Table Of ContentOVIPOSITION BEHAVIOUROF THREE INTRASPECIFIC
VARIANTS OF THEVISCERALLEISHMANIASIS (KALA-AZAR)
VECTORPHLEBOTOMUSARGENTIPES
1
K. Ilango2
(With one text-figure)
Key words: Phlebotomus argentipes visceral leishmaniasis vector, oviposition behaviour,
,
intraspecific variation
Oviposition behaviour ofPhlebotomus argentipes Annandale & Brunetti sensu lato studied in
thevisceralleishmaniasis(VL,kala-azar)endemicandnon-endemicpartsofTamilNadusuggests
that (i) the species has 3 intraspecific variants (possibly representing separate species), (ii) the
meannumberofeggslaidperflyishigherinthefliesfedon cattlethanon humanbeings,(iii)the
varianthuman-fedformis sympatricwiththeneighbouringcattle-fedform,whileboththecattie
fed variants are allopatric in nature, (iv) the possible cause for the vector capacity ofthe form
feeding on humans is discussed, (v) research on the behaviour, based on genetics and using
molecularbiologicaltoolssuchasisoenzymeanalysisandDNApawprinting,isneededtoresolve
thetaxonomic statusofP. argentipes.
Introduction leads to divergence ofbehaviour and formation
oftwoormorespecies(Dobzhanskyetal. 1976).
Phlebotomus argentipes Annandale & Thisisusuallyfoundindiseaseendemicregions.
Brunetti sensu lato, described by Annandale To differentiate such closely related species,
(1908), has been studied extensively as a vector morphological taxonomy serves a limited
of the Indian visceral leishmaniasis (VL, kala- purpose, but molecular techniques and genetics
azar). The currently known geographical and basedbehaviouralstudiesareextremelyreliable.
biologicalvariationsofP. argentipesmayconsist In view of this, while surveying the wetland
ofacomplex ofsibling species (Seccombe etal. mosquito fauna ofTamil Nadu, the oviposition
1993), that are morphologically similar but behaviour ofP. argentipes was studied in parts
different in behaviour. Recently, two ofthe state where kala-azar is endemic.
morphospecies found sympatrically were
described from the city of Chennai (=Madras) Study Area
(Ilango et al 1994), one of the known foci of
VL. In Tamil Nadu, the city of Chennai and
Incriminationofvector species amongthe two rural districts, Ramanad and Tirunelveli,
species complex is extremely important for known endemic foci ofVL, were surveyed for
taxonomists before developing any control thephlebotominesandflyfaunaduring 1987-90.
strategies. However, theproblemamongclosely Recently, afewcases ofkala-azarwerereported
allied variants in insect vectors is that from Chennai, but the disease was unknown in
competition forresources, such as feeding hosts the Ramanad and Tirunelveli district. Chennai
andmatingsites,insimilarecologicalconditions, was, therefore, considered an endemic focus,
whileRamanadandTirunelveliweredesignated
'AcceptedJuly,1999 as non-endemic. For the present study,
TreshwaterBiologicalStation,ZoologicalSurveyofIndia,
1-1-300/B,AshokNagar,Hyderabad500020, Tirunelveli (peridomestic) and Chennai
AndhraPradesh,India. (domestic and peridomestic) were chosen for
JOURNAL, BOMBAYNATURAL HISTORYSOCIETY, 97(3). DEC. 2000 363
OVIPOSITIONBEHAVIOUROFTHEVISCERALLEISHMANIASISVECTOR
sample collection because they are widely
separated from one another, and represent
different habitats. Further, in Chennai, samples
were collected from the centre of the city,
Royapettah (domestic) where VL was knownto
exist, andfromthesuburbanvillagePoonamalle,
30 kmwestofChennai, fromwhere VL wasnot
known.
Method
Veeravandiyur village in Tirunelveli
districtandPoonamallevillagenearChennaiare
identical habitats in their housing pattern,
surrounded by cattle sheds, paddy fields and
irrigation ponds. Royapettah has typical urban
dwellings with crowded housing. Stray cattle
were often found on the streets. Humans and
cattle are the sources of blood meal for
P. argentipes priorto oviposition.
As P. argentipes is nocturnal, night
collectionofsampleswasmadefrombothhuman
dwellingsandcattlesheds. Inallthe3 studysites, Fig. 1. Locations ofthree intraspecific female
blood-fed females were collected from the variants (A, B, C) ofP. argentipes collected. Bar
abdomen of cattle in Veeravandiyur and diagrams representthe mean no. ofeggs laid per fly
Poonamalle villages, humans also servedasbait attracted to both hosts.
simultaneously. Blood-fedflieswereindividually
storedin !4"x3" glasstubesandleftundisturbed (A) Veeravandiyurvillage, Tirunelveli
overnighttooviposit. 5%glucosesolutionsoaked Total no. offlies captured (N) = 39
in cotton was supplied to each fly as nutritional No. ofeggs laidper fly
supplement. Mean (x) = 71.64 ±3.64 (s.d)
Range (R) = 65-77
Results
(B) Royapettah in Chennai
Fig. 1 shows the locations (ABC) from Total no. offlies captured (N) = 21
whichthefemalesofP. argentipeswerecollected; No. ofeggs laidper fly
thebar diagrams representthe mean no. ofeggs Mean (x) = 41.66 ±4.83 (s.d)
laidperfly.ThedistancebetweenVeeravandiyur Range (R) = 32-50
(A)andRoyapettah(B)orPoonamalle(C)is680
km and Royapettah (B) and Poonamalle (C) (C) Poonamalle village near Chemiai
30 km. In Veeravandiyur and Poonamalle Total no. offlies captured (N) = 32
villages, the female flies showed a greater No. ofeggs laidper fly
preference for cattle than for human beings, Mean (x) = 69.00 ±4.46 (s.d)
whereas in Royapettah they were equally Range (R) = 54-76
364 JOURNAL, BOMBAYNATURAL HISTORYSOCIETY, 97(3) DEC 2000
OVIPOSITIONBEHAVIOUROFTHEVISCERALLEISHMANIASISVECTOR
Discussion P. argentipes collected from endemic and non-
endemicareasofvisceralleishmaniasis, inwhich
The present study reveals some intriguing the relative size of the fourth antennal ascoids
biological variations in the ovipositionbehaviour shows character displacement. According to
ofP. argentipes collectedfrom3 differentplaces, Brown and Wilson (1956), character
theirhostpreferenceandthemeannumberofeggs displacement is observed in two closely related
laidper fly. The eggs laidby the variants AC are specieswhentheirallopatricpopulationsarevery
similar in their oviposition sites and meanno. of similar and their sympatric populations distinct
eggs laidperfly, butbotharequitedifferentfrom in one or more characters. The disparate
B. The ecological distribution ofthese variants characters could be morphological or
shows thatA is allopatric to BC and B sympatric behavioural. In this study, the pattern of
to C. AC are more strongly attracted to a blood distribution and oviposition behaviour of three
meal fromcattle thanfromhumans. B is attracted variants of P. argentipes suggests that it may
to both cattle and humans, the latter providing a consistofseveralisomorphic species distributed
better opportunity to transmit kala-azar. across the Indian Subcontinent.
Severalpossibleexplanationscanbegiven According to Tabachnick and Black
forthe differences inbehaviouranddistribution (1995), current species identification using
of these variants. For AC, feeding on cattle isoenzyme analysis, DNA probes and PCR
appearstobemore advantageous, astheyoffera delimits species and provides genetic
large, open body surface where the blood meal relationships. Molecular taxonomy promises to
can be taken immediately after mating. Cattle be an important tool for (1) discrimination of
blood is richer in iron than human blood and cryptic members of species complexes, (2)
perhaps they are less sensitive to biting. Hence, identificationofmorphologicallysimilarspecies
cattlearepreferredbyAC. Humanbloodmealis at any life stage, and (3) rapid identification of
preferred by B, which could be the vector of small arthropods (eg. mites, sandflies,
visceral leishmaniasis. Culicoides). Population genetics characterises
Theseobservationscoincidewiththeknown genetic variation within and among populations
findings on the two morphologically different ofa species. Members ofspecies complexes and
species. In the present study, the intraspecific morphologically similar species are likely to be
variants AC are similar to the morphological descendents of populations that were once
species A, which occurs in Tamil Nadu and the membersofasinglespecies. Studiesthatexamine
whole of South Asia and has perhaps no role in gene flow withrespect to components ofvector
thetransmissionofkala-azar.ThevariantBfound capacity provide insights into vector species
inRoyapettah,andalsoreportedfromothermajor complexes and variation within species.
endemic areas like Bihar and West Bengal, is a Hence, molecular taxonomy and
morphologically identifiable species B and is populationgeneticsstudiesareurgentlyrequired
consideredavectorspecies. toresolvethetaxonomic status ofP. argentipes,
P. argentipes is consideredtobe a species to understand the pathogenic transmission,
complex with member species differing in the epidemiology and control ofthe disease.
lengthsofthefourthantennalascoids(Lewisand
Killick-Kendrick 1973), of the labrums (Lewis Acknowledgement
1987) and in cuticular hydrocarbons (Kamhawi
et al. 1992). Recently, Ilango (1998) reported I thankthe Zoological Survey ofIndia for
differences between the specimens of support.
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OVIPOS1TIONBELIAVIOUROFTHEVISCERALLEISHMANIASISVECTOR
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