The Larval Ecology of Aedes aegypti and Ae. albopictus in Three Topographical Areas of Southern Thailand Warabhorn Preechaporn, Mullica Jaroensutasinee and Krisanadej Jaroensutasinee Computational Science Graduate Program, School of Science, Walailak University, Thasala, Nakhon Si Thammarat 80161, Thailand
Abstract This study investigated the prevalence of Aedes aegypti and Ae. albopictus larvae in three topographical areas (i.e. mangrove, rice paddy and mountainous areas). Samples were collected from 300 households in nine districts. Ae. aegypti and Ae. albopictus were found in 17 out of 26 types of water containers in mangrove, rice paddy and mountainous areas. Ae. aegypti and Ae. albopictus laid eggs in different container types depending on topographical areas. Ae. aegypti larvae were found most in preserved areca jars in mangrove and mountainous areas and in banana trees in rice paddy areas. Ae. albopictus larvae were found most in preserved areca jars in mangrove areas, in plant axils in rice paddy areas and in metal boxes in mountainous areas. Ae. albopictus larval indices were higher than Ae. aegypti larval indices in all three topographical areas. House index (HI) and Breteau index (BI) were not different in the three topographical areas but different between mosquito species. HI for both Ae. aegypti and Ae. albopictus in all three topographical areas were greater than 10%, which indicated high risk of DHF transmission in these areas. Keywords: Aedes aegypti, Aedes albopictus, topography, container index, house index, Breteau index, southern Thailand.
Introduction The dengue vectors in southern Thailand are primarily Aedes aegypti and Ae. albopictus.[1,2] An epidemic of dengue haemorrhagic fever (DHF) occurred in southern Thailand (e.g. Samui Island in 1966 and 1967[3]) where Ae. aegypti and Ae. albopictus were abundant and widespread.[4] In Thailand, Ae. albopictus has been found in forested habitats ranging in elevation from 450 m to 1800 m as well as in a variety of other habitats in rural and suburban areas.[1,5,6,7] Ae. albopictus is capable of breeding in a wide range of container types and waterholding containers. General breeding sites, such jmullica@wu.ac.th
as tree holds, coconut shells, fruit peels, water jars, unused and discarded tyres, and old boats or cars holding water have been found to contain Ae. albopictus larvae.[4] Key breeding sites (i.e. the most abundant larval habitats) of Ae. aegypti are cement tanks, and earthen jars inside and outside dwellings.[8-10] Despite the fact that Ae. albopictus is expanding its distribution throughout the world,[11-13] little is known about the preferred sites of Ae. albopictus. Previous studies report that Ae. albopictus is capable of breeding in small aquatic sites such as tree holes in forested habitats as well as in a variety of other habitats in rural and suburban areas.[9,10,14-16] Vector
204
Dengue Bulletin – Volume 30, 2006
The Larval Ecology of Aedes aegypti and Ae. albopictus in Southern Thailand
factors comprise of mosquito density, behaviour, vectorial competency, food level, duration of development, size at emergence, flight range, survival and biting activity.[17-19] Since preventive actions are an important part of the control strategy, topographical factors that influence breeding sites of Ae. aegypti and Ae. albopictus larvae need to be investigated.[5,6] Nakhon Si Thammarat province is located in southern Thailand (Figure 1). Since 1984, there have been several cyclic DHF outbreaks in this area, especially in 1990 when a large outbreak occurred. After that, there was a decline but DHF reappeared again in 1998 and in 2002.[20] The number of deaths in Nakhon Si Thammarat was the highest in Thailand in
the year 2002 (i.e. 6603 DHF cases reported or 631.40 cases per 100 000 people and the fatality rate was 0.92).[21] This study aimed to examine the effect of topography on key breeding sites of Ae. aegypti and Ae. albopictus.
Materials and methods Data collection Aedes survey was conducted in Nakhon Si Thammarat province located 8° 32’ 16.5” N latitude and 99° 56’ 50.7” E longitude in AprilMay 2006 covering three topographical areas (i.e. mangrove, rice paddy and mountainous areas) (Figure 1). Samples were collected in households from all sub-districts in nine districts
Figure 1: (a) Map of Thailand. (b) Map of 3 topographical areas: mangrove, rice paddy and mountainous areas (a) Thailand (b) Nakhon Si Thammarat
12345 12345 12345 mangrove 12345 12345 12345 rice paddy 12345 12345 12345
12345 12345 mountainous 12345 12345 areas
Dengue Bulletin – Volume 30, 2006
205
The Larval Ecology of Aedes aegypti and Ae. albopictus in Southern Thailand
using stratified simple random sampling. Topography was assigned as stratums. There were 100 households per topographical area with a total of 300 households in this study.
Entomological studies All water containers were sampled for mosquito larvae, both indoors and outdoors, within 15 m of the houses using fishnets.[22] Very small water containers were emptied through the fishnet. Larger water containers were sampled by dipping the net in the water, starting at the top of the container and continuing to the bottom in a swirling motion that sampled all edges of the container.[10,15] All live mosquito larvae were collected in plastic bags, taken to the laboratory, preserved and identified up to species level using Rattanarithikul and Panthusiri’s[23] keys. In this study, the first, second instars and pupae were discarded because immature mosquitoes at these stages could not be identified. There were a total of 26 container categories in this study. Plastic water containers were divided into two categories: large plastic containers used for water storage (>100 L) and plastic bottles (i.e. 0.5–2.0 L water bottle). Earthen jars were classified into two categories: small earthen jars with a volume of ≤100 L and large earthen jars with a volume of >100 L. Three larval indices (i.e. house index (HI), container index (CI) and Breteau index (BI)) were worked out as per standard WHO guidelines.
types of water containers were compared using independent sampled t-tests. The number of positive containers, the number of households that had positive containers and the number of Ae. aegypti and Ae. albopictus larvae in the three topographical areas were analysed using one-way ANOVA tests and Post-hoc tests with Bonferroni adjustment. The larval indices were compared between topographical areas, mosquito types and the interaction between topographical areas and mosquito types using chi-square tests. All significant tests were twotailed.
Results Households that had water containers For indoor containers, the mangrove areas had the highest number of houses that had large earthen jars and cement tanks but the lowest number of houses that had plastic containers, refrigerators with plates and vases (Table 1). For outdoor containers, the mangrove areas had the highest number of houses that had small earthen jars but the lowest number of houses that had cement tanks and old cars/boats and included dry water containers at the time of inspection in data analysis (Table 1).
Ae. aegypti and Ae. albopictus larvae From three topographical areas, Ae. aegypti larvae were found in 13 out of 26 types of water containers, Ae. albopictus larvae were found in 15 out of 26 types of water containers and both Aedes sp. larvae were found in 11 out of 26 types of water containers (Table 2). For indoor containers, Ae. aegypti larvae were found in three types of water containers: antguards, cement tanks and plastic containers. From these three types of indoor containers, Ae. aegypti larvae were found most in ant-guards
Statistical analysis All variables were tested for normality using the Komogorov-Smirnov test. The equality of variances was evaluated using Levene’s test. Descriptive statistics of the data were analysed. The numbers of mosquito larvae in different
206
Dengue Bulletin – Volume 30, 2006
The Larval Ecology of Aedes aegypti and Ae. albopictus in Southern Thailand
Table 1. The number of households ( X ± SD ) that had indoor/outdoor water containers in three topographical areas: mangrove, rice paddy and mountainous areas (*P<0.05, **P<0.01, ***P<0.001) Container types Mangrove Indoor Small earthen jars Large earthen jars Cement tanks Plastic containers Refrigerators with plates Vases Ant-guards Water plant pots Outdoor Small earthen jars Large earthen jars Cement tanks Old cars/boats Coconut shells Plastic bottles Metal boxes Plant pots Plastic containers Used cans Discarded tyres Plant axils Animal pans Preserved areca jars Areca husks Banana trees Tree holes Bamboo clumps 0.62±0.49 0.73±0.45 0.02±0.14 0.00±0.00 0.17±0.38 0.06±0.24 0.51±0.50 0.26±0.44 0.39±0.49 0.10±0.30 0.21±0.41 0.01±0.10 0.24±0.43 0.11±0.31 0.07±0.26 0.03±0.17 0.00±0.00 0.02±0.14 0.35±0.48 0.76±0.43 0.25±0.83 0.01±0.10 0.26±0.44 0.15±0.36 0.46±0.50 0.13±0.42 0.42±0.55 0.08±0.27 0.33±0.47 0.03±0.17 0.24±0.43 0.08±0.27 0.06±0.28 0.16±0.58 0.02±0.14 0.01±0.10 0.49±0.50 0.75±0.44 0.02±0.14 0.06±0.24 0.30±0.46 0.09±0.29 0.45±0.50 0.18±0.39 0.32±0.49 0.12±0.33 0.25±0.44 0.01±0.10 0.18±0.39 0.15±0.36 0.05±0.22 0.09±0.29 0.01±0.10 0.02±0.14 F2,297 = 7.595** F2,297 = 0.122 F2,297 = 7.207** F2,297 = 4.629** F2,297 = 2.423 F2,297 = 2.347 F2,297 = 0.412 F2,297 = 2.489 F2,297 = 1.004 F2,297 = 0.441 F2,297 = 1.930 F2,297 = 0.810 F2,297 = 0.696 F2,297 = 1.225 F2,297 = 0.157 F2,297 = 2.823 F2,297 = 1.007 F2,297 = 0.202 207
The number of households ( X ± SD ) Rice paddy Mountainous Statistical test
0.19±0.39 0.26±0.44 0.67±0.47 0.38±0.49 0.00±0.00 0.10±0.30 0.39±0.49 0.01±0.10
0.20±0.40 0.04±0.24 0.41±0.49 0.54±0.50 0.06±0.24 0.23±0.42 0.47±0.50 0.00±0.00
0.14±0.35 0.02±0.22 0.29±0.46 0.59±0.49 0.01±0.10 0.12±0.33 0.31±0.47 0.02±0.14
F2,297 = 0.707 F2,297 = 16.737*** F2,297 = 16.754*** F2,297 = 4.923** F2,297 = 4.629** F2,297 = 3.905* F2,297 = 2.712 F2,297 = 1.007
Dengue Bulletin – Volume 30, 2006
The Larval Ecology of Aedes aegypti and Ae. albopictus in Southern Thailand
Table 2: Aedes larval occurrence in both indoor and outdoor containers (X) represents present, and (–) represents absent. Container types Ae. aegypti Indoor Small earthen jars Large earthen jars Cement tanks Plastic containers Refrigerators with plates Vases Ant-guards Water plant pots Outdoor Small earthen jars Large earthen jars Cement tanks Old cars/boats Coconut shells Plastic bottles Metal boxes Plant pots Plastic containers Used cans Discarded tyres Plant axils Animal pans Preserved areca jars Areca husks Banana trees Tree holes Bamboo clumps X X – – – – X X X X X – X X – X – – X X – – X X X X X X X X X X X – – – X X – – – – X X X X X – X X – – – – – – X X – – X – – – X X – – – – – – X X – – – – Aedes larval occurrence Ae. albopictus Both species
208
Dengue Bulletin – Volume 30, 2006
The Larval Ecology of Aedes aegypti and Ae. albopictus in Southern Thailand
in rice paddy areas (Figure 2a). For outdoor containers, Ae. aegypti larvae were found in 10 out of 26 types of water containers and found most in banana trees in rice paddy areas (Figure 2a). Ae. aegypti laid eggs in different
container types depending on topographical areas (Figure 2a). Ae. aegypti larvae were found most in preserved areca jars in mangrove and mountainous areas and in banana trees in rice paddy areas (Figure 2a).
Figure 2: The number of Aedes larvae in containers (mean±S.E.) (a) Ae. aegypti and (b) Ae. albopictus positive container. *P<0.05, AG = ant-guard, CT = cement tank, PC = plastic container, AH = areca husk, AP = animal pan, BT = banana tree, CS = coconut shell, DT = discarded tyre, LEJ = large earthen jar, MB = metal box, PB = plastic bottle, PJ = preserved areca jar, PP = plant plate, PPO = plant pot, SEJ = small earthen jar, UC = used can (a)
mangrove rice paddy mountainous area
(b)
Dengue Bulletin – Volume 30, 2006
209
The Larval Ecology of Aedes aegypti and Ae. albopictus in Southern Thailand
For indoor containers, Ae. albopictus larvae were found in two types of water containers: cement tanks and plastic containers (Figure 2b). From these two types of indoor containers, the most Ae. albopictus larvae were found in cement tanks in mountainous areas (Figure 2b). For outdoor containers, Ae. albopictus larvae were found in 13 out of 26 types of water containers and found most in preserved areca jars in mangrove areas (Figure 2b). Ae. albopictus laid eggs in different container types depending on topographical areas (Figure 2b). Ae. albopictus larvae were found most in preserved areca jars in mangrove areas, in plant plates in rice paddy areas and in metal boxes in mountainous areas (Figure 2b). The number of positive metal boxes differed between rice paddy and mountainous areas (Figure 2b).
HI for Ae. albopictus was higher than HI for Ae. aegypti (chi-square: topographical areas: χ2 =1.661, ns; mosquito species:χ2 =33.497, 2 1 P<0.001, Table 3). There was no interaction between topographical areas and mosquito species in HI (chi-square:χ2 =2.364, ns, Table 2 3). BI was not different in three topographical areas but BI for Ae. albopictus was higher than BI for Ae. aegypti (chi-square: topographical areas: χ 22 =0.670, ns; mosquito species:χ2 =39.628, P <0.001, Table 3). There 1 was an interaction between topographical areas and mosquito species in BI (chisquare:χ2 =6.759, P<0.05, Table 3). 2
Discussion Our results support previous findings that Ae. aegypti and Ae. albopictus may have different key breeding sites from one area to another.[10,24] This study clearly demonstrates that Ae. aegypti and Ae. albopictus laid eggs in different container types depending on topographical types. Phong and Nam[23] studied Aedes larval occurrence in Viet Nam and found
Larval indices All Ae. albopictus larval indices were higher than Ae. aegypti larval indices in all the three topographical areas (Table 3). HI was not different in the three topographical areas but
Table 3: The number of households and containers, and larvae indices in mangrove, rice paddy and mountainous areas Mangrove area Ae. aegypti No. of households No. of positive households No. of containers No. of positive containers Larval index HI (%) CI (%) BI 13 0.76 14 39 2.54 47 21 1.78 24 38 2.75 37 16 1.55 14 50 6.09 55 55 13 1847 14 Ae. albopictus 55 39 1847 47 Rice paddy area Ae. aegypti 56 21 1347 24 Ae. albopictus 56 38 1347 37 Mountainous area Ae. aegypti 67 16 903 14 Ae. albopictus 67 50 903 55
210
Dengue Bulletin – Volume 30, 2006
The Larval Ecology of Aedes aegypti and Ae. albopictus in Southern Thailand
that Ae. aegypti larvae were mostly found in drums, jars, concrete tanks and discarded objects. On the other hand, Ae. albopictus larvae were mainly found in jars and discarded objects. Wongkoon et al.[10] studied Aedes larval occurrence in Nakhon Si Thammarat, Thailand, and found Ae. aegypti and Ae. albopictus larvae in six water storage containers including pot plants, animal pans, tyres, small water jars, bathroom tanks and concrete tanks. They found that from these six containers, there were a higher number of Ae. aegypti larvae in water containers in bathrooms and concrete tanks than Ae. albopictus.[10] Our results supported previous findings and showed that the key breeding sites of Ae. aegypti were preserved areca jars in mangrove and mountainous areas and in banana trees in rice paddy areas. The key breeding sites of Ae. albopictus were preserved areca jars in mangrove areas, in plant axils in rice paddy areas and in metal boxes in mountainous areas. We found more Aedes larvae in preserved areca jars, banana trees and decay products, which are a signal of good food in terms of quality and quantity and are known to attract ovipositioning females.[24-26] The establishment and spread of Ae. albopictus was associated with a reduction in the abundance and range of Ae. aegypti.[27-30] Ae. albopictus larvae are superior to those of Ae. aegypti in growth and survivorship under conditions of intra- and inter-specific competition in the presence of limiting litter-based resources.[31-33] From our larval survey, we found that all Ae. albopictus larval indices were higher than Ae. aegypti larval indices. This lower number of Ae. aegypti larvae may be because Ae. aegypti tends to disseminate eggs from the same batch among several containers[34-37] and tends to avoid ovipositing in containers that already have larvae from the same female or those of conspecifics.[35] Ae. aegypti females exhibit this strategy to benefit their offspring by decreasing sibling competition and distributing
risk. However, it is counter-intuitive from the perspective of adult survival and conservation of energy reserves. In addition, our results suggest that Ae. albopictus establishes well and in greater numbers than Ae. aegypti in all three topographical areas, especially in mountainous areas. Most Ae. albopictus larvae were found in artificial outdoor containers in the mountainous areas. These results support previous studies that Ae. albopictus inhabits forest areas.[7,9,10,13,15] There were many suitable oviposition sites located within houses in Thailand. Kittayapong and Strickman[11] found that the infestation of indoor containers by Ae. aegypti was greater than outdoor containers. Our results confirm this previous finding that Ae. aegypti larvae were found in a higher number of indoor containers than Ae. albopictus larvae. Many studies have demonstrated that Ae. aegypti rest indoors,[38,39] feed indoors[40] and oviposit indoors.[14] Larval surveillance during this study was important to find out the extent of prevalence of vectors in a locality. The HI in all topographical areas and two Aedes species were higher than the WHO standard for high DHF risk areas (i.e. 10% HI).
Acknowledgements We thank David Harding and two anonymous referees for comments on the previous versions of this manuscript. We also thank Suriyo Chujun, Wirote Ritthathorn and his team at the Vector-Borne Disease Control Center 11.2, Nakhon Si Thammarat, for mosquito larval identification for this study. Special thanks for invaluable help during field surveys and data analysis are offered to Wacharapong Srisang, Jirawat Saetan, and five students from Yuthin Bamrung School. This project was supported by CX-KURUE, the Institute of Research and Development, Walailak University.
Dengue Bulletin – Volume 30, 2006
211
The Larval Ecology of Aedes aegypti and Ae. albopictus in Southern Thailand
References [1] Thavara U, Tawatsin A, Phan-Urai P , Ngamsuk W, Chansang C, Liu M, Li Z. Dengue vector mosquitoes at a tourist attraction, Ko Samui, in 1995. Southeast Asian J Trop Med Public Health 1996 Mar;27(1):160-3. [2] Luemoh A, McNeil D, Kuming M. Water consumption and distribution of dengue larvae in Pattani villages. Songklanakarind Med J 2003;21(3):209-16. [3] Winter PE, Yuill TM, Udomsakdi S, Gould D, Nantapanich S, Russel PK. An insular outbreak of dengue haemorrhagic fever. I. Epidemiologic observations. Am J Trop Med Hyg 1968 Jul;17(4):590-9. [4] Thavara U, Tawatsin A, Chompoosri J. Evaluation of attractants and egg-laying substrate preference for oviposition by Aedes albopictus (Diptera: Culicidae). J Vector Ecol 2004 Jun;29(1):66-72. [5] Thavara U, Tawatsin A, Chansang C, Kongngamsuk W, Paosriwong S, Boon-Long J, Rongsriyam Y, Komalamisra N. Larval occurrence, oviposition behavior and biting activity of potential mosquito vectors of dengue on Samui Island, Thailand. J Vector Ecol 2001 Dec;26(2):172-80. [6] Gould DJ, Mount GA, Scanlon JE, Ford HR, Sullivan MF. Ecology and control of dengue vectors on an island in the Gulf of Thailand. J Med Entomol 1970 Aug 25;7(4):499-508. [7] Scanlon JE, Esah S. Distribution in altitude of mosquitoes in northern Thailand. Mosquito News 1965;25:137-44. [8] Ansari MA, Razdan RK. Seasonal prevalence of Aedes aegypti in five localities of Delhi, India. Dengue Bulletin 1998;22:28-32. [9] Dieng H, Mwandawiro C, Boots M, Morales R, Satho T, Tuno N, Tsuda Y, Takagi M. Leaf litter decay process and the growth performance of Aedes albopictus larvae (Diptera: Culicidae). J Vector Ecol 2002 Jun;27(1):31-8. [10] Wongkoon S, Jaroensutasinee M, Jaroensutasinee K. Larval infestation of Aedes aegypti and Ae. albopictus in Nakhon Si Thammarat, Thailand. Dengue Bulletin 2005;29:169-75. [11] Kittayapong P , Strickman D. Distribution of container-inhabiting Aedes larvae (Diptera: Culicidae) at a dengue focus in Thailand. J Med Entomol 1993 May;30(3):601-6. [12] Rai KS. Aedes albopictus in the Americas. Annu Rev Entomol 1991;36:459-84. [13] Reiter P . Aedes albopictus and the world trade in used tires, 1988-1995: the shape of things to come? J Am Mosq Control Assoc 1998 Mar;14(1):83-94. [14] Makiya K. Population dynamics of larvae overwintering in southern Japan. Japn J Sanit Zool 1968;19:223-9. [15] Eshita Y, Kurihara T. Studies on the habitats of Aedes albopictus , Aedes riversi in the Southwestern part of Japan. Japn J Sanit Zool 1978;30:181-6. [16] Hawley WA. The biology of Aedes albopictus. J Am Mosq Control Assoc Suppl 1988 Dec;1:1-39. [17] Hoeck PA, Ramberg FB, Merrill SA, Moll C, Hagedorn HH. Population and parity levels of Aedes aegypti collected in Tucson. J Vector Ecol 2003 Jun;28(1):65-73. [18] McBride WJH, Ohmann HB. Dengue viral infections; pathogenesis and epidemiology. Microbes Infection 2000;2:1041-50. [19] Rigau-Perez JG, Clark GG, Gubler DJ, Reiter P , Sanders EJ, Vorndam AV. Dengue and dengue haemorrhagic fever. Lancet 1998 Sep 19;352(9132):971-7. [20] Nakhon Si Thammarat Provincial Health Office. The situation of dengue incidence in Nakhon Si Thammarat, 2002, Ministry of Public Health, Bangkok, Thailand.
212
Dengue Bulletin – Volume 30, 2006
The Larval Ecology of Aedes aegypti and Ae. albopictus in Southern Thailand
[21] Bureau of Epidemiology. The surveillance of dengue haemorrhagic fever, the first fifteen order of Thailand, 2002, Office of Dengue Control. [22] Rattanarithikul R, Panthusiri P . Illustrated keys to the medically important mosquitoes of Thailand. Southeast Asian J Trop Med Public Health 1994;25 Suppl 1:1-66. [23] Phong TV, Nam VS. Key breeding sites of dengue vectors in Hanoi, Vietnam, 19941997. Dengue Bull 1999;23:67-72. [24] Wilton DP . Oviposition site selection by the tree-hole mosquito, Aedes triseriatus (Say). J Med Entomol 1968 Jun 10;5(2):189-94. [25] Beehler J, Lohr S, Defoliart G. Factors influencing oviposition in Aedes triseriatus (Diptera: Culicidae). Great Lakes Entomol 1992;25:259-64. [26] Paradise CJ, Kuhn KL. Interactive effects of pH and leaf litter on a shredder, the scirtid beetle, Helodes pulchella , inhabiting tree-holes. Freshwater Biol 1999;41:43-9. [27] Hobbs JH, Hughes EA, Eichold BH. Replacement of Aedes aegypti by Ae. albopictus in Mobile, Alabama. J Am Mosq Control Assoc 1991 Sep;7(3):488-9. [28] Mekuria Y, Hyatt MG. Aedes albopictus in South Carolina. J Am Mosq Control Assoc 1995;5:399-414. [29] Nasci RS, Hare SG, Willis FS. Interspecific mating between Louisiana strains of Aedes albopictus and Aedes aegypti in the field and the laboratory. J Am Mosq Control Assoc 1989 Sep;5(3):416-21. [30] O’Meara GF, Evans LF Jr, Gettman AD, Cuda JP . Spread of Aedes albopictus and declines of Ae. aegypti (Diptera: Culicidae) in Florida. J Med Entomol 1995 Jul;32(4):554-62. [31] Barrera R. Competition and resistance to starvation in larvae of container-inhabiting mosquitoes. Ecol Entomol 1996;21:117-27.
[32] Juliano SA. 1998. Species introduction and replacement among mosquitoes: interspecific resource competition or apparent competition? Ecology 1991;79:255-68. [33] Daugherty MP, Alto BW, Juliano SA. Invertebrate carcasses as a resource for competing Aedes albopictus and Aedes aegypti (Diptera: Culicidae). J Med Entomol 2000 May;37(3):364-72. [34] Fay RW, Perry AS. Laboratory studies of ovipositional preferences of Aedes aegypti. Mosq News 1965;25:276-81. [35] Chadee DD, Corbet PS, Greenwood JJD. Egglaying yellow fever mosquitoes avoid sites containing eggs laid by themselves or by conspecifics. Entomol Exp Appl 1990;57:295-8. [36] Corbet PS, Chadee DD. An improved method for detecting substrate preferences shown by mosquitoes that exhibit ‘skip oviposition’. Phys Entomol 1993;18:114-8. [37] Chadee DD. Effects of forced egg-retention on the oviposition patterns of female Aedes aegypti (Diptera: Culicidae). Bull Entomol Res 1997;87:649-51. [38] Reiter P , Gubler DJ. Surveillance and control of urban vectors. In: DJ Gubler, G Kuno, editors. Dengue and dengue hemorrhagic fever. New York: CAB; 1997. p. 425-62. [39] Scott TW, Amerasinghe PH, Morrison AC, Lorenz LH, Clark GG, Reiter P , Strickman D, Kittayapong P , Edman JD. Longitudinal studies of Aedes aegypti (Diptera: Culicidae) in Thailand and Puerto Rico: blood feeding frequency. J Med Entomol. 2000 Jan;37(1):89101. [40] Russell PK, Gould DJ, Yuill TM, Nisalak A, Winter PE. Short report: dispersal of Aedes aegypti in an urban area after blood feeding as demonstrated by rubidium marked eggs. Am J Trop Med Hyg 1969;18:580-3.
Dengue Bulletin – Volume 30, 2006
213