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Mosquito biosurveillance on Kyushu Island, Japan, with emphasis on anopheles Hyrcanus group and related species (Diptera: Culicidae).

Mosquito-borne disease agents can pose a threat to humans, particularly to deployed troops, both in foreign environments and, if imported, domestically. Gaps exist in the fundamental knowledge regarding mosquito vector species, specifically concerning the species complex in subgenera Anopheles, Aedes, and Culex from central Japan. These 3 subgenera include major vector species that are responsible for transmitting malaria, dengue, Japanese B encephalitis, as well as other pathogenic microorganisms in many parts of the world, particularly in Asia. Anopheles Hyrcanus Group consists of several species that are vectors of malaria, filariasis and other mosquito-borne diseases in the Oriental and Palearctic regions. Currently, about 30 species have been described and named. (1-3) In 2004, about 27 species were listed in the Hyrcanus Group, with 6 species placed in the Lesteri Subgroup, 4 in the Nigerrimus Subgroup, and 17 in the unassigned subgroup. (3) In their 2013 review of the malaria vectors in the Greater Mekong subregion, Hii and Rueda (4) created the new Sinensis Subgroup that contains those previously unassigned species (An. sinensis Wiedemann, An. pullus Yamada, other 6 species). Recently, there is more focus on Anopheles Hyrcanus Group in Asia, primarily to clarify the taxonomy of the species complex and to update the distribution records of vectors and related species. (4-10) Although several Anopheles mosquito publications exist, they were not updated to include recent discoveries, taxonomic records, and related pertinent collection data from central Japan. (11-14) In 2005, Rueda and others (5) noted five species of An. Hyrcanus Group occurring in Japan, namely: An. sinensis, An. engarensis Kanda and Ogama, An. yatsushiroensis Miyazaki, An. sineroides Yamada, and An. lesteri Baisas and Hu. In 2013, Imanishi (15) recorded for the first time An. belenrae Rueda from Hokkaido, Japan. Anopheles pullus and An. kleini Rueda, the primary malaria vectors in South Korea, have never been collected in Japan. (16) Known and potential vectors of malaria in the Hyrcanus Group include An. sinensis, An. lesteri, An. belenrae, An. kleini, and An. pullus. (16)

The purpose of our study was to strengthen mosquito-borne disease biosurveillance capability in Japan by acquiring biogeographic vector data from sites identified as having taxonomic and ecological importance, thereby enhancing the knowledge base associated with potential malaria vectors, and incorporating this information as a component of already in-place mosquito surveillance programs, including the Walter Reed Biosystematics Unit's VectorMap/MosquitoMap, and the US Army Public Health Command Regions--North and Pacific mosquito surveillance training programs.

MATERIALS AND METHODS

Mosquito Field Collection and Identification

Specimen collections were conducted from 2006-2013 from various areas within Kumamoto, Fukuoka, Saga and Nagasaki Prefectures, on Kyushu Island, Japan (Figure 1). Additional specimens were previously collected by Dr Motoyoshi Mogi from 1984-2005 from localities in Saga and Nagasaki Prefectures. These prefectures were selected because the taxonomic records for the Anopheles Hyrcanus Group were unclear or had conflicting information regarding previously reported and described species from this region. The Hyrcanus Group includes all known malaria vector species in Japan (5,14) and it is essential to clarify the taxonomy of the group, including geographic distribution records of the group species. The mosquito taxonomic classification used in this paper follows that of Knight and Stone. (19)

Depending on the habitats (rice paddies, irrigation ditches, permanent and temporary pools, other standing water areas (Figures 2 and 3)), larvae were collected using a standard larval dipper (350 ml, 13 cm diameter) or a white plastic larval tray (25 x 20 x 4 cm) (BioQuip, Rancho Dominguez, CA). Each habitat within a location was surveyed for up to one hour or until about 100 larvae were collected. The latitude and longitude of each location was recorded using a hand-held global positioning system (GPS) unit (Garmin International, Olathe, KS) set to the WGS84 datum. Sampling locations were photographed using a digital camera to assist in verifying the accuracy of the habitat description. Collected larvae were placed in plastic Whirl-Pak bags (118 ml, 8x18 cm) (BioQuip, Rancho Dominguez, CA) and filled approximately XA full with water from the collection site. The Whirl-Pak was then tightly closed to retain air, placed in a cooler, and brought to the laboratory where the larvae were directly preserved in 100% ethanol for molecular identification. The remaining larvae were individually link-reared to adult stage, as morphological voucher specimens for this work (Figure 4). Emergent adults were pinned on paper points, each given a unique collection number, and identified using diagnostic morphological characters (Figure 5).

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

DNA Isolation and Sequencing

For molecular species identification, DNA was isolated from individual larvae, pupae, and adults (1 or 2 legs per adult) by phenol-chloroform extraction, and the PCR amplification protocol, cycling conditions, and direct sequencing were carried out using standard protocol. (17) A fragment of rDNA ITS2 was amplified using the primers 5.8S (5'-ATCACTCGGCTCGTGGATCG-3') and 28S (5'-ATGCTTAAATTTAGGGGGTAGTC-3'). (18) The PCR products were directly sequenced using Big Dye 3.0 (Applied Biosystems, Inc (ABI), Foster, CA) with an ABI 3100 sequencer. Sequences were edited using Sequencher (V4.8, Gene Codes Corporation, Ann Arbor, MI) and aligned in Clustal X.Sequences of An. Hyrcanus Group species (An.sinensis, An. lesteri) are those of previous studies using the primers therein. (17,18) Voucher specimens and collection records will be deposited in the US National Museum of Natural History (USNMNH) of the Smithsonian Institution, Suitland, MD.

Results

The summary of collection localities and larval habitats for Anopheles species (primarily An. sinensis and An. lesteri) from 4 prefectures (Fukuoka, Kumamoto, Nagasaki, Saga) of Kyushu Island, Japan, are presented in the Table (page 18). The map of Kyushu, with collection sites of mosquitoes, is shown in Figure 1. Prior to 2013, larvae of An. sinensis were collected from various habitats either alone or in association with the following Aedes or Culex species: Cx. (Culex) tritaeniorhynchus Giles larvae (in rice fields, irrigation ditches, marsh and drainage areas, ground pits or depressions) in Nagasaki and Kumamoto Prefectures. Aside from An. sinensis, no Anopheles species were collected from any larval habitats in association with Aedes or Culex species. In 2013, other Hyrcanus Group larvae (still to be identified using molecular sequences) were also found in association with the following: Cx. (Cux.) tritaeniorhynchus, Cx. (Cux.) spp.; Ae. (Finlaya) spp.; Ae. (Ochlerotatus) spp. in rice paddies and irrigation ditches in Nagasaki Prefecture (Isahaya, Moriyama, Obama-Unzen, Onakao).

[FIGURE 4 OMITTED]

[FIGURE 5 OMITTED]

During the 2013 survey of various localities in Kyushu Island, the rice paddies where we collected the larvae and pupae of Anopheles Hyrcanus Group had water pH ranging from 6.68-8.61 (mean, 7.77), millivoltage (175.00-237.00 mV; mean, 215.10) and temperature (30.50[degrees]C-32.80[degrees]C; mean, 32.10[degrees]C). Other water habitats (irrigation ditches, ponds, stream margin, pools, and drainage) that were positive for Anopheles larvae and pupae also exhibited variable pH, mV, and temperatures.

Culicine mosquitoes (nonanophelines) collected from Kyushu Island in 2013 included Ae. (Fin.) japonicus (Theobald) from Moriyama and Nagasaki (artificial containers, shrine stone bowls); Ae. (Fin.) togoi (Theobald) from Isahaya (pond); Ae. (Ste.) albopictus (Skuse) from Moriyama and Nagasaki (artificial containers, drainage ditches, shrine stone bowls, tree stumps or holes, temporary seepage); Cx. (Ocu.) bitaeniorhynchus Giles from Moriyama (drainage ditches); and Cx. (Cux.) tritaeniorhynchus from Moriyama, Obama-Unzen, Hitoyoshi (drainage ditches, irrigation ditches, rice paddies). About 60 mosquito larvae collected from Nagasaki Prefecture could not be identified morphologically, including those in Ae. (Finlaya) from Isahaya; Ae. (Ochlerotatus) from Nomozaki and Onakao; and Cx. (Culex) from Moriyama, Nagasaki, Obama-Unzen, Setoishi, Isahaya, Aikawa, and Onakao. Molecular analysis of those unidentified larval specimens of Aedes and Culex, together with both larvae and adults of An. Hyrcanus Group from 4 prefectures, will be completed in the future.

COMMENT

Among the Anopheles Hyrcanus Group species, An. pullus, An. sinensis, An. lesteri, An. kleini, and An. belenrae are known or potential vectors of vivax malaria in the Korean peninsula and other countries. Anopheles sinensis is the most common anopheline species in Japan, including the Ryukyu Islands. (14) It has long been suspected as the most important vector of malaria in Japan, including Okinawa and Hokkaido. Even though indigenous malaria has disappeared, this vector remains abundant throughout Japan. It is a known vector of malaria in South Korea and China, and it has a wide distribution in Asia. (4,5,8-10,14,20) Anopheles lesteri (= anthropophagus) is a very important vector of malaria in China. To clarify and stabilize the taxon, Rueda and others (6) designated and described the neotype and alloneotype of An. lesteri. This species was suspected to be an important vector of indigenous malaria in Japan, particularly in Hokkaido where it commonly occurs in great numbers. It is also common in the Ryukyu Islands and has been found more frequently in coastal regions in Honshu and Kyushu. (14) Anopheles yatsushiroensis is not known as a vector of indigenous malaria in Japan. Anopheles belenrae (Figure 4B), first recorded in Japan in 2013 from Hokkaido, (15) is a potential vector of vivax malaria in Korea. (21) Plasmodium berghei Vincke and Lips, a nonhuman specific parasite, was first detected from An. belenrae adults in South Korea. (22) The morphological details of the head, thorax, abdomen, wings, and legs of An. belenrae are shown in the Walter Reed Biosystematics Unit's website.* The other Hyrcanus Group species (ie, An. sineroides and An. engarensis), as well as several Anopheles (Anopheles) species (An. bengalensis Puri; An. koreicus Yamada and Watanabe; An. lewisi Ludlow; An. lindsayi japonicus Yamada; An. omorii Sakakibara; An. saperoi Bohart and Ingram; An. yaeyamaensis Somboon and Harbach), are not known vectors of indigenous malaria in Japan.

Most mosquito collections, including Anopheles species, noted by Tanaka and others (14) in 1979, are presently deposited at the National Institute of Infectious Diseases (NIID), Tokyo, Japan, where most of the Hyrcanus Group species were examined by author L. M. Rueda during his visit in 2006. In a recent conversation with the authors, Dr Kyoko Sawabe mentioned that there are some possible specimens of An. yatsushiroensis collected by Dr M. Otsuru in 1951 and 1964 on Kyushu Island now deposited at the NIID, Tokyo. These specimens should be examined for further morphological and molecular analysis to clarify the existence of this species. In 2003, Dr Motoyoshi Mogi inquired to check the type specimens of An. yatsushiroensis from the Department of Parasitology (DP), Faculty of Medicine, Kyushu University, Fukuoka, Kyushu (reported as the depository of An. yasushiroensis types by Miyazaki (12) in 1951). However, Professor Isao Tada (former director of the DP) informed Dr Mogi that no type specimens existed at the DP. It may be useful to designate neotypes for An. yatsushiroensis, if it is proven as a valid species.

Although previous researchers considered An. yatsushi roensis as a synonym of An. pullus, they used Korean specimens to obtain their molecular and morphological data. (23,24) However, because the type locality of An. yatsushiroensis is in Japan, it is necessary to do a genetic comparison of An. pullus from South Korea with the topotypic specimens from Japan to resolve definitively if the two are synonyms or not. In 1951, Miyazaki, (12) who first described An. yatsushiroensis, provided elaborate morphological descriptions, ecology, and distributions of this species. We did not collect An. pullus during our previous collections from 2002-2008 in Japan, and no report indicates the existence of An. pullus in that country. Furthermore, An. pullus is considered a major vector of vivax malaria in the Korean peninsula. (16) Through biosurveillance, it is also interesting to investigate if another major Korean malaria vector, An. kleini, is present in Japan.

In our attempt to recollect specimens of the Hyrcanus Group, particularly An. yatsushiroensis, we recently visited numerous localities and conducted extensive larval collections at various habitats in Nagasaki Prefecture and Kumamoto Prefecture (including Yatsushiro City, the type locality of An. yatsushiroensis reported by Miyazaki (12)) and neighboring areas from 2006 to 2013. Unfortunately, we were not able to collect samples of An. yatsushiroensis from 2006 to 2012.

Although Dr Sawabe mentioned that there are some possible specimens of An. yatsushiroensis deposited at the NIID, Tokyo, we have not examined them yet. Furthermore, more than 200 larvae and adults of An. Hyrcanus Group collected in 2013 from Kumamoto and Nagasaki Prefectures are still being examined and analyzed by morphological and molecular techniques. Molecular data (PCR, sequences) will be reported later, particularly from the 2013 specimens for possible presence of An. yatsushiroensis and other species in An. Hyrcanus Group on Kyushu Island.

ACKNOWLEDGEMENT

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

We express our sincere appreciation to the following: Dr Motoyoshi Mogi for arranging the visits of Dr Rueda to Saga and Fukuoka Prefectures, his help in mosquito collections, and for sharing his mosquito specimens; CPT Robert Moore and SGT J. Santano for their help in collecting mosquito samples from Kumamoto Prefecture; Professor Y. Oneda, for his help in collecting samples and guiding us in locating larval habitats in Akagawa and Takegima, Fukuoka Prefecture and Tosu City, Saga Prefecture. Special thanks go to Dr Noburo Minakawa, particularly for making the arrangements for our visit to Nagasaki, and Dr Kyoko Sawabe for correspondence and invitation to visit and examine the mosquito collections at NIID, Tokyo.

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.

(2.) Ramsdale CD. Internal taxonomy of the Hyrcanus Group of Anopheles (Diptera: Culicidae) and its bearing on the incrimination of vectors of malaria in the west of the Palearctic Region. European Mosq Bull. 2001;10:1-8.

(3.) Harbach RE. The classification of genus Anopheles (Diptera: Culicidae): a working hypothesis of phylogenetic relationships. Bull Entomol Res. 2004;94:537-553.

(4.) Hii J, Rueda LM. Malaria vectors in the Greater Mekong Subregion: overview of malaria vectors and remaining challenges. Southeast Asian J Trop Med Public Health. 2013;44(suppl 1):73-165, 306-307.

(5.) Rueda LM, Iwakama M, O'Guinn M, Mogi M, Prendergast BF, Miyagi I, Toma T, Pecor JE, Wilkerson RC. Habitats and distribution of Anopheles sinensis and associated Hyrcanus Group in Japan. J Am Mosq Control Assoc. 2005;21(4):458-463.

(6.) Rueda LM, Wilkerson RC, Li C. Anopheles (Anopheles) lesteri Baisas and Hu (Diptera: Culicidae): neotype designation and description. Proc Entomol Soc Washington. 2005;107(3):604-622.

(7.) Rueda LM, Ma Y, Song GH, Gao Q. Notes on the distribution of Anopheles (Anopheles) sinensis Wiedemann (Diptera: Culicidae) in China and the status of some Anopheles Hyrcanus Group type specimens from China. Proc Entomol Soc Washington. 2005;107(1):235-238.

(8.) Rueda LM, Kim HC, Klein TA, Pecor JE, Li C, Sithiprasasna R, Debboun M, Wilkerson RC. Distribution and larval habitat characteristics of Anopheles Hyrcanus Group and related mosquito species (Diptera: Culicidae) in South Korea. J Vector Ecol. 2006;31(1):199-206.

(9.) Rueda LM, Zhao T, Ma YJ, Gao Q, Guo Ding Z, Khuntirat B, Sattabongkot J, Wilkerson RC. Updated distribution records of the Anopheles (Anopheles) hyrcanus species-group (Diptera: Culicidae) in China. Zootaxa. 2007;1407:43-55.

(10.) Rueda LM, Gao Q. New records of Anopheles belenrae Rueda (Diptera: Culicidae) in North Korea. Proc Entomol Soc Wash. 2008;110:523-524.

(11.) Miyake M. Study on the anopheline mosquitoes in Kyushu. Hukuoka Acta Med. 1950;41:918-927.

(12.) Miyazaki I. On a new anopheline mosquito Anopheles yatsushiroensis n. sp. found in Kyushu, with some remarks on two related species of the genus. Kyushu Mem Med Sci. 1951;2:195-206.

(13.) Otsuru M, Ohmori Y. Malaria studies in Japan after World War II. Part II. The search for Anopheles sinensis sibling species group. Japan J Exp Med. 1960;30:33-65.

(14.) 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). In: Contributions of the American Entomological Institute. Vol 16. Gainesville, Florida: American Entomological Institute; 1979:1-987.

(15.) Imanishi N. Morphological and Phylogenetic Study of Anopheles belenrae First Recorded from Hokkaido, Japan [master's thesis]. Kanagawa, Japan: Meiji University; 2013.

(16.) Klein TA, Kim HC, Lee WJ, Rueda LM, 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, Budapest, Hungary. 2008. 325-331. Available at: http://www.icup.org.uk/reports/ICUP892.pdf. Accessed May 7, 2014.

(17.) 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.

(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). Zoo taxa. 2005;939:1-8.

(19.) Knight K, Stone A. A Catalog of the Mosquitoes of the World (Diptera: Culicidae). Vol 6. College Park, Maryland: Entomological Society of America; 1977.

(20.) Harrison BA, Scanlon JE. Medical entomology studies--II. The subgenus Anopheles in Thailand (Diptera: Culicidae). In: Contributions of the American Entomological Institute. Vol 12, No. 1. Gainesville, Florida: American Entomological Institute; 1979:1-307.

(21.) Rueda LM, Li C, Kim HC, Klein TA, Foley DH, Wilkerson RC. Anopheles belenrae, a potential vector of Plasmodium vivax in the Republic of Korea. J Am Mosq Control Assoc. 2010;26(4):430-432.

(22.) Harrison GF, Foley DH, Rueda LM, et al. Plasmodium-specific molecular assays produce uninterpretable results and non-Plasmodium spp. sequences in field-collected Anopheles vectors. Am J Trop Med Hyg. 2013;89(6):1117-1121.

(23.) Hwang UW, Yong TS, Ree HI. Molecular evidence for synonymy of Anopheles yatsushiroensis and An. pullus. J Am Mosq Control Assoc. 2004;20(2):99-104.

(24.) Shin EH. Hong HK. A new synonym of Anopheles (Anopheles) pullus Yamada, 1937: A. (A.) yatsushiroensis Miyazaki, 1951. Kor J Entomol. 2001;31:1-5.

Leopoldo M. Rueda, PhD

Benedict Pagac, BS

Masashiro Iwakami, BS

Alexandra R. Spring, MS

Maysa T. Motoki, PhD

James E. Pecor, BS

Yukiko Higa, PhD

Kyoko Futami, PhD

Nozomi Imanishi, MS

MAJ Lewis S. Long, MS, USA

COL Mustapha Debboun, MS, USA

* http://www.wrbu.org/SpeciesPages_ANO/ANO_A-det/ANbln_Adet.html

Dr Rueda is a Research Entomologist, Principal Investigator, and Acting 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.

Mr Benedict Pagac is the Chief, Entomology Section at the US Army Public Health Command Region-North, Fort George G. Meade, Maryland.

Mr Iwakami is an Entomologist at the US Army Public Health Command-Pacific, Entomology Program. Camp Zama, Japan.

Ms Spring is a Molecular Biologist at the Entomology Section, US Army Public Health Command Region-North, Fort George G. Meade, Maryland.

Dr Motoki is a Postdoctoral Entomologist at the Entomology Department, Smithsonian Institution, Museum Support Center, Suitland, Maryland.

Mr Pecor is a Museum Specialist at the Walter Reed Biosystematics Unit, Entomology Branch, Walter Reed Army Institute of Research, located at the Smithsonian Institution, Museum Support Center, Suitland, Maryland.

Dr Higa, Dr Futami, and Ms Imanishi are Assistant Professors and Graduate Student, respectively, at the Department of Vector Ecology and Environment, Institute of Tropical Medicine (NEKKEN), Nagasaki University, Nagasaki City, Nagasaki, Japan.

MAJ Long is currently on training leave from his position as 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.

COL Debboun is the Chief of the Department of Preventive Health Services, Academy of Health Sciences, US Army Medical Department Center & School, Fort Sam Houston, Texas. He is also the Chairman of the Army Medical Department Journal Editorial Review Board.
Summary of collection localities and larval habitats for
Anopheles (Anophleles) in 4 prefectures of Kyushu Island,
Japan.

Prefecture          Location           Grid coordinates

Fukuoka      Akagawa, Ogori City       33.34975N/130.51352E
Fukuoka      Takejima, Yasutake-       33.34975N/130.54597E
               mache, Kurume
Kumamoto     Amitsu, Uto City          32.69973N/130.60432E
Kumamoto     Gyokuto City, Tamana      32.91638N/130.62565E
               County
Kumamoto     Hitoyoshi                 32.22652N/130.77038E
Kumamoto     Kato shrine, Yatsushiro   32.47998N/130.57202E
Kumamoto     Lake Ezu                  32.77755N/130.73855E
Kumamoto     Matsubase, Uki City       32.65355N/130.67050E
Kumamoto     Matsubase, Uki City       32.65625N/130.66788E
Kumamoto     Matsubase, Uki City       32.65355N/130.67050E
Kumamoto     Sumiyoshi, Uto City       32.70005N/130.60015E
Kumamoto     Takasima, Yatsushiro      32.52158N/130.57750E
Kumamoto     Tamana City, Tamana       32.91638N/130.54523E
               County
Kumamoto     Ueki City                 32.88017N/130.68148E
Kumamoto     Uto                       32.69660N/130.66845E
Kumamoto     Uto                       32.69660N/130.66845E
Kumamoto     Yatsushiro                32.50033N/130.61932E
Kumamoto     Yatsushiro                32.52158N/130.57750E
Nagasaki     Ariake-cho, Nagasaki      32.69414N/130.32505E
Nagasaki     Goto, Fukue Island        32.67867N/128.76802E

Nagasaki     Goto, Fukue Island        32.67867N/128.76802E
Nagasaki     Goto, Fukue Island        32.67867N/128.76802E
Nagasaki     Goto, Fukue Island        32.67867N/128.76802E
Nagasaki     Goto, Fukue Island        32.67867N/128.76802E
Nagasaki     Isahaya                   32.81308N/130.12767E
Nagasaki     Isahaya                   32.81308N/130.12767E
Nagasaki     Isahaya                   32.81308N/130.12767E
Nagasaki     Isahaya-shi,              32.80759N/130.10737E
               Kamiimuta,
               Moriyama-cho
Nagasaki     Mikawa-machi              32.78590N/129.88779E
Nagasaki     Moriyama                  32.83508N/130.11372E
Nagasaki     Moriyama                  32.83508N/130.11372E
Nagasaki     Nagasaki                  32.77217N/129.86950E
Nagasaki     Nomozaki                  32.58570N/129.75660E
Nagasaki     Obama-Unzen               32.71354N/130.20073E
Nagasaki     Obama-Unzen               32.71354N/130.20073E
Nagasaki     Obama-Unzen               32.71354N/130.20073E
Nagasaki     Obama-Unzen               32.71354N/130.20073E
Nagasaki     Onako                     32.88408N/129.69598E
Nagasaki     Togitsu                   32.82683N/129.84866E
Nagasaki     Tsushima                  34.17745N/129.29039E
Nagasaki     Utzutzugawa               32.79328N/129.92803E
Nagasaki     Utzutzugawa               32.79328N/129.92803E
Saga         Fukutomi                  33.17567N/130.17284E
Saga         Kase                      33.23807N 130.25824E
Saga         Kinyu                     33.24204N 130.29149E
Saga         Morita                    33.09454N 130.10894E
Saga         Nabeshima                 33.27991N 130.26614E
Saga         Shiroishi                 33.17837N 130.14394E
Saga         Shiroishi                 33.17837N 130.14394E
Saga         Yamato-cho                33.14766N 130.14832E
Saga         Yamato-cho                33.14766N 130.14832E
Saga         Tosu City                 33.34463N 130.51352E

Prefecture     Collection        Stage             Collector
                  date

Fukuoka      19-20 Sep 2008    Adult (a)     L. M. Rueda, Y. Oneda
Fukuoka      19-20 Sep 2008    Adult (a)     L. M. Rueda, Y. Oneda
Kumamoto      23 Sep 2008      Adult (a)        L. M. Rueda, M.
                                              Iwakami, J. Santano
Kumamoto      22 Sep 2008      Adult (a)        L. M. Rueda, M.
                                              Iwakami, J. Santano
Kumamoto      12 Jul 2013        Larva       L. M. Rueda, B. Pagac,
                                                   M. Iwakami
Kumamoto      15 Sep 2008      Adult (a)        L. M. Rueda, M.
                                              Iwakami, J. Santano
Kumamoto      24 Sep 2008        Adult          L. M. Rueda, M.
                                              Iwakami, J. Santano
Kumamoto      30 Aug 2006      Adult (a)      M. Iwakami, R. Moore
Kumamoto      17 Sep 2008      Adult (a)        L. M. Rueda, M.
                                              Iwakami, J. Santano
Kumamoto      30 Aug 2006      Adult (a)      M. Iwakami, R. Moore
Kumamoto      22 Sep 2008      Adult (a)        L. M. Rueda, M.
                                              Iwakami, J. Santano
Kumamoto      15 Sep 2008      Adult (a)        L. M. Rueda, M.
                                              Iwakami, J. Santano
Kumamoto      22 Sep 2008      Adult (a)        L. M. Rueda, M.
                                              Iwakami, J. Santano
Kumamoto      22 Sep 2008      Adult (a)        L. M. Rueda, M.
                                              Iwakami, J. Santano
Kumamoto      29 Aug 2006      Adult (a)      M. Iwakami, R. Moore
Kumamoto      29 Aug 2006      Adult (a)      M. Iwakami, R. Moore
Kumamoto      11 Jul 2013     Larva, pupa,      L. M. Rueda, B.
                               adult (a)       Pagac, M. Iwakami
Kumamoto      16 Sep 2008      Adult (a)        L. M. Rueda, M.
Nagasaki      20 Jul 1988      Adult (a)      Iwakami, J. Santano
Nagasaki      17 Jul 2013     Larva, pupa       L. M. Rueda, B.
                                               Pagac, M. Iwakami
Nagasaki      17 Jul 2013        Larva          L. M. Rueda, B.
                                               Pagac, M. Iwakami
Nagasaki      17 Jul 2013      Adult (a)        L. M. Rueda, B.
                                               Pagac, M. Iwakami
Nagasaki      17 Jul 2013        Larva          L. M. Rueda, B.
                                               Pagac, M. Iwakami
Nagasaki      17 Jul 2013      Adult (a)        L. M. Rueda, B.
                                               Pagac, M. Iwakami
Nagasaki      12 Jul 2013      Adult (a)              NG1
Nagasaki      12 Jul 2013        Larva                NG1
Nagasaki      12 Jul 2013        Larva                NG1
Nagasaki      27 May 2006        Adult             T. Yoshio
Nagasaki      27 May 1962        Adult                NU
Nagasaki       9 Jul 2013      Adult (a)        L. M. Rueda, B.
                                               Pagac, M. Iwakami
Nagasaki       9 Jul 2013        Larva          L. M. Rueda, B.
                                               Pagac, M. Iwakami
Nagasaki      20 Jun 1989        Adult              M. Mogi
Nagasaki      15 Jul 2013        Larva                NG2
Nagasaki      10 Jul 2013        Larva          L. M. Rueda, B.
                                               Pagac, M. Iwakami
Nagasaki      10 Jul 2013        Larva          L. M. Rueda, B.
                                               Pagac, M. Iwakami
Nagasaki      10 Jul 2013        Larva          L. M. Rueda, B.
                                               Pagac, M. Iwakami
Nagasaki      10 Jul 2013      Adult (a)        L. M. Rueda, B.
                                               Pagac, M. Iwakami
Nagasaki      16 Jul 2013        Larva                NG2
Nagasaki     7-9 Aug 1956;       Adult                NU
              22 Jul 1962
Nagasaki      27 May 1962        Adult                NU
Nagasaki       9 Jul 2013        Larva          L. M. Rueda, B.
                                               Pagac, M. Iwakami
Nagasaki       9 Jul 2013        Larva          L. M. Rueda, B.
                                               Pagac, M. Iwakami
Saga         13, 20, 28 Aug      Adult              M. Mogi
            2005; 11, 13, 24
              Sep 2005; 10
               Oct 2005;
Saga           17 Sep 2005       Adult              M. Mogi
Saga        2, 5, 10 Jun 1986    Adult              M. Mogi
Saga           16 May 1995       Adult              M. Mogi
Saga           30 May 1985;      Adult              M. Mogi
               14 Jun 1985;
               3, 5, 6, 7,
               20 Jun 1986;
               9 Jun 1990;
               7 Jun 1995;
               3 Jun 1996
Saga           7 May 2000        Adult              M. Mogi
Saga           3 Nov 1997;       Adult              M. Mogi
                7 May 2000
Saga           10 Apr 2000       Adult            T. Sunahara
Saga           5 Jun 1986;       Adult            T. Sunahara,
                24, 25, 26                          M. Mogi
                Apr 2000;
              10, 11, 12, 25
              May 2000; 24,
               25 Apr 2004
Saga           20 Sep 2008       Adult            L. M. Rueda,
                                  (a)               Y. Oneda

Prefecture    Habitat        Collection       Anopheles
              type (b)          No.          (Anopheles)
                                               Species

Fukuoka          RC            JP08-9         sinensis
Fukuoka          RC           KP08-10         sinensis
Kumamoto       ID, RP       JP08-17, 18       sinensis
Kumamoto         PO           JP08-14         sinensis
Kumamoto     ID, RH, RP     JP13-19, 21       Hyrcanus
                                              Group (c)
Kumamoto         DD            JP08-2          lesteri
Kumamoto         LM           JP08-19         sinensis
Kumamoto         RP       JP06-2-37A, 40A      lesteri
Kumamoto         RP          JP08-7, 8         lesteri
Kumamoto         RP        JP06-2-1A, 2A,     sinensis
                          3A, 4A, 6A, 25A;
                             JP08-5, 6
Kumamoto         ID           JP08-17B        sinensis
Kumamoto       HD, WT        JP08-1, 4         lesteri
Kumamoto         RP         JP08-15, 16       sinensis
Kumamoto       ID, RP       JP08-12, 13        lesteri
Kumamoto         RP       JP06-1-50A, 51A      lesteri
Kumamoto         RP        JP06-1-1A, 2A,     sinensis
                            3A, 4A, 5A,
                              7A, 16A
Kumamoto         SP           JP13-18         Hyrcanus
                                              Group (c)
Kumamoto         RP            JP08-3         sinensis
Nagasaki         RC            JPM-5          sinensis
Nagasaki         ID           JP13-31         Hyrcanus
                                              Group (c)
Nagasaki         RP           JP13-30         Hyrcanus
                                              Group (c)
Nagasaki         RP           JP13-30        Hyrcanus Group (d)
Nagasaki         RP           JP13-32        Hyrcanus Group (d)
Nagasaki         RP           JP13-32        Hyrcanus Group (d)
Nagasaki         PO           JP13-23        Hyrcanus Group (d)
Nagasaki         PO           JP13-23        Hyrcanus Group (d)
Nagasaki         RP           JP13-25        Hyrcanus Group (d)
Nagasaki         --            JPM-5              sinensis
Nagasaki         --            JPM-5              sinensis
Nagasaki         RP            JP13-7        Hyrcanus Group (d)
Nagasaki         RP            JP13-8        Hyrcanus Group (d)
Nagasaki         RP            JPM-5              sinensis
Nagasaki         AC           JP13-26        Hyrcanus Group (d)
Nagasaki         RP           JP13-14        Hyrcanus Group (d)
Nagasaki         RP           JP13-15        Hyrcanus Group (d)
Nagasaki         WC           JP13-16        Hyrcanus Group (d)
Nagasaki         WC           JP13-16        Hyrcanus Group (d)
Nagasaki         RP           JP13-29        Hyrcanus Group (d)
Nagasaki         --            JPM-5              sinensis
Nagasaki         --            JPM-5              sinensis
Nagasaki         RP           JP13-13        lindsayi japonicus
Nagasaki         RP           JP13-13        Hyrcanus Group (d)
Saga             LF           JPM-22-1            sinensis
Saga             ID       JPM-21-1, -2, -3         sinensis
Saga             RP       JPM-8, 9                  lesteri
Saga             CA       JPM-14                   sinensis
Saga             LF       JPM-4, 5, 6, 7            lesteri
Saga             RP       JPM-19-1                  lesteri
Saga             NE       JPM-14, 15, 19-2,        sinensis
                            19-3, 19-5,
                            19-5
Saga             CA       JPM-18                    lesteri
Saga             CA       JPM-8, 15, 16,           sinensis
                            17, 18
Saga             GT       JP08-11                   lesteri

(a) Field collected larvae or pupae, reared to emerged adults.

(b) DD, drainage ditch; HD, hill or road side ditch; ID,
irrigation ditch; LM, lake margin; PO, pond; RC, resting at
cowshed or cattle barn; RH, rock hole, pool; RP, rice paddy;
SP, stream or river margin or pool; WT, water tank, trough or
PVC tube waterer.

(b1) NG1 indicates L. M. Rueda, B. Pagac, M. Iwakami, Y. Higa,
K. Futami, N. Imanishi. NU indicates Nagasaki University,
Entomology Collection. NG2 indicates L. M. Rueda, B. Pagac,
M. Iwakami, Y. Higa, K. Futami.

(b2) CA, road ditch or small canal; GT, ground pit or depression;
ID, irrigation ditch; LF, lotus field; NE, caught by insect net;
RP, rice paddy.

(c) DNA isolation and sequencing still to be completed.

(c1) AC, artificial containers (tires, plastic jugs, kettle, etc);
CA, road ditch or small canal; ID, irrigation ditch; LF, lotus
field; PO, pond; RP, rice paddy; WC, water well/cistern.

(d) DNA isolation and sequencing still to be completed.
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Article Details
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Author:Rueda, Leopoldo M.; Pagac, Benedict; Iwakami, Masashiro; Spring, Alexandra R.; Motoki, Maysa T.; Pec
Publication:U.S. Army Medical Department Journal
Article Type:Report
Geographic Code:9JAPA
Date:Jul 1, 2014
Words:4719
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