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Brief Communication

Population Dynamics of Five Anopheles Species of the Hyrcanus Group in Northern Gyeonggi-do, Korea

Kyoung Yong Jeong1,2, Sunjin Un1, Jongweon Lee1, In-Yong Lee1, Tai-Soon Yong1, Han-Il Ree1
The Korean Journal of Parasitology 2010;48(4):351-353.
Published online: December 16, 2010

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Corresponding author (para@yuhs.ac)
• Received: June 9, 2010   • Revised: August 19, 2010   • Accepted: August 28, 2010

© 2010, Korean Society for Parasitology

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  • To investigate the population densities of potential malaria vectors, Anopheles species were collected by light traps in malaria endemic areas, Paju and Gimpo, Gyeonggi-do of Korea. Five Anopheles Hyrcanus sibling species (An. sinensis, An. pullus, An. lesteri, An. kleini, and An. belenrae) were identified by PCR. The predominant species, An. pullus was collected during the late spring and mid-summer, while higher population consists of An. sinensis were collected from late summer to early autumn. These 2 species accounted for 92.1% of all Anopheles mosquitoes collected, while the other 3 species accounted for 7.9%. Taking into account of these population densities, late seasonal prevalence, and long-term incubation period (9-13 months) of the Korean Plasmodium vivax strain, An. sinensis s.s is thought to play an important role in the transmission of vivax malaria in the study areas.
  • Key words: Anopheles sinensis, Anopheles pullus, Anopheles lesteri, Anopheles kleini, Anopheles belenrae, Plasmodium vivax, malaria, vector, population dynamics
Malaria re-emerged in the Republic of Korea in 1993, despite being declared malaria free in 1979. Over 1,000 cases of vivax malaria are diagnosed annually, with a peak number of cases (4,142) reported in 2000 [1]. Most of the patients reported are from northern Gyeonggi-do (Province) and the north-west Kangwon-do, near the 4 km wide demilitarized zone (DMZ) separating South and North Korea [2].
Eight species of Anopheles mosquitoes have been described in Korea; Anopheles sinensis sensu stricto (s.s.) Wiedemann, An. pullus Yamada (= An. yatsushiroensis), An. lesteri Baisas & Hu (= An. anthropophagus), An. sineroides Yamada, An. kleini Rueda, An. belenrae Rueda, An. lindesayi japonicus Yamada, and An. koreicus Yamada & Watanabe [3,4]. All of these species, with the exceptions of An. lindesayi japonicus and An. koreicus, belong to the Hyrcanus group. The 5 sibling species (An. sinensis, An. pullus, An. lesteri, An. kleini, and An. belenrae) are impossible to distinguish by morphological identification, and therefore identification by PCR was developed to differentiate these species [5-7].
There is still some debate regarding the primary vector species for malaria in Korea. An. sinensis used to be considered the most important vivax malaria vector in Korea, but recently, An. pullus and An. kleini have been proposed to play important roles in malaria transmission. Lee et al. [1] suggested that An. kleini, An. pullus, and An. sinensis are vectors of malaria in Korea based on the finding that higher proportions of An. kleini and An. pullus were captured using Mosquito Magnet traps near the base camps of United States forces in Korea, and on detection rates of circumsporozoite protein by ELISA [1]. Joshi et al. [8] suggested that An. lesteri is a highly competent vector based on its ability to develop oocysts in the midgut and sporozoites in salivary glands of experimentally infected mosquitoes with a Korean isolate of Plasmodium vivax [8]. In this study, we have investigated the population dynamics of members of the Anopheles Hyrcanus group collected by light traps at cow sheds in Paju (City) and Gimpo (City) in 2005.
Mosquitoes were collected on 5 occasions in Paju (latitude 37°48', longitude 126°42') (Jun 2, Jun 6, Jul 5, Jul 26, and Aug 17, 2005) and twice in Gimpo (latitude 37°43', longitude 126°39') (Jun 22 and Sep 21, 2005). Both locations are close to the DMZ, a malaria high-risk area. Light traps were set up at cowsheds and operated throughout the night from 18:00 to 06:00 the following morning. Female mosquitoes were identified using morphological taxonomic keys and descriptions [9-11].
Dry female mosquitoes of the Hyrcanus group were preserved in 75% ethanol for DNA extraction. Genomic DNA from individual mosquitoes was isolated with GeneAll Exgene™ Tissue SV kit (GeneAll, Seoul, Korea). PCR analysis was performed as described by Li et al. [7]. The amplified DNA fragments were separated on 2% agarose gels, and species were identified by size estimation of PCR products with a size marker (øX174/Hae III digest, TaKaRa, Shiga, Japan).
Among the total 1,115 female Hyrcanus group mosquitoes identified by PCR, An. pullus was the most commonly collected species (52.4%), followed by An. sinensis (39.7%), An. lesteri (3.5%), An. belenrae (2.3%), and An. kleini (2.1%). A total of 22 mosquitoes that produced multiple bands were not included. An. pullus was most frequently collected at Paju during June (79.0%) and July (66.7%), whereas An. sinensis was most frequently collected during August and September, accounting for 57.2% and 79.0% of the total collected at Paju and Gimpo, respectively. The other 3 species, An. lesteri, An. belenrae, and An. kleini made up less than 10% of the total mosquitoes collected during any collection period (Table 1).
In summary, An. sinensis populations increased through the summer until early September, whereas An. pullus numbers were highest in late May-June and decreased sharply in August. An. lesteri, An. belenrae, and An. kleini maintained low numbers throughout the season, without having any particular period of prevalence (Fig. 1).
Primary malaria vector species are determined by relative population densities, human feeding habits, susceptibility to malaria parasites, longevity, and other factors. The fact that relative high densities of An. sinensis s.s. or An. pullus were present and both are susceptible to malaria infection and sporozoite development to the salivary glands implicate these 2 species as primary malaria vectors in the study area. Joshi et al. [8] carried out an experimental infection study and reported that vivax malaria sporozoites were not detected in An. pullus, but found in 11% and 64% of An. sinensis and An. lesteri, respectively [8]. Tiburskaja and Vrublevskaja (1977) experimentally infected 77 humans with the North Korean strain of P. vivax through bites of the infected mosquitoes, and resulted that 24.7% of them became ill after a short incubation period (14-22 days) and 75.3% after a long incubation period (1.3% after 1 month, 14.3% after 8 months, 18.2% after 9 months, 18.2% after 10 months, 16.9% after 11 months, 3.9% after 12 months, and 2.6% after 13 months) [12]. Though it is extremely difficult to study the correlation between seasonal occurrences of human cases and vector mosquitoes, most malaria cases of June-August would be infected in the previous year by An. sinensis s.s. rather than An. pullus. The population densities of An. lesteri, An. belenrae, and An. kleini were too low for these species to be considered important vectors in the study areas, accounting only for 3.5%, 2.3%, and 2.1% of the total mosquitoes examined. Lee et al. [1] studied population densities of the Hyrcanus group using methods similar to ours, and reported that An. sinensis s.s. was dominant both in Paju and Gimpo areas, but that An. kleini also occurred with considerably high density, making up 40% of totals at Paju and 14.2% at Gimpo [1]. Our studies, in contrast, identified this species in only 1.3% of totals at Paju and 5.5% at Gimpo. Rueda et al. [13] also carried out similar studies with larvae in Munsan and reported that An. kleini was most abundant in early summer (May to July), whereas An. sinensis was the most frequently collected species in August, September, and October, and An. pullus peaked in May [13], which is a similar result with ours, except for the population density of An. kleini. More comprehensive and detailed geographic studies throughout the Korean Peninsula are required to better understand the dynamics of malaria transmission.
This study was supported by a research grant from Health and Medical Technology R&D Program (A030075), Ministry of Health and Welfare, Korea.
  • 1. Lee WJ, Klein TA, Kim HC, Choi YM, Yoon SH, Chang KS, Chong ST, Lee IY, Jones JW, Jacobs JS, Sattabongkot J, Park JS. 2007. Anopheles kleini, Anopheles pullus, and Anopheles sinensis: potential vectors of Plasmodium vivax in the Republic of Korea. J Med Entomol 2007;44:1086-1090.
  • 2. Ree HI. Unstable vivax malaria in Korea. Korean J Parasitol 2000;38:119-138.
  • 3. Ree HI. Studies on Anopheles sinensis, the vector species of vivax malaria in Korea. Korean J Parasitol 2005;43:75-92.
  • 4. Rueda LM. Two new species of Anopheles (Anopheles) Hyrcanus group (Diptera: Culicidae) from the Republic of South Korea. Zootaxa 2005;941:1-26.
  • 5. Wilkerson RC, Parsons TJ, Albright TA, Klein TA, Braun MJ. Random amplified polymorphic DNA (RAPD) makers readily distinguish cryptic mosquito species (Diptera: Culicidae: Anopheles). Insect Mol Biol 1993;1:205-211.
  • 6. Ree HI, Yong TS, Hwang UW. Identification of four species of the Anopheles Hyrcanus complex (Diptera: Culicidae) found in Korea using species-specific primers for polymerase chain reaction assay. Med Entomol Zool 2005;56:201-205.
  • 7. Li C, Lee JS, Gorebner JL, Kim HC, Klein TA, O'Guinn ML, Wilkerson RC. A newly recognized species in the Anopheles Hyrcanus group and molecular identification of related species from the Republic of Korea (Diptera: Culicidae). Zootaxa 2005;939:1-8.
  • 8. Joshi D, Choochote W, Park MH, Kim JY, Kim TS, Suwonkerd W, Min GS. The susceptibility of Anopheles lesteri to infection with Korean strain of Plasmodium vivax. Malar J 2009;8:42.
  • 9. Tanaka K, Mizusawa K, Saugad ES. A revision of the adult and larval mosquitoes of Japan (including the Ryukyu Archipelago and the Ogawawara Islands) and Korea (Diptera: Culicidae). 1979, 16:Contributions of the Am Entomol Inst; pp ii-vii. pp 1-987.
  • 10. Lee KW. A revision of the illustrated taxanomic keys to genera and species of female mosquitoes of Korea. 1998, Department of the Army, 5th Med. Detach., 168th Med. Battalion, 18th Med. Comn.
  • 11. Ree HI. Taxonomic review and revised keys of the Korean mosquitoes (Diptera: Culicidae). Korean J Entomol 2003;33:39-52.
  • 12. Tiburskaja NA, Vrublevskaja OS. The course of infection caused by the North Korean strain of Plasmodium vivax. WHO MAL 1977;895:1-19.
  • 13. Rueda LM, Brown TL, Kim HC, Chong ST, Klein TA, Foley DH, Anyamba A, Smith M, Pak EP, Wilkerson RC. Species composition, larval habitats, seasonal occurrence and distribution of potential malaria vectors and associated species of Anopheles (Diptera: Culicidae) from the Republic of Korea. Malar J 2010;9:55.
Fig. 1
Population trends of Anopheles mosquitoes collected by light trap from Paju (A) and Gimpo (B), Korea.
kjp-48-351-g001.jpg
Table 1.
The number of female Anopheles mosquitoes captured by light trap in 2005
Table 1.
Site Date sinensis pullus lesteri belenrae kleini Total
Paju June 28 (15.4) 144 (79.1) 4 (2.2) 6 (3.3) 0 (0.0) 182
July 94 (26.3) 238 (66.7) 3 (0.8) 13 (3.6) 9 (2.5) 357
August 215 (57.2) 138 (36.7) 14 (3.7) 6 (1.6) 3 (0.8) 376
Subtotal 337 (36.8) 520 (56.8) 21 (2.3) 25 (2.7) 12 (1.3) 915
Gimpo June 27 (27.0) 58 (58.0) 8 (8.0) 1 (1.0) 6 (6.0) 100
September 79 (79.0) 6 (6.0) 10 (10.0) 0 (0.0) 5 (5.0) 100
Subtotal 106 (53.0) 64 (32.0) 18 (9.0) 1 (0.5) 11 (5.5) 200
Total 443 (39.7) 584 (52.4) 39 (3.5) 26 (2.3) 23 (2.1) 1,115

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Population Dynamics of Five Anopheles Species of the Hyrcanus Group in Northern Gyeonggi-do, Korea
Korean J Parasitol. 2010;48(4):351-353.   Published online December 16, 2010
DOI: https://doi.org/10.3347/kjp.2010.48.4.351
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Population Dynamics of Five Anopheles Species of the Hyrcanus Group in Northern Gyeonggi-do, Korea
Korean J Parasitol. 2010;48(4):351-353.   Published online December 16, 2010
DOI: https://doi.org/10.3347/kjp.2010.48.4.351
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Population Dynamics of Five Anopheles Species of the Hyrcanus Group in Northern Gyeonggi-do, Korea
Image
Fig. 1 Population trends of Anopheles mosquitoes collected by light trap from Paju (A) and Gimpo (B), Korea.

Fig. 1

Population Dynamics of Five Anopheles Species of the Hyrcanus Group in Northern Gyeonggi-do, Korea
Site Date sinensis pullus lesteri belenrae kleini Total Paju June 28 (15.4) 144 (79.1) 4 (2.2) 6 (3.3) 0 (0.0) 182 July 94 (26.3) 238 (66.7) 3 (0.8) 13 (3.6) 9 (2.5) 357 August 215 (57.2) 138 (36.7) 14 (3.7) 6 (1.6) 3 (0.8) 376 Subtotal 337 (36.8) 520 (56.8) 21 (2.3) 25 (2.7) 12 (1.3) 915 Gimpo June 27 (27.0) 58 (58.0) 8 (8.0) 1 (1.0) 6 (6.0) 100 September 79 (79.0) 6 (6.0) 10 (10.0) 0 (0.0) 5 (5.0) 100 Subtotal 106 (53.0) 64 (32.0) 18 (9.0) 1 (0.5) 11 (5.5) 200 Total 443 (39.7) 584 (52.4) 39 (3.5) 26 (2.3) 23 (2.1) 1,115
Table 1. The number of female Anopheles mosquitoes captured by light trap in 2005

Table 1.

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