A review on Anopheles subpictus Grassi—A biological vector

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A review on Anopheles subpictus Grassi—A biological vector
  Acta Tropica  115 (2010) 142–154 Contents lists available at ScienceDirect Acta Tropica  journal homepage: www.elsevier.com/locate/actatropica Review A review on  Anopheles subpictus  Grassi—A biological vector Goutam Chandra ∗ , Indranil Bhattacharjee, Soumendranath Chatterjee Department of Zoology, Mosquito and Microbiology Research Units, Parasitology Laboratory, The University of Burdwan, Burdwan, West Bengal 713104, India a r t i c l e i n f o  Article history: Available online 11 February 2010 Keywords: Anopheles subpictus Geographical distributionSibling speciesHuman pathogensBionomicsVectorInsecticide resistanceControl a b s t r a c t  Anopheles subpictus  is a complex of four isomorphic sibling species A, B, C and D and is recognized as aprimary vector of malaria, a disease of great socio-economic importance, in Australasian Zone, Celebes,Portuguese Timor and South East Asia and a secondary vector in Sri Lanka. This species is also a vectorof some helminth and arboviruses. This species has been reported so far from nineteen countries of theOriental and Australasian Zones.  An. subpictus  complex is the most abundant anopheline in most partsof the Indian subcontinent, with a widespread distribution eastwards and southwards to Papua NewGuinea, westwards to Iran and northwards to China. Resistance to insecticide is alarming in many partsoftheworld.Differentaspectsofthisimportantmosquitospeciesincludingattemptsrelatedtoitscontrolhave been discussed which will be highly useful to carry out further research. © 2010 Elsevier B.V. All rights reserved. Contents 1. Introduction..........................................................................................................................................  143 2. Sibling species and their identification..............................................................................................................  144 3. Distribution ..........................................................................................................................................  145 4. Larval habitat.........................................................................................................................................  145 4.1. Far east........................................................................................................................................  145 4.2. India ..........................................................................................................................................  145 4.2.1. West Bengal.........................................................................................................................  145 4.2.2. Maharashtra ........................................................................................................................  145 4.2.3. Lakshadweep .......................................................................................................................  145 4.2.4. South India..........................................................................................................................  145 4.2.5. Gujrat ...............................................................................................................................  145 4.2.6. Uttar Pradesh .......................................................................................................................  145 4.2.7. Goa..................................................................................................................................  146 4.3. Sri Lanka......................................................................................................................................  146 5. Association with other anopheline species..........................................................................................................  146 5.1. India ..........................................................................................................................................  146 5.2. Indonesia .....................................................................................................................................  146 6. Bionomics ............................................................................................................................................  147 6.1. Resting habit..................................................................................................................................  147 6.1.1. India.................................................................................................................................  147 6.1.2. Indonesia............................................................................................................................  147 6.1.3. Sri Lanka ............................................................................................................................  147 6.2. Man-hour density ............................................................................................................................  147 6.2.1. India.................................................................................................................................  147 6.3. Age determination............................................................................................................................  147 ∗ Corresponding author. Tel.: +91 9434573881. E-mail address:  goutamchandra63@yahoo.co.in (G. Chandra).0001-706X/$ – see front matter  © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.actatropica.2010.02.005  G. Chandra et al. / Acta Tropica 115 (2010) 142–154  143 6.3.1. India.................................................................................................................................  147 6.4. Blood meal analysis ..........................................................................................................................  147 6.4.1. India.................................................................................................................................  147 6.4.2. Indonesia............................................................................................................................  148 6.4.3. Sri Lanka ............................................................................................................................  148 6.4.4. Vietnam, Nepal, India, Ceylon, Indonesia, Territory of Papua New Guinea........................................................  148 6.5. Man-biting habit .............................................................................................................................  148 6.5.1. India.................................................................................................................................  148 6.5.2. Sri Lanka ............................................................................................................................  148 6.6. Seasonal prevalence..........................................................................................................................  149 7. Role as vector of human pathogens..................................................................................................................  149 7.1. Role as malaria vector........................................................................................................................  149 7.1.1. Australasian zone...................................................................................................................  149 7.1.2. India.................................................................................................................................  149 7.1.3. Indonesia............................................................................................................................  149 7.1.4. Malaysia ............................................................................................................................  149 7.1.5. Maldives ............................................................................................................................  149 7.1.6. Pakistan.............................................................................................................................  149 7.1.7. Philippines..........................................................................................................................  149 7.1.8. Portuguese Timor (East Timor).....................................................................................................  150 7.1.9. Sri Lanka ............................................................................................................................  150 7.2. Role in transmission of filarial nematodes...................................................................................................  150 7.2.1. India.................................................................................................................................  150 7.2.2. Indonesia............................................................................................................................  150 7.3. Role in transmitting Japanese encephalitis virus ............................................................................................  150 7.3.1. India.................................................................................................................................  150 7.4. Role in transmitting  West Nile virus ..........................................................................................................  150 7.4.1. India.................................................................................................................................  150 8. Analysis of relationship between  An. subpictus  larval densities and environmental parameters using Remote Sensing (RS),a Global Positioning System (GPS) and a Geographic Information System (GIS) ...................................................................  150 8.1. Indonesia .....................................................................................................................................  150 9. Control strategies ....................................................................................................................................  150 9.1. Chemical based control measures............................................................................................................  150 9.2. Status of insecticide resistance...............................................................................................................  151 9.2.1. India.................................................................................................................................  151 9.2.2. Sri Lanka ............................................................................................................................  151 9.3. Non-chemical based control measures ......................................................................................................  151 9.3.1. Control by larvivorous fishes.......................................................................................................  151 9.3.2. Neem products as mosquito repellent .............................................................................................  151 9.3.3. Control by other agents.............................................................................................................  151 10. Conclusion...........................................................................................................................................  151 References ...........................................................................................................................................  151 1. Introduction  Anopheles subpictus  Grassi, 1899 (previously known as  An.rossii  Giles), having a hierarchy under Order-Diptera, Sub-order-Nematocera, Family-Culicidae, Subfamily-Anophelinae, Genus-  Anopheles  and Subgenus- Cellia , Type form available at the RomeUniversity Museum, Rome, is a wide spread species. This specieshas been reported so far from nineteen countries of the Orientaland Australasian Zones.  An. subpictus sensu lato  is the most abun-dant anopheline in most parts of the Indian subcontinent (Rao,1984), with a widespread distribution eastwards and southwardsto New Guinea (Cooper et al., 2006), westwards to Iran (Sedaghat and Harbach, 2005) and northwards to China (Riley and Yu, 1932).  An. subpictus  breeds in a variety of habitats like flowing orstagnant waters, clear or turbid waters, water with or withoutvegetation, unshaded or slightly shaded water bodies, wells, bur-row pits, channels, ponds, tanks ground pools, fallow and freshlyflooded rice fields, cement cisterns, tree holes, lake margins, freshor brackish waters etc. and the adult has a flight range of 1.5–6km(Nagpal and Sharma, 1995).  An. subpictus  complex is shown to comprise of four repro-ductively distinct species, designated as A, B, C and D, occurringsympatrically in villages of Pondicherry, southeast India. It is rec-ognized as a primary or secondary vector of malaria, a disease of great socio-economic importance, in different parts of the world(Russell and Jacob, 1939; Russell and Rao, 1940; Roy, 1943; vanHell, 1952; Russell et al., 1963; Ferreira and Breda, 1963; Reid,1968;Leinetal.,1975;Panickeretal.,1981;Kulkarni,1983;Hearthet al., 1983; Chatterjee and Chandra, 2000).  West Nile virus  hasbeen isolated from  An. subpictus  in Asia (Manson-Bahr and Bell,1991) such as in India (Habalek and Halouzka, 1999).  An. subpictus is the vector of nocturnally periodic  Wuchereria bancrofti  in Flo-res of Indonesia (Manson-Bahr and Bell, 1991). Thenmozhi et al. (2006) reported this species as a vector of Japanese encephalitisvirus (JEV) in Cuddalore, an area of Tamilnadu, India, endemic forthe disease.A review on different aspects like identification of siblingspecies,distribution,larvalhabitat,associationwithotheranophe-line species, bionomics (resting habit, man-hour density, agedetermination, blood meal analysis, man-biting habit, seasonalprevalence), role as vector of human diseases, analysis of rela-tionship between  An. subpictus  larval densities and environmentalparametersusingRemoteSensing(RS),aGlobalPositioningSystem(GPS)andaGeographicInformationSystem(GIS),controlmeasurestaken against this species including the status of insecticide resis-tance has been presented here, which is still lacking, as a readyreference on this widely distributed, highly prevalent and medi-cally important mosquito species.  144  G. Chandra et al. / Acta Tropica 115 (2010) 142–154  Table 1 Morphological, biological and cytological differences among  An. subpictus  sibling species.Species Inversions onX-chromosomeEgg Larva Pupa Adult Breeding habitatsMean ridge no.(range)Frill Seta 4M Seta 7-1 Female palpi (apicalpale band vs.sub-apical dark band)(Salinity range %)A X+ a + b 35 (31–36) Opaque 2-branched(rarely 3)Simple; as long ashairs 6 and 9Longer than Paddy fields(0.0054–0.2636)Riverine pools(0.0247–0.7827)Brack waters(0.5574–5.3554)B Xab 18 (16–20) Transparent 2-branched(rarely 3)Branched 4–5;shorter than hairs 6and 9Shorter than Brack waters(0.5574–5.3554)C Xa+ b 27 (25–29) Semitransparent 3-branched(rarely 2)Branched 2;shorter, but longerthan in sp. BEqual to Paddy fields(0.0054–0.2636)Riverine pools(0.0247–0.7827)Brack waters(0.5574–5.3554)D X+ a b 22 (21–24) Semitransparent 3-branched Branched 3;shorterEqual to Paddy fields(0.0054–0.2636)Riverine pools(0.0247–0.7827)Brack waters(0.5574–5.3554) Source : Suguna et al. (1994). 2. Sibling species and their identification  An. subpictus  complex consists of four sibling species. Based onthe morphological differences in the eggs of   An. subpictus , Reid(1966) suggested that it might be a species complex, and Suguna (1982)reportedforthefirsttimeprovidingclearevidencethatthistaxon was a complex of two sibling species, A and B. Later in duecourseoftime,thistaxonwasfoundtobeacomplexoffoursiblingspecies, A, B, C and D (Suguna et al., 1994).Differences in egg morphology and in the banding patternin polytene X-chromosome due to a paracentric inversion wereresponsiblefortheidentificationofspeciesAandB.SpeciesAwithX+ a genotype (standard arrangement) was predominant in inlandvillages while in the coastal villages species B with Xa inversionarrangement was found. Species B together with species A wasfoundintheUnionTerritoryofPondicherryinIndia(Suguna,1982).Thefoursiblingspecies,provisionallydesignatedasA,B,CandDwereidentifiedbyexaminingpolytenechromosomesfromovariesof adult females collected from the field and those from salivaryglands of larvae collected from breeding sites. Two inversions ontheX-chromosome,a,asmallinversiontowardsthetipofthechro-mosomeandb,aninversioninthemiddleofthechromosome(thissame inversion was designated as a in the earlier publication of Suguna (1982), and their combinations +a+b, ab, a+b and +ab werefound with a total absence of heterozygotes in the natural popula-tions examined. This was taken as an evidence for the recognitionof the four species (Suguna et al., 1994).InversionsonpolyteneX-chromosomearediagnosticcharactersin the identification of sibling species. The four inversion arrange-mentsobservedwere:speciesA–X+ a + b ,speciesB–Xab,species–C Xa+ b , and species – D X+ a b.Reuben and Suguna (1983) reported morphological differencesin eggs, larvae, pupae and adults between sibling species A andB. Now species C and D have also been reported within the freshwater breeding populations in Pondicherry (Suguna et al., 1994).Differencesinegg,larval,pupalandadultmorphologicalcharactersamongthefourspecieswerealsoobserved(Sugunaetal.,1994)and these are summarized in Table 1.  An. subpictus  population from villages around Delhi, India wasidentified as species A (Subbarao et al., 1988) by examining ovar- ianpolytenechromosomesofadultfemalescollectedfromthefield,followingthereportof Suguna(1982).However,theridgenumber on egg float ranged between 21 and 30. This does not correspondwith the characters of species A which has on an average 33 ridges(Suguna,1982)butcorrespondstothoseofspeciesCof Sugunaetal. (1994). Atrie (1994) reported that in the Delhi population of adult females,theapicalpalebandwaslongerthansub-apicaldarkband,which is the characteristic feature of species A. Recently, Singh etal.(2004)examinedfield-collectedadultfemalesfromSonepatdis-trict, Harayana and from their isofemale lines, eggs, larvae, pupaeand adults, for morphological characters following Suguna et al.(1994).SpeciesA,CandDwerefoundinalmostequalproportions,andnovariationwasobservedintheproportionofthethreesiblingspeciesfromfield-collectedadultsandisofemalelines.  An.subpictus breeding took place in the river bed pools in the villages.Thus, in northern India, all three fresh water breeding speciesare sympatric. In Sri Lanka, both species A and B were identified(Abhayawardana et al., 1996) based on species-specific diagnos- tic inversion genotypes reported by Suguna (1982). In Sri Lanka, species A was found to be more endophilic and seasonally moreabundant than species B (Abhayawardana et al., 1996).No studies have been reported so far on the biological char-acteristics of these four sibling species. Detection of sporozoitepositive specimens in coastal villages of Pondicherry by Panickeret al. (1981), suggests that species B may be a vector, and of thoseby Kulkarni (1983) in Bastar district, Madhya Pradesh in India and Amerasinghe et al. (1991, 1992) in an irrigation development areaof Mahawali project in Sri Lanka suggest that fresh water breedingsibling species may also be playing a role in malaria transmis-sion. In Sri Lanka, recently both species A and B were identified(Abhayawardana et al., 1996) based on species-specific diagnostic inversion genotypes suggested by Suguna (1982).Recent advances in molecular systematics have proved sim-ple and reliable methods for unambiguous species identification(Manguin et al., 2008). DNA characters have been used to identify and to reveal genetic variation of many different  G. Chandra et al. / Acta Tropica 115 (2010) 142–154  145 organisms. Different target genes such as internal transcribedspacer 2 (ITS2), cytochrome oxidase I (COI) and II (COII)have been used for species identification or genetic popula-tions in many  Anopheles  species particularly the members of the  Anopheles  complexes (Yajun et al., 2006). A modern assay has been developed by Curtis and Townson (1998) from theITS2 region of the 5.8S and 28S rDNA cistron. In GenBankdatabase, there are 9 entries of ITS2 (AF406613–AF406616,AY049004, EU847232, EF601868–EF601870) (Djadid et al., 2003);14 entries of COI (AF417711, AF222327, AY29970, AY917203,DQ310145–DQ310147, DQ310149, EU143303–EU143308); and 6entries of COII (U94314, AF417747, EF601864–EF601867) of   An.subpictus . 3. Distribution  An. subpictus s.l.  is a wide spread predominant house-frequenting mosquito species among the anophelines, reportedfrom as many as 19 countries (Table 2) including different states of India (Table 3) extending from 43 ◦ 57 ′ East to 154 ◦ 30 ′ East andfrom 53 ◦ 56 ′ North to 11 ◦ 30 ′ South. From Sri Lanka A and B siblingspecieshavebeenrecognizedandfromIndiafoursiblingspeciesA,B, C and D have been recognized and from the rest of the countriessibling species composition is not clearly known. 4. Larval habitat 4.1. Far east  Almostanytemporaryorpermanentcollectionofwater,sewagepolluted pools or brackish water were common breeding place(Covell, 1944) and its larvae were common in burrow pits, buffalo wallows, brick-pits and roof-gutters. 4.2. India4.2.1. West Bengal Timber (1935) found  An. subpictus  larvae in clean, partiallyshaded pools containing a good deal of aquatic vegetation, in shal-low, temporary collections of water and in rice fields of WesternBengal. It was also a pool breeder in Calcutta (Siddons, 1946). A studyonverticaldistributionofanophelinelarvaebasedonovitrapcollectioninmultistoriedbuildingsinCalcuttashowedthathighest  An. subpictus  larval density was achieved from the first floor (Hati,1986).During1-yearstudyperiodatmetrorailconstructionsiteinCalcutta, out of 3806 water holding spots (pockets and containers)examined, 20.6% were observed positive for mosquito larvae and  An. subpictus  was prevalent in 14.6% (115) of the occupied habi-tats (Chatterjee et al., 1988). Mean per dip density of   An. subpictus was 2.01, 0.03 and 1.40 in ponds, drains and submerged fields of Tarakeswar, where larval densities in all the breeding sites werehigher in rainy season (Chatterjee and Chandra, 2000). 4.2.2. Maharashtra BarberandRice(1938)noticeditslarvaeinthepools,springsandwells in certain places of Poona. It was the most common speciesthroughout the area of North Kanara, Bombay Presidency, espe-ciallyinthecoastalregionandtheirlarvaewerefoundinbothsalineand brackish water (Singh and Jacob, 1944). 4.2.3. Lakshadweep Roy et al. (1978) recorded the absence of anophelines in BitraIsland at the time of filarial survey in 1954, but  An. subpictus  wasfound to breed both in fresh and brackish water during surveycarried out in May 1976. 4.2.4. South India An. subpictus  breeds profusely in water collections and fallowrice fields (Dhanda and Kaul, 1980) of southern India, where the larval incidence was high throughout the year. CytotaxonomicalstudiessuggestedtheexistenceoftwodistinctsiblingspecieslikeAandBin  An.subpictus populationsincoastalareasofIndia(Suguna,1982; Reuben and Suguna, 1983). A (less saline tolerant) breed infresh water and occurs in inland as well as in coastal localities.Species B breeds in brackish water and has so far been recordedonly on the coast (Panicker et al., 1981). 4.2.5. Gujrat  Intradomestic water collections comprised 27.84%  An. subpic-tus  larvae in Kheda district (Yadav et al., 1989).  An. subpictus breeds in canal-irrigated area which included irrigation chan-nels, drains, seepage, water pools, ponds and paddy fields inKheda district. In non-canal-irrigated and riverine areas, ponds,small pools, rivers and riverbed pools were the major breed-ing sources. Wells and intradomestic water storage containersalso provided breeding opportunities through out the year. Rain-water collections also supported the breeding of   An. subpictus (Bhatt et al., 1991). Gupta et al. (1992), while studying the intradomestic mosquito breeding sources in the entire ruralNadiad Taluka of Kheda district, found that  An. subpictus  couldbreed in over head tanks, underground tanks, outside and insidetanks, earthen mud pots and also in miscellaneous containersindicating its potential and preference to breed in intradomes-tic water collections.  An. subpictus  was observed to breed inwater hyacinth infested ponds as well as weed free ponds. Inhyacinth infested ponds,  An. subpictus  was predominant duringthe summer (37.9%) and winter (29.5%) seasons, where as inweed free ponds it bred profusely during monsoon (59.2%). InNadiad Taluka 12.65%, 13.34% and 25%  An. subpictus  mosquitoeswere found in irrigation wells, draw wells and disused wells,respectively (Rajnikant Bhatt et al., 1992, 1993). According to Bhatt et al. (1993)  An. subpictus  was ubiquitous and they col-lected a total of 25,858 anopheline larvae comprising of 15species emerged from 1104 samples of immature from 9 breed-ing habitats of the non-canal area of Kheda district. Percentagesof   An. subpictus  were 72.28%, 66.82%, 86.23%, 30.64% and 52.07%in ponds, wells, rice fields, rivers and riverbed pools, respec-tively. The figures were 17.28%, 34.585%, 97.35% and 85.25% inseepage drains, swamps, borrow-pits and hoof/tyreprints, respec-tively.  An. subpictus  was the predominant species in the ricefields and the most dominant species in borrow-pits (Bhatt et al.,1993). 4.2.6. Uttar Pradesh SharmaandPrasad(1991)carriedoutstudiesonecologicalsuc-cession and association of anophelines in selected paddy fields of Dadraul PHC of Shahjahanpur district, during the paddy field cul-tivation period from June to October. Breeding of five anophelineswas observed in paddy fields. Out of the adults that emerged fromlarval collections, the percentage of   An. subpictus  was the highest.  An.subpictus breedingoccurredintheearlystageofricecultivationandstoppedbeforethebreedingof   An.nigerrimus started,i.e.nearly30 days after rice transplantation. An inverse correlation betweenlarval density of   An. subpictus  and the height of the rice plants wasobserved. Breeding of   An. subpictus  occurred during first week of  JulyandcontinuedtolastweekofAugust.Atotalof211(61.5%)  An.subpictus  larvae were collected from the paddy fields from July toAugust 1988. According to Prasad et al. (1993),  An. subpictus  couldbreed in rice fields during June to October and month wise per-centageof   An.subpictus breedinginricefieldsfromJunetoOctober1991were51.2%,29.0%,21.3%,1.3%andnil,respectivelyinShahja-  146  G. Chandra et al. / Acta Tropica 115 (2010) 142–154  Table 2 Global distribution of   An. subpictus s.l. Serial no. Country References1 Afghanistan Rao (1951), Iyengar (1954), WHO (1959), Fischer (1968), Ward (1972), WHO (2007) 2 Bangladesh Mahmud and Muhammad (1973), WHO (2007) 3 Cambodia Harrison and Klein (1975), WHO (2007) 4 China Riley and Yu (1932), WHO (2007) 5 Indonesia van Hell (1952), Sundararaman et al. (1957), Bruce Chawtt et al. (1966), WHO (2007) 6 Iran Oshaghi et al. (2004), Sedaghat and Harbach (2005), WHO (2007) 7 Maldives WHO (1976), unpublished information, WHO (2007) 8 Malaysia White (2003), WHO (2007) 9 Mariana Islands Iyengar (1955), Ward et al. (1976), WHO (2007) 10 Myanmar (Burma) Covell (1931a), Oo et al. (2004), WHO (2007) 11 Nepal Bruce Chawtt et al. (1966), WHO (2007) 12 Papua New Guinea Russell et al. (1963), Bruce Chawtt et al. (1966), Cooper et al. (2006), WHO (2007) 13 Pakistan Covell (1931a), Rahman and Muttalib (1967), WHO (2007) 14 Philippines Tiedeman (1927), Manalang (1928), WHO (2007) 15 Portuguese Timor (East Timor) Ferreira and Breda (1963), WHO (2007) 16 Sri Lanka (Ceylon) Bruce Chawtt et al. (1966), Amerasinghe et al. (1992), Abhayawardana et al. (1996), WHO (2007) 17 Thailand Scanlon et al. (1968), WHO (2007) 18 Vietnam Bruce Chawtt et al. (1966), WHO (2007) 19 India See Table 3 hanpur district  An. subpictus  was the predominant species in Juneand July in 1991. 4.2.7. Goa Kumar and Thavaselvam (1992) conducted 1-year longitudinalstudy in 9 categories of breeding habitats in Panaji. They showedthat  An. subpictus  larvae can grow with 8 other mosquito generaand species in 247 out of 747, i.e. 39.3% habitats. 4.3. Sri Lanka The seawater brought inland by the tsunami has mixed withmonsoonrainwatertoformpuddlesofvaryingsalinity.Also,thou-sandsofmuddysurfacewaterpuddleshavebeencreatedasaresultof destruction and rehabilitation activities that are already under-way. The brackish puddles are expected to favour the breeding of   An.subpictus siblingspeciesB,whichisawell-knowncoastalbreed-ingspeciesinSriLanka(Briëtetal.,2005).Immatureof   An.subpictus was recorded from all types of wells (Briët et al., 2005). In a small study in tsunami-affected areas in the east coast of Sri Lanka, Briëtet al. (2006), found that anophelines (  An. culicifacies  in wells,  An.subpictus inpoolsafterrains,  An.varuna and  An.vagus inricefields)bredindifferenttypesofhabitats.Larvalpopulationswereaffectedby rainfall, cleaning of wells as well as by chlorination and regularspraying of larvicides. 5. Association with other anopheline species 5.1. India Kant and Pandey (1999) observed a significant positive asso-ciation (without having any adverse effect) of   An. subpictus  with  An. culicifacies ,  An. annularis ,  An. paludis  and  Culex quinquefas-ciatus  in the rice agro ecosystem in Gujrat and a negativeassociation (having adverse effect) with  An. nigerrimus ,  Culex tri-taeniorhynchus  and  Culex vishnui  subgroup.  An. subpictus  larvaewere found to share one habitat with  An. stephensi ,  An. vagus and  An. barbirostris  in Panaji, Goa (Kumar and Thavaselvam,1992). 5.2. Indonesia Larvae of   An. subpictus  were collected in lagoons, rice fields,swamps and ground pools in association with  An. aconitus ,  An.  Table 3 Distribution of   An. subpictus  in different states of India.Serial no. State References1 West Bengal Covell (1931a), Iyengar (1931), Timber (1935), Puri (1948), Siddons (1946), Rao et al. (1973), Soman et al. (1976), Biswas et al. (1988), Mahapatra et al. (1991), Chandra et al. (1994), Tandon and Tandon (1994), Tandon et al. (1995), Malakar et al. (1995), Chandra (1998), Rudra and Chandra (1998), Chatterjee and Chandra (2000), Chandra et al. (2002)2 Maharashtra Covell (1931a), Barber and Rice (1938), Singh and Jacob (1944), Soman (1945) 3 Jharkhand Senior (1946)4 Tamilnadu Covell (1931a), Rajagopalan and Work (1969), Russell and Jacob (1939), Reuben (1978)5 Jammu and Kashmir Rao et al. (1973)6 Nagaland Sarkar et al. (1980)7 Gujrat Covell (1931a), Bhatt et al. (1991) 8 Uttar Pradesh Sharma and Prasad (1991), Bruce Chawtt et al. (1966) 9 Tripura Das et al. (1991)10 Rajasthan Covell (1931a), Bansal and Singh (1993) 11 Orissa Covell (1931a), Chand et al. (1993) 12 Uttaranchal Devi and Jauhari (2004), Bhat (1975), Rao et al. (1973) 13 Bihar Covell (1931a), Bruce Chawtt et al. (1966) 14 Andhra Pradesh Covell (1931a), Bruce Chawtt et al. (1966) 15 Punjab Covell (1931a)16 Madhya Pradesh Bruce Chawtt et al. (1966)17 Karnataka Bruce Chawtt et al. (1966)18 Andaman and Nicobar Islands Krishnamoorthy et al. (2005)
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