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Biosurveillance and morphological variations of larvae and pupae of common malaria vectors, Anopheles (Anopheles) Hyrcanus group species in the republic of Korea.

Malaria is a major health threat to military and civilian personnel as well as family members deployed or residing in the Republic of Korea (ROK). Members of the Anopheles (Anopheles) are placed in 3 groups, namely the Hyrcanus Group (An. belenrae Rueda, An. kleini Rueda, An. sinensis Wiedemann, An. pullus Yamada, An. lesteri Baisas and Hu, An. sineroides Yamada), the Barbirostris Group (An. koreicus Yamada and Watanabe), and the Lindesayi Group (An. lindesayi japonicus Yamada). (1-3) Anopheles kleini and An. lesteri are the primary vectors of Plasmodium vivax malaria near the demilitarized zone (DMZ), while An. sinensis is a very poor vector and the status of the remaining species is undetermined. (4,5) Laboratory studies have shown the potential for An. lesteri as an efficient vector (6,7) and is considered a primary vector (as An. anthropophagus Xu and Feng) in parts of China. (8) In the ROK, the populations of An. lesteri are very low, (9) except on the northwest coastal islands. (10) Females of An. belenrae and An. sineroides have been found positive for P. vivax by enzyme-linked immunosorbent assay and polymerase chain reaction (PCR). (9,11) Species in Barbirostris and Lindesayi Groups have not been implicated as malaria vectors in the ROK. (9)

Knowledge of the species composition of common Anopheles (Anopheles) in various habitats in different provinces is needed for defining malaria vector distributions, biosurveillance and vector control. Data are limited on the collections and habitats for the occurrence and relative abundance of indigenous Anopheles mosquitoes in the ROK.

With several human malaria cases reported annually from the ROK, (10,12,13) there is an urgent need to accurately identify the potential Anopheles mosquito vectors. Misidentifications of species often lead to poor vector surveillance, misunderstanding of the epidemiology of disease transmission, and the development and implementation of ineffective strategies for control measures. (1) Both morphological and molecular analyses are essential in the taxonomy and identifications of members of the Anopheles Hyrcanus Group species, particularly those where their geographic distribution and vector potential are better understood. During the mosquito surveillance, field identifications of live larvae and pupae may also be convenient and necessary, when possible.

Waxy body ornamentations have been previously reported on various insects, particularly scale insects, (14) aphids, (15) and heliconian caterpillar, (16) and they have been shown to be useful for initial identifications during field surveillance efforts. Morphological variations in the body ornamentations for different stages of development, eg, leg paddles observed in the sabethine mosquitoes, Sabethes cyaneus (Fabricius) (17) are important. Knowledge on mosquito body ornamentation is very limited, and little is known about the waxy body covering of larvae and pupae of Anopheles species or its importance in identifications.

Immature stages (both larvae and pupae) and adults of members of the An. (Ano) Hyrcanus Group in the ROK cannot be identified with certainty using morphological techniques. Although there are some slight differences in the branching patterns of the setae in the larval head (setae 3, 7, 9-C), thorax (14-M) and abdomen (5, 9-II; 4, 9-III; 4, 6-IV; 6-V), (3) they are still not very useful in performing accurate identifications of the species, thereby requiring the need for the PCR techniques. Furthermore, specimens must be mounted on glass slides for microscopic morphological examinations of the branching patterns of setae of the head and other body parts, requiring excessive manpower and delays in identification. Some waxy ornamentations or patterns on the dorsal parts of the larval bodies were observed during the conduct of extensive field collections and surveillance of Anopheles mosquitoes from various parts of the ROK.

The main objectives of our study were: (1) to conduct a comparative survey of mosquito larvae from selected habitats using standardized sampling methods to obtain pertinent data on the occurrence and relative abundance of indigenous Anopheles species, and (2) to identify the waxy body ornamentations or patterns of Anopheles (Anopheles) Hyrcanus Group larvae and pupae which may be useful for rapid field identifications during mosquito vector surveillance and control.

MATERIALS AND METHODS

Immature mosquito collections that included both anophelines and culicines were conducted from 3 provinces (Gyeonggi, Gyeongsangbuk, and Chungcheongbuk) of the ROK (Figure 1). Selected habitats were sampled including the following: rice paddies (uncultivated and cultivated), irrigation ditches (concrete and nonconcrete ditches), drainage ditches (concrete and nonconcrete ditches, culvert and dammed ditches), ponds (including pond reservoir), stream margins (including stream ponds, inlets, algal mats), and other habitats (including ground pools, ground depressions, flood pools, rock pools, uncultivated fields, artificial containers).

As part of the mosquito biosurveillance, data were collected monthly from May 2007 to October 2007 and were combined over the sampling periods for each of the selected habitats in 3 provinces (Gyeonggi, Gyeongsangbuk, and Chungcheongbuk). The relative abundance of each Anopheles species in each habitat was calculated as the percentage of the total number of larvae recovered either per month or over the entire 6-month period.

As part of the morphological study of waxy body ornamentations, Anopheles larvae were collected from 9 locations in Gyeongsangbuk Province, including Hayangeup, Gyeongsansi (Collection nos. KSK-509, 511, 513, 514, 520, 522, 523) and Cheongsong-eup, Jinbo-myeon (Collection nos. KSK-529, 533, 543, 545).

Depending on the habitats, larvae and pupae were collected using a standard larval dipper (350 ml, 13 cm diameter) or a white plastic larval tray (25 cm x 20 cm x 4 cm) (BioQuip, Rancho Dominguez, CA). Collected live larvae and pupae, with intact waxy ornamentations or body patterns were placed in plastic Whirl-Pak bags (118 ml, 8 cm x 18 cm) (BioQuip, Rancho Dominguez, CA) filled approximately 1/2 full with water from the collection site. The Whirl-Pak was tightly closed to retain air, placed in a cooler, and brought to the laboratory where selected specimens were photographed on the same day, and 3rd and 4th instar larvae then placed and directly preserved in 100% ethanol (EtOH) for molecular identification. The remaining larvae were individually link-reared to adult stage as morphological voucher specimens for this work. Emergent mosquito adults were pinned on paper points, each given a unique collection number, and identified using diagnostic morphological characters. For molecular species identifications, DNA was isolated from individual larval mosquitoes and adults (1 or 2 legs per adult) by extraction procedure and direct sequencing as described in Wilkerson et al. (12) Sequencing of An. sinensis, An. pullus, An. lesteri, An. belenrae, and An. kleini are those of Wilkerson et al (12) and Li et al (18) using the primers therein. GenBank accession numbers for the above species are in Wilkerson et al (12) and Li et al. (18) Voucher specimens and collection records were deposited in the US National Museum of Natural History, Smithsonian Institution, Suitland, Maryland.

RESULTS

Occurrence and Relative Abundance of Mosquito Larvae from Selected Habitats

A total of 4,576 specimens belonging to 6 species of An. (Ano) Hyrcanus Group species (An. belenrae, An. kleini, An. sinensis, An. pullus, An. lesteri, and An. sineroides) were collected monthly from May 2007 to October 2007 from 7 general habitats by standard larval sampling method. As shown in the Table, all 6 species were collected from irrigation ditches, while only 5 species were collected from rice paddies, ponds, swamps, and other habitats, and only 4 species were collected from drainage ditches, and stream margins. In the irrigation ditches, An. sinensis (71.82%) was the most abundant species, followed by An. kleini (12.84%) and An. sineroides (9.68%). Anopheles larval population increased from 19.92% in June to 24.50% in August. In the rice paddies, An. sinensis (82.09%) had the greatest relative abundance followed by An. pullus (10.38%) and An. kleini (5.04%). Larval population increased from 16.03% in May to 23.81% in June. Except for An. lesteri, all species were collected from the rice paddies. In the pond reservoir, An. sinensis (54.63%) was the dominant species, followed by An. kleini (22.82%) and An.sineroides (12.55%). Larval population increased from 15.75% in July to a peak of 24.28% in August. In the stream margins and swamps, respectively, An. sinensis (80.07%, 36.86%) ranked first in abundance followed by An. kleini (13.07%, 27.78%) and An. pullus (5.85%, 30.38%). Larval population increased from 23.04% and 12.08% in July to 26.37% and 29.31% in August. In the drainage ditches, An. sinensis (51.98%) was the dominant species, followed by An. pullus (20.63%) and An. kleini (9.33%). Larval population increased from 15.38% in June to a peak of 35.90% in August. In all sampled habitats, An. sinensis had the highest relative abundance in all habitats, and its larvae were found in all 7 habitats similar to An. kleini, An. pullus, and An. sineroides. Anopheles lesteri larvae were only collected from the irrigation ditches and swamps, while An. belenrae larvae were only found in rice paddies, irrigation ditches, and ponds. Rueda et al (2) reported the associations of An. (Ano) with other species of Aedes and Culex from different habitats in the ROK.

Morphological Descriptions of 5 Common Anopheles (Anopheles) Species, with Emphasis on Waxy Ornamentations or Body Patterns, Based on Korean Specimens

1. An. belenrae, Larva: Body coloration is usually green or light reddish brown. Thorax has dorsal parts almost covered with white waxy materials, primarily along the anterior and lateral edges. It usually has a slightly pointed waxy ornamentation extending up to the anterior tip of the dorsum of abdominal segment I (Figure 2; collection nos. KSK-545-1001L, KSK-545-1008L, KSK-545-1011L). Abdomen has 2 distinct white waxy ornamentations on the dorsal parts of segments III and V. Abdominal segment III has a dorsal part with white waxy ornamentations of various shapes, including barrel shape (Figure 2A), diamond shape (Figure 2B), and chalice-shape (Figure 2C). Abdominal segment V has a dorsal part with a white waxy ornamentation that is almost similar to that+A4271 Pupa: No live specimen was available to examine.

2. An. kleini, Larva: Body coloration is usually reddish brown to dark brown. Thorax has dorsal parts almost covered with white waxy materials, primarily along the anterior half and narrowly extending towards the anterior edge of abdominal segment I. The tip of this extension is usually blunt (Figure 3B, 3C) or rarely pointed (Figure 3A). Abdomen has one distinct white waxy ornamentation, barrel-shaped, on the dorsal part of segment III (Figure 3; collection nos. KSK-511-1004L, KSK-523-1004L, KSK-545-1005L), and nothing on abdominal segment V. Pupa: Abdominal segments III and IV have dorsal parts with white waxy ornamentations of various shapes, including Aladdin lamp shape (Figure 4A, collection no. KSK-511-1006P), blown tubular glass shape (Figure 4B, collection no. KSK-513-1004P) and cork crown shape (Figure 4C, collection no. KSK-514-1008P; Figure 5A, collection no. KSK-522-1004P).

3. An. pullus, Larva: Body coloration is usually green or brown. Thorax has dorsal parts almost covered with white waxy materials, primarily along the middle part, and narrowly extending towards the anterior edge of abdominal segment I. The tips of this waxy extension are usually blunt (Figure 6A, 6C; collection nos. KSK-543-1005L, KSK-543-1013L) or seldom pointed (Figure 6B, collection no. KSK-543-1006L). Abdomen has one distinct white waxy ornamentation, barrel-shaped, on dorsal part of segment III (Figure 6), and nothing on the abdominal segment V. Pupa: Abdominal segments III and IV have dorsal parts with white waxy ornamentations of various shapes, including Aladdin lamp shape (Figure 7A, 7B; collection nos. KSK-514-1001P, KSK-523-1003P), and pear shape (Figure 7C, collection no. KSK-520-1001P).

4. An. sinensis, Larva: Body coloration is usually green, reddish brown, or dark brown. Thorax has dorsal parts almost completely covered with white or creamish colored waxy materials, primarily along the anterior half, and narrowly extending towards the anterior edge of abdominal segment I. The tip of this extension is usually blunt (Figure 8A, 8B; collection nos. KSK-543-1003L, KSK-545-1007L). Abdomen has one distinct white or creamish waxy ornamentation, barrel-shaped or pear-shaped, on dorsal part of segment III (Figure 8A, 8B), and usually lacking ornamentation on abdominal segment V. It is very rare that dorsal parts of the abdomen have 2 white waxy ornamentations. Greenish larvae usually have no or very light waxy ornamentations on the body. Pupa: Cephalothorax has a cup-shaped white waxy ornamentation on dorsal part. Abdominal segments I-V have median longitudinal white waxy ornamentations on dorsal parts (Figure 5B, 5C; collection nos. KSK-522-1001P, KSK-523-1002P).

5. An. lesteri, Larva: Body coloration is usually green or dark brown. Thorax has dorsal parts almost covered with white waxy materials, and approximately cone-shaped along the median parts. It usually has a slightly pointed waxy ornamentation extending up to the anterior tip of the dorsum of abdominal segment I (Figure 8C, collection no. KSK-545-1009L). Abdomen has 2 distinct white waxy ornamentations on dorsal parts of segments III and V. Both ornamentations are barrel-shaped. Pupa. No live specimen was available to examine.

Comment

The seasonal occurrence and relative abundance of Anopheles larvae varied from one type of habitat to another. These variations may be due to different environmental conditions found in most habitats. Although Anopheles (Anopheles) larvae and pupae have been previously described based on slide-mounted larval and pupal specimens, (2,3,19) little is known about the waxy ornamentation or body covering patterns of these immature mosquitoes in nature. In spite of detailed morphological descriptions of the larvae and pupae in various publications, (2,3,19) identifications keys are often difficult to construct due to much variation of supposed diagnostic characters, including position, types, forms, and number of branches of setae and other body parts. During intensive field surveillance, the use of waxy body ornamentations of the larvae may be useful characters for initial identifications of some Anopheles species, but there is still a need for larval rearing to obtain emerged adults. Available adult identification keys as well as PCR and DNA sequencing for larvae, pupae, and adults may be used to ascertain species identifications. The shapes or patterns of waxy body ornamentations are also not very distinct in first-instar and second-instar larvae, unlike third-instar and fourth-instar larvae of Anopheles mosquitoes. More specimens from the field, as well as from laboratory reared materials are required to further study the morphological variations or body patterns based on body ornamentations as diagnostic characters, in the mosquito larvae and pupae.

ACKNOWLEDGMENTS

We thank Ms Soo-Yun Kim and Ms J. Stoffer for assistance in finalizing the photographs of mosquito larvae and pupae, and B. P. Rueda and C. R. Summers for providing valuable comments and suggestions to improve the manuscript.

This research was performed under a memorandum of agreement between the Walter Reed Army Institute of Research and the Smithsonian Institution, with institutional support provided by both organizations.

The opinions contained herein are those of the authors and do not reflect official views of the supporting agencies.

REFERENCES

(1.) Rueda LM. Two new species of Anopheles (Anopheles) Hyrcanus group (Diptera: Culicidae) from the Republic of South Korea. Zootaxa. 2005; 941:1-26. http://www.mapress.com/ zootaxa/2005f/zt00941.pdf.

(2.) Rueda LM, Kim HC, Klein T, et al. Distribution and larval habitat characteristics of Anopheles Hyrcanus Group and related mosquito species (Diptera: Culicidae) in South Korea. J Vector Ecol. 2006; 31:199-206.

(3.) Tanaka K, Mizusawa K, Saugstad ES. A Revision of the Adult and Larval Mosquitoes of Japan (including the Ryukyu Archipelago and the Ogasawara Islands) and Korea (Diptera: Culicidae). Gainesville, FL: American Entomological Institute; 1979.

(4.) Lee WJ, Klein TA, Kim HC, et al. Anopheles kleini, An. pullus, and An. sinensis: potential vectors of Plasmodium vivax in the Republic of Korea. J MedEntomol. 2007; 44:1086-1090.

(5.) Klein TA, Kim HC, Lee WC, et al. Reemergence, persistence, and surveillance of vivax malaria and its vectors in the Republic of Korea. In: Robinson WK, Bajoni D, eds. Proceedings of the Sixth International Conference on Urban Pests Hungary, Budapest, Hungary. 2008; 325-351. Available at: http://www.icup.org.uk/icupsearchres. asp?snum=0. Accessed February 8, 2017.

(6.) Joshi D, Choochote W, Park MH, et al. The susceptibility of Anopheles lesteri to infection with Korean strain of Plasmodium vivax. Malaria J. 2009; 8:42.

(7.) Joshi D, Kim JY, Choochote W, Park MH, Min GS. Preliminary vivax malaria vector competence for three members of the Anopheles hyrcanus group in the Republic of Korea. J Am Mosq Control Assoc. 2009; 27:312-314.

(8.) Rueda LM, Zhao T, Yajun Ma, et al. Updated distribution records of the Anopheles (Anopheles) hyrcanus species-group (Diptera: Culicidae) in China. Zootaxa. 2007; 1407:43-55.

(9.) Rueda LM, Brown TL, Kim HC, et al. Species composition, larval habitats, seasonal occurrence and distribution of potential malaria vectors and associated species of Anopheles (Diptera: Culicidae) from the Republic of Korea. Malaria J. 2010; 9:55-65.

(10.) Foley DH, Klein TA, Lee IY, et al. Mosquito species composition and Plasmodium vivax infection rates on Baengnyeong-do (Island), Republic of Korea. Korean JParasitol. 2011; 49:313-316.

(11.) Rueda LM, Li C, Kim HC, Klein TA, Foley DH, Wilkerson RC. Anopheles belenrae (Diptera: Culicidae), a potential vector of Plasmodium vivax in the Republic of Korea. J Am Mosq Control Assoc. 2010; 26:430-432.

(12.) Wilkerson RC, Li C, Rueda LM, Kim HC, Klein TA, Song GH, Strickman D. Molecular confirmation of Anopheles (Anopheles) lesteri from the Republic of South Korea and its genetic identity with An. (Ano.) anthropophagus from China (Diptera: Culicidae). Zootaxa. 2003; 378:1-14. Available at: http://www. mapress.com/zootaxa/2003f/zt00378.pdf.

(13.) Foley DH, Klein TA, Kim HC, Brown T, Wilkerson RC, Rueda LM. Validation of ecological niche models for potential malaria vectors, Anopheles (Anopheles) (Diptera: Culicidae), in the Republic of Korea. J Amer Mosq Control Assoc. 2010; 26:210-213.

(14.) Futch SH, McCoy CW, Childers CC. A guide to scale insect identification. Gainsville, FL: University of Florida Institute of Food and Agricultural Sciences; 2015:1-5. Extension Publication #HS-817. Available at: http://edis.ifs.ufl.edu/ch195. Accessed February 2, 2017.

(15.) Labanoski G, Soika G. Aphids (Hemiptera, Aphidoidea) on trees and shrubs belonging to Betulacea family in ornamental plant nurseries. Aphid and Other Hemipterous Insects. 2011; 17: 81-97.

(16.) Barao KR, Silva DS, Moreira GRP. External morphology of the immature stages of Neotropical heliconians: X. Heliconius sara apseudes (Lepidoptera, Nymphalidae, Heliconiinae). Iheringia Ser Zool. 2015; 105:523-533. Available at: http://dx.doi. org/10.1590/1678-476620151054523533.

(17.) South SH, Arnqvist G. Morphological variation of an ornament expressed in both sexes of the mosquito Sabethes cyaneus. Evolution Ecol Res. 2009; 11:1-21.

(18.) Li C, Lee JS, Groebner 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 South Korea (Diptera: Culicidae). Zootaxa. 2005; 939:1-8.

(19.) Harrison BA, Scanlon JE. Medical entomology studies--II. The subgenus Anopheles in Thailand (Diptera: Culicidae). Contr Am Entomol Inst. 1975; 12:1-307.

Leopoldo M. Rueda, PhD

Heung-Chul Kim, PhD

Sung-Tae Chong, MS

Terry A. Klein, PhD

Mustapha Debboun, PhD, BCE

AUTHORS

Dr Rueda is an Adjunct Scientist of the Smithsonian Institution and former Research Entomologist and Chief of the Walter Reed Biosystematics Unit, Entomology Branch, Walter Reed Army Institute of Research, located at the Smithsonian Institution, Museum Support Center, Suitland, Maryland.

Dr Kim is a Research Entomologist, 5th Medical Detachment/Medical Department Activity-Korea, 65th Medical Brigade, Republic of Korea.

Mr Chong is an Entomologist, 5th Medical Detachment/ Medical Department Activity-Korea, 65th Medical Brigade, Republic of Korea.

Dr Klein is the senior Entomologist, Medical Department Activity-Korea, 65th Medical Brigade, Unit 15281, Republic of Korea.

Dr Debboun is the Director of the Mosquito & Vector Control Division, Harris County Public Health, Houston, Texas.

Caption: Figure 1. Geographic locations of the 3 provinces in the Republic of Korea within which mosquitoe collections were conducted.

Caption: Figure 2. Mosquito larvae of Anopheles belenrae, dorsal view, showing waxy ornamentations of the thorax and abdomen (arrows).

Caption: Figure 3. Mosquito larvae of Anopheles kleini, dorsal view, showing waxy ornamentations of the thorax and abdomen (arrows).

Caption: Figure 4. Mosquito pupae of Anopheles kleini, dorsal view, showing waxy ornamentations of the abdomen (arrow).

Caption: Figure 5. Mosquito pupae of Anopheles kleini (A), and An. sinensis (B,C), dorsal view, showing waxy ornamentations of the abdomen (arrow).

Caption: Figure 6. Mosquito larvae of Anopheles pullus, dorsal view, showing waxy ornamentations of the thorax and abdomen (arrows).

Caption: Figure 7. Mosquito pupae of Anopheles pullus, dorsal view, showing waxy ornamentations of the abdomen (arrows).

Caption: Figure 8. Mosquito larvae of Anopheles sinensis (A,B), and An. lesteri (C), dorsal view, showing waxy ornamentations of the thorax and abdomen (arrows).
Relative abundance of Anopheles (Anopheles) larvae on various
habitats in 3 provinces (Geonggi, Gyeongsangbuk, Chungcheongbuk) of
the Republic of Korea (May 2007--October 2007) [part 1 of 2].

                           Relative Abundance (%) (a)

Habitat and Species    May      June     July    August

Rice paddies (n=111) (b)
An. belenrae            1.34     0.00     0.00     0.57
An. kleini              3.01    12.61    10.00     1.98
An. lesteri             0.00     0.00     0.00     0.00
An. pullus             54.18     4.50     0.88     1.98
An. sinensis           33.44    82.88    88.82    95.47
An. sineroides          8.03     0.00     0.29     0.00
Total collected (n)    299      444      340      353

Irrigation ditches (n=84) (c)
An. belenrae           11.11     0.00     0.55     0.78
An. kleini             29.17     2.87    18.78    13.62
An. lesteri             0.00     0.96     0.00     0.00
An. pullus              4.17     6.70     2.21     1.95
An. sinensis           51.39    61.72    78.45    81.71
An. sineroides          4.17    27.75     0.00     1.95
Total collected (n)     72      209      181      257

Drainage ditches (n=18) (d)
An. belenrae            0.00     0.00     0.00     0.00
An. kleini              0.00     0.00    14.29    25.00
An. lesteri             0.00     0.00     0.00     0.00
An. pullus              0.00    16.67     7.14     0.00
An. sinensis            0.00    83.33    78.57    75.00
An. sineroides          0.00     0.00     0.00     0.00
Total collected (n)      0        6       14        4

Ponds (n=61) (e)
An. belenrae            0.16     0.00     0.00     0.99
An. kleini             50.00    16.16    41.22    16.83
An. lesteri             0.00     0.00     0.00     0.00
An. pullus             13.16     8.08     1.53     6.93
An. sinensis           13.16     8.08    57.25    75.25
An. sineroides          2.63    67.68     0.00     0.00
Total collected (n)     38       99      131      202

Stream margins (n=32) (f)
An. belenrae            0.00     0.00     0.00     0.00
An. kleini             66.67     4.76     2.06     0.90
An. lesteri             0.00     0.00     0.00     0.00
An. pullus             33.33     0.00     0.00     0.00
An. sinensis            0.00    95.24    97.94    99.10
An. sineroides          0.00     0.00     0.00     0.00
Total collected (n)     3        21       97      111

Swamps (n=13)
An. belenrae            0.00     0.00     0.00     0.00
An. kleini             83.33     4.65    35.00    41.24
An. lesteri             0.00     0.00     5.00     1.03
An. pullus             16.67    90.70    10.00     2.06
An. sinensis            0.00     0.00    50.00    48.45
An. sineroides          0.00     4.65     0.00     7.22
Total collected (n)     12       43       40       97

Other habitats (n=22) (b)
An. belenrae            0.00     0.00     0.00     0.00
An. kleini              0.00     0.00     0.00     6.25
An. lesteri             0.00     0.00     0.00     0.00
An. pullus              0.00     0.00     8.33     0.00
An. sinensis            0.00     0.00    83.33    81.25
An. sineroides        100.00   100.00     8.33    12.50
Total collected (n)     2        1       12       16

                       Relative Abundance
                            (%) (a)

Habitat and Species   Sepember   October   6-month       Total
                                            Mean     Collected (n)
Rice paddies (n=111) (b)
An. belenrae            0.00       0.62     0.42       0.38 (7)
An. kleini              2.62       0.00     5.04      6.06 (113)
An. lesteri             0.00       0.00     0.00       0.00 (0)
An. pullus              0.75       0.00    10.38      10.4 (194)
An. sinensis           96.25      95.68    82.09     81.45 (1519)
An. sineroides          0.37       3.70     2.07       1.72 (32)
Total collected (n)     267        162                  (1865)

Irrigation ditches (n=84) (c)
An. belenrae            1.27       0.00     2.29       1.24 (13)
An. kleini             11.46       1.16    12.84      11.06 (116)
An. lesteri             0.00       0.58     0.26       0.29 (3)
An. pullus              2.55       1.16     3.12       3.05 (32)
An. sinensis           60.51      97.11    71.82      74.45 (781)
An. sineroides         24.20       0.00     9.68      9.91 (104)
Total collected (n)     157        173                  (1049)

Drainage ditches (n=18) (d)
An. belenrae            0.00       0.00     0.00       0.00 (0)
An. kleini             16.67       0.00     9.33       12.82 (5)
An. lesteri             0.00       0.00     0.00       0.00 (0)
An. pullus              0.00     100.00    20.63       12.82 (5)
An. sinensis           75.00       0.00    51.98      71.79 (28)
An. sineroides          8.33       0.00     1.39       2.56 (1)
Total collected (n)      12          3                   (39)

Ponds (n=61) (e)
An. belenrae            1.10       0.00     3.86       1.44 (12)
An. kleini             12.15       0.55    22.82      17.55 (146)
An. lesteri             0.00       0.00     0.00       0.00 (0)
An. pullus              3.31       3.87     6.15       5.05 (42)
An. sinensis           78.45      95.58    54.63      66.71 (555)
An. sineroides          4.97       0.00    12.55       9.25 (77)
Total collected (n)     181        181                   (832)

Stream margins (n=32) (f)
An. belenrae            0.00       0.00     0.00       0.00 (0)
An. kleini              4.05       0.00    13.07       2.14 (9)
An. lesteri             0.00       0.00     0.00       0.00 (0)
An. pullus              0.00       1.74     5.85       0.71 (3)
An. sinensis           95.95      92.17    80.07      95.49 (402)
An. sineroides          0.00       6.09     1.01       1.66 (7)
Total collected (n)      74        115                   (421)

Swamps (n=13)
An. belenrae            0.00       0.00     0.00       0.00 (0)
An. kleini              2.44       0.00    27.78      20.24 (67)
An. lesteri             7.32       0.00     2.22       1.81 (6)
An. pullus              2.44       1.02    20.48      14.80 (49)
An. sinensis           39.02      83.67    36.86      49.85 (165)
An. sineroides         48.78      15.31    12.66      13.29 (44)
Total collected (n)      41         98                   (331)

Other habitats (n=22) (b)
An. belenrae            0.00       0.00     0.00       0.00 (0)
An. kleini              0.00       0.00     1.04       2.56 (1)
An. lesteri             0.00       0.00     0.00       0.00 (0)
An. pullus              0.00       0.00     1.39       2.56 (1)
An. sinensis          100.00      50.00    52.43      76.92 (30)
An. sineroides          0.00      50.00    45.14       17.95 (7)
Total collected (n)     6          2                     (39)

Notes:

(a.) Relative abundance means for 6 months are based on the total
number of Anopheles larvae collected during the period.

(b.) Rice paddies, vacant or with rice plants

(c.) Irrigation ditches include concrete and nonconcrete ditches

(d.) Drainage ditches include concrete and nonconcrete ditches,
culverts, dammed ditches

(e.) Ponds include pond reservoirs

(f.0 Stream margins include stream ponds, stream inlets, algal mats

(a.) Relative abundance means for 6 months are based on the total
number of Anopheles larvae collected during the period.

(b.) Other habitats including ground pools, ground depressions, flood
pools, rock pools, uncultivated fields, artificial containers
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Author:Rueda, Leopoldo M.; Kim, Heung-Chul; Chong, Sung-Tae; Klein, Terry A.; Debboun, Mustapha
Publication:U.S. Army Medical Department Journal
Article Type:Report
Geographic Code:9SOUT
Date:Jan 1, 2017
Words:4593
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