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Mosquito Surveillance Conducted by US Military Personnel in the Aftermath of the Nuclear Explosion at Nagasaki, Japan, 1945.

On August 9, 1945, the United States military detonated a nuclear bomb over the city of Nagasaki, Japan, marking only the second (and last) time a nuclear weapon was ever used in combat. Five days later, Japan officially surrendered to Allied forces, ending World War II (WWII). On this day, now known as V-J Day (Victory over Japan) President Harry Truman selected General Douglas A. MacArthur to supervise the Allied occupation of Japan. During this occupation in the months after the end of WWII, US military entomologists were tasked with developing and implementing a mosquito control plan for Japan. (1) Challenges related to mosquito control abounded in postwar Japan, many of which had been building during the years leading up to the end of the war. In 1942, there was a Dengue fever outbreak reported from Nagasaki, however, with the destruction of cities and the displacement of populations, information about Dengue fever incidence before American occupation is limited. (2) According to La Casse, (1) Japanese informants claimed that Dengue fever was completely unheard of in Japan before 1942, (1) but approximately 13,000 Dengue fever cases were reported in that year. It is important to note that many houses in Japan were required to keep concrete tanks holding water for fire suppression during wartime and these containers were perfect habitat for container-breeding mosquitoes such as Aedes albopictus Skuse. (2) One of the first directives by US military authorities was to fill with dirt, overturn, or destroy these containers. (2) Other important container-breeding sites included cemeteries, particularly for Ae. albopictus and Ae. togoi (Theobald). Although each gravesite may only have provided habitat for a few larvae, large number of these breeding sites meant large populations of mosquitoes in cities like Nagasaki. (2) Gray articulated this challenge eloquently, while commenting generally on this challenge impacting people across the world: "It is a strange commentary on human intelligence that the graves of the dead are permitted to bring death, disease and discomfort to the living." (2) Mosquitoes collected from "foul-water," including liquid manure tanks, posed another significant challenge. These tanks were present in most agriculture fields and were productive breeding sites for species such as Culex quinquefasciatus Say, Cx. pipiens Linnaeus, and Armigeres species. (2) Finally, rice paddies are of particular concern for the malaria vector, Anopheles sinensis Wiedemann sensu lato in and around Nagasaki. Mosquitoes that breed in containers, polluted water, and rice paddies were the primary concerns for Nagasaki under Allied occupation. In a 1947 report prepared by the Commanding Officer of the US Army 207th Malaria Survey Detachment (MSD), CPT Walter La Casse, noted that there was great concern in early 1946 that an epidemic of Japanese encephalitis (JEV) was a major threat to American forces occupying mainland Japan. (1) Thus, a plan was developed to collect as much bionomics data as possible to help develop mosquito abatement plans. The 207th MSD stationed in Kyoto, Japan, conducted mosquito surveys from 1946-1949. (3) Mosquito taxonomy in Japan was not well established before WWII. Until 1945, only 12 mosquito species were described from the islands; however, by 1959, the total number of species known from Japan was 45. (3)

In this article, we present digitized records and data of mosquito specimens housed within the US National mosquito collection that are associated with US military surveillance in the city of Nagasaki during Allied occupation of Japan. The specimens of interest were donated to the United States National Museum (USNM) collection by Charles A. Triplehorn in November 1973, and are part of the personal collection of Dr Donald J. Borror who is most famous for his work using bioacoustics to track bird distributions. However, in 1945, Dr Borror was a US Navy entomologist deployed to Japan. (4) In correspondence with the South East Asia Mosquito Project (later redesignated as the Walter Reed Biosystematics Unit (WRBU)) staff, Dr Borror mentioned documented paper records by Triplehorn containing detailed collection data. An exhaustive search of the WRBU archives did not discover these records. In 1974, there was at least one attempt to contact Dr Borror to request additional information regarding these collection data, but with no response. This article describes how specimen label data related to these collections were digitized and photographed, and all specimens cataloged and accessioned into the USNM inventory.

MATERIALS AND METHODS

The National mosquito collection is comprised of approximately 1.5 million specimens and is managed by the WRBU. Digitization is continuous, however, generally focused on gathering specimen data related to ongoing vector-borne disease outbreaks or taxonomic revisions. The Nagasaki specimens were due for accession but had a low priority for digitization and had remained unnoticed for decades. Upon rediscovering these specimens during a routine search for species distribution updates, their historical importance was immediately recognized and the rest of the collection was systematically inspected for other specimens collected in post-WWII Japan.

Specimen labels were digitized by entering verbatim label data into a standard USNM entomology EMu (electronic museum) data entry form. All specimens were assigned a unique USNM catalog number to be officially accessioned into the collection. Although all specimens were assigned new catalog numbers, each record retains every associated original specimen number within the individual records. Each specimen received a unique number and all associated preparations (eg, slides) were also assigned the same catalog number so that all objects associated with each specimen can be tracked using the same catalog number. The 2D matrix barcode labels with these catalog numbers were affixed to each specimen. Barcode labels for pinned specimens were added under existing labels and can be read by a barcode scanner when the specimen is inverted, while barcodes were affixed directly to slide preparations (Figure 1). Specimen labels were photographed to allow verbatim data to be independently verified and address possible errors in interpretation. Specimens were photographed using a Dino-Lite Edge handheld digital microscope (Dino-Lite US, Torrance, CA) with extended depth of field capability for vertical imaging to document their current condition. Each specimen was examined and recorded to document its current condition, sex, and if remounting was required. Figures 1, 2, and 3 show 3 specimen records including photographs, digitized label data, and notes.

In order to map these localities, each specimen was geo-referenced using the point-radius method5 which investigates text descriptions of localities on specimen labels as well as any information relevant to the description of the collection site provided in original descriptions. This allows assignment of the most precise gazetteer entry as possible to serve as a centroid of a collection event. (6) To account for the uncertainty of the exact locality, an uncertainty measurement was assigned using the Mammal Networked Information System Georeferencing Calculator (http://maniset.org). (5) This method accounts for errors and missing information including coordinate datum, extent of the named place, and precision of the coordinates assigned. All specimen label data that could be used to characterize the collecting events were captured and retained. (7) This approach has been applied in the past to specimens of the USNM Psychodidae collection. (8,9) As details about the exact collection sites are not available, specimens within the WWII Japan collection were generally assigned a centroid for the city of Nagasaki and an uncertainty measurement encompassing the entire city.

RESULTS

A total of 452 specimens representing 16 unique taxa with a summary list of habitat descriptions (bionomics) reported for each mosquito species are shown in the Table. Although some specimens showed signs of damage, eg, rubbed setae, broken antennae and/or legs, wings, etc, most were in fair shape with labels that could be read clearly. Nearly all specimens in this investigation were found to have been collected in Nagasaki, Japan, in September and October, 1945. Smaller subsets of specimens from the 207th MSD were collected in Nagasaki, Kyoto, and Isahaya-shi between 1947 and 1950. Of the 16 taxa found in this collection, 8 are known to vector pathogens, including Plasmodium sp. (An. sinensis), Japanese encephalitis virus (Ae. togoi, Cx. tritaeniorhynchus Giles, Cx. vishnui Theobald) and Dengue fever virus (Ae. albopictus). In addition, the Table includes the vector status for each taxon.

COMMENT

When considering the time and place of these collections, it is natural to wonder whether these specimens show any signs of radiation exposure that can be measured today. However intriguing, it is not likely that these specimens will have any recordable radiation. One reason is that after the initial explosion over Nagasaki, only low levels of radiation were recorded from areas outside of a 1.5 km radius from ground zero. (10) Additionally, nuclear fallout is expected to affect invertebrates differently depending on their life history; insects that used topsoil would be more adversely affected than those, such as mosquitoes, that use water that is frequently flushed or diluted with rainfall. Fuller et al (11) suggested resilience of aquatic invertebrate populations to radionuclides.

Since data characterizing the risk to insects after a nuclear explosion are rare, studies examining the impact of radiation exposure due to nuclear reactor meltdowns may be more appropriate. Williams et al (12) investigated the effects of the Chernobyl nuclear disaster on local populations of Chironomidae species and found morphological deformities in 60% of field-collected larvae. Although a significant finding, radiation from uncontained nuclear waste was pervasive in this location and had been affecting the ecosystem for years after the disaster. A study investigating the possible impact of the Fukushima Dai-ichi Nuclear Power Plant meltdown of 2011 on local populations of the pale grass blue butterfly (Zizeeria maha) found some evidence of morphological abnormalities attributed to radiation exposure. (13) However, this site also had persistent radiation exposure risk. Biological asymmetry, known as fluctuating asymmetry (FA) can be used as a measure of developmental stability. A study (14) on stag beetles (Lucanus cervus) in Chernobyl found that males in highly contaminated sites had significantly elevated levels of FA in secondary sexual characters compared to males from control sites. A detailed study of FA in mosquito samples from Nagasaki may or may not reveal the physical effects of radiation but data on mating success are no longer possible.

The specimens examined during this study represent a lasting and permanent record for the invaluable work done to characterize and combat the mosquito-borne disease threats during the Allied forces occupation of Japan. Military entomologists and other medical officers during that time made systematic collections to develop bionomic profiles for vector species to inform mosquito abatements plans. Although it has been nearly 75 years since these collections were made, the specimens form a lasting legacy that can be used in taxonomic revisions and to accurately predict species distributions and biology.

ACKNOWLEDGEMENTS

This study was made possible by a FY2017 grant (P0091_17_WR_1.3.1.) from the Armed Forces Health Surveillance Branch and its Global Emerging Infections Surveillance Section.

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

REFERENCES

(1.) La Casse WJ. Mosquito Survey Data on Japan and Their Application in the Control of Mosquito-Borne Diseases. Office of the Surgeon, HQ Corps, APO 301; 1947.

(2.) Gray HF. Mosquito control problems in Japan. Mosq News. 1947;7(1):7-11.

(3.) Tanaka K, Mizusawa K, Saugstad E. A revision of the adult and larval mosquitoes of Japan (including Ryukyu archipelago and the Ogasawara islands) and Korea (Diptera: Culicidae). Contrib Am Entomol Inst. 1979;16.

(4.) Gaunt SL. In memoriam: Donald J. Borror. The Auk. 1989;106:321-323. Available at: https://sora. unm.edu/sites/default/files/journals/auk/v106n02/ p0321-p0323.pdf. Accessed July 9, 2018.

(5.) Wieczorek J, Hijmans R, Guo Q. Point-radius method for georeferencing locality descriptions and calculating associated uncertainty. Int J Geogr Inf Sci. 2004;18(8):745-767.

(6.) GeoNames Website. Available from: http://www. geonames.org/. Accessed March 2018.

(7.) Foley DH, Wilkerson RC, LM Rueda. Importance of the "what," "when," and "where" of mosquito collection events. J Med Entomol. 2009;46(4):717-722.

(8.) Rueda L, Foley D, Pecor D, Wolkoff M. Records and distribution of New World Phlebotomine sand Flies (Psychodidae: Diptera), with special emphasis on primary types and species diversity. US Army Med Dep J. July-September 2015:33-46.

(9.) Rueda L, Pecor J, Wolkoff M, Pecor D, Benyamin S, Bousses P, Debboun M. New records, distribution, and updated checklists of old world Phlebotomine sand flies, with emphasis on Africa, Southwest Asia, and Central Asia. US Army Med Dep J. January-June 2017:65-85.

(10.) World Nuclear Association. Hiroshima, Nagasaki, and Subsequent Weapons Testing [internet]. Updated March 2016. Available at: http://www.world-nuclear.org/ information-library/safety-and-security/ radiation-and-health/hiroshima,-nagasaki,-andsubsequent-weapons-testin.aspx. Accessed March 2018.

(11.) Fuller N, Smith JT, Nagorskaya GL. Does Chernobyl-derived radiation impact the developmental stability of Asellus aquaticus 30 years on?. Sci Total Environ. 2017;576:242-250.

(12.) Williams DD, Nesterovitch AI, Tavares AF, Muzzatti EG. Morphological deformities occurring in Belarusian chironomids (Diptera: Chironomidae) subsequent to the Chernobyl nuclear disaster. Freshw Biol. 2001; 46(4):503-512. Available at: https://onlinelibrary.wiley.com/doi/full/10.1046/ j.1365-2427.2001.00699.x. Accessed July 9, 2018.

(13.) Hiyama A, Nohara C, Kinjo S, Taira W, Gima S, Tanahara A, Otaki, JM. The biological impacts of the Fukushima nuclear accident on the pale grass blue butterfly. Sci Rep. 2012;2(570). Available at: http://www.nature.com/articles/srep00570. Accessed July 9, 2018.

(14.) Meller AP. Developmental instability and sexual selection in stag beetles from Chernobyl and a control area. Ethology. 2002;108:193-204. Available at: https://doi.org/10.1046/j.1439-0310.2002.00758.x. Accessed July 9, 2018.

David B. Pecor, BS

Desmond H. Foley, PhD

Alexander Potter

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

Dr Foley is a Research Entomologist at the Walter Reed Biosystematics Unit, Entomology Branch, Walter Reed Army Institute of Research, and a Research Associate of the Entomology Department within the National Museum of Natural History, located at the Smithsonian Institution, Museum Support Center, Suitland, Maryland.

Mr Potter is a student at Kalamazoo College, Michigan. He completed a Walter Reed Army Institute of Research College Qualified Leaders internship with the Walter Reed Biosystematics Unit in Summer 2017.

Caption: Figure 1. Specimen information Catalog Number: USNMENT01240053 Scientific Name: Aedes (Stg.) albopictus (Skuse, 1894) Sex/Lifestage: Female, Adult Preparation: Pin mounted Notes: Specimen is in good condition with diagnostic characters clearly visible. Some setae appear rubbed on scutum. Specimen has some dust/debris covering exterior. Glue affixing specimen to pin is stable.

Collection data

Locality: Nagasaki, Japan

Collection Date: 9 October 1945

Collector: Borror, D.J.

Verbatim Scientific Name: Ae. albopictus

Additional Information: #8

Caption: Figure 2.

Specimen Information

Catalog Number: USNMENT01240364

Sex/Lifestage: Whole larva

Notes: Specimen is in good condition with diagnostic characters clearly visible. Mounting medium appears to be Canada Balsam and has darkened slightly.

Collection Data

Locality: Iron kettle, bombed area, Nagasaki, Japan

Collector: Borror, D.J.

Additional Information: #18C

Scientific Name: Aedes (Stg.) albopictus (Skuse, 1894) Preparation: Slide mounted

Collection Date: 11 October 1945

Verbatim Scientific Name: Ae. albopictus

Caption: Figure 3.

Specimen information

Catalog Number: USNMENT01240280

Scientific Name: Culex (Ocu.) bitaeniorhynchus (Giles, 1901)

Sex/Lifestage: Male, Adult

Preparation: Pin mounted adult with slide mounted genitalia

Notes: Specimen is in fair condition with diagnostic characters clearly visible. Glue affixing specimen to pin is stable. Slide mounting medium appears to be Euparal and remains clear.

Collection data

Locality: Nagasaki, Japan

Collector: Borror, D.J.

Collection Date: 15 November 1945

Verbatim Scientific Name: Culex (Culex) bitaeniorhynchus

Identified by: S.S. 1973

Additional Information: SEAMP ACC No. PREP 69/1396; #1E
A summary of the mosquito specimens considered within this study.
Species names are presented along with the total number of specimens
associated with each taxon, each species vector status and the
collection site description used to inform species bionomics
profiles.

Species Name           Specimen    Vector            Collection Site
                         Count     Status            Description

Aedes (Hul.)              13       WNV               Fire tub,
japonicus                                            cemetery urn,
(Theobald, 1901)                                     rock hole

Aedes (Stg.)              127      DENV, CHIKV,      Bamboo stump,
albopictus                         ZIKV              bamboo vase,
(Skuse, 1894)                                        concrete tub,
                                                     creek, pan, iron
                                                     kettle bombed
                                                     area, cemetery
                                                     urn, wooden tub

Aedes (Tan.) togoi        149      JEV               Bamboo stump,
(Theobald, 1907)                                     bucket, cement
                                                     tank, ditch,
                                                     fire tub, rock
                                                     hole, tank in
                                                     bombed area,
                                                     wooden barrel

Anopheles (Ano.)          15                         Cement tank,
koreicus Yamada                                      seepage pool
and Watanabe, 1918

Anopheles (Ano.)          31       Brugia malayi     Ditch, grassy
sinensis s.l.                      and secondary     pool, nightsoil
                                   vector of         pool, pond, rice
                                   Plasmodium sp.    paddy

Armigeres (Arm.)          22       Wuchereria        Crack, nightsoil
subalbatus                         bancrofti         pool
(Coquillett, 1898)

Culex (Cui.)              21                         Cave pool, creek
pallidothorax                                        in bombed area
Theobald, 1905

Culex (Cux.)               6       Wuchereria        Concrete tank,
quinquefasciatus                   bancrofti         stone pool
Say, 1823

Culex (Cux.)              23       JEV               Cement tank,
tritaeniorhynchus                                    fire tub,
Giles, 1901                                          nightsoil pool,
                                                     pond, rice paddy

Culex (Cux.)               7                         No data
vagans Wiedemann,
1828

Culex (Cux.)               1       JEV               Artificial pond
vishnui Theobald,
1901

Culex (Eum) hayashi       14                         Air raid
Yamada, 1917                                         shelter, cement
                                                     tank, lily pond,
                                                     ground pool

Culex (Lop.)               9                         Cave pool
infantulus Edwards,
1922

Culex (Ocu.)               5                         No data
bitaeniorhynchus
Giles, 1901

Tripteroides (Trp.)        8                         Bamboo stump
bambusa (Yamada,
1917)

Uranotaenia (Ura.)         1                         No data
bimaculiala
(Leicester, 1908)

WNV indicates West Nile virus; DENV, Dengue virus; CHIKV, chikungunya
virus; ZIKV, Zika virus; JEV, Japanese encephalitis virus.
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Author:Pecor, David B.; Foley, Desmond H.; Potter, Alexander
Publication:U.S. Army Medical Department Journal
Article Type:Report
Geographic Code:9JAPA
Date:Jan 1, 2018
Words:2894
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