Diversity of Anopheles species and trophic behavior of putative malaria vectors in two malaria endemic areas of northwestern Thailand

Journal of Vector Ecology

Volumn 39, Issue 2, 2014, Pages 424-436

  Tainchum, Krajana ^a   Ritthison, Wanapa ^a   Chuaycharoensuk, Thipwara ^a   Bangs, Michael J ^a,b   Manguin, Sylvie ^c   Chareonviriyaphap, Theeraphap ^a  

^a KASETSART UNIVERSITY   (Thailand)

^b Public Health and Malaria Control Department Papua   (Indonesia)

^c INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Anopheles dirus; Anopheles maculatus; Anopheles minimus; Malaria; Species complexes; Thailand

Indexed keywords

ANOPHELES DIRUS; ANOPHELES MACULATUS; ANOPHELES MINIMUS;

ANIMAL; ANOPHELES; CLASSIFICATION; DISEASE CARRIER; GENETICS; MALARIA; PHYSIOLOGY; THAILAND; TRANSMISSION;

ANIMALS; ANOPHELES; INSECT VECTORS; MALARIA; THAILAND;

EID: 84909949572     PISSN: 10811710     EISSN: 19487134     Source Type: Journal    
DOI: 10.3376/i1081-1710-39-424     Document Type: Article

References (64)

1. Apiwathnasor, C., S. Prommongkol, Y. Samung, D. Limrat, and B. Rojruthai. 2002. Potential for Anopheles campestris (Diptera: Culicidae) to transmit malaria parasites in Pa Rai subdistrict (Aranyaprathet, Sa Kaeo Province), Thailand. J. Med. Entomol. 39: 583-586.
2. Baimai, V., C.A. Green, R.G. Andre, B.A. Harrison, and E.L. Peyton. 1984. Cytogenetic studies of some species complexes of Anopheles in Thailand and Southeast Asia. Southeast Asian J. Trop. Med. Publ. Hlth. 15: 536-456.
3. Baimai, V., R.E. Harbach, and U. Kijchalao. 1988. Cytogenetic evidence for a fifth species within the taxon Anopheles dirus in Thailand. J. Am. Mosq. Contr. Assoc. 4: 333-338.
4. Baimai, V. 1989. Speciation and species complexes of the Anopheles malaria vectors in Thailand, pp. 146-162, Third Conference on Malaria Research. Malaria Division, Department of Communicable Disease Control, Ministry of Public Health, Thailand.
5. Bhumiratana, A., B. Wattanakull, S. Koyadun, S. Suvannadabba, J. Rojanapremsuk, and W. Tantiwattanasup. 2002. Relationship between male hydrocele and infection prevalences in clustered communities with uncertain transmission of Wuchereria bancrofti on the Thailand-Myanmar border. Southeast Asian J. Trop. Med. Publ. Hlth. 33: 7-17.
6. Bhumiratana, A., S. Koyadun, M. Srisuphanunt, P. Border and imported bancroftian filariases: baseline seroprevalence in sentinel populations exposed to infections with Wuchereria bancrofti and concomitant HIV at the start of diethylcarbamazine mass treatment in Thailand. Southeast Asian J. Trop. Med. Publ. Hlth. 36: 390-407.
7. Bhumiratana, A., A. Intarapuk, P. Sorosjinda-Nunthawarasilp, P. Maneekan, and S. Koyadun. 2013. Border malaria associated with multidrug resistance on Thailand-Myanmar and Thailand-Cambodia borders: transmission dynamic, vulnerability, and surveillance. Biomed. Res. Int. 2013: 363417.
8. BVBD. 2013. Annual report 2013 pp. 143, Malaria situation 2013. Bureau of Vector Borne Disease, Department of Disease Control, Ministry of Public Health, Nonthaburi.
9. Chareonviriyaphap, T., S. Sungvornyothin, S. Ratanatham, and A. Prabaripai. 2001. Insecticide-induced behavioral responses of Anopheles minimus, a malaria vector in Thailand. J. Am. Mosq. Contr. Assoc. 17: 13-22.
10. Chareonviriyaphap, T., A. Prabaripai, M. J. Bangs, and B. Aum-Aung. 2003. Seasonal abundance and blood feeding activity of Anopheles minimus Theobald (Diptera: Culicidae) in Thailand. J. Med. Entomol. 40: 876-881.
11. Corbel, V., F. Nosten, K. Thanispong, C. Luxemburger, M. Kongmee, and T. Chareonviriyaphap. 2013. Challenges and prospects for dengue and malaria control in Thailand, Southeast Asia. Trends Parasitol. 29: 623-633.
12. Divis, P.C., S.E. Shokoples, B. Singh, and S.K. Yanow. 2010. A TaqMan real-time PCR assay for the detection and quantitation of Plasmodium knowlesi. Malar. J. 9: 344.
13. Dusfour, I., J.R. Michaux, R.E. Harbach, and S. Manguin. 2007. Speciation and phylogeography of the Southeast Asian Anopheles sundaicus complex. Infect. Genet. Evol. 7: 484-493.
14. Eamkum, P., S. Sungvornyothin, O. Kritpetcharat, J. Daduang, U. Lek-Uthai, L. Charerntanyarak, and P. Kritpetcharat. 2014. A single-round multiplex PCR assay for the identification of Anopheles minimus related species infected with Plasmodium falciparum and Plasmodium vivax. Parasitol. Int. 63: 442-449.
15. Garros, C., L. L. Koekemoer, M. Coetzee, M. Coosemans, and S. Manguin. 2004. A single multiplex assay to identify major malaria vectors within the African Anopheles funestus and the Oriental An. minimus groups. Am. J. Trop. Med. Hyg. 70: 583-590.
16. Gingrich, J. B., A. Weatherhead, J. Sattabongkot, C. Pilakasiri, and R. A. Wirtz. 1990. Hyperendemic malaria in a Thai village: dependence of year-round transmission on focal and seasonally circumscribed mosquito (Diptera: Culicidae) habitats. J. Med. Entomol. 27: 1016-1026.
17. Gould, D. J., S. Esah, and U. Pranith. 1967. Relation of Anopheles aconitus to malaria transmission in the central plain of Thailand. Trans. R. Soc. Trop. Med. Hyg. 61: 441-442.
18. Green, C. A., R. F. Gass, L. E. Munstermann, and V. Baimai. 1990. Population-genetic evidence for two species in Anopheles minimus in Thailand. Med. Vet. Entomol. 4: 25-34.
19. Green, C. A., R. R., P. S., S. P., and B. V. 1991. A newly-recognized vector of human malarial parasites in the Oriental region, Anopheles (Cellia) pseudowillmori (Theobald, 1910). Trans. R. Soc. Trop. Med. Hyg. 85: 35-36.
20. Green, C. A., L. E. Munstermann, S. G. Tan, S. Panyim, and V. Baimai. 1992. Population genetic evidence for species A, B, C and D of the Anopheles dirus complex in Thailand and enzyme electromorphs for their identification. Med. Vet. Entomol. 6: 29-36.
21. Guerra, C. A., R. W. Snow, and S. I. Hay. 2006. A global assessment of closed forests, deforestation and malaria risk. Ann. Trop. Med. Parasitol. 100: 189-204.
22. Harbach, R. E., V. Baimai, and S. Sukowati. 1987. Some observations on sympatric populations of the malaria vectors Anopheles leucosphyrus and Anopheles balabacensis in a village-forest setting in South Kalimantan. Southeast Asian J. Trop. Med. Publ. Hlth. 18: 241-247.
23. Ismail, I. A., V. Notananda, and J. Schepens. 1974. Studies on malaria and responses of Anopheles balabacensis balabacensis and Anopheles minimus to DDT residual spraying in Thailand I. Pre-spraying observations. Acta. Trop. 31: 129-164.
24. Jitpakdi, A., W. Choochote, P. Panart, B. Tookyang, K. Panart, and S. Prajakwong. 1998. Possible transmission of two types of Wuchereria bancrofti in Muang District, Chiang Mai, northern Thailand. Southeast Asian J. Trop. Med. Publ. Hlth. 29: 141-143.
25. Junkum, A., B. Pitasawat, B. Tuetun, A. Saeung, E. Rattanachanpichai, N. Jariyapan, N. Komalamisra, M. Mogi, U. Chaithong, and W. Choochote. 2007. Seasonal abundance and biting activity of Anopheles aconitus (Diptera: Culicidae) in Chiang Mai, northern Thailand. Southeast Asian J. Trop. Med. Publ. Hlth. 38: 215-223.
26. Khamboonruang, C., P. Thitasut, S. Pan-In, N. Morakote, W. Choochote, P. Somboon, and P. Keha. 1987. Filariasis in Tak Province, northwest Thailand: the presence of subperiodic variant Wuchereria bancrofti. Southeast Asian J. Trop. Med. Publ. Hlth. 18: 218-222.
27. Kongmee, M., N. L. Achee, K. Lerdthusnee, M. J. Bangs, S. Chowpongpang, A. Prabaripai, and T. Charoenviriyaphap. 2012. Seasonal abundance and distribution of Anopheles larvae in a riparian malaria endemic area of western Thailand. Southeast Asian J. Trop. Med. Publ. Hlth. 43: 601-613.
28. Linton, Y. M., R. E. Harbach, S. Chang Moh, T. G. Anthony, and A. Matusop. 2001. Morphological and molecular identity of Anopheles (Cellia) sundaicus (Diptera: Culicidae), the nominotypical member of a malaria vector species complex in Southeast Asia. Syst. Entomol. 26: 357-366.
29. Manguin, S., P. Kengne, L. Sonnier, R. E. Harbach, V. Baimai, H. D. Trung, and M. Coosemans. 2002. SCAR markers and multiplex PCR-based identification of isomorphic species in the Anopheles dirus complex in Southeast Asia. Med. Vet. Entomol. 16: 46-54.
30. Manguin, S., C. Garros, I. Dusfour, R.E. Harbach, and M. Coosemans. 2008. Bionomics, taxonomy, and distribution of the major malaria vector taxa of Anopheles subgenus Cellia in Southeast Asia: an updated review. Infect. Genet. Evol. 8: 489-503.
31. Muenworn, V., S. Sungvornyothin, M. Kongmee, S. Polsomboon, M.J. Bangs, P. Akrathanakul, S. Tanasinchayakul, A. Prabaripai, and T. Chareonviriyaphap. 2009. Biting activity and host preference of the malaria vectors Anopheles maculatus and Anopheles sawadwongporni (Diptera: Culicidae) in Thailand. J. Vector Ecol. 34: 62-69.
32. Overgaard, H., Y. Tsuda, W. Suwonkerd, and M. Takagi. 2002. Characteristics of Anopheles minimus (Diptera: Culicidae) larval habitat in northern Thailand. Environ. Entomol. 31: 134-141.
33. Perandin, F., N. Manca, A. Calderaro, G. Piccolo, L. Galati, L. Ricci, M.C. Medici, M.C. Arcangeletti, G. Snounou, G. Dettori, and C. Chezzi. 2004. Development of a real-time PCR assay for detection of Plasmodium falciparum, Plasmodium vivax, and Plasmodium ovale for routine clinical diagnosis. J. Clin. Microbiol. 42: 1214-1219.
34. Poolprasert, P., S. Manguin, M.J. Bangs, S. Sukhontabhirom, S. Poolsomboon, P. Akaratanakul, and T. Chareonviriyaphap. 2008. Genetic structure and gene flow of Anopheles minimus and Anopheles harrisoni in Kanchanaburi Province, Thailand. J. Vector Ecol. 33: 158-165.
35. Poopittayasataporn, A. and V. Baimai. 1995. Polytene chromosome relationships of five species of the Anopheles dirus complex in Thailand. Genome. 38: 426-434.
36. Pothikasikorn, J., M.J. Bangs, R. Boonplueang, and T. Chareonviriyaphap. 2008. Susceptibility of various mosquitoes of Thailand to nocturnal subperiodic Wuchereria bancrofti. J. Vector Ecol. 33: 313-320.
37. Rao, R.U., L.J. Atkinson, R.M. Ramzy, H. Helmy, H.A. Farid, M.J. Bockarie, M. Susapu, S. J. Laney, S.A. Williams, and G.J. Weil. 2006. A real-time PCR-based assay for detection of Wuchereria bancrofti DNA in blood and mosquitoes. Am. J. Trop. Med. Hyg. 74: 826-832.
38. Ratanatham, S., E.S. Upatham, C. Prasittisuk, W. Rojanasunan, N. Theerasilp, A. Tremongkol, and V. Viyanant. 1988. Bionomics of Anopheles minimus and its role in malaria transmission in Thailand. Southeast Asian J. Trop. Med. Publ. Hlth. 19: 283-289.
39. Rattanarithikul, R., K.J. Linthicum, and E. Konishi. 1996a. Seasonal abundance and parity rates of Anopheles species in southern Thailand. Am. Mosq. Contr. Assoc. 12: 75-83.
40. Rattanarithikul, R., E. Konishi, and K.J. Linthicum. 1996b. Observations on the nocturnal biting activity and host preference of anophelines collected in southern Thailand. J. Am. Mosq. Contr. Assoc. 12: 52-57.
41. Rattanarithikul, R., B.A. Harrison, R.E. Harbach, P. Panthusiri, R.E. Coleman, and P. Panthusiri. 2006. Illustrated keys to the mosquitoes of Thailand. IV. Anopheles. Southeast Asian J. Trop. Med. Publ. Hlth. 37 Suppl 2: 1-128.
42. Reiter, P. 2001. Climate change and mosquito-borne disease. Environ. Hlth. Perspect. 109 Suppl 1: 141-161.
43. Rongnoparut, P., S. Yaicharoen, N. Sirichotpakorn, R. Rattanarithikul, G.C. Lanzaro, and K.J. Linthicum. 1996. Microsatellite polymorphism in Anopheles maculatus, a malaria vector in Thailand. Am. J. Trop. Med. Hyg. 55: 589-594.
44. Rongnoparut, P., N. Sirichotpakorn, R. Rattanarithikul, S. Yaicharoen, and K.J. Linthicum. 1999. Estimates of gene flow among Anopheles maculatus populations in Thailand using microsatellite analysis. Am. J. Trop. Med. Hyg. 60: 508-515.
45. Rosenberg, R., R.G. Andre, and L. Somchit. 1990. Highly efficient dry season transmission of malaria in Thailand. Trans. R. Soc. Trop. Med. Hyg. 84: 22-28.
46. Rougemont, M., M. Van Saanen, R. Sahli, H.P. Hinrikson, J. Bille, and K. Jaton. 2004. Detection of four Plasmodium species in blood from humans by 18S rRNA gene subunit-based and species-specific real-time PCR assays. J. Clin. Microbiol. 42: 5636-5643.
47. Saeung, A., V. Baimai, Y. Otsuka, R. Rattanarithikul, P. Somboon, A. Junkum, B. Tuetun, H. Takaoka, and W. Choochote. 2008. Molecular and cytogenetic evidence of three sibling species of the Anopheles barbirostris Form A (Diptera:Culicidae) in Thailand. Parasitol. Res. 102: 499-507.
48. Saeung, A. 2012. Anopheles (Diptera:Culicidae) species complex in Thailand: identificaton, distribution, bionomics and malaria-vector importance. Int. J. Parasitol. 4: 75-82.
49. Scanlon, J.E., E.L. Peyton, and D.J. Gould. 1968. An annotated checklist of the Anopheles of Thailand. Thai Natl. Sci. Pap. Fauna Ser. 2: 1-35.
50. Sinka, M.E., M.J. Bangs, S. Manguin, T. Chareonviriyaphap, A.P. Patil, W.H. Temperley, P.W. Gething, I.R. Elyazar, C.W. Kabaria, R.E. Harbach, and S.I. Hay. 2011. The dominant Anopheles vectors of human malaria in the Asia-Pacific region: occurrence data, distribution maps and bionomic precis. Parasit. Vectors 4: 89.
51. Somboon, P., D. Thongwat, and R.E. Harbach. 2011. Anopheles (Cellia) rampae n. sp., alias chromosomal form K of the Oriental Maculatus Group (Diptera: Culicidae) in Southeast Asia. Zootaxa 2810: 47-55.
52. Sungvornyothin, S., V. Muenvorn, C. Garros, S. Manguin, A. Prabaripai, M.J. Bangs, and T. Chareonviriyaphap. 2006. Trophic behavior and biting activity of the two sibling species of the Anopheles minimus complex in western Thailand. J. Vector Ecol. 31: 252-261.
53. Suwonkerd, W., H.J. Overgaard, Y. Tsuda, P.S., and M. Takagi. 2002. Malaria vector densities in transmission and non-transmission areas during 23 years and land use in Chiang Mai province, Northern Thailand. Basic Appl. Ecol. 3: 197-207.
54. Takai, K., T. Kanda, K. Ogawa, and S. Sucharit. 1987. Morphological differentiation in Anopheles maculatus of Thailand accompanied with genetical divergence assessed by hybridization. J. Am. Mosq. Contr. Assoc. 3: 148-153.
55. Takken, W. and N.O. Verhulst. 2013. Host preferences of blood-feeding mosquitoes. Annu. Rev. Entomol. 58: 433-453.
56. Tananchai, C., R. Tisgratog, W. Juntarajumnong, J.P. Grieco, S. Manguin, A. Prabaripai, and T. Chareonviriyaphap. 2012. Species diversity and biting activity of Anopheles dirus and Anopheles baimaii (Diptera: Culicidae) in a malaria prone area of western Thailand. Parasit. Vectors 5: 211.
57. Thongsahuan, S., V. Baimai, Y. Otsuka, A. Saeung, B. Tuetun, N. Jariyapan, S. Suwannamit, P. Somboon, A. Jitpakdi, H. Takaoka, and W. Choochote. 2009. Karyotypic variation and geographic distribution of Anopheles campestris-like (Diptera: Culicidae) in Thailand. Mem. Inst. Oswaldo Cruz. 104: 558-566.
58. Tisgratog, R., C. Tananchai, W. Juntarajumnong, S. Tuntakom, M.J. Bangs, V. Corbel, and T. Chareonviriyaphap. 2012. Host feeding patterns and preference of Anopheles minimus (Diptera: Culicidae) in a malaria endemic area of western Thailand: baseline site description. Parasit. Vectors 5: 114.
59. Upatham, E.S., C. Prasittisuk, S. Ratanatham, C.A. Green, W. Rojanasunan, P. Setakana, N. Theerasilp, A. Tremongkol, V. Viyanant, S. Pantuwatana, and R.G. Andre. 1988. Bionomics of Anopheles maculatus complex and their role in malaria transmission in Thailand. Southeast Asian J. Trop. Med. Publ. Hlth. 19: 259-269.
60. Vanwambeke, S.O., P. Somboon, R.E. Harbach, M. Isenstadt, E.F. Lambin, C. Walton, and R.K. Butlin. 2007a. Landscape and land cover factors influence the presence of Aedes and Anopheles larvae. J. Med. Entomol. 44: 133-144.
61. Vanwambeke, S.O., E.F. Lambin, M.P. Eichhorn, S.P. Flasse, R.E. Harbach, L. Oskam, P. Somboon, S.V. Beers, B.H.B. Van Benthem, C. Walton, and R.K. Butlin. 2007b. Impact of land-use change on dengue and malaria in northern Thailand. Eco. Hlth. 4: 37-51.
62. Walton, C., J.M. Handley, C. Kuvangkadilok, F.H. Collins, R.E. Harbach, V. Baimai, and R.K. Butlin. 1999. Identification of five species of the Anopheles dirus complex from Thailand, using allele-specific polymerase chain reaction. Med. Vet. Entomol. 13: 24-32.
63. Walton, C., P. Somboon, S.M. O'Loughlin, S. Zhang, R.E. Harbach, Y.M. Linton, B. Chen, K. Nolan, S. Duong, M.Y. Fong, I. Vythilingum, Z.D. Mohammed, H.D. Trung, and R.K. Butlin. 2007. Genetic diversity and molecular identification of mosquito species in the Anopheles maculatus group using the ITS2 region of rDNA. Infect. Genet. Evol. 7: 93-102.
64. Yasuoka, J., and R. Levins. 2007. Impact of deforestation and agricultural development on anopheline ecology and malaria epidemiology. Am. J. Trop. Med. Hyg. 76: 450-460.