Biosystematic studies on the Simuliidae (Diptera) of the Amazonia onchocerciasis focus

121 Pages·1997·43.1 MB·

by  A J Shelley

Bull. nat. Hist. Mus. Lond. (Ent.)66(1): 1-121
Issued26June 1997
Biosystematic studies on the THE NATURAL
HISTORY MUSEUM
Simuliidae (Diptera) of the
Amazonia onchocerciasis focus
A.J. SHELLEY & C.A. LOWRY
Medicaland VeterinaryDivision*, DepartmentofEntomology, TheNaturalHistory
Museum, CromwellRoad, London, SW75BD, U.K.
M. MAIA-HERZOG &A.RA. LUNA DIAS
DepartamentodeEntomologia, Instituto Oswaldo Cruz, RiodeJaneiro, Brazil-
M.A.R MORAES *SjiW Sb ^ Vl
Departamentode Patologia, Instituto Evand.ro Chagas, Belem, Para, Brazil.
CONTENTS
Introduction 2
TheAmazoniaonchocerciasisfocus 2
Material and Methods 5
Acknowledgements 7
KeystothesimuliidspeciesoftheAmazoniaonchocerciasisfocus
ofBrazil 7
Speciesdescriptions:
Simulium(Hemicnetha)rubrithorax 9
Simulium(Notolepria)exiguum 12
Simulium(Psaroniocompsa)quadrifidum 15
Simulium(Psaroniocompsa)cauchense 17
Simulium(Psaroniocompsa)oyapockense 19
Simulium(Psaroniocompsa)roraimense 22
Simulium(Psaroniocompsa) incrustatum 24
Simulium(Psilopelmia)bipunctatum 28
Simulium(Psilopelmia) iracouboense 30
Simulium(Psilopelmia) lutzianum 34
Simulium(Psilopelmia)rorotaense 36
Simulium(Psilopelmia)suarezi 40
Simulium(Trichodagmia)guianense 40
Simuliumgoeldii 43
DistributionandBiology 45
Parasitological FindingsandEpidemiological Implications 49
References 52
Maps,colourplatesand figures 57
Tables 92
Appendix 1 -materialexamined 95
Appendix 2-datafromman-bitingcatchesanddissectionsforparity 116
Index 121
WorldHealthOrganizationCollaboratingCentreforthestudyofSimuliidaeandPhlebotominaeinrelationtoOnchocerciasisandLeishmaniasis.
©TheNaturalHistoryMuseum, 1997
A.J. SHELLEY,C.A.LOWRY,M.MAIA-HERZOG,A.P.A.LUNADIASANDM.A.P.MORAES
SYNOPSIS. A comprehensive revision of the systematics, distribution, biology and medical
importance ofthe fourteen simuliidspecies intheAmazoniaonchocerciasis focus is presented
withspecialemphasisonBrazil.Thesystematicssectionprovideskeystotheadults,pupaeand
larvae,fullmorphologicaldescriptions,taxonomicdiscussionsanddistributioninLatinAmerica;
sixnew synonyms andthree lectotypesarecreated.The relative importanceofthese species in
boththeBrazilianandVenezuelanpartsofthefocusaswellasinotherpartsofLatinAmericais
then discussedbyreviewingtheirdistribution in the focus, thebiology ofeach speciesand the
medical importance ofthe vector species. The paper provides a baseline for new biomedical
studiesbeinginitiatedin Brazilonvectorsimuliids.
INTRODUCTION ofthediseaseatMinacu,Goias,2500kmstothesouth
of the Amazonia focus prompted recommendations
forfurtherresearchintothediseaseinBrazil(Moraes,
Human onchocerciasis is a rural disease caused by a 1991; Shelley, 1991) and epidemiological and ento-
filarial nematode worm (Onchocerca volvulus) whose mological research have now recommenced in the
skin-inhabiting larvae (microfilariae) produce loss of Amazonia focus with a view to assessing control
elasticity,de-pigmentationanditchingoftheskin,loss strategies for the disease. Access to the Amazonia
ofvisualacuity,andinseverecasesblindness.Itaffects focus is now easier because of increased military
about 17 million people, mainly in Africa, but also in manoeuvres and the creation ofthe Yanomami Sani-
Latin America. Before 1965 onchocerciasis in Latin tary District by the Ministry of Health. During the
America was only known in Mexico, Guatemala and 1970s thepresence, atthe Serrados Surucucus, oftin
northern Venezuela, but during that decade new foci miners(manyfromMinacu)isthoughttoberesponsi-
were discovered in Colombia, Ecuador, Brazil and bleforthedisseminationofonchocerciasistothenew
southernVenezuela as development ofrural areas ac- Goias focus.An invasion duringthe lastdecadeofup
celerated (Shelley, 1988a). The disease was first to 40,000 tin and gold miners and their subsequent
recorded in Brazil in 1967 from a North American dispersal to locations throughout Brazil is likely to
missionarychildwhohadbeenlivingatamissionpost causethefutureappearanceofnewdiseasefociwhere
in theYanomami area in northern Brazil (Map 1), and potential vectors are present.
laterMoraes(Moraesetai, 1979)showedthepresence This paperpresents the original biosystematic data
ofadiscretefocusofthisdiseaseprincipallyinvolving collectedduringthe 1970sfromtheAmazoniafocusin
Yanomami IndiansinAmazonia.Thediseasewasthen Brazil, interpreted with the assistance ofmore recent
detected in the adjacent region ofVenezuela(Rassi et taxonomic findings from other parts of the country,
ai, 1977). The exact prevalence of onchocerciasis and correlates these to data from the Venezuelan part
couldnotbecalculatedatthetimebecausetheinacces- ofthe focus to produce the first comprehensive ento-
sibility of the area precluded the examination of mological overview fortheAmazoniaonchocerciasis
representative numbers ofIndians. The epidemiologi- focus as a whole. The paper thus provides a sound
cal and some entomological work carried out during basis and recommendations for the further entomo-
the 1970s in this area ofBrazil, its relevance to other logical studies anticipated inbothcountriesunderthe
fociinLatinAmericaandviewsonthefuturedispersal control programme for human onchocerciasis in the
and control ofhuman onchocerciasis have now been Americas currently being coordinated by the World
reviewed (Moraes, 1991; Moraes & Shelley, 1986; Health Organization.
Moraesetai,1979; Shelley, 1988a, 1991).
The majorobjectives ofentomological work in the
Brazilian part of the focus were to investigate the THEAMAZONIA ONCHOCERCIASIS
simuliids present in this hithertounprospectedregion FOCUS
and to determine the vector species of O. volvulus.
Later, studies on vector species were made in areas
circumjacent tothe focus in orderto assess the feasi- The Amazonia onchocerciasis focus straddling the
bility of onchocerciasis dispersing to these areas border between Brazil and Venezuela is the most re-
through infected individuals passing from the focus moteofthefociofLatinAmerica(Map 1).Itconsistsof
along the Northern Perimeter road to farming areas isolatedcommunitiesofinfectedYanomami Indiansin
aroundBoaVista.Whenthispossibility wasshownto contrast to the larger aggregations of infected people
be minimal because ofdisrepairofthe road and poor seen in the more populated areas ofmostofthe other
vectorsusceptibility to Onchocercavolvulus(Shelley foci in Latin America. It covers part ofnorth-western
etai, 1987b)interestinonchocerciasisanditsvectors Roraima and northern Amazonas State in Brazil, and
waned.However,thefindingofanautochthonouscase south-easternAmazonasTerritoryandsouthernBolivar
BIOSYSTEMATIC STUDIES ON SIMULIIDAE
StateinVenezuela, andalmostcoincideswiththearea Serra dos Surucucus - the FUNAI post (2°42'N
(about 200,000knr) inhabited by Yanomami Indians. 63°09'W) lies by a stream in a small savanna area
Few ofthe estimated 20,000 Yanomami indians have surrounded by forest at an altitude of 800m. A high
beenexamined,butgenerallythediseaseappearstobe onchocerciasis prevalence of 95% (of 18) was re-
mainlyhyperendemic(morethan60%prevalencerates cordedin 1977.Alatersurveyreportedin1992recorded
and disease with pathogenic effects) in the highland asimilarlyhighprevalencerateof82.2%(of 169)and
central part of the focus and hypoendemic (less than average skin microfilarial densities of 17.8 mff/mg
40% infection rates and disease having no social ef- (personal communication, DrMarcianodaVila). The
fects) in the lowland periphery as a result ofdifferent current population is 1358. Various small rivers and
vector species (Godoy etal. 1989; Rassi etal., 1977; streams occur in this area in the dry season, the only
Tada, 1983; reviews in Moraes et al., 1979; Shelley, locality in the focus where Roraima sandstone is
1988a; Yarzabal et al, 1985). The existence of two present. The Igarape Majeba emerges from forest,
smallerfociinnorthernAmazonasTerritoryandsouth- traverses the savanna by the FUNAI post and then
ern Bolivar State of Venezuela figured in Basanez & againentersdenseforest.Itis3-5mwide,shallow,and
Yarzabal (1989) needsconfirmation. runsoverrocks,sandandmudwithamediumflowand
Communities(malocas)affected byonchocerciasis several waterfalls. The other important water course,
intheBrazilianpartofthediseasefocusoccurin most theIgarapeFalemuisabout2kmsfromthepost,is6m
oftheareaoccupiedbyYanomami Indians, whonum- wide and has clear water flowing fast over rocks. It
beredabout7000inthe 1993censusbytheMinistryof supplies water for a hydroelectric dam. Other water
Health. Although only six localities were visited, courses in the area are a shallow 1.5m wide forest
Yanomamiswereoftenpresentonvisitsfrominacces- stream with muddy water and medium flow close to
sible malocas and they were also examined. In most the abandoned mission post; the shallow, 2m wide,
casestheMissionorFUNAI(NationalIndianFounda- slow flowing, clear Igarape da Floresta in forest 1km
tion) post is a medical centre serving several malocas from the FUNAI post; and a 5m wide, shallow, clear
inthearea, someofwhich maybequitedistant. Inthe forest stream with slow flow at Dalem some 4 hours
1970stheonlyareastudiedthatwasfreeofthedisease walk (15-20kms) from the FUNAI post. Numerous
was the Marari mission in the south (Rassi et al.. otherwatercoursesatsomedistancefromtheFUNAI
1976a,b)butYanomamisfrom the R.Cauabori and R. post were not sampled.
Marauia to the southwest of that mission were not
examined.Theseauthorsalsorecordedtheabsenceof Parimiu-Thisisarelativelynewmissionpost(3°19'N
onchocerciasisin several localitiestotheeast,outside 62°58'W)ontheR. Uraricoeirainforestatanaltitude
Yanomami territory. More localities were studied for of300m.Anonchocerciasisprevalencerateof23%of
onchocerciasis prevalence than for vectors, and these 26examined was recorded in 1977 in this population
are reviewed in Moraes et al. (1978. 1979. 1986). currently numbering 290. The river at this point is
Sampling localitieswerelimited bytheavailabilityof about 15m wide in the dry season with extensive
missionandFUNAI posts with landingstripsforlight rapids over rocks covered by Podostemaceae. No in-
aircraft. Briefdetails ofthe localities sampled during formation is available on streams in the area.
the present entomological work are as follows (see
Map 1) (population estimates based on 1993 census, Mucajai-theMucajaimissionpost(2°45'N,62°14'W)
unless indicated otherwise): isonthebanksoftheR.Mucajaiinforestatanaltitude
of 200m. Onchocerciasis prevalence was low on the
Auaris-theAuarismissionpost(4°00'N,64°29'W)is first survey in 1977 (7.6% of65 examined) and again
the most northern of the localities sampled and is (3.1% of63 examined) 7 years later in a population
situatedattheedgeofthe R.Auaris in aforested area thenof366.TheR.Mucajai400mdownriverfromthe
atan altitudeof670m. Low prevalence rates (19% of mission is 50m wide, rocky with rapids, turbid water
126) of onchocerciasis were found in 1976 in the and submerged vegetation and Podostemaceae(broad
YanomamiandMaiongongIndiansinthearea,whose leaved and strap-leaved species) growing on rocks.A
population is now 912. Skin microfilarial densities 5mwidestream,theIgarapeCoroconai,emergesfrom
then averaged less than 1 mf/mg. Infections with the the forest andjoins the riverat the rapid.
non pathogenic filaria Mansonella ozzardi were also
present(36.5%of126).InthedryseasontheR.Auaris Catrimani - the Catrimani mission post (1°45'N,
is 7m wide with a bottom of large rocks and mud, 62°17'W)isatanaltitudeof230minforestclosetothe
turbid waterand amedium flow. The 2m wide creek, R. Catrimani, a short distance from the Northern Pe-
Igarape Hutumati, has a medium flow on a muddy rimeter Road. Onchocerciasis prevalence was low
bottom and emerges from the forest to join the R. (8.3%of36examined)in 1977andthediseasewasnot
Auaris nearthe mission post. Both flood their banks detected in local Indians 7 years later (0% of 49
and run fasterduring therains. examined). The Yanomami population is currently
A.J.SHELLEY,C.A. LOWRY,M. MAIA-HERZOG,A.P.A.LUNADIASANDM.A.P.MORAES
401. During the dry season (January 1979) the river filarialdensitiesfrom3.2-18.3/mg.Mansonellaozzardi
waslow,about50mwide,fastflowing,exposinglarge iscommonly found in high densities inthebloodand
rocks with species ofPodostemaceae attached to the skinsnipsandMicrofilariabolivarensisisalsopresent
sides andproviding ahabitatforsimuliids. Inthewet (Godoy etal., 1980a,b, 1989).
season the rapids and forest become inundated and Theregioninwhichthefocusliesisoneofthemost
preclude sampling. No local streams are present. isolatedinAmazoniaandbecauseofitsinaccessibility
itsgeology,localclimateandfloraandfaunaarelittle
Toototobi - the Toototobi mission post (1°45'N, known. Huber etal. (1984) summarise available data
63°37'W) is situated alongside the R. Toototobi at on the geology, soils, climate and give details of
180maltitudeindenseforestinthesouthofthefocus, surveys of the vegetation of the Parima mountain
close tothe borderwithVenezuela. A prevalence rate watershed, from which the headwaters of the R.
of 91.7% of 97 Indians examined and average skin Orinoco in Venezuela and the R. Branco in Brazil
microfilarialdensitiesof14.2inthebuttockand5.8mff/ arise. The main part of the Parima and Urucuzeiro
mgintheshoulderregionswererecordedin 1976.The rangesthatdivideVenezuelafromBrazil liesbetween
currentpopulationis627. Indiansfromhereregularly 800and 1200m;varioussmallerrangesoccurbetween
visitvillagesinVenezuela(R. UnguetuandR. Siapa). this and lowland areas (around 100m) in Brazil. The
The river here is about 12m wide with medium flow Parima mountain range consists largely of granite
over rocks and mud, which sometimes become ex- intrusionsinanunderlyingGuayanaShieldbasement.
posed during long dry seasons. In the wet season the InBrazil these are largely alkalinefromthe R.Auaris
riverfloodsthe forest.A streamrunsthroughthe for- inthenorthtotheR. Mucajai, whilefromsouthtothe
estclose tothe missionpost. Urucuzeiro mountainsofAmazonasstateacidicgran-
In Venezuela, onchocerciasis was found in ite and gneiss are present; no Roraima sandstone
Yanomami villages at three main locations, the formationsoccurbutarepresentintheadjacent,lower
headwater region of the R. Orinoco (in the Parima mountain ranges of Surucucus and Uafaranda. Two
mountain range and adjoining lowland forest), the types ofsoil predominate in the Brazilian part ofthe
Siapa river basin of the R. Negro near the Serra de focus:shallowlithosolsandred-yellowpodsolsoflow
Unturan in the FederalTerritory ofAmazonas, and in fertility and high aluminacontent in the uplands, and
theupperR.CauraregioninBolivarState(Basanez& red-yellow podsols mixed with lithosols and
Yarzabal, 1989;Godoyetal,. 1989;Rassi<?f<a/., 1977; diastrophic red-yellow latosols inthe lowlands.
Tada, 1983).Inthefirstareaonchocerciasiswasfound No accurate climatic data are available for every
in several Yanomami villages in highland savanna in partofthe area; those available are mainly fromVen-
the Parima mountains at two mission posts named ezuela. Manydataareconflicting, butthemaintrends
ParimaA (1050m) and Parima B (950m), in villages areasfollows.TheclimateoftheParimamountainsis
neartheOrinoquito(Coyowa-teri)missionpostinthe oftheMonsoontypecharacterisedbyhighrainfallfor
forested foothills of the Parima mountains by the R. 8-10months andlow rainfall, atthe beginningofthe
Orinoquito (250m), and at mission posts in lowland year,for2-3 months,agenerallyisothermictempera-
tropical forest (100-150m) at Platanal and Boca de tureregime,andpredominantwinddirectionfromthe
Mavaca.Yanomami Indiansfurtherdown theOrinoco EtoNE(tradewinds)inthedrierseasonandfromSto
atBocadeOcamoandTamaTamamissionpostswere SE(intertropicalconvergence)fortherestoftheyear.
freeofthedisease. Prevalenceratesofonchocerciasis IntheParimamountainsofVenezuelarainfallislower
were over 70% and skin microfilarial densities were thaninotherpartsoftheregionandoccursthroughout
high(meanof50.3mff/mgofskin)inCoyowa-teriand theyear,butshowsabiseasonalpatternwithmorerain
Parima A and B; both prevalence rates (50% and (above 100mmpermonth)betweenMarchandOcto-
below) and skin microfilarial densities (no densities ber/Novemberandless(around50mm),orsometimes
given) were lower in the lowland forested areas. norain,fromDecembertoFebruary.Lowlandareasin
Mansonelliasis occurred at low prevalence levels in Venezuelashowanon-seasonaltropical lowlandrain-
the Parima area (Beaver et ai, 1976; Botto et al., fall pattern where no month has less than 100mm of
1983). A low prevalence rate ofonchocerciasis (50% rainfall. Savannas are present in humid premontane
of 40) and low skin microfilarial densities (2.9 per forest in the two Parima areas with annual rainfall of
biopsy) of onchocerciasis were recorded from the 1100-1200 mm and an average temperature range of
Siapabasin.A survey of30villages in a700km wide 18-24°C.AtOrinoquitotheveryhumidtropicalforest
strip across Bolivar State showed the presence of has anannual rainfall of3750-5000mm andanaver-
onchocerciasis only amongst seven villages of agetemperatureof26°C. On the Brazilian sideofthe
Yanomami Indians living in a forested, highland re- focusthereisanincreaseinannualrainfallfrom 1500
gion (600-900m) ofthe Upper Caura river area near mm in savanna areas around Boa Vista to more than
thePacaraimamountainsnorthoftheBrazilianborder. 2000 mm in the mountainous areas ofthe Surucucus
Prevalence rates varied from 9-85% and skin micro- and upper Uraricoeira river near Auaris. Average
.
BIOSYSTEMATIC STUDIES ON SIMULIIDAE
monthly temperature maximaand minimashow little Auaris-July 1986(wetseason),March 1977(dry/wet
variation, maximabeing similarin both mountainous seasontransition). Bitingcatches weremadetodeter-
and lowland areas but minima being lower at the mineO.volvulusinfectivityratesandthebitingbehav-
higher altitudes (Venezuela: Parima mountains aver- iour of anthropophilic species. Experimental infec-
age maximum temperature 28°C, minimum 16°C, tions(seebelow)werecarriedouttodeterminewhich
lowlandlocalitymaximum31°C,minimum22°C).At anthropophilic simuliid species are potential vectors
Toototobidatafrommissionariesindicatethatclimate of O. volvulus. Immature stages of simuliids were
varies annually, clearly illustrated by the great varia- collectedfromtheR.AuarisandtheIgarapeHutumati.
tioninriverdepthfromoneyeartoanother(Fig.266).
ThewetseasonusuallyextendsfromApriltoSeptem- Serra dos Surucucus - May 1982 (rainy season),
berbut in 1978 and 1979 rainfall was very low in the December 1986 (dry season). Nobiting catches were
wet season. carried out here but the following streams (igarapes)
ThevegetationintheVenezuelanParimamountains were sampled for immature stages: Igarapes Majeba,
in areas of acidic quartz and igneous outcrops is Falemu, da Floresta, and unnamed streams at the
similar to that of the Guayana Highlands although abandoned mission post and Dalem.
containing more widespread neotropical taxa. Some
species occuruniquely inparts ofthe range.The lack Mucajai-January 1977, (dry season)July 1984(wet
of uniformity of the flora is attributed to the differ- season). Daylongbitingcatches were notcarriedout.
encesinaltitude,soilsandwatercoursesinthearea.In The R. Mucajai andthe IgarapeCoroconai weresam-
the Brazilian Parima mountains, vegetation has been pled for immature stages.
dividedintothefollowingtypes:submontaneforeston
TerraFirme(600-1000m), similarin speciescompo- Catrimani-January 1977 (dry),January 1979(dry),
sition to the adjacent Guayanan-Amazonian lowland July 1984(wetseason).Bitingcatchesandexperimen-
forest except for white sand formations with vegeta- tal infection studies were carried out to determine
tion similar to areas of the R. Negro, e.g. Auaris; bitingbehaviour,parousandinfectionrates.Immature
montane cloud forest above 1000m; summit and out- stages were collected in the R. Catrimani.
crop floras at high altitudes with cloud forest and
shrubby vegetation; river margins with common Toototobi - December 1975 (wet season), February
riverine Amazonian species; and savanna found only 1976 (wet/dry season), August 1976 (dry season),
in the Serra dos Surucucus. This area is particularly October 1976(wetseason), December 1976(wetsea-
interesting because it has Roraima sandstone forma- son),August 1977 (dry season), December 1977 (dry
tions and is composed ofmontane forest and a small season).Bitingcatchesweremadetodeterminebiting
areaofsavannaandisclassifiedasarefugeforseveral behaviour, parous and infection rates.Anthropophilic
plant families. flieswereexperimentally infectedwith O. volvulusto
determinethepotentialvectorspecies.Immaturestages
werecollectedfromthe R.Toototobi andanunnamed
MATERIALAND METHODS Igarape nearthe mission post.
Biting catches using Yanomami volunteers were
Sampling of adult simuliids attracted to Yanomami carried out at most localities to determine species
volunteers, and of immature stages from breeding biting man, preferential biting sites on body, biting
grounds,approachedbyfootorcanoe,wascarriedout times and to provide material forparity and infection
at the localities indicated below, but several major rate studies. Methods forcollecting and dataanalysis
constraints hindered collections at many ofthe sites. are described in Shelley etal. (1982) and dissections
Logistical difficulties were enormous: the expense of forparityfollowedthemethodsofLacey&Charlwood
getting to the study area by aircraft was a major (1980).
constraintforseasonalsampling;thelackofmotorised The methodology forexperimental infectionofan-
canoes and roads restricted prospecting of immature thropophilic species to determine potential vectors is
stages tothe environs ofthe mission or FUNAI post; given in Shelley & Arzube (1985). Dissections for
the communication problem with Yanomami Indians experimentalandnaturalinfectionratesweremadeof
unable to speak Portuguese precluded more intense alcohol preserved flies (that had not been scored for
sampling on biting habits; and the lack of facilities, parity in natural infection studies) using the method
such as electricity and housing severely restricted described in Nelson (1958). No domestic animals
microscopic work in thefield. exceptchickensanddogswerekeptatthemissionand
Collections to show seasonal trends were made at FUNAIpostsinBrazilsohostpreferencestudieswere
ToototobiandtoalesserextentatAuarisandCatrimani not attempted.
Dates ofcollection and season were as follows: Collections of immature stages were made in a
A.J. SHELLEY,C.A.LOWRY,M.MAIA-HERZOG,A.P.A. LUNADIASANDM.A.P. MORAES
variety ofwatercourses ofwhich the following were distal point of the wing to the mid- point on a line
the most common types: shaded forest streams & drawnfromthebaseofthecostalveintothebaseofthe
savannastreams, rapids in largerivers with speciesof wingon its posteriormargin.
Podostemaceaegrowingon submergedrocks, slowto Wingwidth-astraightlinedrawnatthewidestpoint
medium-flowing rivers with beds of mud, rocks or between the anteriorand posteriormargins.
sand and waterfalls.
Observations in the paper are largely based on Pupa
specimensdepositedinTheNaturalHistoryMuseum,
(formerlytheBritishMuseum(NaturalHistory)),Lon- Cocoon lengthdorsally-acurved linefromtheante-
don, UK; all species are also represented in the riormargintotheposteriorpointofattachmenttothe
collections at the Instituto Oswaldo Cruz substrate with the cocoon lying in a lateral position.
Cocoon length ventrally - a straight line from the
(DepartamentodeEntomologia), RiodeJaneiro,Bra-
anterior to posterior points ofattachment ofthe co-
zil. Material has been conserved as follows: larvae,
coon tothe substrate.
pupae,individuallyrearedadultswiththeirpupalpelts
andfemalesfrombitingcatches-in80%alcohol;indi- Pupa length - a straight line from the frons to the
posterior end ofthe abdomen with the venter upper-
vidually reared adults in association with their pupal
most.
pelts(inglycerine in small polypropylene phials)and
Gill length-acurvedlinealongthelongestunbroken
femalesfrombitingcatches-inthepinnedcollections;
all stages on microscope slides in Berlese mountant; filamentfrom itsdistal tiptothebase ofthemain gill
individually reared adults and man-biting females trunkat itsjunction with thethorax.
testedforcuticularhydrocarbons-preserveddry;chro- Larva
mosomal preparations from larval silk glands on
microscopeslideswithaccompanyingphotographsof Body length - a curved line from the base of the
some of the karyotypes, larval cadavers-on micro- posterior circlet to the point of attachment of the
scope slides or in 80% alcohol. Descriptions ofadult mandibletotheheadcapsulewiththelarvainalateral
colorationforeachspecieshavebeenbasedonpinned position.
specimens while colourplates are from both pinned Headcapsulelength-astraightlinefromtheposterior
andalcoholpreservedmaterial,preparedaccordingto margin to the most anterior point of the cephalic
the techniquedetailed in Shelley etal. (1989). Scutal apotome.
patterns of S. rubrithorax, S. oyapockense and S. Head capsule width - a straight line between the
wraimense vary with direction of illumination. For lateral margins at the widest point (always in the
eachofthesespeciesdescriptionsofscutalpatternsare posteriorhalf).
givenwiththemainlightsourceineitherananterioror
posterior position. Each specimen was arranged as Terminology ofstructures in adults, pupae and lar-
follows:dorsalsurfaceparalleltothemicroscopestage, vaefollows Shelley etal. (1989). At the beginning of
with a diffuse background light to the left of the each species description the following information
observer (at about 7 o'clock and shining on to the regarding the original description and subsequent
whole specimen and sufficiently bright to prevent synonymies is given: species or synonym name, au-
shadow formation) and a focussed fibre optic light thor,dateofpublication:firstpageonwhichdescription
placedeitheranteriororposteriortothe specimenon occurs, primarytype and sex, collection locality, date
the samehorizontal plane as the microscope stage. ofcollection,{collector),(currentdepository),[details
Most measurements were made using a camera ofsynonymy]. Names in previously published works
lucida, later replaced by an image analysis system that are misidentifications or junior synonyms are
(KontronElektronikVideoplanwithaZeissAxioskop referredtointhispaperbythespeciesnameusedinthe
20andanSV6microscopes). Bodylengthsforall life systematics section. Table 4 provides a list ofnames
stages were measured from material in a lateral posi- usedforthese species in previous publications.
tion maintained in glass beads within a watchglass Thefollowingacronymsareusedfordepositoriesof
containing alcohol (orCarnoys fixative in thecase of specimens referredto in thispaper.
some larvae). Gill and wing dimensions were meas- BMNH TheNatural HistoryMuseum,London,U.K.
ured from specimens in alcohol or slide mounted. DDSV SecciondeOncocercosis,Divisionde
Points ofmeasurement(Fig. 1) wereas follows: DermatologiaSanitaria,VilladeCura,Aragua
State,Venezuela.
Adults DERM LaboratoriodeEntomologiadelaDivisionde
EndemiasRurales,Maracay,AraguaState,
Bodylength-acurvedlinedrawnfromthefronstothe Venezuela.
tipofthegenitalia. ESUCV EscueladeCiencias,UniversidadCentralde
Wing length - a straight line drawn from the most Venezuela,Venezuela.
1
BIOSYSTEMATIC STUDIES ON SIMULIIDAE
FSPUSP InstitutodeHigiene,SaoPaulo, Brazil. thatareeasilydamaged (e.g. scales)arenotgenerally
1ND InstitutoNacionaldeDermatologia,Villade used, the main characters being easily observed in
Cura,Aragua,Venezuela undissected material whereverpossible.
IOC InstitutoOswaldoCruz,RiodeJaneiro,Brazil Thekeyfunctionsforthefourteenspeciesthatoccur
IP InstitutePasteur,Paris,France in the Brazilian partoftheAmazoniafocus. Itcan be
INPA InstitutoNacionaldePesquisasdaAmazonia, used as a starting point only for identification of
NMV NMaatnuaruhsi,stoBrraizsiclh.esMuseum,Vienna,Austria. sspheocuiledsbienntohteedVtehnaetztuheelraenthzeofnoelloofwitnhgesfpoeccuise,sbouctcuirt
SMT StaatlichesMuseumfiirTierkunde,Dresden, also: beaupertuyi, covagarciai, matteabranchia, mo-
Germany.
rae,parimaenseandperflavum. Descriptionsofthese
STMPR DepartmentofMicrobiology,Schoolof
speciesaregiveninRamirezPerez(1983)andRamirez
Medicine,SchoolofTropical Medicine, San
Perezetal. (1982, 1984, 1986).
Juan,PuertoRico.
USNM UnitedStatesNationalMuseum,Washington,
D.C.,U.S.A. Females
ZMHU ZoologischesMuseumderHumboldt-
Universitat.Berlin,Germany. 1 Scutumorangeorbrown 2
Full data for the very extensive material on which Scutumblack 6
thisworkisbasedaregiven inAppendix 1 (p.95)and 2 Scutumwithpattern 3
thisshouldbeconsultedforgeographical information.
Scutumwithoutpattern 5
Voucher specimens of O. volvulus infective larvae
mounted in Berlese on slides have been deposited in 3 Scutumbrownwithmedianandpairoflateralvittaeand
the World Health Organization Collaborating Centre lateral margins silver pruinose (anterior illumination)
forthe Filarioidea, International InstituteofParasitol- (ColourPlate 1,Fig. 18) rubrithorax
ogy, Winches Farm Lane, St Albans, Hertfordshire, - Scutumorangewithwhite vittaeorcunae 4
U.K.
4 Scutum with pair of anterior, submedian, silver cunae
(ColourPlate2,Fig.30) bipunctatum
Acknowledgements. We would like to acknowledge - Scutum with pair of submedian silver vittae running
thesupportgivenbyourcolleaguesintheMinistryofHealth, from anteriortoposteriorborders (ColourPlate 2. Fig.
Brasiliaduringthe 1970s,especially DrsLelioB.Calheiros, 31) iracouboense
Marcos Porto, Agostinho Cruz Marques and Ernani Mota.
5 Paraproct large, three times length ofcercus (Fig. 99).
Withouttheirforesightandlogisticalandpoliticalsupportfor Cibarium with 1+1 groups of sharp, submedian teeth
onchocerciasis research none ofthis work would have been (Fig.55) rorotaenseandsuarezi*
possible and the recently initiated control campaign in
Amazoniacouldnothavebegun.Thehospitalityandlogisti- - Paraproctsmall,twicelengthofcercus(Fig.98).Cibarium
cal support ofmissionaries and FUNAI staffare gratefully withblunttuberclesinmedianandsubmedianareas, 1 +
acknowledged. Fundingforthisprojectwasprovidedbythe 1 groupsoffine,sharpteethatbaseofcornuae(Fig.54)
Conselho Nacional de Desenvolvimento Cientifico e /ill:ianuin
Tecnologico,InstitutoOswaldoCruzandMinisteriodaSaude, 6 Scutumwithsilverpruinoseareas 7
Brazil;TheNaturalHistoryMuseum,London,andtheBritish
Council, U.K. and the World Health Organization. Theresa Scutumwithoutsilverpruinoseareas 1
Howard produced Maps 1-3, PeterYork Colour Plates 1^ 7 Scutum mainly black with only humeri, lateral and
(figures 18-35 and 113-131), Drs Joao Batista Vieira and posterior margins silver pruinose (Colour Plate 2, Fig.
MarianodaVilaarethankedforprovisionofthemostrecent 35) goeldii
parasitologicaldataonthefocus,andDrVPy-Danielkindly - Scutumblackwithsilverpruinosepatternondorsum
providedextradataforsomeofthespecies.DrR.W.Crosskey
8
providedvaluablecommentsonthemanuscript.
8 Scutumwithpairofsubmediansilverpruinosecunaein
anteriorhalfofscutum [posteriorillumination] 9
KEYS TOTHE SIMULIID SPECIES - Scutum with pair of submedian silver pruinose bands
OFTHEAMAZONIA joining pruinose anteriorand posteriormargins [poste-
ONCHOCERCIASIS FOCUS OF riorillumination] 10
BRAZIL 9 Nudiocular area absent (Fig. 38). Cibarium unarmed
(Fig.49) cauchense
These keys have been constructed to facilitate rapid - Nudiocularareapresent(Fig.40).Cibariumarmed(Fig.
identification wherepossible. Morphologicalfeatures 51) incrustatum
1 1 31
A.J. SHELLEY,C.A.LOWRY,M.MAIA-HERZOG,A.P.A. LUNADIASANDM.A.P. MORAES
10 Submedian silverbands fineanddivergingposteriorly; Scutumwithsilverpruinosebandsarisinginsubmedian
blackareasare[patternconsistentirrespectiveofillumi- region of anterior margin and with antero-median,
nation]: median, drop-shaped vitta and pair of wide, comma-shapedmark(blackwithanteriorandsilverwith
submedianvittae;anteriorintervittalcunaeinsilverbands posteriorillumination)(ColourPlate3,Fig. 120)
absent(ColourPlate 1,Fig. 21) quadrifidum roraimense
- Submedian silver bands wide; black areas are: [with - Scutumwithsilverpruinosebandsarisinginareabelow
anteriorillumination]medianvittawideningposteriorly, humeri on lateral margins and without comma-shaped
pairofdisc-shapedareasbetween median vittaand lat- mark(ColourPlate4,Fig. 129) guianense
eral scutal marginsandpairofanterior,comma-shaped
marksinsubmediansilverbands;[withposteriorillumi- 9 Submedian,silverpruinose,triangularmarkingslarge;at
nation]disc-shapedblackareasextendtoanteriorscutal least2/3aswideaslongatanteriormarginandextending
border and comma-shaped marks in submedian silver fromanteriormarginfor 1/2to2/3ofthoraxlengthand
sometimesextendingasfinelinesalmosttosilverposte-
bandsappearsilver(ColouoryaPlpaotceke1,nsFiegsan2d3,ro2r4a)imense riormargin(ColourPlate3,Figs 117, 118, 119)
oyapockense
1 Nudiocularareaabsent(Fig.37).Paraproctbroadlyrec- - Submedian,silverpruinose,comma-shapedmarkssmall;
tangular with pointed, anteriorly-directed process (Fig.
92) exiguum atmaximum 1/3aswideaslongatanteriormargin.. 10
- Nudiocular area present (Fig. 45). Paraproct broadly 10 Abdomenwithprominentpruinosepatchatlateralmar-
ginsofeighthtergite cauchense
rectangular with tail-like projection pointing inwards
(Fig. 100) guianense - Abdomen without prominent pruinose patch at lateral
* basedondescriptionbyRamfrezPerezetaI. (1982) marginsofeighthtergite(ColourPlate3,Fiqgusad1r1i5,fi1d1u6m)
Males 1 Scutum with groups ofshort, wide, iridescent goldenor
greensetae,especiallyonanteriorhalf 12
1 Scutumorangeororange-brown 2 - Scutumwithnumerousrecumbent,silverorgoldenhairs
- Scutumblack 6 butlackinggroupsofwidesetae 13
2 Scutumorange-brown, pairoffaint, silvertrianglesex- 12 Only posterior scutal margin faintly pruinose (Colour
tendingintofinevittaeinanteriorhalfofscutum[posterior Plate 3, Fig. 114). Gonostyle with inconspicuous spine
illumination](ColourPlate3,Fig. 113).Scutellumbrown (Figs 133, 134, 135) exiguum
rubrithorax - Lateralandposteriorscutalmarginsobviouslypruinose
- Scutumorange,withorwithoutdorsalpattern.Scutellum (Colour Plate 3. Fig. 121). Gonostyle with well devel-
orange 3 opedspine(Fig. 139) incrustatum
3 Scutumwithsilverdorsal pattern 4 1 Gonostylebroadatbasetaperinggraduallyindistalhalf
(Fig. 136) quadrifidum
- Scutumwithoutpattern* 5
Gonostyle narrow at base and becoming narrower in
4 Scutumwithpairofanterior,submediansilveroryellow distalthird(Fig. 146) goeldii
cunae(ColourPlate4,Fig. 124) * Theyellowcomma-shapedmarksinmaleS. suareziare
bipunctatum andsuarezi
sometimesabsent.
- Scutum with pair of submedian silver bands running
from anterior to posterior border (Colour Plate 4. Fig. Pupae
125) iracouboense
1 Gill fan-shaped,with 18-20filaments 2
5 Ventralplateaswideaslong,withsmallkeel(Fig. 154)
lutzianum Gill notfan-shaped,with4—12filaments 3
- Ventralplatelongerthanwide,withelongatedkeel(Fig. 2 Filaments arising in pairs or singly in basal 1/6 ofgill
155) rorotaenseandsuarezi fromdorsalandventralprimarybranches(Fig.207)....
rorotaense
6 Scutum with silver pruinose dorsal pattern [posterior
illumination] 7 Filamentsarisinginpairsorsinglyfromexpandedbase
ofgill(Fig.208) suarezi
- Scutumwithoutsilverpruinosedorsalpattern 1
3 Gillwith 12filaments(Fig. 209) guianense
1 Pair of silver pruinose bands connecting anterior and
posteriormarginsofscutum [posteriorillumination].... - Gillwithlessthan 12filaments 4
8 4 Gill with8filaments 5
- 1+1 submedian,silverpruinose,comma-shapedortrian- Gillwithlessthan 8filaments 10
gular markings in anterior half of scutum [posterior
illumination] 9 5 Cocoonshoe-shapedandwithanteriorfestoonsobscur-
3
BIOSYSTEMATIC STUDIES ON SIMULIIDAE
ingcephalothoraxofpupa(Fig.180) rubrithorax particularly where longseries ofspecimens arebeing
Cocoon slipper-shaped, cephalothorax of pupa partly examined.Thekeyappliestomaturelarvaewithfully
exposed 6 developed gill histoblasts.
6 Gill filaments fine and flimsy; main trunkdividing ba- 1 Bodyuniformlydark,lengthmorethan 10mm(Fig.213)
sallytoformtwoprimarybranches(Fig.210).. goeldii rubrithorax
- Gillstoutandrigid;maintrunkdividingbasallytoform - Body lightwithdarkbands,lengthlessthan7mm ... 2
threeprimarybranches 7 2 Cuticle surface smooth with numerous setae mainlyon
7 Gill filaments bunched together, depth at most distal dorsalsurface 3
bifurcation less than maximum depthofcephalothorax - Cuticlesurfacesmoothwithoccasionalsetae 7
(Fig. 206) lutzianum
3 Setaeon thoraxandabdomenlargeand platelet-shaped
Gill filamentssplayedout,depthatmostdistalbifurca- (Figs 14,222) guianense
tionmorethanmaximumdepthofcephalothorax 8
Setae on thorax and abdomen small and pointed (Fig.
8 Ventralprimarybranchofgillalmostparalleltoanterior 13) 4
edgeofcephalothorax(Fig. 203)
bipunctatum 4. Ventral papillaepresent(Fig. 217) 5
Ventral primarybranchofgill atrightanglestoanterior Ventral papillaeabsent(Fig. 220) lutzianum
edgeofcephalothorax(Figs 192,204) 9 5. Abdomen with prominentdark bands on first fourseg-
9 Transverse rings on filaments highly accentuated (Figs ments. Head pattern strongly positiveornegative (Figs
192, 193) exiguum 217,229,230) incrustatum
- Transverseringson filamentsfaint(Fig.204) - Abdomen withnodark bandson firstfoursegments,or
iracouboense withfirstsegmentonlywithprominentdarkband.Head
pattern absentorfaintlypositive 6
10 Gillwith6filaments 1 1
6. Ventral papillaelarge(Fig. 215)
Gillwith4filaments 13 cauchenseandquadrifidum
I I Gill long,atleast 1.5timespupal length(Fig. 198) - Ventral papillaesmall (Fig.216)
incrustatum oyapockenseandroraimense
- Gillshort,approximatelylengthofpupa(Figs 196, 197) 7. Poslgenal bridgehighlyreducedorabsent(Fig.243)...
12 bipunctatum
12 Thoracic platelets mainly rounded. Tergite II with or - Postgenalbridgewelldeveloped(Fig. 239) 8
withoutI+1patchesofantero-lateralspinecombs,tergite
III withsuchspine-combs(Fig. 211) oyapockense 8. Abdomen with prominent dark bands on four anterior
narrowsegments(Fig. 214) exiguum
- Thoracic platelets mainly pointed. Tergites II and III
withoutspine-combs(Fig.212) - Abdomenwithoutobviousbandsonfouranteriornarrow
roraimense segmentsorwithonly bandon firstsegmentprominent
(Fig.219) 9
1 Primarybranchingofgillinhorizontalplane;gillbranches
usually bifurcate at same level in basal 1/5 ofgill; ab- 9. Head pattern negative in form of circle with crenated
dominal tergite V with weak submedian row ofspines outerborder(Fig. 232) iracouboense
(usually present) along anterior border terminating in - Headpatternabsentorslightlypositive 10
weakpatchofspinecombsatmargins(Fig. 194)
quadrifidum 10. Mandible with antero-lateral process fleshy and forked
- Primary branching ofgill in vertical plane; gill branch (Fig. 260) goeldii
bifurcationsusuallynotatsamelevelatmidpointofgill; Mandiblewithoutantero-lateralprocess .... rorotaense
tergiteVwithoutspinesorspinecombs(Fig. 195)
cauchense
Larvae
SPECIES DESCRIPTIONS
Two important characters used in identification of
larvaeofNeotropicalspeciesaretheheadspotpattern
and body coloration. Both these characters are now Simulium (Hemicnetha) rubrithorax Lutz
known to show considerable variation in both S.
exiguums.I. andS.guianense.Thiskeyshouldbeused (ColourPlate 1, Figs 18,19; ColourPlate 3, Fig. 113;
taking into consideration that extensive variation in Figs 36, 47, 58, 69, 80, 91, 102, 132, 147, 158, 169,
thesecharacterscouldalsobepresentinotherspecies, 180, 191,213,224,238,249)
10 A.J. SHELLEY,C.A.LOWRY,M. MAIA-HERZOG,A.P.A.LUNADIASANDM.A.P. MORAES
Simulium rubrithoraxLutz, 1909: 132. NEOTYPE9, nantly(orsolely)finesetae;nextquarterwithirregular
BRAZIL: Minas Gerais State, Juiz de Fora, row of both fine and stout setae; distal quarter with
43°22'W 21°47'S, 10.x.1909 (C Chagas) (IOC) regularrow ofmainly stout setae (total of40-48 fine
bydesig-nation ofMaia-Herzog etal. (1984: 352). setaeand22-25 stoutsetae)(Fig.58).Costalbasetuft
[LECTOTYPE 9 designation of Vulcano (1958) ofdark hairs.
invalid as not from syntype series (Maia-Herzog Legs yellow with following dark areas (Colour
etai, 1984)] Plate 1, Fig. 18): fore leg with distal sixth offemur,
SimuliummagnumLane& Porto, in Porto 1940: 383. basalquarteranddistalfifthandoutermarginoftibia,
HOLOTYPE 9, BRAZIL: Mato Grosso, Chapada, basitarsus and tarsi dark brown; mid leg with coxa,
Ponce, 600m, viii.1934 {J.Lane) (FSPUSP). [Syn- distalsixthoffemur,distalquarter, sub-basalspotand
onymy by Py-Daniel, 1989: 255.] outermarginoftibiablack;distaltwofifthsofbasitarsus
and tarsi dark brown; hind leg coxa black, distal
This well known species was only collected in the quarter offemur all oftibia except basal articulation
larval stage in the onchocerciasis focus. The descrip- and median quarter, distal half of basitarsus black;
tion below is therefore based on material collected distal halfoffirst tarsomere and remaining tarsi dark
here and from other parts of Brazil deposited in the brown. Clawscurvedwith largebasal tooth(Fig. 69).
BMNHandIOCandnotedunderMaterial Examined. Halteres pale yellow with slightly darkened stems.
Abdominal tergites predominantly black, but mot-
Female. General body colour orange/brown and tled orange-brown (Colour Plate 1, Fig. 18); basal
black. Body length 3.4-4.5 mm (n=2); wing length scale(tergiteI)velvetyellow/blackwithfringeoflong
3.2^1.6 mm (x=3.8 mm, s.d.=0.4, n=18), wing width golden hairs; tergite II velvetblack with anteriorhalf
1.4-1.9 mm (x=1.7 mm, s.d.=0.4, n=16). mottled with rust coloured patches; tergites III—IV
Headdichopticwithredeyesshowinggoldenhigh- velvet-black; tergitesV-IX shiny black. Tergal plates
lights;nudiocularareawelldeveloped(Fig.36).Frons, sclerotised as in S. exiguum (Fig. 5). Sternites mid to
clypeusandocciputdarkbrownwithsilverpruinosity; palebrown.Genitaliabrown.Eighthsternitewithwell
fronswithnumerous, irregularlyarranged, stouthairs sclerotisedcentralplateand 1+1 groupsof11-13well
predominantlyon margins. Mouthpartsandmaxillary developed setae; gonopophyses large and well devel-
palpsdarkbrown.Antennaebrownwithscape,pedicel oped, subtriangular, covered in setae with some
andbasal thirdoffirstflagellomere yellow. Cibarium sclerotisation on lowersurface (Fig. 80). Cerci hemi-
unarmedwithslighttrough, lightlysclerotisedmargin spherical but slightly flattened on outer surface;
and highly sclerotised cornuae (Fig. 47). paraprocts subtriangular and extremely large (about
Scutum predominantly orange-brown with numer- 2'/2timesaswideascerci)extendingwellbelowcerci
ousrecumbentgolden hairs. Scutal pattern varying in (Fig. 91). Genital fork (Fig. 102) highly sclerotised
appearancewith illumination. Withanteriorillumina- with long vertical anteriorprocess, areaencompassed
tion,thoraxdarkbrownwithfollowingareasgrey-silver by lateral arms relatively narrow, end of stem spatu-
pruinose: wide median vitta originating as triangle late. Spermatheca oval, strongly sclerotised, without
withbaseonanteriormargin,expandingtodrop-shape external sculpturing and spicules in rows; width of
extendingforninetenthsofscutum,dividedlongitudi- membranous area of insertion of spermathecal duct
nally by fine, dark brown line; pair of lateral vittae small, aboutquartermaximumwidthofspermatheca.
beginningatanteriorfifthofscutumandextendingfor
nine tenths of its length; lateral border of scutum Male. General body colour mottled orange-brown
(ColourPlate 1, Fig. 18). With posterior illumination andblack.Bodylength4.0-5.1 mm(n=2);winglength
grey pruinose and brown areas become reversed, the 2.6-3.8 mm (x=3.4 mm, s.d.=0.4, n=9); wing width
previously pruinose vittae appearing dark brown and 1.3-1.9 mm (x=l.6mm, s.d.=0.2, n=9).
thedarkbrownbackgroundsilver-greypruinose;pos- Head holoptic with uppereye facets red and lower
teriormargin greyish black (ColourPlate 1, Fig. 19). eye facets dark red (appearing black in dried speci-
Humeri orange-brown. Paranotal folds dark brown mens). Restofhead coloration as in female.
with silver pruinosity. Pleural region dark, mottled Scutum orange-brown with some black areas and
orange-brown with grey pruinosity; prominent patch silver pruinosity; numerous recumbent, golden hairs
of long, golden hairs on pronotum; pleural tuft of (ColourPlate 3, Fig. 113). Lateral marginsandposte-
prominent, golden hairs. Scutellum mid brown with riorquarterofscutumsilverpruinose.Scutumwithno
lightpruinosityandnumerous,long,recumbent,golden pattern, anteriormargin grey pruinose with anterior
hairsandlong,darkhairsonoutermargins.Postnotum illumination. Scutum with pair of small, faint silver
dark brown with grey pruinosity. trianglesonanteriormarginjoiningpairofsubmedian
Subcostal wing vein withrowof4—6setaein basal narrowsilvervittaerunningtomiddleofscutumwith
half; many sensilla in basal area. Basal quarter ofR posterior lighting. Black areas around humeri and
bare;followingquarterwithirregularrowofpredomi- central third of scutum. Humeri orange-brown. Col-