Geographical distribution of bat flies (Diptera: Nycteribiidae and Streblidae), including two new records, Nycteribia allotopa and N. formosana, collected from bats (Chiroptera: Rhinolophidae and Vespertilionidae) in the Republic of Korea

Authors

  • Heung Chul Kim,

    1. 5th Medical Detachment, 168th Multifunctional Medical Battalion, 65th Medical Brigade, Unit 15247, APO AP 96205-5247, U.S.A.
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  • Sang Hoon Han,

    1. Division of Vertebrates Research, National Institute of Biological Resources, Incheon, 404-170, Republic of Korea
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  • Carl W. Dick,

    1. Department of Biology, Western Kentucky University, 1906 College Heights Blvd. #11080, Bowling Green, KY 42101-1080, U.S.A, and Department of Zoology, Field Museum of Natural History, 1400 South Lake Shore Dr., Chicago, IL 60605-2827, U.S.A.
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  • Yong Gun Choi,

    1. Korean Institute of Biospeleology, Yeongwol Cave Eco-Museum, Yeongwol, Gangwon Province, 230–821, Republic of Korea
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  • Sung Tae Chong,

    1. 5th Medical Detachment, 168th Multifunctional Medical Battalion, 65th Medical Brigade, Unit 15247, APO AP 96205-5247, U.S.A.
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  • Terry A. Klein,

    1. Force Health Protection and Preventive Medicine, 65th Medical Brigade/US Army MEDDAC-Korea, Unit 15281, APO AP 96205-5281, U.S.A.
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  • Leopoldo M. Rueda

    1. Walter Reed Biosystematics Unit, Entomology Branch, Walter Reed Army Institute of Research, 503 Robert Grant Ave., Silver Spring, MD 20910-7500, U.S.A., ruedapol@si.edu
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ABSTRACT:

As part of the 65th Medical Brigade, U.S. Army, arthropod-borne disease surveillance program and in collaboration with the Korea National Institute of Biological Resources (NIBR), bats were captured from caves and abandoned mines in the Republic of Korea. A total of 39 adult bat flies including five species of Nycteribiidae [Penicillidia jenynsii, Nycteribia parvula, N. formosana, N. allotopa mikado, and an unidentified species of Nycteribia (N. cf. formosana)], and one species of Streblidae, Brachytarsina kanoi, were collected from bats belonging to two families, Rhinolophidae and Vespertilionidae. This is the first report of N. allotopa mikado and N. formosana from the Republic of Korea.

INTRODUCTION

Bat flies, belonging to the families Nycteribiidae and Streblidae, are obligate blood-feeding ectoparasites of bats. Both adult males and females feed on the blood of their host. The adults are morphologically specialized (often flattened and ctenoid) for living on the host's pelage and membranes, and have strongly specialized claws adapted for clinging to the bat host hair. The family Streblidae consists of 227 species and are similar to members of Hippoboscidae, except that they are exclusive ectoparasites of bats in climatic zones where winter temperatures are >10° C. Females are larviparous and usually attach mature larvae onto the walls of bat roosts, i.e., caves, under bridges, and man-made structures. The mature larvae immediately pupate, and the winged adults emerge and fly or crawl along the walls to nearby roosting bats. The family Nycteribiidae consists of 275 species which look more like spiders than flies. Similarly, they are exclusive ectoparasites of bats, are larviparous, and attach their larvae to the walls of caves or other structures where bats roost. While the majority of Streblidae species have wings for at least a portion of their adult life, members of Nycteribiidae are wingless and totally dependent on their hosts for transport, distribution, and blood source (Dick and Patterson 2006).

A comprehensive survey of bat ectoparasites in the Republic of Korea (ROK) has not been done, except previous collections which included only five species of Nycteribiidae and one species of Streblidae (Kishida 1932, Theodor 1967, Maa 1967, 1968, Kwon et al. 1994, Lee et al. 1998). This report summarizes the first records of Nycteribia allotopa mikado Maa and N. formosana (Karaman) collected from Miniopterus schreibersi Kuhr and Myotis mystacinus (Kuhr) (Chiroptera: Vespertilionidae) in the ROK, respectively.

MATERIALS AND METHODS

As part of the vector-borne disease surveillance program, the 65th Medical Brigade, U.S. Army, in collaboration with the Korea National Institute of Biological Resources (NIBR), conducted a survey of bats to determine their distributions and ectoparasite host relationships from 2007 – 2009. Bats were captured by sweep net in caves, abandoned mines, and under bridges at 30 collection sites in eight provinces and two metropolitan cities [Gangwon Province (Pyeongchang, Jeongseon, Samcheok, Hwacheon, Yeongwol), Chungcheongnam Province (Gongju), Chungcheongbuk Province (Goesan, Jaecheon, Chungju, Danyang, Okcheon), Gyeongsangbuk Province (Mungyeong, Yecheon, Sangju, Yeongju, Bonghwa, Yeongdeok), Gyeongsangnam Province (Changnyeong, Tongyeong, Changwon, Namhae), Jeollabuk Province (Namwon), Jeollanam Province (Shinan, Gurye, Haenam, Suncheon), Jeju (Province) (Jeju-si, Namjeju), and Daejeon and Gwangju metropolitan cities] (Figure 1). Ectoparasites were removed from the pelage of the bats and sent to the 5th Medical Detachment, 168th Multifunctional Medical Battalion, 65th Medical Brigade, Yongsan Army Garrison, Seoul, Korea, where they were identified under a dissecting microscope using standard keys (Maa 1962, 1967, 1968). Bat flies were sent to the Department of Biology, Western Kentucky University (WKU), Bowling Green, KY, where the identifications were confirmed by Dr. Carl W. Dick. Voucher specimens (six adult bat flies) were deposited at the Field Museum of Natural History, Chicago, while the remaining identified specimens were retained for the detection of zoonotic pathogens.

Figure 1.

Geographical distribution of bat flies (Diptera: Nycteribiidae and Streblidae) collected from bats (Chiroptera: Rhinolophidae and Vespertilionidae) at 30 collection sites in eight provinces and two metropolitan cities in the ROK, 2007–2009. A. Seoul Metropolitan, B. Gyeonggi Province, C. Gangwon Province, D. Chungcheongnam Province, E. Chungcheongbuk Province, F. Daejeon Metropolitan, G. Jeollabuk Province, H. Gwangju Metropolitan, I. Jeollanam Province, J. Gyeongsangbuk Province, K. Daegu Metropolitan, L. Gyeongsangnam Province, M. Ulsan Metropolitan, N. Busan Metropolitan, O. Jeju Province.

RESULTS

A total of 142 bats belonging to ten species was captured. Rhinolophus ferrumequinum (Schreber) (Rhinolophidae) (32.4%) was the most frequently captured bat, followed by M. schreibersi (21.1%), Myotis petax Hollister (9.9%), M. macrodactylus (Temminck) (8.5%), Eptesicus serotinus (Schreber) (8.5%), Pipistrellus abramus (Temminck) (7.0%), Hypsugo alaschanicus (Bobrinskii) (6.3%), M. mystacinus (3.5%), Murina leucogaster (Milne-Edwards) (2.1%), and M. formosus (Hodgson) (Vespertilionidae) (0.7%) (Table 1). A total of 39 adult bat flies (22 females and 17 males) from five species of Nycteribiidae [Penicillidia jenynsii (Westwood), N. parvula Speiser, N. formosana, N. allotopa mikado, and an unidentified species of Nycteribia (=N. cf. formosana)], and one species of Streblidae (Brachytarsina kanoi Maa) were collected from the pelage of 19 out of 142 bats (infestation rate, 13.4%) at Jeju-do, Gangwon, Chungcheongnam, Chungcheongbuk, Jeollanam, Jeollabuk, Gyeongsangnam, and Gyeongsangbuk Provinces, from 2007–2009 (Figure 1). Miniopterus schreibersi (n = 9) accounted for 47.4% of the 19 bats infested with bat flies, followed by R. ferrumequinum (21.1%), M. macrodactylus (15.8%), and M. mystacinus (15.8%). The most commonly collected bat fly was N. allotopa mikado, which was only collected from M. schreibersi, and is the first record of its occurrence in the ROK. A total of 12 bat flies (seven females and five males) were collected from five M. schreibersi at three different sites: an abandoned mine at Mungyeong, Gyeongsangbuk Province, under bridges at Jeju-si, Jeju Province, and an abandoned mine at Daejeon, Daejeon Metropolitan Area (Table 1). This is also the first record of N. formosana in the ROK, with a total of five bat flies (three females and two males) collected from three M. mystacinus captured during different years under a bridge at Yeongwol, Gangwon Province (Figure 1).

Table 1.  Species and numbers of bat flies (Diptera: Nycteribiidae and Streblidae) collected from bats (Chiroptera: Rhinolophidae and Vespertilionidae) and number (%) of infested bats in the Republic of Korea.
Bat Host SpeciesTotal Number of Bats (%)No. (%) InfestedNycteribiidaeStreblidaeTotal (%)
Penicillida jenynsii (Westwood, 1834) Nycteribia allotopa mikado Maa, 1967 Nycteribia formosana Karaman, 1939 Nycteribia cf. formosana Nycteribia parvula Speiser, 1901 Brachytarsina kanoi Maa, 1967
Rhinolophidae          
Rhinolophus ferrumequinum (Schreber, 1774)46 (32.4)4 (8.7)00001M, 1F3M, 3F8 (20.5)
Vespertilionidae          
Eptesicus serotinus (Schreber, 1774)12 (8.5)0000000 
Pipistrellus abramus (Temminck, 1838)10 (7.0)0000000 
Hypsugo alaschanicus (Bobrinskii, 1926)9 (6.3)0000000 
Myotis petax Hollister, 191214 (9.9)0000000 
Myotis formosus (Hodgson, 1835)1 (0.7)0000000 
Myotis mystacinus (Kuhr, 1817)5 (3.5)3 (60.0)002M, 3F0005 (12.8)
Myotis macrodactylus (Temminck, 1840)12 (8.5)3 (25.0)0003M, 5F008 (20.5)
Miniopterus schreibersi (Kuhr, 1817)30 (21.1)9 (30.0)2F7M, 5F001M, 3F018 (46.1)
Murina leucogaster (Milne-Edwards, 1872)3 (2.1)0000000 
Total142 (100.0)19 (13.4)2F7M, 5F2M, 3F3M, 5F2M, 4F3M, 3F39 (100.0)

During this survey only five species of Nycteribiidae (i.e., two new species records and one species near N. formosana), and one species of Streblidae were collected. Three previously reported species of Nycteribiidae [i.e., N. pleuralis Maa, N. pygmaea (Kishida), and N. uenoi] were not collected in this survey. Table 2 shows an updated checklist of nine species of bat flies belonging to three genera, Penicillidia, Nycteribia and Brachytarsina from the ROK, including their associated hosts and collection records.

Table 2.  Checklist of bat flies (Diptera: Nycteribiidae and Streblidae) and associated bat hosts (Chiroptera: Rhinolophidae, and Vespertilionidae) in the Republic of Korea.
Bat Fly Speciesn**Bat Host SpeciesDateLocationGrid CoordinatesReferences
  1. * New record of bat flies in Korea. ** F = Females, M = Males, NR = no host, date or locality record, ***X = In this survey (2007–2009).

Nycteribiidae       
Penicillida jenynsii NRNRNRDistribution recordNR Kishida (1932)
 1F Miniopterus schreibersi 18-Mar-08Hogye-dong, Mungyeong-si, Gyeongbuk Prov.36˚39′32.8″N, 128˚11′34.1″EX***
 1F Miniopterus schreibersi 31-Mar-09Hogye-dong, Mungyeong-si, Gyeongbuk Prov.36˚39′32.8″N, 128˚11′34.1″EX
Nycteribia allotopa mikado*3M, 3F Miniopterus schreibersi 21-Sep-07Bonggae-dong, Jeju-si, Jeju-do (Is)33˚24′39.4″N, 126˚37′15.4″EX
 2M Miniopterus schreibersi 29-Mar-08Haso-dong, Dong-gu, Daejeon Metropolitan36°12′47.1″N, 127°26′20.1″EX
 2M, 2F Miniopterus schreibersi 21-Mar-09Hogye-dong, Mungyeong-si, Gyeongbuk Prov.36˚39′32.8″N, 128˚11′34.1″EX
Nycteribia formosana*1M Myotis mystacinus 5-May-08Hadong-myeon, Yeongwol-gun, Gangwon Prov.37˚07′08.6″N, 128˚36′35.4″EX
 1M, 3F Myotis mystacinus 10-May-09Hadong-myeon, Yeongwol-gun, Gangwon Prov.37˚07′08.1″N, 128˚36′34.9″EX
Nycteribia cf. formosana*1M, 2F Myotis macrodactylus 22-Apr-07Jucheon-myeon, Yeongwol-gun, Gangwon Prov.37°08′59.1″N, 126°27′44.2″EX
 1M, 3F Myotis macrodactylus 3-Oct-07Buk-myeon, Yeongwol-gun, Gangwon Prov.37°15′03.7″N, 128°25′46.1″EX
 1M Myotis macrodactylus 27-Jan-08Imgok-dong, Gwangsan-gu, Jeonnam Prov.35°13′10.4″N, 126°44′41.0″EX
Nycteribia parvula NR Miniopterus sp.NRNRNR Kishida (1932)
 1F Rhinolophus ferrumequinum 10-Sep-07Gyeryong-myeon, Gongju-si, Chungnam Prov.36°24′44.1″N, 127°08′44.3″EX
 1M Rhinolophus ferrumequinum 8-Dec-07Buk-myeon, Changwon-si, Gyeongnam Prov.35°21′29.1″N, 128°35′03.2″EX
 1F Miniopterus schreibersi 21-Sep-07Bonggae-dong, Jeju-si, Jeju Prov.33°24′39.4″N, 126°37′15.4″EX
 1M Miniopterus schreibersi 29-Mar-08Haso-dong, Dong-gu, Daejeon Metropolitan36°12′47.1″N, 127°26′20.1″EX
 2F Miniopterus schreibersi 21-Mar-09Hogye-dong, Mungyeong-si, Gyeongbuk Prov.36˚39′32.8″N, 128˚11′34.1″EX
Nycteribia pleuralis 2F Myotis nattereri amurensis 12-Aug-65Keumnyeong-ri, Hanlim-eup, Quelpart (=Jeju) Is33°22′27.5″N, 126°13′50.1″E Maa (1968)
       
Nycteribia pygmaea 2M, 2F Pipistrellus savii velox (?)15-Jun-55Daegu MetropolitanNR Theodor (1967)
  (=Myotis or Miniopterus)    
Nycteribia uenoi 2M, 2F Pipistrellus (?)(=Myotis or Miniopterus)11-Aug-63Cheongpyung-myeon, Jaecheon-gun, Chungbuk Prov.37°01′14.8″N, 128°10′03.7″E Maa (1968)
 2 Rhinolophus ferrumequinum 1991–1998Jeju Prov.NR Lee et al. (1998)
Streblidae       
Brachytarsina kanoi 1F Rhinolophus ferrumequinum korai 13-Jan-66Dogye-eup, Samcheok-gun, Gangwon Prov.37°19′10.8″N, 129°00′27.5″E Maa (1968)
 2M, 5F Rhinolophus ferrumequinum korai 14-Apr-66Seo-myeon, Yeongwol-gun, Gangwon Prov.37°13′58.2″N, 128°21′25.4″E Maa (1968)
 5M Rhinolophus ferrumequinum quelpartis 2-Feb-66Keumnyeong-ri, Hanlim-eup, Quelpart (=Jeju) Is33°31′30.0″N, 126°46′20.5″E Maa (1968)
 2 Rhinolophus ferrumequinum 1991–1998Jeju-do (Is)NR Lee et al. (1998)
 2M Rhinolophus ferrumequinum 15-Oct-07Hong-do, Shinan-gun, Jeonnam Prov.34°41′00.3″N, 125°11′29.9″EX
 1F Rhinolophus ferrumequinum 8-Dec-07Buk-myeon, Changwon-si, Gyeongnam Prov.35°21′29.1″N, 128°35′03.2″EX
 1M, 2F Rhinolophus ferrumequinum 18-Mar-08Jeongseon-gun, Gangwon Prov.37°22′50.1″N, 128°37′30.3″EX

DISCUSSION

Bats are host to a number of ectoparasites, including mites, ticks, fleas, bat bugs, and bat flies. This is the first record of the bat flies in the ROK, namely N. allotopa mikado and N. formosana, collected from M. schreibersi and M. mystacinus, respectively. Nycteribia allotopa allotopa Speiser was first described from one female and one male collected from Miniopterus sp. in West Sumatra and later from India, Ceylon, Taiwan, and Philippines in 1901. Nycteribia allotopa meridiana Maa collected from the bats, Miniopterus sp. and Vespadelus pumilus Gray in Australia (Maa 1971), and N. allotopa mikado collected from M. schreibersi at Honshu and Ryukyu Islands of Japan, were designated as new subspecies by Maa (1967). These species differ from the type species collected from Sumatra by being slightly smaller in size, having a much broader female post genital plate, and more slender and gently curved aedeagus (Maa 1967). Nycteribia formosana was first described from one female and one male collected from a bat in Taiwan, and was commonly collected from Miniopterus, Rhinolophus, and Myotis in Taiwan and China (Maa 1962). Nycteribia formosana and N. uenoi Maa are difficult to separate morphologically. Dr. Motoyoshi Mogi (Saga Medical School, Japan; personal communication) noted that he previously identified as N. uenoi, the specimens collected from Tsushima Island between Korea and Japan. Using Maa's (1962, 1967, 1968) keys, they did not key out to N. formosana. He commented that there might be problems with Maa's morphological description of N. formasana since it was based on a few specimens from limited localities. He further suggested that morphological similarities between N. uenoi and N. formosana need to be studied, by examining specimens from various localities. It is rather unlikely that they coexist in the Korean peninsula. Nycteribia allotopa mikado and N. formosana have not been reported from the ROK, and their role in the maintenance, transmission, and distribution of zoonotic pathogens is unknown. Korean specimens of Nycteribia sp. (N. cf. formosana) are still being examined to determine their taxonomic status. Recent dramatic changes in the ecologic landscape of the ROK, including road construction, reforestation, and the proliferation of outdoor recreational activities associated with the country's rapid economic development, have increased the likelihood that humans and their domestic animals come into closer contact with bats, their ectoparasites, and associated pathogens. Further studies on the geographical and seasonal distributions of bat flies and their associated hosts are needed to better understand their biology and ecology and to determine their role as potential vectors of zoonotic pathogens.

Acknowledgments

We thank the Dr. Yeon-Soon Ahn, Chief, National Institute of Biological Resources (NIBR), for support in collecting bat ectoparasites. We also thank Dr. Motoyoshi Mogi, Department of Microbiology, Saga Medical School, Japan, and Dr. Joel Gaydos, Armed Forces Health Surveillance Center (AFHSC), Silver Spring, MD, for their support in conducting this work. Part of this work was funded by the AFHSC-Global Emerging Infections Surveillance and Response Systems, Silver Spring, MD, and the National Center for Military Intelligence, Fort Detrick, MD. The views expressed in this article are those of the authors and do not reflect the official policy or position of the Department of Defense, the Department of the Army, or the U.S. Government.

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