during which no food is taken, the entire activity of life seems to be
turned to deep-seated and complicated internal developmental processes.
These inner changes involve an almost complete destruction of many
organs of the larva, and their renewal from certain germs (the imaginal
buds) already present in the larva, as will be seen in the highly
modified Muscidæ. Only a few larval organs become directly transferred
into the body of the pupa and imago. Such are the rudiments of the
genital system. The heart also, and the central portion of the nervous
system, suffer only slight and unimportant, almost trivial, internal
changes. On the other hand, most of the other organs of the larva become
completely destroyed: the hypodermis, most of the muscles, the entire
digestive canal with the salivary glands; while their cells, under the
influence of the blood corpuscles (leucocytes), which here act as
phagocytes, fall into pieces, which are taken up by them and become
digested. Simultaneously with this destructive, histolytic process, the
new formation of the organs by the imaginal buds, already indicated in
the embryo, is accomplished in such a way that the continuity of the
organs in most cases remains unimpaired. This process of transformation
can only be understood by considering that of the embryonal germs of the
organs, (1) only a part is destined for the use of the larva in growth,
and for the performance of certain functions which exhaust themselves
during larval life, so that it is no more capable of farther
transformation, and finally becomes destroyed; while (2) a second part
of the embryonal germs or rudiments persists first in an undeveloped
condition, as imaginal buds, in order to undertake during the pupa stage
the regeneration of the organs.
Though Swammerdam knew that the rudiments of the wings were already
present under the skin of the larvæ, we are indebted, for our
present knowledge, to the thorough and profound investigations of
Weismann on the metamorphosis of the Diptera, and also to the
researches of Ganin and others who have worked on the pupæ of
Muscidæ, in which the development is most complicated and modified.
In the more generalized and primitive Diptera, such as Corethra, the
processes of formation of the pupa and imago are much simpler than
in the muscids and Pupipara. These processes are still simpler in
the Lepidoptera and Hymenoptera, and for this reason we have given a
summary of what has been done on these organs by Newport, Dewitz,
and especially by Bugnion.
Our knowledge of this subject is still very imperfect, only the more
salient points having been worked out, and, as Korschelt and Heider
state, there is still lacking certain proof as to how far the
relations of the internal changes known to exist in the Muscidæ also
apply to other orders of insects, though it must be considered that
in the pupa of Lepidoptera, Hymenoptera, perhaps also the
Coleoptera, and we would add in the Neuroptera as well as the male
Coccidæ, very similar metamorphic processes take place.
_a._ Development of the outer body-form
The form of the imago is completely marked out in the pupa, so that the
transition from the pupa to the imago is comparatively slight and only
depends on the modification and development of the parts already
present.
[Illustration:
FIG. 622.—Anterior part of young larva of _Simulium sericea_, showing
the thoracic imaginal buds: _p_, prothoracic bud (only one not
embryonic); _w_, _w′_, fore and hind wing-buds; _l_, _l′_, _l″_,
leg-buds; _n_, nervous system; _br_, brain; _e_, eye; _sd_, salivary
duct; _p_, prothoracic foot.—After Weismann.
]
In most cases the modification in question consists of the changes
occurring during the passage from the larval form to the imago, the
reformation of parts already present being most marked, while the new
rudiments only participate in a limited way in the process. Thus, for
example, the head of the caterpillar together with the antennæ and
mouth-parts, also the thoracic limbs, pass directly and unchanged from
the larva into the pupa. The compound eyes and the wings are, however,
new formations, the latter arising from imaginal buds. The same is the
case with many other Heterometabola, where the passage of the larva into
the pupa in general is due to a transformation of parts already present.
The changes in the brain, the fusion of certain ganglia of the ventral
nervous cord, the changes in the abdomen, involving the reduction in the
number of segments and the remodelling of the end of the body, and the
formation of the ovipositor or sting, and in the higher Hymenoptera the
transfer of the 1st abdominal segment to the thorax, and the origin of
the genital armature,—all these should here be taken into account.
It should be observed that in every case where the larvæ are footless,
as in Diptera, all the Hymenoptera except the phytophagous ones and
certain coleopterous larvæ, the limbs of the imago stage are, in the
earliest stages, indicated as new structures in the form of imaginal
buds.
=Formation of the imago in Corethra.=—Corethra may serve as an example
of such a relatively simple metamorphosis. Its larva belongs to the
group of eucephalous dipterous larvæ. The head of the perfect insect is
already indicated in the larva, and its parts, with certain
modifications, pass directly into the pupa. The compound eyes, and this
is a rare exception among the Holometabola, are present in the larva. On
the other hand, the thoracic legs, the wings, and halteres are developed
out of new rudiments which are present in the last larval stage, before
pupation. Each thoracic segment has four of them, two ventral and two
dorsal (Fig. 622); the ventral buds becoming the legs. Of the dorsal
pairs, that of the mesothorax develops into wings, that of the
metathorax into halteres, while from the corresponding rudiments of the
prothorax in Corethra arise the stigma-bearing dorsal or respiratory
processes of the pupa, and in Simulium a tuft of tracheal gills (Fig.
623, _ra_; see also Fig. 582).
[Illustration:
FIG. 623.—Late larva of Simulium, showing the rudiments of the pupal
structures within the larval skin: _l^1_, _l^2_, _l^3_, fore,
middle, and hind legs of the fly; _ra_, respiratory appendages of
pupa; _w_, wing of fly; _h_, halter of fly.—After Miall.
]
[Illustration:
FIG. 624.—Imaginal buds in larva of Corethra (diagrammatic
cross-section of thorax): invaginations (_fe_ and _be_) of the
larval hypodermis (_lhy_) in whose bases the rudiments of wings
(_fa_) and legs (ba) arise; _lh_, chitinous integument of the
larva.—After Lang.
]
These imaginal buds may be regarded as evaginations of the outer surface
of the body. The only difference is that the buds of the appendages as a
whole seem sunken below the level of the surface of the body, being
situated at the bottom of an evagination, as in the buds of the head and
trunk in the Pilidium larva of nemertean worms, and in the rudiments of
the lower surface of the body of Echinus present in the pluteus larva.
The lumen of the invagination in which the appendages of Corethra (and
other Holometabola) are situated is called by Van Rees the _peripodal
cavity_, and the external sheath bordering it, which is naturally
continuous with the hypodermis of the body, the _peripodal membrane_
(Fig. 636, _p_).
We must adopt the view that the rudiments of the appendages
(imaginal buds) are from the first divided into ectodermal and
mesodermal portions, which are derived from the corresponding
germ-layers of the larva. The ectoderm of the rudiments of the
appendages is continuous with the peripodal membrane, and through it
with the hypodermis. Weismann was inclined to derive the organs
(tracheæ, muscles, etc.) developing within the germs of the
appendages from a hypertrophy of the neurilemma of a nerve passing
down from within into the imaginal bud, and held that nerves and
tracheal branches soon after passed into the inner surface of the
imaginal bud. (Korschelt and Heider.)
When the imaginal buds of the appendages enlarge, then the peripodal
membranes become correspondingly distended, and the limbs within assume
a more or less crumpled position, and in Corethra are spirally twisted,
while the rudiments of the wings are folded. The completion of the
rudimentary limbs is accomplished simply by their passing out of the
invagination in which they originated. The limbs thus gradually become
free, the peripodal membrane is seen to reach the level of the rest of
the hypodermis and become a part of it, and the base of the extremity is
no longer situated in a cavity.
The internal organs of Corethra undergo but to a slight degree the
destruction (histolysis) which is so thoroughgoing in the Muscidæ.
Kowalevsky states that in the mid-intestine of Corethra a histolysis of
the larval and reconstruction of the imaginal epithelium goes on in the
same way as has been described in Musca. Most of the larval organs pass
without histolytic changes directly over into those of the pupal and
imaginal stages; the muscles in general are also unchanged, but those of
the appendages and wings are made over anew. The last arise, according
to Weismann, in the last larval stage from strings of cells which are
already present in the embryo.
When we consider how insignificant the internal transformations are
during the metamorphosis of the Tipulidæ, of which Corethra serves as an
example, we can scarcely doubt that we here have before us conditions
which illustrate the passage between an incomplete and a complete
metamorphosis. Thus, among other things, should be mentioned the short
duration of the pupa stage and the activity of the pupa, as also the
early appearance of the germs of the compound eyes, a character which
Corethra has in common with the Hemimetabola. (Korschelt and Heider.)
=Formation of the imago in Culex.=—In respect to the formation of the
imaginal head, Culex is still more primitive than Corethra. Miall and
Hammond find from Hurst’s partly unpublished descriptions and
preparations that there are no deep invaginations for the compound eyes
or antennæ of the imago.
“The compound eye forms beneath the larval eye-spots, and is at
first relatively simple and composed of few facets. The number
increases by the gradual formation of partial and marginal
invaginations, each of which forms a new element. The imaginal
antenna grows to a much greater length than that of the larval
antenna, and its base is accordingly telescoped into the head, while
the shaft becomes irregularly folded.[115] Culex, though more
modified than Chironomus in many respects, _e.g._ in the
mouth-parts, is relatively primitive with respect to the formation
of the imaginal head, and shows a mode of development of the eye and
antenna which we may suppose to have characterized a remote and
comparatively unspecialized progenitor of Chironomus.”
=Formation of the imago in Chironomus.=—The development of the head of
the imago of _Chironomus dorsalis_ has been discussed by Miall and
Hammond. The invaginations which give rise to the head of the fly could
not be discovered even in a rudimentary state until after the last
larval moult.
“Weismann has given reasons for supposing that invaginated imaginal
rudiments could not come into existence before the last larval moult
in an insect whose life-history resembles that of Corethra or
Chironomus. If the epidermis were invaginated in any stage before
the ante-pupal one, the new cuticle, moulded closely upon the
epidermis, would become invaginated also, and would appear at the
next moult with projecting appendages like those of a pupa or imago.
This is actually the way in which the wings are developed in some
larval insects with incomplete metamorphosis. In Muscidæ the
invaginations for the head of the imago have been traced back to the
embryo within the egg,[116] but the almost total subsequent
separation of the disks from the epidermis renders their development
independent of the growth of the larval cuticle and of the moults
that probably take place therein.”
The pupal and imaginal cuticles do not follow at all closely the larval
skin, but, says Miall, become at particular places folded far into the
interior. “The folds which give rise to the head of the fly are two in
number and paired. They begin at the larval antenna on each side of the
head, and gradually extend further and further backwards. The object of
the folds is to provide an extended surface which can be moulded,
without pressure from surrounding objects, into the form of the future
head. On one part of each fold the facets of the large compound eyes are
developed; another part gives rise to the future antenna, a large and
elaborate organ, which springs from the bottom of the fold, and whose
tip just enters the very short antenna of the larva. The folds for the
head ultimately become so large that the larval head cannot contain
them, and they extend far into the prothorax. Here a difficulty occurs.
If the generating cuticle of the prothorax were also to be folded
inwards, the future prothorax would take a corresponding shape. But the
prothorax of the fly has a form dictated to it by the limbs which it
bears and by the muscles to which it gives attachment. These call for a
great reduction in its length, and a peculiar shape, which it is not
here necessary to describe. It will be enough to realize that the
epidermis of the future prothorax cannot be sacrificed to the folds
which are to give rise to the head of the fly. All interference between
the two developing structures is obviated by the provision of a
transverse fold, which pushes into the prothorax from the neck, and
forms a sort of internal pocket. The floor of the pocket forms two
longitudinal folds, which prolong the folds originating in the larval
head. The roof of the pocket shrinks up and forms the connection between
the head and thorax of the fly. Ultimately the head-part is drawn out,
leaving the prothoracic structures unaffected.”[117]
[Illustration:
FIG. 625.—Process of formation of the parts of the head of the fly in
the larva of Chironomus (male): _A_, the new epidermis thrown into
complicated folds which have been cut away in places to show the
parts within. _B_, the same parts in horizontal section; _lc_,
larval cuticle; _tf_, transverse fold; _tf′_, upper wall of the
same; _m_, cut edge of new epidermis; _ant_, larval antenna; _an_,
nerve to the same; _ant′_, antenna of fly; _lf_, longitudinal fold;
_o_, eye of fly; _on_, optic nerve; _an′_, root of antennary nerve;
_br_, brain; _œs_, œsophagus; _b_, bulb of antenna of fly; _s_, _s_,
_s′_, blood-spaces.—After Miall.
]
The development of the head of the fly of Chironomus appears, as Miall
and Hammond state, to be intermediate between the groups Adiscota and
Discota of Weismann; _i.e._ “between the types in which the parts of the
head of the fly are developed in close relation to those of the larva,
and the types in which deep invaginations lead apparently to the
formation of similar new parts far within the body, the seeming
independence of the new parts being intensified by thoroughgoing
histolysis,” and they suggest that possibly types may be discovered
intermediate between Chironomus and Muscidæ.
[Illustration:
FIG. 626.—_A_, _B_, _C_, _D_, diagrams of transverse sections showing
the development of the wings, legs, and the imaginal hypodermis of
muscid flies from the imaginal buds of the larva during
metamorphosis: _lh_, chitinous integument of larva from which the
underlying hypodermis (_lhy_) has withdrawn; _iid_, imaginal buds of
wings, _iiv_, of legs; _is_, the cords connecting them with the
hypodermis; _fl_, wing-germs; _b_, leg-germs; _ihy_, imaginal
hypodermis spreading out in _D_ from the imaginal buds. The imaginal
rudiments of the hypodermis are indicated by thick, black outlines,
the larval hypodermis by two thin, parallel lines.—After Lang.
]
We are now prepared to consider the extremely complicated changes, in
the Muscidæ, leaving out of consideration the origin of the wings from
imaginal buds, which has already been discussed on pp. 126–137.
=Formation of the imago in Muscidæ.=[118]—In the flesh, and undoubtedly
the house, and allied flies the germs or imaginal buds of the legs and
wings arise in the same way as in Corethra. But in the Muscidæ, the buds
are situated far within the interior of the body, the peripodal cavities
appear closed, and the peripodal membrane stands in connection with the
hypodermis merely by means of a delicate thread-like stalk. This
connecting cord, which was first detected by Dewitz, and whose
interpretation was entirely right, shows in its interior, as Van Rees
proved, a narrow cavity.
Though the earliest stages in the development of imaginal buds in the
embryo of the Muscidæ are still unknown, yet we shall not go far astray
if we refer them, like the imaginal buds of Corethra, to hypodermal
invaginations. We must, then, regard the stalk-like connection just
mentioned as the long drawn-out neck of this invagination.
In general, the development of the appendages (Figs. 626, 627) goes on
as described in Corethra. The rudiments of the legs enlarge and show at
an early date the first traces of the later joints. They are so packed
in the peripodal cavities that the single joints of the extremities
appear as if pushed in “like the joints of a travelling cup.” (Van
Rees.) The evagination of the completely formed buds of the limbs, which
occurs on the first day after the beginning of pupation, goes on in such
a way that the stalk of the imaginal bud (Figs. 626, _B_; 627, _B_)
shortens, while its cavity widens so that the limbs finally, as in
Corethra, pass out through the widely opened mouth of the peripodal
invagination, which at the same time gradually completely disappears.
The peripodal membrane is converted into a thickened part of the
hypodermis in the region adjoining the base of the leg, and from this
thickened hypodermal portion, the formation of the hypodermis of the
entire imaginal thorax goes on, as the larval hypodermis is gradually
destroyed.
[Illustration:
FIG. 627.—Imaginal buds of muscid flies in process of development:
_A_, brain (_c_) and ventral ganglion (_v_) of a larva, 7 mm. long,
of _C. vomitoria_; _h_, head-rudiment; _rc_, portion of ventral
cord; _pd_, prothoracic rudiment; _vc_{3}_, third nerve; _md_,
mesothoracic rudiment. _B_, mesothoracic rudiment more advanced, in
a pupa, just formed, of _Sarcophaga carnaria_, showing the base of
the sternum and folds of the forming leg, the central part (_f_)
representing the foot. _C_, the rudimentary leg of the same more
advanced; _f_, femur; _t_, tibia; _f_{1}_, _f_{5}_, tarsal joints.
_D_, two buds from a larva, 20 mm. long, of Sarcophaga, attached to
tracheæ; _msw_, mesonotal and wing-germ; _mt_, metathoracic
rudiment. _E_, _r_, mesothoracic germ of a 7 mm. long larva attached
to a tracheal twig.—After Weismann and Graber, from Sharp.
]
We must here settle the question as to the first origin of the
mesodermal portions of the rudiments of the appendages. We can
already distinguish in the imaginal buds of the fully grown muscid
larva a clear separation between an ectodermal and an inner
mesodermal part. Ganin derived the mesodermal part through a sort of
differentiation and separation of the innermost layer of the
ectodermal part, and Van Rees has, in general, confirmed this view.
Kowalevsky, on the other hand, is inclined to the view that the
mesodermal part of the imaginal bud is derived from the embryonal
cells of the mesoderm. He finds scattered throughout the mesoderm,
under the hypodermis of the larva, so-called wandering cells (Fig.
632, _A_, _w_), which are different in appearance from the
leucocytes and from the elements from which the formation of the
mesodermal parts of the imaginal rudiments proceed. Kowalevsky is
inclined to believe that there are in each segment rudiments of the
imaginal mesoderm, but which are so delicate and indifferent that we
cannot find them in the first stages of their origin. From these
mesodermal imaginal rudiments the above-mentioned wandering cells of
the mesoderm are derived, which afterwards come into connection with
the ectodermal portion of the imaginal buds.
Still more complicated and difficult to understand is the development of
the head-section of muscids. We must remember that in muscid larvæ the
head-section exists in its most rudimentary form, being the result of
extreme modification and degeneration. The small size of the head is
also due to the fact that it is more or less retracted within the
thoracic region. Then, as shown by the researches of Weismann, in the
last embryonal stages, the forehead, mandibles, and the whole region of
the head around the mouth invaginate and form a sunken cavity (Fig. 628,
_p_), in which the chitinous supports of the hooks characteristic of
muscid larvæ are soon developed. This sunken part of the head, at whose
inner end is the œsophagus, is called by the not entirely appropriate
name of “pharynx,” and it must at present be remembered that the hollow
space thus named is not a part of the digestive canal. It is an
invaginated section of the head, _and the formation of the head of the
imago mainly depends on the evagination of this region_.
The first rudiments of the most important parts of the head (eyes,
antennæ, and forehead), occur in the youngest larvæ as paired masses of
cells which lie in the thorax next to the two halves of the brain (for
this reason called by Weismann “brain-appendages”), which are from their
first origin connected with the pharynx, and may be regarded as the
imaginal buds of the head. These appear very soon in later stages in the
shape of elongated sacs widening at the hinder end (Fig. 628, _A_ and
_B_, _h_), which from their origin are to be regarded as evaginations of
the pharynx. Very soon epithelial thickenings appear in the wall of this
sac-shaped brain-appendage, in which the rudiments of the parts of the
future head may be recognized.
Disk-shaped thickenings in the hinder widened part of the
brain-appendage form the rudiments of the compound eyes, which therefore
may be called the eye-buds. On the basal surface of the eye-buds is
situated a nervous expansion which is connected by a nerve with the
supraœsophageal ganglion. This nerve becomes the optic nerve of the
perfect animal, while the optic ganglion is clearly separated from the
brain.
In the anterior, more cylindrical or tube-like part of the
brain-appendage we find the “frontal buds” (_ss_), on which the antennal
rudiments (_at_) soon bud out, in exactly the same way as the rudiments
of the limbs arise from the imaginal buds.
[Illustration:
FIG. 628.—Diagrammatic representation of the position of the imaginal
buds in the larva (_A_) and pupa (_B_) of Musca (the wing rudiments
omitted): _as_, eye-buds; _at_, antennal germs; _b^1_-_b^3_, germs
of the legs; _bg_, central ganglionic cord: _g_, brain; _h_,
so-called frontal appendage (_Hirnanhang_): _m_, peripodal membrane;
_o_, opening of the frontal appendage into the pharynx; _oe_,
œsophagus; _p_, so-called “pharynx”; _r_, rudiment of the proboscis;
_ss_, frontal bud; _st_, stalk-like connection of the peripodal
membrane with the hypodermis; _I_-_III_, 1st, 2d, and 3d thoracic
segments.—Adapted from Van Rees, by Korschelt and Heider.
]
Originally (Fig. 628, _A_) the brain-appendages lie tolerably far behind
in the thorax of the larva, so that they connect the hindermost part of
the wall of the pharynx with the foremost section of the brain, which
they surround in the form of a mushroom. Afterwards, however, subsequent
to pupation, they move, together with the central nervous system,
farther forward (_B_), whereby they (if we have correctly understood the
descriptions of Weismann and Van Rees) laterally surround the pharynx
with their anterior end, which is somewhat ventrally bent. At the same
time, there becomes established a gradually widening communication (_B_,
_o_) between the brain-appendage and the pharynx, which soon extends in
the form of a lateral pharyngeal fissure along the entire length of the
brain-appendage. As a result, the cavity of the brain-appendage and the
pharynx so completely unite that the two soon form a single sac, the
head-sac or vesicle (Fig. 6–9, _k_). The walls of this head-vesicle are
the later head-wall, the most important parts of which can now be
recognized (the antennæ, eyes, rudiments of the beak). It is now
necessary that the head-vesicle (Fig. 629, +, +) be, by the eversion of
the pharynx, turned outward in order that the head of the pupa may be
completed. By this eversion of invaginated parts, the former
mouth-opening of the pharynx becomes a neck-section (Fig. 629, +, +) by
which head and thorax are now united. (Korschelt and Heider.)
[Illustration:
FIG. 629.—Diagram of the changes to pupa of Musca before imago
appears; the wing-germs not drawn: _as_, eye-buds; _at_, antennal
germs; _b^1_-_b^3_, leg-germs; _bg_, ventral nerve-cord; _g_, brain;
_k_, head-vesicle (originating from the union of the pharynx with
the hypophysis, _Hirnanhängen_); _oe_, œsophagus; _r_, germ of the
proboscis; _ss_, germ of the forehead; _I_, _II_, _III_, 1st, 2d,
and 3d thoracic segments.—Based on Kowalevsky and Van Rees, with
changes, after Korschelt and Heider.
]
The cause of the eversion of the head-vesicle, which Weismann
directly observed, appears to be due to an increase of the inner
pressure through a contraction of the hinder parts of the body. The
anterior end of the œsophagus now becomes turned down ventrally
corresponding to the conformation of the head of the imago.
It has been shown that the so-called pharynx is only an invaginated
part of the outer surface of the larval head. The brain-appendage
Korschelt and Heider consider to be the diverticulum of this
invagination, in which the single parts of the body lie in an
invaginated state. They may throughout be compared to the rudiments
of the thoracic limbs. All these imaginal buds have been traced back
to the invaginated parts of the outer surface of the body, _i.e._
the ectoderm.
It should be borne in mind that the process of development of the head
of the highly-modified Muscidæ is much more complex than in the more
primitive Diptera.
In their essay on the development of the head of the imago of
Chironomus, Miall and Hammond arrange the dipterous types thus far
examined, in the order of complexity of the invaginations which give
rise to the head of the imago, in the following order:—
1. Culex. Relatively simple. Invaginations of the imaginal buds,
shallow. 2. Corethra, Simulium. } Intermediate. 3. Chironomus,
Ceratopogon. } 4. Muscidæ. Relatively complex. Invaginations
deep, and apparently, but not really, unconnected with the
epidermis.
_b._ Development of the internal organs of the imago
[Illustration:
FIG. 630.—Median longitudinal section through larva of blow-fly during
the process of histolysis: _an_, antenna; between _an_ and _w_,
rudiments of eye; _w_ wings; _h_, halteres; _b_{1}_-_b_{3}_, legs;
_f_, fat-body; _d_, middle of intestine; _n_, ganglia; _st_, stigma;
6, 7, 6th and 7th body-segments.—After Graber, from Sharp.
]
It has already been observed that most of the organs of muscid larvæ
(and this applies to most Diptera, Lepidoptera, Coleoptera, and
Hymenoptera) are destroyed through the action of leucocytes, and that
their reformation is accomplished by definite groups of embryonal cells,
the imaginal buds or folds. Destruction and rebuilding occur during the
pupa stage in such a way that in many cases while this process is going
on the continuity of the organs does not seem to be disturbed. These
transformations especially concern the hypodermis, the digestive canal,
the muscles, the fat-body, and the salivary glands.
The transformation of the tracheal system is only partial, being in part
a simple process of regeneration through cell-division. Slighter changes
affect the heart, the central nervous system, and the reproductive
system (Fig. 630).
[Illustration:
FIG. 631.—Diagram of the formation of the imaginal hypodermis on the
abdomen of Muscidæ: _hi_, imaginal buds of the hypodermis; _lh_,
larval hypodermis.—After Lang.
]
[Illustration:
FIG. 632.—Section through the abdominal bud of the hypodermis of
Musca: _A_, of the larva; _B_ and _C_, of the pupa; _h_, larval
hypodermis; _h′_ separated portion of the same attacked by
phagocytes; _i_, imaginal bud; _k_, phagocytes with what are called
cell-wrecks or fragments (so-called granulated cells); _k′_,
phagocytes enclosing hypodermal nuclei; _m_, mesoderm-germ of the
imaginal bud; _w_, wandering cells.—After Kowalevsky, from Korschelt
and Heider.
]
=The hypodermis.=—The hypodermis of the imago arises through an
extension of the ectodermal part of the imaginal buds. We have already
mentioned this for the thorax. As the appendages of the thorax in the
pupa gradually attain perfection, the hypodermis layer spreads from the
place of their insertion, the layer consisting of numerous small cells
whose origin we must refer to the peripodal membrane. This layer
continues to spread over the surface of the pupal thorax, while at the
same time the area of the larval hypodermis, consisting of large cells,
is seen to diminish. Hence the thin edge of the newly-formed hypodermis
(Fig. 631, _hi_) slowly grows into the space between the superficial
cuticula and the larval hypodermis (Fig. 632, _h_), so that at this
place the old hypodermis undergoing destruction eventually lies on the
inner side of the newly-formed epithelial layer (_B_). We therefore see
from this that, during the replacement of the old hypodermis by the new,
the continuity of the superficial epithelium is never interrupted. Since
the edges of the two kinds of hypodermis overlap, the surface of the
body is nowhere bare of epithelium. The dissolution of the larval
hypodermis is accomplished under the influence of the leucocytes (Fig.
632, _k_), which attack the larval hypodermis-cells and absorb their
contents piece by piece, and so fill themselves with bits of the
hypodermis-cells and their nuclei; since these fragments have the shape
of roundish granules, they were called by Weismann granule-balls. These
granule-balls, which fill the body-cavity of the later pupal stage, are
nothing else than the leucocytes (blood corpuscles) which have absorbed
the fragments of tissue of the larval body.
It should here be said that the destruction of the larval tissues is not
to be attributed to the previous death of the cells, but is the result
of the action of the leucocytes on tissues which, though weakened in
their vital power, are still living. While the completely healthy,
active tissues, _i.e._ those of the imaginal buds, withstand the attacks
of the leucocytes, the less healthy larval tissues are by the attacks of
the leucocytes divided into fragments and eaten and digested by them.
This process is most marked in the histolysis of the larval muscles. The
destruction of most of the larval organs depends, therefore, on the
capacity of the amœboid blood-corpuscles for taking food and on
intracellular digestion, as was first shown by Metschnikoff, who has
given to these leucocytes the name of “phagocytes.”
This process of histolysis goes on in the same way in the head and
abdomen as in the thorax. In the abdomen, as Ganin first proved, there
are in each of the eight segments of which it consists in the larva four
small cellular islets or imaginal buds (Figs. 631, _hi_, 632, _i_), from
which originate the new hypodermis.
Van Rees has lately found in the abdominal segments another pair of
smaller imaginal buds. The four imaginal buds occurring in the last
segment are situated close to each other, encircling the anal opening
(Fig. 633, _ims_), and take part in the formation of the hind-intestine,
the rectal pouches and rectal papillæ. To this segment also belong the
two pairs of imaginal genital buds (rudiments of the external sexual
organs) which were first found by Künckel d’Herculais in Volucella.
The newly formed hypodermis spreads rapidly over the outer surface of
the body, so that hypodermal areas corresponding to the separate
imaginal buds soon unite. Simultaneously with this completion of the
definite epithelial layer the larval hypodermis becomes completely
destroyed by the phagocytes.
=The muscles.=—A similar process of destruction by phagocytes affects
the greater number of the larval muscles, except the three pairs of
thoracic muscles employed in respiration, and which pass intact from the
larva to the imago. Indeed, the dissolution of the muscles is the first
process which occurs in the metamorphosis. The destruction of the larval
muscles is accomplished in such a way that, a great number of leucocytes
which have collected on the surface of the muscular fibres, press
through the sarcolemma and enter within the muscular tissue, filling the
spaces formed between them, By this means the muscles break up into a
number of rounded particles which are taken into the interior of the
leucocytes. Thus a collection of granule-balls arise from the muscles,
which finally separate from each other and become scattered throughout
the body-cavity of the pupa. In the same way as the muscular substance,
the muscle-nuclei are taken up and digested by the phagocytes.
The imaginal muscles develop from the definitive mesoderm which has
originated from the mesoderm of the imaginal buds (Fig. 632, _C_, _m_).
=The digestive canal.=—As in the hypodermis and muscles, the histolysis
of the larval digestive tract and its new formation from separate
imaginal buds go on simultaneously, so that the continuity of the
process is not interrupted.
[Illustration:
FIG. 633.—Digestive tract of a Musca larva with the imaginal germs:
_bd_, cœca; _s_, food-reservoir; _is_, imaginal ring of the salivary
gland (_sp_); _f_, fat-cells at the end of the salivary gland; _pr_,
proventriculus; _r_, its ring; _ie_, imaginal cells of the
mid-intestinal epithelium; _ch_, chyle-stomach; _ma_, urinary tubes;
_im_, imaginal cells of the mid-intestinal, muscular layer; _ims_,
binder, abdominal, imaginal buds; _h_, hind intestinal, imaginal
bud; _ht_, hind-intestine.—After Kowalevsky, from Korschelt and
Heider.
]
The imaginal buds of the much-shortened pupal digestive canal occur in
the mid-intestine (stomach) in the form of numerous scattered groups of
cells (Fig. 633, _ie_), and in the fore- and hind-intestine in the form
of rings (_v_ and _h_) of imaginal tissue. The imaginal ring of the
fore-intestine (_v_) lies in the region of the proventriculus (_pr_,
compare Fig. 635, _im_), while that of the hind-intestine is situated
directly behind the base of the urinary tubes. The regeneration of these
two parts of the digestive canal is not entirely accomplished by these
two rings, but the imaginal rudiments of the neighboring parts of the
outer surface of the body also have a share in it. Thus it appears that
the foremost part of the œsophagus is built up from the imaginal buds in
the region of the mouth, while the imaginal buds surrounding the anus in
the 8th abdominal segment (Fig. 633. _ims_) produce by invagination the
rectal pouches, together with the rectal papillæ.
[Illustration:
FIG. 634.—Cross-section through the mid-intestine of pupa of Musca:
_e_, rejected and degenerate epithelium of the larval stomach; _f_,
cellular layer newly formed around the same; _m_, muscular layer;
_m′_, imaginal cell of _m_; _o_, imaginal bud of the mid-intestinal
epithelium; _t_, tracheal stem.—After Kowalevsky, from Korschelt and
Heider.
]
[Illustration:
FIG. 635.—Longitudinal section through the proventriculus of a muscid
larva: _im_, fore-intestinal, imaginal ring; _oe_, œsophagus; _pr_,
proventriculus.—After Kowalevsky, from Korschelt and Heider.
]
The formation of the mid-intestine (stomach) takes place in such a way
that the island-like imaginal buds spread out by cell-multiplication
over the outer or basal surface of the larval mid-intestinal epithelium
(Fig. 634, _o_), until they finally unite, so as to form the wall of the
imaginal mid-intestine (stomach). At the same time the entire larval
epithelium (_e_) is cast in the interior and forms the so-called yellow
body, which becomes surrounded by a layer of small cells and a
jelly-like mass, and remains until its destruction in the pupal stomach.
The larval muscular layer (_m_) remains intact as long as the imaginal
mid-intestine is not fully developed, when it is attacked and destroyed
by phagocytes. The final muscular layer arises from single cells lying
on the outer surface of the imaginal buds (Figs. 633, _im_, 634, _m′_),
which should be regarded as special imaginal cells of the mid-intestinal
muscular layer.
The transformation of the fore-intestine is introduced by a degeneration
of the proventriculus and sucking stomach. The proventriculus (Fig. 635,
_pr_), which had been formed from a circular fold of the fore-intestine,
disappears by the smoothing out of this folded structure. The sucking
stomach also similarly degenerates by withdrawing gradually into the
œsophagus, so that instead of the original diverticulum there remains
only an enlargement of the œsophageal cavity. At the same time this part
of the canal is attacked and destroyed by phagocytes, while the
destroyed portions become replaced by the gradually extending imaginal
parts of the wall. The imaginal ring of the fore-intestine (Fig. 635,
_im_), which, according to Kowalevsky, is concerned in the formation of
a great part of the definitive œsophagus, becomes closed at its hinder
end so that the communication with the mid-intestine appears to be
interrupted.
The hind-intestine of the imago is rebuilt in exactly the same manner.
Here also the imaginal ring widens and forms a tube, which while it
grows around the openings into the urinary tubes, closes itself against
the mid-intestine, while behind it remains in connection with the larval
hind-intestine. In a similar way the larval hind-intestine is attacked
by the growth from behind of an imaginal ring, which proceeds from
imaginal buds near the anus, until finally, when the entire larval
hind-intestine is reduced to granule-balls, the two imaginal sections of
the tube are brought into contact with each other. (Kowalevsky in
Korschelt and Heider.)
The larval salivary glands (Fig. 633, _sp_) are completely destroyed
by phagocytes. Then succeeds the new formation of these glands from
imaginal buds, which, according to Kowalevsky, form rings situated
at their anterior ends.
The nature of the transformation undergone by the urinary tubes is
not yet well ascertained. According to Van Rees, there is in this
case perhaps a regeneration of the larval cells by division, but on
the other side there may be a histolysis of these elements.
The above-described method of transformation of the digestive canal
seems, according to Korschelt and Heider, to be very common among the
holometabolic insects. It has not only been observed in the Diptera, but
also in the Lepidoptera (Kowalevsky, Frenzel), Coleoptera (Ganin), and
Hymenoptera (Ganin). The stripping off of the epithelium of the
mid-intestine was found by Kowalevsky to occur also in Corethra, Culex,
and Chironomus.
=The tracheal system.=—As we have seen (p. 448), the tracheal system of
caterpillars just before pupation undergoes disintegration, accompanied
by a reformation of the peritoneal membrane and tænidia. The larval
ectotrachea undergoes histolysis, that of the imago being meanwhile
formed; the larval tænidia also break up, dissolve, and are replaced by
new tænidia which arise from the nuclei of the peritoneal membrane. That
the tracheal system in the Muscidæ during metamorphosis undergoes a
transformation is shown, as Korschelt and Heider claim, by the entirely
different shape of the system in the maggot, the pupa, and the fly. The
air is admitted to the tracheal system of the maggot, not by lateral
openings, but through the two stigmata at the end of the body. On the
other hand, the pupa breathes by prothoracic spiracles, while the fly
has six pairs of lateral stigmata of the normal structure. There may be
in the larva and pupa vestigial closed stigmata, as there are in the
thorax of caterpillars, with tracheal branches leading to where were
once functional stigmata. These stigmatal branches, as well as some
other portions of the tracheal system already observed by Weismann,
seem, according to Van Rees, to function as imaginal buds for the
regeneration of the tracheal matrix, while frequently also a
regeneration of this epithelium, by a simple repeated division of cells,
may be recognized. The disintegration of the tracheal system is
accomplished by means of phagocytes in the manner already described.
=The nervous system.=—The central nervous system passes directly from
the larval into the imaginal stage, since it must continue to exercise
most of its functions throughout metamorphosis, though it undergoes
important changes of form and position. At the same time, certain
histological transformations occur which may be regarded as a
histolysis. Such is the destruction and rebuilding in the interior of
the organs, which, however, preserve their continuity. Every case of
destruction of tissues in the pupa has come to be regarded as a
histolysis.
The problem of the transformation of the peripheral nervous system is
not yet well understood. Although during the destruction of the larval
muscles the motor nerves also in part degenerate, in the case of the
nerves distributed to the appendages the conditions are different, as
these may be recognized in the larva in the form of the nerve-threads
which place the imaginal buds in connection with the central nervous
system. These threads, according to Van Rees, pass from the larva into
the pupa and imago, so that with the farther development of the
rudiments of the extremities, only the distal part of the nerves
belonging to them are to be regarded as new formations. (Korschelt and
Heider.)
=The fat-body.=—The larval fat-body is also destroyed through the
activity of the leucocytes in the same way as the other tissues. The
reformation of the fat-body seems to begin in the mesoderm of the
imaginal buds. Possibly, also, the masses or collections of embryonic
cells which are regarded by Schaeffer as “blood-forming cells,” may
serve to regenerate the fat-body. At all events, they have been derived
from the mesodermal tissues. Though Wielowiejsky saw the fat-body of
Corethra arising from a cell-layer situated under the hypodermis, yet it
is not necessary to regard this observation as favorable to the view of
Schaeffer that in Musca the larval fat-body is derived in part from the
hypodermis, and in part from the tracheal matrix, thus from the
ectodermal tissues. (Korschelt and Heider.)
=Definitive fate of the leucocytes.=—We have seen that the formation of
the organs of the imago originates in the imaginal buds, in all cases
where these do not pass directly from the larva into the pupa. The
leucocytes, whose numbers in the pupa are greatly increased, take no
direct part in the formation of the tissues. Their importance seems to
lie in this, that they destroy those larval organs doomed to
destruction, the parts of which they take in and digest, and possibly,
by their powers of locomotion, convey particles of food to the
developing organs.
What, on the other hand, is the fate of the leucocytes after the
developmental processes in the pupa have ceased? There can be no doubt
that a part of the so-called granule-cells are again transformed into
normal blood-corpuscles. Another, and, as it seems, more considerable,
share suffer degeneration. Finally, the leucocytes themselves serve as
nourishment for the newly formed tissues. Of interest in this direction
is the observation of Van Rees, that numerous leucocytes finally pass
into the newly-formed hypodermis and then degenerate in crevices between
the hypodermis-cells. (Korschelt and Heider.)
It has been suggested by Van Rees that the phagocytes attack all the
larval organs indiscriminately, but that the active metabolism of
the imaginal buds preserves them from these attacks. He also thinks
that Kowalevsky is probably right in supposing that the buds render
themselves immune by some poisonous secretion.
Pratt, however, thinks that the supposition of a protecting or
poisonous secretion is scarcely necessary to account for the
phenomenon, and suggests that the larval tissues are a prey to the
phagocytes, because at the end of larval life they become
functionless and inactive, so as to become an easy prey to
phagocytes or disintegrating influences of any sort. On the other
hand, the imaginal buds “in which there is an exceedingly active
metabolism, and _all the larval organs which remain functional
during the metamorphosis_ are immune from the attacks of the
phagocytes. The heart in the muscids continues to beat, as Künckel
d’Herculais has observed, during the entire period of the
metamorphosis, with the exception of a day or two in the latter half
of it. The nervous system must continue functional during the entire
time. The three pairs of thoracic muscles which pass intact from the
larva to the imago are probably employed in respiration during the
metamorphosis. The reproductive glands are, like the imaginal disks,
rapidly growing organs.” He adds that among the other holometabolic
insects many or most of the larval organs remain functional during
metamorphosis, hence there is but little histolysis. “But the larval
intestine would always necessarily become unfunctional, and, as we
have seen, Kowalevsky is of the opinion that the larval mid-gut in
all holometabolic insects contains imaginal disks, and undergoes
degeneration during the metamorphosis.”
=The post-embryonic changes and imaginal buds in the Pupipara
(Melophagus).=—The sheep-tick (Melophagus) is still more modified than
the Muscidæ; the larva is apodous and acephalous, but, as Pratt
observes, much less highly specialized than those of muscids, and in
respect to the position of the thoracic buds it closely resembles
Corethra. They lie just beneath the hypodermis in two very regular rows,
and not in the centre of the body, as in Musca (Figs. 628, 636, _C_).
While, however, in Corethra all the thoracic buds are of larval origin,
arising after the last larval moult, in Melophagus, on the other hand,
each of these buds, except the dorsal prothoracic, arises in the embryo,
as is also the case in Musca.
In the cephalic buds the conditions are similar to those in Musca, but
still more complicated. Instead of a single pair of head-buds, there are
two pairs, one dorsal and one ventral. “The dorsal pair corresponds to
the muscidian head-disks in every respect; they are destined to form the
dorsal and lateral portions of the imaginal head, together with the
compound eyes. The ventral head-disks have no counterpart in Musca. The
fate of these disks or buds is to form the ventral portion of the head,
the paired projections forming the rudiments of the proboscis.
“The formation of the head-vesicle proceeds in a way similar to that in
Musca. The ventral disk fuses early at its lateral edges with the dorsal
pair. The communications between both ventral and dorsal disks and the
pharynx rapidly widen (in the old larva they have already become very
large), and soon the disks and pharynx form together a single vesicle,
which is the head-vesicle.” The imaginal buds of the abdomen Pratt finds
to be exactly as in the corresponding ones of Musca.
In the embryo of Melophagus the cephalic and thoracic imaginal buds
first appear as local thickenings, followed by the invagination of the
ectoderm; the cephalic buds first appear very early in the ontogeny of
the insect (Fig. 636, _C_), just as the germs of the digestive canal,
nervous system, and tracheæ are appearing. The single median thickening
(_v_) is destined to form the ventral cephalic bud, while the pair of
thickenings behind (_d_) become the dorsal buds, those homologous with
the cephalic buds of Musca.
[Illustration:
FIG. 636.—Imaginal buds in Musca,—_A_, in Corethra,—_B_, in
Melophagus,—_C_, in embryo of Melophagus: dorsal view of head; _b_,
bud; _p_, peripodal membrane; _c_, cord; _hy_, hypodermis; _cl_,
cuticula; _st_, stomodæum; _v_, ventral cephalic bud, behind are the
two dorsal cephalic buds (_d_).—After Pratt.
]
The thoracic buds, which arise as hypodermic thickenings, do not appear
until late in embryonic life, until the time of the involution of the
head.
Pratt did not observe in the embryo the buds of the internal organs and
of the abdominal hypodermis, and thinks it probable that they appear
first in the larva.
_c._ General summary
We have seen that in Coleoptera, Lepidoptera, Diptera, and Hymenoptera,
and with little doubt in all the holometabolous insects, the parts of
the imago originate in single formative cellular masses (imaginal buds)
already present in the larva, and often even in the later embryonic
stages. There are such imaginal buds for each part of the body,—for the
appendages of the head, for the legs and wings, for the ovipositor, and
probably for the cercopods, for the hypodermis of the abdomen, and for
the different sections of the digestive canal. We have seen, as
Korschelt and Heider state, that the formation of the mesodermal organs
of the imago (muscles, connective tissue, fat-body) begins in the
mesodermal part of the imaginal buds, whose first origin is still
obscure. Simultaneously with the formation of the imaginal organs, there
goes on under the influence of the leucocytes the destruction of the
larval organs. Both processes (destruction and regeneration) therefore
go on hand in hand, so that the continuity of the organs in question in
most cases remains perfect, inasmuch as the complete destruction only
ensues after the formation of the final organs. The only exceptions are
most of the muscles of the larva, which are destroyed at a very early
period.
Moreover, it is evident that the sharp division into larval, pupal, and
imaginal stages only applies to the external surface of the body, since
they follow one another after successive moults. The processes of the
internal development, on the other hand, form an entirely continuous
series of transformations between which is no sharp line of demarcation.
Yet as a whole the form of the larva, pupa, and imago are kept distinct
in adaptation to their separate environments and habits.
Finally, as Pratt very truly remarks, the epigenetic period in insects,
when new organs are forming, does not end with the birth of the larva
from the egg, but extends through the larval, and even through the pupal
period. “The principal significance of the pupal period and the
metamorphosis is that it is the time when the larval characters which
were adapted for use during a period of free life in the midst of the
development, and which would be valueless to the imago, are corrected or
abandoned.”
HYPERMETAMORPHISM
When an insect passes through more than the three normal stages of
metamorphosis, _i.e._ the larval, pupal, and imaginal, it is said to
undergo a _hypermetamorphosis_. The best-known examples are the
supernumerary stages of Meloë, Stylops, etc.
[Illustration:
FIG. 637.—Hypermetamorphosis of male of _Aspidiotus nerii_: 1, freshly
hatched larva; 2, larva shortly before pupating; _b_, rudiments of
the legs; _fl_, of the wings; 3, pupa before moulting; 4, the same
after moulting; 6, larva farther advanced than in 2; _a_, antennal
rudiments; _b_, rudiments of legs; _v_, stomach; _OG_, brain; _M.
Fl_, rudiments of the elevator and depressor muscles of the wing;
_M. Th_, rudiments of the dorsal muscles; _H_, rudiments of the
testes; 7, pupa shortly before entering upon the imago state (5);
_A_, eyes; _a_, antenna; _o_, mouth; _WD_, wax-glands; _BG_, ventral
nervous cord; _Sb_, caudal setæ; _tr_, tracheæ; _p_, genital
armature.—After Schmidt.
]
As has already been observed, Schmidt has shown that in the male of the
Coccidæ, there is a true hypermetamorphosis, as shown by Fig. 637. In
_Aspidiotus nerii_ there are five stages, there being two larval (1, 2)
and two pupal stages (3, 4, 7). Stage 3 (Fig. 637, 2) may be compared
with the pro-pupa stage of Riley (Fig. 581).
[Illustration:
FIG. 638.—_Mantispa interrupta_, and side view of the same without
wings: natural size.—Emerton _del._ _a_, freshly-hatched campodeoid
larva of _Mantispa styriaca_, enlarged; _b_, the same, but older,
before the first moult; enlarged.—Brauer.
]
We have already, on page 602, described the hypermetamorphosis of the
neuropterous insect Mantispa (Fig. 638).
[Illustration:
FIG. 639.—Triungulin (_a_) of a Californian Meloë: _b_, the three
triungulin claws; _c_, antenna; _d_, maxillary palpus; _e_, labial
palpus; _f_, mandible; _g_, an abdominal joint; _h_, imago, ♀; _i_,
antenna of ♂.—After Riley.
]
In Meloë the freshly hatched larva, or “triungulin” (Fig. 639, _a_), is
an active Campodea-like larva, which runs about and climbs up flowers,
from which it creeps upon the bodies of bees, such as Anthophora and
Andrena, who carry it to their cells, wherein their eggs are situated.
The triungulin feeds upon and destroys the eggs of its hostess.
Meanwhile its inactive life in the bee’s cell reacts upon the organism;
after moulting, the-second larval form (Fig. 640, _b_) is attained, and
now the body is thick, cylindrical, soft, and fleshy, and it resembles a
lamellicorn larva, with three pairs of rather long thoracic legs. This
is Riley’s carabidoid stage. This second larva feeds upon the honey
stored up for the young or larval bees. After another moult, there is
another entire change in the body; it is motionless, the head is
mask-like without movable appendages, and the feet are represented by
six tubercles. This is called the semipupa or pseudo-pupal stage. This
form moults, and changes to a third larval form (_c_), when apparently,
as the result of its rich, concentrated food, it is overgrown,
thick-bodied, without legs, and resembles a larval bee.
[Illustration:
FIG. 640.—Oil-beetle: _a_, first larva; _b_, second larva; _c_, third
larva; _d_, pupa.
]
[Illustration:
FIG. 641.—History of Sitaris: _a_, triungulin or 1st larva; _g_, anal
spinnerets and claspers of same; _b_, 2d larva; _e_, pseudo-pupa;
_f_, 3d larva; _c_, true pupa; _d_, imago, ♀.—After V. Mayet, from
Riley.
]
After thus passing through three larval stages, each remarkably
different in structure and in the manner of taking food, it transforms
into a pupa of the ordinary coleopterous shape (_d_).
The history of Sitaris, as worked out by Fabre and more recently by
Valery-Mayet, is a similar story of two strikingly different
adaptational larval forms succeeding the triungulin or primitive larval
stage. The first larva (Fig. 641, _a_) is in general like that of Meloë,
the second (_b_) is thick, oval, fleshy, soft-bodied, and with minute
legs, evidently of no use, the larva feeding on the honey stored by its
host. The pseudo-pupal stage is still more maggot-like than in the
corresponding stage of Meloë, and the third larva (_f_) is thick-bodied,
with short thoracic legs.
In the complicated life-history of another cantharid, _Epicauta
vittata_, as worked out by Riley (Fig. 642), we have the same
acquisition of new habits and forms after the first larval stage, which
evidently were at the outset the result of an adaptation to a change of
food and surroundings. The female Epicauta lays its eggs in the same
warm, sunny situation as that chosen by locusts (Caloptenus) for
depositing their eggs. On hatching, the active minute carnivorous
triungulin, ever on the search for eggs, on happening upon a locust egg
gnaws into it, and then sucks the contents. A second egg is attacked and
its contents exhausted, when, owing to its comparatively inactive habits
and rich nourishing food after a period of inactivity and rest, the skin
splits along its back, and at about the eighth day from beginning to
take food the second larva appears, with much smaller and shorter legs,
a much smaller head, and with reduced mouth-parts. This is the
carabidoid stage of Riley. After feeding for about a week in the egg a
second moult occurs, and the change of form is slight, though the
mouth-parts and legs are still more rudimentary, and the body assumes
“the clumsy aspect of the typical lamellicorn larva.” This Riley
denominates the scarabæidoid stage of the second larva.
[Illustration:
FIG. 642.—_Epicauta cinerea_: _a_, end of 2d larval stage; _b_,
portion of dorsal skin; _c_, _d_, coarctate larva; _e_, _f_,
pupa.—After Riley.
]
After six or seven days there is another transformation, the skin being
cast, and the insect passes into another stage, “the ultimate stage of
the second larva.” The larva, immersed in its rich nutritious food,
grows rapidly, and after about a week leaves the now addled and decaying
locust eggs, and burrows into the clear sand, where it lies on its side
in a smooth cell or cavity, and where it undergoes an incomplete
ecdysis, the skin not being completely shed, and assumes the semipupa
stage, or coarctate larval stage of Riley.
In the spring the partly loose skin is rent on the top of the head and
thorax, and then crawls out of it the “third larva,” which only differs
from the ultimate stage of the second larva “in the somewhat reduced
size and greater whiteness.” The insect in this stage is said to be
rather active, and burrows about in the ground, but food is not
essential, and in a few days it transforms into the true pupa state.
These habits and the corresponding hypermetamorphosis are probably
common to all the Meloidæ, though the life-history of the other species
has yet to be traced.
In the genus Hornia described by Riley, the wings of the imago are more
reduced than in any other of the family, both sexes having the elytra as
rudimentary as in the European female glow-worm (_Lampyris noctiluca_).
These, with the simple tarsal claws and the enlarged heavy abdomen, as
Riley remarks, “show it to be a degradational form.”
Its host is Anthophora, and the beetle itself lives permanently in the
sealed cells of the bee, and Riley thinks it is subterranean, seldom if
ever leaving the bee gallery. The triungulin is unknown, but the
ultimate stage of the second larva, as well as the coarctate larva, is
like those of the family in general, the final transformations taking
place within the two unrent skins, in this respect the insect (Fig. 643)
approaching Sitaris.
It appears, then, that as the result of its semi-parasitic mode of life
the Campodea-form or triungulin larva of these insects, which has
free-biting mouth-parts like the larvæ of Carabidæ and other carnivorous
beetles, instead of continuing to lead an active life and feeding on
other insects; living or dead, and then like other beetles directly
transforming into the normal pupa, moults as many as five times, there
being six distinct stages before the true pupa stage is entered upon. So
that there are in all eight stages including the imaginal or last stage.
One cannot avoid drawing the very obvious conclusion that the five extra
stages constituting this hypermetamorphosis, as it is so well styled,
are structural episodes, so to speak, due to the peculiar parasitic mode
of life, and were evidently in adaptation to the remarkable changes of
environment, so unlike those to which the members of other families of
Coleoptera, the Stylopidæ excepted, have been subjected. The fat
overgrown body and the atrophied limbs and mouth-parts are with little
doubt due to the abundant supply of rich food, the protoplasm of the egg
of its host, in which the insect during the feeding time of its life is
immersed. Since it is well known that parthenogenesis is due to over, or
at least to abundant nutrition, or to a generous diet and favoring
temperature, there is little reason to doubt that the greatly altered
and abnormally fat or bloated body of the insect in these supernumerary
stages is the result of a continuous supply of rich pabulum, which the
insect can imbibe with little or no effort.
[Illustration:
FIG. 643.—1, Egg-pod of _Caloptenus differentialis_ with the mouth
torn open, exposing the newly hatched larva of _Epicauta vittata_ (1
_a_) eating into an egg and the passage which it made through the
mucous covering; natural size. 2, dorsal view of the 1st larva, or
triungulin, of _E. vittata_; 2 _a_, one side of the head of same
from beneath, greatly enlarged so as to show the mouth-parts; 2 _b_,
terminal joint of maxillary palpus, showing imbrications and
flattened inner surface armed with stout points; 2 _c_, leg, showing
more plainly the tarsal spines; 2 _e_, labrum; 2 _d_, one of the
abdominal joints from above, showing stout points, stigmata, and
arrangement of spinous hairs. 3, eggs of _E. vittata_, the natural
size indicated at side. 4, dorsal view of the carabidoid stage of
the 2d larva of _E. vittata_: 4 _a_, its antenna; 4 _b_, its right
maxilla; 4 _c_, its leg; 4 _d_, side view of same, showing its
natural position within the locust-egg mass. 5, lateral view of the
ultimate or full-grown stage of the 2d larva of _E. vittata_; 5 _a_,
portion of the dorsal skin, showing short setaceous hairs. 6, third
head, or that from the scarabæidoid stage of the 2d larva of _E.
vittata_ from beneath, showing the reduction of mouth-parts as
compared with the first head (2 _a_); 6 _a_, antenna of same; 6 _b_,
maxilla of same; 6 _c_, mandible of same. 7, fourth head, or that of
the full-grown larva of _E. vittata_, from above; 7 _a_, leg of
same; 7 _b_, the breastplate or prosternal corneous piece. 8,
lateral view of the pseudo-pupa or coarctate larva of _E. vittata_,
with the partially shed skin adhering behind: 8 _a_, dorsal view of
same; 8 _b_, its head, from the front; 8 _c_, same from side; 8 _d_,
tuberculous leg; 8 _e_, raised spiracle; 8 _f_, anal part of same,
9. lateral view of the true pupa of _Epicauta cinerea_ Forst: 9 _a_,
ventral view of same. 10, _Epicauta vittata_ (lemniscata or
trivittate var.). 11, _Epicauta cinerea_ Forst. (= _marginata_
Fabr.). 12, antenna of the triungulin of _Epicauta pennsylvanica_:
12 _a_, maxilla of same; 12 _b_, labial palpus of same. 13. ♂
_Hornia minutipennis_, dorsal view; 13 _a_, lateral view of same; 13
_b_, simple claw of same; 13 _c_, coarctate larva; 13 _d_, leg of
ultimate stage of 2d larva.—After Riley.
]
[Illustration:
FIG. 644.—Triungulin stage of _Stylops childreni_.
]
The life-history of the Stylopidæ is after the same general fashion,
though we do not as yet know many of the most important details. The
females are viviparous, the young hatching within the body of the
parent, as we once found as many as 300 of the very minute triungulin
larvæ issuing in every direction from the body of what we have regarded
as the female of _Stylops childreni_ in a stylopized Andrena caught in
the last of April. The larvæ differ notably from those of the Meloidæ in
the feet being bulbous and without claws, yet it is in general
Campodea-like and in essential features a triungulin (Fig. 644). The
intestine ends in a blind sac, as in the larvæ of bees, and this would
indicate that its food is honey. The complete life-history of no
Stylopid is completely known. It is probable that, hatched in June from
eggs fertilized in April, the larvæ crawl upon the bodies of bees and
wasps; finally, after a series of larval stages as yet unknown,[119]
penetrating within the abdomen of its host before the latter hibernates,
and living there through the winter. The females, owing to their
parasitic life, retain the larval form, while the free males are winged,
not leading in the adult stage a parasitic life, though passing their
larval and pupal stages in the body of their host, and are so unlike
ordinary beetles as to be referred by good authorities to a distinct
order (Strepsiptera).
[Illustration:
FIG. 645.—_Stylops childreni_, ♂: _a_, abdomen of Andrena with ♀
Stylops (_b_).
]
The triungulin stage of these insects corresponds in general to the form
of the larval Staphylinidæ and allied families, such as the
Tenebrionidæ, which are active in their habits, running about and
obtaining their food in a haphazard way, often necessarily suffering
long fasts. In the external-feeding, less active coleopterous larvæ,
like the phytophagous species, which have an uninterrupted supply of
nutritious food, we see that the body is thick and fleshy. So also in
the larvæ of the Scarabæidæ, Ptinidæ, and the wood-boring groups. In
internal feeders, like the larval weevils and Scolytidæ, which live
nearly motionless in seeds, fruits, and the sap-wood of plants and
trees, with a constant supply of nourishing, often rich food, the
eruciform body is soft, thick, and more or less oval-cylindrical. So it
is with the larvæ of Hymenoptera, especially in the parasitic forms, and
in the ants, wasps, and bees, which are nearly if not quite motionless,
at least not walking about after their food.
Now the change from the active triungulin stage to the series of
secondary, nearly legless, sedentary, inactive stages is plainly enough
due to the change of station and to the change of food. From being an
independent, active, roving triungulin, the young insect becomes a
lodger or boarder, fed at the expense of its host, and the lack of
bodily exertion, coupled with the presence of more liquid food than is
actually needed for its bare existence, at once induces rotundity of
body and a loss of power in the limbs, followed by their partial or
total atrophy.
That this process of degeneration may even occur in one and the same
stage of larval existence is very well illustrated by what we know of
the life-history of the wasp-parasite of Europe, _Rhipiphorus
paradoxus_. Thanks to the very careful and patient observations of Dr.
T. A. Chapman, we have a nearly complete life-history of this beetle,
the representative of a family in many respects connecting the Meloidæ
and Stylopidæ.[120] Where Rhipiphorus lays her eggs is unknown. Dr.
Chapman, however, found a solitary specimen of the young larva in the
triungulin stage. He describes it as “a little black hexapod, about 1⁄50
inch (.5 mm.) in length, and 1⁄120 inch in breadth, broadest about the
fourth segment, and tapering to a point at the tail; a triangular head
with a pair of three-jointed antennæ nearly as long as the width of the
head, with legs very like those of Meloë larvæ; the tibiæ ending in two
or three claws, which are supported and even obscured by a large
transparent pulvillus or sucker of about twice their length; this was
marked by faint striæ radiating from the extremity of the tibiæ, giving
it much the aspect of a lobe of a fly’s proboscis. Each abdominal
segment had a very short lateral spine pointing backwards; the last
segment terminated by a large double sucker similar to those of the
legs; and the little animal frequently stood up on this, and pawed the
air with its feet, as if in search of some fresh object to lay hold of.”
This almost microscopic larva finds a wasp grub and bores into its body,
probably entering at a point near the back of the first or second
segment behind the head. Dr. Chapman succeeded in finding the larva of
the beetle within that of the wasp, before the latter had spun up.
“Assuming that the wasp larva lives six days in its last skin before
spinning up, I should guess that the youngest of these had still two or
three days’ feeding to do. The Rhipiphorus larvæ were but a little way
beneath the skin of the back, about the fourth and fifth segments
[counting the head as the first], and indifferently on either side. The
smallest of these was 1⁄16 inch in length, and, except its smaller size,
was precisely like the larger ones I am about to refer to, having the
same head, legs, plates, etc. These were of the same size as those of
the larger larvæ, the difference in size of the latter being due to the
expansion of the intermediate colorless integument.”
After the wasp grub has spun the silken covering of its cell the larva
of Rhipiphorus may still be detected in some of them, being rendered
visible by its black legs and dark dorsal and ventral plates. “On
extracting this larva, it bears a general resemblance in size and
outline to the youngest larva of Rhipiphorus that I had found feeding
externally on the wasp grub, but with the very notable exception of the
already mentioned black marks. These are, in fact, a corneous head,
six-jointed legs, and a dorsal and ventral series of plates. I
immediately recognized the head and legs as identical with those of the
little black mite already described, but presenting a ludicrous
appearance in being widely separated from each other by the white skin
of the larva. I have no doubt that the dorsal and ventral series of
black marks are the corresponding plates of the mite-like larva floated
away from each other by the expansion of the intervening membrane. By
measurement also they agree exactly in size, although the larva
extracted from the wasp grub is ten times the length and six times the
width of the little Meloë-like larva. In length it is ⅙ inch (4.5 mm.),
and 1⁄28 inch in breadth.”
The remarkable changes thus described in the larva of this beetle after
it has begun its parasitic life within the body of its host are
especially noteworthy because the great increase in size and difference
in shape, as well as in habits, all take place before the insect has
moulted. The rapid development in size, and consequent distension of the
body and the separation of the sclerites of the segments behind the
head, are paralleled, as Chapman says, by the greatly swollen abdominal
region of the body in _Sarcopsylla penetrans_ and in the female of the
Termitidæ. In those insects this distension is due to the enlargement of
the ovaries and of the eggs contained within them, but in the
Rhipiphorus it is due to the comparative inactivity of the larva, and to
its being gorged with an unending supply of rich food, the blood and fat
of its host. It follows, then, that if a sedentary life and over, or at
least abundant, nutrition will have this effect within the short period
covered by the single first larval stage of the Rhipiphorus, it is
reasonable to infer that the hypermetamorphosis is also due to the same
factors.
Chapman then goes on to say that finally, within six hours of the time
of spinning up of the wasp grub, the Rhipiphorus larva at the end of
Stage 1., which is “usually in motion, and for its situation might be
called tolerably active, is seen to lay hold of the interior of the skin
with its anterior legs, and keeps biting and scratching with its strong
and sharp jaws until it is able to thrust through its head, when, in
less than a quarter of an hour, it completely emerges by a vermiform
movement; and at the same time it casts a skin, together with the black
head, legs, plates, etc.”
The larva, now in its second stage, passes forward and seizes hold of
the upper or lateral aspect of the prothoracic segment of the wasp grub.
On emerging it becomes shorter and thicker, “and very soon loses length
by that curving forward of its head which is so marked in the full-grown
larva, and which does not exist before its emergence.” The larva is now
found “lying like a collar immediately under the head of the wasp grub,
and is attached to it by the head, though not very firmly.” At this
stage the feeding of the young Rhipiphorus is rather sucking than
eating.
[Illustration:
FIG. 646.—First larva (_a_) of _Bruchus fabæ_, greatly enlarged; _b_,
thoracic processes; _c_, head, from front; _d_, from side; _e_,
antenna; _f_, thoracic leg; _g_, rear view of tarsus; _h_, same,
front view.—After Riley.
]
When about 6 mm. in length it moults a second time, and the full-grown
larva closely though superficially resembles a Crabro or Pemphredon
larva, the small head being bent over forwards. By the time it is ready
to pupate it has wholly eaten the wasp larva, and the temperature of the
cell being high, a larva 5 mm. long grows large enough in two days to
fill the top of the cell of its host, and the larva is ready to pupate
about a week after hatching, so that its development is very rapid. The
beetles themselves do not live in the cells. Chapman thinks they
hibernate, and that the eggs are laid in the spring or summer.
We thus have in this insect three larval stages, the triungulin, and two
later stages, the great differences between the first and the last two
being apparently due to their parasitic mode of life, the larva spending
its second stage within its host, involving an existence in a cell with
a high temperature, an uninterrupted supply of rich, stimulating food,
and a comparatively sedentary mode of life compared with that of the
triungulin at the beginning of its existence. It is quite obvious that
the hypermetamorphosis is primarily due to a great change in its
surroundings, _i.e._ the parasitic mode of life of the beetle, habits of
very rare occurrence in the Coleoptera, numerous in species as they are.
[Illustration:
FIG. 647.—First larval stage of _Bruchus pisi_: _a_, egg in pea-pod;
_b_, cross-section of opening of mine; _c_, young larva and opening
on inside of pod by which it has entered, enlarged; _d_, _d_, _d_,
eggs, natural size; _e_, 1st larval stage; _f_, a leg of same; _g_,
prothoracic spinous processes.—After Riley.
]
In this connection attention may be drawn to a supernumerary larval
stage observed by Riley in the pea- and bean-weevils (Figs. 646 and
647). The larva on hatching has long slender legs, though differing from
those of an ordinary coleopterous larva in having but three joints (_j_,
_g_, _h_). This stage is very short, and the legs temporary, as, after
entering the bean or pea, it casts its skin, losing its legs, and
assuming the vermiform shape of the second larval stage. In this case
the change from a pedate to an apodous larva is plainly enough due to
the change from an external feeder, like a chrysomelid larva, to a larva
leading a boring, internal, almost quiescent life.
Certain ichneumons also appear to have two distinct larval stages, as
Ratzeburg inferred that in Anomalon there are four larval stages (Fig.
648).
[Illustration:
FIG. 648.—History of _Anomalon circumflexum_: _A_, 1st instar or
stage. _B_, 2d instar. _C_, larva in the 3d or encysted stage
removed from its cyst. _D_, mature larva. _E_, pupa.—After
Ratzeburg, from Sharp.
]
In another ichneumon, Klapálek detected what he calls the “sub-nymph.”
The insect pupates within the case of a caddis-fly, Silo (Fig. 649).
In the Proctotrypidæ there is also a hypermetamorphosis, though the
remarkable precocious stages they pass through are rather embryonic than
larval.
In a species of Platygaster which is parasitic in the larva of
Cecidomia, the first larva (Cyclops stage) is of a remarkable shape, not
like an insect, but rudely resembling a parasitic Copepod crustacean. In
this condition it clings to the inside of its host by means of its
hook-like jaws, moving about, as Ganin says, like a Cestodes embryo with
its well-known six hooks. In this stage it has no nervous, vascular, or
respiratory system, and the digestive canal is a blind one (Fig. 651).
[Illustration:
FIG. 649.—Metamorphosis of Agriotypus: _A_, larva. _B_, “sub-nymph.”
_C_, case of the Silo, with the string of attachment formed by
Agriotypus. _D_, section of the case: _v^1_, operculum of case;
_v^2_, cocoon; _ag_, pupa of Agriotypus; _e_, exuvia of same; _w^2_,
wall of cocoon; _s_, remains of Silo; _w^1_, closure of case.—After
Klapálek, from Sharp.
]
After moulting, the insect entirely changes its form; it is thick
oval-cylindrical, nearly motionless, with no appendages, but with a
digestive canal and a nervous and vascular system (Fig. 652).
After a second moult the third and last larval stage is attained, and
the insect is of the ordinary appearance of ichneumon larvæ.
Not less striking is the life-history of Polynema, which lays its eggs
in those of a small dragon-fly (_Agrion virgo_). The first larval stage
is most remarkable. It hatches as a microscopic immovable being,
entirely unlike any insect, with scarcely a trace of organization, being
merely a flask-shaped sac of cells. After remaining in this state five
or six days it moults.
[Illustration:
FIG. 650.—Development of Platygaster: _A_, stalked egg: _a_ central
cell giving origin to the embryo. _B_, _g_, germ; _b_, blastoderm
cells. _C_, the same, farther advanced. _D_, cyclops-like embryo:
_md_, rudiments of mandibles; _d_, rudimentary pad-like organs, seen
more developed in _E_; _st_, bilobed tail.
]
The second stage, or Histriobdella-like form, as Ganin names it, is more
like that leech-like worm than an insect.
The third larval form is very bizarre, though more as in insects, having
rudimentary antennæ, mouth-parts, legs, and ovipositor. In this
condition it lives from six to seven days before pupating (Fig. 653).
The strange history of another egg-parasite (Ophioneurus) agrees in some
respects with that of the foregoing forms. It is when hatched of an oval
shape, with scarcely any organs, and differs from the genera already
mentioned in remaining within its egg-membrane, and not assuming their
strange shapes. From the cylindrical sac-like non-segmented larva
resembling the second larva of Platygaster it passes directly into the
pupa state.
A fourth form, Teleas (Fig. 654, _A-D_), is an egg-parasite of Gerris,
and in America one species oviposits in the eggs of Œcanthus.
[Illustration:
FIG. 651.—First larva of Platygaster: _m_, mouth; _at_, rudimentary
antenna; _md_, mandibles; _d_, tongue-like appendages.
]
[Illustration:
FIG. 652.—Second larva of Platygaster: _œ_, œsophagus; _ng_, brain;
_n_, nervous cord; _ga_ and _g_, genital organs; _ms_, muscular
band.
]
The spindle-shaped larva in its first stage roughly resembles a
trochosphere of a worm rather than the larva of an insect so high in the
scale as a Hymenopter. It is active, but after moulting the second larva
is oval, still without segments. Dr. Ayers gives a profusion of details
and figures of the first and second stages of our Teleas, the second
strongly resembling the Cyclops stage of Ganin. He describes three
stages, and though he did not complete the life-history of the insect,
he thinks it changes to an ovoid flattened form which succeeds the
Cyclops stage in other Pteromalidæ, and that there are at least four
ecdyses.
It is difficult to account for these strange larval forms, unless we
suppose that the embryos, by their rich, abundant food, have undergone a
premature development, the growth of the body-walls being greatly
accelerated, the insects so to speak having been, under the stimulus of
over-nutrition and their unusual environment, and perhaps also the high
temperature of the egg, hurried into vermian existence on a plane
scarcely higher than that of an active ciliated gastrula.
Further observations, difficult though they will be, are needed to
enable us to account for the singular prematurity of the embryo of these
parasites. That these stages are reversional and a direct inheritance
from the vermian ancestors of these insects is not probable, but the
forms are evidently the result of adaptation in response to a series of
stimuli whose nature is in part appreciable but mostly unknown.
[Illustration:
FIG. 653.—Third larva of Polynema: _at_, antenna; _fl_, imaginal bud
of wing; _l_, rudimentary legs; _tg_, buds of one of the three pairs
of styles of the ovipositor; _fk_, fat-body; _eg_, ear-like process.
]
[Illustration:
FIG. 654.—_A-D_, development of Teleas; _A_, stalked egg; _B_, _C_,
_D_, the 1st larval stage: _at_, antenna; _md_, hook-like mandibles;
_mo_, mouth; _b_, bristles; _m_, intestine; _sw_, the tail; _ul_,
under lip or labium. _E_, larva of another parasite,
Ophioneurus.—This and Figs. 650–653 after Ganin.
]
It may be noted, however, that the appearance of a primitive band in the
second larval stage suggests the origin of these forms, as well as that
of insects in general, from a Peripatus-like, and again from an earlier
leech-like Annelid ancestor. Hence the first larval or Cyclops stage is
due to a precocious development caused by the unusual environment, and
is simply adaptational, and not of phylogenetic significance.
SUMMARY OF THE FACTS AND SUGGESTIONS AS TO THE CAUSES OF METAMORPHISM
An explanation of the causes of metamorphosis is one of the most
difficult undertakings in biology, and the phenomenon has been
considered as one of the chief difficulties in the way of the acceptance
of the theory of descent.
A review, however, of the facts of hypermetamorphism, particularly the
life-history of Mantispa, throws much light on the subject, since it is
very probable that the supernumerary stages and marked changes of form
characterizing them are due to changes of environment, of habits, and of
food, causes which have exerted such a profound influence on organic
beings throughout all time. Besides these, as the result of changes in
the environment and nature of the food, we have the results brought
about by the use or disuse of structures brought into existence by the
action of stimuli from without, the class of insects abounding in
examples of temporary structures which perform a certain function, and
then disappear.
Again, if the origin of a hypermetamorphosis can thus be explained, it
follows that normal metamorphosis is most probably due to changes of
habitat, of seasons, of food, and to accelerated growth resulting from
the approach of sexual maturity.
The following facts and conclusions appear to be well established:—
1. The apterous insects (Synaptera) are ametabolous, only the winged
insects undergoing a metamorphosis.
2. The complete metamorphosis was not inherited from the primitive
ancestor of all insects, but acquired at a later period (F. Müller). The
eruciform type is a secondary, adaptive form, derived from the earlier,
campodeoid type of larva.
3. The earliest, most primitive pterygote insects passed through only a
slight metamorphosis. In other words, as soon as the wings were evolved
and insects became adapted to live or take refuge in a new medium, the
air, at the approach of the period of adult life, with the ripening or
perfection of the reproductive organs, a metamorphosis began to take
place, and the number of species greatly multiplied. On the other hand,
the Arachnida and Myriopoda, in which as a rule there is no
metamorphosis, being confined to a creeping life, with no change of
medium, remained poor in number of species.
4. At first the nymphs mainly differed from the adults in lacking wings,
though having the same habits; in holometabolous insects, the larva
became adapted to entirely different habits and environments, so that in
Hymenoptera, and especially Diptera, the larva became remarkably unlike
the imago.
5. Until the Mesozoic age, or late in the Carboniferous period, there
were, so far as we now know, only ametabolous and heterometabolous
insects, and these orders (Orthoptera, Dermaptera, Hemiptera,
Plectoptera, Odonata, and Neuroptera) were not numerically rich in
genera and species, while since early Mesozoic times geological
extinction has reduced their numbers.
6. During the Mesozoic age, and since then, the number of species,
genera, families, and orders has greatly increased, and insects have
become more and more holometabolous. The orders of Coleoptera,
Lepidoptera, Hymenoptera, and Diptera are many fold greater in number of
species and variety of form than the heterometabolous orders.
The rapid increase in the number and variety of types of insects
evidently is correlated with the profound geological changes which took
place at the end of the Paleozoic age, involving the appearance of
larger continental masses, or a greater land area, thus opening new
regions for settlement. Also the origin of flowering plants at about
this time undoubtedly had much to do with the genesis of new adaptive
structures, such as the changes in the mouth-parts and wings.
7. The process of metamorphosis, at least in the subtropical, temperate,
and polar regions, is largely dependent on the change from summer to
winter, and, in the tropics, from the rainy to the dry season.
As regards the organization of larval (nepionic) as compared with
imaginal forms, the nymphs and larvæ of insects are, with the exception
of many Diptera, nearly as perfectly developed as the adult. In this
respect the immature insect differs fundamentally from the larvæ of
certain worms (for example, the pilidium of Nemerteans) and from the
pluteus and brachiolaria stages of echinoderms, which possess only
digestive and water-vascular organs.
Insect nymphs and larvæ also differ from the nauplius and zoëa of
Crustacea in having at birth all the most important systems of organs
(digestive, circulatory, respiratory, nervous, muscular, with sometimes
a nearly perfected reproductive system) of the imago, also the same
number of cephalic, thoracic, and abdominal segments and appendages.
Metamorphism in insects involves (except in the Diptera) rather
modifications in the form and functions of organs and appendages already
present than the formation of new ones. In larval Crustacea, the
thoracic and abdominal appendages do not arise until some time after
hatching from the egg.
8. While cases of the suppression or abbreviation of larval characters
and direct development are not uncommon in echinoderms and crustaceans,
in insects this phenomenon occurs only so far as yet known in the
Diptera. In these insects the polypody in the embryo is outgrown, or
lost, the embryos and larvæ not having even the temporary rudiments of
abdominal appendages. The campodeoid characters also are entirely
suppressed, dropped, or lost in the more specialized holometabolous
orders, Lepidoptera, Hymenoptera, and Diptera, though retained in the
more primitive and generalized Coleoptera. (This proves that the
Coleoptera are lower or more primitive and generalized than the other
orders mentioned.) This abbreviation or loss of organs is, as Hyatt and
Arms claim, due to the prepotency of acquired characters in phylogeny,
and are also the result of homochronous heredity.
“The Insecta of the more specialized orders, x.-xvi., afford, next
to some parasites, the most notable examples of this mode of
evolution. Their larval or nepionic, and pupal or neanic, stages are
prolonged at the expense of the ephebic, winged stage, and the
reasons for this prolongation are found in the great number of new
features introduced into these stages of development in these orders
as contrasted with those of the more primitive, and, in large part,
more ancient orders, i.-ix. The law of tachygenesis has been at work
here, as in the former cases alluded to above, and it is shown in
the encroachments of the adaptive characteristics of the
caterpillar, grub, and maggot upon the inherited characteristics of
the Thysanuran stage, which loses its ancestral characteristics,
until in most cases they are either obsolete or recognizable with
difficulty.” (Hyatt and Arms, Natural Science, 1896, p. 400.)
9. In the holometabolous insects there is a resting, quiescent stage
during the pupal period, when the insect takes no food. In this respect
the more specialized insects differ from other metamorphic animals. The
larva has an abundant supply of fat lasting through pupal life, while in
the quiescent pupa, respiration and circulation is much lessened, the
animal being as a rule motionless. This resting stage is also necessary
for the histolysis and formation of the adult body from the imaginal
buds present in the larva.
10. The hypermetamorphosis of Mantispa, Meloë, Stylops, etc., indicate
very plainly that the eruciform type of larva is derived from the
campodeoid, since one and the same insect passes through these stages
before reaching sexual maturity.
11. As observed by Miall, the larva of insects differs from that of
other invertebrate animals in being larger than the adult.
12. The metamorphoses of insects are in some important respects
paralleled by those of the Amphibia. The case of pædogenesis of
Chironomus affords a parallel with that of the Siredon, or larva of
Amblystoma. Also the organs and appendages of the insects, such as
caterpillars, are present, just as the skeleton and other organs of the
tadpole are the homologues of those of the adult, although these parts
undergo a profound modification, and new structures are added. (See the
discussion of this point by Miall, and by Hyatt and Arms.)
=Theoretical conclusions; Causes of metamorphosis.=—It results from a
review of the known facts, together with reasonable inductions from such
facts, that so far from opposing the theory of descent, the facts of
metamorphosis, and particularly of hypermetamorphosis, seem to afford
solid foundation for the theory. While natural selection was not the
initiative cause, it plays a part as one of several factors; but the
fundamental causes are the same as those which have controlled the
origin of species and of the larger groups of animals in general. Owing
to the struggle for existence, due to overcrowding, the early insects
were forced to take to the air, acquiring wings to enable them to avoid
the attacks of creeping and running insects. In the end the insects
became, owing to this acquisition of wings, and afterwards to the
establishment of a complicated metamorphosis, numerically the most
successful type of life in existence, the number of species, extinct and
living, mounting into the millions.
All aquatic insects are evidently the descendants of terrestrial forms,
and the numberless contrivances and temporary larval organs,
particularly of dipterous larvæ, are evidently adaptations to the needs
of the insect during its aquatic life, and which are cast aside when the
creature passes to a different medium. The sudden or tachygenic
appearance of temporary structures, such as hatching spines, various
setæ, spines, respiratory organs, so characteristic of dipterous larvæ,
and of the protective colors and markings of caterpillars, and which are
discarded at pupation, or imagination, are evidently due to the action
of stimuli from without, to the primary neolamarckian factors, the
characters proper to each larval stadium, and to the pupal and imaginal
stadia,—characters probably acquired during the lifetime of the
individual,—becoming finally fixed by homochronous heredity.
LITERATURE ON POSTEMBRYONIC DEVELOPMENT AND METAMORPHOSES
=Herold, Moritz Johann David.= Entwicklungsgeschichte der
Schmetterlinge anatomisch und physiologisch bearbeitet. (Cassel, u.
Marburg, 1815. 33 Taf., 4º, pp. 1–118, i-xxxiv.)
=Ratzeburg, F. T. C.= Ueber Entwickelung des fusslosen
Hymenopteren-larven, mit besonderer Rücksigt auf die Gattung
Formica. (Nova Acta Natur. Curios., xvi, 1832, pp. 145–176.)
=Agassiz, Louis.= The classification of insects from embryological
data. (Smithsonian Contr., ii, Washington, 1851, pp. 28, 1 Pl.)
=Ganin, M.= Beiträge zur Erkenntniss der Entwicklungsgeschichte bei
den Insecten. (Zeitschr. f. wiss. Zool., xix, 1869, pp. 381–451, 4
Taf.)
—— Ueber die Embryonalhülle der Hymenopteren- und
Lepidopteren-embryonen. (Mém. Acad. St. Petersbourg (7), xiv, 1869,
pp. 18, 1 Pl.)
—— Materialien zur Kenntniss der post-embryonalen
Entwicklungsgeschichte der Insecten. (Russian.) Warschau, 1876.
(Abdruck aus den Arbeiten der V. Versammlung russischer Naturf. und
Aerzte in Warschau, 1876. Abstract by Hoyer in Jahresber. der Anat.
und Phys. von Hoffmann und Schwalbe, v, 1876, and in Zeitschr. f.
wiss. Zool., xxviii, 1877, pp. 386–389.)
=Weismann, A.= Die nachembryonale Entwicklung der Musciden nach
Beobachtungen an _Musca vomitoria_ und _Sarcophaga carnaria_.
(Zeitschr. f. wiss. Zool., xiv, 1864, pp. 101–263, Taf. 8–14.)
—— Die Metamorphose von _Corethra plumicornis_. (Zeitschr. f. wiss.
Zool., xvi, 1866, pp. 1–83, 5 Taf.)
=Packard, A. S.= Observations on the development and position of the
Hymenoptera, with notes on the morphology of insects. (Proceedings
Boston Society of Natural History, 1866, pp. 279–295.)
=Künckel d’Herculais=, J. Recherches sur l’organisation et le
développement des Volucelles. Paris, 1875, Pt. I, pp. 208, 12 Pis.;
II, 1881. Atlas of 15 Pls.
=Dewitz, H.= Beiträge zur Kenntniss der post-embryonalen
Gliedmaassenbildung bei den Insecten. (Zeitschr. f. wiss. Zool.,
xxx, Suppl., 1878, pp. 78–105, 1 Taf.; Nachtrag, Ibid., pp. 25–28.)
—— Ueber die Flügelbildung bei Phryganiden und Lepidopteren. (Berl.
Ent. Zeitschr., xxv, 1881, pp. 53–66, 2 Taf.)
=Lowne, B. Th.= Anatomy, physiology, morphology, and development of
the blow-fly. London, Part I, 1880; Part II, 1891.
=Viallanes, H.= Recherches sur l’histologie des Insectes et sur les
phénomènes histologiques qui accompagnent le développement
post-embryonnaire de ces animaux. (Ann. Sc. Nat. (6), xiv, 1882.)
=Metschnikoff, E.= Untersuchungen über intracelluläre Verdauung bei
wirbellosen Thieren. (Arb. a. d. zoolog. Inst. zu Wien., v, 1883.)
—— Untersuchungen über die mesodermalen Phagocyten einiger
Wirbelthiere. (Biol. Centralbl., iii, 1883.)
=Wielowiejsky, H. v.= Ueber den Fettkörper von _Corethra plumicornis_
und seine Entwicklung. (Zool. Anzeiger, vi Jahrg., 1883, pp.
318–322.)
=Pancritius, P.= Beiträge zur Kenntnis der Flügelentwicklung bei den
Insecten. In.-Diss. Königsberg, 1884.
=Rees, J. van.= Over intra-cellulaire spijsverteering en over de
beteekenis der witte bloedlichampjes. (Maandblad voor
Natuurwetenschappen, xi Jaarg., 1884, pp. 28.)
—— Over de post-embryonale ontwikkeling von _Musca vomitoria_.
(Maandblad voor Natuurwetenschappen, Juli, 1885.)
—— Beiträge zur Kenntniss der inneren Metamorphose von _Musca
vomitoria_. (Zool. Jahrb. Abth. f. Anat. u. Ontog., iii, 1888, pp.
1–134, 2 Taf., 14 Figs.)
=Frenzel, J.= Einiges über den Mitteldarm der Insecten, sowie über
Epithel-regeneration. (Arch. Micr. Anat., xxvi, 1885.)
=Kowalevsky, A.= Beiträge zur nachembryonalen Entwicklung der
Musciden. (Zool. Anzeiger, viii, 1885, pp. 98, 123, 153.)
—— Beiträge zur Kenntniss der nachembryonalen Entwicklung der
Musciden. (I. Theil., Zeitschr. f. wiss. Zool., xlv, 1887, pp.
542–594, 5 Taf.)
=Schneider, Ant.= Ueber die Anlage der Geschlechtsorgane und die
Metamorphose des Herzens bei den Insecten. (Zool. Beiträge, 1885, i,
pp. 140–143, 1 Taf.)
=Rehberg, A.= Ueber die Entwickelung des Insectenflügels (an _Blatta
germanica_). (Marienwerder, 1886, pp. 12, 1 Taf.)
=Schäeffer, C.= Beiträge zur Histologie der Insecten. (Spengel’s Zool.
Jahrb., iii, Abth. f. Anat., 1889, pp. 611–652, 2 Taf.)
=Hurst, H.= The post-embryonic development of a gnat (Culex).
Manchester, 1890, pp. 26, 1 Pl.
=Verson, E.= Der Schmetterlingsflügel und die sog. Imaginalscheiben
desselben. (Zool. Anzeiger, xiii, 1890, pp. 116, 117.)
=Bugnion, Edouard.= Recherches sur le développement post-embryonnaire,
l’anatomie, et les mœurs de l’_Encyrtus fuscicollis_. (Recueil zool.
Suisse, v, 1891, pp. 435–534, 6 Pls.)
=Petersen, Wilhelm.= Die Entwicklung des Schmetterlings nach dem
Verlassen der Puppenhülle. (Deutsch. Ent. Zeitschr., 1891, 2 lepid.
Hft., pp. 199–214, 5 Figs.)
=Kulagin, Nicolas.= Notice pour servir à l’histoire de développement
des hyménoptères parasites. (Congrès international de Zoologie, 2^e
Session, à Moscou, 1892, pp. 253–277. Also in Zool. Anzeiger, xv,
1892, pp. 85–87.)
—— On the development of Platygaster. (Journ. of Friends of Nat. Sc.
Moscow. Zool., 1890.) (In Russian.)
—— Beiträge zur Kenntniss der Entwicklungsgeschichte von Platygaster.
(Zeitschr. f. wiss. Zool., lxiii, 1897, pp. 195–235, 2 Taf.)
=Miall, L. C., and Hammond, A. R.= The development of the head of
Chironomus. (Trans. Linn. Soc. London, 2d Ser., v, 1892, pp.
265–279, 4 Pls.)
=Pratt, Henry S.= Beiträge zur Kenntniss der Pupiparen. In.-Diss.
Berlin, 1893, pp. 53 (Archiv f. Naturgesch., 1893), 1 Taf.
—— Imaginal discs in insects. (Psyche, viii, 1897, pp. 15–30, 11
Figs.)
=Gonin, J.= Recherches sur la métamorphose des lépidoptères. De la
formation des appendices imaginaux dans la chenille du _Pieris
brassicæ_. (Bull. Soc. Vaud. sc. nat., xxx, 1894, pp. 1–52, 5 Pls.)
=Heymons, R.= Ueber Flügelbildung bei der Larve von _Tenebrio
molitor_. (Sitz. Ber. Gesell. Natf. Freunde. Berlin, Jahrg. 1896,
pp. 142–144, 1 Fig.)
Also the writings of Malpighi, Swammerdam, De Geer, Lyonet, Bonnet,
Newport, Brauer, Chapman, Fabre, Valery-Mayet, Riley, Chobaut,
Nassonow, Miall (Nature, 1895, pp. 152–158), Hyatt and Arms (Natural
Science, 1896, pp. 395–403).
END OF PART III.
INDEX
[Illustration]
Abantiades, 57.
Abbreviation of larval characters, 707.
Abdomen, 162.
Abdominal appendages, in the embryo, 164;
embryonic appendages, 476;
jointed appendages, 468.
Acetabulum, 94.
Acid, formic, 358;
uric, 352.
Acinose salivary glands, 334.
Acoustic nerve, 290.
Acronycta, 615;
hastulifera, 194.
Acrydium, 421.
Actias luna, its cocoon-cutters, 634.
Adelops, 630.
Adhesive hairs, 111, 113;
fluid, 113;
glands, 360.
Adiscota, 672.
Adminicula, 629.
Adranes cæcus, 57.
Adult insects, tracheal gills of, 476.
Æroscepsis, 265.
Æschna, 53;
rectal respiration in nymph of, 463.
Agriotypus, hypermetamorphosis of, 701.
Aileron, 124.
Air-sacs, 456;
use of, 457.
Aletia xylina, tongue of, 66.
Aleurodicus, 518.
Aleyrodes, 518.
Alitrunk, 90.
Alluring glands, 391.
Alula, 123, 125.
Ametabola, acquired, 599.
Ametabolia, 596.
Amnion, 533;
absence of, 534;
cavity, 532;
fold, 531;
skin, shedding of, 584.
Amphizoa, 461.
Anabolia furcata, buccal organs of, 74.
Anabrus, 49, 73;
cuticula of, 187.
Anal glands, 319, 326, 372;
operculum, 181;
silk glands, 346.
Androconia, 197, 199.
Anisomorpha, 371.
Anisopleura, lateral gills of, 468.
Anobium, 293, 620.
Anomalon, hypermetamorphosis of, 701.
Anophthalmus, brain of, 241;
head of, 74;
olfactory organs of, 276;
salivary glands of, 334;
tongue of, 74.
Anoplus, 101.
Ant, cement glands of, 360;
organ of hearing in, 291;
taste in, 282;
phosphorescent, 424;
poison sac of, 359;
sounds produced by, 294;
stingless, 359.
Antefurca, 92.
Antennæ, 57;
imaginal buds of, 665;
origin of imaginal from larval, 656;
use of, 59, 270.
Antennal auditory hairs, 292;
lobes, 237;
nerves, 650.
Antheræa, 616.
Anthrax, 612.
Anurida, 51;
maritima, 537.
Anurophorus, 424.
Anus, 319;
absence of, 300, 320;
of embryo, 537.
Aphides, changes of color in, 205;
honey dew of, 364;
wax glands of, 364.
Aphis, 616;
reduction of tarsal joints of, 103.
Aphrophora permutata, wings of, 141.
Apis, premandibular segment in embryo of, 52;
germ-layers of, 558.
Apneustic type of tracheal system, 459.
Apodemes, 92.
Apodous larvæ, 103.
Appendages, abdominal jointed appendages, 468;
abdominal, origin of, 550, 551;
abdominal, absence of, 550;
cephalic, origin of, 548;
of embryo, 548, 551;
oral, 549;
thoracic, origin of, 550.
Aquatic insects, 459;
descent of, from terrestrial, 708;
life, adaptations to, 460.
Arachnida, 6.
Arctia, 391.
Arctian larvæ, 615.
Argida, 391.
Armature, 187, 192.
Arolium, 97, 100, 113.
Arthromeres, 30.
Arthropoda, classes of, 3.
Articerus, 57.
Ascalaphus, 616.
Ash, on eversible glands, 377.
Asilus, mouth-parts of, 79.
Aspidiotus, 538, 627;
nerii, hypermetamorphosis of male of, 690;
nerii, metamorphosis of male of, 640, 690.
Ateuchus sacer, 101.
Attacus, mode of escape from its cocoon, 635.
Attacine moths, 634.
Attelabus, 538.
Auditory organs, 287.
Audouin, on the median segment, 163;
on peritreme, 90.
Autolyca, 371.
Auzoux, on the salivary glands of silkworm, 332.
Ayers, on embryonic abdominal appendages, 550;
on fecundation of the egg, 505;
on hypermetamorphosis of Teleas, 703;
on origin of heart, 573.
Bætisca, 467.
Balancers, 124.
Balbiani, on the polar cells of Chironomus, 580.
Ballowitz, on spermatozoa, 497.
Band, germinal, 531;
invaginated, 538;
overgrown, 538;
primitive, 531, 536, 545.
Bapata, 392.
Basilar membrane of eye, 253.
Bee, honey, air-sacs of, 458;
breathing of, 456;
cement glands of, 360;
egg of, 521;
flight of, 151;
head, 80;
moulting of, 611;
mouth-parts of, 79;
number of moults of, 618;
premandibular segment in embryo of, 52;
salivary glands of, 334;
sanitary conditions observed by its larva, 623;
seminal packet of, 500;
spermatheca, 506;
tongue of, 80, 81;
tracheæ of, 458;
wax glands of, 364.
Bee’s foot, action of, in climbing, 114;
sting, 172.
Bees, twisted hairs of, 189.
Beetles, anal glands of, 372;
phosphorescent, 424;
tongue of, 73;
tracks of, 106;
walking, 103.
Benasus griseus, tongue of, 73.
Bladder, urinary, 35.
Blanc, on salivary glands of silkworm, 331, 332;
on silk glands of silkworm, 340;
on spinning glands of silkworm, 340.
Blaps, 373;
gait of, 109;
tracks of, 109, 111.
Blastoderm, 526, 529.
Blatta, 43, 69;
egg-tubes of, 501;
embryology of, 537.
Blattidæ, fœtid glands of, 370.
Blepharocera, 474.
Blochman, on embryology of Musca, 530.
Blood, 407;
corpuscles, 407, 419, 574;
crystals from, 407;
-forming cells, 574, 685;
gills, 475;
veins of wings, 121;
lacunæ, 573;
repellent nature of, 374, 407;
serum, 407;
tissue, 408, 419;
vessels in the head, 405.
Blow-fly, duration of embryonic life of, 582;
egg of, 521.
Boas, on spiracles of Melolontha larva, 439.
Bobretsky, on embryology of Pieris, 529.
Body, cavity, formation of, 563, 566;
central, 232, 237;
completion of embryonic, 555;
form, development of outer, 668;
mushroom, 233;
pedunculated, 232, 233;
stalked, 232, 233.
Boll, on repellent glands, 371.
Bombus, 219, 618;
post-embryonic changes in, 661.
Bombyx mori, 339, 366, 405, 496, 499, 608;
embryonic abdominal legs of, 552.
Bordas, on poison glands, 358;
on salivary glands of Hymenoptera, 337.
Bot-fly, of horse, 475;
of ox, 518.
Bothriothorax, 623.
Brain, 222, 226;
development of, 567;
histology of, 238;
modifications of, in different orders, 240.
Brauer, on Campodea-form larvæ, 600–602;
on metamorphosis, 598.
Breathing, mechanism of, 451;
rectal, 463.
Brin, 342.
Bristles, 188.
Bruchus, hypermetamorphosis of, 700.
Buccal appendages, 59.
Bucculatrix, 634.
Buckton, on change of color in aphides, 205.
Buds, antennal, 665;
buccal, 665;
femerotibial, 656;
frontal, 676;
imaginal, 674;
of Encyrtus, 663;
Melophagus, 686;
ocular, 665;
of ovipositor, 665;
of wings, 669.
Bugnion, on composition of head of Hymenoptera, 55;
on the germs of the sexual glands of Encyrtus, 582;
on the imagined buds of ovipositor, 171;
on the post-embryonic changes in Hymenoptera, 663.
Burgess, on colors, 203;
on hypopharynx, 76;
on scales, 195.
Burmeister, on organs of smell, 265.
Bursa copulatrix, 505.
Busgen, on honey dew, 365.
Bütschli, on an under-lip structure in bee, 547;
on origin and morphology of the tracheæ, 447;
on premandibular segment, 52;
on temporary abdominal appendages, 550.
Butterfly, atrophy of tarsi of, 102;
olfactory organs of, 274;
larval, hibernating, 615.
Caddis-worm, blood-gills of, 475;
eversible glands of, 375;
pupal mandibles of, 633.
Cæca of mid-intestine, 300, 325, 347, 348;
secretion of, 348.
Calcar, 97.
Calcaria, 97.
Calculi in intestine, 325.
Calliphora vomitoria, 618;
eggs of, 521.
Callosamia promethea, 192;
number of moults of, 616.
Callosune, 202.
Caloptenus, 43.
Calopteryx, 54, 464.
Caltrops, 189.
Calypta, 124.
Calyx of brain, 233.
Campodea, embryology of, 22, 52;
ligula of, 721;
moulting of, 616;
premandibular segment of, 52.
Campodea-form larva, 600.
Campodeoid characters, loss of, in holometabolous insects, 707;
larvæ, 600.
Capillary tracheæ, 655.
Carabidoid stage, 692.
Carabus, walking, 107;
tracks of, 109.
Cardiac valvule, 312.
Cardioblasts, 572.
Cardo, 63.
Carlet, on the poison apparatus of bees, 357;
on walking in beetles, 109;
on wax glands, 364.
Carus, on the circulation, 397, 409.
Case-worms, blood gills of, 475;
functional salivary glands of, 331;
spinning glands of, 337.
Caterpillar, actions before pupation, 644;
changes in mouth-parts during metamorphosis, 645;
eversible sacs of, 375;
excrement of, before pupation, 644;
internal changes in, 645;
moulting of, 609;
number of moults in, 615.
Catocala, 392.
Cauliculus, 233.
Cavity, peripodal, 669.
Cecidomyia, 113;
urinary tubes of, 351.
Cells, absorbent, 328;
amœboid egg, 529;
egg, 502;
embryonic, of buds of larval Lepidoptera, 655;
genital, 575;
setigenous, 191.
Cement glands, 360.
Centrosome, 525.
Ceratopogon, 678.
Cerci, 164, 178.
Cercopoda, 164, 178.
Cerura, 375.
Ceuthophilus, 393.
Chabrier, on use of elytra, 159.
Chalicodoma, 542.
Chambers, egg, 502;
yolk, 502.
Chapman, on cremaster, 636;
the hypermetamorphosis of Rhipiphorus, 697;
on mode of escape from cocoon, 632, 633;
on the moulting fluid, moulting of arctians, 615;
on value of pupal characters, 628.
Chermes, 361.
Cheshire, on admission of air into bee’s cocoon, 623;
on bee’s foot, 114;
on bee’s sting, 172;
on bee’s tongue, 79, 82.
Chiasma, 231.
Chironomus, 36, 491;
formation of the imago in, 671, 678;
polar cells of, 580.
Chitin, 29.
Chlænius, brain of, 241.
Cholodkowsky, on homologies of propleg or abdominal leg of
caterpillars, 552;
on patagia, 89;
on testes of Lepidoptera, 496;
on urinary tubes, 354.
Chordotonal organs, 289.
Chorion, 520, 534.
Chromatin, 498.
Chrysalis, 625;
mode of suspension of, 637.
Chrysopa, 517, 525.
Chun, on the tænidia, 445.
Cicada, shrilling organ of, 295.
Cicada septemdecim, 616;
hatching of, 584.
Cimbex, 374.
Circulation, of blood, 409;
organs of, 397;
peritracheal, 397.
Citheronia, 392.
Claspers, 176, 179.
Claus, on eversible glands, 374.
Clavola, 57.
Climbing, mode of, 116.
Closure, dorsal, of embryo, 556.
Clypeus, 546, 547.
Coarctate Diptera, 620.
Coccidæ, male, 626;
metamorphosis of, 641.
Coccinella, moulting of, 611.
Coccinellidæ, 375.
Cockerell, on hatching of mantis, 584.
Cockroach, 455, 456, 487;
brain of, 229, 242;
cement glands of, 360;
chorion of egg of, 521;
circulation of blood in wings of, 410;
colleterial glands, 506;
deposition of eggs of, 519;
digestion of, 325;
egg-tubes of, 501;
fœtid glands of, 370;
micropyle of eggs of, 523;
mode of hatching, 583;
oötheca of, 517;
wingless, 598.
Cocoon, admission of air in, 623;
breaker, 634;
cutter, 634;
formation of, 619;
mode of escape from, 635;
spinning of, 621.
Cœcal appendages of stomach, 300, 325, 347.
Cœcum of colon, 318, 325.
Cœlom-sac, 563, 566, 576.
Coleoptera, embryology of, 537;
gustatory organs of, 284;
internal changes during metamorphosis of, 641;
larval types of, 604, 606;
number of moults of, 617;
olfactory organs of, 275;
phosphorescent, 421;
pupa of, 630;
salivary glands of, 334;
seminal ducts of, 496;
sounds produced by, 293;
spermatozoa of, 497, 499;
tongue of, 73.
Colleterial glands, 506.
Colon, 317;
cæcum of, 318.
Color sense, 260.
Colors, 201;
dermal, 203;
interference, 201, 202;
metallic, 204;
natural, 203;
optical, 201;
order of development of, 208.
Comb, tarsal, 97.
Commissure of œsophageal ring, 237.
Conditions of existence, 463.
Cone, crystalline, 250, 251.
Conglobate gland, 487.
Coniopteryx, 620.
Conjunctivus, 61.
Conorhinus, 616.
Cope, on causes of segmentation of body of arthropods, 33.
Copidosoma, 623.
Copris carolina, 61.
Copulation, signs of, 507.
Copulatory pouch, 505.
Cord, stigmatic, 460;
supraspinal, 240.
Corethra, 433, 460, 618;
auditory organs of, 291;
formation of the imago in, 668, 678;
plumicornis, wing-germs of, 129;
tracheoles of, 133.
Corixa, eggs of, 538.
Cornea, 250.
Corneal lens, 250.
Corydalus, 46, 48, 59, 70, 460, 468.
Corydalus cornutus, hatching spine of, 585.
Coste, on pigments, 206.
Cotylosoma, 478.
Coxa, 95;
origin of imaginal from larval, 656.
Coxal glands, 369;
sacs, 475;
of myriopods, 14.
Cremaster, 636;
absence of, 636;
mode of formation of, in butterflies, 637.
Cremastral hook-spine, 638.
Cricket, 487;
anal glands of, 372.
Crop, 303, 324.
Crustacea, 4.
Cucujo, 426.
Cuénot, on blood, 374, 408;
corrosive glands, 574;
digestion, 329;
leucocytes, 421;
phagocytes, 421, 422.
Cuilleron, 124.
Culex, 461, 465, 474, 599;
formation of the imago in, 668, 678;
mouth-parts of, 78;
phosphorescent, 424;
sense of hearing in, 292;
urinary tubes of, 350.
Cup, spermatophore, 499.
Cuticula, 187, 203;
new layer of, formation of, 612.
Cyclops stage of Proctotrypid parasites, 701.
Cyphon, 472.
Cytoplasm, 525.
Dahl, on constancy of number of six legs, 100;
on motion of insects on smooth, 100, 111, 113, 116.
Danais, 197, 381;
archippus, hypopharynx of, 75;
plexippus, wings of, 137.
Dandolo, on amount of food eaten by the silkworm, 608.
Datana, 634.
Datana ministra, moulting of, 611;
section of larva, 131;
setæ of, 188;
tænidia of, 444, 448.
Death-watch, 293.
Deltochilum gibbosum, 101.
De Moor, on tracks of insects, 106, 109.
Dermal glands, 365.
Dermaptera, wingless, 598.
Deutocerebrum, 231, 237.
Development, direct, 598.
Dewitz’s discovery of imaginal bud-stalks, 673;
locomotion of insects on smooth surfaces, 111;
on movement of leucocytes independent of the circulation, 413;
openings of glandular hairs, 192;
ovipositor, 168, 170, 171;
stigmata of odonate nymphs, 439;
open tracheal system, 460, 464;
wing-buds, 127, 142.
Diapheromera, 371, 616;
eggs of, 517, 520.
Diaphragm, pericardial, 412.
Didonis, 381, 391.
Digestion, 324.
Digestive canal of imago in the fly, appendages of, 297, 302, 331;
formation of, 681;
histology of, 320;
length of, not a criterion of its habits, 301;
primary regions, 299, 302.
Dimmock, on hypopharynx, 71;
on labrum epipharynx, 44;
on pseudo-trachea, 446.
Diplopoda, 12.
Diptera, coarctate, 620;
cyclorhapha, 621;
development of imago of, 666;
food reservoir of, 305;
germs of genital glands, 580;
hypopharynx of, 78;
larval types of, 607;
mouth-parts of, 78;
olfactory organs of, 273;
origin of legs of imago in, 654;
orthoraphous, 621, 626;
post-embryonic changes in, 666;
salivary glands of, 333.
Dipterous embryo, suppression of polypody in, 707.
Direct development, 598.
Discota, 672.
Division nuclei, 530.
Donacia, 620.
Dorsal organ, 535.
Doryphora, 50;
embryology of, 544;
hatching spine of, 586.
Dragon-fly, 53;
muscles of flight of, 157;
number of moults of, 616.
Draught power, 218.
Drosophila, 518.
Dryocampa, 187.
Dubois on the cucujo, 424, 426.
Ducts, ejaculatory, 496;
seminal, 496.
Dufour, gland of, 358.
Dujardinia, 34.
Dyar on the number of moults, 615.
Dyticus, 461;
foot of male, 93, 99, 114;
larva, poisonous saliva of, 359;
mode of swimming of, 116;
tænidia of, 445;
trail curves of, 108.
Eacles, 616.
Ears, 288.
Eaton, on nymph stage, 594;
of rectal respiration in nymphs of ephemerids, 465.
Ecdysis, 609, 611.
Ectoderm, 534;
formation of, 558.
Ectotrachea, 432, 448, 684.
Egg, 515;
burster, 585;
capsule, 517, 520;
cells, 504;
chambers, 502;
fertilization of, 525;
germs, 502;
guide, 183;
internal structure of, 524;
markings of, 521;
maturation of, 525;
mode of deposition of, 518;
number laid, 515;
ovarian, 501;
ripe, 520;
sacs, 361, 517, 520;
shell, 520;
smaller in holometabolous insects, 515;
tubes, 501;
vitality of, 520.
Ejaculatory ducts, double openings of, 486;
origin of, 578.
Elater of Collembola, 551.
Electricity, influence of, on action of heart, 412.
Eleodes, 372.
Elliott on color sense, 261.
Elmis, 462, 473.
Elytra, 124;
glands in, 125.
Embidæ, 620.
Embryo, 531;
revolution of, 540.
Embryology of insects, 515.
Embryonic life, length of, 582.
Embryonic membranes, involution of, 556.
Embryonic, post-, changes, 650.
Emery, on homologies of the tracheæ, 443;
on the firefly, 424, 427.
Empodium, 97, 111, 116.
Empretia stimulea, 192.
Eucyrtus, 55, 171;
post-embryonic changes in, 663.
Endochorion, 520.
Endoderm, 534, 561.
Endomesoderm, 542.
Endosternite, 94.
Endotrachea, 432, 448.
Entomoline, 29.
Entothorax, 92.
Environment, 463.
Ephemera, circulation in, 409;
double sexual openings of, 489;
nymph of, lacinia of, 61;
thorax of, 91.
Ephemerella, 466.
Ephemeridæ, 459, 460;
double genital openings of, 492;
gills of, 460;
rectal respiration in, 464.
Ephydra, 36, 553.
Epicauta, life-history of, 692.
Epilabrum, 13.
Epimerum, 89.
Epiopticon, 231, 253.
Epipharynx, 43, 54.
Epipleurum, 124.
Episternum, 88.
Erichson on sense of smell, 266.
Eriocephala calthella, mandibles of, 62;
maxillæ of, 68.
Eristalis, 189, 461.
Eruciform type of larva, 602, 605, 705.
Escherich, on male genital organs of beetles, 495.
Euphæa, lateral gills of, 468, 477.
Euphoria inda, moulting of, 611.
Eupolus, 113.
Eupsalis minuta, 103.
Eversible sacs, 475.
Excretion, defined, 327;
process of, 328.
Excretory system, 348.
Exner, on vision, 258.
Exochorion, 520, 534.
Exuvia, 609.
Exuvium, 609.
Eye, 249;
acone, 251;
buds, 665;
compound, 250;
embryonic development of, 567;
eucone, 251, 252;
facetted, origin of, 255;
glazed, 629;
pseudocone, 251, 252;
simple, 249.
Fabre, on life-history of Sitaris, 69.
Facet, 250.
Facets, number of, 249.
Facetted eye, origin of, 255.
Faivre, on function of brain, 244.
Fat, amount of, in caterpillar, 644.
Fat-body, 419;
concretions in, 420;
destruction and reformation of, in muscids during metamorphosis, 685;
origin of, 574.
Feet, post-embryonic development of, 653.
Female reproductive organs, 485, 500;
origin of, 575.
Femur, 96;
formation of, in imago of Lepidoptera, 655.
Fernald, on rectal glands of Passalus, 318.
Fertilization of the egg, 525.
Filator, 340.
Filippi’s glands, 345.
Firefly, 426.
Fischer, on color of butterflies, 200.
Flagellum, 57.
Flea, 438;
hatching spine of, 586;
hypopharynx of, 77;
number of moults of, 617.
Flies, syrphid, 189.
Flight, 148, 219;
theory of, 150.
Fluid, exuvial, 612;
moulting, 612;
softening fluid of moths in escaping from the cocoon, 635.
Fly, blow, hatching of, 585;
development of imago in, 666;
horse, mouth-parts of, 79;
thorax of, 91;
house, length of embryonic life of, 582;
thorax of, 88;
number of moults of, 618;
meat, hatching of, 585;
tenent hairs of, 111.
Fold, amnion, 531.
Folds, gastro-ileal, 317;
giving rise to head of fly, 671.
Folsom, on lateral gills of Euphæa, 468.
Food-reservoir, 305.
Foot, of beetle, 111;
of fly, 111.
Footprints of beetles, 106.
Fore-stomach, 306.
Forel, on gustatory organs, 281;
on honey-dew, 365;
on vision, 256.
Forficula, 454, 491;
fœtid glands of, 369;
hatching spine of, 585.
Formic acid, 358.
Frenulum, 122.
Fulgora, 424.
Funiculus, 460.
Funnel, 313.
Galea, 63, 64.
Galeruca, 113.
Ganglia, function of, 244;
fusion of, 225;
optic, 231, 232;
primitive number of, 567.
Ganglion frontale, 569.
Ganglion opticum, origin of, 567.
Ganin, on abdominal imaginal buds, 170;
on hypermetamorphosis of ichneumon parasites, 701.
Gastro-ileal folds, 317.
Gastropacha, 552;
flattened hairs of, 194.
Gastrophilus equi, 475.
Gastrula, 558;
stage, 535.
Gegenbauer, on homology of wings with gills, 142.
Gehuchten, on histology of muscles, 217;
on the histology of mid-intestine, 316;
on the pyloric valvule, 315;
on secretion, mechanism of, 326.
Gena, 46.
Genital armature, male, 176;
cells, 575;
claspers, 176.
Germarium, 501.
Germ-layers, formation of, 558.
Giard on urinary tubes, 351.
Gills, blood, 475;
in embryo insects, 476;
tracheal, 459;
adult insects, 476;
rectal, 463.
Gilson, on anal glands, 373;
on spinning-glands, 340.
Gissler on anal glands, 372.
Gizzard, 311, 324.
Glands, acid, 358;
adhesive, 360;
alkaline, 358;
alluring, 391;
of androconia, 199;
anal, 319, 372;
accessory of vasa deferentia, 497;
cement, 360;
colleterial, 506;
conglobate, 487;
corrosive, 374;
coxal, 369, 383;
dermal, 365;
defensive, 368;
eversible, 368, 382;
Filippi’s, 346;
fœtid, 369;
mucous, 497;
mushroom, 497;
odoriferous, 381;
repugnatorial, 368;
salivary, 331, 570;
setiparous, 444;
sexual, origin of male, 579;
unicellular, 366;
wax, 361.
Glandulæ mucosæ, 497.
Gnathal segments of embryo, 556.
Gonapophyses, 167, 168.
Gonin, on moulting fluid, 613, 614;
on the post-embryonic changes of Pieris, 651;
on process of pupation, 659;
on tracheæ of wings, 145;
on the wing-germs, 131.
Gorgeret, 170.
Gottsche on vision, 257.
Graber, on abdominal legs of caterpillars, 552;
on blood, 408;
on blood-gills of embryo, 476;
on climbing, 116;
on development of wings, 138;
on flight, 153;
on folding of wings, 155;
on foot-tracks of beetles, 109;
on heart, 398, 400, 402;
on mechanics of segmented body and limbs of insects, 31, 38;
on mechanics of walking, 103;
on organs of hearing, 290;
on organs of smell, 267;
on premandibular segment, 52;
on respiration, 454;
on successive appearance of embryonic segments, 546;
on swimming, 116.
Grassi, on premandibular segment in Apis, 52;
on Scolopendrella, 20.
Grège, 340.
Grès, 340.
Griffiths, on pigments, 207.
Grobben on heart, 399.
Gromphas, 101.
Gross, on color sense, 261.
Gryllotalpa, 572;
maxilla of, 64.
Guide, egg, 183.
Gula, 46, 68.
Gulo-mental region, 46.
Gummy layer of silk, 340.
Gyrinus, 471, 620.
Haase, on coxal sacs, 14;
on eversible glands, 371;
on the formation of the copulatory pouch, 505;
on Scolopendrella, 21, 24;
on the homology of the ovipositor, 171.
Hadenœcus, 44, 392.
Hagen, on colors, 201;
on gills of Perlidæ, 477;
on lateral gills of Euphæa nymph, 468, 477;
on vestigial gills in other odonate nymphs, 469.
Hair-fields, 197.
Hair-forming cells, 188.
Hair-scales, 197;
tactile, 193.
Hairs, 188;
adhesive, 111, 113;
development of, 193;
gathering, 45;
glandular, 190, 192;
nettling, 191;
plumose, 189;
tenent, 99, 190;
in tracheæ, 451;
twisted, 189.