Medical Zoology. Non-Culicidae Haematophagous Nematocera*
Among the haematophagous Nematocera, culicids occupy the first place, on account of their vast number and wide distribution of their species, as well as the importance of their role as vectors in human pathology. However, there are three additional families including haematophagous species deserving studies.
Among them I place first the Psychodidae, which are more similar to culicids and which are also Nematocera vera, furnished with long antennae. As regards the other two families, the Chironomidae, with the subfamily Ceratopogoninae are equally Nematocera vera, but the Simuliidae have antennae with short articles and belong to the Nematocera anomala.
All these species of blood-suckers have been confounded under the name sandflies. In my judgment, this name must be reserved to the cerapotogonids of the genus Culicoides, known among us by the name maruim. Notwithstanding, in the lack of other popular name, sandfly is much used for the genus Phlebotomus.
The most important characters of the non-culicid Nematocera are found together in a table, which allows the determination of the family of any species whatsoever. Moreover, I will give some notes about the three families.
Psychodidae: The family Psychodidae includes very different species as regards their aspect and characters, but all of them united by the wing-venation. All of them are small, with relatively large wings. The members are generally short and long only in Phlebotomus and allied genera. The imagoes are hairy and may present scales but never on their wings, which have a complete venation with the transverse veins near the base, in such a way that the longitudinal veins are very little divergent. Among us, only the females of Phlebotomus suck blood.
Larvae of Psychodidae are aquatic or terrestrial. Those of Phlebotomus are littleknown, because, being undoubtedly all terrestrial, they avoid light and live hidden in the earth, in interstices of rocks or other sheltered places, where they find organic substances to feed upon. Many Psychodidae larvae prefer a little less putrid material; some feed upon algae, Diatomaceae and other small organisms found in purer waters. There are bamboo – and bromeliad-inhabiting species.
Pupae show little motility.
The genus Phlebotomus: of the Psychodidae observed among us, it is the only one that is haematophagous.
As always in the Nematocera, haematophagy is only observed in females.
They are very similar to males, but easily distinguished by the conformation of the posterior part of the body, where there are only two lobes; whereas in the male there exists a complicated prehensive apparatus showing, on either side, a biarticulated dorsal pincer, another ventral piece curved upwards and an intermediary one simple or branched. This apparatus varies in shape and dimensions, and carries elongated claws, bristles and tufts of hair, of varied number and disposition in the different species, which thus can be easily recognized. Females may, sometimes, be classified by the scales and the disposition of hairs on the abdomen dorsum; in a general way, the relative proportion of the palpal articles serves for distinguishing the various species occurring in the same zone. The colour and size of the individuals that have not sucked blood is always less intense, which originated the Brazilian popular name “mosquito-palha” (“straw [coloured] mosquito”). The more or less blackish colour observed in certain individuals is due to the presence of a pigment obtained from previously ingested blood.
Phlebotomus bites are very sensitive. The reaction may be very strong and lasting in persons not immunized by repeated bites.
During biting, these mosquitoes maintain their wings half-opened. By their size and shine, these wings are more conspicuous than the body itself of Phlebotomus.
Phlebotomus may also attack during the day, if in the shadow, but they bite more frequently at dusk and not seldom during the night, if a light is on. They are attracted by light, which allows us to capture them with appropriate traps.
In Rio de Janeiro, two species occur, sometimes found in homes, but apparently more frequent in poultry-yards.
The best known species, and the one that may be considered the type of the genus, is Phlebotomus papatasi, very well studied by Grassi in a well illustrated article. Old World species have been studied by Newstead. There are many isolated descriptions of species found in other regions. Lately, Larousse in France, published monographs of the genus.
In a joint paper with Dr. Neiva in Memórias do Instituto Oswaldo Cruz, I have studied three Brazilian species and given a key, also including Phlebotomus rostrans, described by S. Summers. I give here a copy of it:
1. Hind tibia as long as head and body combined……………… rostrans
1. Hind tibia horter……………………………………………………………. 2
2. Abdominal dorsum with many white scales……………. squamiventris
Abdominal dorsum with long hairs only………………………………… 33 Last palpal article very long…………………………………… longipalpis
Last palpal article not long…………………………………….. intermedius
They show a pair of two-segmented ventral pincers, the apical one with 4-5 arcuate and thick scales in the shape of claws; there is one additional pair of central appendages, constituted by an unarmed, long and arcuate article. Between them there is a pair of intermediary appendages, shorter, and of variable, somewhat more complicatedly shaped.
These appendages show, in well-preserved specimens, a number of hairs, isolated or in tufts.
Afterwards I observed, in a forest in Serra de São Bento, in Santa Catarina, a new species, in which both sexes were more robust and had the longitudinal veins arcuate at the apex.
By the palpi they were similar to Phl. Longipalpis, but the male had the caudal appendages much longer, as one could easily verify at naked eye. The terminal article of the dorsal pincer differed from that of the other species by having five curved bristles, instead of four. All the specimens (some dozens) were sheltered inside an armadillo's lair, and for this reason I have designated them by the name Phl. troglodytes. I did not give a description because I was waiting to find more material, which, however, was not yet possible.
Last year, Larousse described under the name Phlebotomus brumpti a species observed in the north of São Paulo, amidst the forest. It also has a long last tarsal article and five thick and curved bristles on the male's dorsal pincer. If identical to our species, it will be known by Larousse's name. There are, however, certain divergences in the description and in the drawing of the wings to allow us to suppose that it is another species.
Newstead has described a species from Bolivia and Brazil under the name walkeri. It is very close to longipalpis, but differs in the antennae.
Other South American species are: Phlebotomus verrucarum Townsend, from Peru, migonei França, from Paraguay, and teierae Larousse, from Venezuela. There is also a species in Trinidad Island, described some time ago by Knab under the name atroclavatus.
The indigenous names of our species are: birigui, in the South, and tatuquira in the North. The Indian names indicate already that they are indigenous species. Effectively, they are forest inhabitants and can be found in completely deserted places and even at high elevations above the sea. They may appear in cities, but are generally rare and little known. Wherever they are abundant, they attack men, but generally feed upon any vertebrate's blood. Some Old World species often persecute lizards.
In some places the Portuguese names mosquito de palha or asa de palha are used, naturally referring to the yellowish colour of the mosquito.
Ceratopogoninae: The haematophagous Ceratopogoninae are known among us by the names maruim or maruí, when referring to marine species, and mosquitos pólvora in the case of species that do not breed in the sea. Marengoin, used in French, evidently has the same Indian origin. The maruim is called sandfly, or better, mangrove fly in English, and jen-jen, in Cuba. In Paraguay the name of the mainland species is polverino. They are also called midges in England, punkies in the United States and Gnitzen in Germany, but those names are only used there where these small mosquitoes abound.
The Ceratopogoninae, which are small and fold the wing while at rest, are easily distinguished from mosquitoes. Notwithstanding, they do not exceed the length of 2mm, and their bites are most irritating.
The antennae have a discoidal basal article called torus, followed by others, subglobular; only the apical ones are elongated. Their total number is fourteen, not counting the pre-torus, which may precede the torus. Males can be easily distinguished by the basal plumes of the antennae, justifying the name Ceratopogon [bearded horn or antenna], and by the pincers situated on the last segments. They do not suck blood.
The maruim, and some other ten indigenous species more, enter the genus Culicoides, which presents light spots over the dark background of their wings. The membrane of the wings itself is light, but covered with microscopic hairs, whose colour produces those spots, which, in certain positions and with weak magnification, seem very showy.
The genus Cotocripus may be distinguished by having wings densely covered wings with microscopic hairs. The genus Tersesthes has an oviscapt.
Culicoides larvae have the aspect and the movements of nematod worms. They live in the mud of mangroves, in hollows with water and in other water collections.
The larvae of the species from the mainland are unknown.
On their tails, pupae have some organs used to propel the body on dry land. In water they show few movements. Before the ecdysis, the pupa is filled with air, so as to float during ecdysis. Some other times, which seems to be the rule among maruins, the pupa shrinks before ecdysis.
No parasites transmitted by Ceratopogoninae are known, probably because they have a short lifetime and do not repeat the bites very often.
Further details may be found in three articles that I have published in Memórias do Instituto Oswaldo Cruz.
Simuliidae: The family Simuliidae comprehends the sole genus Simulium, represented by numerous species in mountainous regions of all the great continents. They are generally absent from plains, because their aquatic larvae cannot live in waters of little or no current. Simulium seems to be very homogeneous and the first essays to subdivide it gave no satisfactory results, mostly because they have been made based on the knowledge of a limited number of species or because they were based on unimportant characters. These subdivisions, at most, in the present stage of our knowledge, may be considered subspecies or types of groups.
Many inhabitants of Rio de Janeiro know, under the name borrachudo, a small haematophagous dipteron most abundant in mountains. Its bite, better known than its agent, produces a strong itching and opens a hole from which it can be extracted abundant serosity. The serotatic action of the inoculated saliva is very intense, in such a way that a bite on the hand dorsum sometimes produces a swelling of all the region. After many days, the biting points may be recognized by haemorrhagic points. The saliva of this and other species also has a hemolytic power on the blood of some persons and several animals, in such a way that the sucked blood may produce, both in the body and the limbs of the insect, at first a red and afterwards brown to black coloration, due to the haemoglobin and its decomposition. This fact (also observed among species of Phlebotomus) gave rise to the establishment of new species.
The “borrachudo” from Rio de Janeiro has received from Kollar the name pertinax, which I have kept because the species may be identified, not from the description, but from the fact that it is the only one in Rio de Janeiro that became a pest. It has been observed on the coast, from Bahia to Santa Catarina.
Another well known species is the northern pium, which attacks especially people on boats during river voyages, because in that occasion they are not attracted to horses. It has been called Simulium amazonense by Goeldi, but also occurs in the fluvial systems of the São Francisco and Paraná rivers. It is also seen in Peru and has been described under several names.
In Capela Nova do Betim, near Belo Horizonte, I have observed Simulium pruinosum causing serious discomfort by its frequent bites. They even entered houses searching for victims. In the waterfalls of Madeira River, the same was observed for Simulium simplicicolor.
I know some additional eighteen Brazilian species, most of them attacking domestic animals with great intensity. Only exceptionally do they bite people, when larger victims are not available. Species in which females do not need warm blood to mature their eggs are rare.
There are detailed studies about the Brazilian Simuliidae, published by me in Memórias do Instituto Oswaldo Cruz in 1909, 1910 and 1917. The last one refers exclusively to the pium.
Based on those previous works, I will give some notes about simuliids in general and about the species observed among us.
Species of Simulium are generally of a small size; their body length varies between the extremes of 1 and 5mm. The pium is one of the smallest species, with a length of 1.02mm; the common borrachudo ranges from 2 to 2.5mm; few species exceed 3mm. Only scutistriatum sometimes reaches 5mm. The wings, relatively wide, are always hyaline, with reduced and little distinct venation. Together with the short body, the relatively thick and short antennae and legs give the insect the appearance of a small fly, very different from the culicid type. When they try to bite, their flying style reminds that of certain flies or small hymenopterans. Before biting, they are very coy, seeming to look for the right moment and place. Generally they only bite people when not being observed, in such a way that the victims, most often, do not perceive the small aggressors, because the reaction only becomes intense some time after the bite. Borrachudos suck animals up to the point their abdomen becomes completely distended, reaching the size of a small pea. In this state they become almost incapable of flying.
For a characterization of the genus Simulium and, at the same time, of all the family, suffices the following description, given by Schiner in his Fauna austriaca (Vienna, 1864), whose translation I gave in my first article:
Head free, lower face short, proboscis little prominent; palpi with four articles, the basal one short and the apical one somewhat long; antennae short, very thick, with ten articles; male frons so narrow that the eyes almost touch in front, the female frons very wide. Eyes large, reniform, nearly rounded, glabrous. Ocelli absent.
Scutum convex, without transverse suture; scutellum short, semilunar.
Abdomen with seven segments, the first ciliate at margin; anal segment obtuse; genital organs almost always hidden.
Legs relatively short and strong; coxae thick and flattened, metatarsi elongate, the other tarsal articles very short, especially the last; claws glabrous; pulvilli rudimentary.
Squamae rudimentary; halteres exposed, generally bent over abdomen.
Wings long and wide, with thicker veins on the anterior margin, the remainder often barely perceptible. Alulae large, with prominent angle.
I have add here some further characters that may also serve for the distinction of the species.
The female claws have, many times, on their inner side, a small secondary tooth, not always easy to observe; those of the male have an additional exterior tooth.
Not counting a short and little distinct basal article, the palpi have the normal number of five articles.
The wing membrane is covered by microscopic hairs and the costal vein shows spines and cilia of various dispositions. In the legs there may be larger spines and hairs, some of the latter placed on the tarsal dorsum. The tibiae are furnished with spurs, generally more developed on the middle pair, but reduced on the hind one; on the front tibia may exist only one spur and in other cases it is seemingly absent; there are also spurs on the tip of some of the tarsal articles. There are short hairs, mixed up with piliform, narrow and long scales of vivid colour, white or golden. They are found on the top of the head and thorax and also on the legs, where they may become oval. Their form and disposition, as well as their colour, compared to that of their background, serve to characterize some species.
Males are very seldom captured, but may be obtained in large numbers from cocoons. They are smaller than the females and well characterized by the holoptic and divided eyes. Moreover, they have decorative spots of a silvery or mother-ofpearl shine more conspicuous than those in females.
The different species are more easily recognized through the females than through the males, who are very similar to one another.
The largest number of species has imagoes with the bottom of the head and the dorsum of the trunk blackened; the ventral side of the abdomen is generally of the same colour, but it can be a little lighter, chocolate-brown. Legs are, as a rule, mottled in black and yellow; in some places, as well as on the anterior surface of the tibia, the groundcolour may be of a mother-of-pearl white colour, with small, white hairs or scales. In some species the entire body is blackened; in others, the scutum is reddish or frankly red.
Over the black groundcolour there may be mother-of-pearl coloured scales or groups of small hairs, sometimes flattened, or petaloid scales with golden or silvery shine. When these are disposed, on the scutum, in tufts or rows, they become very characteristic in perfectly preserved specimens.
Evolution and biology of the Simuliidae
Eggs of borrachudos are oval-shaped, with the inferior surface flattened, and laid at the margin of running water, on stones or on living or dead leaves and branches. They form a simple layer, white in the beginning, but soon darkened. Larvae mature rapidly and abandon the eggs during the first flood that arrives to bathe them.
Larvae are subcylindrical, with the posterior half somewhat swollen, ending into a kind of sucker; another similar organ ends into a cylindrical process, situated on the ventral surface of the anterior part, where it forms a false foot. Using those two processes, the larva may walk as leeches do. On the head there is also an apparatus to produce a silken thread to fix the larva, abandoned to the current. Once arrived to its chosen place, it becomes fixed only with the terminal sucker and maintains a vertical position within the strongest current, which produces a continuous vibration of the larval body.
The larval head is formed by a chitinous, subglobular capsule, where two ocellar spots are distinguished, one pair of antennae, two combs of pinnate, fan-shaped bristles, one pair of mandibles, one pair of maxillae and a labium, also called the mentum plate. The action of the combs is to lead solid bodies suspended in the water to the mouth, where they are used as food. These consist of debris of every kind and small organisms, both animal and vegetable. In the stomach content, Diatomaceae and other small algae are easily recognized.
On the posterior end there are ramified blood gills, in a ventral position, when not hidden in the rectum. Part of the respiration must be cutaneous. With one exception, I have always found the integument glabrous and transparent, which permits the recognition of the respiratory filaments of the pupa, found near the head during the last larval phase. Wrapped up beneath the integument, they form a black rounded spot. The head is ochre-brown, the body greenish or reddish, in some species becoming dark-olivaceous or blackened.
Wherever small waterfalls are found, larvae may be easily found too, either on plants or on dried branches bathed by the current. Hedychium coronarium, Eryngium, popularly known as “toucan's tongue”, bamboos, reeds and grasses growing near to or inside the water furnish good supports for the larvae on the stems, branches and leaves that resist for a long time to the action of the water. Podostemonaceae (fixed to stones of waterfalls by means of adhesive organs) serve as support for the larvae and cocoons of the pium, and of the Simulium orbitale. Larvae of the common borrachudo may be found on the stones, as well as those of S. rubrithorax, pruinosum and obesum, which form large colonies, where the gregarious larvae are protected by a real web of silken threads.
In still water, larvae do not resist for more than 24 hours, but with artificial ventilation or agitation of the water they may be preserved for a longer time, allowing the observation of their metamorphosis.
In determining the larvae, size, colour and certain structural details may be used; however, only last stage larvae permit an easy diagnosis of all species, based on the shape and ramification of the breathing tubes of the pupa, which can be extracted and unwrapped.
Pupae have a conical shape and consist of a membranous envelope, within which, little by little, it transforms itself into the perfect imago.
They are usually found placed inside a cocoon, open on its superior part and having, more or less, the shape of a paper funnel, flattened against the support. They are formed by silken threads, very distinct or agglutinated. In a few species, the cocoon is substituted by a web of irregular threads, a mere rudimentary sketch of a cocoon. The shape and the structure of the cocoon are themselves already very characteristic, but the pupa presents characters that permit the distinction of species far better than the imago itself. They consist of dark, flat or prominent granules, simple or composite hairs, and breathing tubes forming the appendices already mentioned, which permit the easy distinction of almost all species. The imago, seldom formed, has its ecdysis beneath water. It generally has to wait until the cocoon becomes exposed, in consequence of dry weather. By choosing very dark cocoons and leaving them inside a humid receptacle, one obtains many imagoes, which emerge during the first days after being collected, when exposed to light. By isolating the cocoons with known characters, one may determine afterwards to which species corresponds each pupal form, as well as to which kind of pupa corresponds each species of adult larva. With such knowledge, one can determine the local fauna just by examining the mature larvae and pupae, which may be even empty or little-developed.
There are two types of breathing tubes. The first, observed in S. tulibranchium, auristriatum and in some exotic species, shows a small number of very wide and little ramified tubes. At first sight they seem to differ completely from the second type. It is observed, however, in very similar species.
The fact that it does not show segments, but only very fine and spaced scales or spines, clearly indicate that here it is only represented the basal part of the respiratory appendices, which has assumed an extraordinary development and acquired the function of the segmented tubes.
The latter are well-developed in the second type, and, although closed at the apex, represent tracheae. They are bi- or tri-furcated on the base and each stem is subdivided in branches whose number greatly varies, being however constant within each species. The total number of branches may correspond to even numbers from 4 to 14, 6 and 8 being more frequent. Above 14, it may occur a larger number of branches, which customarily are not counted, the mere definition “many” being sufficient. The length, thickness and form of the apex of the branches also constitute distinctive characters. The spaced sensitive hairs on the anterior part of the pupa may be simple, bifurcated or ramified. The ensemble of these characters permits an easy distinction of most species.
Only when there are six or eight branches on either side, a more detailed study is needed to determine the species.
Pathogenic role of simuliids
It has not been proved yet that simuliids transmit some human disease. On a work about pellagra, the author himself, Sambon, seems to have abandoned the idea that this disease is inoculated by simuliids and, in the case of leprosy, they could, at most, play a very secondary role. It would be easier for them to inoculate some domestic animal disease, but there is no evidence of this fact and we do not even know whether they repeat their bites during sufficiently long intervals to let parasites with complicated evolution mature.
On the other hand, it is perfectly established that, surging in great swarms, they may cause cattle mortality. Bites in great number may kill the animals, either by intoxication, or by asphyxia, because not even the mucosae are spared. Even human victims have been reported. In the United States turkeys are also victimized by a species of Simulium.
Mortality of equine and bovine cattle has been frequently observed in Hungary and the United States, and lately also in Germany. Among us fatal cases are not known, but equines suffer much in certain mountainous regions, where they are persecuted by simuliids attacking different regions of the body. Some attack especially the inner surface of the ears, where they produce a tumefaction and chronic scaling, constant in equines of certain regions, at least during summer. Other species seek the orbital margin and some choose the mane or the belly of horses, where they frequently cannot be observed, even when abundant.
Simuliid mouthparts are well developed, and even in males (which do not suck blood) all the pieces are present. In the palpi, the last two articles are ring-like and in the antepenultimate there exists a dome-shaped organ.
To finish, I give a succinct description of the two most important species.
Simulium amazonicum Goeldi, 1905
Syn.: minusculum Lutz, 1910, nitidum Malloch.
Popular name: Pium
♀ Head: Groundcolour black, covered with bluish-grey pollinosity with silvery shine. Antennae black with ochre-coloured base; palpi dark-brown. Little hairs and piliform scales of head golden or silvery.
Thorax: Scutum furnished with piliform golden scales over dark background; silvery, over white background.
Thorax black in groundcolour, with bluish-grey pollinosity with silvery shine. In fresh specimens three longitudinal velvety-black stripes may be perceived.
Between the anterior part of these stripes there two subtriangular spots, at times black, other times snow-white, according to the incidence of light.
Abdomen: Dorsum with three transverse spots over a black background. Venter corrugated in the longitudinal sense.
Legs: In unfed individuals the fore tibia, the entire middle leg and the base of the hind tibia ochre-coloured; metatarsi and tarsal articles with light base. The remainder groundcolour blackish, with oblanceolate, white and black scales. These are translucid and very deciduous, but are easily perceptible when the background has a different colour. Claws unarmed, black, with a light base.
Wings with the larger veins ochre-coloured. Halteres with yellow capitulum.
Female length from 1 to 2mm.
Males may be distinguished by the sexual characters and are generally somewhat smaller.
Pupae were never found on stones, but I have found many cocoons on Podostemonaceae in waterfalls of the São Francisco river, a little above the city of Juazeiro. It is 2.5mm long. The mouth is oblique, with semilunar margin, somewhat reinforced. The walls consist of brownish silken threads with very large interstices. From the part in contact with the support there is only the lower half. The pupa has a very thin integument; the anterior part is reinforced by fine granules and furnished with short trichomes, generally bifurcated. The branchial apparatus has the same length of the pupa and begins, on both sides, by a thick tube immediately forming two branches. The posterior branch forks again into two branches, which later form other bifurcations, the dorsal being a little above the middle one. The ventral branch divides itself much further above. The branches gradually tapered; the six terminal branches ending into a subconical tip.
The larvae are distinguished only by their very light colour and their small size.
Simulium pertinax Kollar
Syn.: S. inexorabile Schrottky
Popular name: Borrachudo.
(In my first publication I used the name S. venustum, due to the certainly mistaken determination made in Washington. Both its origin and its first stages show that we are dealing with another species.)
♀ Head and body blackish. Antennae with somewhat lighter base. Eyes green. Hair-like scales on scutum not flattened, neither forming tufts. Their colour golden, slightly reddish. Venter, when empty, showing two longitudinal folds. Coxae and trochanters blackish. Femora ochre-coloured (more or less infuscated after absorption of blood). Fore tibia with dark apex, with an ochre groundcolour on the remainder, covered with white pruinosity and small hairs. Hind tibia as the middle one, but with largely black apex. Fore foot black. Hind ones with white metatarsus, with only the tip black. Tarsi with their basal part lighter. Female claws toothed at base. Body length, 2-2.5 mm, after feeding, up to 3mm.
Male somewhat smaller, with eyes united and trifid claws. In both sexes there are no petaloid scales.
Larvae greenish, forming colonies on rocks of rapid rivers. They abound, for instance, above Cascatinha da Tijuca and in a creek that comes down from Gávea.
The brown silken cocoon of the usual shape. The nymph has, on both sides, 8 respiratory tubes started from three branches. The foremost bifurcated; the hind ones with two bifurcations, one upon the other.
Haematophagous Nematocera
GENERAL CHARACTERS OF THE FAMILIES
