocelli. This layer, hidden on each side under the parietal region, thickens and regenerates, forming a circular pad which becomes more prominent and finally assumes the form of the compound eye of the imago.

FIG. 611.—Head of the larva just before pupation: between the two
mandibles (_m_) is seen the relief of the tongue or maxillæ (_m′_);
_f_, spinneret; _l_, labrum; _a_, antenna.
]

FIG. 612.—Same stage as in Fig. 611, but after the removal of the
larval skin, and including the lateral scale: _A_, side, _B_, front,
view; _c_, “cimier” (the dotted line shows the position it takes in
the pupa); _a_, antenna; _o_, eye; _t_, tongue.—This and Figs.
608–611, after Gonin.
]

Finally, this layer gives rise to a conical prolongation (Fig. 612, _c_), which after exuviation appears as a tuft of long hairs, and is called by Gonin the crest (cimier, Fig. 612), which is characteristic of the pupæ of Pieridæ. It is only differentiated towards the end of the 4th larval stage in a median depression of the vertex. It is an imaginal bud in the most general sense of the word.

FIG. 613.—Larva of _Pieris brassicæ_ stripped of its skin some minutes
before pupation: the antennæ (_a_) have been displaced, and the
tongue cut off, to show the palpi (_p_); _c_, cimier: _o_, eye; _m_,
vestige of a mandible; _t_, insertion of the tongue (see Fig. 612);
_aa_, fore, _ap_, hind, wings; _g_, knee of a foot of the 3d pair.
]

On each side the base of the antenna comes in contact with the germ of the crest. The envelopes approach each other, and their thickened part constitutes with the ocular disks a new cephalic wall. The head of the butterfly thus marked off is triangular; all the larval parts remaining out of this area then disappear. The muscles and the nerves are resorbed by histolysis, then the external part of the imaginal envelopes and the old parietal hypodermis, reduced very thin and degenerated, is detached in shreds. The antenna becomes external throughout its whole extent. The transformation is in this case, then, almost as complete as in the thorax of Diptera or Hymenoptera. It is necessitated by the change of form and of volume of the head. The region of the ocelli persists unchanged almost alone from the larva to the imago also. The limit is not well marked between the portion which is the replacement or direct renovation of the epithelium.

=Maxilla and labial palpi.=—The development of the tongue (1st maxillæ) is so like that of the antennæ that it scarcely needs description. Beginning at the last moult, the hypodermic contents of the maxillæ is withdrawn in the cephalic cavity under the form of a hollow bud whose base is turned inward. The invagination remains less distinct than in the antennæ; it does not even reach to the anterior part of the œsophagus. The two symmetrical halves of the tongue approach each other and are thrice folded. When the caterpillar stops feeding, they each curve in in the form of an S, remaining lodged under the floor of the mouth (Fig. 613, _t_).

Underneath are to be seen two other buds, which by an identical process become the labial palpi (Figs. 614, 615, _p_).

At the anterior part of the head, where the organs are very close together, the envelopes form several folds without any further use (Fig. 615, _r_). The two leaves then fuse together and decay as at the surface of the tarsus.

Finally, in the mandibles and the labrum, there is only a cellular thickening without any invagination.

FIG. 614.—Section through the anterior region of the head of Pieris
larva, four days after the 3d moult: _o_, œsophagus; _m_, _m_, 1st
maxillæ containing the two imaginal buds of the tongue; _p_, _p_,
labial palpi; _Tr_, trachea.
]

FIG. 615.—Section through the same place as in Fig. 614, 10 days after
the 3d moult, the imaginal appendages having grown in size: _r_,
_r_, caducous folds of the old hypodermis and of the envelopes.
Other letters as in Fig. 614.—This and Figs. 613–614, after Gonin.
]

=Process of pupation.=—Notwithstanding the great number of persons who have reared Lepidoptera, close and patient observations as to the exact details are still needed. Gonin, who has made the closest observations on Pieris, pertinently asks why the antennæ, which are appendages of the head, are visible in the abdominal region, and why the tongue (maxillæ) is extended between the legs as far as the 3d abdominal segment. To answer these questions he made a series of experiments. Selecting some caterpillars which were about to pupate, he produced an artificial metamorphosis by removing the cuticula in small bits. Exposing the appendages in this way, they preserved the position which they are seen to take during growth. Each wing appeared within the limits of the segment from which it grew out (Fig. 610), not extending beyond, as it does in the normal pupa, so that Réaumur was wrong in saying that “the wings are here gathered on each side into a kind of band, which is large enough to lie in the cavity which is between the 1st and 2d segment.” (8^e Mém., p. 359.)

All these parts are coated with a viscous fluid secreted by special glands, which hardens after pupation upon exposure to the air. So long as the parts are soft, they can easily be displaced. Gonin drew one of the antennæ like a collar around the head, and one half of the tongue upon the outer side of the wing.

“When pupation is normal, the integument splits open on the back of the thorax, and the pupa draws itself from before backwards. Owing to the feeble adherence which the chitinous secretion gives it, it draws along with it the underlying organs. The legs, antennæ, the two halves of the tongue (maxillæ) retained by their end, each in a small chitinous case, can only disengage themselves from it when in elongating they have acquired a sufficient tension. The curves straighten out and the folds unbend. The chitinous mask of the head in withdrawing from the larval skin follows the ventral line; the tongue and labial palpi free themselves from its median part; the antennæ disengage themselves from the two lateral scales. Between these different appendages a space is left on the surface of the head for the eyes, and on the thorax for the legs. These are not completely extended on account of the lack of freedom of the femoro-tibial articulation; the femur preserves its direction from behind forwards, and the knee in the two first pairs remains at the same height. The wings overlie them and cover the under side of the two basal abdominal segments; their surfaces in becoming united increase much in size.”

As the chitinous frame of each spiracle gradually detaches itself, we see a tuft of tracheæ passing out of the orifice. It is at this moment that the provisional tracheal system is cast off, and it is easy to see that the process is facilitated by the simultaneous elongation of all the appendages. The permanent tracheæ can follow this elongation because they are sinuous, and need only to straighten their curves. It is, however, not the same with the tracheoles, as we have seen in the case of the wings (p. 133), and their extension or stretching is thus explained by a very simple mechanism.

“The position which the organs assume in the chrysalis is not due to
chance, everything is determined in advance, and the microscope
shows us that the structure of the hypodermis is specially modified
in all the parts which remain external. It is a fact well known to
those who rear Lepidoptera that if this normal arrangement is
disturbed there are few chances that the perfect insect will
survive. A leg lifted up, or an antenna displaced, leaves a surface
illy protected against external influences. Almost always this
accident causes a drying of the chrysalis.

“Several interesting experiments may be cited as bearing on this
subject. If during transformation the chitinous mask of the head is
separated from the integument beneath, it is arrested half-way in
its development, and the antennæ and tongue are not fully extended.
When the case or skin of the caterpillar is drawn, not from before
backward, but in the opposite direction, all the appendages of the
thorax are placed perpendicularly to the body. Dewitz and Künckel
d’Herculais, in stating that the skin of the caterpillar splits open
along its whole length, show that they were ignorant of the
mechanism; for it is precisely because the chitinous larval skin
splits open only in front that it preserves sufficient adherence to
the organs beneath to draw them after it in the direction of the
abdomen.

“To only read modern authors, one would suppose that the mechanism
of pupation had remained hitherto unknown. In reality, it did not
escape the notice of Swammerdam or of Réaumur, both of whom have
described it with care. The first attached too much importance to
the flow of blood, the action of which would be rather to push the
organs out than to extend them over the surface of the thorax; the
second insists on the movements of the insect. This factor, very
admissible in caterpillars, ‘whose under side is situated on a
horizontal plane’ (iii, 9^e Mémoire, p. 395), cannot be invoked for
those which suspend themselves by the tail, as in the genus
Vanessa.” (Gonin.)

_b._ The Hymenoptera

In the Hymenoptera, Ratzeburg was the first to figure and describe the numerous intermediate stages between the larva and pupa, his subjects being the ants, Cynips, and Cryptus, which pass through five stadia before assuming the final pupal shape.

In the bees, as we have observed in the larvæ of Bombus (Proc. Bost. Soc. Nat. Hist., 1866), after hardening a series in alcohol of young in different stages of development, it will be found difficult to draw the line between the different stages since they shade insensibly into each other, those represented in Fig. 616 being selected stages. The head of the incipient semipupa distends the prothoracic segment of the larva whose head is pushed forward and the thoracic segments are much elongated, while the appendages and wings are well developed, and have assumed the shape of those of the pupa. Development both in the head and thorax begins in the most important central parts, and proceeds outwards to the periphery. During this period the “median segment,” or 1st abdominal, has begun to pass forward and to form a part of the thorax.

FIG. 616.—Transformation of the bumblebee, Bombus, showing the
transfer of the 1st abdominal larval segment (_c_) to the thorax,
forming the propodeum of the pupa (_D_) and imago: _n_, spiracle of
the propodeum. _A_, larva; _a_, head; _b_, 1st thoracic, _c_, 1st
abdominal, segment. _B_, semipupa; _g_, antenna; _h_, maxillæ; _i_,
1st, _j_, 2d leg; _k_, mesoscutum. _l_, mesoscutellum; _m_,
metathorax; _d_, urite (sternite of abdomen); _e_, pleurite; _f_,
tergite; _o_, ovipositor; _r_, lingua; _q_, maxilla.
]

In what may be termed the 3d stage (Fig. 616, _C_), though the distinction is a very arbitrary one, the change is accompanied by a moulting of the skin, and a great advance has been made towards assuming the pupal form. The abdomen is very distinctly separated from the thorax, the propodeum being closely united with the thorax, and the head and thorax taken together are nearly as large as the abdomen, the latter now being shorter and perceptibly changed in form, more like that of the completed pupa, while there are other most important changes in the elaboration of the parts of the thorax, particularly the tergites, and of the head and its appendages. Meanwhile the ovipositor has been completed and nearly withdrawn within the end of the abdomen.

The next to study the transformations of the Hymenoptera was Ganin, who discovered the early remarkable pre-eruciform larvæ, as we may call them, of certain egg-parasites (Proctotrypidæ). He discovered the imaginal buds of the wings in the third larva of Polynema (Fig. 185), but his observations, and those of Ayers, need not detain us here, as they have little to do with the subject of the normal metamorphosis of the Hymenoptera, and will be discussed under the subject of Hypermetamorphosis.

To Bugnion we owe the first detailed account of the internal changes in the Hymenoptera, his observations being made on a chalcid parasite, _Encyrtus fuscicollis_, a parasite of Hyponomeuta. The apodous larva (Fig. 618) moults but once, the next ecdysis being at the time of pupation. It passes through a semipupal stage.

FIG. 617.—Encyrtus larva: 1, 2, 3, ganglia in front of the brain; _m_,
mouth; _s. gl_, silk-gland; _br_, brain; _n_, nervous cord; _w_, bud
of fore, _w′_, bud of hind, wing.
]

Bugnion observed in the larva of Encyrtus three pairs of lower thoracic or pedal imaginal buds, two pairs of upper or alary buds, a pair of ocular or oculo-cephalic buds destined to build up all the posterior part of the head, a pair of antennal buds, and three pairs of buds of the genital armature (ovipositor). He also detected the rudiments of the buccal appendages under the form of six small buds (Fig. 619), which do not invaginate, and are not surrounded by a semicircular pad. Also in the abdomen, behind each pair of stigmata, there is a group of hypodermic cells (Fig. 617), which, without doubt, correspond to the wing-buds, but are not differentiated into a central bud and its pad, and does not merit the name of imaginal bud. In fact, except the eye-buds, which are unlike the others, he only observed the imaginal buds of the legs, wings, and ovipositor. The antennal buds are, like those of the buccal appendages, without an annular zone.

The pedal buds were detected in the middle of larval life. They each form a central bud surrounded by a circular thickening. They gradually elongate and become tongue-like and somewhat bent; soon a linear opening or slit appears, forming the mouth of a cavity which communicates with that of the body, allowing the passage into them of the tracheæ, muscles, and nerves, and afterwards of the blood. Finally, the buds grow longer and slenderer, are bent several times, and show traces of the articulations; and soon under the old larval skin, now beginning to rise in anticipation of the moulting, we see the coxa, femur, tibia, and tarsus of the perfect insect, the tarsal joints not yet being indicated.

FIG. 618.—Older Encyrtus larva, lateral view, showing the buds of the
antennæ (_ant_), legs, and wings (_w_, _w′_): _oe_, œsophagus;
_q^1_, _q^2_, _q^3_, buds of the genital armature; _o_, rudiment of
the sexual gland (ovary or testis); _ur.t_, urinary tube; _st_,
stomach; _i_, intestine (rectum); _n_, ventral nervous cord; _r_,
rectum; _sp^1_-_sp^9_, spiracles.
]

FIG. 619.—A still older larva, ready to transform. The imaginal buds
of the antennæ (_f_), eyes, wings (_a^1_, _a^2_), and legs have
become elongated: _ch_, chitinous arch; _b_, mouth; _o_, eye-bud;
_g_, brain; _e_, stomach; _x_, rudiment of the sexual glands (either
the ovary or testis).—This and Figs. 617 and 618, after Bugnion.
]

The wing-buds (_a^1_, _a^2_) appear at the same time as those of the legs, as racket-shaped masses of small cells situated directly behind the 1st and 2d pair of stigmata, in contact with the tissue ensheathed by the corresponding tracheal vesicle (Fig. 618). Afterwards they have exactly the form of those of the Lepidoptera (Fig. 619).

The proliferation of the hypodermis is not limited to the thorax, but takes place at corresponding points in the first seven abdominal segments. These abdominal agglomerations of cells do not give rise to true buds, but serve simply to reconstitute the hypodermis of the abdominal segments at the time of metamorphosis.

=Ocular or oculo-cephalic buds.=—The eye of insects, as is well known, is a modification of a portion of the integument, the visual cells being directly derived from the hypodermis, the cornea being a cuticular product of this last, like chitinous formations in general.