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Mosquitoes of Green, Orchid, and Islands

MOSQUITO SURVEYS CARRIED OUT ON GREEN ISLAND, , AND PENGHU ISLAND, , IN 2003

Hwa-Jen Teng, Guo-Chin Huang, Yung-Chen Chen, Wei-Tai Hsia, Liang-Chen Lu, Wen-Tang Tsai,1 and Mei-Ju Chung2 Medical Entomological Laboratory, Research and Development Center, Center for Disease Control, Department of Health, , 1Penghu Health Bureau, Penghu, and 2Taitung County Health Bureau, Taitung, Taiwan.

Field surveys of mosquitoes were carried out on Green, Orchid, and Penghu Islands in 2003 to ascertain the status of mosquito vectors. Eighteen species of mosquitoes were collected, including three species of Anopheles, four species of Aedes, eight species of Culex, two species of Armigeres, and one species of Malaya. Seventeen previously recorded species were not collected in this study but 11 species collected had not previously been recorded. Ten newly recorded species, An. maculatus, An. takasagoensis, Ae. alcasidi, Ae. lineatopennis, Ae. vexans vexans, Ar. omissus, Cx. vishnui, Cx. halifaxii, Cx. hayashii, and Cx. neomimulus, were collected on Green Island and one previously unrecorded species, Ar. subalbatus, was collected on Orchid Island. Potential vectors An. maculatus and An. sinensis, malaria vectors in Korea and Mainland China, Ae. albopictus, a vector of dengue in Taiwan and West Nile virus in the USA, Cx. vishnui and Cx. tritaeniorhynchus, Japanese encephalitis vectors in Taiwan, Ae. vexans vexans, an eastern equine encephalitis vector in the USA, and Cx. quinquefasciatus, a vector of filariasis in Taiwan and West Nile virus in the USA, were among the mosquito species collected.

Key Words: mosquito fauna, Penghu Island, Green Island, Orchid Island, (Diptera, Culicidae) ( J Med Sci 2005;21:51–6)

There are about 500 arboviruses in the world. Wild animals West Nile virus to North America [2,3], Ross River fever to often serve as amplifiers or reservoirs of these vector-borne the South Pacific [4], Japanese encephalitis to Australia [5, infectious diseases [1]. Occasionally, these viruses are 6], and a reemergence of malaria in Korea are examples of transmitted from animals to humans by a group of mosquito this [7]. Basic information about mosquito status in various vectors. The infection may then be transmitted from infected locations is important to understand the risk of mosquito- humans to other humans by a different group of mosquito borne infectious diseases in specific areas. vectors. Due to the increasing mobility of humans and Mosquitoes on Green Island, Orchid Island, and Penghu animals through modern transportation, mosquito-borne Island in Taiwan have been studied exclusively in connection infectious diseases are spreading. The introduction of the with malaria and dengue. In addition to Taiwan proper, cases of human malaria and the presence of its vector, Anopheles minimus L., were recorded on each of the islands in 1940 [8]. In 1978, Lien thoroughly summarized the status Received: October 21, 2004 Accepted: January 4, 2005 of mosquito distribution in Taiwan, including on Green, Address reprint requests and correspondence to: Dr. Hwa-Jen Teng, Orchid, and Penghu Islands [9]. No papers related to the Medical Entomological Laboratory, Research and Development mosquitoes on these islands have been published since that Center, Center for Disease Control, Department of Health, 161 Kun- Yang Street, Nan-Kang, Taipei 115, Taiwan. time. This paper is a record of our survey results from 2003. E-mail: [email protected] It provides information about the mosquitoes on these

Kaohsiung J Med Sci February 2005 ¥ Vol 21 ¥ No 2 51 © 2005 Elsevier. All rights reserved. H.J. Teng, G.C. Huang, Y.C. Chen, et al islands and briefly discusses the potential vector status of N mosquito species. Zhongliao Village

Gongguan Village MATERIALS AND METHODS

Survey areas Nanliao Village Green Island, Orchid Island, and Penghu Island were chosen as locations to conduct the surveys because of the record of malaria and the presence of its mosquito vector, An. minimus, during the malaria endemic period. Green and Orchid Adult collection site Islands are small island townships of in the Larval collection site 0 750 1,500 3,000 Pacific Ocean. Green Island, with an area of approximately Road Meters 15 km2, is located 10 km east of Taitung City at 22°38’– Figure 1. Mosquito collection sites on Green Island, Taitung County. 22°42’ N and 121°27’–121°33’ E. The temperature remains between 20°C and 29°C and it rains year round. Orchid N Island, with an area of approximately 48 km2, is situated about 80 km southeast of Taitung City at 22°00’–22°60’ N Langdao Village and 121°29’–121°36’ E. Rain falls year round and the annual average temperature is 22.6°C (range, 16.8–28.4°C). Penghu

Island consists of 64 islands of different sizes with a total Yeyou Village Dongqing Village land area of approximately 127 km2. It is located at 23°47’– 23°9’ N and 119°18’–119°42’ E. The rainy season is between April and September and there is a strong Northeast wind from October to March. The average temperature is 23°C, reaching 28.3°C in July and 16.2°C in February.

Hongtou Village Mosquito collection Adult collection site Larval collection site The survey was conducted on Green Island in September Road 2003 and on Orchid and Penghu Islands in October 2003.

The geological positioning system, GeoExplorer 3 (Trimble 00.51 2 3 4 Km Navigation Ltd, Sunnyvale, CA, USA), was used to locate the Figure 2. Mosquito collection sites on Orchid Island, Taitung County. collection sites (Figures 1–3). Although immature mosquitoes were collected mainly from streams, they were also taken from N ponds, ditches, rock holes, and plant axils. A 14-cm-diameter dipper was used to collect larvae from possible mosquito breeding sites along the banks of streams, ponds, and ditches. Paisha A Pest-O-Lite trap placed near a house and a Center for Dis- ease Control (CDC) light trap placed in a field near a breeding stream were used to collect adult mosquitoes on 2 or 3 con- Shiyu Township Hushi Township secutive nights. Mosquitoes were observed under micro- scopes in the laboratory and identified with mosquito keys Magong City Kouyieh for Taiwan prepared by the CDC. Village Dengue vector mosquitoes were collected monthly by the local health bureaus in Taitung and Penghu Counties. Adult collection site The village sample proportion (number of village surveys/ Larval collection site Road total number of villages) varied from 33.3% to 207.2% per 0 0.51234Km month except for January and February in Penghu Island (8.2%). There were three villages on Green Island, four on Figure 3. Mosquito collection sites on Penghu Island.

52 Kaohsiung J Med Sci February 2005 • Vol 21 • No 2 Mosquitoes of Green, Orchid, and Penghu Islands

Orchid Island, and 97 on Penghu Island. A stratified cluster vectors are An. maculatus and An. sinensis (malaria vectors in sampling technique was used to sample residential premises Korea and Mainland China), Ae. albopictus (a vector of dengue in each village by randomly selecting and surveying the in Taiwan and West Nile virus in the USA), Cx. vishnui first house and then inspecting surrounding residences. (a Japanese encephalitis vector in Taiwan), and Ae. vexans The sample size was 50–147 premises per village per visit. vexans (an eastern equine encephalitis vector in the USA). In total, 650, 1,200, and 108,097 premises (63.3%, 143.7% and The five species of mosquito from three genera collected 373.2%, respectively, of the total premises in 2003) were on Orchid Island were similar to the collections of Anopheles inspected on Green, Orchid and Penghu Islands, re- mosquitoes in surveys conducted in 1982, 1985, 1987, and spectively. Local inspectors visually identified all larvae, 1990 [8,10]. An. sienesis and An. maculatus were found but such as Aedes spp., on the spot. An. minimus was not. Among the collected mosquito species, An. maculatus and An. sinensis have been reported as malaria vectors in Korea and Mainland China, and Cx. RESULTS quinquefasciatus is a vector of filariasis in Taiwan and West Nile virus in the USA. A total of 14 species of mosquitoes belonging to five genera Japanese entomologists have reported five species were collected on Green Island. Three species of Anopheles, of anopheline mosquitoes on Penghu Island; however, four species of Aedes, five species of Culex, and one species in the Taiwan Provincial Malaria Research Institute studies each of Armigeres and Malaya were identified. Eleven of 1954, only An. sinensis larvae were found [8]. In our study, previously recorded species were not collected in this study two anopheline mosquitoes, An. maculatus and An. sinensis, but 10 collected species had not been previously recorded were collected. Among the collected species, An. maculatus (Table). The newly recorded species were An. maculatus and An. sinensis are known malaria vectors in Korea and Theobald, An. takasagoensis Morishita, Ae. alcasidi Huang, Mainland China, Ae. albopictus is a vector of dengue in Ae. lineatopennis Ludlow, Ae. vexans vexans Meigen, Taiwan and West Nile virus in the USA, Cx. vishnui and Cx. Ar. omissus Edwards, Cx. vishnui Theobald (previously tritaeniorhynchus are Japanese encephalitis vectors in Taiwan, treated as Cx. annulus Theobald in Taiwan), Cx. halifaxii and Cx. quinquefasciatus is a vector of filariasis in Taiwan Theobald, Cx. hayashii Yamada, and Cx. neomimulus Lien. and West Nile virus in the USA. On Orchid Island, where only streams and containers During the investigation, Green and Penghu Islands were were checked, five species of mosquitoes belonging to three each in their dry season and Orchid Island was very windy. genera were collected. Sixteen previously recorded species The number of dengue vector mosquitoes collected on Penghu were not collected in this study but one collected species Island in October 2003 was greater than in January but lower had not been previously recorded. The newly recorded than the highest which was recorded in March (Figure 4). species was Ar. subalbatus Coquillett. Another small peak was detected in June. In this investigation, Only streams and containers were checked on Penghu only Ae. albopictus was collected, but the September 2004 Island, yielding six species of mosquitoes belonging to routine survey found 6.7% Ae. aegypti and 93.3% Ae. albopictus three genera. Twelve previously recorded species were not (CDC, unpublished data). The seasonal fluctuation may be collected in this study. attributed to a combination of the two species of Aedes and The density of mosquitoes collected in September and mosquito preventative measures, in the form of mosquito- October 2003 was low for both larvae (0.002–0.056 An. breeding site reductions, conducted at the time of the maculatus or An. sinensis larvae per dip) and adults (Table). On inspections. The population densities of dengue vectors on two to three consecutive nights, the light traps collected Green and Orchid Islands were not clear because of the low a total of 10 females on Green Island, 18 females on Orchid density of these mosquitoes and the small number of villages Island, and eight females and two males on Penghu Island. examined. Ae. aegyptii was recorded on Orchid Island [9,10] but not on Green Island [9] before 1978. Our data did not confirm the presence of this species on Orchid Island. DISCUSSION

In this study, 14 species of mosquitoes belonging to five genera ACKNOWLEDGMENTS were collected on Green Island. In 1953, only An. sinensis was found [8]. Among the collected mosquito species, potential This study was partially supported with a research grant

Kaohsiung J Med Sci February 2005 ¥ Vol 21 ¥ No 2 53 H.J. Teng, G.C. Huang, Y.C. Chen, et al

Table. Mosquito species on Green Island, Orchid Island, and Penghu Island before 1978 and in 2003 surveys

Mosquito Before 1978 [9] 2003 surveys Collection sites species Green Island Orchid Island Penghu Island Green Island Orchid Island Penghu Island

An. indefinitus ––+––– – An. ludlowae ––+––– – An. maculatus –++33L1P3F 10L 1L Stream, light trap An. minimus +++––– – An. sinensis +++8L1P 9L16F 5L Stream, pond, light trap An. takasagoensis –––1L––Stream An. tessellatus +–+––– – Ae. aegypti –++––– – Ae. albolineatus +––––– – Ae. albopictus +++23L – 9L1F Artificial container, light trap Ae. alcasidi –+–4L– –Rock hole Ae. lineatopennis –––6L– –Pond Ae. v. vexans ––+2F– –Light trap Ar. baisasi –+–––– – Ar. omissus –––1P– –Plant axil Ar. subalbatus ––+– 1F – Light trap Cx. alis –+–––– – Cx. bicornutus ++–81L – – Stream, artificial container Cx. bitaeniorhynchus +++–16L – Stream, pond Cx. fuscanus +++––– – Cx. fuscocephala +++––– – Cx. halifaxii –––1P– –Artificial container Cx. hayashii –––7L––Stream Cx. neomimulus –––17L – – Artificial container, pool Cx. quinquefasciatus +++– 1F 6F1M Light trap Cx. sitiens ––+––– – Cx. tritaeniorhynchus +++– –1FLight trap Cx. vishnui –++4P5F – 1F Stream, light trap Ml. genurostris ++–2L– –Plant axil Mi. luzonensis –+–––– – Oc. melanopterus ++–––– – Oc. togoi +++––– – Or. anopheloides +––––– – Or. lanyuensis –+–––– – Tp. cheni –+–––– – Genus total 5 8 4 5 3 3 – Species total 15 21 18 14 5 6 –

An. = Anopheles; Ae. = Aedes; Ar. = Armigeres; Cx. = Culex; Ml. = Malaya; Mi. = Mimomyia; Oc. = Ochlerotatus; Or. = Orthopodomyia; Tp. = Tripteroides; F = female; L = larval stage; M = Male; P = pupal stage (all pupae were identified at adult stage).

(DOH92-DC-2009) from the Center for Disease Control, Heng Lan (retired), Miss Chao Lin from the CDC, and Department of Health, ROC. We wish to thank Mr. Chun- inspectors from the Penghu and Taitung Health Bureaus for

54 Kaohsiung J Med Sci February 2005 ¥ Vol 21 ¥ No 2 Mosquitoes of Green, Orchid, and Penghu Islands

4.5 Figure 4. Monthly succession Green Island of dengue vectors on Green 4.0 Orchid Island Island, Orchid Island, and ▲ Penghu Island Penghu Island in 2003 (CDC 3.5 data).

3.0

2.5

immatures per 100 premises

Aedes 2.0 ▲

(Breteau Index)

1.5 ▲ ▲ ▲ 1.0 ▲ ▲ ▲ 0.5 ▲ ▲

No. of containers with ▲ ▲ 0.0 ▲ 123 456 7891011 12 Month their participation in the surveys. implications for the epidemiology of Japanese and Murray Valley encephalitis viruses in Australia. J Med Entomol 2000; 37:797–801. 6. Johansen CA, Nisbet DJ, Zborowski P, et al. Flavivirus iso- REFERENCES lations from mosquitoes collected from western Cape York Peninsula, Australia, 1999–2000. J Am Mosq Control Assoc 1. Beaty BJ, Marquardt WC. The Biology of Disease Vectors. Niwot, 2003;19:392–6. CO: The University Press of Colorado, 1996. 7. Feighner BH, Pak S, Novakoski WL, et al. Reemergence of 2. White DJ, Kramer LD, Backenson PB, et al. Mosquito Plasmodium vivax malaria in the Republic of Korea. Emerg surveillance and polymerase chain reaction detection of Infect Dis 1998;4:295–7. West Nile virus, New York State. Emerg Infect Dis 2001;7: 8. Department of Health, Executive Yuan, R.O.C. Malaria 643–9. Eradication in Taiwan, 1991. 3. Estrada-Franco JG, Navarro-Lopez R, Beasley DWC, et al. 9. Lien JC. Ecology and control of mosquitoes in Taiwan. Special West Nile virus in Mexico: evidence of widespread circulation Publication of the Institute of Zoology, Academia Sinica 1978;3: since July 2002. Emerg Infect Dis 2003;9:1604–7. 37–69. [In Chinese] 4. Russell RC. Vectors vs. humans in Australia—who is on top 10. Lien JC, Cheng CI, Lien SC. A team approach to a disease down under? An update on vector-borne disease and research survey on an aboriginal island (Orchid Island, Taiwan). IV. on vectors in Australia. J Vector Ecol 1998;23:1–46. Mosquitoes and chiggers on Lan-Yu (Orchid Island), Taitung 5. Kay BH, Farrow RA. Mosquito (Diptera: Culicidae) dispersal: Hsien, Taiwan. Chin J Microbiol 1974;7:36–41.

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