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.
[Illustration:
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.
[Illustration:
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.
[Illustration:
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.
[Illustration:
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.
[Illustration:
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.
[Illustration:
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.
]
[Illustration:
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.
[Illustration:
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.
[Illustration:
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.)
Among Orthoptera Acrydians moult five times; _Diapheromera femorata_ but
twice (Riley); a katydid (_Microcentrum retinervis_) moults four times
(Comstock). _Mantis religiosa_, according to Pagenstecher, moults seven
times, having eight stages, including that before the amnion is cast,
but the first “moult” being an exuviation of the amnion, the number of
stages is seven. Cockroaches (_Periplaneta americana_) are said by
Marlatt to “pass through a variable number of moults, there being
sometimes as many as seven.”
In the Homoptera there are, in general, from two to four moults; thus in
Typhlocyba there are five stages, and in Aphis at least three, and in
Psylla four during the nymphal state. Psocus has four. Riley states that
the nymph of the female coccid, _Icerya purchasi_, sheds its skin three
times, and that of the male twice. Notwithstanding its slow growth,
Riley says, the 17–year Cicada moults oftener than once a year, and the
number of larval stages probably amounts to 25 or 30 in all. The bed-bug
sheds its skin five times; and with the last moult appear the minute
wing-pads characteristic of the adult. In _Conorhinus sanguisuga_ there
are “at least two larval stages and pupal stages.” (Marlatt.)
In the dragon-flies moulting occurs, Calvert thinks, many times, since
the rudiments of wings are said by Poletaiew to only appear in odonate
nymphs after the third or fourth moult.
In the May-fly, Chloëon, the number of ecdyses is 20. The neuropterous
_Ascalaphus_ (Helecomitus) _insimulans_ of Ceylon moults three times
before pupating. Among the Mecoptera Felt has shown that _Panorpa
rufescens_ moults seven times.
In Coleoptera the normal or usual number is not definitely known; Meloë
moults five times, but this is a hypermetamorphic insect; _Tribolium
confusum_ has been carried by Mr. Chittenden through seven moults.
_Phytonomus punctatus_, the clover-leaf weevil, moults three times,
according to Riley, who has observed that _Dermestes vulpinus_ passes
through seven larval stages.
In the breeding jars, with plenty of food and a constant temperature
of from 68° to 78° F., the larvæ cast their 1st skin in from four to
nine days, the great majority moulting at seven days. Under the same
conditions the 2d skin was cast at from four to seven days, the
majority moulting at six days; the 3d skin at from three to six
days, the majority moulting at five days; and the 4th skin at from
three to six days, the majority moulting at five days; the 5th skin
at from five to seven days, and the 6th skin at six days. There are
thus seven larval stages. (Report for 1885, p. 260.)
Riley has ascertained that by rearing isolated larvæ of _Tenebrio
molitor_, one after being kept nearly a year had moulted 11 times,
when it died. A second larva, hatched June 5, had moulted 12 times
by June 10 of the following year, (1877), when it also died. Of _T.
obscurus_ three larvæ were reared to the imago state. One moulted 11
times by Aug. 30 of the same year, pupated Jan. 20, 1877, and
finally became a beetle Feb. 7, 1877. The other two both moulted 12
times, and reached the imago stage Feb. 18 and March 9,
respectively. “All were, as nearly as possible, under like
conditions of food and surroundings, and in all cases the moult that
gave the pupa is not considered among the larval moults.”
Two larvæ of the museum pest (_Trogoderma tarsale_) were kept by
Riley in a tight tin box with an old silkworm cocoon. “They were
half-grown when placed in the box. On Nov. 8, 1880, there were in
the box 28 larva skins, all very much of a size, the larva having
apparently grown but little. The skins were removed and the box
closed again as tightly as possible. Recently, or after a lapse of
two years, the box was again opened and we found one of the larvæ
dead and shrivelled up; but the other was living and apparently not
changed in appearance. There were 15 larva skins in the box. He
could not tell when the one larva died, but it is certain that
within a little more than three and a half years, two larvæ shed not
less than 43 skins, and that one larva did not, during that time,
appreciably increase in size. We know of no observations which
indicate the normal or average length of life, or number of moults
in either Tenebrio or Trogoderma, but it is safe to assume from what
is known, in these respects, of allied species, that in both the
instances here referred to, but particularly in the case of
Trogoderma, development was retarded by insufficient nutrition, and
that the frequent moulting and slow growth resulted therefrom, and
were correlated.”[99] Further observations such as these are greatly
needed.
Of the Siphonaptera the common cat and dog flea (_Pulex serraticeps_)
moults three times before pupating. (Howard.)
In Lepidoptera the usual or average number of moults is four, but the
number varies considerably, the greatest number yet known occurring in
_Phyrrarctia isabella_, which, Dr. Dyar informs me, moults 10 times.
From Dyar’s observations it appears that there are usually five larval
stages, but six and seven stages are not infrequent, while there are
seven in _Seirarctia echo_, eight in _Ecpantheria scribonia_, Scepis,
and Apatelodes, and nine and ten in arctians, while the European _Nola
centonalis_ moults nine times, other species of this genus shedding
their skins six times. (Buckler.) (Psyche, v, pp. 420–422.) _Callosamia
promethea_ appears, as a rule, to moult but three times. _Orgyia
antiqua_ was found by Hellins to moult from three to five times. Riley
found that in _O. leucostigma_ the males moult four times, the female
four, but sometimes five times, while Dyar states that in _O. gulosa_
the male larvæ moult three or four times, the female always four times;
in _O. antiqua_, however, there are six stages, and in the female seven.
Lithocolletis, Chambers thinks, as a rule, moults eight times, and
Comstock thinks that _L. hamadryadella_ casts its skin seven or eight
times.
In the blow-fly (Calliphora) Leuckart and Weismann have inferred at
least two moults, while Weismann suspected that there are as many as
four. In _Musca domestica_ we have observed that the larva moults three
times; in Œstridæ there are three larval stadia. (Brauer.) In Corethra
there are four larval moults, and Miall thinks there are probably as
many in Chironomus. Passing to the phytophagous Hymenoptera, there are
three moults or four larval stages in _Nematus erichsonii_, but Dyar
informs us that less than four stages in saw-fly larvæ is very rare,
that he has only one record of less than five, and that that is
doubtful; “five for nematid, six and seven for others, is certainly the
rule. The highest I have is the indication of 11 stages for _Harpiphorus
varianus_, but this again is an inference only, and attended with
doubt.” (Can. Ent., xxvii, p. 208.) In Bombus we have observed five
different sizes of larvæ, and hence suppose the least number of ecdyses
is five, while we are disposed to believe that this insect, as well as
wasps and bees, in general shed their skins as many as eight times
during their entire existence.
The honey-bee, Cheshire thinks, since he has found the old and ruptured
pellicles, probably moults six times before it spins its cocoon, or
passes into the semipupa condition. (Bees and Bee-keeping, p. 20.)
As to the cause of the great number of moults in the arctians and in the
beetles experimented with by Riley, it would seem that cold and the lack
of food during hibernation were the agents in arctians, and starvation
or the lack of food in the case of the beetles, such cause preventing
growth, though the hypodermis-cells retained their activity.
=Reproduction of lost limbs.=—Here might be discussed the subject of the
renovation or renewal of maimed or lost limbs, or the reparation of
other injuries. As is well known, the cœlenterates, echinoderms, and
worms under certain circumstances multiply by self-division, or if
artificially mutilated, the parts are gradually restored by
cell-proliferation or histogenesis. It is so with the antennæ and legs
of crustaceans as well as the digits and tail of salamanders. The
experiments first made by Le Pelletier[100] on spiders, and later by
Heineken,[101] and others after him, on different spiders, as well as on
Orthoptera and Hemiptera (Blatta, Reduvius, etc.), have proved that
antennæ and legs and other external parts which have been injured or
shortened, or entirely cut off in young individuals, are replaced at the
next, or after successive moults, though generally in diminished size.
This does not usually occur in adult life, and the process of reparation
of lost parts is apparently due to the active growth of the cells of the
parts affected during the process of moulting, when the histolysis of
the maimed or diseased parts is succeeded by the rapid development of
new cells, not only of the hypodermis, but also of the more specialized
tissues within. And this tends to prove that such histolysis and making
over of the muscles and other structures within occur especially in all
metamorphic insects, and also in ametabolous forms, though the process
has been most thoroughly examined in the Diptera, where these changes
are more marked.
Gonin has found that the thoracic legs of the caterpillar correspond
only to the tarsi of the imago (Fig. 608). It results, he says, from
this fact that in accordance with the observations of Réaumur (which
were wrongly interpreted by Newport and Künckel D’Herculais) that the
amputation of the legs of the larva does not involve the entire leg, but
only the extremity of the leg of the imago.
=Formation of the cocoon.=—While the larvæ of many insects, as those of
the butterflies, suspend themselves before transforming, and spin no
cocoon, or dig into the earth for protection and to secure an immunity
from too great changes of temperature, a large proportion of the larvæ
of metabolous insects which lead an inactive pupal life, line their
earthen cells with silk, or spin a more or less elaborate case of silk,
called the _cocoon_. We have seen that the inactive pupa of the male
scale-insects is covered by the scale itself, or even in one case the
insect forms a true cocoon of fibres of wax. The aquatic larvæ of the
Neuroptera and Coleoptera creep out of the water, and by the movements
of their bodies make a rude earthen cell in the bank, while that of
Donacia spins a dense, leathery cocoon (Fig. 567) in the earth. The
larvæ of the Embiidæ are protected by a cocoon, which they renew at each
moult. Coniopteryx spins an orbicular cocoon, the Hemerobiidæ a
spherical, dense, whitish one. The Trichoptera transform within their
larval cases, which thus serve as cocoons, as do certain case-bearing
Lepidoptera, notably the Psychidæ.
[Illustration:
FIG. 567.—Cocoon (natural size) of _Donacia proxima_.
]
[Illustration:
FIG. 568.—Cocoon and larva of _Lucanus dama_.
]
The pupa of certain leaf-eating beetles (Chrysomelidæ), as well as the
Coccinellidæ, Dermestidæ, Hister, etc., are usually protected by the
cast larval skin, which is retained, forming a rude shelter. While many
beetles spin an oval cocoon (Gyrinus, Silphidæ), the wood-boring species
make one of chips glued together, and that of Lucanus, which feeds on
decayed wood, is lined with silk (Fig. 568). Anobium constructs a silken
cocoon, interweaving the fine particles of its thin castings; the larvæ
of weevils also usually spin silken cocoons.
[Illustration:
FIG. 569.—Larva (_a_), puparium (_b_), and imago (_c_) of Sarcophaga,
enlarged.
]
[Illustration:
FIG. 570.—_a_, _Erax bastardi_; _b_, pupa.—After Riley.
]
The larval skin of the coarctate Diptera is retained as a protection for
the soft-bodied pupa within, the old larval skin separating from the
integument of the semipupa. To this cocoon-like covering of the
coarctate pupa we have restricted the term _puparium_, originally used
by Kirby and Spence to designate the pupa. The puparium is usually
cylindrical or barrel-shaped, rounded at each end.
[Illustration:
FIG. 571.—Puparium of _Hypoderma bovis_: _a_, side; _b_, ventral view,
showing exit hole of adult; _c_, cap which splits off for exit of
fly.—After Clark, from Osborn, Bull. 5, Div. Ent. U. S. Dept. Agr.
]
In the _Diptera cyclorhapha_, or common house and flesh flies, etc., the
puparium remains in vital connection, by means of four tracheæ, with the
enclosed pupa, which escapes from the case through a curved seam or lid
at the anterior end and not by a slit in the back, as do the
orthoraphous families, represented by the horse-fly (Tabanidæ, Asilidæ,
Fig. 570), etc., where in some cases the obtected pupa remains within
the loose envelope formed by the old larval skin, which Brauer calls a
false puparium. The dry, hard puparium is burst open at the cephalic end
when the fly emerges, by means of the frontal vesicle, which is
distended with fluid (Fig. 571).
The exact mode of spinning the cocoon by caterpillars has been carefully
observed by L. Trouvelot in the case of the polyphemus silkworm.
“When fully grown, the worm, which has been devouring the leaves so
voraciously, becomes restless and crawls about the branches in
search of a suitable place to build up its cocoon; before this it is
motionless for some time, holding on to the twig with its front
legs, while the two hind pair are detached; in this position it
remains for some time, evacuating the contents of the alimentary
canal until finally a gelatinous, transparent, very caustic fluid,
looking like albumen, or the white of an egg, is ejected; this is a
preparation for the long catalepsy that the worm is about to fall
into. It now feels with its head in all directions, to discover any
leaves to which to attach the fibres that are to give form to the
cocoon. If it finds the place suitable, it begins to wind a layer of
silk around a twig, then a fibre is attached to a leaf near by, and
by many times doubling this fibre and making it shorter every time,
the leaf is made to approach the twig at the distance necessary to
build the cocoon; two or three leaves are disposed like this one,
and then fibres are spread between them in all directions, and soon
the ovoid form of the cocoon distinctly appears. This seems to be
the most difficult feat for the worm to accomplish, as after this
the work is simply mechanical, the cocoon being made of regular
layers of silk united by a gummy substance. The silk is distributed
in zigzag lines of about one-eighth of an inch long. When the cocoon
is made, the worm will have moved his head to and fro, in order to
distribute the silk, about 254,000 times.
“After about half a day’s work, the cocoon is so far completed that
the worm can hardly be distinguished through the fine texture of the
wall; then a gummy resinous substance, sometimes of a light-brown
color, is spread all over the inside of the cocoon. The larva
continues to work for four or five days, hardly taking a few minutes
of rest, and finally another coating is spun in the interior, when
the cocoon is all finished and completely air tight. The fibre
diminishes in thickness as the completion of the cocoon advances, so
that the last internal coating is not half so thick and so strong as
the outside ones.” (Amer. Naturalist, i, p. 86.)
The mode of spinning the cocoon of an ichneumon (Microgaster) parasitic
on Philampelus has been well described by John P. Marshall, as follows:—
[Illustration:
FIG. 572.—Microgaster larvæ; spinning their cocoons: _a_, enlarged
view of 5.—After Marshall.
]
The first appearance of the parasite is represented in Fig. 572, 1.
A warty excrescence appears on the back of the caterpillar, which
slowly emerges until it is seen to be a larva enclosed in a delicate
transparent membrane, as represented in 2. This it soon succeeds in
bursting, and, rising to its full length, balances itself a moment
as in 3, then, bending double, it ejects from its mouth a glairy
liquid, which instantly changes to silk, and fastens the posterior
end to the skin of the caterpillar, as shown in 4, side view. It now
begins to spin its cocoon by attaching a silken thread to the silky
mass by which it had previously fastened itself to the caterpillar,
and forming a series of loops of uniform size, first from right to
left, and then back again from left to right, as represented in the
front view, 5, and better in the enlarged view, _5^a_, the arrow
heads showing the direction in which the head of the larva moved
while forming the loops. The ends of the series, numbered 1, 2, 3,
4, are fastened to the edges of the ventral side of the body, which
thus serves as a measure of the width of the cocoon, and also acts
as a support for the frail fabric in the first stages of spinning.
After the larva has fastened the fabric as far up on its ventral
surface as it can, conveniently, it then begins to spin free, as
shown in the side view, 6, where it is represented as just
completing the first half of its cocoon, which resembles in form a
slipper. This accomplished, the larva ceases to spin for the time
being, bends its head, as in 7, towards its ventral surface, and
pushes the half cocoon free from its body. The form of the silken
fabric enables it to stand unsupported, while the larva, sliding its
head down to the base, holds on firmly until it swings its posterior
end into the toe of the slipper.
Figure 572, 8, shows it in the act of changing end for end, and in 9
the larva is seen erect, beginning at the base to complete the other
half of its cocoon; 10 shows the larva contracting its body as it
spins upward for about half the length of the cocoon, when it again
changes end for end, as shown in 11, where it is beginning at the
upper part to unite the two sides, finally enclosing itself as
represented in 12.
It may now be seen, under the microscope, through the meshes of its
cocoon actively engaged in lining the interior with layers of very
fine silk ejected from its mouth in great abundance. One half of the
cocoon is first lined by a forward and back movement of its head,
and then reversing its position, it lines the other half in a
similar manner.
In one case the larva was disengaged from the skin of the
caterpillar, after beginning its cocoon. It, however, began again,
and spun a portion while lying on the table. This was removed, when
it began a third time, and completed its cocoon.
In about 10 days the insect made its appearance through a hole in
the upper end, as represented in 13. The top was eaten off in a
perfect circle and hung by a few threads, so as to resemble a lid as
it was thrown back.
One caterpillar observed had between 300 and 400 cocoons on its back
and sides, and another was dissected after more than 30 larvæ had
escaped, and 130 were discovered in the soft integuments of the
back.
The figures from 1 to 13 are magnified five diameters, but in order
to observe the spinning of the cocoon a power of 50 is required.
(Amer. Naturalist, xii, pp. 559, 560.)
Certain differences observed by W. A. Buckhout in a Microgaster
parasitic on the different species of Macrosila, are referred to in
the same volume, p. 752.
[Illustration:
FIG. 573.—Body of larva of Lithocolletis. swollen and filled with
cocoons of Copidosoma, enlarged.
]
While those chalcidid larvæ which feed internally on their host, as
a rule, transform into naked, more or less coarctate pupæ, Howard
states that the larvæ of Copidosoma, Bothriothorax, Homalotylus, and
perhaps others, which are much crowded within their host, cause a
marked inflation of the body of the latter (Figs. 573, 574). The
nature of this cocoon-like cell, and how it is produced, is unknown.
“Its structure shows it not to be silk, nor yet the last larval skin
of the parasite, and whether it is an adventitious tissue of the
host-larva or a secretion of the parasite, or is explicable upon
other grounds, I cannot say.”
The silken cocoon of an aphidiid ichneumon has been found by Miss
Murtfeldt, and also by Dr. Riley, under a rose aphid in which it had
lived, and referred by Howard to the genus Praon (Fig. 575).
=Sanitary conditions observed by the honey-bee larva, and admission of
air within the cocoon.=—Cheshire has observed that after the larva of
the honey-bee has spun its cocoon or silken lining of its cell, it
observes the following means of preserving cleanliness. The food given
to the larva, especially during the latter part of the growing period,
contains much pollen, the cases of the grains of which consist of
cellulose, which is indigestible.
[Illustration:
FIG. 574.—Coccinellid larva infested by _Homalotylus obscurus_,
enlarged.
]
[Illustration:
FIG. 575.—Cocoon of Praon under the body of a dead Aphis,
enlarged.—This and Figs. 573 and 574 after Howard, from Insect Life.
]
[Illustration:
FIG. 576.—Pupation of Proctotrupes in the body of a larva of a beetle,
representing a case mentioned by Dr. Sharp, where the parasites have
pupated on the outside of the host, a pair of each attached to
nearly each segment of the body of their host.—After Sharp.
]
“These cases, with other refuse matters, collect in quantity within
the bowel, which becomes distended, since it has no opening. The
imprisoned larva, having little more than enough room for turning,
must be freed of these objectionable residua.... In a word, the
larva turns its head upon its stomach, and pushes the former towards
the base of the cell until its position is reversed, the tail being
outwards; and, thus placed, it laps up all residue of food,
especially from its old clothes previously referred to, until they
are dried, and practically occupy no space. It now throws up its
stomach and bowel, with all their contents, and without detaching
them from its outer skin, which is moulted as before, but in this
instance to be pressed against the cell, so as to form for it an
interior lining. The dejectamenta of the bowel in this way lie
between the cast skin and cell-wall (as seen at _e_, Fig. 577), and
so the larva remains absolutely unsoiled. It now turns its head and
resumes its old position, joining its cocoon to the edges of its
last cast skin, so that its habitation is relined, it is cleansed,
and air can still pass to it through the imperceptible openings left
by the bees in the sealing. This point is of radical importance,
since breathing is carried on pretty rapidly during the latter part
of its subsequent transformations, the absorbed oxygen permitting
then of a production of heat, and causing also considerable
diminution in weight.”
[Illustration:
FIG. 577.—Larva and pupa of honey-bee in their cell: _SL_,
spinning-larva; _N_, pupa; _FL_, young feeding larva; _co_, cocoon;
_sp_, spiracles; _t_, tongue; _m_, mandible; _an_, antenna; _w_,
wing; _ce_, compound eye; _e_, excrement; _ex_, exuvium.—After
Cheshire.
]
As to the passage of air into the bee’s cocoon, Cheshire states that
before the cocoon can be built, a cover, technically called sealing, is
put over the larva by its nurses. These covers are made of pollen and
wax, and are pervious to the air. They are more convex and regular in
form than those sealing in the honey.[102]
THE PUPA STATE
The word _pupa_ is from the Latin meaning baby. Linnæus gave it this
name from its resemblance to a baby which has been swathed or bound up,
as is still the custom in Southern Europe. The term _pupa_ should be
restricted to the resting inactive stage of the holometabolous insects.
Lamarck’s term _chrysalis_ was applied to the complete or obtected
pupa of Lepidoptera and of certain Diptera, and _mumia_, a mummy, to
the pupæ of Coleoptera, Trichoptera, and most Hymenoptera. Latreille
(1830) also restricted the term pupa to the “oviform nymph,” or
puparium, of Diptera. Brauer applies the term _nymph_ to the pupa of
metabolous insects.
[Illustration:
FIG. 578.—Pupa obtecta: _a_, of Sesia, with its cocoon-cutter on the
head; _b_, of _Tortrix vacciniivorana_.
]
The typical pupa is that of a moth or butterfly, popularly called a
chrysalis. A lepidopterous pupa in which the appendages are more or less
folded close to the body and soldered to the integument, was called by
Linnæus a _pupa obtecta_; and when the limbs are free, as in Neuroptera,
Mecoptera, Trichoptera, and the lepidopterous genus Micropteryx it is
called a _pupa libera_ (Fig. 579). When the pupa is enclosed in the old
larval skin, which forms a pupal covering (puparium), the pupa was said
by Linnæus to be _coarctate_. The pupa of certain Diptera, as that of
the orthoraphous families, is nearly as much obtected as that of the
tineoid families of moths, especially as regards the appendages of the
head; the legs being more as in _pupæ liberæ_ (Fig. 580).
[Illustration:
FIG. 579.—Pupa libera of neuropterous insects _a_, _Corydalus
cornutus_; _b_, Sialis; _c_, Hemerobius.
]
The male Coccid anticipates the metabolous insects in passing through a
quiescent state, when, as Westwood states, it is “covered by the skin of
the larva, or by an additional pellicle.” The body appears to be broad
and flat, the antennæ and fore legs resting under the head, while the
two hinder pairs of legs are appressed to the under side of the body.
There is but a slight approach to the pupa libera of a metabolous
insect.
Riley states that the male larva of _Icerya purchasi_ forms a cocoon
waxy in character, but lighter, more flossy, and less adhesive than
that of the female egg-cocoon. It melts and disappears when heated,
proving its entirely waxy nature. When the mass has reached the
proper length, the larva casts its skin, which remains in the hind
end of the cocoon, and pushes itself forward into the middle of the
cocoon. The pupa (Fig. 581) is of the same general form and size as
the larva. All the limbs are free and slightly movable, so that they
vary in position, though ordinarily the antennæ are pressed close to
the side, as are the wing-pads; the front pair of legs are extended
forward. “If disturbed, they twist and bend their bodies quite
vigorously.” The pupa state lasts two or three weeks. A similar pupa
is that of _Icerya rosæ_. (Riley and Howard.)
[Illustration:
FIG. 580.—Pupa obtecta of Diptera: _a_, Ptychoptera; _b_, _Tabanus
atratus_; _c_, _Proctacanthus philadelphicus_; _d_, _Midas
clavatus_.
]
[Illustration:
FIG. 581.—Pupa libera of _Icerya purchasi_, ventral view.—After
Riley, Insect Life.
]
The metamorphosis of _Aspidiotus perniciosus_ is of interest. The
male nymph differs much after the first moult from the female,
having large purple eyes, while the female nymph loses its eyes
entirely. It passes into what Riley terms the _pro-pupa_ (Fig. 582,
_b_), in which the wing-pads are present, while the limbs are short
and thick. The next stage is the “true pupa” (Fig. 582, _c_, _d_),
in which the antennæ and legs are much longer than before. There is
no waxy cocoon, but only a case or scale composed of the shed larval
skin, i.e. “with the first moult the shed larval skin is retained
beneath the scale, as in the case of the female; with the later
moultings the shed skins are pushed out from beneath the scale,” and
when they transform into the imago they “back out from the rear end
of their scale.”
[Illustration:
FIG. 582.—_Aspidiotus perniciosus_, development of male insect: _a_,
ventral view of larva after first moult; _b_, the same, after
second moult (pro-pupa stage); _c_ and _d_, true pupa, ventral and
dorsal views. All greatly enlarged.—After Riley.
]
The pupæ of Coleoptera and of Hymenoptera, though there is, apparently,
no near relationship between these two orders, are much alike in shape,
and, as Chapman pertinently suggests, those of both orders are helpless
from their quiescence, and hence have resorted for protection to some
cocoon or cell.
But it is quite otherwise with the pupæ of Lepidoptera and Diptera,
which vary so much in adaptation to their surroundings, and hence afford
important taxonomical and phylogenetic characters. This, as regards the
Lepidoptera, was almost wholly overlooked until Chapman called attention
to the subject, and showed that the pupæ had characters of their own, of
the greatest service in working out the classification, and hence the
phylogeny, of the different lepidopterous groups. We have, following the
lead of Chapman, found the most striking confirmation of his views, and
applied our present knowledge of pupal structures to dividing the
haustellate Lepidoptera into two groups,—Paleolepidoptera and
Neolepidoptera.
The pupæ of the Neuroptera, Coleoptera, and Hymenoptera differ
structurally from the imago, in the parts of the head and thorax being
less differentiated. Thus in the head the limits or sutures between the
epicranium and clypeus, and the occiput and gula, are obscurely marked,
while the tergal and pleural sclerites of the imago are not well
differentiated until the changes occurring just before the final
ecdysis.
It is easy, however, to homologize the appendages of the pupæ with those
of the imago of all the holometabolous orders except in the case of the
obtected pupa of the Lepidoptera (and probably of the obtected dipterous
pupæ), where the cephalic appendages are soldered together.
That the appendages of the lepidopterous pupa are, as generally
supposed, merely cases for those of the imago has been shown by Poulton
to be quite erroneous. He says: “If we examine a section of a pupal
antenna or leg (in Lepidoptera), we shall find that there is no trace of
the corresponding imaginal organ until shortly before the emergence of
the imago. In the numerous species with a long pupal period, the
formation of imaginal appendages within those of the pupa is deferred
until very late, and then takes place rapidly in the lapse of a few
weeks. This also strengthens the conclusion that such pupal appendages
are not mere cases for the parts of the imago, inasmuch as these latter
are only contained within them for a very small proportion of the whole
pupal period.” On the other hand, Miall and Hammond claim that there is
a strong superficial contrast as to the formation of the imaginal
organs, between Lepidoptera and tipularian Diptera, the appendages,
wings, and compound eyes being substantially those of the imago. “With
the exception of the prothoracic respiratory appendages and the
tail-fin, there is little in the pupa of Chironomus which does not
relate to the next stage.”
The exact homology of the “glazed eye” of the lepidopterous pupæ and of
the parts under the head, situated over the maxillæ, is difficult to
decide upon, and these points need farther examination. In the dipterous
pupa it is interesting to observe that the halteres are large and broad,
which plainly indicates that they are modified hind wings. The number
and arrangement of the spiracles is different in pupæ from those of the
larva and imago.
[Illustration:
FIG. 583.—_Simulium piscicidium_: _a_, larva; _b_, _c_, _d_, pupa;
_e_, thoracic leg; _f_, row of bristles at end of body. _A_, _S.
pecuarum_, pupa; _a_, _b_, _c_, adminicula.—After Riley.
]
There are also secondary adaptive structures peculiar to the pupa, which
are present and only of use in this stage. These are the thoracic,
spiracular, or breathing appendages of the aquatic Diptera (Fig. 583),
the various spines situated on the head or thorax, or on the sides, or
more often at the end of the abdomen, besides also the little spines
arranged in more or less circular rows around the abdominal segments,
the cocoon-breaker, and the cremaster of many pupæ.
In the pupa of certain Diptera, there is a terminal cremaster-like
spine, as in that of _Tipula eluta_ (Fig. 584), _Tabanus lineola_ (Fig.
585), besides adminicula or locomotive spines like those of
lepidopterous pupæ (Fig. 580, _a_, _b_, _c_).
[Illustration:
FIG. 584.—Pupa of _Tipula eluta_.
]
[Illustration:
FIG. 585.—Pupa of _Tabanus lineola_.—This and Fig. 584 after Hart.
]
[Illustration:
FIG. 586.—Pupa of _Galerita lecontei_, and of _Adelops hirtus_ (_a_,
_b_, _c_).—After Hubbard.
]
The pupæ of Coleoptera are variously spined or hairy (Fig. 586). Those
of Hydrophilus and of Hydrobius are provided with stout spines on the
prothorax and abdomen which support the body in its cells, so that, as
Lyonet first showed, though surrounded on all sides by moist earth, it
is kept from contact with it by the pupal spines; other pupæ of beetles,
such as that of the plum weevil, which is also subterranean, possess
similar spines. The abdomen of many coleopterous pupæ, such as those of
Carabidæ, end in two spines, to aid them in escaping from their cells in
wood or in the earth; others have stiff bristles, and others spines
along each side of the abdomen (Fig. 586). All these structures are the
result of a certain amount of activity in what we call quiescent pupæ,
but most of these are for use at the end of pupal life, at the critical
moment when by their aid the insect escapes from its cocoon or
subterranean cell, or if parasitic, bores out of its host.
If we are to account for the causes of their origin, we are obliged to
infer that they are temporary deciduous structures due to the need of
support while the body is subjected to unusual strains and stresses in
working its way out of its prison in the earth, or its cell within the
stems and trunks of plants and similar situations. They are pupal
inheritances or heirlooms, and well illustrate the inheritance of
characters acquired during a certain definite, usually brief, period of
life, and transmitted by the action of synchronous heredity.
The pupæ of certain insects are quite active, thus that of Raphidia,
unlike that of Sialis, before its final ecdysis regains its activity and
is able to run about. (Sharp, p. 448.)
_a._ The pupa considered in reference to its adaptation to its
surroundings and its relation to phylogeny
The form of the pupa is a very variable one, as even in Lepidoptera it
is not entirely easy to draw the line between a pupa libera and a pupa
obtecta (Fig. 578); and though the period is one of inactivity, yet when
they are not in cocoons or in the earth in subterranean cells, their
form is more or less variable and adapted to changes in their
surroundings. Even in the obtected pupa of butterflies, there is, as
every one knows, considerable variability of shape and of armature,
which seems to be in direct adaptability to the nature of their
environment. Scudder has well shown that in certain chrysalids, such as
those of the Nymphalidæ, which are variously tuberculated, and hang
suspended by the tail, and often hibernate, these projections serve to
protect the body. All chrysalids with projections or ridges on different
parts of the body, being otherwise unprotected, move freely when struck
by gusts of wind, hence “the greater the danger to the chrysalis from
surrounding objects, the greater its protection by horny tubercles and
roughened callous ridges.” The greater the protection possessed in other
ways, as by firm swathing or a safe retreat, the smoother the surface of
the body and the more regular and rounded its contours. The tendency to
protection by tubercles is especially noticeable in certain South
American chrysalids of nymphalid butterflies. This response to the
stimuli of blows or shocks is also accompanied by a sensitiveness to the
stimulus of too strong light.
Previously Scudder[103] had made the important suggestion that the
smooth crescent-shaped belt of the “glazed eye” or “eyepiece” of
chrysalids is, as an external covering of the eye, midway between that
of the caterpillar and the perfect insect, and he asks: “May it not be a
relic of the past, the external organ of what once was? And are we to
look upon this as our hint that the archaic butterfly in its
transformations passed through an _active_ pupal stage, like the lowest
insect of to-day, when its limbs were unsheathed, its appetite
unabated?” etc. Scudder also shows that “the expanded base of the sheath
covering the tongue affords protection also to the palpi which lie
beneath and beside the tongue.”
All this tends to show the importance of studying the structure of the
pupa, in order to ascertain how the pupal structures have been brought
about, with the final object of discovering whether the pupæ of the
holometabolic insects are not descended from active nymphs, and if so,
the probable course of the line of descent.
_b._ Mode of escape of the pupa from its cocoon
[Illustration:
FIG. 587.—Pupa of _Micropteryx purpuriella_, front view: _md_,
mandibles; _mx. p_, maxillary palpus, end drawn separately; _mx.′
p_, labial palpi; _lb_, labrum.
]
“In all protected pupæ,” as Chapman says, “the problem has to be faced,
how is the imago to free itself from the cocoon or other envelope
protecting the pupa.” In the Coleoptera and Hymenoptera the imago
becomes perfected within the cocoon or cell, as the case may be, and as
Chapman states, “not only throws off the pupal skin within the cocoon,
but remains there till its appendages have become fully expanded and
completely hardened, and then the mandibles are used to force an outlet
of escape,” and he calls attention to the fact that “in many cases, even
in some entire families, they are of no use whatever to the imago except
in this one particular,” and he cites the Cynipidæ as perhaps the most
striking instance of this circumstance.
In those Neuroptera which spin a silken cocoon, _e.g._ the Hemerobiidæ,
the Trichoptera, and in Micropteryx (Fig. 588), the jaws used by the
pupa for cutting its way out of the cocoon are even larger in proportion
than in the pupa of caddis-flies (Fig. 588), being of extraordinary
size.
[Illustration:
FIG. 588.—Mandibles (_md_) of _Micropteryx purpuriella_,
enlarged.—Author _del._ _A_, pupal head of a hydropsychid
caddis-fly, showing the large mandibles.—After Reaumur, from Miall.
]
In Myrmeleon the pupa pushes its way half out of the cocoon, and then
remains, while the imago ruptures the skin and escapes (Fig. 589, _a_).
Thus in the Neuroptera and Trichoptera we have already established the
more fundamental methods of escape from the cocoon, which we see carried
out in various ways in the more generalized or primitive Lepidoptera.
The most primitive method in the Lepidoptera of escaping from the cocoon
seems to be that of Micropteryx.
[Illustration:
FIG. 589.—Larva of Myrmeleon with (_a_) its cocoon and cast pupa-skin.
]
“In this genus,” says Chapman, “though it is nominally the pupa that
escapes from the cocoon, it is in reality still the imago, the imago
clothed in the effete pupal skin. To rupture the cocoon it uses not
its own jaws, but those of the pupal skin, energizing them, however,
in some totally different way from ordinary direct muscular action,
their movements being the result of the vermicular movements of the
pupa, acting probably by fluid pressure on the articular structure
of the jaws, by some arrangement not altogether different perhaps
from the frontal sac of the higher Diptera. In the Micropteryges the
jaws of the pupa not only rupture the cocoon, but appear to be the
most active agents in dragging the pupa through the opening in the
cocoon and through any superincumbent earth, being merely assisted
by the vermicular action of the abdominal segments, and we find in
accordance with this circumstance that the pupal envelope is still
very thin and delicate, and has little or no hardening or roughness
by which to obtain a leverage against the walls of the channel of
escape.” (Trans. Ent. Soc. London, 1896, pp. 570, 571.)
[Illustration:
FIG. 590.—Pupa of Talæporia: _a_, cocoon-cutter; with vestiges of four
pairs of abdominal legs, and the cremaster.
]
Some sort of a beak or hard process, more or less developed, according
to Chapman, adapted for breaking open the cocoon exists in nearly all
the Lepidoptera with incomplete pupæ (_pupæ incompletæ_), except the
limacodid and nepticulid section. “In all these instances the pupa
emerges from the cocoon precisely as in the Micropteryges, that is, the
moth it really is that emerges, but does so encased in the pupal skin.
To achieve this object, it seems to have been found most efficient to
have three, four, or five abdominal segments capable of movement, but to
have the terminal sections (segments) soldered together.”
This cocoon-breaker, as we may call it, is especially developed in
_Lithocolletis hamadryadella_. As described by Comstock, it forms a
toothed crest on the forehead which enables it to pierce or saw through
the cocoon.
“Each pupa first sawed through the cocoon near its juncture with the
leaf and worked its way through the gap, by means of the minute
backward-directed spines upon its back, until it reached the upper
cuticle of the leaf. Through this cuticle it sawed in the same way
that it did through the cocoon. The hole was in each case just large
enough to permit the chrysalis to work its way out, holding it
firmly when partly emerged. When half-way out it stopped, and
presently the skin split across the back of the neck and down in
front along the antennal sheaths, and allowed the moth to
emerge.”[104]
We have observed and figured the cocoon-breaker in Bucculatrix,
Talæporia (Fig. 590, _a_), Thyridopteryx, and Œceticus, and rough knobs
or slight projection answering the purpose in Hepialidæ, Megalopyge,
Zeuzera, and in Datana.[105] See also the spine on the head of _Sesia
tipuliformis_ (Fig. 578).
The imago of the attacine moths cuts or saws through its cocoon by means
of a pair of large, stout, black spines (_sectores coconis_), one on
each side of the thorax at the base of the fore wings (Fig. 591), and
provided with five or six teeth on the cutting edge (_C_, _D_).
[Illustration:
FIG. 591.—Cocoon-cutter of the Luna moth: front view of the moth with
the shoulders elevated and the rudimentary wings hanging down: _s_,
cocoon-cutter; _p_, patagium. _B_, represents another specimen with
fully developed wings: _ms_, scutum; _st_, scutellum of the
mesothoracic segment; _s_, cocoon-cutter, which is evidently a
modification of one of the pieces at the base of the fore wings; it
is surrounded by membrane, allowing free movement. _C_ and _D_,
different views of the spine, magnified, showing the five or six
irregular teeth on the cutting edge.
]
[Illustration:
FIG. 592.—Larva and pupa of a wood-wasp (Rhopalum), enlarged: _h_,
temporary locomotive tubercles on head of pupa.—Trouvelot _del._
]
Our attention[106] was drawn to this subject by a rustling, cutting,
and tearing noise issuing from a cocoon of _Actias luna_. On
examination a sharp black point was seen moving to and fro, and then
another, until both points had cut a rough irregular slit, through
which the shoulder of the moth could be seen vigorously moving from
side to side. The hole or slit was made in one or two minutes, and
the moth worked its way at once out of the slit. The cocoon was
perfectly dry. The cocoon-cutter occurs in all the American genera,
in _Samia cynthia_, and is large and well marked in the European
_Saturnia pavonia-minor_ and _Endromis versicolora_. In _Bombyx
mori_ the spines are not well marked, and they are quite different
from those in the Attaci. There are three sharp points, being acute
angles of the pieces at the base of the wing, and it must be these
spines which at times perform the cutting through of the threads of
the cocoon described by Réaumur, and which he thought was done by
the facets of the eyes. It is well known that in order to guard
against the moths cutting the threads, silkraisers expose the cocoon
to heat sufficient to destroy the enclosed pupa. In Platysamia the
cocoon-cutters, though well developed, do not appear to be used at
all, and the pupa, like that of the silkworm and other moths
protected by a cocoon, moistens the silk threads by a fluid issuing
from the mouth, which also moistens the hairs of the head and
thorax, together with the antennæ. It remains to be seen whether
these structures are only occasionally used, and whether the
emission of the fluid is not the usual and normal means of egress of
the moth from its cocoon. Dr. Chapman remarks that throughout the
obtected moths “there are many devices for breaking through the
cocoon: specially constructed weak places in the cocoon, softening
fluid, applied by the moth, assisted by special appliances of
diverse sorts, such as in Hybocampa[107] and Attacus,” etc.
As to the fluid mentioned above, Trouvelot states that it is
secreted during the last few days of the pupa state, and is a
dissolvent for the gum so firmly uniting the fibres of the cocoon.
“This liquid is composed in great part of bombycic acid.” (Amer.
Naturalist, i, p. 33.)
The pupa of the dipterous genus Sciara (_S. ocellaris_ O. S.)
resembles a tineid pupa, and before transforming emerges for about
two-thirds of its length from the cocoon; the pupa-skin remaining
firmly attached in this position.[108]
Certain hymenopterous pupæ are provided with temporary deciduous
conical processes. Thus we have observed in the pupa of _Rhopalum
pedicellatum_ two very prominent acute tubercles between the eyes
(_h_, Fig. 592). As the cocoon is very slight, these may be of use
either in extracting itself from the silken threads or in pushing
its way along before emerging from the tunnel in the stem of plants.
(See also p. 611.)
_c._ The cremaster
Although this structure is in general confined to lepidopterous pupæ,
and is not always present even in them, since it is purely adaptive in
its nature, yet on account of its singular mode of development from the
larval organs, and the accompanying changes in the pupal abdomen, it
should be mentioned in this connection. The cremaster is the stout,
triangular, flattened, terminal spine of the abdomen, which aids the
pupa in working its way out of the earth when the pupa is subterranean,
or in the pupa of silk-spinning caterpillars its armature of secondary
hooks and curved setæ enables it to retain its hold on the threads of
the interior of its cocoon after the pupa has partially emerged from the
cocoon, restraining it, as Chapman well says, “at precisely that degree
of emergence from the cocoon that is most desirable.” He also informs us
that while in the “_pupæ incompletæ_ the cremaster is attached to an
extensible cable, which always allows some emergence of the pupa, in the
pupæ obtectæ there is no doubt but that in such cases as the Ichthyuræ,
Acronyctæ, and many others, it retains the pupal case in the same
position within the cocoon that the living pupa occupied; this is also
very usually the case in the Geometræ and in the higher tineids (my
pyraloids).”
In many of the more generalized moths there is no cremaster
(Micropteryx, Gracilaria, Prodoxus, Tantura, Talæporia, Psychidæ,
Hepialidæ, Zeuzera, Nola, Harrisina), though in Tischeria and
Talæporia (Fig. 590, but not in Solenobia) and Psychidæ, two stout
terminal spines perform the office of a cremaster, or there are
simply curved setæ on the rounded, unarmed end of the abdomen, as in
Solenobia.
In the obtected Lepidoptera, for example in such a group as the
Notodontidæ, where the cremaster is present, though variable in
shape, it may from disuse, owing to the dense cocoon, be without the
spines and hooks in Cerura, or the cremaster itself is entirely
wanting in Gluphisia, and only partially developed in Notodonta. In
the butterflies whose pupæ are suspended (Suspensi), the cremaster
is especially well developed. Reference might here be made to the
temporary pupal structures in certain generalized moths, which take
the place of a cremaster, such as the transverse terminal row of
spines in Tinea, the two stout spines in Tischeria, and the dense
rough integument and thickened callosities of the pupal head and end
of abdomen of Phassus, which bores in trees with very hard wood;
also the numerous stout spines at the end and sides of the abdomen
in Ægerians. These various projections and spines, besides acting as
anchors and grappling hooks, in some cases serve to resist strains
and blows, and have undoubtedly, like the armature in the larvæ and
imagines of other insects, arisen in response to intermittent or
occasional pressure, stresses, and impacts.
=Mode of formation of the cremaster and suspension of the chrysalis in
butterflies.=—We are indebted to Riley[109] for an explanation of the
way the cremaster has originated, his observations having been made on
species of over a dozen genera of butterflies (Suspensi).
He shows that the cremaster is the homologue of the suranal plate of the
larva.[110] The preliminary acts of the larva have been observed by
various authors since the days of Vallisneri, _i.e._ the larva hanging
by the end of the abdomen, turning up the anterior part of the body in a
more or less complete curve, and the skin finally splitting from the
head to the front edge of the metathoracic segment, and being worked
back in a shrivelled mass toward the point of attachment. The critical
feat, adds Riley, which has most puzzled naturalists, is the independent
attachment of the chrysalis and the withdrawal from and riddance of the
larval skin which such attachment implies. Réaumur explained this in
1734 by the clutching of the larval skin between sutures of the terminal
segments of the chrysalis, and this is the case, though the sutures act
in a somewhat different way.
Before pupation the larva spins a mass or heap of silk, the shape of
which is like an inverted settee or a ship’s knee, and “one of the
most interesting acts of the larva, preliminary to suspension, is
the bending and working of the anal parts in order to fasten the
back of the (suranal) plate to the inside of the back of the settee,
while the crotchets of the legs are entangled in the more flattened
position or seat.”
In shedding the larval skin, the following parts are also shed, and
have some part to play in the act of suspension: _i.e._ 1st, the
tracheal ligaments (Fig. 593, _tl_), or the shed tracheæ from the
last or 9th pair of spiracles; 2d, the rectal ligament (Fig. 593,
_rl_), or shed intestinal canal; 3d, the Osborne or retaining
membrane (_membrana retinens_, Fig. 593, _mr_), which is the
stretched part of the membrane around the rectum and in the anal
legs, and which is intimately associated with the rectal ligament.
[Illustration:
FIG. 593.—Shrunken larval skin of _Vanessa antiopa_, cut open from
the back and showing (_mr_) the retaining membrane, (_rl_) the
rectal ligament, and (_tl_) the tracheal ligaments.
]
The structures in the chrysalis are, first, the cremaster, with its
dorsal (Fig. 594, _dcr_) and ventral (_vcr_) ridges, and the
cremastral hook-pad (_chp_), said by Riley to be “thickly studded
with minute but stout hooks, which are sometimes compound or
furnished with barbs, very much as are some of our fishing-hooks,
and which are most admirably adapted to the purpose for which they
are intended.”
[Illustration:
FIG. 594.—Ideal representation of the anal subjoint of _Vanessa
antiopa_, from behind, with the spines removed, and all parts
forced apart by pressure so as to show the homologies of the parts
in the chrysalis which are concerned in pupation: homologies
indicated by corresponding letters in Fig. 595, except that _r_
(the rectum) corresponds with _pr_ in Fig. 595.
]
[Illustration:
FIG. 595.—Anal parts of chrysalis of _Vanessa antiopa_, just prior
to final extraction from shrunken larval skin: _c_, cremaster;
_chp_, cremastral hook-pad; _h_, one of the hooks, more enlarged;
_vcr_, ventral cremastral ridge; _dcr_, dorsal cremastral ridge;
_lr_, larval rectum; _pr_, pupal rectum; _rp_, rectal plate; _sr_,
sustentor ridges; _mr_, _membrana retinens_; _rl_, rectal
ligament; _tl_, tracheal ligament; the 11th or last
spiracle-bearing joint and the 12th joint being numbered.
]
Secondly, there are the other structures, viz., the sustainers
(_sustentors_), two projections which Riley states “homologize with
the soles (_plantæ_) of the anal prolegs, which take on various
forms (3), but are always directed forward so as easily to catch
hold of the retaining membrane.” These sustentors are, however, as
Jackson[111] has shown, and as we are satisfied, the vestiges of the
anal legs.
[Illustration:
FIG. 596.—_A_, chrysalis of Terias. _B_, posterior end of chrysalis
of Paphia. _C_, posterior end of chrysalis of Danais. _E_, one of
the sustainers of Terias, greatly enlarged to show its hooked
nature. All the parts of subjoint lettered to correspond with Fig.
595.
]
Thirdly, the sustentor ridges, which, as Riley states, may be more
or less obsolete in some forms, in Paphia (Fig. 596, _B_) and
Limenitis form “quite a deep notch, which doubtless assists in
catching hold of the larval skin in the efforts to attach the
cremaster.”
[Illustration:
FIG. 597.—Pupation of butterflies: _a_, attachment of larva of
_Danais archippus_; _p_, attachment of larva of _Paphia
glycerium_; _b_, ideal larva soon after suspension; _d_, ideal
larva a few hours later, the needle (_n_) separating the forming
membrane from the sustainers; _l_, ideal larva just before
splitting of larval skin, with retaining membrane loosened from
the sustainers and showing its connection both with the larval and
pupal rectum. In all the figures the joints of the body are
numbered; the forming chrysalis is shaded in transverse lines; the
intervening space between it and larval skin is dotted: _h_, is
the hillock of silk; _hl_, hooks of hind legs; _ap_, anal plate;
_lr_, larval rectum; _pr_, pupal rectum; _mr_, retaining membrane;
_c_, cremaster; _s_, sustainers.—This and Figs. 593–596 after
Riley.
]
“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.
[Illustration:
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.
]
[Illustration:
FIG. 599.—Pupa of the same.
]
[Illustration:
FIG. 600.—Imago of the same.—This and Figs. 598 and 599 after Newport,
from Gegenbaur.
]
[Illustration:
FIG. 601.—Nervous system of the larva of _Sphinx ligustri_.
]
[Illustration:
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.)
[Illustration:
FIG. 603.—Changes in the nervous system of _Vanessa urticæ_, during
and after pupation.—After Newport.
]
[Illustration:
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.
[Illustration:
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.
[Illustration:
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.
]
[Illustration:
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.
[Illustration:
FIG. 608.—Feet of the Pieris butterfly withdrawing from those of the
larva.
]
[Illustration:
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.
[Illustration:
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.
[Illustration:
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.
]
[Illustration:
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.
[Illustration:
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.
[Illustration:
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.
]
[Illustration:
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.
[Illustration:
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.
[Illustration:
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.
[Illustration:
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.
]
[Illustration:
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.
The ocular buds appear towards the end of larval life as a simple mass
of hypodermic cells, and form a compact layer on the dorsolateral face
of the prothoracic segment, and clothe the cephalic ganglion or brain
like a skull-cap. The central portion only is destined to form the eye,
while the peripheral pad, continuing to thicken, gives rise to a
voluminous and rounded mass, which meets on the median line that of the
opposite side, and forms the integument of all the posterior part of the
head.
Bugnion also observed on the median line a group of small hypodermic
cells which he regarded as the rudiment of the anterior ocellus, but he
did not detect those of the posterior ocelli.
=The antennal buds.=—These appear at an early date under the cuticle of
the head, as two distinct rounded cellular masses, with a central
cavity, but no annular zone (Fig. 619, _f_). Each one grows longer in a
transverse sense, and its summit, extended from the outer side, curves
downward. It now forms a hollow tube folded at the end, and terminated
by a disk whose centre is perforated (Fig. 619, _f_). Afterwards, when
the larva is ready to transform, it grows longer, becomes folded on
itself in its cavity, and, passing beyond on each side the limits of the
larval head, encroaches on the prothoracic segment.
=The buds of the buccal appendages.=—Towards the end of the larval
period, the buds of the mouth-parts appear as small digitiform
projections, situated on each side and below the mouth. Formed of small
epithelial cells pressed against each other, they are all directed
anteriorly, and possess no furrow or pad.
The 2d maxillæ (labium) is formed of two separate parts. The imaginal
buds of the lower lip appear on each side of the median line, with a
fissure indicating the differentiation of the palpus. On each side are
to be seen the 1st maxillary buds, bearing each a rudimentary palpus,
and, farther in front, the buds of the mandibles.
=The buds of the ovipositor.=—The six stylets of the ovipositor arise
from six small imaginal buds which become visible in the second half of
the larval period, on each side of the median line, on the lower face of
the three last segments (Fig. 620, _q^1_, _q^2_, _q^3_). The bud is
differentiated into a central discoidal bud, a furrow, and a marginal,
rather thick swelling or pad. Afterwards, these buds elongate and form
small papilliform projections directed backwards (Fig. 621); but only
during the pupal period do they, as already observed in Bombus, approach
each other and assume their definite shape as an ovipositor.
[Illustration:
FIG. 620.—End of larva of Encyrtus of 2d stage, showing the three
pairs of imaginal buds of the ovipositor _q^1_, _q^2_, _q^3_.
]
[Illustration:
FIG. 621.—The same in an older larva ready to transform: _i_,
intestine; _x_, genital gland; _a_, anus.—After Bugnion.
]
Finally, Bugnion states that while metamorphosis in the Hymenoptera is
less highly modified than in the Muscidæ, it is more marked than in the
Coleoptera and Lepidoptera. In these orders the pupa moves the abdomen,
but in Hymenoptera it is absolutely immovable throughout pupal life, as
long as the integument is soft.
DEVELOPMENT OF THE IMAGO IN THE DIPTERA
The flies, particularly the Muscidæ and their allies (Brachycera), are
the most highly modified of insects, their larvæ having undergone the
greatest amount of reduction and loss of limbs, this atrophy involving
even most of the head. The following account has been prepared in part
from the works of Weismann, Ganin, Miall, and Pratt, but mostly from the
excellent general summarized account given by Korschelt and Heider.