Bionomics, ecology and vectorial characteristics of the onchocerciasis in Latin America and the forest zone of west Africa with reference to the situation in Guatemala and Liberia

WORLD HEALTH ORGANIZATION ORGANISATION MONDIALE DE LA SANTE oNcno/wP/75.10 ORIGINAL: ENGLISH EXEERT COMMITTEE ON EPIDE},IIOLOGY OF ONCI{OCERCIASIS Geneva, lO-18 November 1975 Draft agenda item 3.2 CS, J ECOLOGY AND VECTORIAL CHARACTERISTICS OF THE ONCIIOCERCIASIS IN I.ATIN AMERICA AND THE FOREST ZONE OF WEST AI'RICA WIIH REFERENCE TO THE SITUATION IN GUAIEMAI.A AI{D LIBERIA by R. Garms ard-Nocht-Institute for Maritime and Tropical Diseases . Hamburg, Federal Republic of Germany (- )lJ o t1 C I I I 1 i}' .it 1. INTRODUCIION Blackflies (Sirnuliidae) are the only known vectors of hrmran onchocerciasis, due to Onchocerca volvulus both in Africa and the Western llemisphere. Soon after the discovery of the disease in Guatemala, Robles (1919) suggested that blackflies, being a cormon nuisance in the coffee-growing areas, where the infections occur, might be the carriers. This was confirmed some years later by Blacklock (1926) in Africa, who demonstrated the full develop- ment of the parasite in Simuliun damrosum. Although a few other species occasionally bite man, in the forest zone of West Africa only those species belonging to the Simuliuo damnosum complex are concerned as vectors. In the Western Hemisphere the situation is more complex due Eo Ehe presence of a large ntrmber of man-biting species. The vector efficiency of most of them has not yet been sufficiently c larified. It is controversial whether O. volvulus was carried with African slaves to the New World and had adapted itself to neotropic blackfly species, or whether the parasite was indigenous much earlier in this continent (Ruiz, 1952; Figueroa, f963). Evidence based on transmission experiments with a variety of O. volvulus strains from Guatemala (De Leon & Duke, 1966; Duke et aL.,L967; Duke &Moore, L974), Venezuela (Duke, regions (Duke et a1., 1966), led to the hypothesis (Duke, The issue of this document does not constitute formal publication. lt should not be reviewed, abstracted or quoted without the agreement of the World Health Organization. Authors alone are responsible for views expressed in signed articles Ce document ne constttue pas une publrcation. ll ne doit farre I'objet d'aucun compte rendu ou r6sumd ni d'aucune citation sans I'autorrsation de l'Organisatron Mondiale de la Sant6. Les opinions exprim6es dans les artrcles sign6s n'engagent que leurs auteurs. L97O) , I,Iest African fo 1970) that Onchocerca rest and savanna -Simulium complexes in West Africa and Latin funerica are dist.inct entities of considerable evolutionary antiquity. In principle, a long period of adaptation is probably not necessary for the parasite to establish itself in a new blackfly host. Even pre-adaptation may be anticipated. This is indicated by the observation that O. volvulus can develop in several blackfly species unlikely to be vectors, because they r.. diGf6ffi,rtside the endemic areas or fly-man contact is only occasional (Gibson & Dalmat, 1952; Duke, 1962; Wegesa, L967, L97O). 2. VECTORS IN I"ATIN A},IERICA In Ehe Western Hemisphere onchocerciasis foci are known from Mexico, GuaEemala, Venezuela, Colombia and Brazil. Further foci may occur outside these countries, indicated by findings oNcHo/wP/75.10 Page 2 of single cases in Surinam (Hartz, 1950) and Ecuador (Burch, 1961). Most of the information on the vector is available from Mexico and Guatemala, where investigations on blackflies started soon after the discovery of the first Arnerican onchocerciasis focus (Hoffmann, l93O; Strong, 1931). Only very few observations were published on the other foci. 2.L Presumed vectors of O. volvulus and main man-biti,ng species 2.L.L Guatemala and Mexico: There are Ehree foci in Mexico (0axaca, north and south foci of Chiapas), and four in Guatemala (two in Huehuetenango in the north-\^rest, and two on the western slopes of the Sierra Madre along the Pacific coast). Ihey are all located in mountainous areas, usually at altitudes between 5OO and 15OO m, covered by humid forests or coffee plantations. Three spec ies S. ochracetrm, S, met4llicum and S. callidum, in order of imporEance, have been incriminated by most authors, (Strong, 1934; Elishewitz, 1953; Dalmat., 1955; De Leon, L957; Vargas, L962; Davies, 1968). s ochraceum was considered as the main vector , since this. species is highly anthropophilic, whereas S. metallicum and S. callidum were found to be roostly zoophilic. S. gonzalezi S veracruzanum and S. haematopotum were considered as possible but not proven vectors in limited circumstances (Da1mat, 1955; Vargas, 1960). By means of transmission experiments it was shor"m that 0. volvulus can complete its development in S. ochraceyrn S. metallicum S. callidum (Gibson, 1965; De Leon & Duke, 1966), S. veracruzanum and S. haematopotun Gibson & Dalmat, L952). 2.L.2 Venezuel-a: Two foci exist along the slopes of the coastal mountains, but sporadic cases occur also in other regions (Convit, L974). Altit.udes of the foci ranged from 8OO to 1OOO m. S. metallicum seems to be the main vector, but S. exigur:rn was considered as a secondary one (Lewis & Ibrte, de Aldecoa, 1962; Convit, L974). Duke (1970) showed that 0. volvulus completes its development to the infective stage in both species. 2.L.3 Colombia: One focus is known at the Micay River on the western slopes of the Andes close to the Pacific coast (Corredor, L974). S. exiguurn S metal-1icum S callidtm and to a lesser extent S. sanguineum are the main man-biti,ng species (Barreto, 1969; Guttman, L972). These species are mostly zoophilic, but in the absence of cattle and horses the presumed vector, S. exiguun, could become anthropophilic (Barreto et aL., L97O; Trapido et al., L97L; Corredor, L974). 2.I.4 BrazLl: 0nchocerciasis was discovered in mountainous areas close to the Venezuelan border(I'1oraes,L974).Man-bitingb1ackf1ieswereidentifiedasS.pintoi,@ and S. amazonicr.rn (Rassi, L974, cited by Moraes, L974). Natural infections with sausage st,ages, believed to be those of 0. vo_\,ulus, were found in S. amazonicum (Rassi et a1., L975). 2.2 Distribution and biology of vector species The general aspects of the biology of American blackflies vrere recently reviewed by Jaurnback et al. (1971). Very detailed and inEensive studies on the main vector species were carried out in Guatemala from 1947 to 1953 by Dalmat (1955). The mosE important aspecEs will be briefly reviewed here. 2.2.1 Simulium ochraceum has been recorded from Bolivia , Colombia, Ecuador, Guatemala, Jamaica, I'lexico and Panama (Vulcano, L957). It shows a preference for rugged mountainous terrain, and was collected most coflmonly at altitudes between 9OO and I5OO m. Breeding sites are very small streams usually concealed by a thick overgrow of vegeEation and dense canopy. In Guatemala and Mexico, these habitats are typically found in the coffee-growing areas along the slopes of the vol-canoes. At the breeding sites, the streams show an optimum width of 0.3 to 1.5 m, and an optimum depch of 2.5 to 12.7 cm. The duration of Ehe pre-imaginal development, which is a key factor for the performance of any larviciding measures, was determined by Dalmat (1955): eggs hatch within three to 10 days, development of larvae takes seven to 15 days, the duration of the pupal stage is four t,o six days. Different figures r^rere report.ed by Vargas (L962): egg five days, larvae 23-44 days, pupa five days. oNcHo/wP/ 75. 10 Page 3 S. ochraceum is considered to be extremely anthropophilic. In the Presence of horses, mules, cows and other animals it showed a strong Preference for man (Giaquinto, L937; Dalmat, 1955). The female S. ochracer-m usually bites the upper parts of the human body. The species is generally exophagic but, at high densities, may even enter houses or bite at night-time. Adult flies can be caught throughout the year, buE bit.ing densities are highest around the middle of the dry season (Dalmat, 1955; Vargas, L962). Longevity and flight range were investigated by means of capture, marking, release and recapture experiments (Dalnat , 1952; Dalmat & Gibson, L952). The observed maximum flight range was 10.1 km. One female was recaptured 62 days after release. Average Parous rates determined by Garrns (1975) were t+O%. This gives evidence Ehat this vector can live for a long time and may travel considerable distances, even in mountainous or forested areas. 2,2.2 Simulitrm metallicum has been recorded from Belize, Colombia, Cost.a Ri-ca, Ecuador, Guatemala, Mexico, Trinidad and Venezuela (Vulcano, 1957). This species is much less fastiduous in its larval habitat requirements than S. ochraceum , and is more adaptable to different types of breeding sites. In Guatemala and Mexico i-t. was found in small, meditm and large streams (Dalmat, 1955). Imnature stages were collected from streElms from 2.5 cm to more than 5 m wide (optimum 0.3 to 2.4 n) and a depth from 2.5 cm to more Ehan 1 m (optimurn less than 3O cm). In Venezuela, breeding-areas were strictly limited to parts of smal1 streams (Lewis & Ibafrez de Aldecoa, L962). Shade and vegetation was not a requirement for breeding sites, which were either open to sun or well shaded by trees and shrubs. According to Dalmat (f955) the first stage larvae hatched from three to 2O days, the larval development took six to 20 days, and the pupal stage lasted four to 10 days. Elishewitz (L952) reported four to five days for the egg stage, 26 to 30 days for the larvae and four to seven days for the pupal stage. s metallicum is much more zoophilic than s ochraceum although it might attack hurnans in large numbers (Giaquinto, L937; Dalmat, 1955). When biting man it usually prefers to feed on the lower parts of the body, which is in contrast to the biting behaviour of S. ochraceum. S. netallicum is a very nervous feeder, which is easi ly disturbed, and flys around a long time before settling which may indicate thaE humans are not the preferred hosts. In Venezuela a contrasting picture was observed. Females were much more attracted to man than to animals (Lewis & Ibaf,ez de Aldecoa, 1962). By means of capture, marking, release and recapture experiments (Dalmat, 1952; Dalmat & Gibson, 1952) a flight range up to 1l km was determined. One female was caught 85 days after release. Parous rates were 46% for flies caught in Venezuela (Lewis & Ibaflez de Aldecoa, L962), ar.d. 23% for flies caught in Guatemala(Garms, I975). 2.2.3 Simulirmr callidum is recorded from Belize , Colombia, Guatemala, Mexi.co (Vulcano, 1957) and Costa Rica (Travis et al., L974). Breeding sites are similar to those of S. metallicun but the iunature stages are seldom found in large numbers. The species is usually found in areas which are not very heavily wooded, and in streams which are only lightly shaded, if at all. S. callidum was taken at altiEudes from 3OO to 1800 m , exceptionally up to 2500 m. Width of breeding sites ranged from 2.5 cm to more than 5 m (optimum 0.3-4.5 m), depth fro'm less than 2.5 cm to more than 1 m, optimurn 2.5 to 30 cm (Dalmat, 1955). Duration of the aquatic stages, as determined by Dalmat (1955) were: egg three to eight days, larvae eight to 25 days, pupae three to six days. A maximum flight range of 11.8 km was observed, and females can survive at least 20 days in nature (Dalmat & Gibson, 1952; Dalmat, L952). Average parous rates deter:urined by Garms (1975) were 39%. Like S. metallicr.rm this sPecres 1s also definitely zoophilic. Man is never aEtacked in large numbers. 2.2.4 Simulir-un gonzalezi and S. haematopotrmr: S. gonzalezi has been recorded from Mexico and Guatemala, S. haematopottm from Mexico, Costa Rica, Guatemala and Panama (Travis et al.. L974). Both species show a definite preference for streams over 5 m wide. The breeding sites are found in the lower regions of the volcanic slopes, where the streams are morphologi- cally oIder. Female flies may attack man in good nunbers, but are definitely more zoophilic(Dalmat, 1955). oNcHo/I.IP/ 75. 10 Page 4 2.2.5 Simuliur exigur:m. Records are from Venezuela, Colombia, Bolivia (Vulcano, 1957), Ecuador (Leon & Wygodzinsky, 1953). This species $ras believed to occur also in Guatemala and I'lexico, but Vargas & Diaz (1953) identified it as another species, which they named S. gonzalezi. In Venezuela irurature stag,es of S. exiguun are more cormron in large streams than in small ones. When comparing the attractiveness of this species to different hosts it appears that both man and mules are bitten in considerable nrmbers. Flies feed indifferently at the upper and lower parts of the human body (Lewis & Ibafrez de Aldecoa, L962). In Colombia, S. exi-gurm is considered to be mainly zoophilic, but in absence of animals it bites man, thus becoming a vector of onchocerciasis (Corredor, L974). In Venezuela parous rates were much higher (7g%) ttran those of S. metallicum (46%) (Leutis & Ibaiez de Aldecoa, L962). 2.3 Discrimination of vectors and vector-parasite relationships Ihe evaluation of the relative efficiency of the Middle and South American blackfly species as vecEors of O. volvulus has been based primarily on epidemiological evidence, rather than on direcE studies of the transmission potenti-als. S. ochraceLrm was considered to be the mosE important vecEor, since only in this species the area of distribution showed a certain correspondence with that of the endemic zones; since i-t exhibits a significanE anthropophilic behaviour, and bites humans mainly on the upper parts of fhe body where the chance of picking up microfilariae is greatest (Elishewitz, t953; Dalmat, 1955; Vargas, L962). 2.3.L Natural infection rates Most studies making a direct determination of the vectorial importance of the different species by dissection of wild caught females remained i-nconclusive. Almost al1 studies were carried out in Guatemala. Gibson (1951) and Dalmat (1955) who reported dissections of about 20 OOO flies, detecEed filarial infections La O.43% of 8654 S. ochraceum , Ln O.49% of 94L2 S. metallicum, and in 0.087. of L229 S. callidrm. Conclusions on the vectorial capacities of these species cannot be drawn from these figures, since information on the stages of filaria observed, and on the 0 volvulus infect,ion rates of the hr:man population was not given. De Leon (1963) reported dissections of 2254 S. ochraceun , 2637 S. metall-icrrn 434 S. ca11id,"Ir, and 2IO S. gonzalezi. A11 species harboured filarial infections sausage stage larvae in 0.8, O.6, O.46, L.4T.respectivelyandthe infective stage larvae in0.71,0. 19, O.O, O.O% respectively). Also in these studies infectivity rates remained undetermined because the infective stage of the O. volvulus larvae were not dis tinguished from a nematode cournonly developing in the Malpighian tubules of Guatemal-an bIackfly. However, the scarcity of mature infections in the species concerned is indicated by the observation that De Leon i-n about 50 OOO dissected female flies, never saw infecti.ve larvae in the head parts of the flies. Garms (1975) recorded infection rates in 1.5% in S. ochraceum (out of 3513 females dissected), O.Zg% in S. merallicr:m (32L2 females), O.2l% in S. caLlidun (468 females) and 1.37" in S. gonzalezi were only found (113 females). Infective larvae indistingui shable from those of O. volvulus in S. ochraceum (three flies). A single fIy had infective larvae in the head. Only in S. ochraceum wa s there a correlation between the infection rates in the human and in In the endemic zone, uP t.o L5% of the Parous flies were infecEed,the f1y populations. whereas none were infected in the non-endemic area. This supports the assumption that S. ochracetrm is the main, or possibly the only vector of importance in Guatemala. Much higher infection rates were reported by NeLtel (f960) from the Chiapas focus in Mexico S ochraceum L3-L4%, s metallictm 7-2O%, S. call:!4um 2-5%). But it is not clear whether this referred only to sausage stages or rather to micro filariae in Ehe stomach of the flies. Only a few data r^rere reported from foci in other countries. In Venezuela (San-Antonio/ Guanaguana area) Lewis & Iba?(ez de Aldecoa (L962) dissected 585 S. exiguum, of which 0.2% conEained sausage stage larvae, and 433 S. metallicum 2.5% of them were harbouring sausage, and 1.6% vermiform stage larvae. Peffalver (cited by Convit, 1974) found sausage stage larvae in 8% of S. metallicr.m females. In BraziL, i-nfections so far Iilere recorded on1-y from S. amazonicum. Out of 972 females O.72% were found to be lnfected with sausage stage larvae, which were believed to be of 0 vol-vulus (Rassi et a1. , L975). oNcno/lrP/75.10 Page 5 The evaluation of all these results is complicated by the fact that blackflies are not only vectors of O. volvulus , but also may be carriers of animal filariae, whose developmental stages cannot be accurately distinguished from those of 0. volvulus. Especially Onchocerca spp. of caEtle, which are frequently bitten by the suspected vectors, are coflmon in most of the endemic areas (Gibson, 1965). Onchocerca-like worms were also recovered from a spider monkey in the northern Chiapas focus (Caballero et al., 1958). The presence of non-hunan filariae in anthropophilic blackflies was confirmed by observations made by Gibson & Dalmat (1952) who found that S. gonzalezi and S. haematopotrm were infected in areas where human onchocerciasis was absent. The infections were believed to be of bovine origin. Garms (1975) described infective larvae of an unknown filariae from S. metallicum , probably of ani-mal origin. But this species was neither an Onchocerca species of cattle, nor any of those species which were previously described from blackflies , L956; Nelson & Pester, 1962; Duke, 1967; Voelker & Garms, L972). Sausage stage larvae infections were also found in S. metallictrm outside the endemic area. 2.3.2 Experimental st.udies Experimental investigations into vector-parasite relationships are difficult, because it is not, yet possible to colonize Middle American blackflies. Newly hatched flies obtained from pupae refused to bite man, or could be maintained for a few days only (Gibson, 1965). Itost experi-ments were therefore carried ouE with wild-caught female flies which were fed on microfilarial-carriers. Stil1 these seldom survived more than one week in captivity. Gibson(1965) had to infect about 15 OO0 flies to get a few advanced stages of O. volvulus but succeeded to show the full development of O. volvulus in S. ochraceum S. metallicum and S. ca1lidum. At a temperature of 20"C the development was completed after L2 days. It was observed that S. callidum shows a greater mortality rate during the first days after infection with O. volvulus than do S. metallicum or S. ochraceurn IIe suggested that the former species is not as efficient a vector as the latter two. In experiments carried out by De Leon & Duke (1966) the development of O. volvulus was completed in all three species after seven to eight days at a temperature of 22o-27"C. s ochraceum showed the highest ingestion of microfilariae and several hundreds could be counted in one fly. In comparison with the other two species it showed the greatest ability to survi.ve such high microfilaria intakes. Considering that, S. ochraceum is markedly anthro- pophilic; reaches its highest densities in areas, where there is the greatest, amount of onchocerciasis; is very aggressive in biting, often attacks in enormous numbers; is biting at the uPPer parts of the body where microfilariae are most abundant, and has been found naturally infected with infective larvae of O. volvulus type, they concluded that S. ochraceum is the most important vector of onchocerciasis in Guatemala. IE was noted, in S. ochr'aceum , that after high int.akes of microfilariae a large number of Ehem was eli.minated during the first 48 hours at, the microfilarial stage. This was shown to be due to the well-developed cibarial armature of the buccopharyngeal apparatus of the fly, where microfilariae, en route to the stomach, are frequently severely damaged (Bain et al. , L974i Omar & Garms, L975). Such an armature is absent in S. metallictm and S. calIidum. Conse- quently a much higher proportion of ingested microfilariae may invade the thorax, causing relatively higher mortality rates among these flies after infection. S. metalli cum could only survive the ingestion of about a thirtieth of the nr:rnbers of microfilariae tolerated by S. ochraceum (De Leon & Duke , L966). 2.4 Erantitative aspects and dynamics of transmission The results of transmission experiments carried out in the laboratory, and the determina- tion of natural infection rates re do not allow to draw any conclusion concerning the vectorial capaeity and relative importance of the different species. The transmission poten- tial of each species expressed as the estimated number of 0. volvulus larvae delivered t.o man in a given period of time by each vector species, can be deter:urined only in long-term studies under various levels of onchocerciasi-s endemicity, and at different seasons. No reliable information is yet available. In Guatemala, i-nvestigations were complicated by the surprisingly low infectivity rates of the f1y populations (Dalmat, 1955; De Leon, 1963; Garms, 1975). oNcHo/wP/75.10 Page 6 This is in contrast to the situation in West Africa, where in hyperendemic areas, up to 5% of the S. damnostrm females may harbour infective larvae of 0. volvulus (Onchocerciasis Cont.rol Progranrne, 1973) The reasons for the low infectivity raEes are not at all clear. A short life span of the flies is probably not the limiting factor, since DaImaE & Gibson (1952) showed by means of capture, marking, release and recapture exP eriments that S. ochraceunr may survive up to 62 days ,andS metallicum even up to 85 days. Garms (1975) determined moderate or high parous rates, although infection wiEh O. volvulus may have a delecerious effect uPon the flies (Dalmat & Gibson, irf52). It seems po"ribl. th"t the transmission potential may be influenced by the low mean temperatures prevailing in large parts of the endemic area, which are close to the critical temperature of 18'C for the developmen t of O. volvulus as deEermined in experiments with S. woodi in East Africa (Wegesa, 1966). Low infectivity rates of the vector may explain the extraordinary situation in Guatemala, where onchocerciasis foci remained smal1 and limited, and have been stable for the last 4O years, despite large scale movements of the human population (seasonal workers in the coffee plantations), and the fact that the presume d vector, S. ochraceum, occurs also outside the endemic zones. Ihis indicates that only in areas with very high fly densities, which are said to occur only in the onchocerciasis areas, the disease may be self-perpetuating. It has been suggested (Hamot, 1974) that the actual reproducEive rate of the disease along the limits of the existing foci must be very close to one. Ihis situation, which may also apply Eo other foci in Latin America, is favourable for the successful implementation of control measures. Data on the amount of transmission effected by the different vectors are indispensable for the proper planning and evaluation of control operations. This transmission potential should be established in different areas, in order to determine the critical transmission level below which parasite transmission would be interrupted. Since individual dissection of the large ntrmbers of flies that are necessary for the estimaEion of reliable figures, would be extremely time consuming and tedious, concentration methods like those used in filariasis vectors(Mul1er & Denham, 1974) should be exploited for their potential usefulness in onchocerciasis research. These studies would also require the establishment of diagnostic characters or techniques to distinguish the developmenEal slages of O. volvulus from those of 0. gutturosa as well as other filariae carried by Simulium species of the Western Ilemisphere. 3. VECTORS IN THE FORXST ZONE OF WEST AFRICA In the forest zone of West Africa species of the Simulium darnnosum complex are considered tobetheon1yvectorsof@.Afewotherspeciesoccasiona11ybiteman. These are of no epidemiological importance, although S. dukei can support the complete develop- ment of the parasite (Duke, 1962; Disney, l97la). Also S. ovazzae which is widely distributed in the forest zone of West Africa (Disney, 1971b; Garms, L972) may prove to be a suitable intermediate host. Simulium damnosum, previously regarded as a homogeneous species turned out to be a complex of cytologically different forms (Dunbar, 1966, L969). Recently, the WesE African examples were separated into eight species (Vajime & Dunbar, 1975), and at least one more species exists in the forest zone of Cameroon (Va3ime, personal comnunication, 1974). Several of these species have a well-defined geographical distribution, and the diversity in breeding habits and bionomics observed in Ehe S. damnosum complex apparently reflects the different ecological requirements of the species. Moreover, differences concerning the transmission pattern of the disease may be associated with these cyt,ological entities. 3.1 Distribution of Simulium darnnosum complex in the forest zone A rnap on the gene ral distribution of S. damnosum sensu lato was compiled by Philippon et al. (1969), who also listed the relevant publications. The map shows that S. damnosum is present everywhere in the forest zone. More recently, Garms (Lg73a) "t,rdi.ffiffiibu-tion of S. damnosum in Liberia. The complex was found throughout the country, but breeding sites appeared to be more cortrnon in regions, where the original tropical rain forest had been destroyed and was replaced by farmland, rubber plantations, low bush or savanna-Iike vegetation. oNcrro/wP/75.10 page 7 Records on the distribution of the sibling species of the S. damrosum complex were published by Garms (L973a) and Garms & Vajime (1975) for Liberia and Guinea, by Qul116vere (L974) for lvory Coast, Mali, Ghana and Upper Volta, and for the whole of West Africa with the original description of the species of the complex (Va5ime & Dunbar, L975). Six species of the S. damnosum complex were discovered in the forest zone of WesE Africa. 3.1.1 Simulium squamosum Enderlein (= S. darnnosumItBillerr form, Vajime, 1973) has been recorded from hi1ly areas of the forest zone of Cameroon (Disney, 1970; Vajime & Dunbar, 1975 ). It is known also from the Guinea savanna of Cameroon and from Upper Volta (VaSime & Dunbar, 1975). 3.1.2 Simuliun yahense Va,jime & Dunbar (= S. damnosum trYahtt form, Vajime, 1973) is apparently restricted to the western parts of West Africa. It was recorded from Liberia and Guinea(Garms, L973a; Garms & Vajime, 1975) and from Ivory Coast, (Qui116v6r6, L974). It is widely distributed throughout the forest zones of these countries, but in Guinea its distribution extends much farther to the north (11'.50'N) into the Fout.a Djallon mountains (Garms, L973a) These findings may represenE relics of a former much wider distribution, since the forest originally covering this highland mass had been eliminated during the last century and a half(Church, i968). S. yahense has not established itself in the savanna zones of Guinea which suggests that its distribution is restricted to areas where smaller waEercourses flow perennia I 1y. 3. 1.3 Simulir-un sanctipauli vaj ime & Dunbar (= S. damnosuo rrBandamart form, Vajirne,1973) found in Liberia (Garms,appears to be restricted to the forest zone of West Africa. It was L973a) and Ivory Coasr (Qui116v6r6, L974). 3.L.4 Simulium soubrense vaj ime & Dunbar (= S. damnosum rrsoubrert form, Vajime, 1973) has been recorded from Liberia, Guinea (Garms, L973a; Gar.ms & Vajime, L975), Ivory Coast (qui116v6r6, L974) arrd Dahomey (Vaiime & Dunbar, L975). Its distribution extends from the forest to the Gui.nea savanna. 3.1.5 Simulium daurnosm Theobald s.s. (= S. damrostm rrNiletr form , Vajime, 1973) is the most wide-spread species of the complex, and the only one found across the continent (Vajime & Dunbar, L975). In l,lest Africa it was found in Liberia, Guinea (Garms & Vajime, 1975), Ivory Coast, Ghana, Mali, Upper Volta (quil16v6re, L974), Nigeria (Va3ime & Dunbar, 1975) and Cameroon (Disney, 1970). 3.1.6 An additional species, which has not yet been described, was found in the forest zone of Casreroon (Vajime, 1974, personal conmunication). 3.1.7 Ihree species, notably S. sudanense , S. sirbanrsr and S. dieguergnse, are aPParently confined to the savannas of West Africa. Ihey are not recorded from the forest zone. 3.2 Bionomics and ecology of Elqltr-rm j@gs.!g complex Ihe biology and ecology of S. darrrosum s.1. have been recentl y reviewed (Onchocerciasis Control Programte, 1973) in extenso in Annex III-1 of the report rr0nchocerciasis Control in the Volta River Basinrr p."p.tEl-6frf,Epreparatory assistance mission of the onchocerciasis controlproject in the Volta River Basin. Therefore, only the most important infor-mation pertinent to the transmission and epidemiology of onchocerciasis in the forest zone shall be discussed here. 3.2.1 Breeding places In the watercourses shaded, and S damnosr-rm forest zone, irmrature stages of s damnosum s.1. inhabit a wide range of types of . Larvae and pupae can be found in the smallest streams, that may even be heavilyin Large rivers as well. This contrasts the situation in savanna areas, where is usually much more adapted to larger watercourses. Evidently this wide spectrunxdifferent ecological requirements of the siblings.reflects the oNcrro/I.rPl 75. to Page 8 Information on t,he breeding habits of the vari-ous species of the complex were given by Vajime & Dunbar (f975) and Ganns & Vajime (f975). The breeding habits of one of the complex, S. yahense , are distinct.ly different from Ehose of the others. This species inhabits small watercourses, sometimes under conditions similar to those described for s ochraceum , the most important vector of onchocerciasis in Middle America. S. yahense hras not found in la rge rivers, and usually was not associated with the other species of the complex. Although occurring sym.patrically in the same regions, its breeding places are clearly separated from those of the other species of the S. damrosulr complex The breeding habits of S. sanctipauli are in contrast to those of S. yahense. S. sanctipauli primarily inhabits very 1arge rivers, and is never found in small streams. S. squamosum, s soubrense and S damrosrm s. s. are also river-breeding species. The distri- bution of the last mentioned species extends to the savanna region, it can breed in channels of irrigation systems. where like S. sirbanum Suitable supports are a prerequisite for the development of the ir@ature stages of all species. llost of them show a preference for plant supports (dead leates, aquatic vegetation, imersed bushes, trees, grasses). Usually they do not settle directly on the rocks. S. soubrense was observed to behave differentl y, since large masses of larvae and pupae were found on the rocks of big waterfalls in the Cestos River in Liberia (Garms, L973a). In contrast to the sit,uation in the savanna areas artificial breeding places (irrigation plants, dams, bridges, fish fences) are of no significant importance in the forest zone. Ilowever, artificial changes of the whole environment by the elimination of the original high forest may have an important influence on the distribution pattern of the complex. In Liberia, breeding sites of S. damnostrm s.1. appeared to be significantly more cormon in areas where the rain-forest had been destroyed and replaced by farmland, plantations, Iow bush or savanna-like veget.ation. Therefore, the development of the country, being linked with an increase of the population, involves Ehe risk of spreading of the vector and intensification of the transmi-ssion. 3.2.2 Biology of adult flies Studies on bionomics of the adult flies are complicated, because identification of the sibling species has so far only been possible in the larval stage. Accordingly, conclusions can be drawn onty Eentatively by correlating observations on females caught close to breeding sites with rhe larva1 populations identified therein. 3.2.2.L lation cs and bitin dens iti-es : Biting densities of fIy populations are prinarily governed by the hydrobiological conditions and the productiviEy of the breeding sites, which may be subjected to considerable seasonal vari-ations. Three types of annual variations in the fly populations were listed by Le Berre (1966). (1) Synchronous tyPe of variation: Variations of fly populations are directly correlated to the water-levels, i.e. fly densities are highest in the rainy season, and lowest in the dry season. Q) Inverse type of variation: Breeding places are producing flies mainly during the dry season at low water 1eve1s. (3) Bimodal type of variation: Breeding places are producing flies at low and at high water-levels. The synchronous type of variation was said to be characteristic at large water-courses in forest areas. fhis was confirmed by our own observations made in Liberia (Garms, 1973b). Near large rivers biting densities were lowest in the dry season, i.ncreased with rising water levels at the beginning of the rainy season, and had their peak at the height of the rains. The low productivity of breeding sites at low water levels is presumably due Eo a lack of holding siEes or supports for the larvae, raEher than to other ecological conditions such as shortage of food. This is indicated by our observation that shortly after suPPorts such as palm-branches or bushes had been artificially fixed in the rapids they became densely covered with larvae of the S. damnosum complex. Larvae did noE settle on the rocks themselves. As water leveIs i-ncrease larvae find suitable supports on grasses and other plants, which have grown between oNcHo/wP/75.10 Page 9 the rocks or on sandy islands during the dry season, and on submerged bushes and trees. The drastic increase of blackfly populations at the onset of the rains may be partly due to the extensive supply of food provided by masses of organic matter washed inEo the rivers. This synchronous type of variation is primarily associated with the breeding of S. sanctipauli. A quite different type of variation was observed in areas, where S. yahense breeds in small streams. It can be considered as a fourth type of annual variation. Fluctuations are much Iesspronouncedthan with the other types, and biting densities may be more or less constant throughout the year. This is due to the fact that, in conErast to the situation in the savannas, small streams in forest areas may flow throughout the year. Larvae of S. yahense find their support. on masses of floating vegetation, that do not exist in big rivers. During the rainy season the water-Ievels in these streams may rise considerably after heavy rainfalls, but generally return to normal shortly afterwards. Unlike the situation in the savanna, where similar habitat,s usually are densely occupied by S. hargreavesi , which possibly is more competitive than S damnosum in the forest S. yahense is the only species developing mass populations under these conditions. 3.2.2.2 Dispersal and movements of female flies: It is well known that S. damnosufl can travel over long distances up to 150 km (Onchocerciasis Control Programne, 1973 ). For the forest this has been confirmed by means of capture, marking, release and recapture experiments (Ihompson, personal cormunication, 1974). The dispersal of the flies can be linear, along Lhe watercourses alone, or radial, i.e. in all directions from the breeding places. A linear dispersal is found particularly in the savanna regions during the dry season. Flies stick close to the T^ratercourses, because outside the gallery forests there is insufficient dense plant cover and the humidity is extremely low. With the first rains, weeks before tributary streams are in flow, radial dispersal to areas far away from the rivers becomes possible. In the forest zone, a radial dispersal is possible throughout the year, though it greatest in the rainy season. In Liberia, at distances of more than 10 kn from river flies or more could be caught per man per day during the rainy season. At the end of rains they abrupEly disappeared from most of the area, and they were then concentrated river (Garms, 1973b). is 500 the at the Duke (1975) found that, in the forest of Cameroon, parous and infective flies were proportionally more abundant inland than on the river bank. Ihis contrasted with the situa- tion in the savannas where nulliparous flies dispersed mainly inland away from their riverine breeding sites. 3.2.2.3 Daily biting rhythm: FLies may bite from dawn to dusk. According to our own observations in Liberia (Gar:ns, L973b) daily feeding cycles showed two peaks, one in the morning and one in the afternoon, the latter being the more pronounced. During the dry season both peaks are separated by several hours of low biting activity. I{ith the onset of the rainy season the second peak begins earlier, and at the height of the rainy season biting extends over the whole day. Temperatures seem to play the preponderant part among the factors influencing the biting rhythm (Le Berre, L966). llhereas in the savannas parous females bite in larger numbers in the morning and at midday (Onchocerciasis Control Progrannre, 1973), differences lilere less pronounced in the forest zone of Liberia (Garms , L973a). 3.2.2.4 Zoophily: Females of the S. darnnosum complex are found feeding on man everyvhere in the forest zone of West Africa. However, anthropophily is facultative; in presence of animals, and in uninhabited areas they may exhibit a noticeable zoophilic behaviour, which significantly may reduce the probability of transmission. Zoophily has been confirmed in the forest zone by direct observat,ions of flies feeding on birds and other animals (Garms & Voelker, L969 Disney, 1972); by means of precipitin tests on wild-caught engorged flies (Disney & Boreham, tg69); by the occasional finding of remains of avi-an blood in females (Garms & Voelker, L969), and the presence of developing filariae other than O. volvulus in the flies(Duke, 1967; Garms d Voelker, L969). In Liberia, in areas along the large rivers, where S. sanctipauli- was breeding, up to more than 5O% of the infective flies were harbouring infec- tive larvae of non-human origin oNcHo/wP/75.10 Page 10 3.2.2.5 Longevity: Longevity of fly populations i-s one of the key parameters Soverning the transmission of O. volvulus. It can be determined directly by studying the regression of fly populations after treatment and elimination of breeding sites, or by capture, marking, release and recapture experiments. I"lore usually it is estimated indirecEly by establishing survival probabilities from age composition of f1y populations, as exPressed by the parous rates. Parous rates pry may be used as a parameter when longevities of f1y populations from different areas or at different seasons are compared. For epidemiological evaluations and the determination of the amount of transmission it is necessary to have an estimaEe of the proportion of flies within a population thaE are potentially infective. It is generally agreed that flies coming to the Ehird or subsequent blood meal have reached Ehis 'repidemiologically dangerous agerr. Considering that the time interval between two blood meals is about three to five days (Thompson, L974), flies will be eight to IO days old by the Eime of the third meal. Life expectaEion of forest flies was found to be significantly shorter than Ehat of flies from Ehe savannas. It was calculated (Le Berre et al. , L964; Le Berre, 1966) that in the forest of the Ivory Coast only seven out of 1OO0 newly emerged flies will survive to the dangerous age, against 22O in the Guinea savanna, and 350 in the Sudan savanna. Annual parous rates determined by Garms (1973b) in an area of uhe evergreen rain-forest in Liberia coincide sharply with those recorded by Le Berre (1966) from the Ivory Coast (LL%). In Liberia, parous rates showed a well-defined seasonal cycle, in that almost all flies were nulliparous at the peak of the rains, while in the dry season parous rates increased Eo more than 30%. The finding of such extremely low parous rat.es cannot be used to generalize for the whole forest zone. Duke (1968), in a forest envi.ronment in Cameroon reported annual parous rates of 387., and in Liberia (Gar:nrs, unpublished) varying parous rates were found in ecologically different areas. At the majority of the cat.ching sites intermediate parous rates of L6 Eo 20% were determined, but annual parous raEes were above 30% and seasonally reached 60% at a catching site located at the upper course of the St. Paul River. This relatively high parous rate in one of the driest parts of Liberia is similar to that of the long-living S. damnosurn populations found in the savannas of West Africa (Le Berre, 1956). 3.3 Dynamics of transmission 3.3.1 Types of transmission By means of transmission experiments it was shown that different Onchocerca-Simulium complexes occur in llest Africa (Duke et at., L966; Lewis & Duke, L966). Two main strains of O. volvulus were distinguished, a forest strain extending over the foresE zone and the greater part of the Guinea savanna, and a Sudan savanna strain confined to the Sudan savanna and Ehe extreme north of the Guinea savanna. Both strains show good development only in S. dannosrm present in their corresponding bioclimatic zones, and little or no development in flies from the zones where the other strain is found. Furthermore, factors governing transmission in forest and savanna are clearly different in several aspects, which in turn has a significant influence on the epidemiology of the disease. (1) Distribution of breeding sites: Breeding places in the savanna are largely confined to the rivers. In the forest, all sma1l streams are potential breeding sites of S. yahense. (2) Dispersal of female flies: Radial dispersal is possible at all seasons in the forest, though reduced in Ehe dry season. Linear dispersal occurs in the savannas, radial dispersal is only possible during the rainy season. Dispersal pattern of parous and nulliparous females differ in forest and savanna (Duke, L975). (3) LongeviEy: Life expectation of f1y populations is much shorter in the forest zones than in the savannas (Le Berre, 1966; Mil1s, L969). (4) Intrinsic factorsl Usually infective forest flies carry significantly more infective larvae than flies from the savannas. On an average the number of infective larvae per infec- tive fly is about two in the savanna, and more than five in the forest (OCP 1973). More than 6O infective stage larvae of O. volvulus were observed in a single fly in Liberia (Garms , L973) oNcHo/wP/ 75 . 10 page 11 3.3.2 Natural infection rates Since only parous flies can be infected, natural infection rates depend largely on the age composition of the vector population. Usually infection rates are recorded in relation to parous raEes. Furthermore, infection rates are directly linked to infection rates in the huoan population and to the intensity of man-fIy contact (degree of anthropophily). It cannot be excLuded that flies from different regions, or the different specles of the S. darrnosr:m complex may show a different suceptibility or tolerance towards the infection with O. volvulus. Infection rates of fly populations are usually much lower than those of the hr.rman popula- tions. At a hyperendemic village in the forest zone of Cameroon the infection raEe of the fly population was 13.5% only (Duke, 1968). In Liberia (Garms, L974) no direct correlation at. all existed beEween infection rates in fly and in human populations. In hyperendemic areas where 68 to 78% of the population were carriers of microfilariae, infection rates of the parous flies could vary from a high-level of 46% to a very low leveI of LO%. Generally, infection rates were highest in densely populated areas where a close contact between man and flies can be assumed, whereas in forested areas 1ow infection rates were observed. When evaluating infection rates among fly populations it must be borne in mind thaE thoracic infections of O. volvulus cannot yet be distinguished with certainty from those of other filariae. 3.3. 3 Transmission potential In order to conpare Ehe intensity of transmission of 0. volvulus in differenE areas Ehe number of infective larvae carried by s damrostm coming to bite man within a given period of time is a suitable parameter, usually defined as the transmission potential (Duke, 1968). When evaluating the data it must be considered that in nature only some of the third stage larvae are actuaLly infective (Bain et al., 1969), and that not all of them leave the vector during the blood meal and enter the host (Duke, 1973). Furthermore, the esEimaEed transmi.ssion potential does not reflect the acLual risk for the local population, since no person is fully exposed 12 hours a day throughout the year as this index demands. Only flies reaching the dangerous age can be potentially infective. Therefore the transmission potential is largely influenced by the longevity of fly populations. This was demonstrated by Mills (L969), who calculated, taking into account the different longevity of fly populations in different bioclimatic zones, that these populations could transmi.t L4 L84 infective O. volvulus larvae per man per year in the Sudan savanna, 7432 in Ehe Guinea savanna, and only 266 in the forest. However, direct determinations of the transmission potential by means of dissection of wild-caught flies, showed clearly that even in forest areas the amount of transmission may be very high. In four villages in Cameroon, where 3L%, 64%, 77% aod, 7L% of the people were carriers of microfilariae Duke et a1. (1972) calculated annual transmission potentials of 897 ' 2806, LO 42L and 87 846 larvae respectively. They concluded that, under foresg conditions, annual transmission potentials of 3O0O or above appeared to be corErensurate with a high prevalence of onchocerciasis and with the occurrence of skin and eye lesions. Similar studies were conducted inecologically different areas (coastal savanna, rubberplantations, evergreen high forest, semideciduous forest) of Liberla (Garms, 1973b, L974). A forest type of transmission was encountered everywhere in the country. But the transmissionpotential varied considerably in different regions. Figures ranging from 15 to lO OOO infective O. volvulus larvae Eheoretically transmitted per man per year were calculated, and a ,,,rltiplicifr?ffirent transmission patterns was observed. rt \ilas obvious that there was no direct correlation between fly densities and t,ransmission potentials, and between infection rates in fly and human populations. The vector population of any area showed special features concerning population dynamics, age composition, infection rates r{ith O. volvulus and otherfilariae, and species of the S. damrostrm complex. a oNcHo/wP/7s.10 Page 12 Since females of the S. dannosun complex cannot yet be identified in the adult stage, no direct investigations into the vectorial importance of the different species were carried out. I{hen the distribution of the various siblings is compared with the areas in which onchocerciasis is endeoic, participaEion of all species in the transmission of O. volvulus is suggested. Considering that the observed differences in larval bionomics wilI not be restricted only to the iunature forms, but may be found in aduLt fly populations as well, it appears to be almost certain that vectorial capacities will consequently be different. In Liberia this was indicated by the observati.on, that high rates of infections with fllariae other Ehan o volvulus were only found i.n areas where S. sanctipauli was breeding. 4. SI]MMARY The present review deals with the bionomics, ecology and vectorial characteristics of the onchocerciasis vectors of the Western llemisphere and the forest zone of West Africa. Results of our own studies carried out in Guatemala and Liberia were discussed. Particular emphasis is placed upon the factors primarily related to the epidemiology and transmission of onchocerciasis, i-ncluding distribution of the species, breeding places, population dynamics, biting densities, dispersal of females, longevity, host preference, natural infection rates and dynaroics of transmission. In the WesEern llemisphere a large nr-mber of man-biting species has to be considered as potential vecEors. Detailed information on their bionomics is only available from Guatemala and Mexico, where S. ochracer:m is incriminated as Ehe most important vector. However, littIe attempt has been made towards a quantitative assessment of the relative importance of the various species. Investigations should therefore be directed towards a better understanding of the aspects of transmission dynamics which is a prerequisite for the planning, implementation and evaluation of control operations. Studies are complicated by the presence of filaria other than O. volvulus in the flies. Methods for differential identification of filariae encounEered in the vectors have to be developed. In the forest zone of l{est Africa only species of the S. damnosuo compl-ex are involved in transmission. There is a complete knowledge on the bionomics and transmission characteristics of the complex as a whole. Still, little progress has been made Eowards a differential study of the sibling species, because of the complicated nature of the techniques required and the fact that identification of adult flies is not. yet possible. In order to study the epidemio- logical importance of the sibling species, methods for separation of the adult flies based on their external characters have to be introduced. ACKNO}ILEDGEI,IENT I would like to express my thanks to Dr. J. Ilamon, World Health Organization, who kindly provided me with valuable information and literature that were helpful in the preparation of this review. 0NcH0 /I,I P/ 75 . I 0 Page 13 REFERENCES Anderson, R. C. (1956) The life cycle and seasonal transmission of Ornithofilaria fallisensis Anderson, a parasite of domestic and wild ducks, Can. J. Zoo1., 34, 485-525 Bain, O., Durette-Desset, M.-C. & De L6on, J. R. des microfilaires pa r Simulium ochracer:m et Ann. ParasiE. 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(1968) A review of past and present aspects of Simulium control in Mexico together with recornrnendations for the future conduct of control schemes and an outLine of an eradicaEion scheme in the north focus of onchocerciasis in Chiapas Stat.e, Unpublished report to PAIIO, 52 pp. De L6on, J. R. (L957) Simuliid vectors of onchocerciasis in Guatemala, L6, 523-529 BulI. Wld Hlth Org. De L6on, J. R. (1963) Entomologia y transmision, in: Enfermedad de Robles. Universidad de San Carlos de GuaEemala, Ed Univers itaria Guaterna la 43, L25-L82 De Ldon, J. R. & Duke, B. O. L. (1966) Experimental studies on the transmission of Guatemal-an and West African strains of Onchocerce lelvuluq by S. caltidum Trans. roy. Soc. trop. Med. Hyg., @, 735-752 Disney, R. H. L. (1970) A note on variati-on vrithin SimuLium damnosum in Ehe forest zone of West Cameroon, Ann. Erop. l'led. Parasit., 64, L29-L3O ( Sinulium ochraceum, S. metallictrm and oNcHo/wP/75.10 Page 14 Disney, R. H. L. 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