Medical Zoology. Anatomical and Morphological Characters of Mosquitoes of the Family Culicidae

Medical Zoology. Anatomical and

Morphological Characters of

Mosquitoes of the Family Culicidae *

Long-legged mosquitoes, also known in Brazil by the names of muriçocas and carapanãs, belong to the Order Diptera, characterized by two wings, two halteres and a suctorial proboscis, and to the Suborder Nematocera vera, whose antennae have many long articles. The Culicidae or culicids, as we say in English, may be recognized by the wings, densely covered with scales, and the pungitive proboscis, which lacks in the genera Corethra, Corethrella, Sayomyia and Mochlonyx, nowadays considered in a separate family: Corethridae or Culicimorphae. Culicid larvae live in water, as well as nymphs, which are mobile, but do not feed. Before metamorphosis, they become filled with air and float, in such a way that the imago may emerge through a dorsal cleft of the nymphal integument.

Eggs may be laid in highly dry places, but always above water or periodically flooded. However, as a rule, they are laid on the water surface, where they float by means of an air-chamber. They may be isolated, occupying a horizontal position, or packed together, like cartridges, in the form of canoes, their position then being vertical. In this case, larvae are formed with the head upside down, emerging inside the eater by occasion of the ecdysis.

In species frequenting human abodes, evolution may be very rapid, lasting a little more than a week during warm weather. If circumstances are less favourable, or if other species are involved, it may last much longer.

The larvae, which are rapidly formed in the eggs, breathe water by means of their branchial appendices or by their posterior stigmata, placed on the dorsal surface in the subfamily Anophelinae or within a breathing tube in other mosquitoes. The larvae generally feed upon debris or small aquatic organisms, but some species, characterized by very strong mandibles, feed upon other organisms, including larvae of their own or of other species.

Larvae of the domestic species are found in any deposit of water, either collected for human and animal use or during rainfalls, such as basins, water-pots, waterreservoirs, earthen vessels, garden tanks and even cans and bottles filled with rainwater. Swamp mosquitoes breed in stagnant or low-flowing waters with aquatic vegetation and in lakes and swamps fed by river overflow. Forest mosquitoes live in water deposits found in tree holes and, among us, especially in the water contained inside bromeliads and bamboos.

Adult culicids (Fig. 5 and 6) present a well marked dimorphism which allows the distinction of sexes at first sight. The secondary sexual characters are observed in the antennae, the palpi, the mouthparts and claws; the primary ones appear examining the posterior part of the abdomen.

As in all other Diptera, the body of culicids shows three main segments, the head, the thorax and the abdomen.

The head (Fig. 1-4) is formed by the largest number of segments, so closely united that they are only indicated by their corresponding appendices. Its form is subglobular or hemispherical, the flatter portion being turned backwards and linked to the thorax by a thin neck. It has two large compound eyes, only separated by a narrow vertex, but there are no vestiges of ocelli. Behind the eyes a triangular occiput is seen, and below it, the nape. The antennae are placed into a reentrance of the eyes, which thus become reniform; the part situated between the eyes is called frons and, beneath it, we can see the clypeus, of a semiconical shape. Below it, the proboscis protrudes, having a maxillary palpus on both sides. The remainder of the face is formed by two cheeks or genae. Below the proboscis there is the mentum region, and beneath the nape, the gulla. In the mosquitoes, the compound eyes occupy the greatest part of the lower side of the head, meeting on the midline.

The culicid antennae are formed by 14 articles in females and 15 in males, the basal one being flattened and discoidal, the others elongated. They are clothed with hairs disposed in verticils or whorls, generally shorter in females, which have the antennae only pilose, and longer in males, whose antennae appear plumose. This character permits the distinction of sexes in almost the totality of the mosquitoes; and only in some lesser important species there is not this well marked difference.

The maxillary palpi vary in length, form and number of articles. Species with elongate palpi in both sexes (Anophelinae and Megarhininae) may be called macropalpae, those with short palpi in both sexes micropalpae, to those with long papi in males and short ones in the females (Dendromyia etc.) the designation heteropalpae is applied (Culicinae).

When the palpi are long, they may have five articles, which seems to be the normal maximum. As a consequence of a more or less complete fusion or suppression, the number may be reduced to two, as it may be observed in short palpi. Even as for the palpi, which are long in both sexes, the male ones differ from those of females.

The proboscis has a variable length, but it is always very long. In Megarhininae, it is curved on the apical part, and in males of Limatus it shows a middle angle. In other species it is straight, but, being very thin, it may appear somewhat arched in dry specimens.

The labium cannot be differentiated in either sexes and its integument corresponds to that of the rest of the body. The included parts are made up of smooth chitin of an ochre-colour and vary little in their shape, according to their adaptation. The mandibles lack in all non-blood-sucking males and females. On the tip of the proboscis two valves may be perceived. Called labella, they correspond to the labial palpi. The maxillae, always present, have their base united to that of the corresponding maxillary palpi. In the hypopharynx a common salivary duct may be perceived.

The thorax, as in all Diptera, is formed by three fused segments. The middle one (mesothorax) occupies almost all the dorsal region, ending into a trilobate or crescent-shaped scutellum. Of the prothorax only the humeral lobes appear in dorsal view; of the metathorax one sees in the midline a semi-oval segment, the metanotum; generally bare or with a terminal tuft of short bristles, and seldom showing some flat scales. Other bristles appear on the mesonotum, especially on the scutellar margin. The wings and the halteres originate from the lateral parts of the mesonotum and metanotum. The legs are placed on the ventral side, each pair corresponding to a thoracic segment.

The abdomen is composed of nine segments. Its form is generally cylindroconical, but it may be dorsoventrally or laterally compressed, in greater or lesser extent. On the eighth segment opens the anal orifice; the ninth corresponds to the exterior genital parts, in the

shape of two lateral lobes in the female (Fig. 8) and of two pincers in

the male (Fig. 7). Their structure and that of the accessory appendages in the male is used in systematic, but cannot be appreciated when only females are available, for these are obtained with greater facility. Fortunately, they may be perfectly determined by characters common to both sexes.

In the culicid wing, we distinguish an upper and a lower surface; the anterior margin or costa, uniting the base with the apex and the posterior margin, shows a fringe of longer scales and an incision near the base. The veins carry rows of variously-shaped scales, generally shorter and wider on the internal rows.

The longitudinal veins or nerves are the following: the costal vein, which forms the margin of the entire wing, albeit thinner on the hind margin. Behind it may be perceived the first longitudinal vein, the sub-costal, which enters the costa before the apex. From it, there starts the second longitudinal, whose bifurcation contains, a little before the bifurcation, the third vein, which is simple; its basal part forms an obtuse angle and seems to be a supernumerary crossvein, in opposition to the normal transverse vein uniting the third to the fourth longitudinal veins. The latter starts at the base, as a rule, and ends up into a second bifurcation. Near the middle, it is linked by the second transverse vein to the superior branch of the fifth, which shows a third, very long bifurcation. It starts at the base, as well as the sixth longitudinal or anal vein, which, after a more or less sinuous course, ends without bifurcating in the middle part of the hind margin. In a few species there is an indication of a seventh longitudinal or axillary vein.

In systematic, the position of the transverse veins among them and in relation to the base is used.

About the legs of the mosquitoes a few words suffice. The segments are those already described for the Diptera, but relatively thin and long. The first tarsus (also called metatarsus) is similar in length to the tibia, the other tarsi are much smaller. The last one possesses a pair of claws, which may be simple or composed and furnish sexual and specific characters. Some mosquito species, without medical importance, frequently have on their legs, often in only one pair, some lateral tufts of long hairs or bristles, rendering them oar-like and very conspicuous.

Scales. Mosquitoes are almost entirely clothed with scales, which exceptionally lack only on the thoracic and abdominal dorsum. The clypeus, the halteres, the metanotum and the antennae are generally devoid of scales, but they may be partially or entirely dressed with shining scales. The claws never show scales, as in all other insects.

Scales may be considered as modified hairs, showing many transitions from them. Mosquito scales are similar to those of the Lepidoptera and show great variations in their form. When flat, they are generally juxtaposed and often imbricate. In certain regions, such as on the notum and oftentimes on the occiput, there may exist long and curved scales in many directions, being prominent or erect. Sometimes they form lateral tufts on the abdomen, some other times on the thorax, the antennae or the legs.

In order to designate the shape of scales it is convenient to use the expressions employed in the descriptions of leaves and petals. Thus, one can talk about linear, lanceolate, oblanceolate, oval and oboval, obtriangular scales etc. The expression spindle-shaped, oftentimes employed for pointed, elliptical scales, is not very correct, but one understands that we are only dealing with the projection of a fuse. These scales are often narrow, long and curved or twisted. Other times scales have their apical part truncated or ending into two or three points. Thus, we shall have shovel-like or spathulate scales.

A characteristic shape is the obtriangular, with a somewhat rounded apex, which reminds one of the shape of a folded fan. It characterizes the wings of Culex. Oboval and scarcely wide scales are found on the wings of Taeniorhynchus. Cyclolepidopteron has balloon-shaped scales, oboval and very wide. Mansonias have scales that I have called securiform [sickle-shaped] and Blanchard bannerlike scales. They are asymmetric, corresponding to a wide oboval with one of the sides obliquely truncated on the apical half. To substitute descriptions, we may also talk about Culex-, Taeniorhynchus-, Mansonia-scales, etc.

Scales may have their own colour, generally white, ochre or dark, as it can be well verified examining a wing of Mansonia titillans with incident light. Scales of a golden, bronzy, green or blue colour do have a proper pigment, and the hue varies with the incidence of light, in such a way that the same scale may appear white, sky-blue, etc. As in the wings of the brilliant butterflies of the genus Morpho we are dealing here with colours due to interference on thin lamellae. These shining scales, not observed in European species, are preferably found in phytophilous mosquitoes.

The internal anatomy (Fig. 7 and 8) of culicids corresponds to what has already been exposed for Diptera in general. There are, however, some points that must be stressed.

The absorbed blood passes from the proboscis to the pharyngeal cavity and thence, though the oesophagus, to the cheliferous venter, which becomes enormously dilated. The oesophagus diverticula (which may be 3 in number) are not filled with blood. The salivary glands of mosquitoes are well developed and occupy the antero-inferior part of the thorax. There is, on both sides, a shorter median lobe, whose darker cells seem to produce the toxic and irritating substance inoculated at the occasion of the bite. On both sides of it, there is a longer and lighter tube; sometimes one of these tubes bifurcates.

Glands are readily recognizable by the excretory tube, reinforced by chitinous rings reminiscent of a trachaea. The three tubes on one side are united into a common tube, which, higher up, unites itself to the tube on the other side. In malaria, sporozoids accumulate in the salivary glands, especially in the middle part, which permits to recognize the infecting mosquitoes. Sporocysts are found on the wall of the cheliferous intestine, beyond the Malpighian tubules, in which it may be observed the development of larvae of Filaria immitis of dogs and, in the thoracic muscles, larvae of Filaria bancrofti. Mature larvae, in order to pass to the definite host, seek the proboscis sheath, formed by the labium.

Mosquito larvae (Fig. 9) go through some moults, but the various instars do not show major differences. Only the spinous combs are more developed in adult larvae, which are easily recognized by the size and the development of the nymphal eye, which corresponds to the compound eye. Smaller larvae only have simple eyes.

In the larvae, always apodous, we distinguish the head, three thoracic segments, completely fused into a thoracic mass and nine abdominal segments.

The head is formed by a chitinous, sub-spherical capsule, dorso-ventrally flattened, or is sub-quadrate when seen from above. It is generally naked, with a few larger bristles, which may be composite or assume the appearance of spines, which distinguishes the genus Uranotaenia. There are two more or less developed antennae with indication of a segmentation. In the tip there are some spines and sensorial hairs, amidst which may be a lateral tuft of branched bristles. The palpi are little developed. The larval mandibles and maxillae are of the masticatory type, moving in the horizontal plane. On their inner side they are dentate and furnished with combs or brushes on the outer side, serving to establish a flow directed towards the mouth. Below the latter, the lower labium forms an odd plate, more or less triangular, with a larger tooth in the middle and a series of lateral teeth. This labial or mentonian plate is one of the most characteristic organs. On the anterior part of the head there exists, on both sides, a little organ generally in the shape of a bristle, but in two species it suffices to identify the larvae, because in one it appears as a composite papilla, and in the other like a Charcot's crystal. The length of these styli preorales and the distance of their base also affords good characters.

The thoracic bristles or chetae indicate its three-segmented composition and are the only well differentiated part. The thorax may be wider than the head, or narrower as in many Culex.

The abdominal segments form rings somewhat convex in the middle. The penultimate carries a breathing siphon of very variable shape and length, whose structure is enough to characterize the greatest number of species. In Culicinae there are combs of compound spines and bristles, often in tufts, which afford additional characters. In the Anophelinae the breathing siphon is lacking or completely rudimentary. The last segment, also called anal, forms an angle with the rest of the body. In addition to combs of spines and bristles, it usually shows some four membranous blades serving as blood gills. They have a triangular shape, sometimes very elongated.

Culicid nymphs (Fig. 10) are constituted by a voluminous cephalothorax and a nine-segmented abdomen, ending into two caudal follicles used as oars and which may be substituted by tufts of small bristles. The integument, in its greater extension, is naked and the covering reduced to a few bristles, either isolated or in tufts.

The cephalothorax, very elevated, is laterally compressed, so as to form a very thick vertical disk, whose shape, somewhat irregular, is destined to guard the head and thorax of the imago, with the appendices and extremities folded down. These become more distinct when ecdysis is about to take place. In the beginning of the nymphal phase one perceives only the compound eyes and, on the dorsal side of the appendices, hollows that resemble little horns of varied shape. They substitute the breathing tube of the larva, guaranteeing the access of air. Their morphological characters allow certain conclusions regarding adults; it is easier, however, to make determinations based on the imago, after ecdysis. The latter may last eight days in some larger species, but generally it is observed already after two or three days after the transformation of the larva.

Eggs show many variations, which, however, are of small practical importance.

Fig. 1 – male head; Fig. 2 – Anopheles maculipennis female head

18x; Fig. 3 – male head; Fig. 4 – Culex pipiens female head 24x; Fig.

5 and 6 – male and female of Stegomyia argentea (syn. taeniata, fasciata and calopus). 6x; Fig. 7 – male sexual organs of Aedes 30x;

Fig. 8 – abdomen end of Anopheles female 50x; Fig. 9 – larvae of

Anopheles (horizontal) and Culex (diagonal), 6x; Fig. 10 – nymphae

of Culicidae 10x. The plates 3 and 4 are copied from Carroll's, the

rest according to Eysell's originals.

* Paper by Adolpho Lutz published in 1921 in A Folha Medica, v.2, n.16, p.123-5, with ten figures (n.1-10). Translated into English by Professor Nelson Papavero. [E.N.]