Chapter XXX: Part III: The Metamorphoses of Insects (1)

We have seen that the embryo rapidly passes through extraordinary changes of form, and now, after hatching, especially in the insects with a complete metamorphosis, the animal continues to undergo striking changes in form, in adaptation to different modes of life.

The life of a winged insect, such as a butterfly, fly, or bee, may be divided into four stages: the embryo, or egg state, the larva, pupa, and imago,—the term _metamorphosis_ being applied to the changes after birth, or post-embryonic stages of life. The transformations of the more specialized orders of insects involve wonderful changes of form, which are only paralleled in other types of animals by the metamorphoses of the echinoderms, of certain worms, and of the Crustacea, as well as by those of the frog. An insect, such as a butterfly or bee, during its post-embryonic life lives, so to speak, three different lives, having distinct bodily structures and existing under quite dissimilar surroundings and habits; so that a caterpillar is practically a different animal from the pupa, and the latter from the imago, with different organs, the appendages and other structures being so modified as to be, so far as regards their functions, radically different. These changes of functions or of habits have also been plainly enough the exciting cause of the divergency in structure of what fundamentally is one and the same organ, the change having been brought about by adaptation of the same organs to quite different uses.

The changes are not only observable in the body and its appendages, but also in the internal organs, and consequently are both structural and physiological. The term _larva_, as applied to the first stage of animals, is a very variable and indefinite one, that of insects in general being a much more highly organized animal than the larva of a worm, starfish, or crustacean.

_a._ The nymph as distinguished from the larval stage

As there is no marked difference between the different stages of the young in the insects with an incomplete metamorphosis (Heterometabola), the chief difference being the possession of the rudiments of wings and the absence of a resting stage, the terms _larva_ and _pupa_ are in reality scarcely applicable to them, and we much prefer the term _nymph_, first proposed by Lamarck for the active “pupa” of Orthoptera, Hemiptera, the Odonata and Ephemeridæ, and adopted in part by many. Indeed, in the more generalized and older orders, the larval and pupal stages are not differentiated, though the term _larval_, in its general sense, will probably always be used; just as we speak of the larval stages of worms, echinoderms, or Crustacea.

Eaton in his elaborate work on the Ephemeridæ employs the term
_nymph_ to designate all the aquatic or early stages in the
development of the young after hatching, and he urges that the
old-fashioned usage of _larva_ and _pupa_ seem scarcely worth
retention. “Nymphs are young which live an active life, quitting the
egg at a tolerably advanced stage of morphological development and
having the mouth-parts formed after the same main type of
construction as those of the adult insect.” The word _nymph_ is used
in the same sense by McLachlan, and by Cabot. Calvert also applies
the term _nymph_ “to the stage of odonate existence between the egg
and the transformation into the imago.” On the other hand, Brauer
applies the term _nymph_ to the pupa of holometabolous insects. For
larval Hyatt proposes the term _nepionic_.

_b._ Stages or stadia of metamorphosis

The intervals or periods between the moults or ecdyses of caterpillars and other eruciform larvæ are called stages or _stadia_; thus, as most caterpillars moult four times, we have five stages or stadia, or stage (stadium) I to V. As observed by Sharp, there is, unfortunately, no term in general use to express the form of the insect at the various stadia; “entomologists say, ‘the form assumed at the first moult,’ and so on.” Hence he adopts a term suggested by Fischer,[86] and calls the insect as it appears after leaving the egg the first _instar_, and what it is after the first moult the second instar, and so on; hence the pupa, or chrysalis, which assumed that condition after moulting five times would be the sixth instar, and the butterfly itself would be the seventh instar.

_c._ Ametabolous and metabolous stages

In the Synaptera development is direct, the young differing neither in form, structure, or habits from the adult. Hence they are said to be _ametabolous_. Since there is an absence of even a tendency to a partial metamorphosis, it is evident that the insects have not inherited a tendency to undergo a transformation, but that it is an adaptation induced in the hexapod type after the first winged insects appeared, and which became more marked in the more specialized insects and at a period comparatively late in geological history, _i.e._ perhaps at or soon after the beginning of the Carboniferous period.[87]

The transformations of the pterygote insects vary greatly in degree, and it is difficult to draw the line between the grades. Those in which the adults differ from the freshly hatched young only or mainly in having wings are generally said to have an incomplete or gradual metamorphosis. There is no inactive, resting, or pupal stage, and the wings are acquired only after successive moults. Insects with an incomplete metamorphosis are the Orthoptera, Dermaptera, Platyptera (Mallophaga, Plecoptera, Corrodentia, Embidæ), Ephemeridæ, Odonata, Thysanoptera, and Hemiptera, with the exception of the male Coccidæ, in which there is a resting or sub-nymph stage. As regards the number of moults in the Synaptera, Grassi states that in Campodea there is a single fragmentary ecdysis, while Sommers tells us that _Macrotoma plumbea_ sheds its skin throughout life, even after attaining its full size.

As an example of the partial metamorphosis of the hemimetabolous insects we may select that of the locust, in which there are five moults and six stages (instars), as seen in Fig. 558, five of which are nymphal. In the first two stages there are no rudiments of wings, these appearing after the second moult. Besides the acquisition of wings there are slight differences after each moult, both in structure and color, besides size, so that we may always recognize the comparative age and the particular stage of growth of any individual.[88]

We have watched the development of _Melanoplus spretus_ from the egg
to the imago, and examined thousands of specimens which show the six
stages. On the other hand, European authors differ as to whether
there are three, four, or five moults in the migratory locust.[89]
It is not improbable that, as is the case with many other insects,
the number of moults may vary according to the temperature and food,
variation in these agencies causing either retardation or rapidity
in development.

Those with a complete metamorphosis are said to be _metabolous_ or _holometabolous_. (Lang.)

Leach[90] in 1815 gave the name of Ametabola to insects without, and Metabola to insects with a metamorphosis.

FIG. 558.—Partial metamorphosis of _Melanoplus femur-rubrum_, showing
the five nymph stages, and the gradual growth of the wings, which
are first visible externally in 3, 3_b_, 3_c_.—Emerton _del._
]

Latreille (1831) called insects with an incomplete metamorphosis
_homotenous_ (which means similar to the end of life), and those
with a complete metamorphosis, _polymorphous_. For the different
degrees of metamorphosis of insects he employed two terms: for the
incomplete degree, _metamorphosis dimidia_, and for the total or
pupal, _metamorphosis perfecta_.

Westwood in his Introduction to the Modern Classification of Insects
(1839), taking into account the relation of the larva with the
imago, divided insects into two divisions: the _Heteromorpha_, or
those in which there is no resemblance between the parent and its
offspring, and _Homomorpha_, in which the larva resembles the imago,
except in the absence of wings.

FIG. 559.—Manometabolous metamorphosis of the cockroach (_Phyllodromia
germanica_) with its four nymphal stadia _a-d_; _e_, _h_, adult;
_f_, female with egg-case; _g_, egg-case.—From Riley.
]

From the point of view of the degree of metamorphosis, insects have been divided into _Heterometabola_ and _Metabola_.

I. _Heterometabola._—This group may be divided as follows:

1. _Manometabola_,[91] embracing those forms with a slight or gradual metamorphosis, but which are active in all the stages, without any resting stage. The orders passing through this degree of metamorphosis are the following: Orthoptera, Dermaptera, Platyptera, Thysanoptera, and Hemiptera (Coccidæ excepted).

In all these groups, the only external differences of importance between the freshly hatched nymph and the adult is the presence of wings. The chief difference internally is the complete development of the sexual glands.

It should be observed, however, that in the last nymph stage of the Thysanoptera the articulations of the limbs are enveloped by a membrane and the wings enclosed in short fixed sheaths; the antennæ are turned back on the head, and the insect, though it moves about, is much more sluggish than in the other state. (Haliday.) Hence here we have a close approach to the following degree.

2. _Heremetabola_,[92] including those forms with a gradual though slight or incomplete metamorphosis, but with a quiescent or resting stage at the close of the nymph life. Lang has emphasized this stage, calling attention to the fact that the fore legs of the nymph of the 17–year Cicada, which lives underground on the roots of trees, are thick and adapted for digging. The transition from the nymph to the winged adult is signalized by the decided change in form of the fore legs, as well as by the acquisition of the wings. “The last larval stage is, then, what is called _quiescent_, _i.e._ the organization of the imago develops within the chrysalis at the expense of the accumulated reserve material.” (Lang.) There seems to be a resting stage, when the insect does not perhaps suck the sap from the roots, and awaits in its chamber its approaching change to the imago; but we should scarcely apply the term _pupa_ to this stage, though the antennæ of the freshly hatched larva are larger and longer than in the fully grown nymph and are distinctly 8–jointed.

3. _Hemimetabola._—In this division, so named by Brauer, the changes are more marked, though there is no truly inactive pupa-like stage. The orders are Perlaria (Plecoptera), Odonata, and Plectoptera (Ephemeridæ). The freshly hatched nymphs of these three groups are much alike in shape, that of Perlidæ, and indeed most of the Platyptera, being more generalized, unless we except that of Chloëon; all closely recall Campodea, and are therefore in the Campodea-stage. These nymphs are indeed more generalized than the freshly hatched nymph of Blattidæ, or any other of the orders mentioned except the Platyptera, to which perlids belong. They all have feet, and the body is more or less flattened. (Fig. 560.)

II. _Holometabola._—In this division we have for the first time a true larva, and a pupa stage as distinguished from the imago. Moreover, the insect at each stage is distinguished by radical differences in form, surroundings, and in the nature of the food, while the pupa is inactive, usually immovable, and incapable of taking any food, and is often protected by a cocoon spun by the larva. The holometabolous orders are the Neuroptera, Coleoptera, Mecoptera, Trichoptera, Lepidoptera, Siphonaptera, Diptera, and Hymenoptera.

As we have among worms, echinoderms, and Crustacea certain
exceptional species in a metamorphic group whose metamorphosis is
suppressed, their development being direct, so there is in pterygote
insects, though in a very much less degree, cases of direct
development. In the wingless cockroaches such as Pseudoglomeris,
etc., of the tribe of Periphæriides, in some of which, however, the
males are winged, and in the Hemiptera, occur wingless forms such as
the lice and bed-bug. The Mallophaga are all wingless, while certain
Dermaptera (Chelidura, Anisolabis) are also apterous. The absence of
wings in such cases is due to disuse from parasitism, or to a life
under stones or in cracks and fissures, where the insects are driven
to avoid their enemies, and hence do not need wings. The growth of
wings and consequently the development of a metamorphosis is
suppressed, so that, as Lang says, “in contrast to the original
ametabola of the Apterygota, we have here an _acquired ametabola_.”

It is rare that, after the rudiments of wings have once appeared in
the very young, they should disappear in the late nymph stage; this
is, however, said by Walsh to be the case with the Ephemerid Bætisca
(Fig. 440). This is a case of retardation in an acquired
ametabolesis.

THE LARVA

The term _larva_ is peculiarly applicable to the young of the holometabolous orders. The name (Latin, _larva_, a mask) was first given to the caterpillar because it was thought by the ancients to mask the form of the perfect insect. Swammerdam supposed that the larva contained within itself “the germ of the future butterfly, enclosed in what will be the case of the pupa, which is itself included in three or more skins, one over the other, that will successively cover the larva.” What led to his conception of the nature of these changes was probably his observations on the semitransparent larva of the gnat, in which the body and limbs of the pupa can be partially seen; for Weismann has shown that the great Dutch observer’s belief that the pupal and imaginal skins were in reality already concealed under that of the larva is partially founded in fact. Swammerdam states: “I can point out in the larva all the limbs of the future nymph, or Culex, concealed beneath the skin,” and he also observed beneath the skin of the larvæ of bees, just before pupating, the antennæ, mouth-parts, wings, and limbs of the adult. But, as we shall see farther on, the discovery by Weismann in the larva of the germs of the imago has completely changed our notions as to the nature of metamorphosis, and revolutionized our knowledge of the fundamental processes concerned in the change from larva to pupa, and from pupa to imago.

Not only are the larvæ of each order of insects characteristic in form, so that the grub or larva of beetles is readily distinguished from those of other orders, or the maggot of flies from the apodous larva of wasps and bees, but within the limits of the larger orders there is great diversity of larval forms, showing that they are the result of adaptation to their surroundings. This is especially the case with the larvæ of the Coleoptera, Lepidoptera, Diptera, and Hymenoptera.

In general, the larvæ of insects may be divided into two types,—the _Campodea-form_, or campodeoid, sometimes called thysanuriform, and the _eruciform_.

_a._ The Campodea-form type of larva

This is the most primitive and generalized type of larva (Fig. 560). A Campodeoid larva is one nearest in general shape to Campodea, the form which we have seen to be the nearest allied to the probable ancestor of the insects, and it also resembles the nymphs of the heterometabolous insects, before the appearance of their rudimentary wings.

Brauer, in 1869,[93] first suggested that the larvæ of a great number of insects may be traced back to Campodea and Iapyx. The Campodea-form larva is active, with a more or less flattened body, well developed mandibulate mouth-parts, and usually long legs. The nearest approach to the form of Campodea is the freshly hatched nymph of cockroaches (Blattidæ), Forficula, Perlidæ, Termitidæ, Psocidæ, Embidæ, Ephemeridæ, Odonata, especially the more generalized Agrionidæ, the nymphs of Hemiptera, the larvæ of certain Neuroptera, the active pedate larvæ of the more generalized Coleoptera, such as those of Carabidæ, Cicindelidæ, Dyticidæ, etc., and the first larva (instar) of Stylopidæ and Meloidæ (Fig. 560, _d_).

While the Campodea-shape is retained throughout nymphal life, of the orders above mentioned the Neuroptera and Coleoptera alone have a true resting pupal stage.

It should also be observed that great changes in the form of the nymph occur within the limits of the Orthoptera; the nymph of all the families except that of the Blattidæ, evidently the most generalized and primitive, being more or less specialized, while the nymphs of the other orders all vary in degree of specialization and modification. The process of adaptation once begun went on very rapidly, as it has in many other orders of insects, as well as in animals of other phyla.

FIG. 560.—Examples of campodeoid nymphs and larvæ: _a_, Campodea; _b_,
Podura (Degeeria); _c_, Lepisma; _d_, triungulin larva of Meloë;
_e_, Perla; _f_, Forficula; _g_, Chloëon; _h_, May-fly (Palingenia);
_i_, Æschna; _j_, Atropos; _k_, Myrmeleon; _l_, Sialis; _m_,
Corydalus; _n_, Cicada.
]

_b._ The eruciform type of larva

Brauer also sagaciously pointed out that “a larger part of the most highly developed insects assume another larva form, which appears not only as a later acquisition, through adaptation to certain definite conditions, but also arises as such before our eyes. The larvæ of Lepidoptera, of saw-flies, and Panorpidæ show the form most distinctly, and I call this the caterpillar form (_Raupenform_). That this is not the primitive form, but one later acquired, we see illustrated in certain beetles. The larvæ of Meloë and of Sitaris, in their fully grown conditions, possess the caterpillar form, but the new-born larvæ of these genera show the Campodea-form. The last form is lost as soon as the larva begins its parasitic mode of life.... The larger part of the beetles, the Neuroptera (in part), the bees and flies (the last with the most degraded maggot form), possess larvæ of this second form.” In 1871 we adopted these views, giving the name _eruciform_ to this type of larvæ, and afterwards Lubbock adopted Brauer’s views. Brauer considered that the eruciform larva was the result of living a stationary semi-parasitic life on plants, in carrion, or burrowing in the trunks and branches or leaves and buds of trees, where they do not have to move about in search of their food. The change from the Campodea-form to the eruciform larva is a process of degeneration and often of atrophy of the limbs, and, in the footless forms of dipterous and hymenopterous insects, of the gnathites, accompanied by a tendency of the body to become more or less cylindrical.

The first steps in the origination of the eruciform larva were apparently taken in the order Neuroptera, as restricted by Brauer and by myself, where, though the larvæ are campodeoid, there is a true resting pupal stage. The most generalized larval form is perhaps that of the Sialidæ (Fig. 560, _l_), in which the body tends to be slightly cylindrical, though the legs are long, and the gnathites well developed for seizing and biting their living prey. The terrestrial larvæ of the Hemerobiidæ, though modifications of the sialid larval form, are considerably specialized in adaptation to their active carnivorous habits. But the life-history of Mantispa, where there are two larval stages, gives us plainly enough the key to the mode in which the complete metamorphosis was brought about. The larva, born a true Campodea-like form, with large, long, 4–jointed legs, has a structure which would enable it to move about freely after its prey, beginning at once to live a sedentary life in the egg-sac of a spider; before the first moult it loses the use of its legs, while the antennæ are partly aborted. The result is that, owing to this change of habits and surroundings from those of its active ancestors, it changes its form, and the fully grown larva becomes cylindrical, with small slender legs, and, owing to the partial disuse of its jaws, acquires a small, round head.

EXAMPLES OF COLEOPTEROUS LARVÆ, SHOWING THE PASSAGE FROM THE
CAMPODEOID TO THE ERUCIFORM TYPE OF LARVÆ.

FIG. 561.—Coleopterous larvæ showing passage from campodeoid to
eruciform larvæ: _a_, _b_,
Harpalus; _c_, Dyticus; _d_, Staphylinus; _e_, Silpha; _f_,
Melanactes; _g_, Ludius; _h_, Elater; _i_, Donacia;
_j_, Chrysobothris; _k_, Orthosoma; _l_, Coccinella; _m_, Byrrhus;
_n_, Trox; _o_, _p_, Lachnosterna; _q_,
Labidomera; _r_, Ptinus; _s_, Anobium; _t_, Balaninus (entirely
apodous).
]

Its antennæ, mouth-parts, and legs not only retarded in growth, but retrograding and becoming vestigial, the body meanwhile becoming fat and cylindrical, an apparent acceleration of growth goes on within, with probably an enlargement of the intestine and fat-body, and thus the pupal form is perfected while the larva is full-fed and quiescent. It is not improbable that in the primitive neuropteron, as the result of a mode of life like that of Mantispa, the quiescent life of the later stages graduated into a quiescent, inactive pupal life, allowing the changes going on in the internal organs to result in a complete metamorphosis, which was transmitted to the later Neuroptera, thus making the complete metamorphosis a fixed, normal condition. It thus appears that a change of habits and of food, and more especially the fact that the nymph became so surrounded with an abundance of food close at hand that it did not have to run actively about and seize it in a haphazard manner, were the factors bringing about a change from the Campodea-form nymph to the eruciform larva, thus inducing a hypermetamorphosis.

The larvæ of the Mecoptera (Panorpidæ, Fig. 562, _b_) are still more caterpillar-like, and besides their cylindrical body, rounded head, small short gnathites, small thoracic legs, they have what appear to be 2–jointed legs to each of the nine abdominal segments, and the close resemblance to caterpillars is farther carried out by the presence of a pair of prothoracic spiracles, none existing on the other two thoracic segments.

FIG. 562.—Examples of eruciform larvæ: _a_, Phryganea; _b_, Panorpa;
_c_, Sesia; _d_, _d_, caterpillars; _e_, Selandria; _f_, Tipula;
_g_, Simulium; _h_, Chionea; _i_, Musca; _j_, Tachina; _k_, Braula;
_l_, flea; _m_, Tremex; _n_, coarctate larva of Meloë; _o_, bee
(Andrena).
]

In the Meloidæ (Fig. 560, _d_) and Stylopidæ the first larval stage is Campodea-form; the changes will be described in the subsequent section on Hypermetamorphosis, and while these cases of change from a campodeoid to an inactive eruciform larva are very salient, if we compare the graduated series of larval forms throughout the order of Coleoptera, as represented by the illustrations in Fig. 561, we shall see that in nearly, if not each, case the form of the boring or mining, or bark or bud or seed-inhabiting grub is the result of a change of habit and commissariat from active predaceous larvæ, like those of the Carabidæ and other adephagous families, together with those of the Staphylinidæ, with their flat body, big mandibles, and well-developed maxillæ, to the cylindrical bodies of such larvæ as those of Dermestes and Anthrenus, which live a more sedentary life, to the root-feeding wire-worm or elaterid larvæ, and scarabæid grubs, onward to the phytophagous Chrysomelidæ, with the mining and boring buprestids and cerambycids,—in all these forms we see a gradual atrophy of the legs, which is fully carried out in the vermiform or maggot-like larva of the weevils. These changes throughout the members of the entire order are epitomized in the life-history of the Meloidæ, in which there are three typical forms of larva: the Campodea-form (triungulin stage), eruciform (second or carabidoid stage), and vermiform (coarctate) larva.

FIG. 563.—_Prodoxus cinereus_: _a_, apodous larva; _b_, head and
prothoracic segment; _c_, anal hooks; _d_, pupa; _e_, cast pupal
shell protruding from stalk of Yucca; _f_, female; _g_, side view of
♂ clasper.—After Riley, from Insect Life.
]

FIG. 564.—Larva of _Limacodes scapha_, nat. size.
]

In the Lepidoptera the eruciform, pedate type is adhered to throughout the order, with the rare exception of the nearly apodous mining larva of Prodoxus (Fig. 563, _a_), Phyllocnistis, and Nepticula, which have no thoracic legs, and the limacodid larvæ, whose abdominal legs are totally aborted, while the thoracic ones are much reduced (Fig. 564).

In the Hymenoptera the phytophagous forms are eruciform, while by the agency of the same factors as already mentioned, _i.e._ a sedentary or parasitic life and abundance of food within constant reach, the larvæ lose their legs and become vermiform.

In the Diptera, which are the most highly specialized of insects, the maggot or vermiform shape, and absence of any legs, prevails throughout the order, though the eucephalous larvæ show their origin from a primitive eruciform type of larva. The highly specialized larvæ of the Culicidæ and Simuliidae are undoubtedly related to the earliest and most generalized types, while the maggots of the parasitic flies (Tachinidæ) and other muscids are later degradational forms, and the result of adaptation induced, as in the previous cases, by a sedentary or parasitic mode of life, living as they do immersed in an abundance of rich nitrogenous food, with the result that the mouth-parts have become atrophied by disuse, while the limbs have become entirely aborted, though the thoracic imaginal discs develop normally in the embryonic or pre-larval stages.

It appears, therefore, highly probable that the metamorphoses of insects are the result of the action of change of conditions, just as the polymorphism of Termites is with little doubt the result of differences of food and other conditions. These matters will be farther discussed under the head of Causes of Metamorphosis.

LITERATURE ON ANCESTRY OF INSECTS, ETC.

=Müller, Fritz.= Für Darwin, 1869, pp. 144, 67 Figs.

=Brauer, Friedrich.= Betrachtung ueber die Verwandlung der Insekten im
Sinne der Descendenz-Theorie. (Verhandlung d. k.k. zool. bot.
Gesell. Wien., 1869, 1 Taf., pp. 1–20.)

=Packard, A. S.= Amer. Naturalist, iii, p. 45, March, 1869.

—— Proc. Boston Soc. Nat. Hist., xiv, 1870, p. 61.

—— Amer. Nat., iv, Feb. 1871, p. 756; v, 1871, pp. 52, 567.

—— Embryological Studies. (Memoirs Peabody Acad. Sc. Salem, 1871–72.)

—— Our common insects, 1873, Chapter on Ancestry of Insects, pp.
175–178.

—— Third Report U. S. Ent. Commission, 1883, pp. 295–304.

=Lubbock, John.= On the origin of insects. (Journ. Linn. Soc., London,
xl, 1873.)

—— Origin and metamorphoses of insects. (Nature, 1873 [in book form,
1874], pp. 108, 66 Figs.)

=Mayer, Paul.= Ueber Ontogenie and Phylogenie der Insekten. (Jena.
Zeitschr. Wissens., x, 1876, pp. 125–221, 4 Taf.)

=Hyatt, A., and Arms, J. M.= Insecta. (Bost. Soc. Nat. Hist. Guides
for science-teaching, viii.) Boston, 1890, pp. 300, 13 Pls., 223
Figs.

_c._ Growth and increase in size of the larva

The rapidity of growth and enormous increase in size in early life is especially noticeable in caterpillars and other phytophagous larvæ. The latest observations are those of Trouvelot on _Telea polyphemus_. When this silkworm hatches, it weighs 1⁄20 of a grain.

When

10 days old it weighs ½ a grain, or 10 times the original weight.
20 days old it weighs 3 grains 60 times the original weight.
30 days old it weighs 31 grains 620 times the original weight.
40 days old it weighs 90 grains 1800 times the original weight.
56 days old it weighs 207 grains 4140 times the original weight.

“When,” he says “a worm is 30 days old, it will have consumed about 90 grains of food; but when 56 days old, it is fully grown and has consumed not less than 120 oak leaves, weighing ¾ of a pound; besides this it has drank not less than ½ an ounce of water. So the food taken by a single silkworm in 56 days equals in weight 86,000 times the primitive weight of the worm. Of this about ¼ of a pound becomes excrementitious matter, 207 grains are assimilated, and over 5 ounces have evaporated.”[94]

Dandolo stated that the Asiatic silkworm (_Bombyx mori_) weighs on
hatching not over 1⁄100 of a grain, but when fully grown about 95
grains. During this period, therefore, it has increased 9500 times
its original weight, and has eaten 60,000 times its weight of food.
Newport thought this estimate of the amount of food was a little too
great. But comparing it with Trouvelot’s estimate for the American
silkworm, which weighs when hatched five times as much, it would not
appear to be so. Newport found that the larva of _Sphinx ligustri_
at the moment of leaving the egg weighs about 1⁄80 of a grain, and
when fully fed 125 grains, so that in the course of 32 days it
increases about 9976 times its original weight. This proportion of
increase is exceeded by the larva of _Cossus ligniperda_, which,
boring in the trunks of trees, remains about three years in the
larva state, and increases, according to Lyonet, to the amount of
72,000 times its first weight.

Newport adds that those larvæ in which the proportion of increase is
the greatest, are usually those which remain longest in the pupa
state, as in the silkworm. “Thus Redi observed in the maggots of the
common flesh-flies a rate of increase amounting to about 200 times
the original weight in 24 hours, but the proportion of increase in
these larvæ does not at all approach that of the Sphinx and Cossus.”
From his observations on the larva of one of the wild bees
(_Anthophora retusa_) Newport believes that this is also the case
with the Hymenoptera. The weight of the egg of this insect is about
1⁄150 of a grain, and the average of a full-grown larva 68⁄10
grains, so that its increase is about 1020 times its original
weight; “which compared with that of the Sphinx of medium size, is
but as 1 to 9¾, and to a Sphinx of maximum size only as 1 to a
little more than 11.”

The growth is most rapid after the last moult. “Thus a larva of
_Sphinx ligustri_, which at its last change weighed only about 19 to
20 grains, at the expiration of eight days, when it was fully grown,
weighed nearly 120 grains.” (Newport.)

_d._ The process of moulting (ecdysis)

Insects periodically shed the exoskeleton, together with the chitinous lining of their internal organs of ectodermal origin, which thus sloughed off are called the _exuvia_. The process in the locust has been described by Riley.[95] It occupies from half to three-quarters of an hour (Fig. 565). This process has naturally, from the ease with which it can be observed, been most frequently examined in the Lepidoptera, though careful and detailed observations of the inner and outer changes are still greatly needed, especially in other orders. In the caterpillar of most moths, especially one of the more generalized bombycine moths, on slipping out of its egg-shell the head is of enormous size as compared with the body, but the latter soon fills out after the creature has eaten a few hours; the head, of course, does not during this time increase in size, and the larvæ of different instars may be exactly distinguished, as Dyar has shown, by the measurements of the head.

FIG. 565.—Process of moulting from nymph to imago in the locust (_M.
spretus_): _a_, nymph with skin just split on the back; _b_, the
imago drawing itself out, at _c_, nearly free; _d_, the imago, with
wings expanded; _e_, the same with all parts perfect.—After Riley.
]

Before the caterpillar moults, it stops feeding, and the head is now small compared with the body; the head of the second instar is now large, situated partly under the much-swollen prothoracic segment, and pushes the head of the first instar forward.

Newport has well described the mode of shedding the skin in _Sphinx ligustri_, and his detailed description will apply to most lepidopterous larvæ.

The whole body is wrinkled and contracted in length, and there are
occasionally powerful contractions and twitchings of its entire
body; the skin becomes dry and shrivelled, and is gradually
separated from the new and very delicate one of the next instar
beneath. After several powerful efforts of the larva the old skin
cracks along the middle of the dorsal surface of the mesothoracic
segment, and by repeated efforts the fissure is extended into the
1st and 3d segment, while the covering of the head divides along the
vertex and on each side of the clypeus. “The larva then gradually
presses itself through the opening, withdrawing first its head and
thoracic legs, and subsequently the remainder of its body, slipping
off the skin from behind like the finger of a glove. This process,
after the skin has once been ruptured, seldom lasts more than a few
minutes. When first changed the larva is exceedingly delicate, and
its head, which does not increase in size until it again changes its
skin, is very large in proportion to the rest of the body.” (Art.
Insecta, etc.)

Trouvelot’s account is more detailed and an advance on that of
Newport’s view. He explicitly states, and we know that he was a very
close observer, that the old skin is detached by “a fluid which
circulates between it and the worm.” His account is as follows: The
polyphemus worm, like all other silkworms, changes its skin five
times during its larval life. The moulting takes place at regular
periods, which comes around about every 10 days for the first four
moultings, while about 20 days elapse between the fourth and fifth
moulting. The worm ceases to eat for a day before moulting, and
spins some silk on the vein of the under surface of a leaf; it then
secures the hooks of its hind legs in the texture it has thus spun,
and there remains motionless; soon after, through the transparency
of the skin of the neck, can be seen a second head larger than the
first, belonging to the larva within. The moulting generally takes
place after four o’clock in the afternoon; a little before this time
the worm holds its body erect, grasping the leaf with the two pairs
of hind legs only; the skin is wrinkled and detached from the body
by a fluid which circulates between it and the worm; two
longitudinal bands are seen on each side, produced by a portion of
the lining of the spiracles, which at this moment have been partly
detached; meanwhile the contractions of the worm are very energetic,
and by them the skin is pulled off and pushed towards the posterior
part; the skin thus becomes so extended that it soon tears just
under the neck, and then from the head. When this is accomplished
the most difficult operation is over, and now the process of
moulting goes on very rapidly. By repeated contractions the skin is
folded towards the tail, like a glove when taken off, and the lining
of the spiracles comes out in long white filaments. When about
one-half of the body appears, the shell still remains like a cap,
enclosing the jaws; then the worm, as if reminded of this loose
skull-cap, removes it by rubbing it on a leaf; this done, the worm
finally crawls out of its skin, which is attached to the fastening
made for the purpose. Once out of its old skin, the worm makes a
careful review of the operation, with its head feeling the aperture
of every spiracle, as well as the tail, probably for the purpose of
removing any broken fragment of skin which might have remained in
these delicate organs. Not only is the outer skin cast off, but also
the lining of the air-tubes and intestines, together with all the
chewing organs and other appendages of the head. After the moulting,
the size of the larva is considerably increased, the head is large
compared with the body, but 8 or 10 days later it will look small,
as the body will have increased very much in size. This is a certain
indication that the worm is about to moult. Every 10 days the same
operation is repeated. From the fourth moulting to the time of
beginning the cocoon the period is about 16 days. (Amer. Naturalist,
i, pp. 37, 38.)

Little has been recorded as to the exact mode of casting the larval
skin in Coleoptera. Slingerland states that _Euphoria inda_ when
pupating sheds the larval skin off the anal end in the same way as
in caterpillars, while in _Pelidnota punctata_ the larval skin
splits down the whole length of the back, retains the larval shape,
and forms a covering for the pupa which remains inside. (Can.
Entomologist, xxix, p. 52.) The old larval skin in the Coccinellidæ
and certain Chrysomelidæ is retained crumpled up at the end of the
body, while in Dermestes, Anthrenus, etc., it cloaks the pupa.

Not only is the integument, with its hairs, setæ, and other
armatures, as well as the cornea or facets of the eyes, shed, but
also all the lining or intima of those internal organs which have
been originally derived by an ingrowth or invagination of the
ectoderm are likewise cast off, with the probable exception, of
course, of the mid-intestine, which is endodermal in its origin.
Even so early an observer as Swammerdam noticed that the internal
lining of the alimentary canal comes away with the skin. He states
that the larva of _Oryctes nasicornis_ sheds both the lining of the
colon, and of the smaller as well as the larger branches of the
tracheæ.

Careful observations are still needed on the internal changes at
ecdysis of most insects. Newport seems to have observed more closely
than any one else, notwithstanding the great number who have reared
caterpillars but have not carefully observed these points, the
extent of the process internally. He informs us: “The lining of the
mouth and pharynx, with that of the mandibles, is detached with the
covering of the head, and that of the large intestines with the skin
of the posterior part of the body, and besides these also the lining
of the tracheal tubes. The lining of the stomach itself, or the
portion of the alimentary canal which extends from the termination
of the œsophagus to the insertion of the so-called biliary vessels,
is also detached, and becomes completely disintegrated, and appears
to constitute part of the _meconium_ voided by the insect on
assuming its imago state.” (Art. Insecta, p. 876.) Newport states on
another occasion that he had “noticed the remarkable circumstance
[now explained by the fact that the mid-intestine is of endodermal
origin] that the mucous lining of the true ventriculus was not cast
off with the rest, but was discharged with the fecula.”[96]
Burmeister also observed that the smaller tracheæ as well as the
internal tunic of the colon of Libellulæ are shed.

In the apodous larvæ of Hymenoptera which live in cells, as we have
observed in those of Bombus, during the process of moulting, the
delicate skin breaks away in shreds, probably owing to the tension
due to the unequal growth of the different parts of the body. “Thus
after the skin beneath has fully formed, shreds of the former skin
remain about the mouth-parts, the spiracles, and anus. Upon pulling
upon these, the lining of the alimentary tube and tracheæ can be
drawn out, sometimes, in the former case, to the length of several
lines.”[97] We then added, “As all these internal systems of vessels
are destined to change their form in the pupa, it may be laid down
as a rule in the moulting of insects and Crustacea, that the lining
of the internal organs, which is simply a continuation of the outer
tegument, or arthroderm, is, in the process of moulting, sloughed
off with that outer integument.” We have satisfied ourself that in
the larvæ of the Lepidoptera (_e.g._ Datana) the tracheæ at the time
of ecdysis undergo a complete histolysis, and arise _de novo_ from
hypodermal cells, the so-called spiral threads originating from
elongated peritracheal nuclei. (See p. 449, Fig. 412.) This is
undoubtedly also the case with the salivary ducts, which are
strengthened and rendered elastic by tænidia like those of tracheæ.
As the urinary tubes are diverticula of the proctodæum, itself an
ectodermal invagination, they may also, though not lined with a
chitinous intima, be renewed. With little doubt the intima of the
ducts of poison, spinning, and most, if not all the other glands,
though certainly the dermal glands, is exuviated. We have found that
the lobster in moulting sheds, besides the skin with the most
delicate setæ, the lining of the proventriculus, and the apodemes of
the head and thorax, hence it is most probable that the tentorium of
the head of insects as well as the apodemes and phragmas of the
thorax are exuviated.

The formation of the inner skin, or that of any succeeding stage (instar), is due to the secretion of the structureless chitinous layer by the cells of the hypodermis, during the process of histogenesis. These cells at this time are very active, and the formation of the new layer of chitin arrests the supply of nourishment to the old skin, so that it dries, hardens, and with the aid of the fluid thrown out at this time separates from the new chitinous layer secreted by the hypodermis.

Mention of this fluid, which Newport was the first to observe, and
which he says causes the separation of the old from the underlying
fresh integument of the caterpillar, recalls a passage in
Hatchett-Jackson’s Studies in the morphology of the Lepidoptera,
which we quote on a succeeding page, where he calls attention to the
formation of such a liquid, which in the reptiles facilitates the
process of moulting, adding, “Whether such is the case with the
moult of the caterpillar, I do not know.” Is it not also possible
that the growth of the setæ or tubercles on the cuticle of the
caterpillar may likewise serve to loosen and detach the overlying
skin about to be cast off? After writing the foregoing, we find that
Miall and Denny have suggested that the setæ of the cockroach
probably serve the same purpose as the casting-hairs of the crayfish
and reptiles.

It is well known that in the crayfish and in lizards the skin is
first loosened by the growth of temporary hairs or setæ, which
locally grow inward from the old cuticle and push the skin away when
it is shuffled off by the movements of the body, jaws, and limbs, as
well as the body in general.[98]

Such spines arise in the pupa of many insects, for Verhoeff finds that the spines and teeth of pupal fossorial and other Hymenoptera, as well as Coleoptera, function as moulting-processes for loosening and pushing off the last larval skin, rather than for locomotion. He also claims that the spines of the pupa of the dipterous Anthrax are both for locomotion and for boring, especially the spines on the head and tail. He therefore divides these pupal spines into helcodermatous (boring or tearing) and locomotor spines.

Gonin has fully confirmed Newport’s discovery of the exuvial fluid. He states that during pupation the outside of the pupa, especially the parts of the head and thorax “is coated with a viscous liquid secreted by special glands.” The parts only harden subsequent to pupation after exposure to the air (p. 41). His observations were made under the direction of Professor Bugnion, who kindly writes us:—

“M. Gonin has proved the formation of a liquid which passes under
the cuticle at the time of the last moult and facilitates
exuviation. We think that this liquid is secreted by large cells
(unicellular glands) which we see especially on the surface of
segments 1–3. These cells form part of the hypodermis, and their
pores open under the cuticle.”

In a subsequent letter enclosing a sketch kindly made for me by M.
Gonin (Fig. 566), Professor Bugnion writes me Aug. 24, 1897,
regarding the functions of the large hypodermal cells (_l. hy_), as
follows: “It seems to me, in fact, after having again examined the
sections, that the function of these cells is not sufficiently
elucidated. Indeed these cells occur only in the section passing
through the 1st segment, between the head and 1st thoracic segment.
It would seem, if these cells supply the liquid which lubricates the
surface at the time of ecdysis, that they should be spread over the
entire surface of the body. Moreover, these cells have no distinct
orifice, and although there is seen at times to issue streams of a
substance (coagulated by the reagents), they cannot be compared with
true unicellular glands like those of the epidermis of fishes,
amphibians, etc.

“On the other hand, if it is the blood which oozes out on the
surface (according to your hypothesis), it would seem that the loss
of blood would cause the death of the larva. I believe then it is
due to the secretion of the hypodermis which spreads over the whole
surface when the cells are still soft (not yet hardened from contact
with the air). At all events, there is a liquid spread over the
surface; it is this liquid which glues the wings and the legs to the
body at the moment the caterpillar issues from the rent in its skin.
If at this instant we plunge the pupa in the water the liquid is
dissolved, and the feet, wings, etc., are not glued to the body.”

Dr. T. A. Chapman also writes us: “There is no question about the
existence of a fluid between the two skins at moulting. In hairy
larvae the hairs are always wet at first, or if the skin be renewed
rather more quickly than the larva does it naturally, the wetness of
both surfaces is obvious. I do not know the nature of the fluid, but
it is related to that which hardens into the dense pupal case, and
also hardens in a less degree the skin of the larva. I suppose it
must contain some chitin in a soluble form. If a newly cast larva
skin be taken, there is no difficulty in extending the shrivelled
mass to its full length and dimensions, but if a short time elapses,
this chitin hardens, and the skin cannot be extended after soaking
in water, alcohol, ammonia, or any other solvent I have tried.”

It has been stated that there is a subimaginal pellicle in Lepidoptera, but as Dr. Chapman writes me, “what has been observed has been some of the inner pupal dissepiments, such as the pupal cases of the under wings,” etc. They may be observed in the head of the tineid pupæ, and other small moths. We have thought that the delicate, purplish, powdery layer left in the cast shells of the pupæ of saturnians, Catocalæ, and other moths, might possibly be such a pellicle, but this view has been dispelled by the following statement of Professor Bugnion in a letter answering an inquiry whether he had noticed such a pellicle.

“A liquid which is secreted in a few minutes at the time of the last
moult, forms in drying a yellowish layer spotted with black (in
_Pieris brassicæ_). This layer extends around the entire pupa, and
serves both to protect it and to glue together the wings, legs,
etc., in their new position. The dried liquid on the surface of the
pupa, and by means of which the appendages are glued to the surface,
very likely corresponds to the pellicle of which you speak.” The
newly exposed integument is at first pale and colorless, but soon
assumes the hues peculiar to the species, and the insect, at first
exhausted, after a short rest becomes active.

FIG. 566.—Transverse section through the prothoracic segment
(ventral face) of larva of _Pieris brassicæ_, about 12 hours
before pupation: _c_, cuticula; _l. hy_, large glandular (?)
hypodermal cells; gradually passing into normal hypodermal cells
(_hy_).—Gonin _del._
]

E. Howgate has noticed under the microscope peculiar internal
movements in a small immature transparent geometrid while moulting.
“Each separate segment,” he says, “commencing at the head, elongated
within the outer skin, whilst the next ones remained in their former
state. Each segment in its turn behaved in this curious manner until
the last was reached, when the motion was reversed and proceeded
toward the head, when it was again reversed.... The whole proceeding
appeared as if the larva was gliding within itself, segment after
segment, the outer skin remaining as if held by the other segments,
whilst the particular one in motion freed itself within. After
remaining motionless for a short interval, the skin near the head
swelled and burst, open at the back.... Presently out comes the head
of the new caterpillar, pushing forward the old one.... After a
short struggle the new true legs appear, pushing off and treading
under foot the old ones. Then by violent wriggling movements the
abdominal legs were extricated. Then all is clear, and the larva,
which is quite exhausted, coils itself up and literally pants for
breath.” (The Naturalist, November, 1885, No. 124, p. 366, quoted in
Psyche, iv, p. 327, 1887.)

Since the worms and most other ametabolous invertebrates are not
known to moult their integument, the body steadily increasing in
size without frequent changes of skin, it seems that growth may go
on and still be accompanied by considerable changes in shape of the
body without change of skin. Frequent ecdyses appear, then, to be
the result of the great and sudden changes of the body, necessitated
by the adaptation of the animal to new or unusual conditions of
life. In young Daphnia, a cladocerous crustacean, as many as eight
moults were observed in a period of 17 days, and spiders frequently
moult even after reaching their full size. The swollen bodies of the
gravid female of Gastrophysa, Meloë, or of Termites, and of the
honey ant show that the skin can stretch to a great extent, but in
the metamorphoses of Crustacea and of insects, whose young are more
or less worm-like or generalized in form, with fewer segments and
appendages, or with appendages adapted for quite different uses from
those of mature life, the necessity for a change of skin is seen to
be necessary for mechanical reasons. Hence Crustacea and insects
moult most frequently early in life, when the changes of form are
most thoroughgoing and radical, while simple growth and increase in
size are most rapid at the end of larval life, as seen both in
shrimps and crabs, and in insects.

The hibernating caterpillars of certain butterflies are known to
moult once oftener than those of the summer brood. Mr. W. H. Edwards
has discussed the subject with much detail. “There seems,” he says,
“to be a necessity with the hibernators of getting rid of the rigid
skin in which the larva has passed the winter; that is, if the
hibernation has taken place during the middle stages, as it does in
Apatura and Limenitis. In these cases very little food is taken
between the moult which precedes hibernation and the one which
follows it, and the larva while in lethargy is actually smaller than
before the next previous moult. The skin shrinks, and has to be cast
off before the awakened larva can grow. Those species (observed)
whose larva moults five times in the winter brood require but four
moults during the summer.” He adds that while the larva is in
lethargy, it is actually smaller than before the next previous
moult. Dr. Dyar writes: “I think there is no doubt about the number
of stages of arctian larvæ. They seem to have a great capacity of
spinning out their life-history by interpolated stages (as regards
width of head). I think it is because so many of them hibernate, and
only a single brood extends throughout the season.” (Psyche iii, p.
161.)

On the other hand, it is difficult to understand why the
caterpillars of arctians moult so frequently, nearly twice as often
as in most other caterpillars, though the changes of form and
armature are so slight.

Dr. Chapman also writes me: “Arctians resemble bears (Arctos), polar
and others, in having long hairs to protect them during winter, and
are, in fact, typically hibernators. Many of them have to
half-hibernate, having warmth enough to keep them awake, but not
enough food for growth, but their tissues, at least the chitinous
ones of the cutis, and also probably, and perhaps especially, of the
alimentary canal, become old and effete, and require the
rejuvenescence acquired by a moult. Other smooth-skinned hibernators
have similar capabilities.”

Chapman has shown in his paper on Acronycta that these caterpillars
of this genus illustrate how larvæ may lose a moult, and they do so
to acquire a sudden change of plumage.

=The number of moults in insects of different orders.=—It will be seen from the data here presented that the number of moults is as a rule greatest in holometabolic insects with the longest lives, and that an excessive number of ecdyses may at times be due to some physical cause, such as lack of food combined with low temperature.

In Campodea there is a single fragmentary moult (Grassi), while the Collembola (_Macrotoma plumbea_) shed their skin throughout life. (Sommer.)

In the winged insects, especially Lepidoptera, the number of moults is dependent on climate. Insects of wide distribution growing faster in warmer climates consequently shed their skins oftener; for example, the same species may moult once oftener in the southern than in the northern States, as in the case of _Callosamia promethea_, which in West Virginia is double-brooded. Hibernating larvæ moult once oftener than those of the summer brood. (W. H. Edwards.) Weniger by rearing the larvæ of _Antheræa mylitta_ and _Eacles imperialis_, and which, when reared under normal conditions, actually have six stages, found that when reared in a warm moist atmosphere of about 25° C. they have but five stages, _i.e._ moult but four times. In the hot and moist climate of Ceylon, _A. mylitta_ has but five stages. (Psyche, v, p. 28.)