9
Transactions of the Royal Society of Tropical Medicine and Hygiene (2005) 99, 106—114 Malarial vectors in an irrigated rice cultivation area in southern Sri Lanka D.A.R. Premasiri a,b , A.R. Wickremasinghe c,, D.S. Premasiri a , N. Karunaweera d a Malaria Research Unit, Department of Parasitology, Faculty of Medicine, University of Colombo, Kynsey Road, Colombo 8, Sri Lanka b Regional Office, Anti-Malaria Campaign, Puttalam, Sri Lanka c Department of Community and Family Medicine, Faculty of Medicine, University of Kelaniya, P.O. Box 6, Ragama, Sri Lanka d Department of Parasitology, Faculty of Medicine, University of Colombo, Kynsey Road, Colombo 8, Sri Lanka Received 3 September 2003; received in revised form 20 February 2004; accepted 23 February 2004 Available online 25 September 2004 KEYWORDS Malaria; Vectors; Climate factors; Irrigation; Rice cultivation; Sri Lanka Summary Entomological surveys were carried out from March 1998 to December 1999 to study the prevalence, distribution and abundance of malarial vectors in relation to selected environmental factors and potential mosquito breeding sites in irrigation channels in 15 villages in the Lunugamvehera Irrigation and Settlement Project, a malaria-endemic area of southern Sri Lanka. Mosquito collections were made at monthly intervals using four sampling methods. Thirteen anopheline species were collected. Following monsoonal rains, anopheline breeding took place primarily in rainwater accumulations. During the inter-monsoonal period, pools formed in the irrigation system, semi-permanent pools formed as a result of rainfall and permanent ground pools were the major breeding sites of anophelines. Very little anopheline breeding took place within the irrigation channels. Amongst the seven anopheline species collected from human dwellings, Anopheles subpictus was the most prevalent, followed by A. culicifacies; together these two species comprised more than 99% of the indoor resting population. The number of days of rain was an important macro-epidemiological factor influencing the density of malarial vectors. There was no consistent trend between the amount of water released or the number of days of water release from the reservoir and the outdoor or indoor resting densities of anophelines. © 2004 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved. * Corresponding author. Tel.: +94 11 2598014; fax: +94 11 2598014. E-mail address: [email protected] (A.R. Wickremasinghe). 1. Introduction Malaria is endemic in the dry zone of Sri Lanka and continues to be a major public health 0035-9203/$ — see front matter © 2004 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.trstmh.2004.02.009

Malarial vectors in an irrigated rice cultivation area in southern Sri Lanka

Embed Size (px)

Citation preview

Page 1: Malarial vectors in an irrigated rice cultivation area in southern Sri Lanka

Transactions of the Royal Society of Tropical Medicine and Hygiene (2005) 99, 106—114

Malarial vectors in an irrigated rice cultivationarea in southern Sri Lanka

D.A.R. Premasiria,b, A.R. Wickremasinghec,∗, D.S. Premasiria,N. Karunaweerad

a Malaria Research Unit, Department of Parasitology, Faculty of Medicine, University of Colombo,Kynsey Road, Colombo 8, Sri Lankab Regional Office, Anti-Malaria Campaign, Puttalam, Sri Lankac

Department of Community and Family Medicine, Faculty of Medicine, University of Kelaniya,P.O. Box 6, Ragama, Sri Lankad Department of Parasitology, Faculty of Medicine, University of Colombo, Kynsey Road,Colombo 8, Sri Lanka

Received 3 September 2003; received in revised form 20 February 2004; accepted 23 February 2004Available online 25 September 2004

KEYWORDSMalaria;Vectors;Climate factors;Irrigation;Rice cultivation;Sri Lanka

Summary Entomological surveys were carried out from March 1998 to December1999 to study the prevalence, distribution and abundance of malarial vectors inrelation to selected environmental factors and potential mosquito breeding sitesin irrigation channels in 15 villages in the Lunugamvehera Irrigation and SettlementProject, a malaria-endemic area of southern Sri Lanka. Mosquito collections weremade at monthly intervals using four sampling methods. Thirteen anophelinespecies were collected. Following monsoonal rains, anopheline breeding took placeprimarily in rainwater accumulations. During the inter-monsoonal period, poolsformed in the irrigation system, semi-permanent pools formed as a result of rainfalland permanent ground pools were the major breeding sites of anophelines. Verylittle anopheline breeding took place within the irrigation channels. Amongst theseven anopheline species collected from human dwellings, Anopheles subpictuswas the most prevalent, followed by A. culicifacies; together these two speciescomprised more than 99% of the indoor resting population. The number of daysof rain was an important macro-epidemiological factor influencing the density ofmalarial vectors. There was no consistent trend between the amount of waterreleased or the number of days of water release from the reservoir and the outdooror indoor resting densities of anophelines.© 2004 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd.All rights reserved.

* Corresponding author. Tel.: +94 11 2598014;fax: +94 11 2598014.

E-mail address: [email protected] (A.R. Wickremasinghe).

1. Introduction

Malaria is endemic in the dry zone of Sri Lankaand continues to be a major public health

0035-9203/$ — see front matter © 200doi:10.1016/j.trstmh.2004.02.009

4 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved.

Page 2: Malarial vectors in an irrigated rice cultivation area in southern Sri Lanka

Material vectors and environmental factors 107

problem in the country (Silva, 1994). To date, 22anopheline species have been reported in Sri Lanka(Amerasinghe, 1991), and Anopheles culicifacies(Giles) was incriminated as the principal vectorof malaria in Sri Lanka during the early part ofthe twentieth century (Carter, 1930; Carter andJacocks, 1929). Until recently, A. culicifacies sib-ling species B was considered to be responsiblefor malaria transmission in Sri Lanka (Green andMiles, 1980). The detection of A. culicifacies sib-ling species E by Surendran et al. (2000) has raisedconcerns about its importance as a major vectorof malaria in the country, as reported in south India(Kar et al., 1999). Although A. culicifacies is still re-garded as the most important vector, the possibilitythat other anopheline species play a role as sec-ondary vectors or as potential vectors, dependingupon locality and seasonal abundance, also exists(Abhayawardana and Herath, 1994; Herath et al.,1983). Amerasinghe et al. (1992) reported that A.subpictus is the most abundant endophilic anophe-line which may play a role in malaria transmissionin Sri Lanka. Anopheles culicifacies and A. subpic-tus bite indoors and outdoors but the other speciesare primarily outdoor biters.

Mhisuhtppaiaattsipstd

2

2

TcS

situated in the dry zone of southern Sri Lanka(Figure 1). The population consisted of approxi-mately 14 000 villagers resident in 15 hamlets. Themajority of families owned rice fields irrigated bythe Lunugamvehera reservoir.

The village ecosystem of the area comprised anirrigation reservoir, lowland irrigated rice fields andhomesteads. Rice fields were located just below thereservoir. Irrigated water flows through a networkof canals to the paddy fields. There was a con-tinuous or intermittent water supply to the fieldsthrough the canal system, depending on the avail-ability of water in the reservoir and the stages ofgrowth of crops. Two main canals extend from thereservoir and provide water to the rice fields. ‘Dis-tributory canals’ connect the main canal to the‘field canals’ which supply the rice fields of 10 to15 farmers.

2.2. Mosquito collection

Mosquitoes were collected at monthly intervals us-ing four standard sampling methods from March1998 to December 1999.

2

Imlspcmcfofrwwk

2

Ofitlcneswe

Vector control strategies adopted by the Anti-alaria Campaign in Sri Lanka are based on restingabits of A. culicifacies and primarily involvendoor residual insecticide spraying. Larval controltrategies are directed at the primary vector alone,sing measures such as larviciding major breedingabitats (Amerasinghe, 2001). Given the recent de-ection of A. culicifacies sibling species E and otherotential vectors, knowledge of the species com-osition of anophelines is important in selectingppropriate vector control measures. Mathemat-cal models based on the correlation betweennopheline species and environmental factors suchs rainfall, temperature and humidity may be usedo forecast increases in vector abundance and,hereby, malaria epidemics. In this study, the sea-onal distribution of anopheline species was studiedn an irrigated rice cultivation area in Sri Lanka andotential vector breeding sites within the irrigationystem were identified. An attempt was madeo predict vector densities by correlating vectorensities with specific environmental factors.

. Materials and methods

.1. Study area

he study was carried out from March 1998 to De-ember 1999 in the Lunugamvehera Irrigation andettlement Project area, a malaria-endemic area

.3. Indoor resting mosquitoes

ndoor resting mosquitoes were collected, atonthly intervals, by pyrethrum spray sheet col-ections (PSC) in 120 houses, which were randomlyelected at the beginning of the study. Bedrooms,referably with complete walls, were selected andollections were made during the morning. Theovable furniture in bedrooms was removed andlean white sheets were spread on the floor andurniture. A 0.2% solution of pyrethrum in keroseneil was sprayed into the inner space of the roomrom the inside and outside at the eaves of theoom, using a hand-operated spray gun. The roomas then left closed for about 10minutes. The dooras then opened, the white sheets removed and thenocked-down mosquitoes collected using forceps.

.4. Outdoor resting mosquitoes

utdoor resting mosquitoes were collected from sixxed stations at monthly intervals by cattle-baitedrap collections (CBTC) and cattle-baited hut col-ections (CBHC). The traps were made of whiteotton drill (dimension 3m × 3m × 1.5m) withet windows (2m × 1m) on the sides. They wererected using strong poles of 2m in height, and fouride sticks of the same height. A gap of 15—25 cmas allowed between the ground and bottom of thedge of the trap for mosquito entry.

Page 3: Malarial vectors in an irrigated rice cultivation area in southern Sri Lanka

108 D.A.R. Premasiri et al.

Figure 1 Map of Sri Lanka showing the Lunugamvehera Irrigation and Settlement Project area.

A standard hut approximately 2m × 1.25m ×1.25m was constructed at each site for CBHC. Thehut was made of sticks and poles and thatched withwoven cadjan leaves. A gap of about 10—15 cm be-tween the ground and the cadjan thatched wall anda space approximately 5 cm between the roof andthe walls were left for movement of mosquitoes.A removable door made of sticks and cadjan wasfitted to facilitate movement in and out of the hut.

At sunset, a calf was guided into each trapand hut and tethered to the central pole and leftthroughout the night. The calf was removed atdawn after collecting the mosquitoes. All anophe-lines resting inside the huts and traps were col-lected using a mouth-operated aspirator and a flashtorch.

2.5. Larval collections

Immatures were collected from selected examplesof all types of breeding sites available in boththe irrigated and non-irrigated areas by dippingwhite plastic larval ladles with extensible handles(125mm diameter, 250ml capacity) into the waterto collect samples. Larvae collected during field

2.6. Species identification

All live mosquitoes collected by CBHC and CBTC,mosquitoes knocked down by PSC, and adultsemerging from larvae were identified using anachromatic magnifying lens (×10) and the tax-onomic keys prepared by Carter (1950) andAmerasinghe (1990).

2.7. Climate and irrigation data

Climate data including rainfall, temperature andrelative humidity of the study area were obtainedfrom the meteorology field station of the Depart-ment of Irrigation situated at Lunugamvehera. Theamount of water released from the reservoir andnumber of days of water release to the canal systemwere obtained from the office of the Department ofIrrigation situated in the area.

2.8. Data analysis

Vector densities were log-transformed and Pear-son’s correlation coefficients were used to inves-tigate the associations between anopheline (larvalavj<

sampling were transferred to net covered plasticwater containers at the field station and fed on lar-val food and yeast until adults emerged for speciesidentification.

nd adult) densities and irrigation data and climaticariables. Bonferroni correction was done to ad-ust P values for multiple hypothesis testing and P0.01 was considered statistically significant. The

Page 4: Malarial vectors in an irrigated rice cultivation area in southern Sri Lanka

Material vectors and environmental factors 109

feasibility of using such data in predicting vectordensity was investigated.

2.9. Ethical considerations

Ethical clearance to conduct the study was obtainedfrom the Ethical Review Committee of the Facultyof Medicine, University of Colombo, Sri Lanka. Per-mission to conduct the study was obtained from theMinistry of Health, the Southern Provincial HealthAuthority, the Anti-Malaria Campaign and the Irri-gation Department.

3. Results

From the larval collections, a total of 41 942immatures was collected from 78 107 dips and18 408 female anopheline mosquitoes representing12 species were identified at emergence as adults.Anopheles subpictus (56%) was the most abundantspecies among the larval collections. A total of69 809 adult female anopheline mosquitoes repre-senting 13 species was collected from indoor andoutdoor catches. Anopheles subpictus was the mosta(rs

3

Ae

sam

ecte

bai0 90

rainwater accumulations, followed by unprotectedwells, rock pools, stream-bed pools and marshes(Table 2). The highest density of anophelines inthe irrigated areas was found in the tank seep-ages, followed by the natural river below the dam,canal seepages, reservoir margins, non-harvestedrice fields, harvested rice fields and distributorycanals. The main canal and the field canals had thelowest density of larvae within the irrigation sys-tem.

Anopheles subpictus was the most predominantspecies found in all types of breeding sites exceptin the distributory canals and semi-protected wellswhere A. culicifacies was predominant. In the fieldcanals, A. varuna was predominant, and in marshylands, A. barbirostris was predominant. The otherfavoured breeding sites of A. culicifacies werecanal seepage pools, rainwater accumulations,unprotected wells, stream-bed pools, burrow pitsand reservoir margin pools.

3.2. Adult mosquito populations

Two peaks of indoor resting vector densities wereobserved during the year, coinciding with themlcsaHaoC

bundant anopheline species collected from CBHC67%) and indoor catches (94.5%). Anopheles niger-imus (42%) was the most abundant outdoor restingpecies collected from CBTC (Table 1).

.1. Larval collections

mong the breeding sites sampled in highland ar-as, the highest density of anophelines was found in

Table 1 Relative abundance of anopheline species byment Project area, Sri Lanka

Anopheline species Percentage of mosquitoes coll

Pyrethrum spraysheet (n = 15 765)

Cattle(n = 5

A. culicifacies 5.12 0.02A. subpictus 94.50 5.40A. annularis 0.01 0.24A. vagus 0.21 8.90A. acconitus — 0.02A. barbirostris — 0.39A. jamesii — 1.35A. nigerrimus — 42.34A. pallidus 0.01 0.55A. peditaeniatus — 39.90A. tessellatus 0.05 0.60A. varuna 0.10 0.28A. karvari — 0.01

pling technique, Lunugamvehera Irrigation and Settle-

d

ted trap0)

Cattle baited hut(n = 3144)

Larval sampling(n = 18 408)

14.98 8.2467.02 56.220.12 1.243.28 11.140.12 0.430.06 3.913.70 0.176.65 9.140.12 0.972.29 5.550.61 0.031.05 2.96— —

onsoonal rains. The outdoor resting anophe-ine population had two distinct peaks per year,orresponding to the period following the mon-oonal rains. Seasonal variations in densities ofnophelines in both PSC and CBHC were similar.owever, the peak density of outdoor restingnophelines evaluated by CBTC generally occurredne to two months later than the peaks of PSC andBHC.

Page 5: Malarial vectors in an irrigated rice cultivation area in southern Sri Lanka

110 D.A.R. Premasiri et al.

Table2

Densities

ofanophelin

elarvae

indifferentbreeding

habitats,Lunugamvehera

Irrigation

andSettlementProjectarea,SriLanka

Breeding

site

Density

(no.

oflarvae

per100dips)

A.cu

licifacies

A.subp

ictus

A.an

nularis

A.va

gus

A.acon

itus

A.ba

rbirostris

A.jamesii

A.nige

rrim

usA.pa

llidus

A.pa

ditaen

iatus

A.tesselatus

A.va

runa

Total

Maincanal

0.17

1.25

0.05

0.39

0.01

0.27

0.00

0.50

0.20

0.34

0.00

0.26

3.43

Distributorycanal

6.80

1.91

0.05

0.75

0.50

0.90

0.00

0.64

0.23

0.14

0.00

1.80

13.72

Fieldcanal

0.44

0.53

0.11

0.22

0.20

0.69

0.02

2.17

0.29

0.71

0.05

2.84

8.27

Stream

bedpool

2.99

23.20

1.22

1.22

1.09

0.88

0.00

0.07

0.07

0.00

0.14

6.67

37.55

Paddyfie

ld(non-harvested)

0.30

8.83

0.04

2.17

0.03

0.03

0.00

6.49

0.24

3.63

0.00

0.11

21.87

Paddyfie

ld(harvested)

0.60

11.74

0.00

5.03

0.02

0.33

0.06

0.67

0.00

1.57

0.00

0.13

20.16

Tank

seepagepool

0.02

36.93

0.00

9.84

0.00

0.00

0.00

0.68

0.00

0.62

0.00

0.00

48.09

Canalseepage

pool

12.38

15.10

0.00

3.58

0.00

2.99

0.09

0.77

0.32

1.68

0.00

0.09

37.01

Marsh

0.06

3.97

0.14

2.55

0.16

6.22

0.02

4.41

0.19

3.03

0.00

0.00

20.74

Burrow

pits

2.42

20.43

0.04

4.85

0.22

1.47

0.00

1.13

0.17

2.47

0.00

0.00

33.20

Spill

canalp

oolin

g1.01

37.38

0.06

5.87

0.00

0.00

0.00

0.00

0.00

0.00

0.00

0.00

44.33

Spill

canalm

arginpooling

0.00

7.77

0.00

1.17

0.00

0.87

0.00

5.44

0.58

0.78

0.00

4.08

20.68

Tank

2.29

13.03

9.41

2.98

0.00

2.02

0.80

2.77

2.98

0.00

0.00

0.00

36.28

Unprotected

well

6.93

53.07

0.06

0.74

0.00

0.12

0.37

0.68

0.00

0.50

0.00

0.62

63.10

Semi-protectedwell

15.47

7.73

0.00

0.11

0.00

5.64

0.00

0.00

0.00

0.00

0.00

3.09

32.04

Rock

pool

0.60

57.22

0.00

0.00

0.00

0.30

0.00

0.90

0.10

0.00

0.00

0.00

59.12

Rainwater

colle

ction

8.92

40.95

0.00

3.79

0.00

0.33

0.00

6.60

0.04

1.67

0.04

1.14

63.49

3.3. Climate and irrigation data

The total annual rainfall for 1998 and 1999 was771.5mm and 1018.0mm respectively. The highestrainfall was observed during the months of Novem-ber 1998 to January 1999 (Figure 2). The meanmonthly relative humidity was over 90% during thestudy period while the mean monthly temperatureranged from 26.7 to 30.8 ◦C (Figure 2).

3.4. Correlations between anophelinedensities and climate data

The outdoor resting density of all anophelines (byCBTC) was positively correlated with the numberof days of rain two months previously. Anophelesculicifacies was very rarely found in CBTC. Larvaldensities of A. culicifacies were correlated withthe number of days of rain during the currentmonth (Table 3). The outdoor resting densities ofA. subpictus (by CBTC) were positively correlatedwith the number of days of rain during the currentmonth.

3d

Lcmtdd

4

TtbirkS

ptiyaeisif

.5. Correlations between anophelineensities and water release

arval densities of A. subpictus were negativelyorrelated with the amount of water released twoonths previously (Figure 3, Table 4). There was norend in the correlations between the number ofays of water release and indoor or outdoor restingensities.

. Discussion

hirteen anopheline species were collected fromhe study area, all of which have been describedy Amarasinghe (1991). Vector incrimination stud-es under experimental and field conditions haveevealed that all the identified species, except A.arvari, may play a role in malaria transmission inri Lanka (Konradsen et al., 2000).Even though A. culicifacies is recognized as the

rincipal vector of malaria in Sri Lanka, A. subpic-us comprised 94% of the indoor resting anophelinesn the study area and was recorded throughout theear. Although A. subpictus has been reported to besecondary vector of malaria in Sri Lanka (Heratht al., 1983), it is possible that it may be play-ng a more important role in transmission in thetudy area as it is the most prevalent anophelinen intradomestic (indoor) habitats. Given the lowrequencies of other potential vectors, such as A.

Page 6: Malarial vectors in an irrigated rice cultivation area in southern Sri Lanka

Material vectors and environmental factors 111

Figure 2 Climatic details of the Lunugamvehera Irrigation and Settlement Project area, Sri Lanka.

Table 3 Correlation between anopheline density and rainfall by sampling method, Lunugamvehera Irrigation andSettlement Project area, Sri Lanka

Lag period(months)

Pearson correlation coefficient (P) between vector density and rainfall

All anophelines A. culicifacies A. subpictus

Rainfall No. of daysof rain

Rainfall No. of daysof rain

Rainfall No. of daysof rain

Pyrethrum spray sheet collection0 0.110 (0.627) 0.269 (0.227) 0.184 (0.413) 0.376 (0.085) 0.070 (0.758) 0.230 (0.304)1 −0.095 (0.684) 0.136 (0.555) 0.081 (0.728) 0.205 (0.372) −0.143 (0.536) 0.094 (0.685)2 −0.233 (0.322) −0.200 (0.398) −0.002 (0.372) −0.053 (0.825) −0.259 (0.271) −0.222 (0.348)

Cattle baited trap collection0 0.176 (0.434) 0.180 (0.424) 0.446 (0.038) 0.466 (0.029) 0.520 (0.013) 0.608* (0.003)1 0.344 (0.127) 0.415 (0.061) −0.035 (0.879) 0.083 (0.722) 0.384 (0.086) 0.493 (0.023)2 0.519 (0.019) 0.580* (0.007) −0.230 (0.330) −0.046 (0.848) −0.107 (0.652) −0.180 (0.447)

Cattle baited hut collection0 0.494 (0.019) 0.523 (0.013) 0.431 (0.045) 0.476 (0.025) 0.500 (0.018) 0.520 (0.013)1 0.343 (0.128) 0.513 (0.017) 0.253 (0.268) 0.351 (0.118) 0.257 (0.260) 0.462 (0.035)2 0.099 (0.678) 0.097 (0.684) −0.140 (0.556) −0.272 (0.246) −0.040 (0.867) −0.029 (0.902)

Larval sampling collection0 0.365 (0.094) 0.468 (0.028) 0.525 (0.012) 0.540* (0.009) 0.248 (0.266) 0.342 (0.120)1 0.108 (0.642) 0.313 (0.167) 0.102 (0.660) 0.250 (0.275) −0.154 (0.505) 0.057 (0.806)2 −0.063 (0.791) −0.133 (0.575) −0.171 (0.472) −0.206 (0.384) −0.391 (0.088) −0.380 (0.098)

∗ Significant P value after correcting for multiple comparisons.

Page 7: Malarial vectors in an irrigated rice cultivation area in southern Sri Lanka

112 D.A.R. Premasiri et al.

Figure 3 Water release patterns from the reservoir, Lunugamvehera Irrigation and Settlement Project area, Sri Lanka.Amount of water is measured in acre-feet (ac.ft).

Table 4 Correlation between anopheline density and water release in canal system by sampling method,Lunugamvehera Irrigation and Settlement Project area, Sri Lanka

Lag period(months)

Pearson correlation coefficient (P) between vector density and water release

All Anophelines A. culicifacies A. subpictus

Amount No. of daysof release

Amount No. of daysof release

Amount No. of daysof release

Pyrethrum spray sheet collection0 0.360 (0.100) 0.209 (0.352) 0.255 (0.252) 0.153 (0.496) 0.371 (0.089) 0.222 (0.322)1 −0.050 (0.829) −0.087 (0.708) −0.172 (0.455) −0.163 (0.481) −0.020 (0.931) −0.053 (0.820)2 −0.415 (0.069) −0.167 (0.483) −0.529 (0.017) −0.346 (0.135) −0.372 (0.106) −0.121 (0.612)

Cattle baited trap collection0 0.508 (0.016) 0.323 (0.143) −0.109 (0.631) −0.001 (0.997) −0.090 (0.692) 0.197 (0.380)1 0.349 (0.121) 0.133 (0.565) −0.343 (0.127) −0.443 (0.044) −0.558∗ (0.009) −0.580∗ (0.006)2 −0.137 (0.566) −0.186 (0.431) 0.286 (0.221) 0.021 (0.930) −0.781∗ (<0.001) −0.584∗ (0.007)

Cattle baited hut collection0 0.206 (0.358) −0.053 (0.816) −0.106 (0.638) −0.273 (0.219) −0.158 (0.482) −0.018 (0.938)1 −0.234 (0.307) −0.377 (0.092) −0.441 (0.045) −0.512 (0.018) −0.280 (0.220) −0.366 (0.102)2 −0.641∗ (0.002) −0.346 (0.135) −0.575∗ (0.008) −0.342 (0.140) −0.705∗ (0.001) −0.416 (0.068)

Larval sampling collection0 −0.105 (0.641) −0.327 (0.137) −0.081 (0.719) −0.224 (0.316) −0.159 (0.480) −0.346 (0.115)1 −0.297 (0.191) −0.267 (0.242) −0.314 (0.165) −0.459 (0.036) −0.250 (0.274) −0.194 (0.399)2 −0.513 (0.021) −0.141 (0.554) −0.534 (0.015) −0.194 (0.411) −0.302 (0.196) 0.036 (0.880)

∗ Significant P value after correcting for multiple comparisons.

Page 8: Malarial vectors in an irrigated rice cultivation area in southern Sri Lanka

Material vectors and environmental factors 113

varuna and A. vagus, their role in malaria transmis-sion in the area needs further investigation.

Although two peaks of indoor and outdoor restingvector densities were observed per year, the indoorresting vector densities peaked during the mon-soonal rains while outdoor resting densities peakedafter the rains. Anopholes nigerrimus and A. ped-itaeniatus, absent in indoor resting populations,comprised 82% of CBTC probably due to their ex-clusive exophilic nature.

The seasonal distribution of anophelines variesin time and space, depending upon environmen-tal conditions and availability of breeding habitats.Climatic factors, the most important being rain-fall, could affect mosquito populations. In additionto increasing the extent of vector breeding sites,rainfall modifies temperature and relative humid-ity, two important conditions affecting vector sur-vival (Pampana, 1969). Sri Lanka experiences tworainy seasons from November to January during thenortheast monsoon and from May to July duringthe southwest monsoon. Mosquito abundance in SriLanka is related to rainfall and other climatic pa-rameters (Peiris et al., 1992; Shakoor, 1990). In thisstudy, anopheline populations were more abundantdsaomo

itmTitmbtddo

i1dtmcalftl

Temperature and humidity are climatic factorsknown to influence vector density by their influ-ence on mosquito activities and longevity. It is wellknown that the rate at which a mosquito populationincreases is generally faster in warm climates thanin cold climates. Small increases in temperature atlow temperatures could have a significant effect onthe rate of development than similar changes athigher temperatures. The lack of a relationship be-tween either temperature or relative humidity andvector abundance in this study is probably due tothe very little variation in both the indices duringthe study period.

A number of components of the irrigation systemfavoured formation of breeding sites for malarialvectors. The irrigation canal system and irrigationpractices may influence the breeding of anophelinevectors by creating stagnant water pools within theirrigation system’s boundaries when water is notflowing through the system. Stagnant water bod-ies along the boundaries of canals may be createdby surface runoff and seepage during water flow.Among all mosquito breeding habitats identified inthe Lunugamvehera irrigation system, the lowestdensity of anopheline larvae were observed withintuaasvtArbampn

lttdatticwli

ssl

uring the monsoons and immediate post-monsooneasons. During the dry seasons, the anophelinebundance was relatively low. Reduced availabilityf rainfed breeding habitats and the drier climateay have beenmajor limiting factors for the growthf mosquito populations during the dry season.Larval densities of A. culicifacies correlated pos-

tively with the number of days of rainfall duringhe current month, possibly due to rainwater accu-ulations being one of its primary breeding sites.he lack of such a relationship with A. subpictuss probably due to its wide range of breeding habi-ats. Outdoor resting densities of adult anophelineosquitoes correlated significantly with the num-er of days of rain two months previously. Althoughhe associations between rainfall and vector abun-ance is inconsistent, it appears that the number ofays of rain is a better indicator than the amountf rainfall in predicting vector densities.Entomological monitoring was done in six sites

n the study area which covers an area in excess of000 km2 but monitoring of climatic variables wasone only at one meteorological station. Correla-ional analysis with climate data was done using theean vector densities for all six sites. The lack of aonsistent relationship between vector abundancend climate data may be due to data at a macroevel being used. The results might have been dif-erent if climate data were available for each en-omological monitoring site, as vector abundance isikely to depend on microepidemiological factors.

he irrigation canal system (i.e. main canal, distrib-tory canal and field canal). The highest density ofnopheline larvae was observed in seepage waterccumulations along the boundaries of the canalystem and below the reservoir dam. These poolsaried in size and retained their breeding poten-ial throughout all phases of the irrigation cycle.lthough the density of anopheline larvae in the ir-igation canal system per se was low, canal-relatedreeding sites significantly contributed to the over-ll anopheline larval density of the area. The for-ation of canal-related stagnant water bodies de-ended on the amount of water released and theumber of days of water release.Indoor resting densities of A. culicifacies corre-

ated negatively with the amount of water releasedwo months previously. A two-month lag betweenhe amount of water released and changes in theensity of adult vectors is biologically plausible,s time is needed for the vector breeding siteso become established and for actual breeding toake place. Outdoor resting species breed primarilyn non-harvested paddy fields. These species in-reased during the months in which the amount ofater released and the number of days of water re-eased were greater, possibly due to water collect-ng in the rice fields which favours vector breeding.An increase in the amount of water released re-

ulted in a decrease in larval density in the canalystem after a period of two months for all anophe-ines and A. culicifacies. Increasing the amount of

Page 9: Malarial vectors in an irrigated rice cultivation area in southern Sri Lanka

114 D.A.R. Premasiri et al.

water released appears to be effective in reduc-ing oviposition and breeding of anophelines withinthe canal system. However, water release couldalso cause a rise in the water table creating asource of still water in which malarial vectorscould breed. The results suggest that the amountof water released could be considered an impor-tant factor in predicting vector density in irrigationsystems.

Among the limitations, the inability to sampleall breeding sites and variations in local weatherconditions in the study area may have affected thevector abundance reported in this study. Mosquitocollections were done at monthly intervals andrapid changes in weather conditions and avail-ability of breeding sites within the month mayhave influenced vector densities. Environmentalconditions at the time of collection and the ef-fectiveness of malaria control interventions in thearea are other factors that may have influencedvector densities in particular habitats.

As only a few mosquito species in Sri Lanka areestablished as malarial vectors, it is important tomonitor the density of these species indoors, out-doors and in their breeding habitats throughout the

species in Sri Lanka. Proc. Sri Lanka Assoc. Adv. Sci. 50, 12(abstract).

Amerasinghe, F.P., 1990. A guide to the identification of theanopheline mosquitoes (Diptera: Culicidae) of Sri Lanka. 1Adult females. Ceylon J. Science 21, 1—16.

Amerasinghe, F.P., 1991. A catalogue of the mosquitoes (Diptera:Culicidae) of Sri Lanka. Natural Resources, Energy and Sci-ence Authority of Sri Lanka (NARESA), Colombo.

Amerasinghe, F.P., 2001. Malaria vectors in Sri Lanka. In: Klinken-berg, E. (Ed.), Proceeding of a Workshop on Malaria Risk Map-ping in Sri Lanka - Implications for its use in Control. Inter-national Water Management Institute, Colombo, pp. 20—23.

Amerasinghe, P.H., Amerasinghe, F.P., Wirtz, R.A., Indrajith,N.G., Somapala, W., Pereira, L.R., Rathnayaka, A.M.S., 1992.Malaria transmission by Anopheles subpictus (Diptera: Culici-dae) in a new Irrigation Project in Sri Lanka. J. Med. Entomol.29, 577—581.

Carter, H.F., 1930. Further observations on the transmission ofmalaria by anopheline mosquitoes in Ceylon. Ceylon J. Sci-ence (D) 4, 159—176.

Carter, H.F., 1950. Ceylon mosquitoes: list of species and namesof mosquitoes recorded from Ceylon. Ceylon J. Science (B)24, 85—115.

Carter, H.F., Jacocks, W.P., 1929. Observations on the transmis-sion of malaria by anopheline mosquitoes in Ceylon. CeylonJ. Science (D) 2, 67—86.

Green, C.A., Miles, S.J., 1980. Chromosomal evidence for siblingspecies of the malaria vector Anopheles culicifacies Giles. J.Trop. Med. Hyg. 83, 75—78.

Herath, P.R.J., Abeyawardana, T., Padmalal, U.K.G.K., 1983. A

K

K

P

P

S

S

S

year to control malaria effectively. Information onthe seasonality of mosquitoes would be useful instratifying malaria-endemic areas and optimizingcontrol operations.

Conflicts of interest statementThe authors have no conflicts of interest concerningthe work reported in this paper.

Acknowledgements

We are grateful to the Deputy Director of Irriga-tion (Southern region) and Chief Resident Engineer-Kirindioya Irrigation and Settlement Project (KOISP)for their corporation in obtaining climate and ir-rigation data. We thank the staff of the MalariaResearch Unit, Faculty of Medicine, Universityof Colombo and the Malaria Research StationKataragama for their help. This study received fi-nancial support from WHO/TDR.

References

Abhayawardana, T.A., Herath, P.R.J., 1994. Sporogonic de-velopment of Plasmodium vivax in common anopheline

study of the role of different indigenous anopheline speciesin the transmission of human malaria in Sri Lanka. Proc. SriLanka Assoc. Adv. Sci. 39, 6 (abstract).

ar, I., Subbarao, S.K., Eapen, A., Ravindran, J., Satyanarayana,T.S., Raghavendran, K., Nand, N., Sharma, V.P., 1999. Evi-dence for a new vector species E within the Anopheles culi-cifacies complex (Diptera: Culicidae). J. Med. Entomol. 36,595—600.

onradsen, F., Amerasinghe, F.P., van der Hoek, W., Ameras-inghe, P.H., 2000. Malaria in Sri Lanka: Current Knowledge onTransmission and Control. International Water ManagementInstitute, Colombo.

ampana, E., 1969. A Textbook of Malaria Eradication, seconded. Oxford University Press, London.

eiris, J.S.M., Amerasinghe, F.P., Amerasinghe, P.H., Rath-nayeke, C.B., Karunarathna, S.H.P.P., Tsai, T.F., 1992.Japanese encephalitis in Sri Lanka-the study of an epidemicvector; incrimination, porcine infection and human disease.Trans. R. Soc. Trop. Med. Hyg. 86, 307—313.

hakoor, W.K.T.M., 1990. Environmental factors determin-ing recurrent malaria epidemics in Sri Lanka. In: Ra-masamy, R. (Ed.), Current Status of Malaria Research inSri Lanka. Institute of Fundamental Studies, Kandy, pp.85—90.

ilva, K.T., 1994. Malaria eradication as a legacy of colonial dis-course: the case of Sri Lanka. Parassitologia 36, 149—163.

urendran, S.N., Abhayawardana, T.A., De Silva, B.G.D.N.K., Ra-masamy, R., Ramasamy, M.S., 2000. Anopheles culicifaciesY-chromosome dimorphism indicates sibling species (B andE) with different malaria vector potential in Sri Lanka. Med.Vet. Entomol. 14, 437—440.