Mosquito Surveys Carried out On Green Island, Orchid Island, and Penghu Island, Taiwan, in 2003

Mosquito Surveys Carried out On Green Island, Orchid Island, and Penghu Island, Taiwan, in 2003

Mosquitoes of Green, Orchid, and Penghu Islands MOSQUITO SURVEYS CARRIED OUT ON GREEN ISLAND, ORCHID ISLAND, AND PENGHU ISLAND, TAIWAN, IN 2003 Hwa-J...

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Mosquitoes of Green, Orchid, and Penghu Islands

MOSQUITO SURVEYS CARRIED OUT ON GREEN ISLAND, ORCHID ISLAND, AND PENGHU ISLAND, TAIWAN, 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, Taipei, 1Penghu County 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) (Kaohsiung J Med Sci 2005;21:51–6)

There are about 500 arboviruses in the world. Wild animals often serve as amplifiers or reservoirs of these vector-borne infectious diseases [1]. Occasionally, these viruses are transmitted from animals to humans by a group of mosquito vectors. The infection may then be transmitted from infected humans to other humans by a different group of mosquito vectors. Due to the increasing mobility of humans and animals through modern transportation, mosquito-borne infectious diseases are spreading. The introduction of the

Received: October 21, 2004 Accepted: January 4, 2005 Address reprint requests and correspondence to: Dr. Hwa-Jen Teng, Medical Entomological Laboratory, Research and Development Center, Center for Disease Control, Department of Health, 161 KunYang Street, Nan-Kang, Taipei 115, Taiwan. E-mail: [email protected] Kaohsiung J Med Sci February 2005 • Vol 21 • No 2 © 2005 Elsevier. All rights reserved.

West Nile virus to North America [2,3], Ross River fever to the South Pacific [4], Japanese encephalitis to Australia [5, 6], and a reemergence of malaria in Korea are examples of this [7]. Basic information about mosquito status in various locations is important to understand the risk of mosquitoborne infectious diseases in specific areas. Mosquitoes on Green Island, Orchid Island, and Penghu Island in Taiwan have been studied exclusively in connection 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 of mosquito distribution in Taiwan, including on Green, Orchid, and Penghu Islands [9]. No papers related to the mosquitoes on these islands have been published since that time. This paper is a record of our survey results from 2003. It provides information about the mosquitoes on these 51

H.J. Teng, G.C. Huang, Y.C. Chen, et al

islands and briefly discusses the potential vector status of mosquito species.

N

Zhongliao Village Gongguan Village

MATERIALS AND METHODS Survey areas 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 Islands are small island townships of Taitung County in the Pacific Ocean. Green Island, with an area of approximately 15 km2, is located 10 km east of Taitung City at 22°38’– 22°42’ N and 121°27’–121°33’ E. The temperature remains between 20°C and 29°C and it rains year round. Orchid 2 Island, with an area of approximately 48 km , is situated about 80 km southeast of Taitung City at 22°00’–22°60’ N 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 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.

Mosquito collection The survey was conducted on Green Island in September 2003 and on Orchid and Penghu Islands in October 2003. The geological positioning system, GeoExplorer 3 (Trimble Navigation Ltd, Sunnyvale, CA, USA), was used to locate the collection sites (Figures 1–3). Although immature mosquitoes were collected mainly from streams, they were also taken from 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. A Pest-O-Lite trap placed near a house and a Center for Disease Control (CDC) light trap placed in a field near a breeding stream were used to collect adult mosquitoes on 2 or 3 consecutive nights. Mosquitoes were observed under microscopes in the laboratory and identified with mosquito keys for Taiwan prepared by the CDC. Dengue vector mosquitoes were collected monthly by the local health bureaus in Taitung and Penghu Counties. The village sample proportion (number of village surveys/ total number of villages) varied from 33.3% to 207.2% per month except for January and February in Penghu Island (8.2%). There were three villages on Green Island, four on 52

Nanliao Village

Adult collection site Larval collection site

0

Road

750

1,500

3,000 Meters

Figure 1. Mosquito collection sites on Green Island, Taitung County. N

Langdao Village

Yeyou Village

Dongqing Village

Hongtou Village

Adult collection site Larval collection site Road

0

0.5

1

2

3

4

Km

Figure 2. Mosquito collection sites on Orchid Island, Taitung County. N

Paisha Township

Shiyu Township

Hushi Township

Kouyieh Village

Magong City

Adult collection site Larval collection site Road 0 0.5 1

2

3

4 Km

Figure 3. Mosquito collection sites on Penghu Island. 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 sampling technique was used to sample residential premises in each village by randomly selecting and surveying the first house and then inspecting surrounding residences. The sample size was 50–147 premises per village per visit. In total, 650, 1,200, and 108,097 premises (63.3%, 143.7% and 373.2%, respectively, of the total premises in 2003) were inspected on Green, Orchid and Penghu Islands, respectively. Local inspectors visually identified all larvae, such as Aedes spp., on the spot.

RESULTS A total of 14 species of mosquitoes belonging to five genera were collected on Green Island. Three species of Anopheles, four species of Aedes, five species of Culex, and one species each of Armigeres and Malaya were identified. Eleven previously recorded species were not collected in this study but 10 collected species had not been previously recorded (Table). The newly recorded species were An. maculatus Theobald, An. takasagoensis Morishita, Ae. alcasidi Huang, Ae. lineatopennis Ludlow, Ae. vexans vexans Meigen, Ar. omissus Edwards, Cx. vishnui Theobald (previously treated as Cx. annulus Theobald in Taiwan), Cx. halifaxii Theobald, Cx. hayashii Yamada, and Cx. neomimulus Lien. On Orchid Island, where only streams and containers were checked, five species of mosquitoes belonging to three genera were collected. Sixteen previously recorded species were not collected in this study but one collected species had not been previously recorded. The newly recorded species was Ar. subalbatus Coquillett. Only streams and containers were checked on Penghu Island, yielding six species of mosquitoes belonging to three genera. Twelve previously recorded species were not collected in this study. The density of mosquitoes collected in September and October 2003 was low for both larvae (0.002–0.056 An. maculatus or An. sinensis larvae per dip) and adults (Table). On two to three consecutive nights, the light traps collected a total of 10 females on Green Island, 18 females on Orchid Island, and eight females and two males on Penghu Island.

vectors are 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 (a Japanese encephalitis vector in Taiwan), and Ae. vexans vexans (an eastern equine encephalitis vector in the USA). The five species of mosquito from three genera collected on Orchid Island were similar to the collections of Anopheles mosquitoes in surveys conducted in 1982, 1985, 1987, and 1990 [8,10]. An. sienesis and An. maculatus were found but 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. quinquefasciatus is a vector of filariasis in Taiwan and West Nile virus in the USA. Japanese entomologists have reported five species of anopheline mosquitoes on Penghu Island; however, in the Taiwan Provincial Malaria Research Institute studies of 1954, only An. sinensis larvae were found [8]. In our study, two anopheline mosquitoes, An. maculatus and An. sinensis, were collected. Among the collected species, An. maculatus and An. sinensis are known malaria vectors in Korea and Mainland China, Ae. albopictus is a vector of dengue in Taiwan and West Nile virus in the USA, Cx. vishnui and Cx. tritaeniorhynchus are Japanese encephalitis vectors in Taiwan, and Cx. quinquefasciatus is a vector of filariasis in Taiwan and West Nile virus in the USA. During the investigation, Green and Penghu Islands were each in their dry season and Orchid Island was very windy. The number of dengue vector mosquitoes collected on Penghu Island in October 2003 was greater than in January but lower than the highest which was recorded in March (Figure 4). Another small peak was detected in June. In this investigation, only Ae. albopictus was collected, but the September 2004 routine survey found 6.7% Ae. aegypti and 93.3% Ae. albopictus (CDC, unpublished data). The seasonal fluctuation may be attributed to a combination of the two species of Aedes and mosquito preventative measures, in the form of mosquitobreeding site reductions, conducted at the time of the inspections. The population densities of dengue vectors on Green and Orchid Islands were not clear because of the low density of these mosquitoes and the small number of villages 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 were collected on Green Island. In 1953, only An. sinensis was found [8]. Among the collected mosquito species, potential Kaohsiung J Med Sci February 2005 • Vol 21 • No 2

ACKNOWLEDGMENTS This study was partially supported with a research grant 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 species

Before 1978 [9] Green Island

2003 surveys

Collection sites

Orchid Island Penghu Island Green Island Orchid Island Penghu Island

An. indefinitus An. ludlowae An. maculatus

– – –

– – +

+ + +

– – 33L1P3F

– – 10L

– – 1L

An. minimus An. sinensis

+ +

+ +

+ +

– 8L1P

– 9L16F

– 5L

An. takasagoensis An. tessellatus Ae. aegypti Ae. albolineatus Ae. albopictus

– + – + +

– – + – +

– + + – +

1L – – – 23L

– – – – –

– – – – 9L1F

Ae. alcasidi Ae. lineatopennis Ae. v. vexans Ar. baisasi Ar. omissus Ar. subalbatus Cx. alis Cx. bicornutus

– – – – – – – +

+ – – + – – + +

– – + – – + – –

4L 6L 2F – 1P – – 81L

– – – – – 1F – –

– – – – – – – –

Cx. Cx. Cx. Cx.

+ + + –

+ + + –

+ + + –

– – – 1P

16L – – –

– – – –

Cx. hayashii Cx. neomimulus

– –

– –

– –

7L 17L

– –

– –

Cx. Cx. Cx. Cx.

+ – + –

+ – + +

+ + + +

– – – 4P5F

1F – – –

6F1M – 1F 1F

+ – + + + – – 5 15

+ + + + – + + 8 21

– – – + – – – 4 18

2L – – – – – – 5 14

– – – – – – – 3 5

– – – – – – – 3 6

bitaeniorhynchus fuscanus fuscocephala halifaxii

quinquefasciatus sitiens tritaeniorhynchus vishnui

Ml. genurostris Mi. luzonensis Oc. melanopterus Oc. togoi Or. anopheloides Or. lanyuensis Tp. cheni Genus total Species total

– – Stream, light trap – Stream, pond, light trap Stream – – – Artificial container, light trap Rock hole Pond Light trap – Plant axil Light trap – Stream, artificial container Stream, pond – – Artificial container Stream Artificial container, pool Light trap – Light trap Stream, light trap Plant axil – – – – – – – –

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, Department of Health, ROC. We wish to thank Mr. Chun54

Heng Lan (retired), Miss Chao Lin from the CDC, and inspectors from the Penghu and Taitung Health Bureaus for Kaohsiung J Med Sci February 2005 • Vol 21 • No 2

No. of containers with Aedes immatures per 100 premises (Breteau Index)

Mosquitoes of Green, Orchid, and Penghu Islands 4.5

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

Green Island Orchid Island ▲ Penghu Island

4.0 3.5 3.0 2.5 ▲

2.0 1.5 1.0





▲ ▲





0.5





0.0 1

2

3

4

5

6

7

8

9







10

11

12

Month

their participation in the surveys.

REFERENCES 1. Beaty BJ, Marquardt WC. The Biology of Disease Vectors. Niwot, CO: The University Press of Colorado, 1996. 2. White DJ, Kramer LD, Backenson PB, et al. Mosquito surveillance and polymerase chain reaction detection of West Nile virus, New York State. Emerg Infect Dis 2001;7: 643–9. 3. Estrada-Franco JG, Navarro-Lopez R, Beasley DWC, et al. West Nile virus in Mexico: evidence of widespread circulation since July 2002. Emerg Infect Dis 2003;9:1604–7. 4. Russell RC. Vectors vs. humans in Australia—who is on top down under? An update on vector-borne disease and research on vectors in Australia. J Vector Ecol 1998;23:1–46. 5. Kay BH, Farrow RA. Mosquito (Diptera: Culicidae) dispersal:

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6.

7.

8. 9.

10.

implications for the epidemiology of Japanese and Murray Valley encephalitis viruses in Australia. J Med Entomol 2000; 37:797–801. Johansen CA, Nisbet DJ, Zborowski P, et al. Flavivirus isolations from mosquitoes collected from western Cape York Peninsula, Australia, 1999–2000. J Am Mosq Control Assoc 2003;19:392–6. Feighner BH, Pak S, Novakoski WL, et al. Reemergence of Plasmodium vivax malaria in the Republic of Korea. Emerg Infect Dis 1998;4:295–7. Department of Health, Executive Yuan, R.O.C. Malaria Eradication in Taiwan, 1991. Lien JC. Ecology and control of mosquitoes in Taiwan. Special Publication of the Institute of Zoology, Academia Sinica 1978;3: 37–69. [In Chinese] Lien JC, Cheng CI, Lien SC. A team approach to a disease survey on an aboriginal island (Orchid Island, Taiwan). IV. Mosquitoes and chiggers on Lan-Yu (Orchid Island), Taitung Hsien, Taiwan. Chin J Microbiol 1974;7:36–41.

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