NationalLibraryOfScotland/medical-history-of-british-india huggingface dataset:
Studies on the Mouth Parts and Sucking Apparatus
of the Blood-Sucking Diptera.
No. 2.
Some Observations on the Morphology and Mechanism of the Parts
in the Orthorrapha.
SINCE the discovery of the practical importance of the blood-sucking
Diptera the attention of investigators has to a large extent been concen-
trated on the study of their binomics, distribution and classification, to the
neglect of the problems which attracted the older entomologists, and the study
of the homology of the parts and of the mechanism by which they act have
received little attention. Much of this neglect is due, no doubt, to the fact
that so large a proportion of the recent work has been done by medical men and
others to whom entomology was of interest mainly as an applied science, and
these problems, fascinating though they are to the zoologist, have no apparent
connection with the rôle played by insects in the transmission of disease. It is
not unnatural that such a restricted point of view should have led to misconcep-
tions, and more especially since the mosquito, which, on account of its great
economic importance, has been more studied than all the rest of the group
together, happens to be a very highly specialised form. Moreover, most of the
common mosquitoes are small and delicate flies, and are not at all easy to dissect,
and it is not to be wondered at that many points in their anatomy and physio-
logy should have been missed, when a comparative study was not attempted.
In such a compact natural group as the Diptera, in which, although the varia-
tion in form is very great, the general principles of structure are maintained
throughout, questions of the homology and of mechanism are intimately bound
up with one another, and it is of the first importance to compare the separate
parts one fly with those, often. markedly different in appearance, which ful-
fil the same function in the others. The comparative method, indeed, is not only
the one by which the more strictly zoological side of the question is to be
attacked, but it is of great assistance in elucidating the physiology of the
proboscis, a matter of importance to the parasitologist.
I do not propose to attempt in the following pages any comprehensive
review of the subject, not having at hand the necessary literature, but to
discuss some of the more important points of structure and their bearing on the
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mechanism of the proboscis. At the outset it will be well to emphaize the
fact that the process by which a blood-sucking fly obtains blood from the host
is essentially a mechanical one, in the sense that it is governed by the ordinary
principles of muscle movement and of physics. Any explanation of the process
which is not in accord with the anatomy of the parts, or which takes no account
of ordinary physical laws, must be rejected. One may add, that any hypothesis
which would attribute to an organ in one fly a function which it does not
possess in another is to be regarded with suspicion, and that due regard is to be
given to the observed habits of the insect, when the size of the fly and other
circumstances permit of observation. A critical examination of the method of
feeding with these points in mind will show that the subject is by no means so
simple as at first appears, and that many of the statements current, especially
with regard to the mosquito, are vague and inaccurate.
It will be convenient to discuss the subject in two parts, the making of the
wound and the sucking up of the blood.
The Biting Apparatus and its Mechanism.
The biting apparatus in the orthorraphic flies is ordinarily described as
consisting of the paired mandibles and maxillæ, the labrum-epipharynx, and the
hypopharynx. The orthorraphic biting flies are sharply distinguished from
those of the Muscid group by the fact that the labium does not enter into the
wound at all, functioning mainly as a sheath for the other parts.
The first question which attracts one's attention is as to the nature and
origin of the force by which the " piercing stylets " are driven into the skin of
the host. Most accounts of the mouth parts of the mosquito simply state that
the piercing parts are thrust into the skin, without attempting to explain how
this is done, though Nuttall and Shipley go so far as to say that the man-
dibles enter the skin when the labrum is thrust in, by means of the " same
elastic force which induces the sharpened end of a piece of whale-bone to
pierce a soft body if the other end is pushed towards the surface," and they
note the presence of muscles for the retraction and protrusion of the maxillæ.
Annett, Dutton and Elliot state definitely that " the piercing of the skin is
brought about by muscular force directed from the body of the insect, the
muscles attached to the bases of the stylets serving to keep them rigid."
Actual observation does not help us much in the case of any of these flies, for
all the parts concerned are small and concealed by the labium. The position
of the fly while in the act of feeding is, however, of some importance. If it
were simply a question of vis a tergo, then one would expect that the piercing
parts would be brought into line with the long axis of the body, for it is obvious
that the muscles concerned would act at a great mechanical disadvantage if
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they had to propagate a force through an angle. But this does not occur as a.
general rule. The only striking case in point is that of Hœmatopota, which
when in the act of feeding raises the posterior part of the body so much that
it makes with the surface of the skin an angle of nearly half a right angle.
The posterior surface of the head and the anterior surface of the prothorax are
moulded to fit one another, and, as the neck is a very short one, it is probable
that some force at least can be propagated from the thorax, though not, it
should be noted, through the neck. But even in this case it is improbable that
the force from behind enters largely into the mechanism, for in Tabanus
and the allied genera, although the mouth parts are almost identical, the posi-
tion assumed by the fly is such that the body is parallel with the skin and the
proboscis perpendicular to it. Ceratopogon assumes a position similar to that
of Hœmatopota, but as the proboscis is perpendicular to the long axis of the
body the manœuvre cannot possibly bring the two into the same straight line.
In Anopheles the proboscis is directed straight forwards in the position of rest,
and to reach the skin at all the insect has to raise the hind end of the body
and to depress the proboscis, thus doing away with the apparent advantage of
its attitude ; as a matter of fact the proboscis is bent downwards very nearly
to a right angle, as shown in Nuttal and Shipley's admirable drawing.
The attitude assumed by the fly when feeding therefore renders the opera-
tion of a force propagated from the thorax unlikely. We have next to consider
how far the anatomical arrangements are adapted for such a force. So far as
the muscles are concerned the question is a simple one. In all cases the feet
are provided with claws admirably adapted to enable the fly to take a firm hold
on the skin, and it might be supposed that the extension of the joints of the
middle and hind legs would result in a forward thrust of the thorax and head of
the fly. The ends of the piercing organs being then applied to the skin, they
must enter or else bend forward, and we know that the latter, at least in the
case of the mosquito, where the piercing stylets are readily seen when they are
separated from the retracted labium, does not occur : in any case mere bending
would not be of advantage, unless we adopt the view noted above for the
mandibles, that the potential force produced by their flexion is used up in
piercing the skin. A moment's consideration will show that this explanation
will not suffice, either for the mandibles alone or for the piercing parts as a
whole, for it would follow that the cutting edges of the blades must be
directed forwards, while as a matter of fact those stylets which have cutting
edges at all have them directed in the lateral plane.
Bending and elastic rebound are therefore out of the question for any of
the mouth parts. There remains the simple thrust, which is rendered unlikely
by the attitude of the fly. But a forward thrust cannot be propagated without B
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some rigid structure through which it can act and, in this case the necessary
rigidity would have to be ensured by the neck. As a matter of fact the neck
of these flies is not at all adapted for such a purpose. Its length varies a good
deal in the different forms, being very short in the Tabanidœ, and compara-
tively long in the mosquito. But in no case does it possess an amount of
rigidity sufficient to permit of the propagation of a force capable of driving the
stylets into the skin. By far the greatest portion of the wall of the neck
consists of a soft and flexible membrane, attached in front to the borders of the
occipital foramen and behind to the opening into the thorax. In this there are
developed thin plates of chitin, one on each side, usually free from one another,
but approaching in the middle line ventrally. These cervical sclerites are
loosely articulated with the epicranium in front, but in none of the species
which I have examined do they take part in a definite articulation with the
thorax. In the Tabanidœ the cervical sclerites are displaced backwards out of
the neck, and are found at the sides of the thoracic inlet, two of the three pairs
being entirely free from chitinous attachments. The cervical sclerites, in fact,
are mere strengthenings of the integument of the neck, and fill no other
functions than those of affording additional support in the cases where the neck
is long, and of providing attachments for the muscles which move the head.
The neck is a soft canal, capable of distension as blood flows through the
œsophagus, a point well shown in Nuttall and Shipley's drawing of the mosquito
in the act of feeding.
The motive force must then lie in the head. or the neck. The latter may
be disposed of in a word or two. The muscles it contains are very small, and
are merely the representatives in this region of the fibres which connect
adjacent segments elsewhere in the insect body. Their function can be no
more than to move the head on the neck, the looseness of the membraneous
wall permitting of a certain amount of retraction and rotation, easily seen
when a mosquito is beginning to feed and is searching for a suitable spot for
the puncture. It is impossible to conceive of any arrangement of muscles by
which the neck could be extended in such a way as to drive the mouth parts
into the wound, nor can any such muscles be found by section or dissection.
The argument brings us to the conclusion that the muscles which make
the wound are situated in the head of the fly. Before going further it will be
well to consider for a moment the origin of the several organs ordinarily des-
cribed as the piercing stylets. The labrum-epipharynx (Text-figure 2, page
27) is the result of the fusion of the labrum, which is an extension down-
wards of the clypeus, and in other insects connected with it by a freely
moveable joint enabling it to act as a true upper lip, with the epipharynx, an
outgrowth of the stomodæum, and in these flies easily traced upwards to its
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termination in the first part of the sucking apparatus. The fusion between
them is not so close that the two become welded into one organ, for the
epipharynx in all forms retains the shape of a nearly closed canal ; the labrum
may, as in the mosquito, adapt itself to the shape of the epipharynx, or it may
remain flattened and blade-like. There is in all the forms which I have ex-
amined evidence of a joint between the labrum and the clypeus, at the situa-
tion of the corresponding joint in insects such as the cockroach, which have a
freely moveable upper lip, and in the region of this joint the labrum and epi-
pharynx are much less firmly united than elsewhere. The hypopharynx is
usually described as an outgrowth from the lower lamina of the stomodæum,
corresponding to the epipharynx, but it would be more accurate to describe it
as consisting of two laminæ, the upper one of which is derived from the stomo
-dæum, the lower from the labium, the two enclosing between them the sali-
vary duct. The distinction between the two laminæ can be made out by
dissection in the larger Tabanidœ, in which it is quite easy to pull away the
lower lamina still attached to the base of labium, and to leave the upper
lamina, along with the salivary duct, still attached to the first sucking chamber.
In all these biting flies, which must of necessity introduce the saliva into the
wound, the lower lamina of the hypopharynx is completely separated from the
labium, but in very nearly allied forms, and even in the males which do not
suck blood, as in the case of the mosquito, the lower lamina remains attached
to the labium. The separation is evidently due merely to the necessity of in-
troducing the saliva into a comparatively deep wound, into which the labium
does not enter.
The mandibles (Text-figure 1, page 13) represent the appendages of the
fourth segment of the insect head, and are homologous with those of other
insects, such as the beetles, in which they act as cutting and tearing weapons.
Similarly the maxillœ correspond to the appendages bearing the same name,
but with much more obvious functions, in other arthropods. They are the
only appendages in the Nematocera which retain at all closely the primitive form-
Now, to repeat the statement made in the opening paragraph, we should
regard with suspicion the supposed function of the labrum-epipharynx and
hypopharynx as piercing organs, if for no other reason that they are homo-
legous with structures which do not ordinarily possess such a function, whereas
we would confidently expect the mandibles and maxillæ to play a prominent
part in the making of the wound. It is now necessary to examine the mus-
culature and armature of these organs, to see how far they are consistent with
this view.
There is only one muscle attached to the labrum-epipharynx, and this is
found in the same place as that which in the cockroach lifts up the upper lip
B 2
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It is conspicuous in Tabanus, in which it has been figured by Meinert and
Hansen, and occurs also in the mosquito, and is very clearly shown in
Nuttall and Shipley's drawings. It lies immediately behind the articulation
between the labrum and the clypeus, arising from the internal surface of
the latter and finding attachment to the proximal extremity of the labrum at
the point where it is only loosely attached to the epipharynx ; it is difficult to
decide its exact point of insertion, or its function. Meinert regarded it as a
depressor in Tobanus, while Nuttall and Shipley describe it in Anopheles
as an elevator. Whatever its function may be, one thing is clear, that it
cannot act as an extensor of the labrum. It is of constant occurrence in the
N e m a t o c e r a .
The hypopharynx has no muscle attached directly to it, so we have to pass
further back, to the sucking chambers to which the epipharynx and the hypo-
pharynx are so intimately attached. Here we find another proof, incidentally,
that the forward thrust of the body of the fly cannot act as a motive power, as
far as these two organs are concerned, for in no member of the group is there
any chitinous connection between the wall of the head capsule and the sucking
apparatus. Force transmitted to the head from behind can only be propagated
to the labrum, and through it to the epipharynx by the attachment of the
labrum to the clypeus, and to the hypopharynx by means of its loose basal
attachment at the proximal end of the labium. There are, however, certain
muscles attached to the sucking chambers which undoubtedly have the power
of raising and lowering them, and with them the stylets which arise from them.
These muscles can only be made out as definite bundles in Tabanus, in which
they have been figured by Meinert. There are two sets, one of which is in-
serted at the upper end of the first sucking chamber, and by pulling in an
upward direction retracts the chamber and with it the labrum-epipharynx and
bypopharynx ; the second set are attached about the same place but pull in a
downward direction, and will therefore thrust the stylets into the wound. In
Simulium the retractor muscles are present, as figured by Meinert, but the
protractors do not exist as a distinct bundle. In Anopheles the first sucking
chamber is a very small one, and the protractor and retractor muscles are not
distinguishable. It is possible that some of the fibres of the muscle termed by
Nuttall and Shipley the elevator of the palate may act as protractors and
retractors to a slight extent.
Whatever be the true function of these muscles it is evident that they are
not essential to the act of insertion of the proboscis, for they do not occur in an
equal degree of development throughout the group, and are not to be distin-
guished in the mosquito, the piercing apparatus of which is at least as efficient
as that of any of the other flies. In any case, it is almost inconceivable that
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such small muscles, acting at such a manifest disadvantage, could drive the
labrum-epipharynx into the skin, even in the case of Tabanus. The extent of
their action in protracting and retracting the labrum-epipharynx is limited to
the amount of bending which can take place in the labrum at that portion of
its upper end which is only loosely attached to the epipharynx. The utmost
capacity of the protractor muscles can only suffice to stretch the proximal end
of the labrum until it is in the same straight line as and in contact with the
epipharynx. The amount of retraction is less easy to define, for it is limited
only by the loose joint between the labrum and the clypeus, and there is
nothing to prevent the first chamber, which in all cases is connected to the
second by a membraneous canal, from being drawn up within the head, except
the muscles which support it and connect it with the wall of the head capsule.
It will be necessary to refer to this point later on, but for the present it will
be sufficient to state, that the anatomy of the parts indicates that though a
certain amount of retraction and protraction of the first sucking chamber can
take place, the action is not a powerful one, and the limit of extension is such
that the distal ends of the labrum-epipharynx and hypopharynx cannot
extend further than the level of the ends of the mandibles and max
i l l æ . T h e f a c t t h a t p r o t r a c t o r a n d r e t r a c t o r m u s c l e s c a n n o t b e d i s t i n g u i s h e d i n t h e
highly efficient mouth parts of the mosquito is a strong argument against their
taking any prominent part in the making of the wound in the closely allied
flies.
One other point occurs to one in this connection. No matter what the
armature of the tip of the labrum-epipharynx may be, and as will be shown
later it is ill adapted for piercing, it would work at a very great mechanical
disadvantage if actuated by a simple forward thrust, without any lateral move-
ment or rotation. If one attempted to drive a carpenter's augur through a
piece of wood without the usual rotatory movement, the amount of force
required would be infinitely greater than it normally is. Rotation of the
labrum-epipharynx and hypopharynx is of course anatomically impossible.
It will be convenient to sum up the argument at this point. The driving
force by which the piercing parts are inserted into the skin is not derived from
the muscles of the legs or thorax, because the neck is too flexible and slender
to transmit such a force. It is not to be found in the muscles of the neck,
for these are sufficient only to move the head on the thorax in the adjustment
of the proboscis to a position favourable for feeding, and there is no arrange-
ment by which the neck could be forcibly extended so as to drive the stylets
into the skin. The position of the proboscis in relation to the long axis of the
body is a most unfavourable one for the exercise of any thrust from behind, as
such a thrust would tend to bend the proboscis backwards towards the thorax.
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The ingenious suggestion of Nuttall and Shipley that the mandibles enter
the skin by means of an elastic rebound from a bent position will not hold for
either the mandibles or the other stylets, for the cutting edges are invariably
directed laterally, and moreover in most of these forms the stylets are flattened
from side to side. The labrum-epipharynx and. hypopharynx are capable of a
certain amount of protraction and retraction, but the movement of protraction
is limited to the amount necessary to bring their distal ends to the level of the
tipe of the mandibles and maxillæ, and is in any case not a powerful move
ment, nor does it occur with such uniformity, at least as regards the degree of
development of the muscles concerned, that one is justified in regarding it as
an. essential factor in the making of the wound.
There remain for consideration the mandibles and maxillæ, true append-
ages, homologous with those which are used by other arthropods to obtain
their food, and those which, on general zoological principles, one would expect
to find functioning as cutting organs.
In the mouth parts of insects there are many wonderful contrivances
elaborated by nature to achieve her end, but nothing more remarkable than the
adaptation of these appendages to their present function. Throughout the
group, notwithstanding the individual variations, the mandibles and maxillæ
preserve their distinctive character in such a way that one can readily discern
in them the resemblance to the cutting and clasping appendages from which
they have originated. So close is the resemblance that a general description
will apply to any of the forms in the group. The mandibles are flattened. and
blade-like, terminating in a sharp point, slightly recurved after the manner of
a sabre, and armed on the inner edge of the blade with a single row of fine
serrations strikingly like those on the edge of a saw. The two mandibles are
in the same plane, their inner edges being directed towards one another and
almost meeting in the middle line in the position of rest. At the base of the
blade the mandible is articulated to the edge of the gena, in a position corre-
sponding to the ginglymus in other insects, and the articulation is such as to
permit of an inward and outward movement of the blade, on the pivot formed
by the point of attachment. This is very well shown in the larger Tabanidæ.
The base of the mandible in these forms divides into a pair of stout cornua, the
external one of which is articulated to the gena, the internal one free. To
each of these cornua muscles are attached, by the contraction of which the
mandible is alternately rotated inwards and outwards on its pivot, the muscles
attached to the internal cornu acting as adductors of the blade, those attached
to the external one as abductors. Now the cutting edge is internal, and this
edge is not straight, but curved outwards, so that the motion of adduction does
not merely displace the cutting edge inwards, but draws it obliquely through