SOUTHEAST ASIAN J TROP MED PUBLIC HEALTH

MOSQUITO FAUNA OF “TOH DAENG” SWAMP FOREST,

Chamnarn Apiwathnasorn1, Yudthana Samung1, Samrerng Prummongkol1, Chotechuang Panasoponkul1 and Sumat Loymek2

1Department of Medical Entomology, Faculty of Tropical Medicine, Mahidol University, Bangkok; 2Bureau of Vector Borne Disease, Department of Disease Control, Ministry of Public Health, Nonthaburi, Thailand

Abstract. Entomological surveys (2001-2005) were carried out in Narathiwat Province to determine fauna of the peat swamp forest. Fifty-four species belonging to 13 genera were identified from 837 larval specimens and 3,982 adult mosquitoes. These included the major vectors for Brugian fillariasis: Mansonia annulata, Ma. bonneae, Ma. dives, Ma. uniformis and Ma. indiana. Ma. annulata and An. letifer were reported for the first time in Thailand as lymphatic filariasis vectors. Three species inhabiting Nepen- thes pitchers (N. mirabilis): Tripteroides tenax, Toxorhynchites manopi and Uranotaenia edwardsi, were recorded for the first time in Thailand; Zeugnomyia gracilis was also found common in the peat swamp forest.

INTRODUCTION the mosquito fauna. The present study de- scribes the current mosquito fauna in the Toh Peat swamp forests in Thailand cover Daeng peat swamp. about 64,000 ha, and are located mostly in the South. “Toh Daeng” is the largest swamp MATERIALS AND METHODS forest occupying 8,000 ha (Phengklai et al, 1991). This forest supports primary peat Study area swamp, Melaleuca woodland and scrub and The “Toh Daeng” peat swamp forest is degraded grasslands. These unique habitats located in Narathiwat Province, 1,149 km support a large variety of flora and fauna. south of Bangkok. The site lies parallel to the Some 470 plant species in 124 families have eastern coastline of southern Thailand, about been recorded; 217 bird, 52 reptile, 62 fish, 7 km inland. The northern and southern 19 amphibian, 106 butterfly and 60 mammal parts of the swamp drain into the Bang Nara species have been identified (Phlengklai et River and Su-ngai Kolok River, respectively. al, 1991; Vijarnsorn, 1996; Hankaew, 2003). Toh Daeng contains a research and visitor’s Lymphatic filariasis is a serious mosquito- facility, “Sirindhorn Research and Nature borne disease associated with this peat Study Center”, located in the wildlife con- swamp forest, where little is known about servation area. The surrounding areas are privately owned and used for agricultural Correspondence: Chamnarn Apiwathnasorn, Department of Medical Entomology, Faculty of purposes (rice, rubber and fruit plantations) Tropical Medicine, Mahidol University, 420/6 and settlements. The peat swamp forest is Ratchawithi Road, Bangkok 10400, Thailand. characterized by low-lying flat land with 1.0- Tel: 66 (0) 2354 9100-19 ext 1571 1.5 m water present throughout the year. The E-mail: [email protected] deposited organic materials causes the

720 Vol 40 No. 4 July 2009 MOSQUITO FAUNA OF SWAMP FOREST water to be acidic (pH of 4.0-5.5). The poor merged plants and trees in the swamp nutrient content of the acidic soil impedes forest. The collecting equipment was modi- agricultural use preventing other trees, ex- fied from the device made by Batzer (1993) cept Melaleuca cajuputi, from becoming es- and the collecting technique was recently tablished in the swamp due to lack of soil described by Apiwathnasorn et al (2006a). within the peat swamp forest. The area has The larvae were mounted on slides and a constant mean temperature of 26-27ºC with the species identified using the key of an annual rainfall of 2, 560.2 mm and an av- Apiwathnasorn et al (1991). erage of 171 days of rain per year with the Processing of collected specimens heaviest rainfall in November-December. As Narathiwat Province is an area en- There is no distinct dry season; the average demic with Brugian filariasis, dissection for humidity is 77-83% (Phlengklai et al, 1989). filarial parasites was carried out on the head Five sites from different habitats were cho- and thorax portions of Mansonia mosquitoes sen to capture the mosquitoes. The habitats and other potential species obtained from the were located in the core or preservation zone human-landing and cow-baited catches. The (primary swamp forest), periphery or con- details of this dissection technique are de- servation zone (secondary swamp forest) scribed by Leemingsawat et al (1987). Some and development or agricultural zone. adult mosquitoes were pinned and the re- Mosquito collection mainder was preserved dry for further ex- To optimize the diversity of col- amination. Immature stages collected from lected, five collection methods were utilized ovitraps were kept alive and reared to adults in the study: -baited traps (cow and either in single or in mass. Dead specimens cat, 2 traps per night), human-landing and/or larval and pupal skins were removed catches (5 persons per night), light traps (5 daily and preserved in 70% alcohol. Larval traps per night), and direct search from and pupal specimens were slide-mounted breeding places by dippers, pipettes and using Hoyer’s medium (Rattanarithikul, oviposition traps (30 traps per site). The col- 1982). Adult specimens were examined un- lections were conducted 4 days per month. mounted or on pin-mounted paper points. monitoring traps, oviposition and The species of the mosquito specimens were light traps, were placed at random in the identified using standard light microscopy wildlife conservation areas while the others and a range of taxonomic authorities and keys were conducted at all three collection sites. (Thurman, 1959; Wharton et al, 1962; Peyton In order to develop practical, effective and Scanlon, 1966; Bram, 1967; Harrison and and inexpensive oviposition traps, discarded Scanlon, 1975; Huang, 1979; Rattanarithikul, soft-drink bottles, such as 1-liter Coca-Cola 1982). or Sprite plastic bottles were cut in half and RESULTS used, the lower part hanging from tree trunks in the forest throughout the period A total of 3,982 mosquitoes were col- of investigation. Mosquito larvae found in lected, 1,704 from human-landing catches, oviposition traps were collected monthly 2,009 from animal-baited traps, 269 from and brought back to the laboratory for iden- light traps and 837 larval specimens from 54 tification. species in 13 genera (Table 1). Of the collec- Special attention was also given to the tion methods used, the animal-baited traps collection of Mansonia larvae from sub- yielded the greatest number of species, com-

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Table 1 Mosquito species composition and abundance in Toh Daeng peat swamp forest, September 2001 to December 2005.

Adult mosquitoes Immature mosquitoes Mosquito species collected by method collected Human- Cow- Light Ovi- Pitcher landing baited traps position plants catches catches traps

Aedes (Aedimorphus) caecus 100 -- Aedes (Aedimorphus) mediolineatus 0140 - - Aedes (Aedimorphus) stenoetrus 000 +- Aedes (Aedimorphus) vexans 0380 - - Aedes (Fredwardsius) vittatus 030 -- Aedes (Stegomyia) albopictus 11105 +- Aedes (Verrallina) sp 000 +- Anopheles (Anopheles) barbirostris 080 -- Anopheles (Anopheles) barbumbrosus 0460 - - Anopheles (Anopheles) campestris 050 -- Anopheles (Anopheles) nigerrimus 1 168 0 - - Anopheles (Anopheles) peditaeniatus 0 186 0 - - Anopheles (Anopheles) letifer 46 45 0 - - Anopheles (Anopheles) sinensis 020 -- Anopheles (Cellia) nivipes 070 -- Anopheles (Cellia) tessellatus 090 -- Anopheles (Cellia) vagus 040 -- Armigeres (Armigeres) kuchingensis 100 -- Armigeres (Armigeres) subalbatus 86 3 0 - - Armigeres (Armigeres) theobaldi 200 -- crassipes 14 44 0 - - Coquillettidia nigrosignata 83 0 37 - - Coquillettidia ochracea 113 -- (Culex) annulus 003 -- Culex (Culex) bitaeniorhynchus 4102 - - Culex (Culex) fuscocephala 040 -- Culex (Culex) gelidus 29 88 37 - - Culex (Culex) pseudosinensis 600 -- Culex (Culex) pseudovishnui 9023-- Culex (Culex) sinensis 500 -- Culex (Culex) tritaeniorhynchus 14 113 27 - - Culex (Culex) vishnui 940 -- Culex (Culex) whitmorei 090 -- Culex (Culiciomyia) pallidothorax 0042-- Culex (Eumelanomyia) brevipalpis 007 +- Culex (Lophoceraomyia) curtipalpis 000 -+ Heizmannia (Heizmannia) reidi 89 0 0 - - Mansonia (Mansonioides) annulata 391 0 31 - - Mansonia (Mansonioides) bonneae 566 653 0 - -

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Table 1 (Continued).

Adult mosquitoes Immature mosquitoes Mosquito species collected by method collected Human- Cow- Light Ovi- Pitcher landing baited traps position plants catches catches traps

Mansonia (Mansonioides) dives 46 26 0 - - Mansonia (Mansonioides) indiana 72 15 0 - - Mansonia (Mansonioides) uniformis 117 502 0 - - Mimomyia elegans 005 -- Mimomyia fusca 0018-- Ochlerotatus (Finlaya) albotaeniatus 000 +- Ochlerotatus (Finlaya) niveus subgroup 0 0 0 - - Ochlerotatus (Kenknightia) dissimillis 100 +- Ochlerotatus (Mucidus) quasiferinus 020 -- Tripteroides (Rachionotomyia) tenax 000 -+ Toxorhynchites (Toxorhynchites) manopi 000 -+ Uranotaenia (Uranotaenia) annandalei 007 -- Uranotaenia (Uranotaenia) edwardsi 0017-- Uranotaenia (Uranotaenia) longirostris 005 -- Zeugnomyia gracilis 000 ++ Total 1,704 2,009 269 + +

prising 50.0% of the total number of species leaf axil found in Trang Province, southern caught, followed by human landing catches Thailand by Benjaphong and Rattanarithikul (44.4%), light traps (29.6%) and oviposition (1991). traps (18.5%). Owing to breeding place surveys, habi- The mosquitoes collected were: Manso- tat features associated with each mosquito nia (61.0%), Anopheles (13.2%), Culex (11.2%), species were mainly paddy fields, riverine Coquillettidia (4.6%), Aedes (4.3%), Armigeres habitats and primary swamp forest. Larvae (2.3%), Heizmannia (2.2%) and others (2.2%; and pupae of various mosquito species ob- Ochlerotatus, Uranotaenia, Mimomyia, tained from natural containers of plant ori- Toxorhynchites, Tripteroides and Zeugnomyia). gin (tree holes and pitcher plants) and ovi- Animal-baited traps and landing catches position traps were reported for the first were similar in recording the most abundant time. Immature Cx. curtipalpis, Tp. tenax and species (Mansonia spp), while a greater num- Tx. manopi were recovered from pitchers of ber of uncommon species were recorded Nepenthes mirabilis with larval density vary- with other collecting means; for instance, a ing from 2 to 73 larvae per pitcher cup, Cx. large number of Ze. gracilis specimens was curtipalpis was the most abundant. Ae. obtained from oviposition traps. The discov- albopictus, Oc. albotaeniatus, Oc. dissimillis and ery of Ze. gracilis in Narathiwat Province Oc. niveus subgroup were collected from tree provided an additional distribution record holes and oviposition traps in the wildlife that was previously reported from a fallen conservation zone. The oviposition traps

Vol 40 No. 4 July 2009 723 SOUTHEAST ASIAN J TROP MED PUBLIC HEALTH also yielded many immature specimens, in- lected from larger trees, Metroxylon sagus and cluding the genus Aedes, Culex, Ochlerotatus, Melaleuca cajuputi, but in fewer numbers of Tripteroides and Zeugnomyia. Apart from land- larvae per scraping (1-7). Ma. uniformis was ing catches, An. letifer larvae were also dipped recovered from most of the host plants, how- from peat swamp water in varying densities ever, Ma. bonneae preferred submerged (1-16 larvae/dip). Paddy fields in the devel- plants rather than floating aquatic plants, opment zone around the peat swamp favored Eichhornia crassipes and Pistia stratiotes. breeding habitats for various zoophilic Ninety-one An. letifer specimens were species of the genus Aedes (Ae. caecus, Ae. captured by human landing and cow-baited mediolineatus, Ae. vexans), Anopheles (An. methods with an infection rate of 2.2% by barbirostris, An. campestris, An. donaldi, An. dissection for B. malayi. An. letifer was re- nigerrimus, An. peditaeniatus, An. sinensis, An. ported for the first time in Thailand as an nivipes, An. tessellatus and An. vagus) and additional vector for Brugian filariasis with Culex, particularly the vectors of Japanese B outdoor biting habit during the day and the encephalitis (Cx. fuscocephala, Cx. gelidus, Cx. night. An. letifer has been reported as a vec- pseudovishnui, Cx. tritaeniorhynchus and Cx. tors for filariasis and malaria in vishnui) most of which were captured by cow- and is predominant in peat swamp areas baited traps. (Wharton et al, 1962; Thevasagayam and Fah, 1980; Rahman et al, 1997). An. letifer was ear- DISCUSSION lier reported in Thailand by Iyengar and Menon (1956), Reid (1963) and Scanlon et al Brugian filariasis transmitted by Man- (1968), however, no specimens were avail- sonia mosquitoes is the only main vector- able for confirmation of species presence borne disease occurring in the peat swamp (Harrison and Scanlon, 1975). The present forest of Narathiwat Province with wild and study confirms the presence of An. letifer in domestic as reservoir hosts the peat swamp forest of Narathiwat Prov- (Phantana et al, 1987; 1995; Kobasa et al, 2004; ince, where adults were captured from Apiwathnasorn et al, 2006b). In our study, baited traps and the larvae were found Mansonia mosquitoes were collected with breeding in peat water. each method used except for oviposition In summary, the abundance and species traps, and were found widely distributed distribution varied by swamp topography throughout the peat swamp, particularly in (the wildlife conservation area in the central the wildlife conservation area. The most zone surrounded by arboreal lowland and abundant species were Ma. bonneae (26.8% riverine vegetation with agricultural devel- of all mosquitoes collected) followed by Ma. opment areas in the outmost areas). Many uniformis (13.6%) and Ma. annulata (9.3%). species collected in the present study are The prevalence of mosquitoes infected with known to be vectors of diseases: Ae. B. malayi was 0.47% for Ma. annulata and albopictus (a vector of dengue fever), An. 0.25% for Ma. bonneae by dissection. Imma- barbirostris and An. letifer (vectors of malaria ture bonneae and uniformis were obtained and lymphatic filariasis), Oc. niveus sub- from common sedges of the family group (vectors of bancroftian filariasis, ru- Cyperaceae: Cyperus babakan, C. corymbosus, ral type), and Cx. fuscocephala, Cx. gelidus and Lepironia articulata, Rhynchospora corymbosa, Cx. tritaeniorhynchus (vectors of Japanese B Scirpodendron ghaeri, Scleria sumatrensis, and encephalitis). Notably Ae. aegypti was absent Sacclolepis indica. The larvae were also col- from the specimens collected, possibly be-

724 Vol 40 No. 4 July 2009 MOSQUITO FAUNA OF SWAMP FOREST cause this species is more commonly found Batzer DP. Technique for surveying larval popu- indoors in urban areas. The roles of these lations of Coquillettidia perturbans. J Am Mosq species in transmitting disease have not been Control Assoc 1993; 9: 349-51. determined in Narathiwat Province. Three Benjaphong N, Rattanarithikul R. Zeugnomyia species of mosquitoes were found for the gracilis Leicester (Diptera: Culicidae), a new first time breeding in pitcher plants (N. genus and species occurrence record from mirabilis): Cx. curtipalpis, Tp. tenax and Tx. Thailand. Mosq Syst 1991; 23: 53. manopi. Zeugnomyia gracilis, recovered from Bram RA. Contributions to the mosquito fauna oviposition traps, was also reported for the of Southeast Asia.-II. The genus Culex in first time in the peat swamp forest of Thai- Thailand (Diptera:Culicidae). Contrib Am land. Information regarding mosquito fauna Entomol Inst (Ann Arbor) 1967; 2: 1-296. in the Toh Daeng peat swamp is still inad- Hankaew C. Integrated management plan on equate. Some endemic species have yet to peat swamp forests, Southern Thailand. be discovered and identified. Workshop on approaches for integrated and wise use of peatlands in Thailand. Royal Princess Hotel, Narathiwat, Thailand. 9-11 ACKNOWLEDGEMENTS April, 2003: 9pp. We are grateful to Professor David Harrison BA, Scanlon JE. Medical entomology- Molyneux and Dr Philip J McCall for their II. The subgenus Anopheles in Thailand valuable comments and suggestions during (Diptera:Culicidae). Contrib Am Entomol Inst (Ann Abor) 1975; 12: 1-307. data analysis. We thank the Leverhulme Trust for the financial support provided Huang YM. Medical entomology studies-XI. The throughout the present study and special subgenus Stegomyia of Aedes in the Oriental Region with keys to the species thanks to the Faculty of Tropical Medicine, (Diptera:Culicidae). Contrib Am Entomol Inst Mahidol University for providing the re- (Ann Amor) 1979; 15: 1-79. search facilities. Iyengar MOT, Menon MAU. The mosquitoes of south Thailand. Bull Entomol Res 1956;47: REFERENCES 785-95. Apiwathnasorn C, Komalamisra N, Thongrung- Kobasa T, Thammapalo S, Suvannadabba S, et al. kiat S, Sucharit S. A simplified key for larval Identification of Brugia malayi-like microfi- identification of Mansonia mosquitoes in lariae in naturally-infected cats from Thailand. Mosq-Borne Dis Bull 1991; 8: 1-5. Narathiwat Province, Southern Thailand. J Trop Med Parasitol 2004; 27: 21-5. Apiwathnasorn C, Samung Y, Prummongkol S, Asavanich A, Komalamisra N. Surveys for Leeminsawat S, Deesin T, Vutikes S. Determina- natural host plants of Mansonia mosquitoes tion of filariae in mosquitoes. In: Sucharit S, inhabiting Toh Daeng peat swamp forest, Supavej S, eds. Practical Entomology, malaria Narathiwat Province, Thailand. Southeast and filariasis. Bangkok: Siriyod Printing Asian J Trop Med Public Health 2006a; 37: 279- (Thailand), 1987: 42-6. 82. Peyton EL, Scanlon JE. Illustrated key to the fe- Apiwathnasorn C, Samung Y, Prummongkol S, male Anopheles mosquitoes of Thailand. Asavanich A, Komalamisra N, Mccall P. Bio- Bangkok: US Army Medical Component, nomics studies of Mansonia mosquitoes in- Southeast Asia Treaty Organization, 1966: habiting the peat swamp forest. Southeast 47pp. Asian J Trop Med Public Health 2006b; 37: 272- Phantana S, Sensathien S, Choomphon S. Microfi- 8. lariae in cat in Narathiwat, southern Thai-

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