Myiasis in Man and Animals in the Old World: A Textbook for Physicians, Veterinarians and Zoologists

f. Cragg (1955, 1956) and Cragg and Cole (1956); ::,^. Figure 55. Posterior vie see also the summarizing notes by Hall (1948).

^-

1949),’

of larva of Lucilia cupri,

(Weidcmann)

Pathogeneszs In many areas of the world L. sericata is known as a primary producer of sheep myiasis, either alone or at 49

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES from the nose (Symes and Roberts, 1932). Such cases,

rot.

Wet weather, hard driving or improperly-trained

dogs may cause the animals to sweat, stimulate bacterial growth, and thus pave tlie way for fly attack and oviposition. Larvae in the wool may remain either on the skin surface, causing comparatively little damage except to the fleece, or they may bore inward with more serious consequences. Pre-existing wounds, even small ones, favour the facultative parasitism of the maggots.

Some breeds of sheep

are more

susceptible

to strike

than others. Large numbers of larvae hatched in the fleece are more dangerous than only a few, and they will almost invariably burrow deeper. The larvae also migrate in search of a soft or more easily invaded part, such as the flanks or the fleshy part of the haunch. Most frequently sheep are struck in the breech and around the tail, where the skin is contaminated. Lambs and shorn sheep are less liable to attacks, but when struck they usually suffer a much more extensive invasion of the tissue. The lesions and the maggots irritate the animals, they do not feed properly and become poor in condition. Death may occur within a few days, but is probably due to a toxaemia and even septicaemia. The maggots of L. sericata are also well-known as facultative wound parasites in animals other than sheep, mainly cattle and horses, and in humans where they normally behave in quite a benign way. They remain restricted to the dead tissue and moreover stimulate the healing process. This observation, as already mentioned in the section on history, has led to their use for surgical purposes, especially for the treatment of osteomyelitis wounds. The beneficial effect of the larvae is due to the secretion ofallantoin as proved by Robinson (1935). If, however, not enough necrotic tissue is available, the maggots start to invade the healthy tissue (Stewart, 1934). It may be that strains exist which show more malignant attitudes than others. Larvae of-L. sericata have also been discharged from the ear of humans (Platt and Scott, 1935; Smart, 1936) and

50

which are rarely observed, actually represent only special form of wound-myiasis.

a

Distribution L. sericata is a very common fly in the more temperate Holarctic region. In the Southern hemisphere, however, it has probably been introduced only in historic times, and from many parts it has not yet been recorded, but may appear sooner or later as a notorious follower of man. In some sheep-farming areas of the Southern hemisphere, it has become, in addition to indigenous species of blowflies, less important producer of - a- more - or -sheep-strike, as in South Africa, Australia and New Zealand. areas of the

"

’

least as the most important species. These countries are Great Britain (Davies, 1934; Ratcliffe, 1935; Haddow and Thomson, 1937; MacLeod, 1937, 1943), Holland (Baudet and Nieschuiz, 1933), Baluchistan (Janjua, 1939). In other parts of the world, such as in South Africa (Hepburn, 1943), Australia (Waterhouse and Paramonov, 1950), and New Zealand (Macfarlane, 1942), it is of minor importance, and the place of chief myiasis producer is taken over by other species of blowflies, while L. sericata often acts as a secondary invader, A summary of sheep-strike in Scotland by L. sericata is given by Haddow and Thomson (1937). Positive knowledge as to the exact reasons for primary strike is still lacking, but several important predisposing causes have been reported. The main initial cause is the bacterial activity in the wool, which is especially stimulated by contamination with urine and faeces. Where the wool is kept moist by water and sweat, the bacteria produce decomposition of the fibres, the so-called wool-

2. Lucilia cuprina (Wiedemann)Sheep Green Bottle

Musca cuprina Wiedemann, Auss. ^weifl. Ins. 2, 1830, 654. Lwilia cuprina Seguy, Encycl. ent. {A) 9, Aubertin, Linn. Soc. J. Zool. 38, 1933, 413, figs. Waterhouse and Paramonov, Ausf. J. sci. Res. {B) 3, 1950, 310, figs.; Zumpt, Flieg. pal. Reg. 64i, 1956, 46, figs. Phoenicia cuprina Kano and Sato, Jap. J. exp. Med. 22, 1952, 36, figs. Lucilia dorsalis Rob.-Desvoidy, Ess. Myod. 2, 1830, 453; Waterhouse and Paramonov, Austr. J. sci. Res. {B} 3, 1950, 310. Lucilia argyrocephala Macquart, Mem. Soc. Roy. Agric. Arts Lille 1846, 326; Malloch, Ann. Mag. nai. Hist (9), 17,1926, 506. Lucilia pallescens Shannon, Insec. Inscit. menst., 12, 1924, 78. Phoenicia pallescens Hall, Blowflies of N. America 1948, 247, figs. Lucilia sericata Smit (nee Meigen), Sci. Bull. Dep. Agric. S. Afr. no. 62, 1928, 1; and Rep. Dir. Vet. Serv.

1928’, 159,’figs.;

Onderstepoort 1931, 299, figs. For further synonyms and taxonomic references

see

Zumpt (I956a). History L. cuprina was, like L. sericata, originally described under Musca^ by Wiedemann in 1830 from China. Later authors then transferred it to Lucilia. In contrast with L. sericata, it remained unknown to the medical and veterinary world until the early thirties of this century, when Australian scientists accumulated a considerable amount of evidence showing that L. cuprina was the most important sheep blowfly on this continent, and not L. sericatOy which had been confused with it by former authors. Basing his work on these findings, Hepburn (1943) demonstrated that exactly the same situation was encountered in South Africa, and that almost all former records of-Z-. sericata as a sheep myiasis fly in South Africa had to be read to refer to L. cuprina, also for instance the major contribution by Smit (1931). However, Roubaud (1914) had already reported that L. argyrocephala was an important producer of cutaneous mviasis in man and domestic animals in West Africa and the genus

SUBORDER: BRACHYCERA

Figure 56. Lucilia cuprina (Wicde-

mann). Cephaloskeleton, anterior spiracle and posterior peritremal plates of third larval stage. Kano and Sato)

in Abyssinia, but not L. sericata, and in 1926, Veneroni reported the same from Somaliland. Neither author knew that L. argyrocephala was a synonym of L. cuprina, but they were aware that it differed from L. sericata in morphological as well as biological respects. The modern literature on L. cuprina is extensive due to the great economic importance of this fly, and only the most important papers will be mentioned in the following paragraphs, from which further references may be taken. The basic taxonomic paper is again that by Waterhouse and Paramonov (1950) already quoted under L. sericata, but the splitting of the species into two subspecies, namely L. cuprina cuprina (Wiedemann) and L. cuprina dorsalis Rob.-Desvoidy has not been accepted by later

authors.

Morphology ImagoAdults which are reared from larvae in wounds should always be carefully compared in both sexes with L. sericata. The males of the two species are easy to separate from one another by the great differences in the abdominal ventral hairs; and if there are any doubts, the comparison of the hypopygia will give a clear answer. For separating the females, only fully-hardened specimens should be used,

(After

Larva ISpinulation similar to L. sericata., but segments X and XI with complete posterior bands. Larva IIDistribution ofspinules similar to the first stage, but segments VIII and IX show complete bands at the anterior margins. Anterior spiracles usually with five branches.

Larva III (Fig. 56)Compared with L. sericata, segment X generally also has one or two rows of spinules dorsally. With respect to this spinulation a certain variability seems to exist, especially when specimens from different localities are compared with one another. This is also true for the shape of the ventral cornuae of the cephaloskeleton which Waterhouse and Paramonov (1950) used for separating the third larval stages of L. cuprina and L. sericata.

which have the fore-femora bright metallic green in L. cuprina. Other useful differences lie in the width of the irons in both sexes, and in the number of the occipital

hairs. Metallic green, blue or coppery flies caught on the wing and suspected of being L. cuprina or L. sericata, or any other blowfly of veterinary importance, should be sent to a

specialist for identification. Egg as in Lucilia sericata.

Figure 57. Myiasis in sheep due to Lucilia cuprina (Wiedemann). (Reproduced by courtesy of the Veterinary Research Laboratory, Onderstepoort}

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Reliable features, however, seem to be provided by the arrangement of the tubercles on the upper posterior cavity and, in fully sderotized specimens, by the structure of the peritremal ring. In L. cuprina the distance between the inner tubercles is approximately equal to the distance between the inner and outer tubercles, and the peritremal ring lacks the inner projection.

Biology L. cuprina is in its life-history similar

to

play

L. sericata, but

it inhabits the drier and warmer parts of Africa and Asia. Its introduction to Australia and to the New World is

probably quite recent. The bionomics in South Africa were studied by Smit under the name of L. sericata. L. cuprina breeds there in carrion almost continuously throughout the year, and 9-10 generations may be completed within one year. The incubation period of the eggs lasts from 8 hours to 3 days. The shortest feeding period of all three larval stages together was 2 days, but under cooler or otherwise less favourable conditions, it may take up to three weeks. The mature larvae leaving the carrion may burrow into the soil immediately, where the puparium is formed after a few hours, or they may crawl around for days or even weeks, before they come to rest as prepupae. The final formation of the puparium again may take a few hours only, or several days to weeks. The pupal stage was found to last 7 days in summer, but up to 115 days in winter. Unfavourable conditions in the dry and cold season are overcome in the prepupal, pupal and more rarely in the adult stages. The flies do not oviposit in winter; from spring to autumn they produce on the average 1,000 eggs per female. The maximum life-span of a fly in summer is about one month, but at lower temperatures it may be extended up to 3 months. About the superiority of the survival value in carrion of L. cuprina over other blowfly larvae in South Africa, see Ullyett (1950). L. cuprina is the most important sheep strike fly in South Africa and in Australia (see also Norris, 1959), especially to Merino breeds which with their dense fleece are very attractive to the ovipositing flies under certain circumstances. The larvae feed on the epidermal cells, the extravasating lymph and the necrotic tissues, but they do not flourish on this diet as well as on meat (Fiedler,

(1931)

1951).

.

Necrotic tissues in wounds of other animals and of humans are equally attractive and allow a complete development of the larvae. The flies are often found feeding on fallen fruit, the nectar of flowering plants, and on the honeydew of aphids, but for maturing the eggs the females need a protein meal, which can be provided, in the absence of carrion, by feeding on the faeces of sheep and other animals

(Webber, 1958). Paihogenesis L. cuprina is the principal blowfly causing sheep strike in South Africa and in Australia, and it is also known to

a role as a myiasis-causing agent in domestic animals and in humans in Rhodesia, Kenya, Uganda, Abyssinia, Somaliiand, in parts’ofWest Africa, and in India. In South Africa, in over 90 per cent of sheep strikes the larvae of L. cuprina are the primary invaders (Hepburn, 1943), and in Australia the percentage, varying with the different areas, also lies between 60 and over 90 per cent (Mackerras and Fuller, 1937). The pathogenesis of L. cuprina in S. Africa has been discussed in an excellent paper by Fiedler (1951). The relevant chapters may be quoted in English translation : ’ In a several-day-old infestation by L. cuprina the following picture may be seen. The parasitized sheep is restless, stamps its hooves, and bites or rubs the affected areas. Externally these show a dark discoloration of the wool, which when palpated is moist, due to the strong secretion of lymph. If the wool staple is opened the larvae are found singly, and often also in greater numbers, in round pockets which they have made in the wool. At the slightest disturbance, for instance exposure to direct sunlight, the larvae immediately crawl deeper into the wool. ’ In all cases it is surprising that the majority of the larvae, depending on the length of the neece, are situated several centimetres away from the skin in exudatesaturated parts of the wool. Furthermore, below the soaked fleece large areas of the epidermis are eaten away, and thus resemble superficial, moist wounds. At a later stage the wool in these areas falls out completely, and an open skin wound the size of a dinner plate is often found, which then shows a tendency to dry out. In the meantime the larvae have migrated to healthy skin areas. These are then attacked in the same manner as before until the larvae fall off for pupation on the ground. ’ Extensive histological changes of the skin take place due to the larval infestation. The epidermal cells are dissolved and removed within a short time by the action of the alkaline proteolytic enzyme. The superficial cell layers of the dermis may disappear in a similar way. After reaching this stage the activity of the larvae stops, but the action of the secreted digestive juices continues for some time. An inflammation of the affected skin results, in which the dermis undergoes extensive thickening coupled with hyperaemia. Similarly a leukocytic infiltration between the hair follicles takes place. ’ This inflammatory process is the cause of the abovementioned excessive lymph exudate. As long as the wool remains on the affected areas and the enzymatic action of the digestive juices continues, no scab is formed, and necrosis of the upper cell layers sets in. These are again attacked by the larvae, and although granulation tissue is rapidly formed, the wound does not heal. Only after the sheath of the fibre has been damaged to such a degree that the wool falls out do the larvae finally migrate into the surrounding healthy wool. The damage to the dermis, however, never goes so deep as to destroy the papillae, so that after the wound has healed new growth of wool

again sets in. ’ As shown by Bull (1931) similar inflammatory

52

SUBORDER:BRACHYCERA reactions, and also purulent conditions, result from the continuous irritation of urine and liquid faeces, especially when these areas are situated between folds of skin. They are ideally prepared for attack by primary myiasis

1883, and it is most probable that L. cuprina was introduced to this continent from South Africa during the last

flies.

3. Lucilia richardsi CollinRichards’ Green Bottle Lucilia richardsi Collin, Trans. R. ent. Soc. Lond. 1926, 259; Seguy, Encycl. ent {A} 9, 1928, 157, figs.; Aubertin,

Generally speaking, the affected areas have no typical putrefactive odour, and only when bacterial decomposition the lymph which has entered the fleece takes place, is of this unpleasant odour given off. Other L. cuprina females are quick to lay their eggs in these favourable spots. Secondary flies which complete the destructive work are attracted as soon as a larger wound, with its putrefactive odour indicative of decomposing animal proteins, is ’

formed.’ Even a small infested area of the skin disturbs the sheep considerably and its body-temperature rises quickly to 41 C and more. As in the case of L. sericata strike in Great Britain, a spread of the infection worsens the condition very quickly and death may occur within a few days. The fact that L. sericata does not play an important role as primary invader in sheep strike in S. Africa and in Australia may be due to several factors, of which the climatic conditions certainly are of great importance. Another reason may be that the larvae of L. sericata are perhaps not able to digest the intact epidermal layers as described by Fiedler, and that the so-called wool-rot is of decisive importance in moist and temperate areas. However, in the temperate winter-rainfall area of the Western Cape, L. cuprina is also the principal sheep myiasis fly, and not L. sericata (Monnig and Cilliers, 1944), so that no satisfactory explanation can yet be given. An interesting and well-known observation is that in areas where both Lucilia species occur, the presence of young L. cuprina larvae stimulates the oviposition of L. sericata. There are several records of L. cuprina causing a traumatic myiasis in animals other than sheep and in humans. Roubaud (1914) briefly mentioned a case in a dog and one in a man from West Africa, and attacks on camels in Abyssinia; Veneroni (1926) says that in Somaliland larvae have been found in wounds of man, dogs, goats and cattle, and Patton (1921) refers to L. cuprina as being common in India and known to lay eggs occasionally in the diseased tissues of animals. A case of cutaneous myiasis in a bullock in Australia is recorded by Wilkinson and Norris (1961). Hopkins (1944) mentioned six human cases from Uganda. In four instances the larvae were from wounds, in one case from an arm burnt by lightning, and in another from an ear injured by burns.

century.

Linn. Soc. J. Zool, 38, 1933, 416, fig.;

Zumpt,

Flieg.pal. Reg. 64i, 1956, 53, figs. (nee Meigen), List. Brit. Dipt.

Lucilia splendida Verrall

1901, 27. Lucilia pilosiventris Richards Soc. Lond. 1926, 27.

(nee Kramer), Trans. R.

ent.

History This species was formerly confused with L. sericata and species, and only in 1926 did Collin succeed in clearing its status. It is quite common in Great Britain, in Finland and in France, and has been recorded also from several other European countries. The adults are separable from L. sericata mainly by the greater number of antero-dorsal bristles on the mid-tibia (see Zumpt, 1956&). As in all Lucilia species, the male terminalia are characteristic. The immature stages, which are found in carrion, are not described. some other

Pathogenesis Nuorteva (1958) records a case of traumatic myiasis in the European Nightjar (Caprimulgus europaeus) from Finland. 4. Lucilia caesar (Linnaeus)European Green Bottle

Musca caesar Linnaeus, Syst. Nat.^ ed. 10, 1758, 595. Lucilia caesar Rob.-Desvoidy, Ess. Myod. 2, 1830, 452; Seguy, Encycl. ent. {A} 9, 1928, 152, figs.; Aubertin, Linn. Soc. J. Zool. 38, 1933, 400, figs.; Spence, Proc. R. ent. Soc. Lond. (B) 23, 1954, 29, figs.; Zumpt,

Flieg. pal. Reg. 64i, 1956, 45, figs. Musca splendida Meigen, Syst. Beschr. zweifl. Ins. 5, 1826, 56. Somomyia jeddensis Bigot, Ann. Soc. ent. Fr. (5) 7, 1877, 255. Lucilia angustifrons Townsend, Smithson Misc. Coll. 51, 1908, 120. History Lucilia caesar, already described by Linnaeus, was generally considered by former authors to be a species with a very wide distribution, including North and South America, Australia and New Zealand. This is not true,

Malloch first indicated in 1927 and Aubertin later confirmed when revising the genus Lucilia on a worldwide basis. L. caesar is actually restricted to the Palaearctic region, and all records from other zoogeographical regions go back to misidentifications. Also with respect to records from the Palaearctic region, L, caesar has often been confused with other species, especially, for instance, with L. illustris^ and records before Seguy’s work (1928) and Aubertin’s paper (1933) should be used with caution.

as

Distribution L. cuprina is a common fly in the Ethiopian region and

originally

most probably an African element which then invaded the Near East, India and some other tropical of parts the Oriental region. Its introduction to Australia is of recent date, and the same may be true for Hawaii, islands in the Pacific Ocean and for the New World. There are no records of sheep strike in Australia before

53

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Morphology ImagoMetallic green or bluish flies of 6-11 mm in length. The male is readily recognizable by its big, bright metallic hypopygium, which is small in the related L. illustris^ and blackish to dark green. The hypopygial structures of the two species are quite different, and when mounted, no confusion with any other species should be possible (see Zumpt, 19566). The separation of the female, however, is difficult and better left to the expert.

L. caesar from N. America before Hall (1948) for instance refer mostly to L. illustris.

Larval stages I-IIINo accurate description of the larval stages seems to exist in the literature; that given by

Larval stages I-III (Fig. 58)All three larval stages have been adequately described by Kano and Sato (1952). The third stage is characterized by its cephaloskeleton, which has a pigmented area below the posterior extremity of the ventral cornua, but an accessory oral sclerite is lacking. The distance between the inner tubercles on the upper margin of the posterior cavity is approximately equal to the distance between the inner and the outer tubercles. The posterior peritremal plates are similar to those of L. sericata.

James (1947)

is inadequate. Dr. Kano kindly sent me a few third instar larvae from Japan, labelled L. caesar. The preparation of the cephaloskeleton and the posterior peritremal plates did not show any significant differences from L. illustris.

Biology L. caesar is a carrion breeder. Pathogenesis

L. caesar has been reported from the British Isles to be involved in cases of sheep myiasis. Haddow and Thomson (1937) regard it as a secondary invader, after L. sericata have struck the host. But MacLeod (1937) suggests that L. caesar ’ is a true primary species which, however, rarely acts in this capacity, not because it is unable to do so, but because its range of attracting odours is more limited than that of L. sericata, or possibly is seldom, trespassed on by healthy sheep under normal conditions ’. L. caesar is also reported as a myiasis-producing fly from Tripolitania (Onorato, 1922), from Northern Russia (Portschinsky, 1916), and from Switzerland by Galli-Valerio (1939), where it is said to have caused wound-myiasis in man. Distribution

Widely distributed in the Palaearctic region, but evidently more common in the Western parts than in the East. 5. Lucilia illustris (Meigen)

Musca illustris Meigen, Syst. Beschr. zweifi. Ins. 5, 1826, 54. Lucilia illustris Seguy, Encycl. ent. [A) 9, 1928, 153, figs.; Aubertin, Linn. Soc. 7. Zool. 38, 1933, 402, fig.; America 1948, 224, figs.; Kano and Sato, Jap. J. exp. Med. 22, 1952, 34, figs.; R. Soc. Proc. Land. {B} 23, 1954, 29, figs.; ent. Spence, Zumpt, FUeg. pal. Reg. 64i, 1956, 46, figs. Musca parvula Meigen, Syst. Beschr. s.weijl. Ins. 5, 1826, 55. Musca equestris Meigen, Syst. Beschr. yoeifi. Ins. 5, 1826, 57. Musca muralis Walker, List Brit. Dipt. Mus. 4, 1849, 888. Calliphora simulatrix Pandelle, Rev. Ent. Caen 15, 1896, 218. Lucilia purpurea Townsend, Smithson. Misc. Coll. 51, 1908,

Hall,

Blowflies of N.

Morphology AdultSimilar to L. caesar, but both sexes are well characterized by the structure of the male hypopygium and the female ovipositor. With some experience, the relative length of the third antennal segment is also of use. For further details see Aubertin (1933) and Zumpt

(19566).

Biology L. illustris is a carrion breeder, and the adults appear in the early spring. In North America, Japan, and in Finland, it is a very common species. In other parts of Europe it is evidently rarer, but certainly still often confused with L. caesar. Under fairly high temperatures the larval period lasts from 2 to 5 days, and the puparia may be formed from 3 to 12 days after the larvae have hatched from the eggs (Hall, 1948).

Pathogenesis Haddow and Thomson (1937) found L. illustris involved sheep myiasis in Scotland as a secondary invader in three cases. The primary invader was L. sericata.

in

Distribution L. illustris is a Holarctic fly and distributed from North America through Europe to the Far East. It is not known from the Mediterraneum and does not occur in the Ethiopian region. Sen.-White, Aubertin and Smart (1940) mention it from the Indian Himalayas and from

Rangoon. 6. Luctlia ampullacea Villeneuve

Lucilia ampullacea Villeneuve, Bull. Mus. Hist. nat., Paris 28, 1922, 515 ; Seguy, Encycl. ent. {A} 9, 1928, 148, figs.; Aubertin, Linn. Soc. J. Zool. 38, 1933, 403, fig.; Kano and Sato, Jap. J. exp. Med. 22, 1952, 33, figs.; Spence, Proc. R. ent. Soc. Lond. (5) 23, 1954, 29, figs.; Zumpt, Flieg.pal. Reg. 64i, 1956, 44, figs. Lucilia flauipennis Kramer (nee Macquarc), Abh. naturf. Ges. Goriitz 1917, 283. Lucilia krameri Seguy, Encycl. ent. B II Dipt. 2, 1925, 94.

History

122. History As the list of synonyms reveals, this species has been described several times, and it has been confused with other species, especially with L. caesar. Records of

54

This is another species which was confused by former authors with L. caesar, until Kramer examined the male genitalia. "Unfortunately, the name he gave was already preoccupied by flavipennis Macquart, which is today one of the numerous synonyms of L. sericata,

SUBORDER: BRACHYCERA

Figure 58. Lucilia UlustTis (Meigen). Cephaloskeleton, anterior spiracle and posterior peritremal plates of third larval stage. {After Kano and Sato)

Morphology AdultThis species is very similar to L. porphyrina and L. papuensis of the Far East and only recognizable with certainty by the male terminalia (see Aubertin, 1933, and

Zumpt, 1956&).

Larval stages l-lll (Fig. 59)The larval stages have been described by Kano and Sato (1952). The third

stage is characterized by the cephaloskeleton having a pigmented area below the posterior extremity of the ventral cornua as in L. illustris, but in addition to it; an accessory oral sclerite is developed as in species of Calliphora. The anterior spiracles have six to nine branches. Posterior spiracles with an inner peritremal projection. Distance between the inner tubercles on upper margin

lorsal

.

,

,

Cephalopharyngeal sclente Figure 59. Lucilia ampullacea Villeneuve. Cephaloskeleton, anterior spiracle and posterior peritremal plates of third larval stage. {After Kano and

Sato) Anterior spi raci

55

Pigmented area

cornua

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES in 1891 also reared adults from a case of myiasis in a toad, but identified them as L. silvarum (Meigen). This was probably a misidentification and the flies he obtained were L. bufonivora, but since then several other authors have referred cases of toad-myiasis to L. silvarum, and it is still an open question whether this species, which is very

of the posterior cavity approximately equal to the distance between the inner and outer tubercles.

Biology L. ampullacea breeds in carrion.

similar to L. bufonivora, may perhaps also cause myiasis in amphibians. In my revision of the CalHphorinae of the Palaearctic region (Zumpt, 1956A), I expressed the opinion that both species may act as myiasis producers, but I now incline to the view that probably only L. bufonivora is the actual producer, and that all records referring to L. silvarum, including that by Hall (1948), may be due to a confusion of these two species (see also

Pathogenesis Heim de Balsac (1937) records a case of traumatic myiasis in a young specimen of the Fat Dormouse {Glis glis} in France.

Distribution

L. ampullacea seems

to

be quite common in the Far

East, but of rarer and more patchy occurrence in Europe. According to Sen.-White, Aubertin and Smart (1940), Dodge, 1952).

An important paper on the morphology and biology bufonivora is by Brumpt (1934), who succeeded in clearing up the major facts of the life-history of this obligatory parasite of toads and other amphibians. No important contributions have been made since then by

it is also known from Algeria, Northern India and Australia, but the latter record is very doubtful.

of L.

7. Lucilia porphynna (Walker)

Musca porphyrina Walker, J. Proc. Linn. Soc. 1, 1857, 24. Lucilia porphyrina Aubertm, Linn. Soc. J. Zool. 38, 1933, 408, fig.; Thomas, Proc. ^ool. Soc. Lond. 121, 1951, 173, figs.; Zumpt. FHeg.pal. Reg. 64i, 1956, 50, figs. There are a great number of synonyms to this species, which are listed by Zumpt (1956&).

other authors. Aubertin (1933) wrote that the North American Lucilia elongafa Shannon was a synonym of L. bufoniuora. This was strongly objected to by Hall (1948) for morphological reasons, and also a paper by James (J". Wash. Acad. Sci. 37, 1947, 366) on the life-history of this fly suggests that the two species are actually distinct. James found larvae of L. elongata parasitizing the toad Bufo boreas Baird and Girard, but in quite a different way from that which is known for L. bufonivora.

History This species is very similar to L. ampullacea and separable from it mainly by the structure of the male and female terminaHa. It is a common fly in the Oriental region. The larvae develop in carcasses, and the adults are frequent visitors to human dwellings. In India, Dasgupta (1962) found that eggs are occasionally laid on the common Asiatic Toad {Bufo melanostictus}. The larvae hatch out of the eggs in about two days and produce deep lesions which sometimes reach the paratoid gland. Also pre-existing wounds of the toads are attacked. The toads soon die and the maggots continue feeding on

Morphology ImagoThe adults of£. bufonivora are very similar to those of L. silvarum, which seems normally to have a saprophagous mode of life. Both species are characterized by two or more fairlv long marginal bristles on abdominal tergite III, in connection with a blackish basicosta of the wing. L. bufonivora normally shows only two pairs of post-sutural acrostichal bristles, and L. silvarum has three

the carcass. 8. Lucilia

bufonivora MoniezToad Bottle Bull. sci. Depart. Nord. 8, 1876, 25; Seguy, Encycl. ent. {A} 9, 1928, 150, figs.; Aubertin, Linn. Soc. J. Zool. 38, 1933, 419, fig.; Brumpt, Ann. Parasit. hum. comp. 12, 1934, 81, figs.; Schumann, Wiss. Ztschr. Univ. Greifswald 3, 1954, 256, figs.; Zumpt, Flieg. pal. Reg. 64i, 1956, 44, figs.

Lucilia

bufoniuora Moniez,

History The first observations on fiy-maggots parasitizing the head cavities of toads were made by the forester Dr. Urversen in Bohemia and published in 1865 by Boie. A year later Weijenberg discussed similar cases from Holland, and in 1870, La Fontaine wrote in a book on reptiles and amphibians in Luxemburg, that myiasis in toads was quite common in August and September, and that it ended fatally. Moniez (1876) succeeded in rearing the adults and described the fly. Since then, several more cases have been recorded (see Brumpt, 1934). Dunker 56

Figure 60. Hatching larvae of Lucilit Brumpt)

bufonivora

Moniez.

(After

SUBORDER: BRACHYCERA pairs. This feature, however, is variable in both species, and the separation is therefore possible with certainty only by dissecting the male genitalia (see Aubertin, 1933 ; Zumpt, 1956A). Length of body between 6 and 11 mm. EggIt measures 1-2-1-3 mm in length and is of whitish colour.

Larva I (Fig. 60)Brumpt (1934) figured the hatching larva, but did not give a description of it.

Larva IISecond to tenth segment with complete anterior spinose bands, the eleventh with only an anterior ventral band. Complete posterior bands are present on the sixth to eleventh segments. Anterior spiracles each with four to six branches.

Larva. Ill (Figs- 61-63)Complete spinulose bands are present on the second to eleventh segments anteriorly, and on the seventh or eighth to eleventh posteriorly. Tubercles of last segment relatively small. Anterior spiracles each with four to six branches. Figure 62. Myiasis due to Lucilia bufonivora Moniez in a toad ; (above) healthy animal; (below) animal infected for 24-36 hours. (After Brumpt)

The eggs are deposited by the fly on the skin of the host, preferably on the back of the flanks. The larvae are fully developed in the shell after 24 hours, but they do not hatch spontaneously. Normally the majority of the larvae appear on the third and fourth days, and often this coincides with a moult of the toad which is accompanied by an exudation. Some eggs may lie for many more days on the skin.

1 mm

Figure 61. Lucilia bufoniwra Moniez. Posterior view of last segment of third-stage larva (Pi-7 == tubercles of cavity ; Afp = anal tubercle). {After Schumann)

Biology The larvae of L. bufonivora are obligatory parasites of several amphibians, and are no longer able to develop in carrion as is the related L. silvarum, but they both have probably, and even only relatively recently, come from the same root. Brumpt (1934) found in France that the main host is the Common European Toad {Bufo vulgaris), and the Midwife Toad {Alytes obstetncans} is also readily oviposited on by the flies. But the author only once obtained an oviposition on the Edible Frog {Rana esculenta) and the Spotted Salamander {Salamandra salamandra), but never on the Common Grass Frog {Rana temporaria} and several tritons. In the Leningrad district, however, Portschinsky found the Common Grass Frog and also the Field Frog {Rana arvalis) infested.

57

Figure 63. Myiasis due to Lucilia bufonivora Moniez in a load. Animal infected for 48-72 hours. In the case above, both nasal cavities are united and form a single ulceration. The animal below shows the right eye also infected. {After Brumpt)

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES case in which two small batches of those of the Palaearctic region by Zumpt (19564), and eggs had been deposited behind the right shoulder of a those of New Zealand by Miller (1939). The numerous toad on August 8th at 3 p.m. The first larvae hatched species of the Australian continent are at present in a on August 10th at 10 p.m., and the rest the next day fairly confused state (see Hardy, 1937), but a modern until 7 p.m. On August i7th the toad died, and the nasal revision is in preparation by Paramonov. It is therefore Brumpt describes a

cavities were densely beset with larvae. The maggots continued feeding on the dead toad and four mature larvae appeared two days later, of which one pupated, but the others died. Brumpt did not describe how the young larvae reach the nasal cavities, where the development takes place, His drawings of an infection (Figs. 62 and 63) reveal that other head cavities, like the orbits, are very quickly invaded too. The host will probably die just before, or just when the larvae have reached maturity. There are probably three generations during the summer, and hibernation takes place in the larval stage, The adults are diurnal and attracted for feeding to dead toads, rarely to meat and fruit. Live amphibians are attacked only by females ready for oviposition.

able. All Calliphora species develop in decomposing organic matter, which explains the trend towards an occasional facultative parasitism. Most species are oviparous, but some deposit freshly-hatched larvae. An outstanding phenomenon occurs in Calliphora stygia, which in New Zealand is oviparous in cool weather, but changes to a larviparism in the hot months.

Calliphora vicina Rob.-Desvoidy, Ess. Myod. 2, 1830, 435; Hall, Blowflies of N. America 1948, 307, figs.; Schumann, Wiss. Ztscfir. Unw. Greifswald 3, 1954, 257, figs.; Zumpt, Flieg. pal. Reg. 64i, 1956, 22, figs.; Kano and Morikawa, Bull. Tokyo med. dent. Univ. 4, 1957, 69, figs. Musca erythrocephala Meigen, Syst. Beschr. zweifl. Ins. 5, 1826, 62 (preocc.). Calliphora eythrocephala Seguy, Emycl. ent. (A} 9, 1928, 136, figs.; and most former authors. For further synonyms and taxonomic references see

The infestation of toads and frogs seems usually to lead

death.

Distribution

L. bufmimra is found in the temperate zone of the Palaearctic region, and may also occur in North America, where it is perhaps confused with L, silvamm, but this is a problem which remains to be cleared up.

Genus: CalUphora Rob.-Desvoidy CalUphora Rob.-Desvoidy, Mem. presentes Acad. roy.

The same is true for the larval taxonomy which can only be taken up when the imagines are clearly recogniz-

/. Calliphora victim Rob.-DesvoidyEuropean Blue Bottle

Pathogenesis to

not advisable to give a key to the imagines of those species which have been found involved in cases of myiasis, but rather to wait until this genus has been thoroughly studied.

Hall

Sci.

(1948) and Zumpt (1956i).

Inst. France 2, 1830, 433.

Mya Rondani (nee Linnaeus), N. Ann. Sci. Nat. Bologna (3) 2,1850,175.

History This common fly of the Northern hemisphere is better known as Calliphora erythrocephala (Meigen), a name which, however, is preoccupied. Hall then replaced it by G. vicina, a step followed by most modern taxonomists and now also widely accepted in the applied field.

Sonmmya Rondani, Dipt. ilal. Pndr. 4, 1861, 9. Acrophaga Brauer and Bergenstamm, Denkschr. Akad. Wiss. Wien 58, 1891, 367. Neocalliphora Brauer and Bergenstamm, id. ibid. 391. Neopollenia Brauer, S.B. Akad. Wiss. Wien, math.-naturw. Cl. 108 (I), 1899, 496. Eucalliphora Townsend, Smithson. misc. Coll. 51, no. 1803, 1908, 118. Adicfusina Surcouf, N. Arch. Paris 6, 1919, 85. Pnekon Surcouf, id. ibid. 112. Xemcalliphora Malloch, Trans. Proc. N.Z. Inst. 55, 1924,

Morphology ImagoBody

robust, measuring 5-12 mm in length. Thorax bluish black, with a thin whitish pruinosity; abdomen metallic dark blue, with a silvery tesselation.. Legs black, sometimes partly black-brown. In the male the eyes are close together, the frons at its narrowest part measuring only one-seventh to one-eighth of eyelength ; in the female the eyes are separated from one another by a broad frons which is more or less extensively reddish. Buccae in both sexes yellow or orange for the greater part, only darkened posteriorly. Buccal hairs are also black. The basicosta of the wing is yellow.

639. Atmesia Villeneuve, Bull. Ann. Soc. ent. Belg. 56, 1927, 357. Stobteola Enderlein, Mitt. dtsch. ent. Ges. 4, 1933, 126. Acrcinesia Hall, Blowflies of N. America 1948, 272. The genus Calliphora is especially rich in species in the Holarctic and Australasian regions, while in the Ethiopian region only one species occurs which is restricted to the more temperate southern parts, and in the tropics to the higher altitudes. The taxonomy is difficult and based mainly on the male terminalia, so that a correct identification can normally be made only by an expert. The North American species have been dealt with by Hall (1948),

EggBanana-shaped, white, about 1 -7 mm long. Larva 1 (Fig. 64)Second to seventh segment with complete anterior bands; sixth to eleventh with posterior spinose bands, but those on the sixth to the eighth or ninth not continuous over dorsum, and those on the 58

SUBORDER: BRACHYCERA PupanumOf normal shape, with the external characters of the mature larva.

Biology

Figure 64. CaKiphora vicina Rob.-Desvoidy. Cephaloskeletons of: (a) first; (&) second; and (c) third larval stages. {After Hall)

Figure 65. Posterior peritremes of: (c) Ca^Aora MCIMO Rob.-Desvoidy; and (fc) C. Mmiton’a (L.). {After Hall)

sixth and seventh narrow. Cephaloskeleton slender and weak. Posterior spiracles each with two ovate orifices which appear more or less united basally.

The adults are attracted to any foul-smelling product of decay, of which carrion is by far the most satisfactory. They commonly invade houses, especially in the cooler season, and may become a great nuisance. The eggs are deposited’ on the breeding medium, where the larvae hatch in a day’s time or less. During a life-time 540-720 eggs are produced, which are deposited in batches of up to 180 eggs at a time. Under warm and otherwise favourable conditions the larvae feed for 3-4 days, and the puparium is formed about 2-3 days later. In cooler climates the larvae may feed for as long as 9 days. The pupal stage lasts at least one week, but may be considerably lengthened under unfavourable conditions. The winter of the temperate zone is probably passed in the so-called ’ prepupal stage’, that is, as a non-feeding mature larva which has left the breeding-medium. In England the whole life-cycle (egg to egg) requires at least 29 days, while in Texas it may, be accomplished within 15 days. Parker (1922) suggested that C. vicina was able to reproduce by paedogenesis. This assumption has been clearly disproved by Keilm (1924c).

Pathogenesis The larvae of C. vicina have been found several times involved in traumatic myiasis in man and animals. Onorato (1922) cited four cases from humans in Tripoli, twice concerning the rectal region, secondary to ulcers, once the ear secondary to otitis, and lastly the oral cavities secondary to stomatitis. In Great Britain this fly plays a minor role in secondary sheep myiasis (Haddow and Thomson, 1937; MacLeod, 1937), but the larvae are not able to act as primary invaders (Ratcliffe, 1935).

Larva JI (Fig. 64)Bands wider and composed of larger spines than in the previous instar. Second to ninth segments with complete anterior spinose bands, while those on the eighth and ninth segments weak and sometimes absent dorsally; seventh to eleventh segments with posteroventral bands, and those on the eighth to eleventh complete. Anterior spiracle with seven to ten branches. Cephaloskeleton more heavily sclerotized than in the first instar, with strongly arched labial sclerites. Peritremal ring of the posterior spiracle open.

Larva III (Figs. 64,65 and 66)The mature larva reaches a length of up to 19mm. Second to ninth segments with complete spinose bands, anterior bands not complete dorsally on tenth to twelfth segments; sixth to eleventh segment posteriorly with spinose bands which are complete on the ninth to eleventh. Last segment with a large area of ventral spines. Anterior spiracle with seven to ten branches; posterior spiracles each in a closed peritreme which shows a button and three slits. Cephalo-

Figure 66. CaUifihora vicina Rob.-Desvoidy. Posterior view of the last segment of third-stage larva (Pi-; = tubercles of cavity; Afp = anal

skeleton with an accessory oral sclerite.

tubercle). {After Schumann)

59

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES In Tasmania, however, C. vicina is an important sheep myiasis fly (Ryan, 1954). Onorato(1922) again mentioned the larvae as causing severe infections in various animals in Tripoli. Carter and Blacklock (1913) reported an infection with larvae of Calliphora vicina, Muscina stabulans

Calliphora 434.

and Fannia canicularis in the ’ nose and regions of the face surrounding the mouth ’ of a tuberculous Vervet Monkey {Cercopithecus aethiops) in captivity. A second infested wound was found near the groin of this monkey. An interesting record is by Derksen (1938) who found hundreds of maggots and also eggs on a few specimens of the Common Noctule (^Nyctalw noctula} in Germany. The maggots were causing a fatal traumatic myiasis all over the body; and acted in this case as primary

Hall

invaders. More than eleven generations were reared by Bogdanow (see Haddow and Thomson, 1937), exclusively on human faeces. It is therefore not surprising that this fly is also accused of being involved in cases of intestinal and urinary myiasis. Eidmann (1936) recorded two instances from Germany in which living larvae were passed with human faeces, but he says that they had apparently been ingested with infected meat. An infection via anus or via urethra is of course possible under certain circumstances, and in this connection a case reported by Harvey (1934) is conclusive. It concerned a 59-year-old farm labourer in England. The original site of the infection was probably a permanent opening into the bladder made for extravasation of urine following obstinate urethral stricture. The larvae had appeared in the vomit, faeces, and the discharge of the bladder. More than 100 adults were obtained from isolated larvae. Leclcrcq (1949) reported a case of urinary myiasis in an old man from Belgium who passed about a dozen almost mature maggots with the urine. He thinks that the fly oviposited on the entrance of the urethra, and that the young larvae crawled actively into the urinary passages where they continued their development.

fulvibarbis Rob.-Desvoidy, Ess. Myod. 2, 1830,

Calliphora rubrifrons Townsend, Smithson. Misc. Collect. 51, 1908, 116.

For further synonyms and

taxonomic references see

(1948) and Zumpt (1956^).

History This species, which is very common in certain parts of the Northern hemisphere and rare in others, has been confused in the literature with some closely related species, and a clear separation has been made possible only in the last decade by a careful study of the male genitalia. Adults reared from cases of myiasis should be sent to a specialist for correct identification.

Morphology ImagoA robust fly like C. vicina, and of quite similar general appearance, but C. vomitoria is on the average a little bigger, measuring from 10 to 14 mm in body-length. The eyes of the male are very narrowly separated from one another; in the female the frons at vertex measures about two-thirds of eye-length. The buccae are black, but the hairs on the ventral and posterior parts are predominantly reddish. The basicosta of the wing is black.

Larva ISimilar to that of C. vicina, but posterior bands of sixth and seventh segment lacking. Larva IIAlso similar to C. vicina, but eleventh segment complete, but extremely narrow, posterior band. Larva III (Figs. 65 and 67)According to Kano and Okazaki (1955), who give a drawing of the third larval

with a

Distribution

Calliphora vicina was probably originally a Holarctic species, which a long time ago found its way to many parts of the Oriental and Australasian regions, and in the New World to several places in the Neotropical region. Human traffic certainly favours the spread of this semi-domestic fly. It does not occur in Africa south of the Sahara, and contradicting records are due mostly to confusion with the closely related Calliphora croceipalpis. 2. Calliphora vomitoria

(Linnaeus)Red-bearded

Figure 67. Calliphora i-omitoria (L.). Ccphaloskeleton of third-stage larva. {After Hal!)

stage, the spinose bands of the last three segments are not as well developed as in C. vicina. The question arises, however, whether the features of spinulation are constant throughout the area of distribution of these two flies, and in cases of myiasis it is always advisable to try to rear the adults.

PupariumPractically

Blue Bottle

Musca vomitoria Linnaeus, Syst. Nat., ed. 10, 1758, 595. Calliphora vomitoria Seguy, Encyd. ent. {A) 9, 1928, 140; Hall, Blowflies of North America 1948, 313, figs.; Kano and Okazaki, Bull. Tokyo med. dent. Uniu. 2, 1955, 106, figs.; Zumpt, Flieg. pal. Reg. 64i, 1956, 23, figs. Calliphora brunnibarbis Rob.-Desvoidy, Ess. Myod. 2, 1830, 434.

not

separable from that ofC. vicina.

Biology The bionomics ofG. vomitoria have not yet been studied extensively as those of C. vicina, but they are probably very similar in most respects. as

Pathogenesis to

60

The larvae of C. vomitoria have been found several times be involved in sheep strike in Great Britain, but only

SUBORDER: BRACHYCERA as secondary or even tertiary invaders

Thomson, 1937;

(Haddow and

MacLeod, 1937, 1943).

Miller (1939a) gives a description of the imago and the third larval stage, and compares them with other Calliphora species in New Zealand. The fly is similar to C. vicina, but the abdomen is brilliantly violet-blue and shows no tessellation.

Onorato

(1922) mentions it in the same capacity from Tripoli. Because this fly, like C. vicina, oviposits on meat, the larvae may easily be swallowed with food and re-appear in the stool, giving the impression of causing an intestinal myiasis. Cases of true intestinal myiasis due to these flies have not yet been confirmed beyond any doubt, and corresponding reports may all be labelled as ’ pseudo-

5. Calliphora stygia (Fabricius)Golden-haired Blowfly

Musca stygia Fabricius, Spec. Iw. 2, 1781, 438. Calliphora stygia Hardy, Bull. ent. Res. 23, 1932, 550, fig.; and Proc. Linn. Soc. N.S.W. 62, 1937, 19; Fuller, Proc. Linn. Soc. N.S.W. 57, 1932, 78. figs.; Norris, Mon. biol. 8, 1959, 527, fig. Calliphora villosa Rob.-Desvoidy, Ess. Myod. 2, 1830, 437. Musca laemica White, DieffenbacKs Travels in New Zealand 2,

;

myiasis (Zumpt, 1962c). Distribution C. vomitoria is distributed all over the Holarctic region and has evidently been introduced to the Hawaiian Islands and some other parts of the Oriental and the Australasian regions, but most of these records need confirmation. Former records from the Cape Province are due to confusion with the similar C. croceipalpis. C. vomitoria certainly does not occur anywhere in Africa south of the Sahara.

1843. 291. Calliphora laemica Hardy, Proc. Linn. Soc. N.S.IV. 62, 1937, 19; Miller, Cawthron Inst. Monogr. 2, 1939, 32, figs.

3. Calliphora croceipalpis Jaennicke

Calliphora croceipalpis Jaennicke, Abh. senckenb. Ges, 6, 1867, 376; Zumpt, Explor. Pare not. Albert, Miss. de WitteS7, 1956, 95, fig. Calliphora capensis Brauer and Bergenstamm, Denkschr. Akad. m’cn58, 1891,442. Calliphora paro.so.cra. Speiser, Kilimandjaro-Ivferu Exp. 2, 1910, Abt. 10, 155. History

In general appearance C. croceipalpis is reminiscent of C. vicina and of C. vomitoria in the adult stage. The buccae are, however, completely black and beset with black hairs. The basicosta of the wing is brown, and in this respect intermediate between the two Holarctic species. In the male the eyes are separated by a narrow frons, in the female they are broadly separated. The body-length varies between 7 and 12 mm. Geographically C. croceipalpis is restricted to the eastern, central and southern parts of the Ethiopian region, and its area of distribution does not overlap those of C. vicina and C. vomitoria,. It is a common fly in South Africa, but in tropical parts is probably restricted to higher altitudes. The larval stages have not yet been described adequately. Porter (1924) reports two cases of myiasis from the Transvaal. In the first, the larvae had been ’ removed from a patient’s ear ’, and in the second case, some larvae ’ were obtained from the freshly passed stool of a native child in Johannesburg ’. No further details were given, and no other cases have come to my knowledge. 4. Calliphora icela (Walker)

Musca icela Walker, List Dipt.

Brit, Mus. 4, 1849, 897. Calliphora icela Miller, Cawthron hst. Monogr. 2, 1939,

38, figs. History A species of very little economic importance, which has been reared from sheep a few times in New Zealand.

History The first Australian blowfly strike was probably in 1870 as recorded by a stock inspector in Tasmania (Ryan, 1954), and the species involved was evidently C. stygia, because the most important blowfly nowadays in Tasmania, Lucilia cuprina, was imported at a much later date. In 1910, Froggatt found larvae ofC. stygia breeding in sheep on the Australian continent, and since then it has been recognized as one of the important primary sheep invaders of Australia (Mackerras and Fuller, 1937). Calliphora laemica replaces C. stygia in New Zealand and is listed by Murray (1956) as a synonym of this species. Hardy (1937) treated C. laemica as a distinct species owing to slight differences in the male genitalia, and Norris (1959) again expressed doubt about the conspecificity of C. stygia and C. laemica because of biological differences. Curiously enough, the first record of myiasis caused by C. laemica in New Zealand concerns a Green Gecko {Naultinus pentagonalis}. The larvae were found to have invaded the skin of the head and the intestine (Colenso, 1879). The first record of sheep myiasis is evidently by Cunningham in 1896 (see Miller, 1939&), but the name of the fly is not mentioned.

Morphology ImagoNon-metallic, thorax blackish with a dense bluish and white pollinosity ; abdomen brown-olivaceous tessellated, with long yellow hairs laterally and ventrally. The male has the eyes touching medially, with the upper facets greatly enlarged and demarcated from the lower ones. In the female the eyes have no strikingly enlarged facets, and are separated by a broad frons, measuring at vertex about three-quarters of eye-length. Face in both sexes predominantly orange, antennal groove and third antennal segment more or less blackened. Legs with femora and tibiae yellow-orange, and the tarsi contrastingly black. A pair before me. measures 12mm in length.

Egg and larvae I and II 61

are not described.

’

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Larva HI (Fig. 68)The average length of the mature larva is about 20 mm. The segments bear bands of small denticles at the anterior margins. Anterior spiracle with nine to twelve branches; posterior peritremes with slender slits similar to those in C. vicina. Cephaloskeleton with a relatively slender labial sclerite.

Puparium is

Pathogenesis In New Zealand C. stygia is the most important myiasis fly, causing 95 per cent of strikes, whereas the remaining 5 per cent are due to Lucilia sericata^ and very occasionally Chrysomya rvfifades and Ophyra rostrata were also found to be involved (Macfarlane, 1938). In Tasmania, C. stygia was perhaps the only sheep myiasis fly until Lucilia cuprina and Calliphora vicina were introduced. From the Australian continent it has been recorded as ’ initiating less than 10 per cent of strikes in districts where it is abundant, although it is present in a higher percentage of strikes started by L. cuprina ’ (Norris, 1959).

not described.

Biology Calliphora stygia is well adapted to lower temperatures. The adults may even appear in winter during any mild

Figure 68. Calliphora stygia (Fabricius). Cephaloskeleton and posterior peritremes of the third larval stage

Distribution

spell, and they attain great abundance in spring and early summer. They are active in bright sunlight as well as on dull overcast days. Indoors, they may fly at any hour,

C. stygia is recorded from New Zealand, Tasmania and many parts of the Australian continent, where it seems to be especially common in the more temperate zones.

even in darkness. The larvae are found in carrion in great numbers, especially in autumn and winter, but relatively few in summer. This is caused partly by increased predation by Chrysomya mftfacies during the warmer months, but is also to some extent due to a direct effect of high temperatures. Hibernation takes place in the soil as prepupae or in the pupal stage. In Australia C. stygia is oviparous, but in New Zealand it is oviparous only in cool weather, the flies depositing the first larval stage in hot weather. This biological difference induces Norris (1959) to suggest that the flies in New Zealand may represent a different species, formerly described as C. laemica (White), "

’

"

"

6. Calliphora albifrontalis Malloch-Western Australian Brown Blowfly

albifrontalis Malloch, Proc. Linn. Soc. N.S.W. 57, 1932, 67; Norris, Man, bid. 8, 1959, 530. Musca australis Boisduval, Voy. I’Astrobe, Ent. 2, 1835, 669

"

Calliphora

(preooc.). Calliphora australis Hardy, Bull. ent. Res. 23, 1932, 551. Calliphora maryfulleri Hardy, Proc. Roy. Soc. Qd. 57,1947,56. History There is confusion about the nomenclatorial status of this species, which is closely related to C. stygia and

62

SUBORDER:BRACHYCERA

apparently restricted to Western Australia. Mr. K. R. Norris (by letter) kindly informed me that the valid name

albifrontalis Malloch Boisduval is preoccupied. the conspecificity of these proposed C. maryfulleri as a

is C.

Morphology

ImagoI have not seen any adults, but according to Hardy (1937), the imago must be similar to C. stygia. The male, however, has no enlarged upper eye-facets and the eyes are separated from one another by a narrow frons. There are also differences between the male terminalia of the two species- Egg and larval stages are not described, but Mackerras and Fuller (1937) state that the maggots of C. stygia and C. albifrontalis ’ are very much alike’. Biology C. albifrontalis is a carrion breeder and the adults have been trapped on the tableland of Western Australia only in late autumn, winter and early spring. The species * was unrepresented in the trap catches for the remainder of the year, though other species of Calliphoridae were present. If this is a true picture of the seasonal occurrence, then C. albifrontalis may be adapted to survive the hot and very dry south-western Australian summer in the larval or pupal stage, unless it becomes extinct annually over wide areas, which are repopulated in the autumn from coastal regions’ (Norris, 1959). Pathogenesis

C. albifrontalis is a primary invader and said to be the most important sheep myiasis fly in the southern parts of south-western Australia. Mackerras and Fuller (1937) recorded it in 45 out of 310 strikes in Western Australia. Distribution

Apparently restricted

to

parts and the posterior spiracles’. The figures she gives do not coincide, however, with specimens named C. hilli

(1932), because M. australis which I received from K. R. Norris, and it is therefore Hardy (1947), unaware of better to refrain from making a redescription. There was great confusion about the status of Patton’s two species, at a later date substitute for M. australis. Calliphora hilli until Dr. S. J. Paramonov synonymized it with Hardy’s C.fallax (K. R. Norris, by letter). Norris (1959) writes that this species ’ has a superficial

Western Australia.

7. CaIHplwra hiW PattonHill’s Brown Blowfly

Calliphora hilli Patton, Philipp. J. Sci. 27, 1925, 400. Calliphorafallax Hardy, Bull. ent. Res. 21, 1930, 446, fig.; Fuller, Proc. Linn. Soc. N.S.W. 57, 1932, 80, figs.; Norris, Monogr. biol. 8, 1959, 530. Calliphora rufipes Miller (nee Macquart), Cawthron Inst. Monogr. 2, 1939, 30, figs. Calliphora milleri Hardy, Proc. Linn. Soc. N.S.W. 42, 1937, 22. History

resemblance to C. stygia, but is more closely allied to C. augur in important features of its reproduction. It is ovoviviparous, and the first instar larva bears a striking resemblance to that of C. augur. ’ Up to 20 per cent of the " brown " blowflies taken in traps in the Canberra district may be C. fallax. For the most part these were counted as C. stygia by past investigators, but as C. fallax usually constitutes only a very small proportion of the catch, conclusions regarding C. stygia would not have been affected seriously.’ C. hilli also occurs in New Zealand. 8. Calliphora augur (Fabricius)Lesser Brown Blowfly

Musca augur Fabricius, Syst. Ent. 4, 1775, 777. Calliphora augur Malloch, Proc. Linn. Soc. N.S.W. 52, 1927, 310; Hardy, Bull. ent. Res. 23, 1932, 555, fig.; Fuller, Proc. Linn. Soc. N.S.W. 57, 1932, 81, figs.; Norris, Mon. biol. 8, 1959, 531, fig. Calliphora villosa Rob.-Desvoidy, Ess. Myod. 2, 1830, 437. For further synonyms see Hardy (1932a). History This species, together with the closely related C- nociva, has been recognized by Mackerras and Fuller (1937) as the most important sheep myiasis fly in Australia after Lucilia cuprina. There is quite a long list of synonyms, but the status of some of them is not yet fully cleared.

Morphology Imago (Fig. 69)The adult fly is characterized by a yellow abdomen with a broad blue-green median vitta with a yellow pruinosity on the last tergite. The mesonotum is densely covered by a dark blue and partly whitish pollinosity. The legs have yellow femora and tibiae, but the tarsi are contrastingly black. The head is predominantly yellow, parafrontalia and third antennal segment are more or less blackened. In the male the eyes are close together, the frons measures at its narrowest point about the width of one ocellus; the upper facets are distinctly enlarged but the facets decrease in size towards the smaller ventral ones. In the female, the eyes are broadly separated from one another, the frons at vertex measures about one-half of eye-length. Length of body : 8-11 mm.

This is a species of little importance which has been reported from only a few cases of sheep myiasis. It has been bred from carrion, dead fresh-water crayfish, and accumulations of dead moths. Fuller (1932a) described the third instar larva for the first time. It is said to be very similar to that of C. stygia and ’ can only be separated on the structure of the mouth

Hardy (1932a) placed C. augur with the very similar C. nociva into the subgenus Proekon Surcouf, in which both species are distinguished from other species - by the presence of only two pairs of presutural acrostichal bristles.

Egg and larvae I and 63

// are not described.

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES hold pest. From trapping experiments it was calculated that in two successive days in December 1952, the population of C. augur at Canberra was about 350 flies per acre. C. augur is oviparous, laying batches of about 50 eggs, from which the highly active first instar larvae promptly hatch. This kind of reproduction gives the species a great advantage over other oviparous species in exploiting small and quickly perishable carcasses. Larval development can take place in a great variety of decomposing organic matter, for instance in dead insects, snails, fresh-water crayfish, sour milk and cheese, fermenting grain and bone manure. Fifty specimens of C. augur have been reared from a bird cadaver smaller than a sparrow.

Pathogenesis

Figure 69. Calliphora augur (Fabricius). Female fly

Calliphora augur is an important sheep myiasis fly in Australia (see Mackerras and Fuller, 1937). Of 603 strikes in a Canberra flock C. augur was found to be involved in 165, of which it may have initiated about a quarter. Norris (1959) mentioned a case of myiasis in a Brown Hawk {Faico berigord}^ in which several hundred larvae were detected in the nostrils and other head cavities. He says that ’ undoubtedly C. augur causes traumatic myiasis of other native birds and animals, and probably some at least of such human myiasis as are reported in eastern Australia ’. According to Dr. Lee (by letter) it has been found on several occasions in of human wounds, and in one case in the vagina of a sick

Larva HI (Fig. 70)The mature larva reaches a length up to 18mm. Fuller (1932a) says in her description that the spinulation is very much like that in C. stygia. The labial sclerite is stouter, however, and the slits of the posterior peritremes are relatively shorter.

Puparium is not described. Biology

An account of the known biological facts of C. augur is given by Norris (1959). This fly may occur in great abundance during early summer, when it constitutes a large proportion of the huge population of blowflies buzzing in the bush and the paddocks. It is also a house-

old

woman.

Distribution

According to Hardy (1937), C. augur ’occurs in Tasmania, Victoria and perhaps in certain mountain areas of New South Wales as a permanent resident; it is also found in the southern coastal regions of Queensland and in the sheep country of the two latter states as a seasonal fly only. The limit of its western occurrence is not known ’. 9. Calliphora nociva Hardy Calliphora nociva Hardy, Bull. ent. Res.

23, 1932, 556.

History C. nociva was separated from C. augur as a distinct species only in 1932. The main differences lie in the width of the male frons, and the colouring of the abdomen m both sexes. The male genitalia are said to be inseparable from those of C. augur.

Morphology

Imago-In contrast with C. augur, the broad median vitta on the abdomen ofC. nociva is of a vivid blue colour with a white pruinosity on the last tergite. In the male the frons at its narrowest point measures at least twice the width of one ocellus, and the upper eye-facets are comparatively smaller. In the female I cannot find a significant difference with respect to the width of frons in the two species. Figure 70. Calliphora augur (Fabricius). Cephaloskeleton and posterior peritremes of the third larval stage

Egg and larval stages 64

are not described.

SUBORDER: BRACHYCERA History Another fly from New Zealand, which is characterized by hairy and almost holoptic eyes in the male sex. It shows a violet-blue abdomen with greenish reflections and golden hairs on the pleura and the venter. The legs are yellow. The larval stages are not described, but Miller (19396) says that a male and a female have been reared from, a ’ struck’ sheep.

Biology and Pathogenesis the following remarks: ’Small numbers of this species have been reared from carrion at Canberra and Cunnamulla (south-west Queensland), but there is very little information about its bionomics. ’ Calliphora nociva occurred in 56 per cent of strikes containing Calliphora species, and was present in nearly 50 per cent of strikes examined from its area of distribution. Like the closely related C. augur, it occurs in higher incidence than other species in wound myiasis (Mackerras and Fuller, 1937). Further investigation of its biology and ecology is highly desirable.’ Norris

(1959) makes

Genus: Pachychoevomyia Villeneuve Pachychoeromyia Villeneuve, Bull. Soc. ent. Fr. 1920, 225. In 1910, Austen described a ’ Cordylobia praegrandis’ from three females which he had received from the Cape,

Distribution

Hardy (1932a) says that ’ this fly is a seasonal one in New South Wales and at Canberra, but along the coastal area of South Australia it would seem to be permanently established and becomes a pest inland, attacking sheep’.

Natal and N.W. Rhodesia. No details about the life-

most parts of Victoria,

history were known to him, but he supposed that this species should be ’ in its larval stage a subcutaneous parasite in mammals’. The author had made two errors. Firstly, his species was morphologically not related to Cordylobia^ but to Auchmeromyia, as Roubaud, and Rodhain and Bequaert stated shortly afterwards, and secondly, the larvae are blood-sucking and live in the burrows of the Warthog [Phacochoems aethiopicus} like species of Auchmeromyia.

10. Calliphora quadrimaculata (Swederus)

Musca quadrimaculata Swederus, Stock Nya. Handl. 8, 1787, 289. Calliphora quadrimaculata Miller, Cawthron Inst. Monogr. 2, 1939, 43, figs. For further synonyms see Miller (1939a). History This fly, with the two following species, is characterized by hairy eyes, and all three are endemic in the New Zealand subregion. Miller has described the imago and the third instar larva of C. quadrimaculata and compared it with other Calliphora species of this island. It has been found very occasionally in cases of sheep myiasis, mainly as a secondary fly, and is to be regarded as being of little economic importance. //. Calliphora hortona

(Walker)

Musca hortona Walker, List Dipt. Brit. Mus. 4, 1849, 894. Calliphora hortona Miller, Cawthron Inst. Monogr. 2, 1939, 46, figs. Pollenia auronotata Macquart, Dipt. exot. Suppl. 5, 1855, 115.

F igure 71. Pachychoeromyia praegiandis (Austen). Female fly. (After

Austen)

History This fly is very similar to C. quadrimaculata, and apart from the male terminalia, separable mainly by its black palpi. It has been recorded from New Zealand and the Auckland islands, and also from the beach at Sydney, where it has probably been introduced with human traffic. It breeds especially in decaying sea-weed. Miller (1939a) mentioned that this species has been reared from infested wool as well as from a few cases of sheep-myiasis, which were caused primarily by Calliphora

He gives descriptions of the imago and the third instar larva. stygia and Lucilia sericata.

12. Calliphora nothocalliphoralis Miller

Calliphora nothocalliphoralis Miller, Cawthron Inst. Mon. 2, 1939, 49. 65

But this is actually all that is known so far. Roubaud

(1914) mentioned the larva and said that it was very similar other Parvae of Auchmeromyia species, but he did not give a description. Benoit (1957) saw several adults which had been reared from larvae found in a wart-hog burrow at Lake Victoria. The life-history is therefore roughly known, so far as the host and the blood-sucking habit are concerned. The mature larva must be much larger than those of the Auchmeromyia species, and it is certainly also characterized by some differentiating features. But this still remains to be studied. The adult fly (Fig. 71), in contrast with the Auchmeromyia species, has the thoracic squama provided with. long erect hairs on the upper side, and the male terminalia also show features which justify Villeneuve’s proposal to place to

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES this species into a distinct genus and not to Auchmeromyia, as done by Roubaud, Rodhain and Bequaert and also by

Patton (1935). The adult flies are readily recognizable by their large size (14-18 mm) as well as the predominantly yellowbrown colouring’, reminiscent of that of Auchmeromyia and Cordylobia. The mesonotum shows two widely separated, blackish longitudinal stripes, and the last two abdominal tergites are darkened; the foregoing ones mostly have black bands on the hind margins and there is a narrow median longitudinal line. The legs are totally yellow-

brown. Pachychoeromyia praegrandis (Austen) is distributed all over Africa south of the Sahara, but is not common everywhere and completely absent in some areas. Its area of distribution is therefore a patchy one. Since its first discovery, it has also been found in association with the Antbear {Orycteropus afer} and the Aardwolf {Proteles

cristatus). Genus: Auchmeromyia Brauer and Bergenstamm Auchmeromyia. Brauer and Bergenstamm, Denkschr. Akad. Wiss. WienSS, 1891, 391. Choeromyia Roubaud, C.R. Acad. Sci. Paris 153, 1911, 553.

(b)

There are five species of Auchmeromyia known, all of which are restricted to Africa south of the Sahara. In general appearance the adults are reminiscent of Cordylobia, but the cerci are always fused, as in the closely related Pachychoeromyia praegrandis (Austen). The larvae are temporarily blood-sucking ectoparasites of burrowing animals, mainly warthogs and antbears, but one, namely A. luteola, has become a permanent inhabitant of primitive human dwellings. The larval stages of only A. luteola have been described, but those of the other species are probably very similar and may not even be clearly separable from them. The adults are predominantly yellow-brown and show a more or less developed dark pattern. They may be distinguished by the following key ; 1

(2) Abdominal tergite III (second visible segment) of male about 1^- times as long as tergite IV; in the female it is about twice as long as tergite IV (see Fig. 72). 8-13 mm. 1. A. luteola (Fabricius)

2 (1) Abdominal tergite III in both sexes not or slightly longer than tergite IV. (The following species which have not yet been found in human dwellings, are well characterized by the male genitalia (hypopygium), but in outer features they are verv similar to one another. Only the males are now followed up ; they are easily recognizable by their

(d)

large hypopygium)......................... 3 3

(4)

Hind margin of abdominal tergite IV (third visible one) with a slight, but distinct, incision. 8-11 mm.

4

(3)

Hind margin of abdominal tergite IV straight

Figure 72. Abdomen of; (, .-1.

.

2. A. bequaerti Roubaud .

5

66

choerophaga (Roubaud) ; bequaerti R(

SUBORDER: BRACHYCERA 5 (6) Mesonotum without well-marked, longitudinal dark stripes; the abdomen is mainly yellow, with only small and ill-defined vittae at the posterior segmental margins. 10-11 mm. 5. A. boueti (Roubaud) 6

(5) Mesonotal stripes broad and well marked, abdomen with a distinct and large blackish pattern. 8-11 mm. The following two species can be distinguished only by the male genitalia (see

Zumpt, 1959a). 3. A. reidi

Zumpt

4. A. choerophaga (Roubaud) ]. Auchmeromyia luteola

(Fabricius)Congo Floor Maggot

Musca luteola Fabricius, Syst. Antl. 1805, 286. Auchmeromyia luteola Newstead, Dutton and Todd, Ann. trap. Med. Parasit. 1, 1907, 49, figs.; Roubaud, Etud. Fa. parasit. Afr. occ. franc. 1, 1914, 44, figs.; Patton, Ann. trop. Med. Parasit. 29, 1935, 201, figs.; Garrett-Jones, Bull. ent. Res. 41, 1951, 679, figs.; Zumpt, Explor. Pare nat. Albert Miss. de Witte 87, 1956. 153, figs. Ochromyia senegalensis Macquart, Dipt. exot. Suppl. 4, 1851, 244. Somomyia {Ochromyia) subtranslucida Bertolini, Memr. Accad. Bologna Sci. 1st. 12, 1861, 45, fig. Cosmina latecincta Bigot, Ann. Soc. ent. Fr. (5) 4, 1874, 240. Auchmeromyia tilhoi Surcouf and Guyon, Bull. Mus. nat. Hist. nat. 1912, 423.

History The first sound studies on the morphology and bionomics of the larvae are those by Dutton, Todd and Christy (1904) in the Congo. They also succeeded in correlating the adults with these larvae, and it was the late Major Austen who identified the species already described in 1805 by Fabricius. Further studies were undertaken by Wellman (1906), Rodhain and Bequaert (1913), Schwetz (1914), and especially by Roubaud (1913 and 1914) who dealt not only with A. luteola, but also with other Auchmeromyia species in a monographic form. Finally, the latest and most comprehensive paper with respect to the bionomics is the one by Garrett-Jones (1951). Formerly the maggots of this fly were thought by several authors to be transmitters of sleeping sickness.

Morphology Imago (Fig. 72)Body yellow-brown,

with a blackish

pattern forming two mesonotum, almost

longitudinal but variable vittae on completely covering the last two abdominal tergites and also partly tergite III. In the female tergite III is about twice as long as tergite IV, in the male it is about 1^- times as long as tergite IV.

The body-length varies from 8-13 mm. The female fly is relatively easily recognizable by its broad abdominal tergite III; the male may be superficially confused with Cordylobia anthropophaga, although it

has broadly separated eyes and very long, completely fused cerci. Auchmeromyia species other than A. luteola live in association with wild animals and do not normally enter human habitations.

EggWhitish in colour, about as long (l-4-l-5mm) as that of the common house-fly, but nearly twice as broad, tapering at the anterior end and rounded at the posterior. The surface is covered with a fine reticulate pattern, although appearing smooth to the naked eye.

Larva IThe newly-hatched larva is 1 -5-2 mm long, of a waxy, creamy colouring. It becomes visibly thinner and greyer if unfed for some days, but remains as active as before. The cephaloskeleton is well-developed; the last segment shows five pairs of pointed fleshy processes. The engorged larva is bloated and the cuticle is taut. The shiny white tracheal system forms a conspicuous pattern against the freshly ingested blood. When ready to moult, the first larval instar has reached a length of up to 4-5 mm.

Larva 11The second larval stage may reach a length of up to 12 mm before moulting. It is morphologically very similar to the third stage, but the posterior peritremes show only the usual

two slits.

Larva 111 (Figs. 73 and 74)The fully-grown third larval stage may reach a length of up to 18 mm. The twelve body segments are clearly visible. Laterally they each bear two or more protuberances with a small posteriorlydirected spine and a small pit. The ventral side of the body is flattened; the segments are provided with transverse foot-pads, bearing backwardly directed spines which are bigger than those on the remaining surface. The last segment is large, provided with five pairs of finger-like protuberances, and with a pair ofperitremal plates which are relatively small and widely separated from one another. PupariumIt is chestnut during the first days, later becoming blackish-brown. The average length is 15 mm.

Biology The staple diet of the adults appears to be human faeces, but they are also fond of fallen fruit and fermenting vegetables. Faeces of monkeys and pigs are attractive too, but not those of dogs, cats and cattle. Mating takes place in daylight, and one male can fertilize several females. Oviposition and development continues all the year round without diapause. The female produces up to six batches of eggs, the greatest number of eggs deposited petfemale being about 300. By means of the ovipositor, they are laid singly into the dry dusty soil or sand in shaded places. Under experimental conditions, the female lives for as long as 93 days, the male for 85 days. Hatching of eggs is dependent on temperature and relative humidity (R.H.). At 26-28C and 50-60 per cent R.H. it takes 36-60 hours, at 23C and 10 per cent R.H. from 3 to 7 days after oviposition. All larval stages are blood-sucking. The host’s skin is scraped by the mouth-hooks and the minute toothed maxillary plates in front of them. The feeding act

67

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES estimated as 21 days, giving a life-cycle of ten weeks in all. Under these conditions, A. luteola may complete five generations a year. Floor maggots can fast for a considerable time, depending on temperature, R.H., stage, and number of previous blood-meals. At 28-5C and 90 per cent R.H., unfed first larvae starved for up to 20 days, the last larval stage at about 90 mg survived for 47 days. At the same temperature but 10 per cent R.H., the survival time is much less. On the other hand, lower temperatures extend the survival time. At 23C and 60 per cent R.H., the newly hatched larvae can fast for up to 37 days. The pupal stage lasts about 9 days at 34C, about 11 days at 28-5C, and 15-16 days at 23C. It is not dependent on the relative humidity. Garrett-Jones says that A. luteola is ’ probably entirely specific to man ’. This is certainly not true. It is hardly believable that man is the original and sole host of this fly. Apart from the fact that the larvae have been found associated with domestic pigs, if the ecological conditions are favourable (Roubaud and Holstein, 1950), I have seen several adult specimens which were caught in the entrances to burrows of antbears and warthogs in the Cameroons, in Tanganyika, and in Kenya. Moreover, in northern Bechuanaland I caught two males in my tent in an area completely uninhabited by humans for a radius of at least 30 miles. However, warthogs and antbears may not be true hosts of A. luteola, because only a few specimens, among great numbers of the usual Auchmeromyia species associated with these animals, have so far been found near the burrows. I suspect that the original host may be a burrowinhabiting animal not yet traced by the entomologist.

Figure 73. Auchmeromyia luteola (Fabricius). Third dorsal and ventral view

Pathogenesis Figure 74. Auchmeromyia luteola (Fabricius). Posterior view of 1 segment of third-stage larva

normally lasts about 20 minutes; in newly-hatched maggots often only 10 minutes. In the engorged larva, the red ingested blood shines through the body-wall. Under normal conditions a meal is taken every night, except for a day missed before each moult. There are three larval stages. The time of moulting is evidently related to weight. The first occurs after the larva has gorged to a weight of 1-5-2-1 mg, the second after having reached 12-19 mg. The minimum weight for pupation is about 97-5 mg. The minimum number of meals for complete development is probably six (two per stage) ; at 28-5C and 60 per cent R.H., the larvae pupated under experimental conditions after the sixteenth or seventeenth meal. The duration of the life-cycle can be only roughly estimated. Larvae in an inhabited hut probably take their first meal three days after the eggs are laid. If they feed four times a week and live at an average temperature of 25C, they need about 46*days to develop into files. The mean interval from emergence to oviposition might be

68

The bite of the larva, and also the release after feeding, is normally felt as a slight prick. Sometimes the wound bleeds. Sensitive persons may feel pain, swelling, or irritation afterwards. In heavily infested huts, however, the maggots may become a serious nuisance, and the natives have been known to sit up all night to avoid them. The larvae o{ A. luteola do not transmit any disease. Distribution

Auchmeromyia luieola occurs only in Africa south of the

Sahara, including the Cape Verde Islands. It is not found on Madagascar. Its area of distribution in Africa is not yet completely known, and it may be expected to many territories from which it has not yet been recorded (comp. map by Garrett-Jones, 1951), However, Cape and probably also not in the drier parts of south-western Africa. Otherwise its range includes very wet and very dry macroclimates. The range is probably determined by the ’ host-availability ’ rather than climatic limits. Where humans still sleep in a primitive way on the floor on blankets or mattresses, the maggots can reach them and therefore persist. Where, however, they adopt a more civilized way of life and use bedsteads, the maggots will die out, occur in

it definitely does not occur in the

SUBORDER: BRACHYCERA Congo, and which has also been found at the Kunene river in S.W. Africa. Like other Auchmeromyia species, it is associated with warthogs and antbears, and Roubaud (1914) found the larvae in their burrows and gave some biological data. Experimentally, the larva can be maintained on humans as well as on domestic pigs. The larval stages covered 16 days and during this time eleven blood-meals were taken. Under natural conditions, however, it is estimated that the larvae may require up to 3 months before reaching maturity because the chance for sucking blood usually occurs only rarely. In morphological respects, he could detect no useful features for separating the third larval stage from that of A. luteola. The taxonomy of the adults has been dealt with by Zumpt (I959a).

2. Auchmeromyia bequaerti RoubaudBequaert’s Warthog Fly

corner of the

Auchmeromyia (Choeromyia) bequaerti Roubaud, Bull. sci. Fr. Selg. (7) 47, 1913, 198; and Etud. Fa. parasit.

Afr. occ. franc. 1, 1914, 41.

Auchmeromyia bequaerti Patton, Ann. trop. Med. Parasit. 29, 1935, 205, figs.; Zumpt, Bxplor. Pare nat. Albert Miss. de Witle 87, 1956, 156, figs.; and Novos Taxa ent. 12, 1959, 1, figs. History

The species was described from the Congo (Sankisia) and later found to be widely distributed over eastern and southern Africa. As far as is known today, A. hequaerti ranges from the eastern Congo and Tanganyika southwards to the northern parts of South West Africa, the Transvaal and Natal (Zululand). The adults are quite common in and near the burrows of warthogs (Phaco- 5. Audmieromyia boueti (Koubaua)Bouei’’s Warthog Fly choerus aethiopicus) and antbears [Orycteropus qfer). The Choeromyia boueti Roubaud, C.R. Acad. Sci., Paris 153, larvae are numerous in all stages in the loose sand of the 1911, 554; and Etud. Fa. parasit. Afr. occ. franc. 1, 1914, 40, figs. burrows, but they have not yet been properly studied. that of the is similar to Auchmeromyia boueti Patton, Ann. trop. Med. Parasit. 29, very However, morphology A. luteola, and only a detailed examination will perhaps 1935, 214, figs.; Zumpt, Expl. Pare nat. Albert Miss. de Witter, 1956, 156, figs. reveal taxonomic differences. The adult flies may be superficially confused with Cordylobia anthropophaga, the Tumbu Fly, as for instance History Like the preceding species, A. boueti is a West African Bedford did (1927), when he wrote that he ’ had taken numerous flies at the entrances of wart-hog burrows species, but probably not distributed as far eastwards. in several places in the Transvaal and Zululand. C. There are only a few locality records available, and anthropophaga never occurs in association with warthogs A. boueti may even be restricted to Upper Senegal. The larval stages have not been described, and the only and antbears. The Auchmeromyia species are not easily separable from biological data known are that it lives in association with one another by outer features, but are well characterized warthogs and antbears like A. choerophaga. by the male genitalia (see Zumpt, 1956a and 1959fl). Genus: Neocordylobia Villeneuve Neocordylobia Villeneuve, Bull. Soc. Path. exot. 22, 1929, 439. ?

3. Auchmeromyia reidi ZumptReid’s Warthog Fly Auchmeromyia reidi Zumpt, Novos Taxa ent. 12,

1959, 1, figs.

History This species was discovered by E. T. M. Reid near Guar in the Sudan, and could only recently be separated from the closely related A. bequaerti and A. choerophaga. It also inhabits the burrows of warthogs, but no further

biological data are known. f. Auchmeromyia choerophaga (Soiibaud)Rottbaud^s Wart-hog Fly

Choeromyia choerophaga Roubaud, C. R. Acad.

Sci. Paris, 153, 1911,554; and Etud. Fa. parasit. Afr. occ. franc. 1, 1914, 41, figs. Auchmeromyia choerophaga Patton, Ann. trop. Med. Parasit. 29, 1935, 210, figs.; Zumpt, Expl. Pare nat. Albert Miss. de Witte 87, 1956, 156, figs.; and Novos Taxa ent. 12, 1959, I, figs.

History A. choerophaga is

a

West African species which extends

its area of distribution eastwards up

to

the north-eastern 69

In 1929, Villeneuve described from one male and two females a new species of fly which to him looked very similar to Cordylobia anthropophaga. A careful investigation revealed that it was even generically different from that species, and he called it Neocordyiobia roubaudi Villeneuve. Patton (1936d) reports that this fly ’ is commonly found in and around the burrows of the Aardvark’ and he placed it into the genus Cordylobia, a view which was not accepted by later authors (comp. Zumpt, 1956a}. Neocordylobia roubaudi has a wide distribution in Africa south of the Sahara, but it is definitely not as common as the Auchmeromyia species. Originally described from Senegal and from Uganda, it has been recorded also from

Kenya, Tanganyika, Ruanda-Urundi, Transvaal, Mozambique and Natal. Most specimens were found in the entrances of burrows of the warthog (JPhacochoerus aethiopicus}, which in many areas inhabits the former burrows of the antbear (Orycieropus qfer). Nothing is known about the life-history of this fly, and it can only be surmised that the larvae may have one similar to those of the Auchmeromyia species. But it is also possible that the life-history is similar to that of Cordylobia, or that this species is not even parasitic at all. The

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Key to the Third Instar Larvae or the antbear need not necessarily be the eventual host, which may be quite a different animal only 1 (4) Slits of posterior peritremes slightly sinuous warthog

occasionally using these burrows. A second species of the genus, Neocordylobia tauffliebi., has been described by Zumpt [Nouos Taxa ent. 10, 1958, 8, fig.) from the Congo, and it is known to occur also in the Cameroons and in Ghana. With regard to this species, it is not even known whether it has been found in association with a burrowing animal.

Genus: Cordylobia Grunberg Cordylobia Grunberg, S.B. Ges.

naturf.

(Figs. 79 and 83).......................... 2 2 3’

(2)

Labial sclerites short and hook-shaped (Fig. 82). 2. C. ruandae Fain

4

(1)

Slits of posterior peritremes tortuous (Fig. 88). 3. C. rodhaini Gedoelst

1. Cordylobia anthropophaga (Blanchard)Tumbu Fly

Ochromyia anthropophaga Blanchard, Bull. Soc. ent. Fr. 1893, 127, figs. Cordylobia anthropophaga Grunberg, S.B. Ges. naturf. Freunde Berlin 1903, 412, figs.; Roubaud, Etud. Fa. parasit. Afr. occ. franc. 1, 1914, 114, figs.; BIacklock and Thompson, Ann. trop. Med. Parasit. 17, 1923, 443, figs.; Patton, Ann. trop. Mod. Parasit. 30, 1936, 58, figs.; Bertram, Ann. trop. Med. Parasit. 32, 1938, 433, figs.; Zumpt, Expi. Pare nat. Albert Miss. de Witte 87, 1956, 158, figs.; and S. Afr. med. J. 33, 1959, 862, figs. Cordylobia murium Donitz, S.B. Ges. naturf. Freunde Berlin 1905, 245, figs, Cordylobia gruenbergi Donitz, S.B. Ges. naturf. Freunde Berlin 1905, 252.

develop in skin-boils on mammals, cause coinciding clinical pictures, and their larvae are very similar to one another, so that a generic unification is advisable for practical reasons also. The imagines may be separated by the following key :

(2) In the male, the eyes are close together and width of the frons at the narrowest point measures not more than twice the diameter of the anterior ocellus; outer vertical bristle wanting. In the female, the frons measures about three-sevenths of eye-length at vertex, inner and outer vertical bristles are developed. The body in both sexes is

predominantly yellow-brown, measuring 6-12 mm in length. 1. C. anthropophaga (Blanchard)

(1) Male

3

(4) Smaller species of 7-10 mm body-length.

History The larvae of the Tumbu fly were first discovered by Coquerel and Mondiere in Senegal, in humans and dogs.

They announced their findings in two short communications in 1862 (comp. Blanchard, 1893). The adult fly was unknown to them, and they thought that they were dealing with true oestrid larvae. Infestations were

especially common in the district of Cayor, and the larvae the French inhabitants as ’ vers de was successful in rearing the adults, and sent them to Emile Blanchard who labelled them as Ochromyia anthropophaga. R. Blanchard validated the name in 1893, giving recognizable descriptions of larvae and imagines. However, it was wrong to place this species into the genus Ochromyia Macquart which is nowadays a synonym ofBengalia Rob.-Desvoidy. Grunberg (1903) recognized this error and erected the new genus Cordylobia for the Tumbu fly. Two years later, Donitz (1905) created two more Cordylobia species, namely C. murium and C, gruenbergi which are now regarded as being conspecific with C. anthropophaga. The first sound summary on the knowledge of the Tumbu fly was given by Roubaud (1914), which was followed by the outstanding classical paper by BIacklock and Thompson (1923) on the morphology, bionomics and pathogenesis of this fly, based on very exact investigations in Sierra Leone. Unfortunately, the authors attributed the name Cordylobia anthropophaga to Grunberg, following Austen who thought that Blanchard’s name should be treated as a ’ nomen nudum ’.

were

with broad frons, its width at the narrowest point nearly one third of eye-length or more ; outer vertical bristle present. Females with the frons at vertex from three-sevenths to one-half as wide as one eye is long and the abdomen almost wholly glossy black............................... 3

2

Arista

with relatively short hairs, which do not exceed about twice the width of the aristal base in length. Male abdomen yellow, with the hind margins of the segments broadly blackened. Female abdomen almost totally glossy black. 2. C. ruandae Fain

4

78),

Freunde Berlin 1903,

afr. 3, 1914, 475.

This genus is restricted to Africa south of the Sahara and contains three species, which have been placed by most former authors, and also by Zumpt (1956a), in two distinct genera. However, Cordylobia ruandae in the adult stage is in several respects intermediate between Cordylobia anthropophaga and Stasisia rodhaini, and it is therefore advisable to place all three into one genus. Apart from this morphological fact, all three species

1

Labial sclerites long and curved (Fig.

1. C. anthropophaga (Blanchard)

410. Stasisia Surcouf, Rev. Zool.

(3)

(3) Larger species of 11-14 mm body-length.

Arista with longer hairs up to four times as long as the width of the aristal base. Abdomen in both sexes glossy black, sometimes more or less glossy redbrown. 3. C. rodhaini Gedoelst

70

known

Cayor’.

to

Later, Berenger-Feraud

SUBORDER: BRACHYCERA

The existing literature on C. anthropophaga is fairly extensive and widely scattered, but only a few new facts have been added to the work by Blacklock and Thompson, which is still the basic paper on the Tumbu fly. Morphology Imago (Fig. 75)Stout,

predominantly yellow-brown consisting of two ill-defined, longitudinal vittae covering the area between the dorso-central and intra-alar bristles, or they may be more or less extended to both sides. The abdomen is provided with black, irregular transverse bands which are subject to some variability. The female normally has broader abdominal bands than the male, but the abdomen flies. The thorax shows a black pattern

Figure 75, Cordylobia anthropophaga (Blanchard). Male fly

Figure 76. Cordylobia anthropophaga (Blanchard). Second and first instar larvae. (After Blacklock and Thompson)

becomes almost completely black as in the related Larva I (Fig. 76)The newly-hatched larvae are white C. ruandae. The face is yellow, and the arista shows hairs and measure from 0-75-1 mm in length. Thirteen segon both sides, which are distinctly shorter than in C. ments may be counted, the last two posterior ones are ruandae. The legs are yellow. Length of body is very not yet completely fused as in the later stages. A cephaloskeleton is clearly visible. The segments are variable, between 6 and 12 mm. It is fairly difficult to recognize the adult fly if it has partly covered with minute, backwardly" and also forwardly-directed spines, which are especially dense not been reared from the larva extracted from hosts. Species of Awhmeromyia and Neocordylobia are similar to and striking on the twelfth segment. This segment Cordylobia in general appearance, and are often confused is furthermore provided with three pairs of soft digital with them, even by entomologists. Bengalis species also processes. The so-called thirteenth segment is small, may be misidentined as Cordylobia^ and there are several and has only a few sparsely distributed spines and four other genera in the Calliphoridae, Muscidae and pairs of digital processes, in addition to the tracheal Tachinidae which contain yellow-brown species super- tubes which open dorsally on flattened eminences. These ficially similar to Cordylobia (comp. Zumpt, 1956a). digital processes of the last two segments are of assistance Parasitologists not well-acquainted with the taxonomy of to the larvae in locomotion. They can attach them to the these groups, should always contact an expert when the ground and thus hold themselves erect, while waving the anterior part of the body in search of a host. correct identification of this important fly is needed. never

^ggIt is white in colour, banana-shaped, and on the average measures 0-8 mm in length. There are longitudinal grooves and also a fine hexagonal reticulation on the surface. The eggs are laid in batches of about 100-300.

Larva II (Fig. 76)This stage is quite different from the first instar larva. It is slightly club-shaped and provided with large and black cuticular spines which are irregularly distributed over the third to the eighth segments. The majority of these spines are directed backwards. Segments

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES IX to XI are almost bare when compared with the preceding ones. They are, however, provided with a few rows of small pale spines posteriorly, whereas segment XII is densely covered with these spinules. The thirteenth segment is indistinctly demarcated, devoid of spines, but provided with two pairs of short processes. Each tracheal tube opens through two slightly bent slits. The cephaloskeleton is strongly scierotized, and armed with two hook-shaped labial sclerites. A great variation in size is seen in the older larvae; when arising from the moult of the first stage, they measure 2-5-4 mm in length. Larva III (Figs. 77-79)Great variation in size is normal also in the third larval stage, even from the same host. The fully-grown, mature larva is, on the average, 13-15 mm long. The body is roughly cylindrical in shape, and only twelve segments are clearly separable. The two hook-shaped labial sclerites are projected. On either side of them there is a ridge of yellow scierotized integument bearing a row of about six small teeth. Backwardly-directed curved spines are densely arranged at least up to segment VIII, whereas the last segments are only partly beset with them. But this feature is subject to some variation, and the last segments may also be relatively densely spinulose. The posterior spiracles

open through three sinuous slits situated on a weakly scierotized peritreme. For its differentiation from Cordylobia ruandae and C. rodhami see under these species.

PupariumIt is dark chestnut in colour. The posterior end is very squarely cut off, and the sides run parallel to each other, giving an elongate appearance; it tapers somewhat abruptly anteriorly. The smallest puparium obtained by BIacklock and Thompson measured 6-5 mm, the largest 11-5 mm. Biology The adult flies are rarely on the wing during the daytime, but may be found resting in dark places, and often on the ceiling of huts and verandahs. They are active in the early morning from seven to nine and in the late afternoon from four to six. At night they rest too, but may be attracted by artificial light. Like other Calliphoridae, the adults feed on the juice of plants, for instance bananas, pineapples and other fruits; and also in decomposing animal substances and on excreta. For oviposition, the female is especially attracted to dry sand which has been contaminated with urine or faeces. If the sand is still too moist, eggs are not laid there, but are often deposited nearby on a dry spot. The flies may also be stimulated for oviposition by the soiled napkins of babies. They will not deposit the eggs on the wet parts, but nearby on the dry cloth. If these napkins or other soiled clothes are not properly cleaned and ironed (they may seem quite clean to the human eye and nose), the flies may be attracted to them in the same way as they are to dry contaminated sand. However. the flies will oviposit only in a shady place; if the clothes are hanging in bright sunlight the flies do not. oviposit, and any eggs that have been deposited previously or any young larvae will be killed within a short time by the heat of the sun. It should be emphasized that the Hies never deposit their eggs on the naked skin, nor attach them to the hairs.

Figure 77. Cordylobia anthropophaga (Blanchard). Ventrs larval stage

72

SUBORDER: BRACHYCERA does not follow that after establishment in the hosttissues development to maturity will take place. This may be due to inborn facilities of the host to react successfully to the infection, or to immunological reactions stimulated by a previous infection. Furthermore, even host species which allow normal maturing of Cordylobia larvae show great differences with respect to the number of larvae reaching maturity, compared with the number of first instar larvae that originally invaded the skin. From this last point of view, several species of wild rats are more suitable hosts than dogs normally are. Blacklock and Thompson (1923) have investigated and discussed this fact to some extent. But most probably the breed and size of the dog also plays a role in this respect. Those with a thin, soft skin seem to be more suitable for the development of the larvae than those with a thicker skin. Guineapigs, like domestic rats, are suitable hosts, and the larvae remain, on the average, 8-9 days in the skin, and the adults hatch from the twenty-second to the twenty-fourth day. In some dogs the development of the larvae may not require more time than in rats, but in others it is extended, or the larvae die after having reached the second or third stage. The same is true for humans. Adult flies have also been obtained from monkeys. In the domestic pig, the invading larvae succumb after a short time, and in the fowl almost immediately. The suitability of other wild animals as hosts for the completion of the life-history is a matter still to be

Fertilization and oviposition continues all the year round, but adults as well as maggot infestations are prevalent in the wet season. The female fly lives for about two weeks, rarely up to three weeks, and during this time produces 300-500 eggs, which as a rule arc deposited in two batches. The larvae hatch after one to three days and remain alive without food for about 9 days, while some of them may even persist for as long as 15 days. They remain just below the surface of the sand, waiting for a host. If the surface of the sand is touched by any object, the larvae quickly crawl out. They adhere to grains of sand, and by means of the posterior end, raise the body and wave about quite actively, seeking a host to which they can attach themselves. Once a larva has succeeded in becoming attached to the skin, it immediately starts to penetrate. The time required for complete penetration depends on the thickness of the skin. On a rat or a guinea-pig it takes from 25 seconds to about half an hour. At the end of the process of invasion the larva is covered by a thin layer of skin; its last segment protrudes slightly from the aperture, but can be withdrawn when touched. The first larval stage moults to the second in the tissue of the host after 2-4 days, and the next moult to the third stage takes place on the fifth or sixth day after invasion. In a rat maturity is reached on about the eighth day. The larva then leaves the boil, drops to the ground and pupates there within 24 hours. At room temperature the fly hatches after 10-11 days; at lower temperatures the pupal stage lasts longer. Infections in man are quite common in many parts of Africa south of the Sahara. Of domestic animals, mainly the dog is afflicted and must be regarded as an important reservoir of the Tumbu fly. Other domestic animals found naturally infected are the cat, goat, rabbit and guinea-pig. The following wild animals have been found infected in various parts of Africa: Long-haired

investigated.

Chimpanzee {Pan troglodytes}, Vervet Monkey [Cercopithecus aethiops}, Red Monkey {Erythrocebus patas)^ Leopard {Panthera pardus}, African Wild Cat {Felis Ubyca} in captivity, ’ Mongoose’, Striped Ground Squirrel [Xerus erythropus}, Nile Rat {Arvicanthis niloticus}, House Rat {Rattus rattus), Multimammate Rat {Rattus natalensis), Red Veld Rat {Rattus chrysophilus), Black-tailed Tree Rat {Rattus paedulcus), Rufous-nosed Rat {Oenomys hypoxanthus}, Cape Pouched Mouse {Saccostomus campestris), Cape Greater Gerbil {Tatera afro), African Giant Rat {Cricetomys gambianus}. Whether records of infestations with Cordylobia anthropophaga in antelopes ’ and in goats actually refer to this species or perhaps to C. rodhaini (

is a matter still to be confirmed. Penetration of the skin by first instar larvae has also been observed in chickens, whereas it does not take place in frogs, lizards and snakes. Of the wild animals listed above, the rats form the main reservoirs of the fly in the field.

Pathogenesis

Although the first larval stage of Cordylobia anthropophaga penetrates the skin of many mammals and even birds, it 73

The actual penetration of the first instar larva into the human skin is normally hardly noticeable, but in some persons an intense cutaneous reaction may occur. During the first two days the developing larva causes a slight itching or pricking at intervals which is easily overlooked. The papula increases in size and becomes red, but the itching usually stops for several days. Then the symptoms recur with greater severity and the pain may interfere with sleep. Serous fluid may be exuded, the surrounding tissues becoming greatly indurated and deeply coloured. Even gland enlargement may occur, or there may be febrile reactions and malaise. The lesion now resembles a boil (Fig. 80). The larvae are usually noticed only when the second or, more commonly, the early third stage has been reached. The larva then enlarges its aperture with considerable force, and probably produces a lytic reaction on the tissues. A clear fluid comes from the cavity at intervals, sometimes. stained with blood or with the faeces of the larva. The chief sites of infection in animals are the feet, the genitals, the tail and the axillary region, but in heavy infections any part of the body may be affected, including the nose. One or two larvae normally do not produce obvious distress, but when they are numerous considerable irritation and restlessness may arise, resulting mainly from septic absorption. Where larvae are close together, great swelling and oedema occur, and the tissues may become gangrenous. The larvae often invade the deeper tissues and may cause great destruction leading to the death of the host,

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES A relative immunity resulting from previous infection is acquired by humans, dogs, guinea-pigs and monkeys, but it does not last very long. In man and the dog it apparently does not persist for much over a year at the most. Other animals may also be able to build up a

2. Cordylobia ruandae FainForest Mouse Fly

Cordylobia ruandae Fain, Ann. Soc. beige. Med trap. 33, 1953, 605, figs.; and Rev. Path. gen. Physiol. din. no. 676, 1956, 579; Zumpt, Expl. Pare nat. Albert Miss. de WitteS7, 1956, 160, fig. History This interesting fly was discovered by Dr. Fain near Astrida in Ruanda-Urundi. At first he found two young

Forest mice {Grammomys dolichurus surdaster), which together showed 15 boils containing third instar larvae of a Cordylobia species. Dr. Fain succeeded in rearing three males and three females from these larvae and could state that they represented a new species. After this finding, about 1,000 rats belonging to fifteen different species were checked in this area, and it was realized that only the Forest Mouse harboured the larvae, and no other species. C. ruandae has not yet been discovered in any other part of Africa, in spite of the fact that the host has a very wide distribution. Morphology ImagoThe adult flies are quite similar to C. anthropophaga, but nevertheless very characteristic and not to be confused with it, if investigated properly. The body is glossy yellow-brown and provided with a black pattern, which in the male sex is similar to C. anthropophaga, but the frons is much wider. In the female the abdomen is almost completely black except for the basal part of tergite I+IL Furthermore, the arista has much shorter hairs than in C- anthropophaga. Length of body varies between 7 and 10 mm.

Egg and larval stages I and II are

Figure 80. Cordylobia infection in a European child. (After Loewenthal)

not yet known.

Larva III (Figs. 81-83)C. ruandae resembles G, anthropophaga far more in this stage than in the adult stage. The segments are densely beset with spinules, which are slightly smaller and closer together than the average in C. anthropophaga. However, I got the impression that this feature may vary to some degree in the larvae of the Tumbu Fly. Another feature, given by Fain (1953) seems to be more reliable, namely the shape of the cephaloskeleton, and especially that of the mouth-hooks-

temporary immunity to Cordylobia infection, but nothing is known. This would be of special interest with respect to wild rats, the main reservoirs in the field. Adult rats are often found infected with a great number of larvae, which cause the death of the host. It may be that those rats had not had a previous infection, or that the immunity had broken down. These are the conclusions drawn by Blacklock and Thompson. But it may also be possible that at least some species of rats are not able to build up an immunity at all.

The slits of the posterior spiracles are more slender and less sinuous than normally found in C. anthropophaga, but I do not know whether this feature too is constant enough to be useful for a differential diagnosis. The larvae before me measure from 5 to 12 mm in

Distribution

Cordylobia anthropophaga is restricted to Africa south of the Sahara, but is widely distributed within this region. There are, however, many large areas which so far appear to be free of this fly. In Southern Africa (comp. Zumpt, 19596), it has been found as far southwards as the Orange Free State, Swaziland and Natal. Great care must be taken in recording the distribution from clinical cases in humans and dogs. Very often the infection has been acquired on a trip to more northern parts of the continent, and is noticed only after returning home, where the fly does not as yet occur. In this way untreated dogs may help to spread the fly to new places.

length. PupariumPractically anthropophaga.

not

separable from that of C.

Biology The adults have probably a crepuscular mode of life. They are sometimes found in houses surrounded by hedges of euphorbes {Euphorbia tirrucalli} and liliaceous plants {Dracaena flagrans] which form the haunts of their hosts near Astrida. As already mentioned, the only host

74

SUBORDER: BRACHYCERA so far known is the

Pupae

are

Forest Mouse {Grammomys dolichurus).

commonly found in the tree-nests of this

rodent.

Pathogenesis Nothing is known about pathological effects caused by the infection. Fain does not say anything about extremely high infections with larvae in single host specimens, and he also does not mention an apparent high mortality among the mice. Distribution

The fly is so far known only from the environs of Astrida in Ruanda-Urundi. 3. Cordylobia rodhaini GedoelstLund’s Fly

Cordylobia rodhaini Gedoelst, Arch. Parasit. 13, 1909, 538, figs.; Patton, Ann. trop. Med. Parasit. 30, 1936, 62, figs.; Bertram, Ann. trap. Med. Parasit. 32, 1938, 341, figs. Stasisia rodhaini Surcouf, Rev. Zool. afr. 3, 1914, 477; Rodhain and Bequaert, Bull. sci. Fr. Belg. (7) 49, 1916, 262, figs.; Zumpt, Expl. Pare not. Albert Miss. de Witie 87, 1956, 161, figs. History

In 1905, Gedoelst described a fly-larva which had been extracted from the skin of the arm of ’ commandant Lund ’, most probably in the Belgian Congo. He could not fix a proper systematic position for this larva, but recognized only that it was not a true oestrid larva and thought it might belong to the Muscidae. Four years later, Gedoelst was able to study the female adult of his ’ larve de Lund ’ and assigned it to the genus Cordylobia^ an opinion held also by several later authors, for instance by Patton (1936a). It was Surcouf who eventually received a male fly and once more took up taxonomic investigations. He came to the conclusion that it should be placed into a distinct genus, a view which was accepted by most later authors. The only detailed study of the life-history of C. rodhaini is by Rodhain and Bequaert (19I6a).

Figure 81. Cordylobia ruandae Fain. Ventral view of third larval stage

0-5 mm

Figure 82. Cordylobia ruandae Fain. Cephaloskeleton of third larval stage

Morphology

Imago (Fig. 84)A big fly measuring from 11 to 14 mm in length. The thorax is black-brown, partly yellow-brown to a variable extent, and densely covered with a yellow toment. Distinct dorsal longitudinal vittae are not developed. The abdomen is normally glossy black and does not show a pollinosity, but specimens occur in which it is shining red-brown. Head predominantly yellowbrown; the eyes are, in both sexes, broadly separated from one another, the frons at vertex measuring one-third to three-sevenths of eye-length. The wings are tinged with

brown.

EggSimilar to that of C. anthropophaga, but uniformly smooth. It measures 0-8-1 mm in length.

Figure 83. Cordylobia

i

indae Fain. Posterior stage

75

spiracle of third larval

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES PupariumGeneral appearance as in C. anthropophaga, from which it is separable by the features as described for the third larval stage.

Biology The life history is evidently quite similar to that of C. anthropophaga, but it has not yet been as intensively studied. The adults also feed on fallen fruits, fermenting vegetables, and on faeces. They are on the wing mainly in the early morning hours and in the late afternoon.

Rodhain and Bequaert observed the occurrence of

oviposition on dry places contaminated with excrement. One female deposited about 500 eggs in four batches, the first 20 days after hatching from the puparium, the last 27 days after hatching. This fly died 7 days later, after having lived for 34 days. A male was kept alive in capFigure 84-. Cordylobia rodhaini Gedoelst. Adult fly. {After Rodhain and Bequaert)

Larva I (Fig. 85)The newly-hatched larva is about 1 mm long and quite different in shape from that of C. anthropophaga. The usual twelve segments are present, the first two incompletely separated. The cephaloskeleton is well marked. The second segment bears, immediately behind the labial sclerites, a range of spines directed forwards and demarcating the border of the first segment. The spinules of the following segments are only sparsely denticulated. According to the drawing published by Rodhain and Bequaert the larva of C. rodhaini lacks the soft digital processes on the last segment, an easily recognizable feature useful for separating it from C. anthropophaga.

Figure 85. Cordylobia rodhaini Gedoelst.

First

tivity for more than 42 days. The larvae hatched after 2-4 days. The experimental infection of man and guinea-pig was difficult, invasion of the skin taking several hours. Only one larva completed its development in the guinea-pig, requiring about 3 weeks. This indicates that man and guinea-pigs are probably not very suitable hosts, although a complete development may take place in humans (see Broden and Rodhain, 1909). In the African Giant Rat, which must be regarded as one of the main reservoirs in nature, the development of the larva requires 12-15 days. The mature larvae leave the boils spontaneously and pupate after 12-48 hours. The pupal stage lasts 23-26 days, and the first batch of eggs is deposited after 17-20 days, so that the whole life-cycle (egg to egg) is estimated to last 55-67 days.

larval stage. (After

Rodhain and Bequaert)

Figure 86. Cordylobia rodhaini Gedoelst. Second larval stage,

Larva II (Fig- 86)The second larval stage is very similar to that of C. anthropophaga; the spines on the anterior segments, however, are relatively larger and fewer in number. There are no digital processes on the last segment.

Larva III (Figs. 87 and 88)The length of 23 mm. The spines

a

mature larva may reach are distinctly longer and

less dense than in the two other Cordylobia species, and not partly grouped in transverse rows. Between the mouthhooks there is a dark bar of spiny processes. The easiest feature, however, by which to separate C. rodhaini from the other two Cordylobia species lies in the structure of the posterior spiracles, which open through three long and very tortuous slits, of which at least one may show

fragmentation in

two.

76

SUBORDER:BRAGHYCERA Pathogenesis The lesions in man are more painful than those of

C. anthropophaga, perhaps due to the greater size attained by the larvae. However, infestations are rare, and normally only one or two larvae are found. But there are exceptions, and very heavy infestations in humans have been known to occur. Broden and Rodhain (1909) reported a case

of 92 larvae, and Gedoelst mentioned one of 87

larvae in a European from the Congo. The boils were located on the back, the arms and the chest. Bertram (1938) saw a case in Mamfe, Nigeria, concerning a 51year-old man, from whom 16 larvae were extracted from discharging pustules on the neck and the left arm. In other humans C. rodhaini boils were found on the scalp, below the lower eyelid, on the trunk, and on the limbs. It is not known whether infections in smaller animals

end fatally.

Distribution C. rodhaini is a fly of the moister parts of tropical Africa, especially the forest regions. It has been recorded from Senegal to the Central African rain forests, and southwards to Angola and Rhodesia.

Genus: Booponus Aldrich Booponus AIdrich, Philip?. J. Sci. 22, 1936, 141. Pavlovskiomyia Grunin, Parasit. Shorn. 9, 1947, 185. The adults are small, predominantly yellow-brown flies, which have, in contrast to Elephantoloemus indicus, a blackish pattern on the thorax, and the arista shows short but distinct hairs on both sides. So far there are four species described, two from the Oriental region and two from the Eastern Palaearctis. The larvae are skinparasites of bovids and deer, but the immature stages of one species from Burma have not yet been discovered. A key to the larval stages cannot be given, because they have not yet been adequately studied. The adults may be distinguished as follows : 1 Infections of humans with the larvae of C. rod/mini have been recorded several times from various parts of tropical Africa, but they are evidently not nearly as common as those with C. anthropophaga. Infections of domestic animals are not yet known. The following wild animals have been found to harbour second and/or third larval stages : Cirne’s and Stuhlmann’s Checkered Elephant Shrew {Rhynchocyon cirnei and R. stuhlmanm), Mona Monkey {Cercopithecus mono). Bay Duiker {Cephalophus dorsalis}, Black-fronted Duiker {Cephalophus nignfrons}, Blue Duiker

{Cephalophus monticold), Grey Duiker {Sylvicapra grimmia}, Punctate and Common Sun Squirrel {Heliosciurus punctatus and H. gambianns}, Sikapus’ and the Speckled Harshfurred Rat {Lophuromys sikapusi and L. ftavopunctatus], Rufous-nosed Rat {Oewmys hypoxanthus), African Giant Rat {Cricetomys gambianus)., Bocage’s Gerbil {Tatera valida). Antelopes and the African Giant Rat are to be regarded as important reservoirs of this parasite.

(2) Body almost wholly yellow-brown;

mesonotum

without dark pattern, and with only three acrostichal bristles behind the suture. 5-6 mm. 1. B. intonsus AIdrich

2

(1) Body with a dark pattern on thorax and abdomen. Mesonotum with four or five acrostichal bristles behind the suture.......................... 3

3 (4) Species from Burma. 6 mm. Larval stages and host not known. 2. B. aldrichi Sen^White a.o, 4 (3) Species from the Asiatic part of the Palaearctic 5

region (USSR) ............................ 5 (6) Frons with 10-14 pairs of parafrontal bristles.

6-7

mm.

3. B. inexpectatus (Grunin) 6 (5) Frons with 7-10 pairs of parafrontal bristles. 5-6 mm. 4. B. borealis

77

Rohdendorf

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES /. Booponus intonsus AldrichOriental Foot

Maggot

Booponus intonsus Aldrich, Philipp. J.

Sci. 22, 1923, 141 ; Woodworth and Ashcraft, id. ibid. 143, figs.; Sen,White, Aubertin and Smart, Fauna Brit. India, Diptera 6, 1940, 78 ; Kranefeld and Van der Schaaf, Ned.-ind. Bl. Diersgeneesk. 49, 1937, 360, figs. Cordylobia intonsa Patton, Ann. trap. Med. Parasit. 30, 1936, 65, fig.

History The Oriental Foot Fly was discovered by Woodworth and Ashcraft (1923) who studied its life-history and pathogenesis in the Philippines, gave descriptions of the early stages and sent three females to Aldrich, who described the imago and founded the genus Booponus on this new species of myiasis-producing fly. In the district of Los

Banos, Luzon, water-buffalo, cattle and goats

were

infected.

When in 1936 Patton published a drawing of several features of the third larval stage, he mentioned that apparently since 1925 no further cases of foot-myiasis due to B. intonsus had been located in the Philippines. Kranefeld and Van der Schaaf (1937), however, report from Celebes that the species had been observed in the northern parts of this island in cattle since 1926.

Morphology ImagoBoth sexes have an almost completely yellowbrown body, only the abdomen may show a few irregular and ill-defined dark markings. The eyes are separated by a broad, subparallel frons, measuring at vertex in the male four-sevenths of eye-length, and five-sevenths of eye-length in the female. The arista is strongly thickened in the basal two-fifths and clearly shows short hairs on both sides. Parafrontalia and -facialia, also the buccae, are densely beset with black hairs; the bucca is about half as high as the eye is long. Body-length 5-6 mm.

Figure 89. Boopom intonsus Aldrich. Empty and living eggs. {After Woodworth and Ashcraft)

deposit their eggs on the hairs. Favoured places for oviposition are the areas between the toes, at the heel under the dew claws, and less commonly as high up as the knee. The incubation period varies considerably, possibly being dependent on certain stimuli. Under laboratory conditions the larvae hatch after 3-5 days, the head pointing towards the base of the hair. They migrate towards the coronary band where they enter the skin. They then lie nearly parallel to the surface, leaving their posterior end exposed. In goats larvae have been found not only on the hooves, but also on other regions of the leg, for instance the knee. This is perhaps due to the comparatively thinner and more tender skin on this host.

The length of the larval period probably ranges from 2 to 3 weeks. The mature larvae leave the boils and drop to the ground, where they pupate. The pupal period lasts approximately 10 days.

^S (Fig. 89)Elongate,

ovoid, dull greyish white. It is attached to a hair by a gelatinous secretion, mostly but singly, sometimes up to four may be found on one hair. Its average length is 0-875 mm.

Larvae I and // have been only incompletely described. Larva III (Fig. 90)Body greyish white, robust, cylindrical. Posterior end rounded and invaginated, with one small pair of tubercles dorsally, another pair ventrally, and a third pair latero-ventrally to the peritremes, which show three almost parallel slits- Segments with irregular rows of short, pale brown, reclinate spines. The length is given from 8-5 to 10 mm.

PupariumRegularly ellipsoidal, brown

to black.

The

anterior spiracles are protruding.

Biology Woodworth and Ashcraft say that the adults may be seen hovering around the legs of water buffaloes and cattle. They alight on the lower portions of the legs and

Figure 90. Booponus intonsus Aldrich. Ventral and dorsal view of third larval stage. Centre; large posterior spiracles. {After Woodworth and

Ashcraft)

78

SUBORDER: BRACHYCERA Larva IIIDensely spinulose on all segments. Posterior spiracles with nearly parallel slits. Body-length of mature larvae 9-10 mm.

Pathogenesis Infestation with the maggots causes lameness, especially in the hind legs. The number of larvae in one animal may be very high, up to 100 have been counted in the legs of a water-buffalo. The condition is found predominantly in the dry season, and may clear up spontaneously after the onset of the rains as a result of the muddy state of the ground. In dry pastures, trenches are dug for the cattle to get mud on their legs.

Puparium not described.

Biology B. inexpectatus is strictly host-specific to the Musk Deer {Moschus moschiferus}. The larvae develop in the skin, mainly of the back. In the Sikhota Alin Mountains every Musk Deer is infested, even the young ones which are

Distribution

Booponus infonsus is so far known only from the Philippines and from Celebes. 2. Booponus aldrichi Sen.-White, Aubertin and Smart

Booponus aldrichi Sen.-White, Aubertin and Smart, Fauna Brit. India, Diptera 6, 1940, 81, fig. History This species has been based on a female caught on the wing at Zibingi in Burma. Nothing is known about its life-history. The mesonotum is said to be blackish except laterally, gold-dusted anteriorly, with traces of four black stripes. Pleura and scutellum clear yellow. The abdomen is predominantly blackish-brown, but the anterior part of tergite I+II is yellow. Wings hyaline, with a yellow tinge, legs yellow. Length : 6 mm.

Figure 91. Booponus inexpectatus (Grunin). Ventral view of second larval stage.

(After Grunin)

3. Booponus inexpecfatas (Grunin)Musk Deer Skin Maggot

Pavlovskiomyia inexpectata Grunin, Parasit. Shorn. 9, 1947, 185, figs. Cordylobia {Pavlovskiomyia) inexpectata Grunin, Rev. Ent. URSS. 30, 1949, 441, figs. Booponus inexpectata Zumpt, Flieg. pal, Reg. 64i, 1956, 82, fig. History

In 1937 Musk Deer in the Sikhota Alin Mountains, Siberia, were found to be heavily infested with skin maggots. Some adults were reared successfully which Grunin recognized as being new, and on which he founded the new genus Pavlovskiomyia. In a later paper he reduced his genus to a subgenus of Cordylobia,, after having studied Patton’s paper (1936a) on this subject. Zumpt eventually placed it into the genus Booponus.

Morphology ImagoThe body is predominantly yellow-brown, but pleura partly greyish and mesonotum -with ill-defined, longitudinal dark stripes. The arista is shortly pilose on both sides. Bucca about two-fifths of eye-length. The flies measure 6-7 mm in length. .

Egg &nd first larval stage

born early in summer. The average number of maggots from a single deer amounts to 700-800, but up to 2,000 have been counted. The development of the larvae lasts approximately 2 months; they leave the boils from mid-August to mid-September and hibernate as pupae. The imagines are on the wing from mid-June to mid-

July. There is a second species of myiasis-producmg fly living in the Musk Deer, namely Hypoderma moschiferi

Brauer. Pathogenesis The deer during the time of infection are very much weakened and lose their normal caution, so that the animals may often be approached very closely.

are not known.

Larva II (Fig. 91)Club-shaped, with strong spines on segments III to VIII, the others finer spinulose. Body length up to 5 mm.

Distribution So far only known from the Sikhota Alin Mountains, Siberia, but most probably distributed farther afield.

79

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Larva HICylindrical, if mature it measures up to 10 mm length. Anterior spiracles with 22-23 holes, posterior spiracles with the usual three slits. The segments are densely spinulose as in B. inexpectatus. The larvae of these two species are evidently very similar to one another.

RohdendorfRed Deer Skin Maggot borealis Rohdendorf, Rev. Ent. URSS 38, 1959,

4. Booponus borealis

Booponus

in

583, figs.

History This species was discovered by a Russian veterinarian near the mouth of the Yenise,in the district of Jermakowsk,

Puparium not described-

where the larvae parasitize the Siberian Red Deer, Rohdendorf received eggs, specimens of the first and third larval stages, and several adults, from which he described this new calHphorid fiy.

Biology B. borealis is so far known only from the Red Deer {Cervus elaphus) in Northern Siberia, and it is perhaps also strictly host-specific like other Booponus species. The larvae develop in skin boils, and eggs have been

Morphology found on the animal, but it is not mentioned whether ImagoThe adults are said to be similar to those of were attached to the naked skin or to hairs. There B. inexpectatus, but the frons is a little broader in both they are probably two generations annually. The pupal sexes, the buccae are higher, there are 7-10 pairs of period lasts about 3 weeks. parafrontal bristles (10-14 pairs in B. inexpectatus}, and the basal thickened part of the arista is relatively longer. Pathogenesis The body-length lies between 5 and 6 mm. Nothing is known about pathological reactions due to the larvae. in 0-9 about mm length. EggBoat-shaped, measuring It is white to light yellow in colour and provided dorsally Distribution with a broad, reticulated stripe. B. borealis is so far known only from the type locality. Larva I (Fig. 92)Rohdendorf described and figured the first tnstar larva in detail, and pointed out that the Genus: Elephantoloemus Austen Elephantoloemus Austen, Proc. zool. Soc. Lond. 1930, 679. The only representative of the genus, E. indicus Austen, is quite similar in morphological respects to the Booponus species; the arista, however, shows hairs on the dorsal side only. With reference to the host-relationship, Elephantoloemus is restricted to the Indian Elephant, whereas the Booponus species parasitize bovids and deer. 1. Etephantoloemus indicus AustenIndian Elephant Skin Maggot

Elephantoloemus indicus Austen, Proc. zool. Soc. Lond. 1930, 680, figs.; id. ibid. 1932 (1933), 869 figs. Cordylobia {Elephantoloemus) indica Patton, Ann. trop. Med. Parasit. 30, 1936, 60, figs. Booponus indicus Sen.-White, Aubertin and Smart, Fauna Brit. India, Diptera 6, 1940, 79, figs.

Figure 92. Booponus borealis Rohdendorf. Dorsal view of first larval stage. (After Rohdendorf)

newly-hatched larva is shorter than the egg-shell, measuring only about 0-7 mm in length. The segments are partly provided with stout spinules. The pseudocephalon beside the mouth-hooks shows a pair of comb-like structures of strong spines.

Larva II is

not known.

80

History The first short report on ’ warbles or swellings’ in the skin of the Indian Elephant {Elephas maximus) was apparently given by Colonel G. H. Evans in his book Elephants and their Diseases, which appeared in 1910 in Rangoon, Burma. He discussed their pathogenicity in a few words, and thought that these larvae belonged to the Oestridae. He probably did not see any adults. Only in 1930 was Austen able to describe the male and female adults, after he had received several reared specimens from the Veterinary Department of Burma. In 1932 he was able also to publish a diagnosis and drawings of the third larval stage. In the scientific literature I found only two more original references to this interesting fly. In 1936 Patton figured and described the male and female genitalia, and Sen.-White, Aubertin and Smart in the Fauna of

SUBORDER: BRACHYCERA closely set, short, transverse rows of minute, triangular and almost colourless spinules.

Puparium not described. Biology and Pathogenesis Evans writes in his above-mentioned book; that ’ the elephants from which these bots were taken literally swarm with swellings in all partshead, ears and body. The scars of recent eruptions are in some parts of the body so closely pitted as to impart to the skin a honeycomb appearance, showing that thousands of the parasites have burrowed out during the last few months. Curiously enough, only the elephants brought from India last year are affected, and no doubt their general unhealthy appearance is due to the presence of myriads of bots beneath the skin.’ He says, furthermore, that the larvae were well-developed towards the end of April and May, and that they produced inflammation and suppuration about them, causing warbles.

British India (1940) placed it into the genus Booponus, and compared the imago with the two other species of this genus known to occur in the Oriental region. This is certainly a very poor record for a fly of evidently great veterinary importance. Astonishingly little has also been done with respect to other arthopod parasites of the Indian Elephant.

Morphology Imago (Figs. 93 and 94}A compactly built little fly of 4-5-6 mm in length. The two sexes are similar to one another, even with respect to the broad frons. The body is yellow to orange with blackish markings on the thorax and the abdomen. These markings cover the anterior Figure 95. Eleph, larva! stage in part of the mesonotum to a varying extent, but shoulders and the scutellum remain light; pleura also partly darkened. The last two segments of the abdomen are There were also tiny white eggs of about 1 mm in always black, but the dark colouring may spread to the length observed on the skin. They were firmly glued to preceding segment. the wrinkles. It has not been confirmed that these eggs actually belonged to Elephantoloemus. Egg and larval stages I and 11 are not known. Larva III (Fig. 95)The mature larva is about 9 mm long. The segments are dorsally and ventrally provided with

Distribution So far this fly seems to be known only from Burma.

81

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIAS IS- PRODUCING FLIES Figure 96(right). Protophormia terraenovae (Rob.Desvoidy) Posterior view of last segment of thirdstage larva. (After Schu.

Genus: Protophormia Townsend Protophormia Townsend, Smithson. misc. Coll. 51, no. 1803, 1908, 123. This genus is monotypic, containing only one species in the Holarctic region. /. Protophormia terraenovae (Rob.-Desvoidy)Subarctic Blowfly

Phormia terrae-novae Rob.-Desvoidy, Ess. Myod, 2, 1830,

467; Zumpt, Flieg.pal. Reg. 64i, 1956, 93, figs. Protophormia terrae-novae Seguy, Encycl. ent. (A) 9, 1928, 168, figs.; Hall, Blowflies of N. America 1948, 174, figs.; -

Figure 97(below), Protophormia terraenovae (Rob Desvoidy). Posterior peri-

Schumann, Wiss. Ztschr. Univ. Greifswald 3, 1954, 260, figs. Musca groenlandica Zetterstedt, Insecta Lapponica 1838, 657. Phormia nignpalpus Rob.-Desvoidy, Hist. nat. Dipt. Ew. Paris 2, 1863,846. Protophormia. a^urea Hennig (nee Fallen), Arb. physiol. angew. Ent. Berl. 6, 1939, 360, figs.

tremes of

third-stage larva. (After Schumann)

History This fly is very common in the cooler parts of the Holarctic region, where it replaces the Chrysomya species of the subtropical and tropical areas. Together with Phormia regina (Meigen), the Black Blowfly of American authors, the genus Protocalliphora and a few other genera, it forms the calliphorid tribe Phonniini, which is completely restricted to the Holarctis. The two species Phormia regina and Protophormia terraenovae are closely related to one another and united by some authors in one genus, but the separation into two distinct genera has now been more widely accepted. P. terraenovae is involved in wound-myiasis in Europe and in North America; P. regina acts in the same capacity in the New World, but is not yet known as a myiasisproducing fly from the Old World.

Morphology ImagoBody dark metallic blue, in certain lights more or less bluish green to black. Legs black. The mesonotal bristles are variable in number and length, and not altogether clearly separable from the other hairs, but the presutural acrostichal bristles are always indistinct. The alar squama is dark brown and densely beset with black hairs. Body-length : 6-11 mm.

bands are present only ventrally. Spines almost all wedgeshaped, with two or three points. The larva reaches a length of up to 6mm.

Larva III (Figs. 96 and 97)The last segment is characterized by strongly developed, fairly pointed tubercles. The posterior peritremes show a weakly developed button. Anterior spiracles each with nine to twelve branches. Cephaloskeleton without specific features. Spinulation similar to that of the second larval stage. The mature larva may attain a length of 17 mm.

PuparwmLight brown

to

almost black, with the external

EggAbout

I -5 mm long, whitish, elongate, slightly curved, with the chorion longitudinally fluted.

features of the mature larva.

Larva ICephaloskeleton strongly developed. There are complete anterior spinose bands on the second to ninth or tenth segments, but incomplete ones on the following segments. Narrow posterior ventral bands are present on the sixth to eleventh segments.

Biology P. terraenovae is saprophagous and appears in the early spring. It prefers relatively low temperatures for breeding, which explains its abundance in the subarctic region and its occurrence in higher altitudes in the temperate zones.

Larva. IIAnterior

spiracles each with ten to twelve ones with two ovate apertures. In contrast with the first larval stage, the second has welldeveloped tubercles on the anal segment. Second to eleventh segments with complete anterior spinose bands, and tenth and eleventh segments also with complete

branches, posterior

posterior bands. On segments VI

to

IX the posterior 82

Pathogenesis In Scotland the fly is known as an occasional sheep mviasis fly, not only as a secondary invader, but in certain areas also as a primary one (MacLeod, 1937 ; Morison, 1942). It appears before L. sericata, and is later replaced. by this species in primary strikes.

SUBORDER: BRACHYCERA There are also several records from bird-nests, where -P. terraenovae attacks the nestlings and causes a malignant wound-myiasis (comp. Peus, 1960), but some, if not all, of these records may be due to a confusion with Protocalliphora.

Distribution P. terraenovae is distributed all over the Holarctic region, being especially common in the northern parts, while in the southern parts it is more or less restricted to higher altitudes. It has been taken within 550 miles of the rswth Pole.

Genus: Protocalliphora Hough Protocalliphora Hough, Ent. News 10, 1899, 65. Avihospita Hendel, Wien. ent. Ztg. 20, 1901, 29. Philomis Enderlein (nee Meinert), Tierwelt Mitielew. 6 (2), 1936, 210Apaulina Hall, Blowflies-of North America 1948, 179. OrneocalUphora Peus, Dtsch. ent. 2. {N.F.} 7, 1960, 198. Trypocalliphora Peus, Dtsch. ent. 2. {N.F.} 1, 1960, 199. The genus Protocalliphora is of Hoiarctic distribution and contains a fairly large number of species in the Old World as well as the New World, but the Palaearctic and the Nearctic regions evidently have no species in common. Earlier records of P. ckrysorrfwea (Meigen) and P. azurea (Fallen) from the United States refer to other species. Specimens of the Nearctic P. hvmdo Shannon and Dobroscky recorded by other authors from Europe, are regarded by Peus as belonging to a distinct species. The taxonomy of this genus is very difficult. Pens’ paper on the Palaearctic species (1960) and Hall’s on those of the New World (1948) have brought it no nearer to its solution. Hall proposed to separate the American species generically from ProtocaUiphora and created the genus Apavlina for them, a step which was rejected by Zumpt (1956&), based on a communication from C. W. Sabrosky, Washington. The main objection to Peus’ paper is that he did not compare the Palaearctic species with those of the Nearctic region, which comprise some intermediate forms between Protocalliphora and his new genus Trypocalliphora created for the species developing subcutaneously. According to Sabrosky (by letter), it should be regarded as ’ a subgenus rather than a distinct genus ’. I was able to study a third instar larva of P. lindneri (Peus), which differs greatly from those of P. azurea (Fallen) and P.falcoziSeguy. The figures by Rohdendorf (1957) also reveal peculiar features. It may therefore be justified to keep Trypocalliphora as a distinct genus. This should only be decided when the whole genus has been better studied and especially when the immature stages of more species from the Paiaearctic as well as the Nearctic regions are known. Peus also erected a subgenus OrneocalUphora within the genus Protocalliphora. The separating feature of OrneocalUphora and Protocalliphora s. str. lies only in the absence or presence of a sexual dimorphism in colouring. This proposal must be vigorously rejected. One of Peus’ new species is based on one female only, another apparently 83

briefly described, but not named. A third species, namely P. asiatica Zumpt, is listed under ’ species new one is

incertae sedis’. These few facts show clearly that the taxonomic situation of the Protocalliphora species is still very unsatisfactory, and therefore I refrain from giving a key to the imagines. Those who want to study this difficult group of flies should start bv consulting the papers by Peus (1960), Gregor and Povolny (1959), Zumpt (1956&) and Hall (1948). The taxonomy of the larval stages has as yet hardly been touched. Coutant (1914) gave a description of a second and a third larval stage under the name of ’ P. azurea ’ from North America, accompanied by several figures; Hall (1948) of the third instars of the American, species P. metallica (Townsend), and P. avium Shannon and Dobroscky. Engel (1920) compared the third instar larva of P. chrysorrhoea (Meigen) with that of P. azwea (Fallen); and Seguy (1941) described the second and third instars ofP.falcozi Seguy, while Rohdendorf (1957) described the third instar larva of ’ P. chrysorrhoea’ which is said by Peus (1960) to be P. azurea (Fallen). The descriptions and figures of these authors reveal that there are differentiating features present which would allow treating of the larvae on a taxonomic basis. This is however a matter to be left to the future. The Protocalliphora larvae are blood-sucking or live subcutaneously on nestlings of a great number of mostly passeriform birds. It is not yet known whether the flies are oviparous or larviparous, but probably they are egg-laying. The pupation takes place in the nests. /. Protocalliphora

Musca

a^urea

azurea (FallenCommon Bird Blowfly

Fallen, K. Vet. Acad. Handl. Stockholm 1816,

245.

Protocalliphora azurea Zumpt, Flieg. pal. Reg. 64i, 1956, 95, figs.; Gregor and Povolny, Ada Soc. ent. Cechoslov. -56, 1959, 37, figs.; Feus, Dtsch. ent. Z. {N.F.} 7, I960, 216, figs. Protocalliphora chrysorrhoea Engel, 2. wiss, InsektBiol. 15, 1920, 257, figs.; Rohdendorf, Rev. Ent. URSS 36, 1957, 119, figs. Phormia caerulea Rob.-Desvoidy, Ess. Myod. 2, 1830, 466. Musca sordida Zetterstedt, Insecta Lapponica 1838, 657. Luciiia dispar Dufour, Ann. Soc. ent. Fr. (2) 3, 1845, 205, figs. History P. azurea, the most common ’ Bird Blowfly ’ in Europe, already described early in the last century, and the closely related P. chrysorrhoea only 10 years later, in 1826. Both names have since then been used several times for American species which actually belonged to other species. The study of the American fauna was not taken up before 1924 by Shannon and Dobroscky, to which revision Hall (1948) added some more species, but none of them is identical with any Palaearctic form. P. a^urea was re-described as Phormia caerulea by Robineau-Desvoidy and as Musca sordida by Zetterstedt. The latter name has often been used by later authors following Hennig (1939), who had suppressed P. azurea. was

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES on the incorrect assumption that it was a synonym of Protophormia terraenovae (R.-D.). Other authors used P. chrysorrhoea for P. azurea, or they regarded P. az.wea and P. chrysorrhoea as belonging to one species. Following

the anterior spiracle with eight branches, whereas P.falcozi shows five to seven, but this may lie within the

interspecific variability. PupariumIt is

a suggestion by Hennig, Zumpt (19566) lowered P. chrysorrhoea to an ecological subspecies of P. awrea. This complicated synonymy was discussed and finally cleared up by Peus (I960).

Morphology Imago (Fig. 98)The

among the

nest

the average 8 mm long and found free material.

on

Biology The larvae are blood-sucking and have been found in the nests of a great number of various species of birds, the majority of which belong to the Oscines of the order Passeriformes- Gregor and Povolny (1959) and Peus (I960) list members of the following families of Oscines : Wagtails {Motacilla alba and M. cinerea). Flycatchers

flies are characterized by a sexual

dimorphism, the males being metallic dark blue with a weak pruinosity on the thorax, the females more or less bluish green, with a distinctly denser pruinosity, and with

Figure 98. Protocalliphora awrea (Fallen). Female fly. {After Lindner)

{Muscicapa hypoleuca and M.. albicollis}, Thrushes and Chats (Turdus merula, Oenanthe oenanthe, Phoenicums ochrurus, Erithacus rubecula), Warblers {Sylvia borin, S. cantillans, S. atricapilla, Phylloscopus collybita, P. trochilus, P. sibilatnx}^ Swallows and Martins (Hirundo mstica^ Delichon urbica)., Wrens {Troglodytes troglodytes). Shrikes [Lamus collurio), Tits {Parw major^ P. afer, P. caeruleus, P. cristatus, P. Body-length: 9-13mmatricapillns), Starlings {Sturnus vulgarise Creepers [Certhia Egg and the first two larval stages are not known. familiaris}, Canaries and Seedeaters {Embem.a citrinella, Larva III (Figs. 99 and 100)The third instar larva was Serinus canarius), and Sparrows {Passer domesticus}. The briefly described by Engel (1920) under ’ P. chrysorrhoea ’, only non-Oscine mentioned by Gregor and Povolny is and more detailed figures were given by Rohdendorf the European Wryneck {Jynx torquila). There are, however, more species to be expected as (1957), under the same name. I cannot take any features from these papers which would allow a clear separation hosts for P. azwea, and former authors have already from P. falcozi, and indisputably correctly identified mentioned additional species. Some of these records are larval specimens are not before me. Rohdendorf figures certainly not reliable, and also the taxonomy of the

more or less clearly defined longitudinal stripes on the thorax. Frons in the male narrow, but slightly variable, measuring at its narrowest point one-seventh to oneninth of eye-length; in the female the frons measures at vertex about two-thirds of eye-length. The thoracic squama is brownish, with a darker-coloured margin.

84

SUBORDER:BRACHYCERA Protocalliphora species has only recently been studied on a

ment of

modern basis so that these former records need confirmation. The percentage of nests infested with maggots of Protocalliphora varies not only with the geographical areas, but especially with the bird-species. Some, like the nests of Tits and Warblers, are favoured, others are more rarely or even only occasionally infested, like the nests of the Wryneck. But very little has yet been done in this field. The number of larvae present in a single nest seems normally to be low, but very heavy infestations may occur and Lindner (1957) mentioned a case where 155 larvae were counted in a single nest of a Serin

cent

Stuttgart in Germany, Lohrl found that 22 per of the nests of Serins were infested, one-eighth of them so heavily that all the nestlings were dying. The corpses, or even very weakened birds, may then become

[Serinus canarius). The larvae are fully grown within one week and have then reached a length of up to 13 mm. Pupation takes nests and, according to several authors, the flies hatch from 10 to 23 days afterwards, dependent on microclimatic conditions. The hibernation is passed in the adult stage. In the temperate zone of Europe there may be two generations a year. Like many other blowflies, the adults are found on flowering plants, and not on carcasses or other decomposing organic matter.

place in the

Pathogenesis The damage caused by the maggots depends, according to Lohrl (1949), on the number of larvae present in the nest, on the size of the larvae compared with that of the nestlings, on the number of nestlings, and on their

Figure 100. Protocalliphora azurea (Fallen). Anterior spiracle of third larval stage. [After Rohdendorf)

nutritional state. Five to ten maggots in the nest of the Collared Flycatcher {Muscicapa albicollis} arc usually not dangerous. The nest of this flycatcher normally contains six nestlings, so that on the average two larvae feed on one bird. If this proportion rises, however, owing to a higher maggot infestation or the death of some nestlings or early fledglings, the weakest nestling or even the whole brood may succumb from loss of blood. In the environ-

recorded from bird’s-nests. Birds bigger than flycatchers probably have more resistant nestlings.

secondarily infested with other bloivfly-larvae, such as those of Protophormia. terraenovae, which has also been

Distribution

Protocalliphora azurea is widely distributed in Europe, from Scandinavia and Great Britain southwards to North Africa and eastwards at least to the Urals, but it may even be found much further to the East. 2. Protocalliphora isochroa Pens

Protocalliphora isochroa Peus, Dtsch. 1960, 218.

ent.

2.

{N.F.} 7,

History

f "//li ,’"

"TIII ii,, 1,1 f.mT’. ,.^\\V-

i/^fi^/^ ^^/’^fu’l}})^^^

n\" 11

X---

This species was based on a pair from Tschernyi-Jar, S.E. Russia, which was originally placed by Zumpt in P. a^urea. Peus could find no differences in the male terminalia, but found some in the external morphology which he thought to be distinct enough to justify a specific separation from P. awrea.

\^

The flies were reared from larvae in the nest of a Tit {Remiza pendulinus}.

Vr perkremes.

SUBORDER: BRACHYCERA and Bequaert (1919). Some of the specimens seen by these authors were 20 mm long, the shortest about 10 mm. They are more elongate than those of the third stage, and the spinulation is much more delicate, but otherwise similarly arranged. The posterior peritremes show two slits each, which are sinuous, and not simply bent as in G. wnjungens.

Larva HI (Figs. 156-158)The mature larva reaches a length of up to 40 mm. The colour is whitish to yellow, and when approaching maturity, irregular dark brown spots appear. The body is composed of the usual twelve segments, but the separation of the first two is ill-defined and detectable only in stretched specimens. The third to eleventh segments are provided with bands of three to four rows of spines which, in each band, decrease in size from the first to the last row. The band is interrupted dorsally, narrowly on the tenth segment and broadly on

PupariumDeep truding.

black, with the anterior spiracles pro-

Biology and Pathogenesis The immature stages of G. pauesii are found in the Black as well as the White Rhinoceros {Diceros bicornis and D. simus). The second and third instar larvae are found attached to the wall of the stomach, apparently without causing severe pathological effects. The eggs are firmly attached to the host’s skin, mainly on the head, at the base of the ears, on the neck and the shoulders. Rodhain (1915) obtained eggs from a caged fly and gave a description and figure of the egg, and later he and Bequaert (1919) were able to describe the first larval stage which had been extracted from an egg. It is still unknown under what circumstances the larvae hatch and how they find their way to the stomach. The mature

Figure 1158. Gyrosligma pavesn (Corti). Third instar larvae attached to the wallII of a rhinoceros stomach. (Reproduced by courtesy of Stuckertberg)

Figure pwesii

larvae are passed through the anus. The pupal stage lasts about 6 weeks. Adults have been reared or caught on the wing in Zululand from March to the beginning of May and from October to December. From a batch of larvae isolated on sand on 19th February two males and four females hatched between 31 st March and 2nd April. The females lived in the cage for 3-5 days and produced eggs. A pair from Fort Jameson in N. Rhodesia hatched on

156(above). Gyrostigma (Corti). Third instar larva in ventral view

Figure 157(right). Gyrostigma pwesii

(Corti). Posterior peri-

tremes of three specimens, in order to show the variability. {After

^w^yy^-

Enderlein}

the eleventh segment. The fifth

I Oth February. to

.

eighth segments have

pad laterally and posteriorly, each with three to five The structure of the posterior peritremes is very characteristic; they are united medially as in the genus Gasterophilus. The three slits in each peritreme are strongly tortuous and extremely long. Their pronounced variability was studied by Enderlein (1901, see Fig. 157). a

Distribution

spines.

Gyrostigma pavesU mav be expected wherever its hosts still occur in Africa. I have seen specimens from Zululand, N. Rhodesia, the North-Eastern Congo, Kenya and Tanganyika, and the species is also recorded from Ethiopia, Gallaland and the Chari district.

131

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES 2. Gyrostigma conjungens EnderleinEnderlein’s Rhinoceros Bot Fly

Gyrostigma conjungens Enderlein, Arch. Naturgesch. 67 (Beiheft) 1901, 24, figs.; Rodhain and Bequaert, Bull. sci. FT. Belg. 52, 1919, 444, fig. Spathicera conjungens Sjostedt, Kilimanjaro-Mem Exp. 190519062 (10), Diptera, 1908, 15, fig. Stomachomyia conjungens Enderlein, Stett, ent. Zfg. 72,

of the scutellum. Wings relatively short and do not reach beyond the tip of the abdomen, predominantly hyaline, a blackish infuscation is restricted to some terminal parts along the veins. Legs yellow, partly

1911, 144. History G. conjungens was described by Enderlein in 1901 from the third larval stage found in a Black Rhinoceros near Kilimanjaro, and for a long time this type series was the only one known. Only in 1959 did the East African Veterinary Research Organisation in Kenya procure a few larvae, recovered from. a Black Rhinoceros in the Makueni district. On my urgent request to try to rear the adults, J. G. Tremlett eventually succeeded in hatching two females. These were sent to me and a description was published (Zumpt, 1962&).

Morphology

Imago (Figs. 159 and 160)The head is yellow and reddish-brown. Frons broad, almost parallel, measuring at its narrowest point 1-2 times the length of one eye. An ocellar triangle and ocelli are not developed. Face yellow, the parafacialia are narrower than in G. pauesii. Antennal groove with a narrow and low median keel. Second antennal segment as large and deeply split as in G. pavesii, but the ventral part is shorter and provided with three finger-like lobes. Thorax is covered with long yellow and reddish hairs, the latter forming two pairs of stiff brushes at the margin

Figure 160. Cyrostigma conjungens Enderlein. Lateral view of antenna

brownish. Abdomen yellow to yellow-brown, laterally and ventrally partly blackish, with yellow hairs which are denser and longer and also more yellow-brown at the hind margins of the segments than on the anterior parts. Length of body : 20-24 mm.

Egg andjirst larval stage are not known. Larva II (Fig. 161)There are three specimens before me which measure 10-11mm in length, but they are not ripe for moulting and those which are may reach a much greater length. With respect to shape and spinulation they are apparently very similar to G. pavesii. I have not yet seen the second instar larvae of this species; according to the description and figure by Rodhain and Bequaert (1919), however, the spines in G. conjungens may be a little more prominent, but otherwise they are arranged as in G. pavesii. The main differences are again found in the shape of the slits in the posterior peritremes. In G. conjungens they are simply bent, in G. pavesii they are sinuous.

Larva III (Fig. 162)The

mature

larva reaches a length

of up to 24 mm. The spinulation is very similar to that of G. pavesii; actual constant differences are very few

Figure 159. Gyrostigma conjungens Enderlein. Fei

and concern only the arrangement and number of certain spines, as studied by Enderlein (1901). The main and very characteristic separating feature lies in the shape of the slits in the posterior peritremes, which are simply bent in G. conjungens, but tortuous in G. pavesii.

132

SUBORDER: BRACHYCERA Biology and Pathogenesis The two adults which J. G. Tremlett hatched came from a Black Rhinoceros (JDiceros bicomis) in the Tsavo National Park in Kenya. The larvae were isolated on the 23rd June, 1961, and the flies appeared on the 6th August, 1961. Nothing is known of pathological effects.

Distribution The larvae which Enderlein studied came from the Kilimanjaro district, while those sent to me by the East African Veterinary Research Organization were collected in the Makueni district and the Tsavo National Park.

0-5 mm Figure 161. Gjyrostigma conjimgens Enderlein. Posterior peritremes of second larva] stage

3. Gyrostigma sumatrensis Brauer Asiatic Rhinoceros Bot Fly

Gyrostigma sumatrensis Brauer, Verh. z,ool.-bot. Ges. Wieh 34, 1884, 269, figs.; Rodhain and Bequaert, Bull. sci. Fr.Belg.52, 1919, 442, fig. History Of this species only the third instar larva is known, several specimens of which were recovered from the Asiatic Two-horned Rhinoceros (Didemoceros sumatrensis} from Sumatra. One of these animals died in the Zoological Gardens of Hamburg, another in Leipzig in Germany. It is known only that they had been imported from Sumatra. Since then no more specimens have found their way to a scientist.

i

conjungens Enderlein. Posterior peritremes of third larval stage

PupariumIn older specimens completely black. The two specimens before me have hatched from puparia which are strikingly different in outer shape. The one is much broader and shorter (17 to 6 mm) than the other, which is slender and elongate (19 to 5mm). This difference is reflected in the shape of the abdomen of the adults, the one being stouter than the other.

Morphology Larva HI (Fig. 163)A single larva before me is 29 mm long; Brauer in his description gave 31 mm. In general appearance it is quite similar to G. pavesii. The bands of spines are composed of three rows which are narrowly interrupted dorsally on segment III to X and broadly on segment XI. Lateral pads are present on segment V to VII as in G. pavesii, but they are weakly developed and’ bare of spines (rarely one present) on the eighth segment. The posterior peritremes have slightly tortuous slits and. are, with respect to shape, somewhat intermediate be-/ tween G. conjungens and G. pavesii.

Figure 163. Gyrostigma sumatrensis Brauer. Posterior peritremes of third larval stage

Hi

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES SUBFAMILY

:

COBBOLDIINAE

Genus: Platycobboldia Townsend Platycobboldia Townsend, Ent. News 45, 1934, 277. Bequaertomyia Seguy, Gen. Ins. 205, 1937, 366. The only representative of the genus, P. loxodontis, is -well characterized in the adult stage and separated from Rodhainomyia roverei and Cobboldia elephantis by features -which are regarded as of generic and even greater importance in other groups of flies. The larval stages of these three species, however, are extremely similar, and reveal that they are actually more closely related to one another than can be deduced from the imagines. The same conclusion must be drawn from the known facts of

their life-histories.

bright orange, whereas the thorax and abdomen show a uniform, metallic dark blue colouring; the legs are deep black. The whole wing is tinged with black. In the male the frons at its narrowest point is about as broad as one eye is long, and is -distinctly broader in the female. Furthermore, the male frons is quite densely beset with black hairs, whereas in the female only a few pale and much shorter hairs are visible. Dorsum of thorax in the male with a short, dense, black pilosity; in the female the dorsum is almost bare and therefore more glossy. The abdomen too shows a different appearance in the sexes, being glossy dark blue and densely pilose in the male, but shorter and less densely pilose and covered with a greyish blue pollinosity in the female. The bodylength of both sexes is between 10 and 13 mm.

1. Platycobboldia loxodontis (Brauer)Blue Elephant Stomach But Fly

Cobboldia elephantis africani seu loxodontis Brauer, Denkschr. Akad. Wiss. Wien., math.-nat. Kl. 64, 1897, 267. Cobboldia loxodontis Roubaud, Et. Fa. parasit. Afr. occ.fr. 1, 1914, 206, figs.; Rodhain and Bequaert, Bull. sci. Fr. Belg. 52, 1919, 412, figs.; Gedoelst, Ann. Parasit. hum. comp. 1, 1923, 354, figs. Platycobboldia loxodontis Zumpt, Proc. R. ent. Soc. Lond. (5), 27, 1958,13. Cobboldia parumspinosa Gedoelst, Rev. Zool. afr. 4, 1915, 158. History The larva was discovered by Dr. J. Kirk on one of Livingstone’s expeditions, in the stomach of an elephant shot on the Zambezi river, and eventually received by Blanchard who described and figured it as ’ ? Cobboldia sp.\ The first description with nomenclatorial standing was given by Brauer (1897), after he had obtained some third instar larvae from the African explorer 0. Neumann. Brauer and also Gedoelst (1915) believed that Blanchard was dealing with a different species, and the latter named it Cobboldia parumspinosa. Some time later Gedoelst was able to study all three larval stages, and came to the conclusion that BIanchard’s and Brauer’s larvae were conspecific. Adults of both sexes had been received by Rodhain and Bequaert from the Congo and were described in 1915 and 1919. Townsend proposed placing Cobboldia loxodontis into a distinct genus, a view accepted by Seguy (1937) and Zumpt (19586).

Figure 165. Platycobboldia loxodontis (Brauer). Anterior part of first larval stage. (After Gedoelst)

Morphology

Imago (Fig. 164)Body flattened dorso-ventrally, with .the frons strongly protruding. In both sexes the head is

Figure 164. Platycobboldia loxodontis (Brauer). Wing. {After Rodhain and

Bequaert)

Figure 166. Platycobboldia loxodontis (Brauer). Ventral and dorsal view of first larval stage. (After Gedoelst)

134

SUBORDER: BRACHYCERA

Figure 168(above). Platycobboldia loxodoniis (Brauer). Ventral view of pseudocephalon of third instar larva

Figure 167(Ieft). Platycobboldia kxodmtis (Brauer). Dorsal and ventral view of third instar larva

Figure 169(right). Platycohboldia loxodontis

(Brauer). Posterior peritremes

of third

instar larva

Egg~This stage has

not been especially described for saw eggs attached to a piece of tusk of an elephant which were quite similarly arranged, and shaped as are those described for Rodhainomfia rmerei.

P. laxodonfis, but I

Larva I (Figs. 165 and 166)This instar was described and figured by Gedoelst (19234), who studied four specimens in the moulting stage which had reached a length of 6-7 mm. The body is clearly composed of twelve segments, and its appearance is already reminiscent of that of the third stage. The pseudocephalon shows two pairs of ocelli, and behind the projecting mouthhooks it is provided with a broad spinulose collar. The cephaloskeleton has three basally-united labial sclcrites on either side, quite an outstanding structure. The arrangement of spinules on the following segments may be taken from Gedoelst’s figures. The posterior spiracles each have two small orifices.

Larva J/The specimens before me are 7-10 mm long. The armature is quite similar to that of the following stage, but the posterior peritremes show the usual two slits.

Larva in (Figs. 167-169)This instar is from 10

to 23 mm long; fully stretched mature larvae may even reach a length of 28 mm. The mouth-hooks are large and projecting, single pointed. Antennal protuberances with two ocelli each. Anterior spiracle with a short, clubshaped tube. The mouth cavity is surrounded by a

135

crown of teeth which are especially long and sharp on the ventral edge, Dorsally the segments bear bands of spines composed of two to six rows from the third to the ninth or tenth, and ventrally down to the twelfth segment. These bands become narrower and are partly interrupted medially on the posterior segments. Posterior lateral spinulose lobes are present on segments V to VII, and bear three to six spines each. The peritremal cavity of the last segment can be completely closed, the upper and lower lips are provided with numerous denticles and together bear three pairs of fleshy tubercles. The three slits of the posterior united peritremes are almost parallel.

PupariumBlack-brown, 15-19 mm long.

Biology

As already mentioned, the eggs are found attached to the base of the tusks, and all three larval stages occur in the stomach of the African Elephant {Loxoaonfa africana), which is the only host. The larvae are not, unlike those of Gasferophilus in equids, attached to the stomach wall, but move freely in the stomach contents, mainly between the wall and the partly digested food. The larvae reach maturity in the stomach and then crawl up to the mouth, from which they are probably ejected when the elephant is feeding. Pupation takes place in the soil, and the flies hatch after 2-3 weeks. In southern Africa adults hatched in January, July and October, so that no seasonal restriction seems to exist. All three larval stages may be

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES found simultaneously in the stomach, and the adults may be expected at any time of the year. The life period of the adults is short. Copulation takes place immediately after hatching from the puparia, and in captivity the flies die within a few days.

Pathogenesis The presence of the larvae in the stomach evidently causes no pathological effects.

Distribution

Figure 171. Rodhainomyia roverei (Gedoelst}. First larval stage.

P. loxodontis is known from many localities in South Africa, the Rhodesias, Mozambique, East Africa, Tanganyika, the Congo, Cameroons, Ghana, and the Ivory Coast, and probably occurs wherever the host still exists.

{After Rodhain and Bequaert)

Genus: Rodhainomyia Bequaert Rodhainomyia Bequaert, Bull. Soc. ent. FT. 89, 1920, 68. This genus too is monotypic and closely related to Platycobboldia, in spite of the fact that the imago of R. roverei, in contrast with P. loxodontis, shows a number of hypopleural bristles, a feature which counts as a family characteristic in other groups of higher flies. 1. Rodfiainomyia roverei (Gedoelst)Green Elephant Stomach Bot Fly

Cohboldia roverei Gedoelst, Rev. Zool. afr. 4, 1915, 156. Cobboldia chrysidiformis Rodhain and Bequaert, Bull. Soc. Path. exot. 8, 1915, 773, figs.; and Bull. sci, Fr. Belg.

52, 1919, 421. figs. Rodhainomyia chrysidiformis Zumpt, Proc. R. ent. Soc. Lond. {B} 27, 1958, 14. History Rodhain and Bequaert (1915

c.

=

cervical area ; a.sp.=

very stout fly of 13-15 mm bodylength. The ground colour is black, but the scutellum and part of the frontal stripe are red-brown in the specimen before me. The pollinosity is silvery white and in the female densely covers the outer two-thirds of the parafrontalia, whereas the inner third is glossy and shows a characteristic, very coarse sculpture, consisting of dense, oblique ripples. Mesonotum and abdomen are also partly polltnose, the latter with a tessellate pattern. The pilosity is short and deep black. Eyes in male large and closely approximated ; in the female they are smaller and widely

153

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIAS IS-PRODUCING FLIES conceal the posterior spiracles; a row of spines is present on each lip. The peritremes are semicircular, with big pores and a button near the inner margin. The mature larva reaches a length of up to 30 mm.

PupariumBlack, measuring 20-23 mm in length.

(b)

Cc; Figure 202. Pharyngobolm africaniis Brauer: (a) and (6) head of male fly in frontal and lateral’ lew; (c) wing. {After Rodhain and Bequaert)

separated from one another, frons at vertex measuring four-fifths of eye-length. Antennal groove wide and deep, provided with a narrow median convexity of even height. Antennae dull black. Mouth-parts reduced to a median globular cone and two swellings below it. The wings are hyaline, only slightly infuscated at base. Legs completely black and very stout.

Larva I is

Figure 203. Pharyngobolus africanus Brauer: (a) third larval stage in dorsal view; (A) second larval stage laterally. {After Rodhain and

not known.

Larva II (Fig. 203)Two specimens before me are 14 and 15mm long. They are relatively more slender than the third instar larvae, but otherwise very similar to them, with an almost identical arrangement of blacktipped spines. The posterior respiratory groove may be completely closed. Larva III (Figs. 203 and 204)The body is yellow and reddish brown, and provided with fairly regular rows of completely dark brown, strongly-pointed spines. Mouthhooks strongly protruding; antennal lobes each with two ocelli. Segments HI to X dorsally in the anterior half with two rows of spines, one of large spines, the other of smaller ones, which are partly irregularly placed. In the posterior half of each segment only one row of big spines is present. The ventral side of the segments shows a similar arrangement of spines, but in the anterior half a third row of partly irregularly-placed spinules is visible. Dorsally segment XI bears spines only in the anterior part, whereas ventrally a posterior row is present. The last segment is bare dorsally, but ventrally an anterior, irregular and partly double row of spines is developed. The two lips are huge and can completely 154

Bequaert)

SUBORDER:BRACHYCERA while skinning some specimens, discovered a number of short, white maggots in the tracheae crawling about in the mucus. He sent them to Froggatt (1913), who recognized a new oestrid species related to Oestrus ouis. He mentioned the ’ very distinctive characters’ of the larvae and the ’ remarkable situation of the developing maggot, not in the frontal sinuses and nasal cavities of the head, as in the sheep nasal fly, but in the windpipe, close to the throat’. Froggatt proposed the name Oestrus macropi, the Kangaroo Bot Fly. Townsend (1916) established the new genus Tracheomyia for this species, and in 1953 Paramonov was able to describe the female adult from three specimens which had been reared. The latest paper is by Grunin (1961), who described and figured the second larval stage, redescribed the third stage, and confirmed the relationship of the Kangaroo Bot to Oestrus, but also its generic distinctness.

Biolog}’ and Pathogenesis

The larvae have been found attached to the wall of the pharyngeal region in the African Elephant (Loxodonta africana). Rodhain and Bequaert (1919) stated that the mature larvae are excreted with the faeces, but this is probably not so. The elephants in the Zoological Garden of Basle are said to have sneezed out the maggots, and I have records according to which single fully-grown larvae were recovered from the trunk. The pupal period of the Basle fly lasted from the 22nd February until the I0th March, 1953. As yet nothing else is known about the biology, nor have any pathological effects of the infestation come to our knowledge. Rodhain and Bequaert say that in the Congo every elephant examined was found to harbour some larvae in the throat.

Distribution P. africamis has been recorded from many places in the Congo, and I have also received a few specimens from Uganda and Northern Rhodesia.

Morphology Imago (Figs. 205 and 206)The ground colour of the head is reddish-brown to yellow covered by a silvery-white pruinosity. The parafrontalia are not provided with large pits as in Oestrus, but have only shallow and small foot-prints bearing black setae; the parafacialia are completely smooth and bare of setae. The antennal groove shows a median keel, which is broadly interrupted in the middle. Mesonotum medially blackish, laterally reddish, and provided with a pair of median, glossy black stripes in the presutural area, which continue into a pair of subquadrangular vittae just behind the suture. The remaining part of the thorax is covered for the greater part with a white to yellow poltinosity. The postscutellum is well-developed. Wing with a characteristic venation, densely yellow on the outer part. Legs yellow. Abdomen black, densely covered with a white pollinosity which, however, leaves several ill-defined spots of variable shape free. Length of body about 9 mm.

Genus: Tracheomyia Townsend Tracheomyia Townsend, Canad. Ent. 48, 1916, 160. This genus which is so far monotypic, is restricted to Australia and shows some relationship to the African genus Kirkioestrus Rodhain and Bequaert. It is peculiar among the Oestrinae because the larvae develop in the tracheae of kangaroos. 1. Tracheomyia macropi (Froggatt)Kangaroo Throat Bot Fly

Oestrus macropi Froggatt, Agric. Gaz. N.S. W. 913, 1567, fig. Tracheomyia macropi Paramonov, Ann. Meg. nat. Hist. (12) 6, 1953, 198, figs.; Grunin, Rev. Ent. URSS 40, 1961,929, figs. History

In 1912 during a large-scale shooting of kangaroos in the "Wallgett district. New South "Wales, T. B. Broughton,

Larva I is not known.

(Froggatt). Wing of female fly. (After Paramonov)

Figure 206. Tracheomyia macropi

Larva II (Fig. 207)Grunin describes the second instar larva as more or less semi-transparent, measuring 4-5 mm in length. The ventral side is concave, the dorsal convex. The last two segments are bent upwards. The spinulation is apparently similar to that in the third stage. Posterior peritremes each with about 40 pores.

Larva 111 (Figs. 208-210)The mature larvae reach a length of up to 14mm and are of oval shape. The Figure 205. Tracheomyia macropi (Froggatt). Female head in frontal view. {After Paramonov)

mouth-hooks are very distinct, the antennal lobes have two ocelli each. The segments are provided ventrally with

155

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES broad anterior bands of broad scales, the posterior margins of which are serrated. Dorsaily only segments II to IV bear anteriorly uninterrupted bands of spines, which are, however, different in shape from those of the ventral surface and which form broad and simplypointed scales. Similar scales are found on aU lateral bulges. Furthermore, the anal and the peritremal cavities are surrounded by dense spines. Posterior peritremes closed and shaped as in Oestrus.

Puparium not described.

Figure 209. Tracheomyia macropi (Froggatt). Third larval stage: (a) ventral scales; (6) = anterior spiracle; (c) cephaloskeleton. {After Grunin)

Biology and Pathogenesis It is known only that the larvae are found in the trachea where they apparently feed on the mucous secretions. The infection is not normally severe. Froggatt mentioned that as a rule one or two larvae were found in each host, and that only occasionally were there as many

^9lh.,

Figure 207 (above). Tracheomyia macropi (Froggatt) : (a) and (6) dorsal and lateral views of second larval stage ; (c) posterior spiracles.

(After Grunin} Figure 210, Tracheomyia macropi (Froggatt). Third posterior view

as half-a-dozen recovered. There are therefore no significant pathological reactions to be expected. Cook’s Kangaroo (Macropus canguru}, the Red Kangaroo (M. rufus) and the Dusky Kangaroo {M. robustus) have been recorded as hosts. TracheFigure 208 (left). omyia macropi (Froggatt). Ventral view of third larval stage. (After Grunin)

156

Distribution

Tracheomyia macropi has so far been found only in kangaroos from (Queensland and N.S. Wales.

SUBORDER: BRACHYCERA

Genus: Kirkioestrus Rodhain and Bequaert Kirkia Gedoelst, Bull. Soc. Path. exol. 7, 1914, 210 (preocc.). Kirkioestrus Rodhain and Bequaert, Bull. Soc. Path. exot. 8, 1915,694. Neokirkia Townsend, Insec. Inscit. menst. 6, 1918, 153. There are two species known which infest antelopes of the tribe Alcelaphini. Adults are extremely rare in

brown, the third for the greater part deep black; arista bare and yellow-brown. Parafrontalia and -facialia without grooves or tubercles, but, like the rest of the face, with dense, fine, erect hairs. Thorax with a yellow and black pollinosity which forms a pattern dependent on the light incidence. The abdomen shows a similar pollinosity and a black pattern, forming patches in the median and hind parts of the segments. Legs yellow-brown, with the femora and tibiae partly blackened. The wings are hyaline, with a few brownish tinges; terminal part of the third longitudinal vein ^4+5) not recurrent; bend of media with a long appendage. Body-length: 11-12 mm. Larva I is not known.

collections, and I have never succeeded in rearing them myself. The imago and third larval stage are well characterized and readily separable from other Oestrinae. The adults may be distinguished as follows: 1

(2) Terminal part of the third longitudinal wing-vein (^+5) not recurrent (Fig. 211). Legs yellowbrown, with the tibiae and femora partiv blackened. 11-12 mm. 1. K. minutus (Rodhain and Bequaert)

2

(1)

Larva IIA few larvae before me measure 7-12 mm in length. They are white, with a spinulation similar to

Terminal part of the third longitudinal wing-vein 215). Legs wholly reddish-brown.

recurrent (Fig. 13-14 mm.

2. K. blanchardi (Gedoelst) 1

2

Key to the Third Instar Larvae segments ventrally without short rows of spines postero-laterally. Lower lip of last segment with about half-a-dozen spines. 1. K. minutus (Rodhain and Bequaert)

(2) Body

Figure 211. Kirkioestrus minutus (Rodhain and Bequaert). Wing of female fly. [After Rodhain and Bequaert)

(1) Body segments V

to XI ventrally with short rows of spines postero-laterally. Lower lip of last segment with about a dozen large spines. 2. K. blanchardi (Gedoelst)

1. Kirkioestrus minutus (Rodhain and Bequaert)Common Nasal Bot Fly

Kirkia minuta Rodhain and

Bequaert, Bull. Soc. Path.

Hairy

exot.

8, 1915,456. Kirkioestrus minutus Rodhain and Bequaert, Bull. sci. Fr. Belg. 50, 1916, 159, fig. Oestrus compositus Gedoelst, Rev. Zool. afr. 4, 1916, 260.

History Rodhain and Bequaert described this species from several third instar larvae and one hatched female. The larvae had been recovered from Hartebeest and Korrigum in the Congo. The only later record is by van Emden (1944), who added the Blue Wildebeest to the list of hosts.

Morphology Imago (Figs. 211 and 212)I have received one male and female, but the former was in such a poor state of preservation that only the terminalia and the wings could be used for microscopic preparations. The following description is therefore based on the female specimen. Body predominantly reddish brown, with a black pattern on thorax and abdomen. It is beset with dense, fine hairs of pale and black colouring. Antennal groove deep, with a low, medially interrupted, keel-like median convexity. The first two antennal segments are yellow-

one

the third stage, but the spines are pale and the posterior peritremes are small and sometimes narrowly open at the inner margin.

Larva III (Figs. 213 and 214)The yellow-brown and relatively slender,

mature larva is Antennal lobes each with three pseudocelli, but one of them is very small. Segments III to XII with anterior bands of spines on the ventral side only. Each band consists of two to

157

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MY IASTS-PRODUCING FLIES African antelopes : Blue Wildebeest {Connochaetes taurinw), Common Hartebeest {Alceiaphus buselaphus), Lichtenstein’s Hartebeest {Alcelaphus lichtensteinii}, and the Korrigum

[Damaliscus korrigum). Figure 213 (left). Kirkwestrus (Rodhain and Bequaert). larval stage in ventral

As in other Oestrinae of the tropical parts of Africa, there is apparently no dependence on the season. Third instar larvae have been found in February, March, July, October and December ; the two adults mentioned above were hatched in September and March. The pupal period lasts about 1 month. No more biological data are known, and no observations have been made about the pathogenesis of the larvae.

\

Distribution

K. minutus is known to occur in the Congo, RuandaUrundi, Tanganyika, Kenya, Natal, Transvaal, Bechuanaland and S.W. Africa. 2. Kirkioestrus blanchardi (Gedoefst)Blanchard’s Hairy Nasal Bot Fly

Kirkia blanchardi Gedoelst, Bull. Soc. Path. exot. 7, 1914,211. Kirkioestrus blanchardi Rodhain and Bequaert, Bull, sci, Figure

214(below).

Kirkioestrus

^ gelg. 50, 1916, 158

^e^^th^d^

^oelst, Bull. Soc. Patk. 7, 1914. 212. ^ -^surcouf, and Bequaert, Bull. Fr. Kirkzoestrus

Rodhain

e.ot.

sci.

Belg. 50, 1916, 153, figs.

Figur( 215. Kirkioestrus blanchardi (Gedoelst). Wing of female fly. {After Rodhain and Bequaert)

History The rather complicated history of this species has been discussed by Zumpt (1962(!). It was quite inadequately described by Gedoelst under two different names in the same paper. In 1915 Rodhain and Bequaert already suggested that both names may refer to the one species only, but van Emden (1944) still did not dare synonymize them definitely.

three rows; the third row is composed of small spines and is often irregular. Posterior peritremes in a shallow groove, the upper margin of which is spineless whereas the lower margin protrudes strongly and bears about half a dozen large and strongly pointed spines. The third instar larvae measure from 12 to 28mm in length.

PupariumThe ventral side is flat, the dorsal side strongly convex. The case measures 16 mm in length and 7 mm in width.

Biology and Pathogenesis The second and third instar larvae have been found in the nasal cavities and frontal sinuses of the following

Morphology Imago (Fig. 215)I have no adults before me, but according to the description given by Rodhain and Bequaert (1916A) they should be rather similar to those of K. minutus. A characteristic feature lies in the wing-venation, the terminal part of ^+5 being recurrent. The legs are said to be wholly bright brownish-red. The ground colour of the abdomen is black-brown and reddish, covered with a golden yellow pollinosity in the anterior part, and a greyish white one posteriorly. The adults which the Belgian authors saw measured from 12-5 to 14 mm in length.

Larvae I and // are not described.

158

SUBORDER: BRACHYCERA Larva HI (Figs. 216 and 217)The mature larvae reach a length of up to 30 mm. The general body shape is as in K. minuius, but the third instar larva is easily separable from this species by the presence of short rows of spines on the lateral and posterior part of segments V to XI. The spinulation on the anterior part of the ventral segments is similar to that in K. minutus, and the dorsal side is bare as in this species. The lower lip of the peritremal groove bears a greater number of spines, numbering about a dozen. PupariumIt has been figured by Rodhain and Bequaert (1916^) under K. surcoufi from a specimen measuring 19 mm in

length and 9 mm in width.

Biology and Pathogenesis The only biological data known are that the larvae have been found in the

Common and Lichtenstein’s Hartebeest {Alcelaphus buselaphus and A. lichtensteinii}. Distribution I saw some of the larvae from the Congo on which Rodhain and Bequaert based their studies, and alsoreceived a few specimens from the Beira district in Mozambique. But the species was originally described from West Africa (Lake Chad area), and it is also recorded from the Ivory Coast. I have never found this type of larva in southern Africa.

Genus: Rhinoestrus Brauer Figure 2l6(nght).Kirkioesirusbl<m(Gedoe)st). Third larval stage in ventral view

chardi

Figure 217 (below). Kirkioestrus blanchardi (Gedoelst). Posterior view of third larval stage

Rhinoestrus

Brauer,

Wien. ent.

Ztg. 5, 1886,

Hippooestrus Townsend, J.N.Y.

ent.

289.

Soc. 40, 1932, 447.

The genus Rhinoestrus so far comprises eleven species, and all those infesting Artiodactyla {Potamochoerus, Phacochoerus, Hippopotamus, Giraffa, Ovis and Antidorcas), are strictly host-specific. Only those developing in the naso-pharyngeal cavities of the perissodactyl genus Equus are known to occur in several species, for instance R. usbekistanicus in the horse, donkey and in Burchell’s Zebra, R. purpureus in the horse and donkey, and R. steyni in both species of zebra in southern Africa. The various species of the genus Equus seem to have a great physiological similarity, judging from their fauna of arthropod parasites (for instance the genus Gasterophilus} as well as from their helminths. On the other hand, Burchell’s Zebra and the Springbuck each harbour two different species of Rhinoestrus (a larger and a smaller one), and the domestic horse is the host of as many as three Rhinoestrus species, which may occur simultaneously in Central Asia. The artiodactyl genera listed above are quite different from, and fairly unrelated to, one another, the host-list itself makes a rather arbitrary impression. I believe that other genera too will prove to be hosts of distinct Rhinoestrus

species. The imagines of Rhinoestrus are not easily separable, some experience and comparative material is necessary for succeeding in a correct identification. The taxonomic features of the adults are quite distinctive, but there is a certain variability and it is difficult to describe them satisfactorily. Those of the third instar larvae are better explained, and the beginner will probably have less difficulty diagnosing the maggots than the adults. and

Key to the Imagines 1

with glossy brown or black tubercles, each of which normally bears a backwardlydirected seta. Parafacialia with dark, black or brown spots which are often developed as

(14) Abdomen

................................

2

(9) Bigger species of 11-15 mm body-length.....

3

papulae 2

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES 3

(4)

The mesonotal pair of longitudinal stripes are narrow, well-defined and nearly reach the transverse suture (see Fig. 235). They are glossy in full extent. Thorax predominantly

14

(1) Abdomen without tubercles, with only small granules

on which the setae are inserted, or almost smooth, Parafacialia without dark spots, the setae are located in little crater-like ’ foot-prints ’, but these are yellow or yellowbrown like the remainder of the parafacialia.. 15

dark-brown; abdomen black. 10. R. antidorcitis Zumpt and Bauristhene 4

15 (16) African species. Wing with the discal cross-vein (r-m) situated opposite or a little before level of the apex of the subcosta (sc). 11-13 mm

(3) The mesonota! pair of prcsutural, longitudinal stripes are iH-defined, and due to a dense wrinkling, dull, or at most glossy only anteriorly. ................................... 5

(Fig. 225). 6. R. nivarleti Rodhain and

5

(6) Body predominantly reddish brown. The

ill-

16

defined pair of mesonotal stripes is reddish and glossy in the anterior part. Species of the

(15)

costa

Palaearctic region.

3. R. 6

(5) Body predominantly dark-brown

(8) Tubercles of parafrontalia another, ones close

8

at most two or

Key 1

a

(2) Smaller species of

to the Third

Instar Larvae

Ventral armature consists of quandrangular two to four uninterrupted rows the anterior part of each segment (see Fig. 244). Dorsal armature absent except on the second segment. 11, R’. vanzyli Zumpt and Bauristhene

on

together (males only considered). 5. R. hippopotami Grunberg

(7) Tubercles of parafrontalia confluent, only

(2)

scales, forming

isolated from one three neighbouring

in the upper part more or less isolated

(Fig. 232).

yellow-

2

few

(1) Ventral

of segments

armature

3

(To

4

(8) Dorsal side of segments III to XII bare,.... 4 (5) Latero-ventral bulges of segments with spines (see Fig. 230).

5

(4) Latero-ventral bulges of

7, R. phacochoen Rodhain and It is inadequately described and not before me in the adult stage).................................. 10

Bequaert, also belongs.

11

of

4. R. steyni Zumpt 8-11 mm body-length.

this group No.

10

consists

pointed spines. Dorsal armature is present or absent.................................. 3

(males

only considered). 9

mm

9. R. tshernyshevi Grunin

brown. The pair of mesonotal stripes is blackish and almost completely dull. Species of the Ethiopian region ........................ 7 7

(sc). 10-11

latifrons Gan or

Bequaert

Asiatic species. Wing with the discal cross-vein (r-m) lying beyond level of apex of the sub-

(11) Mesonotum with glossy black

or black-brown, slightly elevated weals, the presutural pair of inner stripes is smooth and without a dense wrinkling (see Fig. 218). 1. R. purpureus (Brauer)

8. R. giraffae n. sp.

6

without

(7) Last

segment ventrally at the anterior margin

with two to four slightly irregular rows of

spines (see Fig.

234). 9. R. tshernyshevi Grunin

7

(6) Last

8

(3) Dorsal

(10) Mesonotum with densely

wrinkled weals which flat and either dull or partly more or less glossy (see Fig. 240)...................... 12

segments

spinulation.............................. 6

segment bare ventrally (see Fig. 228). 7. R. phacochoeri Rodhain and Bequaert

are

12

(13) Parafrontalia

with relatively flat, largely confluent tubercles. Abdominal tubercles flattened,

of moderate and small size. 11. R. vanzyH Zumpt and Bauristhene

armature present on at least a few

anterior segments 9

(12) Parafrontalia

with big, voluminous tubercles, most of which are clearly isolated, only some near the eye-margin may be slightly confluent,

Abdominal tubercles conical, glossy, median ones

very large. 2. R, usbekistanicus Gan 160

9

5. R. hippopotami Grunberg 10

(9) Latero-ventral bulges of segments with groups of spines

13

........................

(10) Latero-ventral bulges of segments bare.

11

at the

posterior margin............ 11

(12) Eleventh segment dorsally completely bare. 6. R. nivarleti Rodhain and Bequaert

12 (11) Eleventh segment dorsally at the posterior margin with several rows of anteriorly-directed spines.................................. 13

SUBORDER: BRACHYCERA 13

(14)

Last segment bare ventrally (except the terminal bulges which are always spinulose). 10. R. antidorcitis Zumpt and Bauristhene

14 (13) Last segment with four to seven rows of spines

ventrally ...........-l 15

(18)

Posterior peritremes with a typical channel at the inner sides (see Fig. 222).............. 16

16

(17)

Posterior peritremes higher than broad.

17

(16) Posterior peritremes about

18

(15)

1.

jR.

purpureus (Braver)

high as broad. 2. J?. usbekistanicus Gan as

been continued mainly by Russian authors, especially with respect to their veterinary and medical importance. A summary on R. purpureus is given by Grumn (1957).

Morphology

Imago (Figs. 218 and 219)A relatively small fly of 8-11 mm body-length. Eyes in both sexes broadly separated from one another; in the male the frons at its narrowest point measures about two-fifths of eyelength, in the female it is one-and-a-half times as broad as one eye is long. Parafrontalia with mostly isolated, partly ill-defined, broad tubercles. Mesonotum with a pair of presutural median weals which are glossy black or blackbrown, a pair of similar postsutural quadrangular ones,

Posterior peritremes broadly excavated at the inner ventral sides, the margins almost forming

right-angle (see Fig, 222) ............... 19 19 (20) Dorsal surface of segments III and IV with two to three complete rows of spines anteriorly on a

the fifth segment, the rows are medially interrupted, and the sixth has at most lateral groups of spines. 3. R. latifrons Gan

20

(19) Dorsal side of segments III and IV anteriorly with three to four complete rows of spines, fifth segment with three to four medially interrupted ones, and IV to X with lateral groups of spines, 4. R. steyni Zumpt

1. Rhinoestrus purpureus (Braaer)Horse Nasal Bof Fly

Cephalomyia purpureus Brauer, Verb. zool.-bot. Ges. Wien.

Figure 218. Rhinoestrus

1858, 457. Oestrus purpureus Brauer, Mon. Oestriden 1863, 158, figs. Rhinoestrus purpureus Brauer, Wien. ent. Ztg. 5, 1886, 289, fig.; Portschinsky, Mem. Bur. Ent. sci. Comm. Centr. Board of Land Adm. Agric. Petrograd VI no. 6, 1915, 42 pp., figs. (3rd ed.); Rodhain and Bequaert, Bull. sci. Fr. Belg. 50, 1916, 132, fig,; Grunin, Fauna URSS 19 no. 3, 1957, 121, figs,; Zumpt and Bauristhene, Nouos Taxa ent. 28, 1962, 20, 22. Rhineestrus nasalis Brumpt (nee Linnaeus), Precis de Parasitologie 1913, 700, fig. History This species was based on one adult male, caught on the wing near Vienna by Rogenhofer and sent to Brauer, who placed it in the genus Cephalomyia Latreille (the original spelling is Cephalemyia), a synonym of Oestrus Linnaeus. At this time Brauer suggested that tlie sheep was the host of the larval stages. Only in 1886 was it recognized that the horse was the true host. and Brauer created the genus Rhinoestrus for the parasite. He also described the larva for the first time. The classic paper on the morphology, biology and pathogenesis was written by Portschinsky in 1906, and in an enlarged third edition in 1915. The studies on the Horse Nasal Bot have since

161

purpureus (Brauer). Female fly. (After Grunin)

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES and two lateral ones of irregular size. The presutural ones are usually glossy, the postsutural ones are wrinkled. Furthermore, the mesonotum shows setiferous tubercies increasing in size towards and on thescutellum. PoIIinosity yellow-brown and white on a predominantly red-brown surface. Abdomen coloured and poihnose like the thorax,

with glossy black and brown setiferous tubercles. Legs red and yellow-brown, femora more or less darkened.

Larva I (Fig. 220)-Descriptions of the first larval stage given by Larrousse (1921) and Grunin (1957). The freshly ejected larva is nearly 1 mm long; when moulting are

H.WM^

^Wvy/. o’^

Larva III (Figs. 221 and 222)The third instar larva reaches a length of up to 20 mm. It shows rows of spines on both the dorsal and ventral sides of the segments. The second segment has denticles dorsally and vcntrally, the third and fourth segments bear two to three complete rows dorsally, and more or less medially interrupted ones on the fifth and sixth segments. The two following ones have only lateral groups, and on the ninth to the twelfth segments, dorsal spines at the anterior margins are absent. The eleventh segment, however, shows four to five rows of anteriorly directed spines at the hind margin. On the ventral surface there are three to four (on the sixth and seventh segment even five) rows present at the anterior margins of the third to the twelfth segments. In addition to this spinulation, groups of large denticles are found on the posterior margins of the latero-ventral swellings. Both anal bulges have spines. The peritremes are open and a little higher than broad; the channels lie almost opposite one another. Puparium,It is 1213 mm long, strongly convex dorsally, flat ventrally. The fully hardened shell is black.

^-’^NVM’^N^

’s^^Vi/t/i/^L/

Biology The normal hosts of R. purpureus are the horse and donkey and their cross-breeds. Records of the infestation of zebras in Africa with larvae of R. purpureus have not yet been confirmed, and they probably refer to R. steyni or R. usbekisianicus. The female fly produces between 700 and 800 larvae, which are expelled in batches of 8-40 into the nostrils

^

Figure 220. Rhinoestrus purpureus (Brauer) : (n) ventral and (6) dorsal spinulation of the seventh segment; (c) twelfth segment dorsally of the first instar larva. {After Grunin)

to the second stage it has reached a

length of 3-5 mm.

Larrousse compared it with 0. ovis, because both species are sometimes involved in

human ocular mviasis.

7?.

purpureus is easily separable from this species by the strongly curved mouth-hooks, and the eight to twelve terminal booklets arranged in one row. Dorsal surfaces of segments II to XI each with one medially interrupted row of spinules. Last segment in the posterior half with a number of small spines, which are wanting in R. latifrons. The ventral armature is similar to that of R. latifrons (Fig. 221) consisting of 3-4 complete rows of spines, but of 6-7 on the last segment. The lateral rod-like structures, however, are longer and thinner than in R. latifrons.

Larva //-Apart from the shape of the ventral spines, the second instar larva is very like the third instar. On the dorsal surface there are lateral groups of denticles on a few anterior segments. Ventrally the second segment shows a few irregularly placed conical spines but those on the following, down to the twelfth segment, are wedgeshaped, and placed in several dense rows. These spines are colourless and not readily detectable. The posterior peritremes are small, roughly triangular, and each provided with about 40 relatively large pores.

and sometimes also the orbits of the hosts. The first instar larvae are found in the nasal cavities, where they remain in this stage for a few weeks or even months. In southern Russia, for instance, the first instars are present from September until June, steadily decreasing in number. The speed of development of the same batch of larvae varies considerably. Some of them moult to the second stage in March, others later, and in July second instar larvae are still found. The same is true for the third stage , some already appear at the end of March, others only in July and August. The Russian authors believe that there is only one generation in the Ukraine. The older first instar larvae move further up to the posterior parts of the nasal passages, and the second and third instar larvae are also found in the pharyngeal area.

In Usbekistan, however, and other warmer parts of Central Asia, two generations are thought to be accomplished, and the flies are on the wing from March to midJune and again in September and October, and second larval stages are found as early as January. The explanation of this phenomenon is probably that in areas with a cold winter, the development of the first instar larva is considerably retarded during the unfavourable season. Female Hies were kept in captivity for 25 days on the average, but a few lived up to 38 days. The life-span of the males is only about two weeks. The pupal period is given as from 15 to 32 days.

162

SUBORDER: BRACHYCERA Pathogenesis R. purpureus poses

a serious veterinary problem in Russia. Akchurin (1945) described a rhinoestrosis of horses in the Republic of Bachkiriya. During the period from May to August, 1943, 11-2 per cent of the horses of 27 collective farms were infested and over 82 per cent of the affected animals died. In the dead horses larvae were found also in the throat regions and at the base of the tongue; in some instances over 200 specimens were found firmly attached in the nasal and pharyngeal cavities. Karpenko (1947) reported an outbreak of a fatal horse disease with symptoms suggestive of encephalomyelitis in the department of Odessa. Autopsies were performed on over 30 horses, and 8-90 larvae of R. purpureus were collected from the nasal cavities and the ethmoid bone, some of which had penetrated to the olfactory nerves and the soft cerebral membrane. No pathological changes characteristic of encephalomyelitis were found in the internal organs or blood of the animals, and it was concluded that death was due to the infestation, which apparently affected the nervous system and provoked the symptoms observed. Human ocular myiasis due to the first instar larva of R. purpureus has quite frequently been observed (Portschinsky, 1915; Kriimmel and Brauns, 1956), and from the U.S.S.R. also cases with complete destruction of the eye-ball and a following fatal secondary infection have been reported. It remains to be proved whether these cases of malign ophthalmomyiasis were really caused by larvae of Rhinoestrus, or actually by those of Hypoderma^ which have the normal habit of penetrating tissue. The larvae of the nasal bots, if dropped into the orbit, reach the nasal cavities in the true hosts by migrating on the surface of the eye-ball, causing at most a conjunctivitis (ophthalmomyiasis externa). In humans the larvae may wander around for quite a while, but they do not moult to the second stage and apparently do not reach the nasal cavities. A case in Persia recorded by Chams and Mohsenine (1956), in which second instar larva are said to have been recovered from the surface of the cornea, remains to be confirmed.

Figure 221. Rhinoestrus purpureus (Brauer) and R. latifrotis Gan: (a)-(c) third larval stage of R. purpureus in ventral and posterior view ;

((/) third larval stage of R. latifrons in ventral

view.

{After Grunin)

Distribution Rhinoestrus purpureus was originally a Palaearctic species, but it has, together with the horse, reached several parts of the Ethiopian and the Oriental regions, where it occurs sporadically, but is never common, James (1947) does not mention it from the Nearctic and the Australasian regions, and there are no contrary records known to me. 2. Rhinoestrus usbekistamcus GanEquine Lesser Nasal Bot Ply Rhinoestrus usbekistanicus Gan, Bull, A.N. Usbekistan

1947

24;

47, figs,

0-2 mm

Figure 222. Outline of posterior peritremes of: (a) Rhinoestrus latifrons Gan; (A) R. purpureus (Brauer) ; and (c) R. usbekistanicus Gan. {After Grunin)

Grunin, Fauna URSS 19

no,

7, 3, 1957,

Rhinoestrus sz.la.mpi Zumpt, Nows Taxa ent. 14, 1959, 4, fig.; Zumpt and Bauristhene, Nows Taxa ent. 28, 1962, 20, 22.

163

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYlASIS-PRODUCING FLIES History In the past adults and larvae of this species were confused with those of .ft. purpureus, and only in 1947 did Gan recognize differences in the third larval stage and separate it from R. purpureus. In his book on the Oestridae of the U.S.S.R. Grunin (1957) described both adult sexes. In 1959 Zumpt described Rhinoestrus scampi from the African Zebra in Bechuanaiand, but pointed out that it was quite similar to R, usbekistanicus, known to him at that time only from a not quite adequate translation of Grunin’s description. One of the main reasons for regarding the African specimens as distinct was the structure of the phallosome of the only male available to him. Shortly afterwards a second male from a zebra shot in N. Rhodesia was reared, and the dissection of the terminalia proved that those of the first male had been distorted, and that actually the hypopygia of R. usbekistanicus and R. s^lampi coincided in general shape. I have since seen several more specimens, adults and larvae, from the Caucasus, southern Russia, Anatolia, Iraq, Israel, Egypt, Algeria and Tanganyika, so that the area of distribution seems to cover the whole of Africa and extends eastwards far into Central Asia. R. szlampi and R. usbekistanicus are synonymized here for the first time.

The sixth segment has only a few spines laterally, and the following segments are bare, except for about four rows of anteriorly directed spines at the posterior margin of the eleventh segment. The spinulation of the ventral side is quite similar fo that of R. purpureus. The posterior peritremes are not higher than broad and are clearly

Morphology ImagoSeparable from R, purpureus mainly by the relatively ill-defined, flat and dull mesonotal weals. Sometimes the anterior part of the inner presutural stripes is a little shiny, but otherwise the weals are provided with a dense and fine wrinkling. The width of frons at the narrowest point measures about one-third of in the female. Para" eye-length in the male, and frontalia with voluminous light or dark-brown tubercles, most of them clearly isolated, only those near the eyemargin may be partly confluent. Parafacialia with less elevated tubercles, which vary in number and size and are irregularly placed. The ground colour of thorax and abdomen is yellow to reddish-brown, the mesonotal pattern may be of the same colour, or it is more or less darkened or even almost black. The legs are yellow-

Distribution The area of distribution of R. usbekistanicus probably covers the whole of Africa and extends, through the Near East up to Central Asia.

^-^

brown. The tubercles on thorax and abdomen are well

developed and show a fair variability in number and distribution. The poltinosity is yellow and while and forms a cloudy pattern on the abdomen, changing with the incidence of light. Body-length : 8-10 mm. Larva IIt has been briefly described by Gan. who found differences from R. purpureus in the dorsal spinulation. some minor

Larva III do

not know

of a description of this stage.

Larva III (Fig. 222)The spinulation of (tie dorsal side is less regular than in R. purpureus and, at the anterior parts of the segments, ends one or two segments earlier than in this species. Segment III shows two rows of spines which are narrowly interrupted medially. On the two following segments the median gap is much broader.

separable from

[hose of

R.

purpureus.

PupariumOne empty shell before me measures 13 mm in length. It is deep biack-brown, ventrally slightly concave, dorsally strongly convex.

Biology and Pathogenesis In the Palaearctic region R. usbekistanicus infests the horse and the donkey; in Africa south of the Sahara it has been found in Burchell’s Zebra {Equus burchellii). In the semi-arid areas of Central Asia it dominates in numbers over R. purpureus and R. latifrons. In Usbekistan and Tadjikistan there are two generations per year, the adults of the first are on the wing in May and June, those of the second generation in September and October. In southern Africa adults were hatched in August and in October, after a pupal period of three weeks. In Tanganyika a female was caught in September, The pathogenesis of the larvae in horses is said to equal that of R. purpureus.

3. Rfiinoeslrus

latifrons CanHorse Larger Nasal Bot Fly Bull. A.N. Usbekistan 7, 1947, 24; Rubtzov, Ent. Oboy. 30, 1948, 138, figs.; Grunin, Fauna URSS 19 no. 3, 1957, 130, figs.

Rhinoestrus

latifrons Gan,

History This parasite of the domestic horse was confused with R. purpureus until 1947, when Gan first recognized its specificity. In 1959, Zumpt raised the question whether his R. steyni, described a year before from Burcheli’s Zebra in South Africa, was really different from Gan’s species. Unfortunately there is only one male adult known of R. steyni, and of R. laiifrons only two females are before me. Based on Grunin’s description, the third instar larva of R. latifrons is separable from R. steyni, but the differences are slight and may lie within the intraspecific variability, To solve the question of the distinctiveness of these two species, more adult and larva! material must be made available, and for the time being it is expedient to list both forms as good species.

Morphology

ImagoA large fly which is somewhat intermediate between R. antidorcitis and R. hippopotami. The body is predominantly reddish brown, and the mesonotal pair of presutural weals is glossy anteriorly but rather illdefined, The parafrontal tubercles are close together, but still fairly well separated from one another and not

SUBORDER: BRACHYCERA broadiv confluent as, for instance, in R. steyni. The parafacialia show a few black dots only near the eyemargins, but each is provided with a long black seta. The tubercles on the abdomen and those on the mesonotum arc smaller than in R. antidorcitis and more reminiscent of ihose of R. hippopotami. Legs yellow to brown. Bodylength : 11-13 mm. There are two female specimens before me, the width of frons at its narrowest part measuring 1-} of eye-length.

Biology and Pathogenesis The only host so far known is the domestic horse. With respect to biology and economic importance, R. latifrons coincides with R. purpureus. Distribution R. laiifrons has been recorded from the European part of the U.S.S.R., from Kazakistan, Usbekistan, Mongolia and China,

Larva I (Fig. 223)The newly-born larvae are about 1 mm long and separable from those of R. purpweus by the complete lack of dorsal armature.

Larva II is

not

4. Rhinoesirus Steyni ZumptZebra

Larger Nasal Bol Fly

Zumpt, J. ent. Soc. S. Afr. 21, 1958, 56, figs.; Zumpt and Bauristhene, Novos Taxa ent. 28,

Rhinoestrus steyni

described.

1962, 19,21.

Larva III (Figs. 221 and 222)Body broadly oval and dorsallv strongly convex. Second to fourth segments

later two further third instar larvae were found in the same area, and some time later a few larvae were received from the Veterinary Research Laboratories, Onderstepoort, which had been recovered from a Mountain Zebra in 5.W. Africa. No further adults have been obtained.

Figure 223. Rhinoestrus latifrons

Gan. First larval stage ventral view.

History In 1957 six third instar larvae and one second instar larva were recovered from the nasal cavities of a zebra shot in the eastern Transvaal. One male fly hatched from this batch and proved to belong to a new species, which was named in honour of the Director of Nature Conservation in the Transvaal, Mr. T.J. Steyn. One year

in

{After Gan)

Morphology ImagoThe

only known male specimen is 12mm long and characterized by large broadly confluent tubercles on the parafrontalia. The frons at vertex measures three-eighths of eye-length. Thorax brown, with a blackish pattern and a whitish pruinosity. The tubercles on the mesonotum are small and granular, but are bigger and pustular on the scutellum. Abdomen yellow-brown, with small tubercles, which are well separated from one another. Legs with dark and reddish-brown femora and tibiae, knees and tarsi predominantly yellow. A detailed description is given by Zumpt (1958c). Larva I is

not known.

Larva IIThe second instar larva, with respect to armature, is similar to the following stage. Zumpt figured the posterior peritremes and the mouth-parts, which are not separable, however, from those of R. purpureus. two to

threecomP3ete

rows

^P"^

on

the rows are medially interrupted, and on the sixth, at the most lateral groups are present present, i he eleventh segment has dorsally at the posterior margin three, directed ii"^^, of rarely anteriorly inicly iour, spines. spines. four, rows 01 anienoriv On the ventral surface all segments are provided with complete rows of spines, numbering from three to four, and five rows on the last segment. The latero-ventral bulges are beset with small and large spines. The posterior peritremes are strongly excavated at the inner margins. Mature larvae are up to 20 mm long. Puparium is not described. Qirccica

Larva ///-The typical batch contained six third instar ;. .bn..t 20 90^ mature ones mm in larvae, the ^y^ ^ measured about length. The armature of both sides is composed of more R. usbekistanicus in and R. purpureus. rows of spines than , i , , , ’vith denticles dorsally and ventrally. second Third and fourth segments on both sides with three to four complete rows of spines, fifth segment dorsally with three to four rows which are medially interrupted; the sixth to the tenth segments with only lateral groups of spines which gradually decrease in number towards the posterior end. Dorsally the eleventh segment shows four to five rows of anteriorly-directed spines terminally.

^^ ^ ,,

165

.

mTn^hT11 the^fifth

^em

,

,,

i

n

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Ventrally the body bears four to five rows on the fifth segment, five to six rows on the sixth and seventh segments, four to five rows on the eighth to the eleventh segments, and six to seven rows of spines on the last segment. The lateral bulges contain bigger and smaller spines as in R. latifrons. Both terminal bulges are provided -with dense spines, and the posterior peritremes are quite similar in shape to those of R, latifrons.

have only a weak shine. The tubercles are relatively small in the anterior part of the thorax, but increase in size towards and on the scutellum. Legs with yellow-brown tibiae and tarsi; femora partly darkened. Abdomen with a light-brown and partly silvery pollinosity. Tubercles small, the majority isolated and scattered, each with a long black seta.

PupariumThe shell from which the holotypc hatched is 15mm long, nearly black, flat ventrally and slightly convex dorsally.

Larva III (Fig. 224)The mature third instar larvae reach a length of up to 22 mm. They are characterized by the

Larva I and 77 are

not

known.

Biology and Pathogenesis The second and third instar larvae have been found in the nasal cavities of Burchell’s and the Mountain Zebra [Equus burchellii and E. zebra). The pupal period of the only fly which hatched lasted about a month; the fly appeared on the 24th May, 1957. Other third instar larvae were collected in May and July. Nothing is known about the pathogenesis. Distribution

Natal, Transvaal, S.W. Africa.

S. Rhinoestrus hippopotami GruitbergHippopotamus Nasal Bot Fly Rhinoesirus hippopotami Grunberg, S.B. Ges. naturf. Fr. Beri.

1904, 37, figs.; Surcoufand Gedoelst, Bull. Soc. Path, 2, 1909, 615, figs.; Rodhain and Bequaert Bull. sci. Fr. Belg. 50, 1916, 127, figs.; Zumpt and Bauristhene, Novos Taxa ent. 28, 1962, 19, 21. exot,

History As early

1870 Muir mentioned (see Rodhain and a fly maggot found in the head of a hippopotamus on the Upper White Nile. However, the figure he gives is so bad that it is not certain whether he was actually dealing with a Rhinoestrus species. Grunberg then described and figured the third instar larva from the frontal sinus of a hippopotamus shot at Ngaundere in the Cameroons, and a few years later, Surcouf and Gedoelst were able to provide the descriptions of the adults from material they had received from the former Belgian Congo. The last account of the species was given by Rodhain and Bequaert (1916^). as

Bequaert, 1916^)

Morphology ImagoThere is one male before me, which measures 13 mm in length. Head and abdomen are predominantly yellow-brown, the thorax for the greater part blackish. At the narrowest point the frons measures about onethird of eye-length. The parafrontal tubercles are dull and generally separated from one another; sometimes two or three are more or less confluent. The parafacialia are provided with a number of tubercles similar to those

of the parafrontalia, but they are a little smaller and slightly glossy. The mesonotal longitudinal dark vittae are flat and not clearly defined and, owing to fine granulation,

Figure 224. Rhinoestrus hippopotami Grunberg, Posterior view of third instar larva and enlarged psritr;me. (After Sourcoufand Gedoelst)

complete absence of spines

on the

latero-ventral bulges

of the segments, in connection with the presence of a dorsal armature. This dorsal armature consists of two to three complete rows on the second to the fourth segments, and small lateral groups at least to the fifth segment, sometimes down to the seventh segment. On the ventral surface, there are several rows on the second and two to three rows of spines on the third and fourth segments, and three to four rows on the fifth to the eleventh

166

SUBORDER:BRACHYCERA The twelfth segment is bare anteriorly, but the anal bulges are strongly spinulose. The posterior peritremes are of characteristic shape, the channel being strongly narrowed at the margin.

segments.

PupariumShape ]4-16nwiin

as

in R. pwpweus and measuring

length.

Biology and Pathogenesis The third instar larvae are found in the nasal cavities and especially the frontal sinuses of the Hippopotamus

(Hippopotamus amphibius}. No pathological effects have been recorded. Distribution

In the former Belgian Congo; the hippopotamus is quite normally infested, and I also received larval material from Uganda. A hippopotamus shot in Northern Rhodesia (near Monze), however, proved to be free of larvae; and it is possible that the parasite does

yellow-brown, crater-like ’ foot-prints’. This last feature is shared with the Asiatic R. tshemyshevi. The frons of the male at its narrowest point measures about one-fourth of eye-length; in the female, it is distinctly as broad as one eye is long. The parafrontalia have relatively small and low, partly or even predominantly confluent tubercles. This sculpture is subdued, within a certain variability. Mesonotum without weals, but with dense and fine granules, each bearing a black seta. The scutellum too has only granules, and no or

tuberculous sculpture. The pollinosity of the thorax is yellowish. The legs are yellow-brown, with more or less blackened femora. The abdomen of the male is, like the thorax, yellow or reddish brown, with a yellow pollmosity; in the female, however, the ground colour is black and the pollinosity whitish, forming a cloudy pattern which depends on the light incidence. The setiferous granules of the abdomen are similar to those on the thorax. Body-length: 11-13 mm.

not extend as far south as its host.

Larva I is not known.

6, Rhinoestrus nivarleti Rodhain and

Larva II (Fig. 226)Two specimens before me are 11 and 12 mm long. The ventral armature is similar to

BequaertBushpig Nasal Bol Fly Rhinoestrus nivarleti Rodhain and Bequaert, Rev. Zooi. afr. 1, 1912, 370, figs.; and Bull. sci. Fr. Belg. 50, 1916, 119,

figs.; Zumpt, J. ent. Soc. S.

Afr. 21, 1958,

57.

History

To European and native hunters in the Congo forests it was known that bushpigs harboured fly-maggots in the cranial cavities. In 1911 the ’chef de poste’ of Yongama, M. Nivarlet, recovered a number of larvae of the second and third stages and also succeeded in hatching two male flies. They were sent to Rodhain and Bequaert (1912), who recognized a new species and described it as Rhinoestrus nivarleti. In their monograph

Figure 226. Rhinoestrus nwarleii Rodhain and Bequaert. peritremes of second larval stage

that of the third stage, the dorsal one is quite indistinct. The posterior peritremes show a relatively broad channel.

Larva III (Fig. 227)The mature larva reaches a length to 20 mm. The second segment shows the usual dorsal and ventral denticles. On the dorsal surface the third to fifth segments have three to four rows of spines, whereas the sixth and sometimes also the seventh and eighth have only lateral groups of spines. On the ventral surface, the third and fourth segments have two to three rows of spines, the fifth has three to four rows, and the seventh to tenth segments have five to six rows of spines. On the eleventh and twelfth segments the spinulation varies considerably, being composed of three to five rows on the former and one to four irregular and partly medially-interrupted rows on the latter. Small groups of spines on the latero-ventral bulges are developed only on certain segments. The posterior peritremes have a short, funnel-shaped channel. of up

Figure 225. Rhinoestrus niwrleii Rodhain and Bequaert. Wingvenation.

of the African

{After Rodhain and Bequaert)

Oestrmae:

were also able to give a

Rodhain and Bequaert (19166) description of the female fly.

Morphology Imago (Fig. 225)A characteristic and unique feature of both sexes lies in the wing-venation, the discal cross-vein (r-m) being situated opposite or a little before the level

of the apex of the subcosta (sc.). Furthermore, the parafacialia have no dark spots, the setae are located in yellow

PupariumIt is 14-15 mm long and of similar shape other Rhinoestrus species.

167

to

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES

Figure 227. Rhinoestrus Rod ha in and

nivarleii

Bequaert.

Posterior peritremes of third larval stage

Biology and Pathogenesis The only host is the Bushpig {Potamochoerus porcus), and the larvae are found in various cranial cavities. Adults are recorded from May, November and December, but may occur throughout the year. The duration of the pupal period is given as from 28 to 35 days. Pathological effects are not known. Distribution

R. nivarleti is so far known only from the Congo forests. A few bushpigs which I examined in Northern Rhodesia (nr. Monze) and in Mozambique (nr. Beira) were not found to be infested. 7. Rhinoesfrus phacochoeri Rodhain and BequaertWarthog BolFly

Nasal

Rhinoestrus phacochoeri Rodhain and Bequaert, Bull. Soc. Path. exot. 8, 1915, 452; and Bull. sci. Fr. Belg. 50, 1916, 136, figs.; Zumpt and Bauristhene, Novos

Taxaent.28, 1962, 21.

complete to place this species into a key for the African species. The Belgian authors at this time knew only four species of Rhinoestrus^ whereas we now have to deal with nine species in Africa and with twelve altogether. R. phacochoeri belongs to the purpureus-group, measuring 9-1 Omm in length and having dark papulae on the parafrontalia. It seems to have the nearest relationship to R. usbekistanicus, but is certainly different from this species. Larva I is not known.

Larva IIAccording to Rodhain and Bequaert (19166), the spinulation is similar to that of the third stage, but the eleventh segment is provided ventrally with four rows of spines and the last with five rows. Larva III (Figs. 228 and 229)The third instar larva is characteristic and should be readily recognizable. The dorsal side of the segments as well as the latero-ventral bulges are completely bare. On the ventral surface the third to fifth segments show usually two rows of spines, the fifth to eleventh segments three rows of spines. The

History This species was discovered in the Uele district of the former Belgian Congo. It is rare there and was not found in other parts of the Congo, for instance in Katanga and the Lake Albert and Lake Edward areas. I have examined a fair number of warthogs in Northern and Southern Rhodesia, in the Beira district of Mozambique, and in several parts of the Transvaal without success, but recently received a few larvae from Garua in the

Cameroons. Rodhain and Bequaert described the third larval stage both sexes of the imago. I saw the typical batch of larvae in the Tervuren Museum, but the adults could be found neither in Tervuren nor in Antwerp, and they are presumably lost. as well as

Morphology ImagoRodhain and Bequaert (1916^>) gave a rather long description, but it is nevertheless not sufficiently 168

Figure 228. Rhinoestrus phacochoeri Rodhain and Bequaert. Ventrai view of third larval stage. {After Rodhain and Bequaert)

SUBORDER: BRACHVCERA

Figure 229. Rhinoestrus and Bcquacrt. Posterior peritreines of third larval st.’

phacochoeri Rodhain

"

posterior peritremes are also quite characteristically shaped. The mature specimens are 16 mm long. PupanumAbout 12 mm long and of the usual shape found in the genus Rhinoestrus. Biology and Pathogenesis The larvae have been found in the cranial cavities of the Warthog {Phacochoerus aethiopicus). Pathological effects are not known.

Distribution Congo and the Cameroons. 8. Rhinoestrus giraffae nov. spec.Giraffe Nasal Bot Fly ’ Larva of Rhinoestrus from giraffe’ Laurence,

Proc.

zfid. Soc. Lond. 131, 1961, 595, fig. History In 1961, Laurence described and figured the third larval stage of a new Rhinoesims species from the giraffe. In a collection of oestrid larvae presented to the London School of Hygiene and Tropical Medicine, he found no less than 147 larvae which had been recovered from nine giraffes shot near Shinyanga, Tanganyika, during 1946 and 1947, in the course of experimental work on tsetse control. The third larval stage is so well characterized that no doubt about its specific distinctiveness exists, but Laurence pointed out that ’ until the adult ny is reared it is best left without a specific name ’.

Dr. B. R. Laurence was kind enough to send me two specimens of these larvae for our collection. We examined them once more and could only confirm that the giraffe harbours a quite distinct Rhinoesirus species. For practical reasons I thought it better not to leave this species unnamed, especially because it had already been introduced into the literature as a new Rhinoestrus, and I wrote this to the author. Dr. Laurence replied as follows : ’ My own feeling is that these larvae ought not to be named until the adult fly is known. If, however, you feel

Figure 230. Rhinoestrus giraffae nov. spec. Dorsal and ventral view of third larval stage

about this, and want to name the larva from the giraffe, then I think they should be named after the host or after C. H. N. Jackson or after W. H. Potts. Both these gentlemen realized that they had an undescribed differently

species of Oestrid from the giraffe. Jackson was responsible for the collection of this material, so I understand. Personally I would favour the host name.’ This new species is therefore introduced as ’ Rhinoestrus giraffae nov. spec.’ into the literature. The larva should be labelled as the holotype from which Laurence made his drawings, and which is preserved in the London School of Hygiene and Tropical Medicine. 169

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES

O’Smm Figure 231. Rhinoestrus giraffae

nos.

spec. Posterior peritremes of third larval stage

Morphology Imago and thejirst two larval stages are not known.

range and in western Kazakistan. In 1957 Grunin and Sludsky succeeded in finding the puparia and in rearing

Larva III (Figs. 230 and 231)The

three female flies from extracted larvae.

largest larva before length. A band of denticles is present dorsally and ventrally on the second segment, but otherwise the dorsal surface of the following segments is bare. In this respect the larva is reminiscent of that of R. phacochoeri and of R. tshernyshevi, but the posterior margins of the latero-ventral bulges are spinulose in R. giraffae. Furthermore, the ventral surface of the third

me measures 17 mm in

Morphology Imago (Figs. 232 and 233}A small fly of 10-11 mm bodylength. Only the female is known, which shows relatively large eyes and is especially characterized by a longitudinal ridge

on

the lower part of the parafrontalia. The head is

segment bears two to three rows of spines, the fourth and fifth segments three to four rows, the sixth to eleventh segments four to five rows, and the last segment six rows of spines. The posterior peritremes show a relatively broad channel.

Puparium is not known. Biology and Pathogenesis Laurence says that 42 larvae recovered from the Giraffe [Girajfa camelopardalis} were labelled ’ from throat’ and six ’ out of nose’. No further biological data are available.

s

tshernyshevi Grunin. Female fly. {After Gri and Sludsky)

Distribution

R. giraffae is so far known only from the type-locality Old Shinyanga ’ in Tanganyika.

History

yellow-brown, partly waxy shining; ocellar triangle and the third antennal segment are black. Furthermore, the parafrontalia have small black warts, bearing setae. The mesonotum is dull black, but the humeral calli and scutellum are brown. The poilinosity is greyish white. The mesonotal pattern is indicated by hairless tubercles and the remaining mesonotum is covered by short yellowish tipped hairs. The sculpture consists of these grain-like tubercles, probably similar to those of R.

This species was based on a third instar larva found by Tshernyshev in June, 1949, in the nasal cavities of an Argali in the Kulyab district of Tadjikistan. Later more larvae were recovered from the same host in the Dzhambul

nivarleti. Abdomen black like the thorax and with whitish, speckled poilinosity; the pattern it forms changes with the incidence of light. Another characteristic feature of this species is given by the absence of the three

’

9. Rhinoestrus tshernyshevi GruninArgali Nasal Bol Fly

Rhinoestrus tshernyshevi Grunin, Ent. Obozr. 31, 1951, 467, figs.; and Fauna URSS 19 no. 3, 1957, 134, figs.; Grunin and Sludsky, Ent. Obosy. 39, 1960, 210, figs.

170

SUBORDER: BRACHYCERA Biology and Pathogenesis The only host so far known is the Argali {Ovis ammon). The adults which Grunin and Sludsky reared appeared on the 20th and 2IstJune, 1957, after a pupal period of about 3 weeks. Nothing is known about the pathogenesis. Distribution Central Asia. 10. Khinoestrus antidorcitis ,\asal Bol H\-

Zumpt and BaurisiheneSpringbuck Larger

Rhinoestrus antidorcitis

Zumpt

Taxaent.2^ Figure 233- Rhinoestrus tshernysheri Grunin. Frontal view of female head. {After Grunin and Sludsky)

dark basal spots on the wing, which are present in all other Rhinoestrus species.

Larvae I and

// are not known.

Larva HI (Fig. 234)The mature larvae are 27-31 mm long and characterized by the absence of dorsal spinulation. Ventrally, the lateral swellings are also bare, but the segments have anterior rows of spines of characteristic shape. Puparium is known, but

not described.

and Bauristhene, Novas

1962, 11, figs.

History During the last decade intensive investigations on the arthropod parasites of vertebrates have been carried out by the Department of Entomology of the South African Institute for Medical Research. Among the numerous oestrid larvae received for study we occasionally found single unknown larvae of a Rhinoestrus type, recovered from the nasal cavities of springbuck in the Western Transvaal and in S.W. Africa. These larvae apparently belonged to two different species. Thanks to the great interest of the Senior Research Officer of the Lombard Nature Reserve in the Transvaal, Mr. van Zyl, in June, 1961, we were given the opportunity of investigating a fair number of springbuck. He had already started to collect and to isolate larvae ejected from the nostrils of killed antelopes himself. The result of these combined investigations was the discovery of two new species of Rhinoesirus which infest the South African springbuck, often simultaneously.

Morphology Imago (Figs. 235 and 236)This species is rarer than R. vamyli, and only four females have so far been reared. It is a large fty measuring 13-15 mm in length. The eyes of the female are widely separated from one another, the frons at vertex measures about 1-1- of eye-length. Frontal stripe yellow to brown ; parafrontalia with large, voluminous, black or brown tubercles which lie close together and are more or less confluent. The face is yellow, and the parafacialia show a few small dark spots near the eye-margin. Thorax predominantly yellow-brown, with flat, black, fairly glossy weals, and shiny brown or black tubercles which are large, but relatively flat. The pollinosity is yellow to brown. Legs with darkened femora and tibiae, knees and tarsi yellow-brown. Abdomen black, with a cloudy yellow and white pollinosity. Tubercles conical and big. Larva I is not known. Larva //It is separable from the simultaneously occurring R. vanzyli by its pointed denticles. Larva III (Figs. 237-239) The mature larvae, which measure more than 20 mm in length, are yellowish and show more or less developed brown transverse bands

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES dorsally.

Second segment with dorsal and ventral denticles. The third segment shows two to three rows of denticles dorsally, the fourth to sixth three to four rows, those on the sixth being medially interrupted, and the following two segments have only lateral groups of denticles at the anterior margins. The eleventh segment, however, dorsaily bears three complete rows of spinules at the posterior margin. The ventral surface of the body lias three to four rows of spines on the third to the fifth segments, and four to five rows on the sixth to the eleventh segments. The last segment is bare, except for the usual spines on the terminal bulges. The posterior peritremes are

mtidorcitis Zumpt and Bauristhene.

Per

broadly open.

Figu,

fly

;

238. Rhinoestrus antidorcitis Zumpt and Bauristhene. Spines of the ventral surface of the third instar larva

Figure 239. Rhinoestrus antidorcitis Zumpt and Bauristhene. Posterior view of the third

instar

PupariumThe shell is black, ventrally and convex dorsally.

larva

15-17 mm long, flat

Biology and Pathogenesis The only host of this fly is the Springbuck {Antidorcas marsupialis), In the Western Transvaal mature larvae recovered in June, and the adults hatched from the end of July until mid-August, after a pupation period of 49-56 days. The number of larvae of this species and of R. vanzyli found in a single host is low, and no pathological effects have been observed. were

172

SUBORDER: BRACHYCERA Distribution Western Transvaal and S.W. Africa, but probably wherever the

Springbuck occurs.

//. Rhinoesfrus vanzyli Zumpt and BauristheneSpringbuck

Lesser

Nfisal Bol /"/)’

Rhinoesims vanzyli Zumpt and Bauristhene, Novos Taxa ent. 28, 1962, 4, figs.

History The history of this species, named in honour of the Senior Research Officer of the Lombard Nature Reserve,

Western Transvaal, Mr.

J.

H. M.

van

Zyl, has been

discussed under R. antidorcitis.

Morphology Imago (Figs. 240 and 241)The adults are similar to R. usbekistanicus, but readily separable from it by having fiat and largely confluent tubercles on the parafrontalia

Figure 241. Rhinoestrus vanzyli Zumpt and Bauristhene. Head of female fly

and relatively low tubercles of moderate and small sizes on the abdomen. In the male the frons at its narrowest point measures about one-seventh of eye-length; in the female it is about one-third wider than one eye is long. Parafacialia yellow, with blackish, slightly elevated spots which are partly confluent. Thorax with a black and brown ground colour, partly with a yellow to redbrown pollinosity. The mesonotal weals are ill-defined, strongly wrinkled. Legs yellow-brown, femora more or less blackened. Abdomen red-brown or black, with a cloudy silvery-white or yellow pollinosity. Body-length :

9-10 mm.

Larva I

is not known.

Larva II (Fig. 242)The specimens before me are 48 mm long and show a spinulation similar to that of the third stage. The posterior spiracles have relatively few but wide pores.

Larva III (Figs. 243-245)The third instar larvae are 10-17 mm long, white and with yellow-brown posterior peritremes in the younger specimens; yellow-brown with transverse brown vittae and dark-brown peritremes in the maturing larvae. They are quite unique by not having rows of pointed spines on the ventral anterior parts of the third to the twelfth body segments, but square scales; only the second segment shows denticles ventrally, and the

vamyli Zumpt and Bauristhene. Posterior periti me of the second instar larva

Figure 242. Rhinoestr

provided with the usual spines. The latero-ventraf bulges of the segments also are beset with eroups of scales. Dorsally the second segment bears two irregular rows of scales which are quite similar in shape to those on the ventral side, but the following segments are bare. The posterior peritremes are broadly open. terminal bulges are

Figure 240. Rhim

ansyli Zumpt and Bauristhene. Male Hy

i

173

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES PupanumBlack-brown, 6-8 mm long. The characteristic square scales are very distinct, so that the pupal case is also easily identifiable. Biology and Pathogenesis As for R. anfidorcitis, the only host is the Springbuck {Antidorcas marsiipialis}, but R. uan^yli is much more common than the other species. The mature larvae drop in June, and the adults hatch after 30-50 days. Pathogenic effects have not been observed.

Figure 243. Rhinoeslrus uanzyii Zumpt and Bauristhene, Ventral view of third instar larva

Distribution

R. vanzyli has been recorded from the same localities as R. antidorcitis, and the distribution areas of the two species probably coincide. Genus: Oestrus Linnaeus Oestrus Linnaeus, Syst. Nat; ed. 10, 1758, 584. Cephalemyia Latreille, N. Diet. H.N. 23, 1818, 273. Oestroides Gedoelst, Rev. Zool. afr. 1, 1912, 431. Loewioestms Townsend, Insec. Inscit. menst. 6, 1918, 152. This genus contains the well-known and economically important Sheep Nasal Bot Fly [Oestrus ovis), which has gained an almost cosmopolitan distribution. It is of Palaearctic origin, and like a second species of this region, develops in species of Caprini. The other four species of the genus Oestrus are elements of the Ethiopian region and have Alcelaphini and Hippotragini as hosts. The adults are quite well characterized and no difficulties should arise in identifying them. The third instar larvae, however, are very similar to one another and separable only by features which are not always readily detectable and, moreover, show a certain variability.

Key to the Imagines macdonaldt is not known in the adult stage, 1 (2) Wing long and narrow. The discal cross-vein 0,

(r-m) is located before the middle of the discal cell (Ms). 14-18 mm. 4. 0. variohsus (Loew)

Figure 244. Rkinoestrw vanyli Zumpt and Bauristhene- Row of ventral scales of the third instar larva

2 (1) Wing short and broad. The discal cross-vein is located in or beyond the middle of the discal cell...................................... 3 3

(4) Thorax with large but flat tubercles of yellowbrown colour. Mesonotum with a sharplydefined, weal-pattern, as is found in most Rkinoestrus species. 12-15 mm.

6. 0. bassoni

4

(3) Thorax

5

(6) Wing veins black.

Zumpt

with small, black, granular tubercles. Mesonotum without weals .................. 5

12-13 mm.

2. 0. caucasicus Grunin

(5) Wing veins yellow.......................... 7 7 (8) Mesonotum with black hairs. Tubercles on the three brown-dusted presutural vittae tooth-shaped,

6 Figure 245. Rhinoestrw vansyli Zumpt and Bauristhene. Posterior vie of the third instar larva

174

SUBORDER: BRACHYCERA and stronger than those on the intervening black areas. When comparing the same sexes, parafacialia more coarsely rugose and with fewer and larger pits than in the following species. 11-16 mm. 3. 0. aweoargentatus Rodhain and Bequaert

yellow hairs. Tubercles on the brownish or yellow-dusted presutural vittae roundish and not, or only slightly, stronger than those

8 (7) Mesonotum with

on the intervening areas. Parafacialia more finely rugose, with more and smaller pits. 10-12 mm. 1. 0. avis Linnaeus to the Third Instar Larvae known in the larval stage. 1 (4) Dorsal side of segments III to VI anteriorly with rows or patches of spines.................... 2

Key

0. bassoni is

2

not

(3) Segments III

V dorsally with two to three fairly regular rows of spines, the following three segments with lateral groups of spines. Asiatic to

species. 2. 0. caucasicus Grunin 3

(2) Segments III and IV dorsally with quite irregular bands of spines; the following

two or

three seg-

ments with lateral groups only ; rarely segment V shows one almost complete row. African species.

3. 0. aweoargentatus Rodhain and Bequaert

4

(1) Dorsal

5

(6) Dorsal side of second segment without spines.

side of segments without spines, except the second segment, which may have some....... 5 4. 0. variolosus (Loew)

6 (5) Dorsal side of second segment with one or two

irregular, sometimes medially interrupted, of spines.................................. 7

rows

7 (8) Segments VI to VIII ventrally with five to six rows of spines. 5. 0. macdonaldi Gedoelst 8

(7) Segments VI

1.

Oestrus ovis LinnaeusSheep Nasal Bol Fly

to rows of spines.

VIII ventrally with three

to

Reaumur in 1734 published an illustrated paper on the ’ mouche du ver du nez des moutons ’, and Linnaeus also had made this fly a subject of a special paper, before he introduced it into the scientific literature under the now valid name in 1758 (seeBrauer, 1863). The first comprehensive paper on the bionomics, control measures and relation to man was written by Portschinsky (19136), which was followed by a great number of shorter papers by various authors, who dealt with the taxonomy, biology and veterinary and economic importance. The first larval stage of Oestrus ovis has also become known as the cause of ophthalmomyiasis in humans, on which problem Sergent (1952) wrote a basic paper. The varieties created by Gomez in 1946 are to be regarded as only synonyms.

Morphology

Imago (Figs. 246 and 247)Head yellow-brown, with dense, glossy-bottomed black pits on the parafrontalia. In the male the frons at its narrowest point measures a little less than half the eye-length; in the female it is broader than one eye is long. Parafacialia with a number of pate hairs which are situated in pale or slightly darkened ’ foot-prints ’. Mesonotum yellow-brown with small glossy black tubercles of about equal size; on the scutellum they are irregularly placed and consist of smaller and larger ones. The hairs of the mesonotum are yellow, a. characteristic feature for separating 0. ovis from 0. aweoargentatus. Wings with yellow veins; the legs are also yellow or yellow-brown. Abdomen completely black or more or less extensively reddish-brown, with a speckled, greyish or white pollinosity changing with the light incidence. Body-length : 10-12 mm.

Larva I (Figs. 248 and 249)It is spindle-shaped and about 1 -3 mm long when deposited. The cephaloskeleton is relatively large and provided with strongly bent sclerites. The dorsal side bears only a weak spinulosity, consisting of a complete row of denticles on the third-

four

1. 0. ovis Linnaeus

Oestrus ovis Linnaeus, Syst. Nat., ed. 10, 1758, 584; Rodhain and Bequaert, Bull, sci. Fr. Belg. 50, 1916, 85, figs.; Patton, Ind. J. med. Res. 8, 3920. II; Grunin, Fauna URSS 19 no. 3, 1957, 108, figs.; Zumpt, Nouos Taxa ent. 24, 1961, 11. Oestrus ovis var. corsicae Gomez, Rev. iber. Parasii. 6, 1946, 58, fig. Oestrus ovis var. granatae Gomez, Rev. iber. Parasit. 6, 1946, 58, fig. History in

The nasal bot of the sheep was already known to Redi the 17th century and to other pre-Linnaean authors.

175

Figure 246, Oestrus ovis Linnaeus. Female fly.

{After Grunin)

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING PLIES Biology The larvae of Oestrus ouis are well-known parasites in the nasal cavities and the frontal sinuses, sometimes also the maxillary sinuses, of the domestic sheep and goat. In Central Asia the following wild animals have been found to act as hosts of this fly: Argali {Ovis ammon}, Ibex {Capra ibex) and another Capra species in the Caucasus. Bedford (1925) mentioned a number of antelopes ai hosts of Oestrus ouis in southern Africa, but all these records were based on misidentincations, and so far no antelopes or any other wild animals in Africa south of the Sahara have been found to serve as suitable hosts to the Sheep Nasal Bot Fly. The record by Rodhain (1926) that larvae of 0. ovis had been recovered from an Okapi which died in the Zoological Garden of Antwerp, probably does not refer to this species, but to one not yet named. 248(right). Oestrus wis Linnaeus. Freshly hatched first in ventral view. {After Figure

mstar larva

Grunin) Figure 247. Oestrus ovis Linnaeus. Female head in frontal view.

{After Grunin)

segment and a broadly interrupted one on each of the following two segments. On the ventral side, the segments at their anterior margins show two to three complete rows of spines, and a number of hair-like structures laterally. There are 22-25 terminal hooks arranged in two

scallops.

Larva II (Fig. 250)The second instar larvae are white and between 3-5 and 12 mm long. The dorsal side shows only a few weak denticles on the second segment, furthermore the median part of the post-anal bulge is spinulose. Ventrally the segments are provided with rows of peculiarly shaped currycomb-like spines. The posterior peritremes are more or less circular ; the channel is indicated by a distinct suture.

Figure 249(below). Oestrus ovis Linnaeus. Anterior part of the first instar larva in dorsal and lateral view. {After Grunin^

Larva III (Figs. 251 and 252)The third instar larva is up to 20 mm long and yellow in colour when young, changing to a light brown later, and in the maturing stage it shows broad transverse blackish bands dorsally. The second segment is provided dorsally with a variable number of small denticles; the following segments are bare, but provided with a rough leather-like skin pattern, which is, however, distinct only on the darkened parts. Ventrally the segments bear rows of strong spines, which are irregularly placed on the third segment but are fairly regular on the following ones. They number from three rows on the fourth and fifth segments, from three to four rows on the sixth to the eighth, from four to five on the three following ones, and three to four rows again are found on the last segment. The post-anal bulge shows less spines than in 0. uariolosus, the pre-anal bulge is bare. Posterior peritremes are circular, with a central button and without a distinct suture. two to

PupariumBlack, only weakly wrinkled and on the average 15-16 mm long. 176

SUBORDER: BRACHYCERA There are quite a few papers dealing with the bionomics and pathogenesis of 0. ovis, but one of the most conclusive is bv Cobbett and Mitchell (1941), who carried out their investigations in New Mexico and Texas. They proved how greatly dependent upon climatic factors the whole life-cycle of the fly is. In West Texas, with its moderate winters, the flies were active during almost all months of

larval infestation consisted chiefly of first instars which remained quiescent on the nasal mucosa, and did not migrate to the frontal sinuses until the following spring and summer. The flies were active only during the warm days of summer and early fall. Another interesting observation by Cobbett and Mitchell, which has been confirmed by other authors,

Figure 250. Oestrus o-w Linnaeus. Posterior peritremes of second larval stage

Figure 252. Oesli

fSg^.

^KMS-WW. i,

the great difference in the speed of larval development, even of the same deposit. In lambs the larval time in some cases covered only 25-35 days in summer, other larvae needed a longer time to reach maturity, whereas still others remained undeveloped as first instar larvae for as long as 9 months, so that their development would was

k

^".f.ySw’^.ww’:; -

-

’^&^’..». ^w^w !^. *--^v’s?.. .&

require up to 10 or 11 months. The discharged mature larvae required approximately 24 hours to form the puparium, but some needed as long as 5 days for pupating. During the warm days of summer the ^""g’ Pupal period was 27-28 days, but at low temperatures it might be greatly extended, and Bedford (1925) recorded a pupal period of 49-66 days or ’ perhaps gyg^ longer’ during the dry and relatively cold South

.^-.-).

History

6. Portschinskia przewalsfcyi (Portschinsky)

Schnabi described this species from thejakutsk province in north-eastern Siberia and Pleske listed three more specimens from eastern Siberia. Grunin (1962a) saw a fair number of specimens from various localities in eastern Siberia (see Fig. 273). He suggests that the normal host of P. loewii is the Altai Pika {Ochotona alpina), in which larvae belonging to the genus Portschinskia have been found. He described and figured them, but could not prove that they actually belong to P. loewii. Abdomen of the imago with long dark brown hairs anteriorly, the last two segments with pale hairs. -This species is clearly distinguished from all other known species by the slightly convex terminal margin of the second antennal segment (Fig. 274a).

Microcephalus pr^ewalskyi Portschinskv, Hor. Soc. ent. Ross. 21, 1887, 9, fig. Portschinskia pr^ewalskyi Pleske, Ann. Mus. Zool. Leningrad 24, 1926, 224; Grunin, Fauna URSS 19 no. 4, 1962, 90, figs.

2. Portschinskia loewii (Schnabi)

History Of this species, only a few adults are known, namely two males and one female, on which Portschinsky based his description- The males were collected at BurchanBudda, Zinchai province, China, and the female on the

upper Hwang-ho river. The abdomen shows three sorts of hairs, yellow ones anteriorly, black medially and reddish ones apically. Shape of second antennal segment is shown in Fig. 274^.

3. Portschinskia bombiformis (Poftschinsky)

Microcephalus bombiformis Portschinsky, Ann. Mus. St. Petersb. 6, 1901, 420, fig. Portschinskia bombiformis Pleske, Ann. Mus. ZooL Leningrad 24, 1926,225; Grunin, Fauna URSS 19 no. 4, 1962, 88, -fig.

7. Portschinskia himalayana Grunin

Portschinskia himalayana Grunin, Fauna URSS 19 no. 4,

1962, 91, figs. Portschinskia pr^ewalskyi Brunetti (nee Portschinsky) Fauna Brit. India, Diptera 3, 1923, 404, figs.

192

SUBORDER:BRACHYCERA History Brunetti received two males and one female from Andarban, Garhwal district, W. Himalayas, and one male from Sikldro, and referred them to P. fnewalskyi, but Grunin recognized that Brunetti had actually been dealing with and re-describing a new species.

Figure 279. Portschiviskia himalayana Grunin. Male head in frontal view and antenna. {After Brunetd)

In general appearance this species is similar to P. pr^ewalskyi, but yellow hairs are found only on the posterior margin of the third abdominal segment in the male. Otherwise the anterior segments have black hairs in both sexes, the posterior ones reddish hairs. Second antennal segment as in Fig. 279. A detailed description in English is given by Brunetti (1923).

Figure280. Oestroderma potunim Portschinsky. Male fly. {After Grunin)

Morphology Imago (Figs. 280 and 281)Superficially similar to Oestromyia species, but the median convexity of the antennal groove (interfacialium) is narrow as in Portschinskia, and the facial ridges are provided with several

Genus: Oestroderma Portschinsky Oestroderma Portschinsky, Home Sue. ent. nss. 21, 1887, 190. This genus contains one species which in its morphological structure is intermediate between Portschinskia and Oestromyia. In biological respects it coincides with the members of these two genera. A Oestroderma potanini Portschinsky Oestroderma potanird Portschinsky, Horde Soc. ent. ross. 21, 1887, 191, fig.; Grunin, Publ. Acad. Sd. URSS (Ent.) 1962, 96, figs.; and Fauna URSS 19 no. 4, 1962, 99,

figs.

Oeslromfia rubtwm Grunin, C.R. Acad. Sd. URSS (N.S.) 73, 1950, 621, figs. History Portschinsky based this genus and species

on

a

male specimen which had been collected in 1885 near the village Shonpjin in eastern Tibet. The author recognized its close relationship to Oestromyia teporina (Pallas), which was already known to be a subcutaneous in the larval stage. Later authors, however, have placed it with the nasal flies. Only Grunin (1962A) succeeded in clearing up the biology of Oestroderma which is, as was to be expected from the morphology of the imago, quite similar to that of the Oestromyia species. He performed his investigations in the Sayanskii Mts., Siberia. Grunin had previously received larvae of this species and described them as Oestromyia ruhtwm.

parasite

Figure 281. OtsUadirmn folmini PorUchiniky. Head in frontal view and wing. {After Grunin)

of bristles. Thorax dull black, with a short pilosity ; with deep black weals as shown in the figure. Abdomen black, slightly shiny ; wings deeply infuscated ; legs blackish. Body-length: 10-12 mm. rows

mesonotum

Egg (Fig. 282)Yellowish, 0-5-0-6 mm long. Characteristic are its boat-shape and a projection at one end, with which it is attached to the body-hair of the host. 193

MORPHOLOGY, BIOLOGY AND PATHOGENESIS OF MYIASIS-PRODUCING FLIES Genus: Oestromyia Brauer Oestromyia Brauer, Verh. wol.-bot. Ges. Wien 10. 1860, 647. There are at present five recognized species of Oestromyia, three of which are also known in the third larval stage. The genus is of Palaearctic distribution, but one species inhabits only the mountainous parts of almost the entire region, while the other four occur only in the Figure 282. Oesiroderma potamni

Portschinsky. Egg. Grunin)

{After

Asiatic part of it. The taxonomy of this difficult genus has only recently been satisfactorily studied (Grunin, 1962a). The three species of which the larvae are known develop as subcutaneous parasites in Lagomorpha of the genus Ochotona, and in several genera ofRodentia, and it is probable that the other species also have hosts in these orders.

The imagines may be recognized from the following key:

1

(6) Wing at the anterior margin lighter in colour than in the posterior part........................ 2

Larvae i and II are

not described.

mature larva is on the average to the Oestromyia larvae, but the ventral side of each segment is provided with four to

Larva III (Fig. 283)The 14 mm long and similar

2 (3) Inner pair of mesonotal vittae behind the suture more than four times as long as broad. 12 mm. 2. 0. koslowi Portschinsky 3

(2) Inner pair of mesonotal vittae behind the suture less than three times as long as broad.......... 4

4

(5)

five irregular rows of denticles.

Puparium is

not described.

Biology and Pathogenesis The only host so far known is the Altai Pika {Ochotona alpina), which has subcutaneous boils in which the third instar larvae are found. Grunin (1962A) does not give any further biological data.

First longitudinal wing-vein (r^) yellow-brown, only the base with a dark spot. Mesonotal vittae

completely

black,

without

yellow

margins.

11-13 mm. 1. 0. leporina (Pallas) First longitudinal wing-vein (r,) predominantly black. Mesonotal vittae black, with the margins narrowly yellow. 11-13 mm.

5

(4)

6

(I) Wing with anterior

Distribution Central Asia.

5. 0. prodigiosa Grunin not

distinctly lighter in colour

than posterior ............................ 7

7 (8) Wing strongly infuscated, but with ill-defined lighter spots all over the membrane. Inner pair of mesonotal vittae behind the suture oval, about twice as long as broad. 13-14 mm. 4. 0. marmotae Gedoelst Figure 283. Oesiroderma Portschinsky.

of raesonotal vittae behind the suture rectangular, about three to four times as long as broad. 14 mm. 3. 0. scrobiculigera Pleske

8

(7) Wing hyaline. Inner pair

1

(4) Ventral

2

(3)

potanim

Third instar larva. {After

Grunin)

to the Third Instar Larvae surface of segments with two to three rows of pointed denticles .................... 2

Key

Anterior spiracles with a blunt projection (Fig.

293). 4. 0. marmotae Gedoelst 194

SUBORDER:BRACHYCERA 3 (2) Anterior spiracles without (Fig. 289).

a

blunt projection

1. 0. leporina (Pallas) row of scale4 (1) Ventral surface of segments with one like denticles almost truncate terminally. 5. 0. prodigiosa Grunin 1. Oeslnmyin lepcrim

(Pallas)Rcdmt Nuked Grub Fly .

Eriangen Oestrus kporinus Pallas, Nov. species quadrupedum 1778, 50, fig. 145, fig.; Oestromyia leporina Brauer, Mon. Oestriden 1863, Povolny, Price Acta Acad. set. cechoslov. Basis Area. 32, 1960, 33, figs.; Grunin, Fauna URSS 19 no. 4, 1962, 109, figs. Hypoderma satyrus Brauer, Verh. wol.-bot. Ges. Wien. 8, 1858, 462, fig. Oestromyia satyrus Brauer, Mon. Oestriden 1863, 143, 270, fig.; Seguy, Emycl. eat. (A) 9, 1928, 79, figs. Oestromyia pallasi Portschinsky, Ann. Mus. St. Petersburg 7,

1902,205.

.

.

.

Oestromyia ivanovi Grunin, C.R. Acad. Sci. URSS

[N.S.} 66,

1949, 1013, figs. Oestromyia dubinini Grunin, id. ibid. 1015, figs. Oestromyia fallax Grunin, id, ibid. 1015, figs. Oestromyia orba Grunin, id. ibid. 1015, figs. Oestromyia braueri Grunin, id. ibid. 1016. Oestromyia subfallax Grunin, C.R. Acad. Sci. URSS

Figure 284

nyia leponna (Pallas). Male fly. {After Grunin)

part. The eyes are broadly separated in both sexes, but the frons is broader in the female than in the male. Interfacialium bare. Thorax black, with a dense bluish

(N.S.)

73, 1950, 622, figs. History For about 100 years this species was known in the literature as Oestromyia satyrus, originally described by Brauer in 1858 as a Hypoderma species from three specimens caught on the wing in the Steiner Alps in Austria. Brauer suggested in this paper that the host of the larvae could be the Chamois. In 1860 he created the genus Oestromyia for it, and in 1863 he published the first biological observations and reported an experimental infection of a rabbit and guinea pig; the larvae however succumbed after a certain period. Only 1 year later was Brauer able to give a description of the third larval stage and to record the true host of his 0. satyrus in Europe, namely the Common Vole. In 1866 he recorded a Pika as host of the Asiatic 0. leporina, with which 0. satyrus was later synonymized by Grunin. Povolny (1960) gave an excellent summary of what was known of the systematics and the biology of 0. leporina, and he and his collaborators added a number of new observations. The latest summarizing discussions of this variable and widely distributed species is by Grunin (1962a), who synonymized six species with it which he had previously founded on the third larval stage, and a further species created by Portschinsky in 1902.

pollinosity and a distinct pattern of dull and deep black longitudinal vittae. Wings hyaline, with a slight yellowish tinge, veins mainly yellow-brown, only the base of the wing with a few dark spots and the first longitudinal vein (r,) darkened at the base. Legs black. Abdomen glossy black, without pattern or pollinosity. Body-length: 11-13 mm. with a short, somewhat umbrella-like projection posteriorly. The total length is ^-^mm. Larva IRelatively short and composed of twelve distinct segments, which bear rows of small denticles. Posterior spiracles circular.

EggOval,

Morphology Imago (Figs. 284

and 285)Head predominantly orange and yellow, only the ocellar triangle and the parafrontalia black, the latter sometimes only in the unoer upper

S

M"’"’.}

"ft

^-^

:’&"?A5

^^y ?,’>»

*

t.

a fc

’’-.’’

A

History This species was based on four male flies caught on the wing in Sicily and near Mt. Sinai. When writing up his monograph on the Oestridae, Brauer (1863) received a fifth male from Dalmatia. Two of the collectors had noted donkeys in the vicinity of the catching places, and suggested that this animal might be the host of the larvae, but Brauer remained sceptical in this respect. Patton (1921), in a summarizing paper on myiasis-producing flies, then declared definitely that P. silenus develops ’ in the skin of the ass in Egypt’, merely an assumption which was taken over by most later authors. Grunin

&

»>

^^y^^^y

^

(1953, 1962(7} recorded it for the first time from goats and sheep in Central Asia, and Zumpt (1962a) saw larvae from gazelles in North Africa, which he referred to P. silenus, to which Hypoderma ga^ellae Gedoelst from Tanganyika is placed

as a

synonym.

Morphology Imaoo (Fig. 314)Two males before me, identified by Brauer, have tlie thorax and abdomen densely grey and oiive pollinose. There are short yellow hairs on the mesonotum, and longer yellow-white and greyish ones the abdomen. The abdominal tessellation is distinct and changes with the light incidence. The mesonotal stripes are narrow and not shiny. Legs are yellowbrown, with the femora and tibiae more or less blackenedThe three species P. crossii, P. silenus and P. aegagri must be verv similar to one another. According to Patton (1936^), van Emdcn (1950) and Oldroyd (by letter), the abdominal hairs in P. aegagri and P. crossii are shorter, more recumbent and brassy or golden yellow. The differences in the shape of the intcrfaciaiia and the width of the median convexity of the antennal grooves are shown in Fig. 314. It is possible that Grunin (i962a) was right in lumping these three forms, and that the above differences have no real specific value.

on

Id Figure 312. Przhevalskiajia crossii (Patton). Third larval stage: of fifth segment; and (c) poste spinulation frontal view; (6) ventral peritremes

third week of August, the second stages between October and the middle of November, and the last stages in perforated warbles until mid-March.

Pathogenesis Certain herds of goats in the Punjab were found to be

infesteTto Ze"exTent"of"more’than90per cent," and in

a

Egg, Larvae I and // (Figs. 315 and 321)Have been described by Grunin (1962a), but I gained the impression

210

SUBORDER: BRAGHYCERA that his discussion is based on P. crossii, or even taken for a greater part from Soni’s papers (1939-1942).

drawings given by

Mediterraneum where gazelles occur and goats are kept. According to Grunin (1962a) this species is widespread in the central ^aatic parts of the U.S.S.R.

Grunin (1962a) coincide more with the larva of P. cnssii than with larvae which I believe may renresent may actually actually represent P. silenus. These larvae have only a few rudimentary

(Bnuer)-C,,,.. G.at W.rU. Fly (Br,uer)-C..l., ":."ft’"1""’" ""W-"w Brauer, Mm. Oestriden 1863, 281, 134,

Larva III (Figs. 316 and 317)The

,

ng’

and irregularly arranged denticles above the mouth-dots, and hardly traceable in some thev are but they - variable specimens. This feature is therefore intermediate between P. crossii and P. aegagri. The armature of the bodysegments agrees generally with that in Grunin’s figure, the arrangement of spines of the fifth ventral segment and the shape of the posterior peritremes have been drawn from a North African specimen before me,

Austen, Bull. ml. Res. 22, 1931, 423, figs.; Patton, Ann. trap: Med. Parasit. 30, 1936, 466, figs. ; Van Emden, Bull. ent. Res. 41, 1950, 223, fig.

W1"’""1 """turn

’

recovered from 25 mm.

Puparium is

not

a

gazelle. The biggest larva

, ;>’rf Die Rcspirationsorgane der Gastriden. S.B. Akad. Wiss. Wien. math. -nat. A7. 108. 235 (190l’i L’eber die Gattung Gyrostigma Brauer und Gyrostigma conjungens nov. spec. nebst Bemerkungen zur Phvsiologie. Arch. Naturgesch. 67, Festschr. Ed. van Martens, Beihefl 23 (1928^ Sarcophagiden-Studien II. Konoit-ia 7. 147 ENGEL, E. 0. (E920) Dipteren, die nicht Pupiparen sind, als Vogelparasiten. Zl. it’iss. Insekt. Blol. 15, 249 ENIGK, K. (1943) Zur Vorbeuge und Bekampfung der Gastrophitose der Pferde. Z. Veterindrk. 55, 272 EVANS, A. C. (1936) The physiology of the sheep blowfly Lucilia sericata Meig. (Diptera). Trans. R. ent. Soc, Land. 85, 363 EYSELL, A. (1915) Sarcophaga fuscicauda Boettcher, ein Darmparasit des Menschen. Ent. Mitt. 4, 3 FAGGIOLI, R. (1927) Erisialis tenax, parasito accidental del cuerpo humane. Sem. med., B. Aires 34 no. 1734, 887 FAIN, A. (1953) Cordylobia ruandae n.sp., nouvelle mouche a larve cuticole parasitant Ie tissu sous-cutane d’un rongeur

(Grammomys surdaster) au Ruanda-L’rundi (Congo beige). Ann. Soc. beige Med. trop. 33, 603 MAGIS. P.. VERDIN. G., DONKERS, J. and GOBSELS, P. (E959i Sur deux cas de myiases humaines produites par Chrvsomvia bezziana Villeneuve, au Congo beige. Ann. Soc.’beige’Med. trop. 39. 763 FALLIS. A. M. (1940) Studies on Oestrus ovis L. Canad. J. Res. {0} 18, 442 FAL-LKNER, D. E. and K.IXGSCOTE, A. A. (1936) Observations upon the migrations and pathogenesis of Gasterophilus larvae. J. Parasit. 22. 223. FIEDLER, 0. G, H. ’1951; Die Nahrung der Myiasis-FHegen!arven auf dem U’ollschaf. Z. angeu\ Ent. 33. 142 and DL- TOIT. R. ’1954i The protection of sheep against blowfly strike [II. The ! ciilhbert.wn. Miisca, 32

(../l-htdapsis. 187 O/’/wwyw, 14. 15, 117. 143. !^6. 147. 150. 151. 152. 153, 245

rvaSh^wi.f.

ci’f;’)f;;c«;’"f(.

ii-u,

32

Hydrfitnea. -H

/
Radhaiwn’iii. 16. ;J6. 141 mslmlii. li/iiirm. 3. 7;. 42. 62. 238 rostrata. Perwm. 41

234

tiabulorum, \Iusca, 38 ftabtllartim, Mtisciaa, 3, 37. 3S, 238 PackychGeromyia, 2, 46, ^5 pallasi, Oestromyia, 195 Patlasiomyia, 12, 141, 204 /|
230.231. 232

RailbaadilHa. 47 CiihhMia. 136 rortr»i. Rwlhaimmyia. 4. 134. 135. ;J6. TOWI.

PrtstirhviKhwin-ia. 31 /irsdigiina. Otilrwii,. 4. 194. 195. 236 Proekon. 58, 63 Profwwia. 42

Progaslrofiittli^. i 11 Promitscci. 31

262

"

137. 138. 234 ruandae. Cordvhbia. 3. 70. 71. 72, 77, 75, 236 rtsbifrons. CaUi/iiwra. 60 ntb^’}ii. Oeslromyia. 193 ritjibarbt.^. Ce/ihenomyia. 152

INDEX OF PARASITES 152 rtifiharb^. Oestrus. 107 ruficornt!,. Mvsca.

stimulator. Cetihenomvia. 150 stimulator, Oestrus, 150

107 rf;’;rop»’ Parasarcof’haga. ,,;/,r^«.i. Surcofthaga. 3, 7(?7, 237. 239 n^c^. OnM"’^. 3. 62. 90. 91. 92. 93.

Siobbeola. 58

%. 237. 238 ni/i/’eit-ies. Chrysomyia. 92

^omo.^.

nifihcies. Luciiia. 92 rw/;/^.

Al’hiochaeta. 21

n;/;/’^- CnHii’lwra. 63 3, 2/. 237

n^/’cj, .Mi’sa^’iia. w/;/w. Mo^. 21 n//i/!es. Sarcoj>haga. 106 rufifies. Trinnira, 21 /?»//^za. 6, 111. /J^. 139. 140. 141 Huiirniinac. /J^

saigae. Hy/iodenna. 204 Sarcofihaga. 2. 8. 13. 15. !6. 34. 36. 46. 102. 103,104, 107. 108, 109. !1U. 240 saiyrus. Hyfioderma. 395 safvrus. Oeslromvia. 195 scalaris, Aphiochaela. 20 5ca/^u. Fannia. 3. 28, 42. 43. -!-!. 45. 238 j^/am. Megaselia. 3. 79. 20, 21. 237. 238 scalaris. .Musca, 44 wi/aw. ^/iory. 19

’

Schnablia. 189 scrobiculigera. Oeslroinyia. 4. 194, ;95 securifera, Parasarcofihaga. 107 securifera. Sarcophaga. 107 senegalensis. Ochromvia. 67 iwca;rt, ZUC;’/M. 1. 3, 38, 47, 48, 49. 50. 5!. 52. 53. 54. 62, 65, 82, 104. 110, 237, 238,242

Musca. 47 sericata. Phoenicia, 47 sencala.

Psychoda, 2. 19, 238 silenus. Crii-eltia, 210 sexfnmctala,

silenus, Hyfiaderma, 210 silenus. Przhei-alskiana. 4. 205, 206. 208, 209,2/(7. 211,212, 214. 235, 236, 238 siiraritm. Luciiia, 47, 56, 57 shnu!alrt.v. CaHifihora, 54 sinense, Hypoderma, 221

Sonwmya,

58

Somomyia. 89 sordida. .Musca. 83 Sf)athicera. 129. 130 spiracularis. Mcgaseiia. 3, 2/, 22, 238 sfilendida. Luciiia. 53 stdendida, Musca. 53 squamosa, Neoculerebra. 4. 139. ;-W. !41. 234 sfabufans, Musca. 36 siabulans, Muscina. 1. 3. .^. 37. 38. 44. 60, 233.237,238 Slasisia. 70

Steinonvfia. 42 ^y»i, Rhiwesfrus. 4. 159. 160. 161. 16’’ 164.J6J.234 stimiflafor. Ce/ihenrmvw. 4. 147. 14". 7,50 152. 234

Slomachobia. 11 1 Slomachomyia. 129

13. i5. 31. J.i

Trypocalliphora, 83 tshernyshei-i, Rhinoestrus, 4, 160. 167, J70, 171. 236 tuberosa, Parasarcofihaga. 106 iuberosa. Sarcof/haga, 3. ^6 Tyrophaga, 24

sirefistceronlis. Dermar-e^trs^. 202 siriafa. Musca, 108 .(/na/rt.

Rarinia. 108

striata.

Sarcofiha^a.

4. ;/?^- 239

.’trigi/ies. Batrachomyia. 3. J9. 30. 230 Strobiloestrus, 11. 142. /99. 201. 202. 203. 235. 240 jfv?;a. Callilihora. 3. 58, 6/. 62. 63. 64, "65. 230, 238 siygici. .MHSCC. 61 subciitaneus. Oestrus. 218 subfallax, Oeslroniyia. 195 subguUurosae. Parlorskiala, 4, 199, ^0^, 203. 209. 214. 235 siibtrimslucida. Somomyia. 67 subtiibero.-ia. Sarcofihaga, !06 xiimairensis. Gyrsoligma. 4. /.JJ. 234 sniifilens. Oestrus, 221 surroufi. Kirkia, \ 58 slircoiifi. Kirkioestrns. 158. 159 Svnanil’honeura. 31

y/ncAi;, Cephenemyia, 4. 147, ulrichii. Cejihenomyia. 151 unnaria, ScateHa. 28

/J/,

152, 234

usbekislanicus. Rhinoestrus. 4. 159. 160. 161, 162. ;6J, 164, 168. 173. 234. 237

.wi^/;. Rhinoestrus, 4, 14, 160, 171, 172, J7,?. 174 ;wi;y/;’, Sirobiloesirus, 4, ;99, 200, 201,

202, 235. 240 cariulosus. Ce/^haiomyia. 181 rarwio.’iiis. Oestrus, 4. 174, 175, 176, ^J,

182, 185. 235 1’arifies, Balrachomyia, 29 ran^, Chrysomya. 3, 89, 90, 91, 9J. 238

Tachina. 110

varijies, Luciiia, 93 varipes, MicrocallifJhora, 93 veitchi, Passeromyia, 3, 47 vernalis. Oestrus bovis var., 221 ueterinus, Gaterophilus, 1! 7 vicaria, Batrachomyia, 5, 28, 29 ricaria. Chlorops, 29 vicmo. CalUphora, 3, 38, 44, 55, 59, 60, 61.

tarandi. Hyjioderma. 2 14 larancii. Oedemagena, 4. ^/-/. 215.

L’irina,

Syrphidae. 3, ^, 238 szlami’i. Rhinoeslrns. 163. 364 Tabanidae. 5

Tabanomorpha. 5

2!6. 217. 218. 222. 225. 226. 229. 234. 244

Usrandi. Oestrus, 214

tauffiiebi, \’eocordfhb}a, 70 Teichomvza. 15. 16, 2^ lellninnl Chrysomyia. 96 /e%7.v. Eristalh, 2, 3, 22, 23. 24, 238 /e«t7;. 147

263

J^. 109

Af’hiochaeta, 19. 20

INDEX OF HOSTS Aardwolf. 233 Accipiter, 230 (tethiopicus, Phacochoerus, 23-1

afer, Orycteropus, 233 afra, Tatera, 236 africana, Loxodonta, 234 agrestis, Microtiis, 237 Alauda, 231 Alaudidae, 231 alba, Motacilla, 231 albicollis, Muscicapa, 231 albopunctatus, Heleioporus, 230 Alcelaphus, 235 Alces, 234 alces, Alces, 234 alpina, Ochotona, 236 Alytes, 230 ammon, Oi’is, 236 AMPHIBIA, 230 amphibius, Hippopotamus, 234 Antbear, 233 Antelope, Roan, 235 Antelope, Sable, 235 Anthochaera, 233 Anthus, 231 Antidorcas, 235 Apodemus. 236 Aquilidae, 230 Argall, 236 ARTIODACTYLA, 234, 237 arundinum, Redunca, 235 arvalis, Microtus, 237 arrensis, Alauda, 231 Arvicanthis, 236 Arvicola, 237 ater, Partis, 232 atricapillits, Parus, 232 atricapilla, Sylvia, 231 AVES, 230, 237 Bactrian, 237 berigora, Faico, 230 bibromi, Pseudophryne, 230 bicornis, Diceros, 234 Bird, Brush wattle, 233 Bird, Latham-lyre, 233 Blackbird, 231 Blackcap, 231

Blesbok, 235 bonellii, Phylloscopus, 231 borin, Sylvia, 231

Bovidae, 234 « Buffalo, Water, 238 Bufo, 230 Bufonidae, 230 Bunting, Corn, 232 Bunting, Reed, 233

b-drchelii, E^iius. 234 buselaphits, Alcelaphus, 235 Bush-pig, 234

caerulea, HySa, 230 caeruleus, Parus, 232 calandra, EmberUa, 232 Callaeidae, 233 Camel, 237 camelopardalis, Girajfa, 234 campestris, Raphicerus, 235 campestris, Saccostomus, 236 canarius, Serinus, 232 cangwu, Macropus, 233 cannabina, Cardueiis, 232 cantillans, Sylvia, 231 capensis, Motacilla, 231 Capra, 236 Capreolus, 234 capreolus, Capreolus, 234 capreolus, Pelea, 233 Caprimutgidae, 230 Caprimidgus, 230 Cardueiis, 232 carduelis, Cardiielis, 232 CARNIV’ORA, 233, 237 Cat, 237 Cat, African Wild, 233 Cattle, 237 caucasica, Capra, 236 caudata, Marmote. 236 Cephalophus, 234, 235 Cercopithecidae, 233 Cercopithecus, 233 Certhia, 232 Certhiidae. 232 Cervidac. 234 Cenw, 234 Chaffinch, 232 Chamois, 236 ChifEchaff, 231 Chimpanzee, Long-haired, 233

CHIROPTERA, 233 Chiru. 235 Chlons. 232 chloris, Chloris, 232 chrysophilus, Rallus, 236 chrysoptera, Anfhochaera, 233 cinerea, Motacilla, 231 cirnei, Rhynchocyon, 233 Citellus, 236 citrinvlla, Emberiza, 232 citropa, Hyla, 230 coelebs, Fringilla. 232 collurio, Lanius, 232 collybita, Phyiloscopus, 231 communis, Sylvia, 231

264

Connochaeies. 235

CORACIIFORMES, 230 cornix. Con-us, 232 corone. Cornis. 232 Corvidae, 232 Corvus, 232 \ Creeper, Tree, 232 \ Cricetorrys, 236 Crinia, 230 crisfafus, Parus, 232 1 cristatus, Proteles, 233 Crow, Carrion, 232

. ,

Crow, Hooded, 232 cucullatus, Spermestes, 232 cuprea, Nectarinia, 232 curwniae, Ochotona daurica, 236

Dama, 234 dama, Dama, 234 Damaiiscus, 235 daurica, Ochotona, 236 Deer, Musk, 234 Deer, Fallow, 234 Deer, Red, 234 Deer, Roe, 234 Deer, Sika, 234 Delichon, 232 dendyi, Pseudophryne, 230 Dicaeidae, 233 Diceros, 234 Didemoceros, 234 Discoglossidae, 230 Dog, 237 dolichorus, Grammowys, 236 domesSicus, Passer, 232 Donkey, 237 dorcas, OamaUscus. 235 dorcas, Cavlla, 235 Dormouse, Fat, 236 dorsaiis, Cephaiophus, 234 Dromedary, 237 Duiker, Bay, 234 Duiker, Black-fronted, 235 Duiker, Blue, 235 Duiker, Grey, 235

Elephant, African. 234 Elephant, Indian, 233 Elephant Shrew, Cirne’s Checkered, 233 Elephant Shrew, Scuhlmann’s Checkered, 233 elaphus, Cervys, 234 elegans, NauUinus, 230 Elephantidae, 233 Elephas, 233 Elk, 234 Emberiza, 232, 233

INDEX OF HOSTS

Equidae.2^

233 eouinns. Hifipolragus,

EQUUS. 234

friceiorum, Turdus, Enlhacus, 231

231

F.nlkrocebus. 233 tTvthfopus, escitlenia,

Hartebeest. Common, 235 Hartebeest, Lichee nstein’s, 235 \ \ Hawk, Brown. 230 ; Helewporus. 230. 232 l

Xerus. 236

Rana, 230

r^ico. 230 Falconidae. 230

\

Heleioscittras, 236

[ \

Hippopotamidae, 234

’

Hippopotamus. 234 Hippotragus^ 235 hircus. Capra, 236 Hin-indinidae, 231 Hirundo. 231

Felidac. 233

hodgsortii. PanSholo{>s, 235 Honey-eater, Tawny-crowned, 233 Honey-eater, While-cheeked, 233 Honey-eater, Yellow-winged, 233 Hyla. 230

FeHs, 233

Hylidae. 230

jlara, Motacilla, 231 flavopunctatus. Lophwomys, 236 Flycatcher, Coilard. 231 Fivcatcher, Pied, 231

hypopleuca. .Miiscicaf/a, 231 hyfioxanliiiis, Oenomys. 236

Fringilla, 232 Fringillidae, 232 Frog, Blue Mountains Tree, 230 Frog, Burrowing, 230 Frog, Common Grass, 230 Frog, Edible, 230 Frog, Field, 230 Frog, Green Tree, 230 Frog, Leaf Green Tree, 230 Frog, Tree, 230 Frogtet, Common, 230 Froglei, Smooth, 230 fulvorufula, Redunca, 235

ibex, Capra. 236 Ibex, Siberian, 236

FALCONIFORMES, 230 familiaris. Cerlhia, 232 231 Faniail. Black and White,

GALLIFORMES, 237 gambianus, Cricetomys, 236 gambianus, HeSiosciurus, 236 Gazelle 235 Ga^ella, Oryx, 235 Gazclie, Dorcas, 235 Gazelle, Goitred, 235 Gazelle, Grant’s, 235 Gazelle, Mongolian, 235 Gecko, Green, 230 Gekkonidae, 230 Gemsbok, 235 Gerbil, Bocage’s, 237 Gerbil, Cape Greater, 236 gergalis, Microlus, 237 Gira/a, 234 Giraffe, 23-1 Giraffidae, 234 Gliciphiia, 233 glis, Glis, 236 gnou, Connochaeles, 235 Goat, 238 Goat, Wild, 236 Grammomys, 236 granil, Gazella, 235 Greenfinch, 232 griminia, Sylvicapra, 235 griseus^ Passer, 232 Guinea Pig, 238 gullerosa, GazeUa, 235

infrafrenata, Hyla, 230 1NSECTIVORA, 233

Jynx, 231 Kangaroo, Cook’s, 233 Kangaroo, Dusky, 233 Kangaroo, Red, 233 Klipspringer, 235 Kobus, 235 Korrigum, 235 korrigum, Damaliscus, 235 Kudu,235 laevis, Crinia, 230

LAGOMORPHA, 236, 238 Laniidae, 232 Lanius, 232 Lark, Sky, 231 leche, Kobus, 235 Lechwe, 235 Leopard, 233 leucophrys, Rhipidura, 231 libyca, Feh’s, 233 lichlensletnii, Alcelaphus, 235 Lophuromys, 236 Loxodonta, 234 lunatus, Damaliscus, 235 Luscinia, 231

Macropodidae, 233 .Macro/ws. 233 Macroscclididae, 233 major, Parus, 232 MAMMALIA, 233, 237 Mannequin. Bronze, 232 Marmot, Long-tailed, 236 Marmole, 236

265

marmorata,

Uperoleia, 230

MARSUPIALIA, 233 marsupialis, Antidorcas, 235 Martin, African Sand, 232 Martin, European Sand, 232 Martin, House, 232 maximus, Elephas, 233 megarhyrtcha, Luscinia, 231 meianops, Gliciphiia, 233 melanostictus, Bufo, 230 MeUornis, 233 Meliphagidae, 233 Menura, 233 Menuridae, 233 merula, Turdus, 231 Microtus, 237 mona, Cercophiihecus, 233 manacha, Silagra, 232 Monkev, Mona, 233 Monkey, Red, 233 Monkey, Vervet, 233 monticola, Cephalophus, 235 moschiferi, Moschus, 234 Moschus, 234 Motacilla, 231 Moiacitlidae, 231 Mouflon, 236 Mouse, Cape Pouched, 236 Mouse, Field, 237 Mouse, Forest, 236 Mouse, Large Japanese Field, 236 Mouse, Pine, 237 Mule, 237 Muridae, 236 Muscardinidae, 236 Musdcapa, 231 Muscicapidae, 231 mitsimoit, Ovis, 236 nataieiisis, Raiius, 236 Naullinus, 230

Neclarinia, 232 Nectariniidae, 232 niger, Hippoiragus, 235 niger, Meltomis, 233

Nightingale, 231 Niglitjar, European, 230 nigrifrons, Cephalophus, 235 niloticus, Aruicanihis, 236 nipjson, Ceruus, 234 nisus, Accipiter, 230 noclula, Nyctalus, 233 novae-hollandiae, MeUornis, 233 Nyctalus, 233 obslelricans, Alyies,

230

Ochodontidae.. 236 Ochotona, 236 ochurus^ Phoenicwus,

231

Octodoncidae, 236 oeconomus, Microtus, 237

Oenanthe. 231 oenanlhe, Oenanthe, 231

I.XUI’.X 01- HOSTS Ounomys. 236 Ondatra, 237 oreoiragus. Oref^Sra^u^, 23.) Oryctcropodidae. 233

Orycteroplts. 233 Orvx, 235 Oi-is. 236

Pachwephilla. 233 Pachyccphalldac. 233 paedtlicus, Raiius, 236 paiudicola. Ripariii, 232 Pan, 233 Patlthera, 233 Panikohfis, 235 Pardaloie. 233 Paraalolus, 233 pardlis, Panthercl, 233

,

Mlliirrcl. Ra[. Mu>k. .’.;7

R;ll.

SikaplB-

Har,ll.llirr,-il. .’.)’; !fi

R.tl. S]ird Ground. 236

Rai. Nil... 236 Rat. Urd V.-ld, I’ll, Ral. Rilloiis-iios.-il. 296

-’

~"iiilimiiui. KImK/wmit. 233

234 Oideitiocerus, 2.14 Sunbird. C:oppery, 232 Swallow. European. 231 Swallow. Mosque, 232 Swallow. Rutbus-chested, 231 Sil-tflderiantis, Thryonomys, 236 Sylria, 231 Svlfica/ira, 234 .Svlviidae, 231 Suidae,

Rr.’dbiick. C;oii]iili)il. ;;.; Rvfdhurk. MDuiu.tiii. -’.)’.) Rcindrrr. 2.S4 Remizil, 232

REPTIHA. 2.U) Rhcbok. V.-ial. 235 Rhinoceros. Asiatic ’I’u-o-lioi-in’il. 234

Paridae, 232

Rliinocrros, Black. 234

Pans, 232 Passer. 232

Rhinoceros. While. .’.>.;

PASSERIFORME.S, 231 patas, Erythroceblis, 233 Ptiea, 235 pendultnus, Rcrntza, 232 PERISSODACTYLA, 234, 237 Phacochoerus, 234 Phoenicians, 231 phoenicurus, Phoenicurus, 231 fhyUxhraa, Hyla. 230 Phyllcsapus, 231 Picidae, 231 Pig, 237 Pika, Pallas’, 236 Pika, Red, 236 1’ika, Steppe, 236 Pipit, Meadow, 231 I’ipit, Tree, 231 Pilymus, 237 Ploceidae, 232 Ploaiis, 232 Pongidac, 233 Potamochoerus, 234 porcus, Polamochoerus, 234 Poultry, 237 pratensis, Anihus, 231 PRIMATES. 233, 238

Kllipiliurn. ’2’31 Rhynchocyon. 233 Rifiarin. 2.12

swimtrensts.

Rhinoccroiidae. 234 laraildtts, Raitgtfer. 234 laiarica, Saiga, 236

Tukra, 236, 237 mlilisllis. .Miicrii/iiis. 23.1 RODENT].\. 236. 2.1S

Thryowmys, 236

mll/rula. Enlhinis. ’231

nifiiinlris. P,KliKC/’hala.

.

faurintis, Connocfiaeles, 233 lemporaria, Rana, 230 lerreslris, Aruicola, 237

Robin, -’.;/

233

rn/lis. .\tMr,,/,lK. 233 Ruliicaiiru. 236

rupictlpra. Rlll.ititprtl. 236 nislila. Hbui\,l.,. 231 nilitil, Ot/wl’.’m. 236

Simasl’imm. 236

Saiga, 236 Salamander. Spoiled. 2311 Salmiumdm. 2.111

satamandra. Stdanmndra. 230 Salamandridac. 2.10

Tit, Blue. 232 ’[’it. Coal, 232

I’it, Crested, 232 Tit. Ureat. 232 Tit. Penduline, 232 ’I’it, Willow, 232 Toad. Common Asiatic. 230 Toad. Common European, 230 Toad. Midwife. -’JO Toadlci. Brown. 230 "I’oadlet. Southern. 230 Toadlel, Yellow Spotted. 230

’[’r,w/!il.l’luis, 23.1

schoeincltli. Eimirn^is. 233 Sciuridae. 2.16 semirnja. Hinmh. 2.11

;?.,(-W,’,,.

PROBOSCIDEA, 233

Serin. 232

Tri)s,lod\ lidae, 23 I

Prateles, 233 Prolelidae, 233 Pseudophryne, 230 punctallis, Heliosciurus, 236 plisiila, Ochotona, 236

siliil,ilnx. I’ln ’;,"..,;,«., 231

l’L’HLT.!UE.\T.\’l’.\.

slAn/.K.il. hil.hmrm:-’. 236 Stilus.

Didm--. 2.14

SHagril. 2 >’.’

Rabbit, 238

Shrike, Red-backed. 232 speciosa, AfMdrnuts. 236 Song-thrush. 231 Souslik. Long-taiicd Siberian. 236 Sparrow, Grcy-heridcd. 232 Sparrow-ha\\-k. 230

Sparrow. Housr. 232 Spermesles. 2.12 Springbuck. 23~)

SQ.L’A.\[.\1.\,

’1’urdidae. _’.;;

r.iniiis. 231

Sheep. 23H

Rana, 230 Ranidae, 230 Ranpfcr, 234 Raphicems, 235 Rat, African Giant, 236 Rat, Black-tailed Tree, 236 Rat, House, 236 Rat, Larger Cane, 236

l’lirll,,m/,ui. 2.11

23(1

233

2jl Vole. Common. Vole. Narro’.-sk""’-"’ Vole. Rool.

23^_

Vol>-."aicr.-" ;,,/,»,K, &/», ,.,,^,,,. &»^.». -^-

-^

_

INDEX OF HOSTS --"

Waeiail. Grey. .31 Wagtail. While. Wagiaii. Yellow. 231

^’

wren-

Wheatear. ;31

African Little. 232 Whistler. Rufous, 233 Whiiethroal ~’3l 235 Wildebeest

\\"eaver. Wcsl

Black.

231

Wryneck. 231

Warbler. Willow, 231 Warbler. Wood. 231 Warlhos;. 23-1

Weaver. Masked. 232 ,

Wagtail. Cape. 231

Wildebeest. Blue. 235

Warbler. Bonclli’s, 231 Warbler. Garden. 231 \Varbler. Subalpine. 231

Xtrus. 236 .

Yellow-hammer. 232 Zebra. Burchell-s. 23-1 Zebra. Mountain, 23-1

abethica. Ondatra. 237