Chapter XXXIV: Part III: The Metamorphoses of Insects (5)

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).

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).

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.

FIG. 640.—Oil-beetle: _a_, first larva; _b_, second larva; _c_, third
larva; _d_, pupa.
]

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.

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.

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.
]

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).

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.

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.

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).

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).

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.

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.

FIG. 651.—First larva of Platygaster: _m_, mouth; _at_, rudimentary
antenna; _md_, mandibles; _d_, tongue-like appendages.
]

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.

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.
]

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

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.