Journal of the American Control Association, 16(2):lOO-l 13,2000 Copyright O 2000 by the American Mosquito Control Association, Inc.

MOSQUITO SURVEILLANCE IN THE DEMILITARIZED ZONE, REPUBLIC OF KOREA, DURING AN OUTBREAK OF IN 1996 AND 19971

DANIEL STRICKMAN,, MARY E. MILLER,3 HELTNG-CHUL KIM INo KWAN-WOO LEE

5th Medical Detachment, 18th Medical Command, Yongsan Garrison, Seoul, Republic of Korea (APO AP 96205-0020)

ABSTRACT, Since 1993, more than 2,0OO cases of vivax malaria have occurred in the Republic of Korea in an epidemic that ended nearly 20 malaria-free years. Most malaria has occurred in the northwestern part of the country, mainly affecting Korean military personnel. As a part of an operational surveillance effort, we sampled mosquitoes in and near the Demilitarized Zone (Paju County, Kyonggi Province) during the last 2 wk of July in 1996 and from May 15 to September 10 in 1997. The 1st year, landing collections were done at 5 different sites; the 2nd year, carbon-dioxide-baited light traps at 5 sites, larval collections in 10 adjacent fields, and landing collections at 1 site in the Demilitanzed Zone were performed weekly. Of 17 species collected, sinensis was consistently the most abundant mosquito, comprising 79-96Vo of mosquitoes. The diel pattern of biting by An. sinensis varied by location and season, with the majority of individuals biting late at night during warm weather (>20"C) and early at night during cool weather. In contrast, Aedes vexans nipponii (the 2nd most abundant species) bit in the greatest numbers at the same time all season, from 2000 to 2300 h. Among the correlates with abundance of An. sinensis were average nighttime temperature 2 wk previous to the night in question, wind late at night (negatively correlated), and apparent size of the moon (negatively correlated). The data showed that the exact number of An. sinensis biting could not be estimated from numbers collected in carbon-dioxide-baited light traps. On the other hand, a threshold of 15 An. sinensis per trap night corresponded (88Vo accttacy) to a threshold of 12 mosquitoes biting 2 adjacent collectors per night. Larval collections were also significantly correlated with landing collections, despite inexact sampling methods and separation of the larval habitat from the site where landing collections were performed. Operational entomology assets using nighttime temperature records, carbon-dioxide-baited light traps, and larval collections should be able to target their efforts in Korea more efficiently.

KEY WORDS Anopheles sinensis, Plasmodium vivax, malaria, surveillance, Korea

INTRODUCTION spread to many points near the border from Chor- won west to Kangwha Island and south to Inchon The Republic of Korea (ROK) currently is ex- and Seoul (Lee et al. 1998). More infected soldiers periencing an expanding epidemic of Plasmodium (total of 1,596 cases from 1993 through 1997, in- vivax malaia (Feighner et al. 1998, Lee et al. cluding 40 cases in U.S. Army personnel; Feighner 1998). The lst case in the last 2O years occurred in et al. 1998) than infected civilians (total of650 cas- 1993 (Chai et al. 1994), followed by 2 more cases es, Lee et al. 1998) have been detected. in 1994 (Cho et al. 1994). Since then, the number Malaria is not new to Korea (Paik et al. 1988). of new malaria infections has risen exponentially In 1910. the lst documented cases were described to the unofficial total of more than 1,600 cases in from occupying Japanese forces and Korean civil- ROK military personnel in 1998, despite applica- ians distributed throughout the peninsula. The num- tion of chemoprophylaxis to 35,000 ROK troops ber of cases declined steadily during the 1930s (Seminar for Malaria Control, Korean National In- for unknown reasons. Malaria again major stitute of Health, November 25. 1998). The lst 3 became a problem during Korean (1950-53), cases included 2 Korean soldiers stationed near the War when Panmunjom, Paju County, Kyonggi Province. The U.S. forces suffered a 6.6Vo attack rate. In 1960, other case was a civilian woman in the nearby town the ROK and the World Health Organization initi- of Munsan, only 4 km from the edge of the De- ated the National Malaria Eradication Service militarized Zone (DlvlZ) separating the ROK from (NMES). The NMES performed active and passive the People's Democratic Republic of Korea case detection documenting widespread distribution (PDRK). During the next 4 years, the outbreak of vivax malaria in 1960, with the greatest number of cases in the eastern mountains (Kyungsang Puk- do Province). Treatment of cases, vector control, 'The views of the authors do not purport to reflect the and a general improvement in living conditions re- position of the Department of the Army or the Department duced malaria transmission so that by 1965 the only of Defense (para 4-3, AR 360-5). Mention of specific areas with malaria were northwest of Seoul (in- products should not be considered an endorsement. 'To whom corespondence should be addressed at De- cluding the area where the current epidemic start- partment of Entomology, Walter Reed Army Institute of ed), east of Seoul, and the eastern mountainous Research, Washington, DC 20307-5100. area. The NMES was disbanded in 1970 when ma- 3 Present address: 10852 CTY NN. Milton. WI 53563. laria was very much reduced. A thorough search in

100 Moseurross AND MALARIA IN THE DMZ, KoREA 101

were present in Tongil'chon and a pig farm and some domesticated deer were present in Tae- song'dong. The area included numerous ROK and American military activities, including garrisons, training areas, and weapon ranges. A broad valley at least 2 km wide was located on the other side of the border in the PDRK. This valley was almost Panmunlom completely cultivated in rice, which was observed \ on several occasions to be worked with oxen by \*' ." okr"ho^. residents of nearby villages. Higher ground to the \ range ofrocky moun- t north ofthe valley rose into a tains that lacked wooded cover. The population on Sonrfas Teras \ the PDRK side of the border also included consid- \I erable numbers of soldiers, who were sometimes War.ior i Base visible from the DMZ. Sampling in 1996: Landing collections were made from 1800 to 0600 h, with I pair of soldiers 3 s-. o= collecting for 2 h and then switching with another 3: t. pair of soldiers. All landing mosquitoes were cap- E: E. tured with an aspirator and then blown into a paper E6 carton cage, separating each hour's collection. Col- 3: 9l:, :: z- lectors wore the standard U.S. Army field uniform (Battle Dress Uniform, not treated with permethrin) tkm 2: b. and sat with the legs of the trousers rolled up to the knee. Most mosquitoes were collected from ex- Fig. l. Map of study sites in military-controlled area posed skin on the collector's own legs; however, of Paju County. mosquitoes anywhere on exposed skin were cap- tured. Occasions occurred when it was more con- 1986 failed to find a single case in the area where venient for a collector to capture a mosquito from malaria had once been most prevalent. his partner. Temperature and wind speed (as maxi- The principal purpose of the current study was mum value during 90 sec) at the site of the collec- surveillance of malaria vectors as part of a suc- tion were both recorded at the beginning of each cessful effort to protect U.S. forces serving near the hour. DMZ in Paju County. In 1996, only a 2-wk period Five locations within l0 km of each other were was sampled at the time when the vector was sampled in 1996. The placement of collectors at thought to be most abundant. We correctly assumed each location was chosen based on practicality and that the epidemic would increase in 1997, so we proximity to the representative population. The de- planned more extensive vector surveillance in order cision was made to place collectors at a small dis- to make the following determinations: what non- tance (10-50 m) from military or civilian residents vector species of mosquitoes are likely to generate for 2 reasons. First, collectors were active all night complaints about biting in the DMZ; whether diel so that their presence would have been disruptive periodicity of Anopheles sinensis Wiedemann var- for local residents and, 2nd, the number of mos- ied seasonally; whether carbon-dioxide-baited light quitoes attracted to collectors was less likely to be trap and larval collection data could be correlated influenced by movement of residents. Tongil'chon to biting collections of An. sinensls; and whether was a village with approximately 1,000 inhabitants, temperature, wind, and moon could be used to pre- modern masonry housing, paved streets, running dict the biting rate of An. sinensis. water, and electricity. Collections were made at the edge of the village on a small dairy farm overlook- ing a valley with rice fields. Camp Bonifas was a MATERHLS AND METHODS military post adjacent to the DMZ bordered on I Study site: This study was conducted in a mili- side by rice fields. The West Bonifas site was less tary-controlled area north of the Imjin River near than 50 m from the rice fields, whereas the East Panmunjom (37'55'N, 126"38'E; Fig. 1). The area Bonifas site was in the angle of low hills and at consisted of low wooded hills interspersed with val- least 300 m from the nearest rice field. Observation leys usually planted in rice. Intensive rice culture Point Oullette was on a steep hill (lOO m high) had resulted in a drainage pattern dominated by hu- inside the DMZ and directly adjacent to the Mili- man-managed irrigation, with few natural streams tary Line of Demarcation between the 2 Koreas. or ponds. Other crops in the area included peppers, Collections were made just south of the crest of the corn, and ginseng. Large domestic were lo- hill. Taesong'dong was the only ROK civilian vil- cated at only a few sites, probably because of a lage in theDMZ, with approximately 750 residents. curfew on civilian nighttime activity. Dairy cattle Collections were made near the church, within site t02 JounNer- op rgE AvpnrcAN Moseurto CoNTRoL AssocntoN VoL. 16,No.2 of both giant flags raised on towers by the ROK relations), and 2-tailed, linear partial correlation and the DPRK. (Correlation, PartiaD. Phases of the moon and times Sampling in 1997: Following the resulrs of 1996, of sunrise and sunset were calculated using the In- we were particularly concerned about the possibil- teractive Computer Ephemeris (Version 0.51, U.S. ity of seasonal variation in diel periodicity that Naval Observatory Nautical Almanac Office, would have affected the efficacy of insecticidal fog- Washington, DC). ging. In addition, the work was designed to find a The relationship between light trap and landing correlation between light trap, larval, and landing collections was studied by performing linear re- collections, so that light trap and larval survey re- gression on the log of total female An. sinensis in sults could be interpreted according to real risk to the Taesong'dong trap, the mean of females per trap soldiers. These efforts also provided data that could for all 5 light traps, and females captured by 2 col- be used to test the correlation between weather fac- lectors per night. Only 3 observations from the Tae- tors and landing collections. By recording the oc- song'dong light trap had no An. sinensis, which currence of nonanopheline mosquitoes, we devel- then required adjustment by adding l. All other ob- oped information on the biting pressure to be servations were greater than zero, so that a log(r * expected from nonvector species. 1) adjustment was not necessary.a The analysis in- Weekly light trap (Solid State Army Miniature volved a test of the possibility that the ratio of light trap, Driggers et al. 1980) and landing collections trap to landing collections was related to density of were made at Taesong'dong from May 15 to Sep- mosquitoes. We performed the same analysis as tember lO, 1997. Only the week of July 9 was Lines et al. (1991) on our data, regressing the ratio missed, because of a military alert. Traps were of the log of light trap and landing collections on hung from a tree or fence about 1.5 m above the the geomeric mean of light trap and landing ground. Each trap was operated with the light on counts. and was baited with carbon dioxide provided by In a separate analysis, we examined the signifi- dry ice in an insulated, l-liter jug with an open pour cance of a threshold number of female An. sinensis spout. Using this arrangement, the dry ice always in light traps that might correspond to a minimum lasted the entire night. The locations of traps in- number of biting mosquitoes. This analysis was ac- cluded Taesong'dong (approximately 300 m from complished by comparing a series of threshold val- the landing collection site) and 4 weapons training ues of the mean of all 5 light traps to a minimum ranges (designated Texas, Kansas, New Mexico, biting rate (>12 bites per night for 2 collectors). and Oklahoma) located within 15 km of Tae- The correspondence of each threshold value was song'dong. Larvae were collected from lO rice evaluated for standard epidemiologic measurements fields on the morning after each landing collection. (sensitivity, specificity, and accuracy) and tested for The fields were across the road (Highway 1) from significance by chi-square (Griner et al. 1981). The Warrior Base, located I km from Camp Bonifas and threshold with the greatest accuracy and sensitivity 4 km from Taesong'dong. In an effort to perforrn was considered the most appropriate. larval collection in a standard manner. 4 collectors spread out among the fields and captured as many RESULTS anopheline larvae as possible during 30 min of dip- ping with a shallow pan (20 X 36 cm). Each week, Although the data from 1997 were more exten- a subsample of the larvae was reared to the adult sive, the 1996 data had the advantage of greater stage for identification. replication over a short period of time and sampling Analyses: Morphologic characters of adults (K. from several different sites, Anopheles sinensis was W. Lee 1998) were used to identify mosquitoes. consistently the most abundant biting mosquito in Although the characters used to distinguish be- 1996, comprising 79.3-95.8Vo of the mosquitoes tween An. sinensis and An. lesteri Baisas and Hu were sometimes obscured in light trap samples, a Avoiding this adjustment overcame the objection of landing collections produced specimens in much Smith (1995) to the analysis of Lines et al. (1991). Smith better condition. Representative specimens were (1995) was concerned (for landing collections represented deposited in the collection of the 5th Medical De- by x and light trap collections represented by y), that tachment, 18th Medical Command, Yongsan Gar- whereas for constant xly and, changing mosquito density rison. Seoul. ROK. values the ratio of log(-r) to log(v) would be constant, the Excel97 (Microsoft Corp., Seattle, WA) or SPSS ratio of log(-r + l) to log(y + l) would not be constant. (SPSS for Windows, Release 6.1.2, SPSS Inc., Chi- Because log conversion was considered necessary to cago, IL) software were used to perform statistical achieve linearity, the inequivalence of log(,r) and log(x f make analyses. Excel9T calculated linear regression and l) would it difficult analyze constancy of the ratio of landing to light trap collections with respect to mos- SPSS performed chi-square tests of 2 X 2 contin- quito density. Smith (1995) suggested that the problem (Crosstabs gency tables procedure with Pearson's could be avoided if collections were sufficiently large to estimate of chi-square), analysis of variance (one- avoid the log(x + l) conversion or by using Poisson re- way ANOVA with Duncan's multiple range test), gression techniques. Our data allowed us to use the former cross correlation (Graphs, Time Series, Cross Cor- solution. Jurr 20OO Moseurrors eNo MlLnnn nq tHr DMZ, Konte l03

Table 1. Mosquitoes captured >5 times in landing collections at 5 locations in and near the DemilitarizedZone, Republic of Korea, between July 23 and August 2,1996.

Location (No. of nights of collection) E Bonifas (4) Oulleue (2) Taesong (5) Tongil (2) W Bonifas (6)

Species No.l Va2 No. No. Va No. No Vo '72.2 Anopheles sinensis 376.2 95.8 163.0 86.5 79.3 87.0 87.4 278.2 88.2 An. lesteri 6.0 1.5 5.5 2.9 1.6 1.8 s.0 5.0 5.7 1.8 An. yatsushiroensis 0.8 0.2 3.5 1.9 2.8 3.1 0.5 0.5 1.2 0.4 Culex pipiens 6.2 1.6 1.0 0.5 10.2 tl.z 3.5 3.5 8.3 2.6 Aed,es vexans 1.5 0.4 8.5 4.5 2.O 2.2 2.O 2.O 21.7 6.9 Ae. alboscutellaras (Theobald) 1.0 0.3 00 o.4 0.4 0.5 0.5 00

'Per night per 2 collectore. 'Of total at that location. collected at the 5 sites (Table 1). The next most pearance (July 16-August 6). Examining the 2 most abundant biting species, Aedes vexans nipponii abundant species more closely (Fig. 2), Ae. vexans (Theobald), exceeded 0.5 bites/person/h at only I lst appeared early in the season (May) and gradu- site, West Bonifas. Anopheles sinensis, An. lesteri, ally increased in numbers through a series of prob- An. yatsushiroensis Miyazaki, Culex pipiens pal- ably 3 broods. Anopheles sinensis increased sud- /ens Coquillett, and Ae. vexans nipponii were the denly in late June and peaked late in the season. only species present at all 5 sites. Species collected The diel pattern of landing by An. sinensis was landing on humans less than 5 times were An. si- not the same at each location in 1996 (Fig. 3). The neroides Yamada, Cx. bitaeniorhynchus Giles, Cx. pattern of landing at East Bonifas (n : 4 nights) orientalis Edwards, Cx. mimeticus Noe, Cx. tritae- and Tongil'chon (n : 2 nights) was biphasic. In niorhynchus Giles, Ae. koreicus (Edwards), Ae. al- contrast, the pattern of landing at Taesong'dong (n bopictus (Skuse), Ae. esoensis Yamada, Ae. nippon- : 3 nights) and West Bonifas (n : 6 nights) was icus LaCasse and Yamaguti, and Armigeres a single, late-night peak. Despite this variation in s ubalb atus (Coquillett). diel pattern at different locations, it was still useful The species of mosquitoes collected in landing to examine the pattern of activity of landing mos- collections in 1997 followed several different pat- quitoes for all locations during a short sampling terns of seasonality (Table 2). All abundant species period (2 wk), which represented a single point in persisted until late in the season (September), but the seasonal cycle of abundance. The average pat- some appeared earlier (in May, Ae. vexans, An. si- tern for the entire area during late July (determined nensis, Cx. pipiens) than others (in June, Ae. ko- by summing hourly landing collections from all lo- reicus, Ae. albopictus, An. lesteri, Cx. bitaenior- cations for a total of 19 nights) was a peak in land- hynchus). The earlier group gradually increased to ing late at night. Analysis of variance of all loca- mildmum numbers later in the year (August 6-27). tions showed significant differences in number of In contrast, the later group of species reached max- landing An. sinensis between hours of collection (F imum numbers relatively soon after their lst ap- : 3.05, dt : ll,216, P : 0.0008), with statistically

Table 2. Seasonality of mosquitoes collected more than oncer in landing collections during 1997 at Taesong'dong

Date of

Species Total collected First collection Lastcollection Hiehestcollection

Aedes vexans 521 May 15 Sept. l0 Aug. l3 Anopheles sinensis 1,164 May 15 Sept. l0 Aug.27 Culex pipiens 70 May 15 Sept. 10 Aug. 6 Ae. koreicus 66 June 4 Sept. 3 July 16 Ae. albopictus June 11 Sept. 10 Iuly 23 Ae. esoensis 9 June I I Sept. 3 htly 23 An. lesteri 105 June I I Sept. 10 Aug. 6 An. yatsushiriroensis 5 June 24 Iuly 23 htly 3-23 Cx. bitaeniorhynchus 150 June 24 Sept. 3 July 28 Cx- orientalis 10 July 16 Sept. 3 Aug.27 Armigeres subalbatus 16 July 23 Sept. 10 Aug.27 Ae. nipponicus i July 23 July 28 July 28 Ae. alboscutellatus 4 Aug. 13 Aug. 13 Aug. 13 Cx. tritaeniorhynchus t6 Aug. 13 Sept- 10 Aug. l8

I Species colltrted only once: Cx- vagans Wiedemann, May 15; Ae. bekkui Mogi, June l8; Mansonia unifomis (Theobald), Aug. 18. JounNar- oF rns A[4pnrceN Mosqutro CoNrnol Assocra.noN

250 homogeneous groups of 1800-0200 h and 0500 h, F 200 2300-0300 h, and 0200-O400 h. The diel landing pattern of An. sinensis was unique among the 16 150 species collected in 1996 (Table 3). Many of these z species were collected rarely, but the data are in- U) r00 cluded because studies concentrating on these spe- U) cies are unlikely to occur in the near future. The 2 50 species with diel patterns of landing most similar to An. sinensis were An. lestei and,Cx. pipiens pal- 0 lens. Culex bitaeniorhynclrzs was collected only 4 -.-.AE .A 3 times and Ae. esoensis only once, but these includ- *g :E -i< ed late-night collections. All other species were t997 most frequently collected within 2 h after sunset +sinensis -.- vexans (time of sunset between 1942 h and 1951 h during this period). The greatest variety of mosquitoes (10 Fig.2. Seasonal occurrence of Anopheles sinensis and species) was collected Aedes vexans in landing collections (per 2 collectors) in between 2100 h and 2300 h 1997 at Taesong'dong. Note that no sampling took place and the least variety (1 species) between 1800 h on July 9. and l9OO h. Seasonal analysis of An. sinensis and Ae. vexans

100 25 ffro TAESONG E. BONIFAS Ero 860 7', z40 zlo o a- >20 >) 0 0 22W 2M 2400 0200 0400 HOUR HOUR

80 30 '70 c<25 :d 60 W. BONIFAS &o *ro q !+o 9" 230 z,^ fizo 5 0 0 t800 2000 22w 24w 0200 0400 1800 22W 24t0 HOUR

30 )U OULETTE a25 too ALL SITES dzo 8,n o-- 9tt ?'o z2o q.l ql,^ >s >rv 0 0 1800 24rn 22U) 24iJ0 HOUR HOUR Fig. 3. Hourly distribution of Anopheles sinensis captured in landing collections (mean per night for that hour for 2 collectors) during July 23-August 2, 7996, at 5 locations near Panmunjom. Graph for all sites is mean for each hour per night for all locations sampled. JurYe2000 Mosqurrons eNo Malenra rN rur DMZ, Konra IUJ

Thble 3. Total hourly collections of all species of rnosquitoes captured in landing collections (19 all-night collections) at 5 different sites near Panmunjom during July 23-August 2,1996.

ffi Species 1800 1900 2000 2too 2200 2300 2400 0100 0200 0300 0400 0500 Anopheles sinensis 6 12 l08 222 285 391 379 358 410 785 850 229 An. lesteri 0 0 8 8810141081092 An. yatsushiroensis 0 0 11 632223201 An. sineroides o o o 100000000 Culex pipiens 0 0 9 142325159181571 Cx. bitaeniorhynchus 0 0 0 110001100 Cx. orientalis 0 0 0 201100000 Cx. mimeticus 0 0 0 110000000 Cx. tritaeniorhynchus 0 0 0 0r0000000 Aedes vexans 0 0 t14 1797861130 Ae. koreicus 0 0 l1 o00100010 Ae. alboscutellatus 0 o z 2t0101000 Ae. albopictus 0 o 2 o10000000 Ae. esoensis 0 o o o00000010 Armigeres subalbatus 0 o z oooo00000

in 1997 showed that there were 4 statistically dis- May 15, 0511 h on the summer solstice, and 0611 tinct parts of the seasonbased on the ANOVA and h on September l0) were not great enough to be Duncan's multiple range test. These 4 time periods the cause of these seasonal changes in diel landing were May l5-June 18 (6 wk), June 24-July 23 (4 pattern. Although difficult to correlate with diel wk), July 28-August 18 (4 wk), and August 27- landing pattern or total number of An. sinensis, September 10 (3 wk). The pattern of diel period- wind speeds decreased in the latter half of the sea- icity and the total number of mosquitoes both var- son (after JuIy 23), particularly in the early evening. ied seasonally(Fig. 4). Most An. sinensisbit early Nightly variation in temperature documented dur- at night (before 23OOh) in the lst part of the sea- ing ll consecutive nights in 1996 provided some son, tbroughout the night during June 24-July 23 replication of the temperature profile during the (peak at 22OO45OO h), very late at night during peak of the season for An. sinensis (Table 4). Sea- July 28-August 18 (peak at 0200--0500h), and ear- sonal changes in the hourly pattern of temperature lier at night from August 27 to September10 (peak during 1997 were related to changes in the diel at 2O00-23OOh). Changesin time of sunset (1937 landing collection pattern of An. sinensis (Fig. 4). h on May 15, 1959 h on the summer solstice, and In the early part of the season, temperature quickly 1850 h on September l0) and sunrise (0524 h on descended below 20'C, conesponding to a decrease

15 MAY THRU T8 ilJN 28 JUL THRU T8 AUG 50 20 50 20 o40 o4u t{:. tsF' v .^x Ei, lUa Ii' tu- j F20 -z -B SFzo

24 JI,JN THRU 23 JUL 27 AAG THRU TOSEP 50 20 50 20 540 o40 Fn^^ .^l X lu- E E'U E*:: Fzo l0: LF""

;66XVT

Fig. 4. Seasonal diel distribution of Anopheles sinensis in landing collections (solid line), hourly temperature in oC (dashed line), and hourly wind speed (gray line) during 1997, Taesong'dong. JoupNnl on rur AurnIcAN Moseurro Cotrnol Assocrlrrror

Table 4. Hourly temperatureduring 1l nights (July 22-August l) in 1996near Panmunjom.

Temperature ('C) 0.4 Standard z Hour Meanl deviation Range o o) F 1800 28.0 3.41 22.5-33.5 JN lr r.il 1900 27.Vb 2.70 22.5-3r.5 2000 25.7k 2.20 22.O-29.O & -"'n t o 2too 24.8.d 1.99 2l.o-27.O (J 2200 24.7"d 1.56 22.0-26.5 -0.4 2300 24.5,4 1.54 22.0-26.5 2400 24.3.d 1.86 2t.o-2"7.O -0.6 0100 23.9"d 1.66 21.O-27.O 0200 24.Ud l .51 2t.0-26.O -0.8 0300 24.4d 2.21 21.O-29.O -7 -6 -5 -4 -3 -2 -l O | 2 3 4 5 6 7 0400 23.6d 1.38 2r.o-25.O 0500 23.4d 1.39 2r.o-25.O LAG (WEEKS) IMeans not followed by the same superscripted letter were in Fig. 6. Cross-correlation between mean nightly tem- separate homogeneous groups based on analysis of vriance fol- perature (lagged factor) and number of Anopheles sinensis = = lowed by Duncan's multiple range test (F 5.162, df I I,120, captured in landing collections at Taesong'dong, May 15- P < 0.0ool). September lO, 1997. Bars are correlation and lines are twice standard deviation. in landing. From July 23 to August 27, the tem- perature remained above 25"C all night and An. si- Seasonal variation in the mean nighttime tem- nensis continued landing all night. In the last part perature was related to the total number of An. si- of the season (August 27-September l0), temper- nensis capttred per night in landing collections dur- ature descended below 25'C (although above 20"C) ing 1997. Mean nightly temperatureson the night late at night and the landing rate was higher in the of, I wk before, and 2 wk before a landing collec- early part ofthe evening, In contrast to An. sinensis, tion were significantly related to the number of landing collections of Ae. vexans were greatest at landing mosquitoes(Fig. 6). the same time of night during the entire season, Mean nightly wind speedwas not cross-correlat- peaking between 2OO0 and 2300 h (Fig. 5). ed to landing or light trap collections of female An.

15MAY . 18JUN 28JUL - I8 AUG 35 30 l! 25 20 zF q) l5 ql l0 5 0 xxxxxx b65i

24 JUN - 23JUL 27 AUC - IOSEP Q 35 q1 30 2rs F 220 |r: u15 *r l0 5 0 xxx- €odsNs ts5&VX--dddoE :-ddoo HOUR HOUR

Fig. 5. Seasonal diel distribution of Aedes vexans in landing collections during 1997, Taesong'dong. JuNs 2000 Moseurrops ANDMALARTA nq rne DMZ, Konen ro7

250 t.2

I 2ffi A F tt +a 0.8 U) ,l , I 9 rso t l,I 0.6 (a) ItI z gloo A It 0.4 Eso ra I It I 0.2 It

l5- 28- 24- 9- l8- 3- May- May- Jun- Jun- Jul- Jul- Aug- Aug- Sep- 9797n97979797 97 97

+BITING - {- PHASE Fig.7. Moon phase (expressed as proportion of full disk) compared to landing collections of Anopheles sinensis at Taesong'dong, May l5-September 10, 1997. Note that no sampling took place on July 9.

sinensis through 1997. Any further analysis of the The numbers of mosquitoes in light traps during influence of wind on landing in 1997 was unlikely 1997 were compared to landing collections (for pair to produce significant results, because replication of collectors) at Taesong'dong in several ways: ex- occurred over a long period with seasonal effects. amination of relative ranking of species collected, Data from 1996 were collected during a single 2- percentage of each species compared to the total, wk interval so that replication was presumably free and number of females of each species (Table 5). of seasonal variation. For this analysis, we used all Ranking of the 3 most abundant species was similar locations in a single analysis for a total of 19 col- for light trap and landing collections. Absolute lection nights during 1996. The linear regression of numbers of An. sinensis in the Taesong'dong light wind in kilometers per hour (independent variable) trap (1,284) and landing collections (1,164) were on number of landing An. sinensis for each hour of also similar. Regression of the log of the number the night (dependent variable) was weak but sig- of An. sinensis in landing collections at Tae- nificant (y : -0.82(x) + 21.43, 12 -- O.M3, P : song'dong (dependent variable) and the log of the O.Ol77, df : 1,129). Dividing the night into statis- number in the light trap at Taesong'dong (indepen- tically grouped intervals (based on abundance of dent variable) did not result in a significant relation mosquitoes) and performing linear regression of (l:0.051, F:0.75, df : r,r4, P:0.400). wind speed on landing showed an interesting trend. However, regression between the log of landing Regtession was not significant during the period collections and the log of the mean of all 5 light -- - from l8OO to 2200 h (y : 0.0088(r) + 7.O2, f traps was significant 0 : l.l4(x) O.297, 12 : O.OOOO3,P : 0.9683, df : 1,53). Only a weak 0.386, F : lO.O5,df : 1,16, P : O.OO59;Fig. 8). indication of a relationship was found between The ratio of the log of light trap to log of landing wind and landing in the middle of the night from collections (dependent variable) was not constant. : -O.97(x) : 2300 to Ol00 h 0 + 26.91, 12 This proportion decreased significantly 0/ : 0.0995, P : 0.0738, df : l,3l). However, the re- -O.72(x) + 1.065, 12 : O.4O7, F : 10.98, df : gression was stronger during the early morning 1,16, P : 0.00144; Fig. 8) as the number of mos- hours of 0200-{400 h (y : -2.93(x) + 49.75, ,2 quitoes in light trap and landing collections (inde- : 0.2535, P : 0.0028, df : l,3l). pendent variable, expressed as the mean of the logs Hourly landing collections of An- sinensis in of light trap and landing collections) increased. The 1997 were negatively correlated to the phase of the relationship was not significant (l : 0.010, F : moon present during the hour of collection. Con- 0.16, df : 1,16, P : 0.695) when the log of the trolling for effects of wind (zero order partial cor- mean of all light traps was used as a measure of relation : -0.1133, df : 2O2, P : 0.107) and tem- mosquito density. Other differences were found be- perature (zero order partial correlation : 0.1 16l, df tween light trap and landing collections. Aedes vex- : 2O2, P : 0.001), the correlation coefficient be- ans and Cx. tritaeniorhynchus were more abundant tween phase of the moon (or absence if it had not in light traps than in landing collections. In con- yet risen or if it had already set) and hourly landing trast, An. sinensis (by percentage of collection), Ae. collections was -O.2245 (df : 20O, P : 0.001). koreicus, and Ae. albopictus were more abundant This statistical result supported the apparent nega- in landing collections than in light traps. tive correlation between moon phase and total Establishing statistically significant thresholds nightly landing collections of An. sinensis (Fig. 7). was possible for light trap collections of An. sinen- 108 Jor,nNnLor rnp AurnrcAN Moseuno CoNrnol AssocrATroN VoL. 16,No.2

Table 5. Comparison of landing collections and carbon-dioxide-baited light trap collections during May 15- September lO, 1997. Landing collections were at Taesong'dong; light traps were at Taesong'dong, Texas Range, Kansas Range, New Mexico Range, and Oklahoma Range, Paju County. Only those species ranked among the l0 most common by I of the collection methods are included.'

Landing collection Taesong'dong trap All light traps

Species Rank Number Vo Rank Number Rank Number Anopheles sinensis I 1,t64 s3.0 z 1,284 6.8 3 3,826 5.5 Aedes vexans 2 527 24.O I 15,894 83.6 I 56,150 81.4 Culex bitaeniorhynchus 5 150 6.8 J 806 4) 5 1,391 2.O An. lesteri 4 105 4.8 9 26 0.1 11 7l 0.1 Cx. pipiens J 70 t-a 5 154 0.8 4 r,599 2.3 Ae. koreicus 6 66 3.0 l3 z <0.1 t4 ll

I Species not among the 10 most common by any of the collecting techniques (positive collection methods indicated in puentheses: L, lmding collection; T, Taesong'dong trap; A, all light traps): Ae- alboscutellatus (L, A), Ae. nipponicus (L, A), Mansonia unifumis (L, X A), Ae. bekkui (L), An. sineroide.r Yamada (I A), Cr. mimeticus (T, A), Tripteroides bambusa bambusa (Yamada) (A), Ae. chemulpoensis Ymada (A), Cx. jacksoni Edwards (A), Ae. flavopictus fiavopictus Yamada (A), Ae. Iineatopennis (Ludlow) (A). 'NC- not collected.

sis based on landing collections at Taesong'dong in 1997. The most accurate threshold was based on the mean catch for all 5 light traps compared to a landing collection considered to be the minimum 1 significant potential biting rate. Therefore, the fF) threshold of landing rate was either >12 An. sinen- z z.) aa per (i.e., t tl sds night above significant landing rate z chosen based on an average of I potential bite per ,r collector each 2 h) or <12 An. sinensis per night J v1 (i.e., below significant landing rate). Contingency o u.) a tables constructed with light trap thresholds ranging J from 10 to 40 female An. sinensis per night in in- 0 tervals of 5 were all significant at P = 0.05 (n : I 1.5 2 2.5 17). The greatest accuracy (i.e., percentage oftimes LOG (MEAN TRAPS) that the light trap threshold corresponded to the landing threshold) of 88.2Vo was achieved at light trap thresholds of 10, 15, or 2O An. sinensis per t.) night per trap (Fig. 9). As expected, the highest (, sensitivity (lOOVo) was observed at the lowest I threshold of lO An. sinensis per night and the high- dz 0.5 est specificity (lOOVo) at the highest thresholds of 20 or more An. sinensis per night. Using only the 4rLl 0 )z Taesong'dong light trap, maximum accuracy of -0.5 -< 80.07o was achieved at a threshold of 3O An. sinen- '^J -1 ri.r per night in the trap with a sensitivity of 66.7Vo IOOVo (P = 0.098, n : l5). J -1.) and specificity of The number of anopheline larvae captured by 4 2 2.5 0.5 I 1.5 people during 3O min of collection at Warrior Base LOG (DENSITY) was related to the number of An. sinensis captured in landing collections at Taesong'dong on the pre- Fig. 8. Comparison of the logs of nightly mean of vious night (Fig. l0). Regression of the log of the collections of Anopheles sinensis in 5 carbon-dioxide- number of larvae (independent variable) and the log baited light traps and landing collections at Taesong'dong (de- with regression line indicated (top graph), and relationship of the number of adults in landing collections : between ratio of the 2 kinds of collections to combined pendent variable) was significant 0 O.796(x) + density of trap and landing collections with regression line O.7O9,f : O.465,F : 13.(X6, df : I,15, n: 17, indicated (bottom graph), May l5-September lO, 1997. P : 0.00256). Cross-correlation showed a signifi- Juvr 2000 Mosqunors am Malanra tN rnr DMZ, Konra l09

100 90 --5-'* F 80 -\\ z +.SENSITIVITY F.l \ O 70 . {. SPECIFICITY t !_o 60 \ .+ACCURACY 50 \ I 40 l0 t5 20 25 30 35 40 LIGHT TRAPTHRESHOLD

Fig. 9. Accuracy, sensitivity, and specificity of carbon-dioxide-baited light trap catches (mean per night for 5 traps) for prediction of whether or not landing collections at Taesong'dong exceeded 72 Anopheles sinensis per night. Light trap collections expressed as thresholds from 10 to 40 in intervals of 5 female An. sinensis mosquitoes. Data from 17 nights during weekly collections from May 15 to September lO, 199'1, paju County.

cant relationship between the number of landing ROK during l99l-92, 1993-94, and 1995-96 re- mosquitoes and the number of larvae collected on spectively (Kim et al. 1995,1997,1999). the next morning and also 7 days later (Fig. ll). The location of a collection influenced the total number of An. sinensis landing on humans, varying '12 from (for DISCUSSION a mean of females per night 2 collec- tors) at Taesong'dong to 376 at East Bonifas. This Anopheles sinensis was the mosquito most often variation might be explained in part by larval abun- collected in landing collections at 5 different col- dance of the species near the collection sites, be- lection sites during 2 wk in 1996 and throughout cause An. sinensis apparently does not very far the season in 1997. In addition to being a vector of from larval sites when a source of blood meals is P. vivax (Ree et al. 1967) artd Brugia malayi (Ree nearby (Strickman et al. 1999). In addition, partic- l99O), An. sinensis is a very abundant mosquito ular aspects of each collection site could have in- throughout the ROK. This species accounted for fluenced the number of An. sinensls landing. At SlVo of mosquitoes in landing collections in north- Tongil'chon, nearby cattle may have attracted mos- western ROK during July and August (Shim et al. quitoes away from human collectors, because An. 1997), 58Eo of mosquitoes in light traps in 18 cities sinensis is zoophagic (Paik et al. 1988). Although during 5 years in southwestern Korea (Lee and Ree no significant concentrations of large animals were 1991), and 37, 43, and 25Vo of mosquitoes in light present at Taesong'dong, human residents of the traps at f 3 U.S. military installations throughout the village may have attracted mosquitoes away from

t20 250 100 200 rrl 80 150 60 z 100 F J 40 20 50 0 0 15- 29- t2- 25- 10- 24- 7- 19- 4- May May Jun Jun Jul Jul Aug Aug Sep ILARVAE +BITING Fig. 10. Number of larvae of Anophelessinensis captured by 4 collectors during 30 min per week at fields near Warrior Base comparedto number of mosquitoescaptured in landing collections thJprevious nigtt ut Thesong'dong, 1997. 110 JouRNnl op rnr AvpnlcAN Moseurro CoNrnol AssocrerroN VoL. 16, No.2

F 0.8 0.6 Z,s 0.4 YZ 0.2 <=F- lr_ -0.2 r r"l ?;;f: 01234567 -0.4 -0.6 (.) -0.8

LAG OF LARVAL COLLECTION Fig. 11. Cross-correlation between number of Anopheles sinensis larvae captured by 4 collectors during 30 min per week (lag) and number of mosquitoes captured in landing collections at Taesong'dong on previous night (May 15- September lO, 1997). Bars are correlation and lines are twice standard deviation. Landing collection for July 9-lO (which was missing because of military alert) was set at the average of number of mosquitoes collected on the previous and following weeks.

collectors. The relatively low landing rate at Ob- tions. A greater diversity of mosquitoes was col- servation Point Oullette may indicate that females lected in larger numbers in 1997 than in 1996. Sev- of An. sinensis were reluctant to fly to a higher en species in 1997 each accounted for >Z.OVo of elevation to seek hosts. The greater number of mos- the collections (An. sinensis, Ae. vexans, Cx. bitae- quitoes collected at East Bonifas compared to West niorhynchus, An. lesteri, Cx. pipiens, Ae. koreicus, Bonifas could have been associated with the topog- and Ae. albopictus). Seventeen other species were raphy of these 2 nearby sites. Hills on either side collected in 1997, for a total of 24 species that of East Bonifas would have tended to concentrate came to bite humans at a single location in Tae- mosquitoes flying from rice fields. song'dong. Other anophelines landing on humans were much Anopheles sinensis arlrdAe. vexans were present less numerous than An. sinensis. Anopheles lesteri during the entire season. Their numbers were very was the next most abundant Anopheles, accounting low until late June, when rice was well established for only 1.5-5.OVoof mosquitoes (1.6-6.0 females (approximately 33 cm tall) and the average night- per 2 collectors per night) at the 5 locations in 1996 time temperature exceeded 22"C. Both species and only 4.8Vo of the mosquitoes landing during reached their greatest numbers in August, appar- 1997 at Taesong'dong. The vector status of An. /e,r- ently having increased their populations through the teri in Korea is uncertain. This species was lst de- season. Such a steady increase in the populations scribed from the Philippines (Baisas and Hu 1936), was a possibility because rice fields in this area although the distribution of the species as originally retained standing water throughout the growing described extended throughout temperate and trop- season almost until the time of harvest. Because Ae. ical eastern Asia. Since the original description, An. vexans deposits its eggs on moist soil likely to paraliae Sandosham has been raised to a separate flood, it tends to occur in distinct broods caused by species from An. lesteri in southeastern Asia (Har- simultaneous hatching of eggs over a large area. rison et al. 1991). Similarly, An. anthropophagus The number of landing An. sinensis also varied dur- Xu and Feng has been described as a separate spe- ing the season, but in a less regular pattern. Tem- cies in China (Xu and Feng 1975, Ma l98l). No perature during 2 wk before the landing collection information has been published on the actual tax- accounted for more than 5OVoof variation in abun- onomic relationship of Korean An. lesteri and Chi- dance. Possibly, higher temperatures supported nese An. anthropophagzs, although they might be faster larval development resulting in production of expected to be related or identical. A close rela- more adult mosquitoes after 1 or 2 wk. tionship between the 2 species would be significant The seasonal pattern of activity of An. sinensis because An. anthropophagus is the major vector of observed in our study corresponded to previous P. vivax in China (Chi'i et al. 1962). The difficulty studies. New Jersey light traps operated for 6 years and uncertainty of distinguishing adults of An. les- in Paju County collected the greatest number of An. teri from An. sinensis (K. W. Lee 1998) further sinensis in July during 4 years and in August during complicates the situation. We collected An. yatsu- 2 years, with no or very few mosquitoes collected shiroensis (a suspected malaria vector, Paik et al. in May (Kim et al. 1995, 199'7,1999). Black-light 1988) and An. sineroides in very low numbers. traps collected the greatest number of An. sinensis In 1996, only 3 species (An. sinensis, Ae. vexans, in July at 3 of 4 sites in the northwestern part of and Cx. pipiens) were common in landing collec- the ROK, including Paju Counry (Shim et al. 1997). Juxr 2000 Moseurrops eNo Mar-anra rN rur DMZ, Konre ll1

This seasonal pattern corresponds to the incidence decreasing from a positive to a negative proportron of malaria cases, which peaks in August (Yim et as the mosquito population increased (i.e., landing al. 1996, Feighner et al. 1998, Lee et al. 1998). collections were more efficient than light traps at During the season of its peak abundance, An. si- high mosquito densities). The seasonal change in nensis bit most frequently between 0200 and 0500 ratio may have resulted from changes in the pop- h, although departures from this average pattem oc- ulation age structure of the vector; however, we did curred on some nights at some locations. Shim et not measure gonotrophic age in order to test this al. (1997) also observed highest landing rates in possibility. Unfortunately, an estimate of population Paju County late at night, between 010O and (X00 from light trap data alone was not sufficient to h during July and August 1995. Early and late in make an accurate prediction of the ratio of light trap the season, the times of peak landing shifted to an to landing collections. Therefore, using our data, it earlier hour, apparently corresponding to times of would only be possible to make a general estimate night when temperatures were >23"C. Late night of landing rate from light trap data. Another study landing and seasonal shifts in diel activity by An. failed to find a useful index of landing based on sinensis were in marked contrast to Ae. vexans, unbaited light traps for a malaria vector in India, which bit in greatest numbers between 20O0 and An. fluviatilis James (Gunasekaran et al. 1994). In 2300 h throughout the season. Unlike An. dirus contrast, Lines et al. (1991) showed that they could Peyton and Harrison (Colless 1956, Rosenberg and achieve a constant ratio of about 1.5 between a light Maheswary 1982) and An. farauti Laveran (Charl- trap (placed adjacent to humans sleeping under wood et al. 1986), landing by An. sinensls was neg- mosquito nets) and landing collections of An. gam- atively correlated to the apparent size of the moon biae Glles ar.d An. funestus Giles in Africa. during the hour of collection. A less direct approach comparing landing and Mean wind speed during an entire night was not carbon-dioxide-baited light trap collections provid- strongly correlated with the number of An. sinensis ed more promising results in our study. A single captured in landing collections. Closer examination threshold number of An. sinensis in the light traps of the data showed that wind had a great influence accurately predicted whether landing rates at Tae- (accounting for 25Vo of variation) only during the song'dong exceeded a minimum value. Using the late-night peak in landing (0200-{400 h). This may average from all light traps, 15 or more An. sinensis be an indication that mosquitoes landing late at per trap night indicated with 9l%o sensitivity, 837o night traveled a greater distance to find a host, and specificity, and 887o accuracy that more than 12 An- therefore were influenced more by wind before sinensis would bite 2 collectors. A single light trap, reaching the host. although located near the landing collections, was Landing collections of Anopheles are presumably much less predictive. These results show that a light the most accurate way of evaluating the biting rate. trap augmented with carbon dioxide can be used as Although landing collections are practical in the a reasonably accurate tool for determining a treat- sense that they require a minimum amount of ment threshold based on number of landing An. si- equipment, the technique has numerous disadvan- nensis. The results also highlight the importance of tages. Landing collections are tedious and uncom- using replicate traps. fortable, pose a small disease risk to the collectors Despite the inherent inaccuracies of our method (who can take chemoprophylaxis), and include in- for sampling, larval collections were correlated herent biases from collectors' individual attractive- closely to landing collections. Considering that lar- ness to host-seeking mosquitoes. From an opera- val sampling provides immediate results and that it tional standpoint, performing all-night landing can be carried out during daylight hours, applica- collections at all sites where soldiers are scheduled tion of more accurate sampling methods (Ree 1982) to train or deploy usually is not possible. For these might be worthwhile for operational purposes. The reasons, we defined the relationship between light seasonal distribution of larvae at Warrior Base was trap and landing collections of An. sinensis. similar to that observed previously near Seoul (Ree On a seasonal basis the light trap catches and et al. 1981, 1982) and in southwestern ROK (D.- landing collections showed that the same 2 species, K. Lee 1998). In those studies, larvae lst increased Ae. vexans and An. sinensis, were the most abun- in numbers during July and then decreased mark- dant. Perhaps more significantly, the total number edly in late September. These studies also docu- of An. sinensls captured in a nearby light trap was mented some sharp fluctuations in number of larvae close to the total number in landing collections in during the course of the season. 1997. Comparison of weekly landing collections to Probably the most practical result from this study carbon-dioxide-baited light traps did not produce a was establishment of a threshold for light trap col- simple relationship. A significant linear relationship lections of An. sinensis based on landing collec- was found between the log of the mean of 5 light tions. Using this threshold, it would be possible to traps to the log of the landing collection, but this decide when and where to concentrate vector con- relationship accounted for only about 397o of the trol efforts based on an implied landing rate thresh- observed variation. What is more, the ratio of light old. The relationship of landing rates to wind, moon trap to landing collections varied systematically, phase, and temperature could also be useful for pre- t l12 Jouru,rer oF TrrE AMERTCIN Mosqurro Coxrnol AssocrarroN VoL. 16, No. 2 dicting likely landing rate when trapping data are finally, very little information exists on larval hab- not available. itats other than rice fields, particularly early in the Close examination of temperature in Korea could season before planting. Although the current ma- have value in predicting landing populations up to laria epidemic in Korea is an unfortunate event, it 2 wk later, if flnding or estimating an initial landing may stimulate research on the vectors that will en- rate was possible. Temperature might be especially able public health authorities to respond more de- useful for determining the lst seasonal appearance cisively. The malaria situation in Korea could also of large numbers of landing An. sinensis. Using the warrant action from an American perspective, con- mathematical relationship suggested by our data, an sidering that vivax malaria was formerly an over- average nighttime temperature over 20"C corre- whelming problem in the United States (Anony- sponds to a landing rate of 36 mosquitoes per night mous 1920, Faust 1949) and that it has been locally 2 wk later. Larval counts of An. sinensis might pro- transmitted in the USA in recent years (Zucker vide another measure of probable landing rates, al- 1996). American soldiers returning from Korea though important questions remain about the best with active infections (Guzenhauser et al. 1997) method for sampling. could become the source for introduction of P. vi- The time of night of landing is sometimes por- v4.r parasites that are preadapted to temperate con- trayed as a constant feature of a species, but the ditions. data from this study clearly show that the pattern for An. sinensis in Korea can vary from place to ACKNOWLEDGMENTS place and during a season. This variation compli- cates the optimum time for application of insecti- We would like to thank Matthew Koh, Charles cidal fogs, assuming that the times of greatest land- Fields, and John Heitz, who spared no personal ef- ing activity correspond to the times of greatest fort in assuring that these studies were completed; potential exposure to aerial toxicants. Analysis of the numerous American and Korean soldiers who our data indicates that the maximum number of performed landing collections; Dean Giullitto, mosquitoes would be exposed late at night unless James Laufenburg, and Chun-Sep Roh for admin- temperatures descend below 23'C. The effect of istrative support; and Jae-Chul Shim and Han-Il fogging might also be improved by avoiding times Ree for their excellent advice. when the moon is in a large phase. Study of diel periodicity throughout the season at several sites REFERENCES CITED would probably provide adequate data to establish Anonymous. 192O. Malaria mosquito survey: malaria a useful model to maximize the effectiveness of mosquito control. ln:. Report of the College of Agricul- insecticidal fogging. ture and the Agricultural Experiment Station of the Vector control could be a particularly practical University of California, July I, 1919, to June 30, I92O component of attempts to eliminate vivax malaria Berkeley, CA: University of California Press.p 60-61. from the Korean peninsula, because vector activity Baisas FE, Hu SMK. 1936. Anopheles hyrcanus var. si- is limited to a short season. Although the bionomic nensis of the Philippines and certain parts of China, with some comments on Anopheles hyrcanus nigerri- information from this and previous studies is ade- mus of the Philippines. Mon Bull Bur Health Philipp quate pest for rational design of management Manila 16:205-242. plans, a number of questions should be answered Brunetti R. Fritz RE Hollister AC Jr. 1954. An outbreak in order to improve vector control. First, the sys- of malaria in California, 1952-1953. Am J Trop Med tematics of An. sinensis and the related members of Hyg 3:779-788. the Hyrcanus Group are uncertain. Clarifying the Chai I-H, Lim G-I, Yoon S-N, Oh W-I, Kim S-J, Chai J- taxonomic status of An. sinensis. An. lesteri. and Y. 1994.Occurrence of tertian malaria in a male patient An. yatsushiroensis in Korea would make compar- who has never been abroad. Korean J Parasitol 32: isons with these species in other regions much 195-200. Charlwood JD, Paru R, Dagoro H, Lagog M. 1986. Influ- clearer. Second, the flight range of An. sinensis is ence of moonlight and gonotrophic age on biting activ- virtually unknown except for a single study show- ity of Anophelesfarauti (Diptera: Culicidae) from Pa- ing indirect evidence that most individuals do not pua New Guinea.J Med Entomol23:132-135. fly as far as 1 km (Strickman et al. 1999). Better Chi'i H, Chou T-C, Ch'en T-H, Hsueh A-T. 1962. 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