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Seasonal surveillance of deer and horse flies (Diptera: Tabanidae), Gyeonggi province, Republic of Korea
Journal of Asia-Pacific Entomology 23 (2020) 315–319
Contents lists available at ScienceDirect
Journal of Asia-Pacific Entomology journal homepage: www.elsevier.com/locate/jape
Short communication
Seasonal surveillance of deer and horse flies (Diptera: Tabanidae), Gyeonggi province, Republic of Korea
T
Kwang Shik Choia,1, Heung Chul Kimb,1, Sung Tae Chongb, Myung Soon Kimb, Terry A. Kleinb, ⁎ Hyo-Sung Kimc,2, Sang Jae Suhd, a
School of Life Sciences, Kyungpook National University, Daegu 41566, Republic of Korea Force Health Protection and Preventive Medicine, Medical Department Activity-Korea/65th Medical Brigade, Unit 15281, APO, AP 96271-5281, USA c 5th Medical Detachment, 168th Multifunctional Medical Battalion, 65th Medical Brigade, Unit 15247, APO, AP 96205-5247, USA d School of Applied Biosciences, Kyungpook National University, Daegu 41566, Republic of Korea b
A R T I C LE I N FO
A B S T R A C T
Keywords: Tabanidae Deer fly Horse fly Seasonal surveillance Korea
Deer and horse flies, Family Tabanidae, are biological, mechanical, and potential vectors of approximately 27 viral, bacterial, and helminthic pathogens of veterinary and medical importance. Biting fly surveillance was conducted using New Jersey light traps and Mosquito Magnet® traps from May-October during 2015–2018 at eight sites (villages and US military installations and training areas) near/in the Demilitarized Zone and at a US military installation in southern Gyeonggi province, Republic of Korea. A total of 9985 deer and horse flies, comprising 4 genera and 17 species, were collected. The predominant species collected was Chrysops mlokosiewiczi (95.39%), followed by Chrysops suavis (1.48%) and Haematopota koryoensis (1.07%), while the remaining species accounted for only 2.06% of the specimens collected. A bimodal peak was observed for C. mlokosiewiczi in June and late-July, but not for the other two predominant species during the whole of the study period. This study provides and insight into ecological behavior and seasonal abundance of deer and horse flies in Gyeonggi province, Republic of Korea.
Introduction Deer and horse flies (tabanids) are biological and, mechanical vectors of bacterial, or helminthic pathogens of veterinary and medical importance, e.g., anthrax, loiasis, tularemia, and potential vectors of pathogens, e.g., Anaplasma spp., Brucella spp., and viruses causing equine infectious anaemia, pyroplasmidoses, swine fever, and trypanozomiases (Foil, 1989; Krinsky, 1976; Polyakov et al., 1990). Transmission of these pathogens impact the livestock industry, in addition to blood feeding that affects loss of body weight and milk production of cattle and secondary infections at the bite site (Krinsky, 1976). Except for a few species, the behavioral and habitat information for many of the members of the Family Tabanidae are not well known due to their wide range and that most of adult flies only survive a single season in the geographical area under consideration. Adult tabanids generally appear in June, with numbers collected through August in temperate climates. However, some species appear during late spring/ early summer season, while others appear in larger numbers during the
latter part of the summer/early fall season in temperate zones (Mundoch and Takahasi, 1969). Seasonal surveillance of tabanids in Gyeonggi province, Republic of Korea (ROK) during June-August (Suh et al., 2005) and April-October (Suh et al., 2015) showed that few specimens were collected during April and September-October. While the horse flies, Tabanus chrysurus and Tabanus mandarinus, from Jeju Island, ROK, were first recorded by Okamoto (1924), they have not been investigated as biological and mechanical vectors of pathogens of medical or veterinary importance. In this study, we investigated the seasonal abundance of adult tabanids at US military installation/training sites and nearby villages in/near the demilitarized zone (DMZ) and Camp Humphreys in northern and southern Gyeonggi province, respectively, in the ROK.
⁎
Corresponding author at: School of Applied Biosciences, Kyungpook National University, Daegu 41566, Republic of Korea. E-mail address: [email protected] (S.J. Suh). 1 These authors contributed equally to this work. 2 Current address: School of Medicine, Kangwon National University, Chuncheon 24341, Republic of Korea. https://doi.org/10.1016/j.aspen.2020.02.005 Received 1 October 2019; Received in revised form 31 January 2020; Accepted 14 February 2020 Available online 14 February 2020 1226-8615/ © 2020 Published by Elsevier B.V. on behalf of Korean Society of Applied Entomology.
Journal of Asia-Pacific Entomology 23 (2020) 315–319
K.S. Choi, et al.
Fig. 1. Map of the northern and southern part of Gyeonggi province denoting collection sites of horse and deer flies at (A) Neutral Nations Supervisory Commission (NNSC) camp adjacent to the Panmunjom, (B) Daeseongdong village of approximately 200 residents inside the Demilitarized zone (DMZ), (C) South Gate (Southernboundary of the 2km wide DMZ), (D) Camp Bonifas (US Army Installation), (E) Warrior Base (US Army training site approximately 3 km from the DMZ, (F) Tongilchon (village of approximately 200 residents; trap set at a beef farm with approximately 50 cattle and 3 km from the DMZ, (G) Dagmar North training site (DNTA) and (H) Camp Humphreys.
Materials and methods
Table 1 Annual numbers of deer and horse flies collected in Gyeonggi province in the ROK from 2015 to 2018.
Collection sites and sample information
Species
Tabanids (deer and horse flies) were collected concurrently with other biting flies (mosquitoes and biting gnats) at three sites in the DMZ [Neutral Nations Supervisory Commission camp (NNSC) (37°57′16.39′’N, 126°40′50.03′’E), Daeseongdong village (37°56′26.92′’N, 126°40′37.42′’E), and South Gate (gate to the southern boundary of the DMZ) (37°56′03.53″N; 126°43′15.46″E)], and four sites near the DMZ [Camp Bonifas (37°56′0.87′’N, 126°43′17.02′’E), Warrior Base training area (37°55′17.01′’N, 126°44′30.22′’E), Tongilchon village (37°54′32.18′’N, 126°44′01.88′’E), and Dagmar North training area (37°58′29.85″N; 126°50′40.88″E)] in northern Gyeonggi province and at Camp Humphreys (36°57′14.46″N; 127° 1′33.21″E) in southern Gyeonggi province in the ROK using New Jersey light traps and Mosquito Magnet® traps from May-October 2015–2018 (Fig. 1). The tabanids were separated from other biting flies following each collection, and placed dry in 2 ml cryovials and maintained at −80 °C until transported to Kyungpook National University, Daegu in the ROK where they were identified morphologically using a stereoscopic microscope and taxonomic keys of Mundoch and Takahasi (1969) and Suh et al. (2002a,b; 2003).
Year
Total
%
2015
2016
2017
2018
Chrysopsinae (deer flies) Atylotus horvathi Atylotus miser Chrysops dissectus Chrysops japonicus Chrysops mlokosiewiczi Chrysops suavis
8 5 0 0 468 11
0 0 1 0 199 5
12 31 0 1 4075 62
0 2 0 5 4782 70
20 38 1 6 9524 148
0.2 0.38 0.01 0.06 95.39 1.48
Tabaninae (horse flies) Haematopota antennata Haematopota koryoensis Haematopota sinensis Haematopota tamerlani Tabanus aurotestaceus Tabanus griseinus Tabanus loukashkini Tabanus mandarinus Tabanus sapporoensis Tabanus taiwanus Tabanus trigeminus
0 12 1 0 0 0 1 0 0 2 2
0 29 0 0 0 0 0 0 0 0 0
4 66 54 5 1 1 0 0 1 0 0
55 0 11 2 0 0 0 1 0 0 0
59 107 66 7 1 1 1 1 1 2 2
0.59 1.07 0.66 0.07 0.01 0.01 0.01 0.01 0.01 0.02 0.02
Total
510
234
4313
4928
9985
100
Results and discussion population abundance. The highest numbers of tabanids were collected from June-August (Table 2). Similar to results of Suh et al. (2015), C. mlokosiewiczi was collected from late-May-mid-September, with bimodal peaks observed during June (72.26%) and late July (12.26%) (Fig. 2). Bimodal peaks were observed for C. suavis during mid-late June (75.81%) and midSeptember (19.36%) in 2017, while the numbers of specimens collected during 2015–2016 and 2018 were not peaked bimodally (Fig. 3). A unimodal peak was observed for H. koryoensis in mid-July (50.47%) during the study period (Fig. 4). Recent study similarly reported that C. suavis demonstrated bimodal peaks in mid-June and early-September during 2010–2013, while peak populations of H. koryoensis were only observed during late-July (Suh et al., 2015). Although insufficient numbers of Chrysops japonicus and Haematopota antennata were collected for analysis, specimens were collected only during mid-May and late-June-July respectively. Haematopota sinensis demonstrated a
A total of 9985 deer and horse flies belonging to 2 subfamilies, 4 genera and 17 species were collected at US military installations and training areas and associated villages, Gyeonggi province, ROK from 2015 to 2018 (Table 1). Previous surveillance of tabanids from 2003 to 2004 (Suh et al., 2005) reported the presence of only 14 species, while surveillance from 2010 to 2013 reported 20 species (Suh et al., 2015) at sites near/in the DMZ. Similar to the other studies Chrysops mlokosiewiczi was the predominant species, and in collections from 2015 to 2018, it was the most commonly collected species (95.39%), followed by Chrysops suavis (1.48%) and Haematopota koryoensis (1.07%), while the other 14 species accounted for only 2.06% of all species collected. A total of 49.35% of all deer and horse flies were collected during 2018, followed by 2017 (43.2%), 2015 (5.11%), and 2016 (2.34%). No correlations between climate (temperature and precipitation) and the number of collected specimens during each of the years were observed. Further studies are needed to determine factors that affect relative 316
Journal of Asia-Pacific Entomology 23 (2020) 315–319
K.S. Choi, et al.
Table 2 Seasonal prevalence of tabanid flies collected in Gyeonggi province in the ROK from 2015 to 2018 Month
MAY
JUN
JUL
AUG
SEP
Oct
Total
Species
E
M
L
E
M
L
E
M
L
E
M
L
E
M
L
E
M
L
Atylotus horvathi Atylotus miser Chrysops dissectus Chrysops japonicus Chrysops mlokosiewiczi Chrysops suavis Haematopota antennata Haematopota koryoensis Haematopota sinensis Haematopota tamerlani Tabanus aurotestaceus Tabanus griseinus Tabanus loukashkini Tabanus mandarinus Tabanus sapporoensis Tabanus taiwanus Tabanus trigeminus
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 6 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 18 10 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 1641 20 0 0 0 1 0 0 0 0 0 0 0
0 1 0 0 2824 63 0 0 8 2 0 0 0 0 0 0 0
4 4 0 0 2417 25 2 0 19 0 0 1 0 0 1 0 0
4 2 0 0 801 0 18 3 21 4 0 0 0 0 0 0 0
0 4 0 0 312 1 15 54 8 0 0 0 0 0 0 2 0
2 6 0 0 1168 0 24 43 4 0 0 0 0 1 0 0 2
3 4 0 0 197 0 0 6 3 0 0 0 0 0 0 0 0
3 5 0 0 120 2 0 1 3 0 1 0 0 0 0 0 0
0 5 1 0 20 3 0 0 0 0 0 0 0 0 0 0 0
4 2 0 0 5 4 0 0 0 0 0 0 1 0 0 0 0
0 5 0 0 1 17 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
20 38 1 6 9524 148 59 107 66 7 1 1 1 1 1 2 2
Total
0
6
28
1662
2898
2473
853
396
1250
213
135
29
16
23
3
0
0
0
9985
Fig. 2. Annual distributions of the predominant species, Chrysops mlokosiewiczi in Gyeonggi province, ROK from 2015 to 2018. Early and mid-summer bimodal peaks were observed. Data in October were not included due to no collected specimens.
Fig. 4. Annual distributions of the third most commonly collected species, Haematopota koryoensis, in Gyeonggi province, ROK from 2015 to 2018. Only a mid-season unimodal peak was observed. Data in October were not included due to no collected specimens.
Fig. 3. Annual distributions of the second most frequently collected species, Chrysops suavis in Gyeonggi province, ROK from 2015 to 2018. A bimodal peak was observed only for 2017. Data in October were not included due to no collected specimens.
317
Journal of Asia-Pacific Entomology 23 (2020) 315–319
K.S. Choi, et al.
Table 3 Seasonal abundance of adult tabanids collected at eight sites in Gyeonggi province in the ROK from 2015 to 2018 Month
MAY
JUN
JUL
AUG
SEP
Oct
Total
Locality
E
M
L
E
M
L
E
M
L
E
M
L
E
M
L
E
M
L
Camp Bonifas Daeseongdong Dagmar North TA NNSC Camp South Gate Tongilchon Warrior Base Camp Humphreys
0 0 0 0 0 0 0 0
0 0 2 3 1 0 0 0
4 0 6 9 8 0 1 0
38 143 817 481 117 0 63 3
92 42 1659 869 111 0 116 9
103 30 978 1114 154 0 89 5
103 13 167 487 43 0 38 2
31 44 48 126 63 20 58 6
159 32 130 756 25 0 133 15
29 5 19 137 3 0 0 20
6 3 20 101 2 0 1 2
0 0 9 14 2 0 1 3
5 0 3 6 2 0 0 0
0 0 16 5 1 0 1 0
0 0 0 3 0 0 0 0
0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0
570 312 3874 4111 532 20 501 65
Total
0
6
28
1662
2898
2473
853
396
1250
213
135
29
16
23
3
0
0
0
9985
Table 4 A total number of deer and horse flies collected at seven sites in/near the DMZ in northern Gyeonggi province and at Camp Humphreys in southern Gyeonggi province, ROK, from 2015 to 2018 Locality Species
Camp Bonifas
Daeseongdong Village
Dagmar North TA
NNSC Camp
South Gate
Tongilchon Village
Warrior Base TA
Camp Humphreys
Total
Atylotus horvathi Atylotus miser Chrysops dissectus Chrysops japonicus Chrysops mlokosiewiczi Chrysops suavis Haematopota antennata Haematopota koryoensis Haematopota sinensis Haematopota tamerlani Tabanus aurotestaceus Tabanus griseinus Tabanus loukashkini Tabanus mandarinus Tabanus sapporoensis Tabanus taiwanus Tabanus trigeminus
4 2 0 0 559 0 0 2 2 0 0 0 1 0 0 0 0
0 0 0 0 307 1 0 1 2 1 0 0 0 0 0 0 0
10 27 1 2 3664 108 6 1 49 4 1 0 0 1 0 0 0
6 6 0 3 3981 13 36 55 3 2 0 1 0 0 1 2 2
0 3 0 1 452 21 7 44 4 0 0 0 0 0 0 0 0
0 0 0 0 20 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 487 5 5 1 3 0 0 0 0 0 0 0 0
0 0 0 0 54 0 5 3 3 0 0 0 0 0 0 0 0
20 38 1 6 9524 148 59 107 66 7 1 1 1 1 1 2 2
Total
570
312
3874
4111
532
20
501
65
9985
North training area (72.97%). Haematopota koryoensis (1.07%) was the third most commonly collected species, with the NNSC camp accounting and the South Gate entrance area accounting for 51.4% and 41.2%, respectively, of all specimens collected. The NNSC camp is located near a low lying area that often floods and an intermittent stream bordered by a forest that might provide adequate diversity of tabanids collected (Hyun and Shin, 1975; Kim et al., 1973). This study provides basic information for the relative species abundance of tabanids that are biological, mechanical, and potential vectors of viruses, bacteria, and helminths that pose a threat to local and military populations, wildlife, and domestic animals and birds. Further studies are needed to determine the seasonal and annual distribution of this and other species to determine factors related to ecological behavior of tabanids for the development of mitigation strategies for their control.
unimodal peak in late-June-early July (60.61%) similar to results of Suh et al. (2005) (75.31%), while an apparent peak populations were not observed during 2010–2013 (Suh et al., 2015). The remaining species were generally collected throughout June-August. Although the numbers and species of horse and deer flies collected during this study differed from previous surveillance (Suh et al., 2005, 2015), all studies showed that the peak occurrence of tabanids was from June-August. Surveillance of adult tabanids in the southern part of Korea demonstrated that most species populations peaked between the end of June and early July (Hyun and Shin, 1975; Kim et al., 1973). Previous surveillance data indicated that low winter temperatures and precipitation affect adult population more than high temperatures during the adult stage. However, this study reported that the results between the mean numbers of tabanids collected based on annual temperatures and precipitation variations were not significantly different (Suh et al., 2015). A total of 17 species of tabanids were distributed at eight sites in this study area from 2015 to 2018 (Tables 3 and 4). The highest numbers of tabanids were collected at NNSC (41.17%) and Dagmar North (38.8%). Chrysops mlokosiewiczi was the most frequently collected species at all collection sites (95.39%). NNSC (41.8%) accounted for the highest proportion of C. mlokosiewiczi collected, followed by Dagmar North training area (38.47%), while the remaining collection sites accounted for 19.73% of all specimens collected. Chrysops mlokosiewiczi (0.2%) were collected only during mid-July at a beef farm in Tongilchon. Surveillance at the site was only performed during 2015. At Dagmar North TA, the highest numbers of tabanids were collected during June (89.16%). Chrysops suavis (1.48%) was the second most frequently collected tabanid, with the highest proportion collected at Dagmar
Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments We thank COL Derek C. Cooper, Commander, 65th Medical Brigade and COL Jon Allison, Chief, Force Health Protection and Preventive Medicine, 65th Medical Brigade for their support of vector-borne disease surveillance at US military installations/training sites and 318
Journal of Asia-Pacific Entomology 23 (2020) 315–319
K.S. Choi, et al.
associated villages in the Republic of Korea. Funding for this work was provided by the Armed Forces Health Surveillance Branch, Global Emerging Infections Surveillance and Response System, Silver Spring, MD (ProMIS ID # P0025-2016-2018-ME). The opinions or assertions contained herein are the private views of the authors, and are not to be construed as official, or as reflecting the views of the Department of the Army or the Department of Defense. This research was also supported by Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education, Republic of Korea (grant No. 2017R1D1A2B03029971).
Korea. Bull. Korean Entomol. Inst. Korea Univ. 5, 55–62 (in Korean). Krinsky, W.L., 1976. Animal disease agents transmitted by horse flies and deer flies (Diptera: Tabanidae). J. Med. Entomol. 13, 225–275. Mundoch, W.P., Takahasi, H., 1969. The female Tabanidae of Japan, Korea and Manchuria. Mem. Ent. Soc. Washington 6 pp. 4, 110–118. Okamoto, H., 1924. The insect fauna of Quelpart Island. Bull. Agri. Expt. Stn. Govt. Gen. Chosen. 1, 157–158. Polyakov, V.A., Anisimovich, V., Uzakov, U., Veselkin, G., 1990. Tabanidae. In: Veterinary Entomology and Arachnology. Agropromizdat, Moscow, pp. 14–19. Suh, S.J., Choi, K.S., Kwon, Y.J., 2002a. Taxonomic revision of Tabanus mandarinus species group (Diptera: Tabanidae) from Korea. Entomol. Res. 32, 113–118. Suh, S.J., Choi, K.S., Kwon, Y.J., 2002b. Taxonomy of Tabanus immanis species group (Diptera: Tabanidae) in Korea. Insect Koreana 19, 277–282. Suh, S.J., Choi, K.S., Kwon, Y.J., 2003. Taxonomy of Tabanus cordiger species group (Diptera: Tabanidae) in Korea. Entomol. Res. 33, 1–3. Suh, S.J., Kim, H.C., Chong, S.T., Kim, M.S., Klein, T.A., 2015. Seasonal abundance of deer and horse flies (Diptera: Tabanidae) in the northern part of Gyeonggi-do, Republic of Korea. Korean J. Parasitol. 53, 307–314. Suh, S.J., Kim, H.C., Klein, T.A., Chong, S.T., Lee, W.J., Kwon, Y.J., 2005. Tabanid flies (Diptera: Tabanidae) of the northern part of Gyeonggi province, Republic of Korea. Entomol. Res. 35, 195–198.
References Foil, L.D., 1989. Tabanids as vectors of disease agents. Parasitol. Today 5, 88–96. Hyun, J.S., Shin, T.H., 1975. Seasonal abundance of tabanid flies in Jeong-up based on the numbers captured in traps. Korean J. Entomol. 5, 17–21 (in Korean). Kim, C.W., Kim, J.I., Shin, T.H., 1973. On the Tabanidae from Cheunra-Bukdo province in
319
Contents lists available at ScienceDirect
Journal of Asia-Pacific Entomology journal homepage: www.elsevier.com/locate/jape
Short communication
Seasonal surveillance of deer and horse flies (Diptera: Tabanidae), Gyeonggi province, Republic of Korea
T
Kwang Shik Choia,1, Heung Chul Kimb,1, Sung Tae Chongb, Myung Soon Kimb, Terry A. Kleinb, ⁎ Hyo-Sung Kimc,2, Sang Jae Suhd, a
School of Life Sciences, Kyungpook National University, Daegu 41566, Republic of Korea Force Health Protection and Preventive Medicine, Medical Department Activity-Korea/65th Medical Brigade, Unit 15281, APO, AP 96271-5281, USA c 5th Medical Detachment, 168th Multifunctional Medical Battalion, 65th Medical Brigade, Unit 15247, APO, AP 96205-5247, USA d School of Applied Biosciences, Kyungpook National University, Daegu 41566, Republic of Korea b
A R T I C LE I N FO
A B S T R A C T
Keywords: Tabanidae Deer fly Horse fly Seasonal surveillance Korea
Deer and horse flies, Family Tabanidae, are biological, mechanical, and potential vectors of approximately 27 viral, bacterial, and helminthic pathogens of veterinary and medical importance. Biting fly surveillance was conducted using New Jersey light traps and Mosquito Magnet® traps from May-October during 2015–2018 at eight sites (villages and US military installations and training areas) near/in the Demilitarized Zone and at a US military installation in southern Gyeonggi province, Republic of Korea. A total of 9985 deer and horse flies, comprising 4 genera and 17 species, were collected. The predominant species collected was Chrysops mlokosiewiczi (95.39%), followed by Chrysops suavis (1.48%) and Haematopota koryoensis (1.07%), while the remaining species accounted for only 2.06% of the specimens collected. A bimodal peak was observed for C. mlokosiewiczi in June and late-July, but not for the other two predominant species during the whole of the study period. This study provides and insight into ecological behavior and seasonal abundance of deer and horse flies in Gyeonggi province, Republic of Korea.
Introduction Deer and horse flies (tabanids) are biological and, mechanical vectors of bacterial, or helminthic pathogens of veterinary and medical importance, e.g., anthrax, loiasis, tularemia, and potential vectors of pathogens, e.g., Anaplasma spp., Brucella spp., and viruses causing equine infectious anaemia, pyroplasmidoses, swine fever, and trypanozomiases (Foil, 1989; Krinsky, 1976; Polyakov et al., 1990). Transmission of these pathogens impact the livestock industry, in addition to blood feeding that affects loss of body weight and milk production of cattle and secondary infections at the bite site (Krinsky, 1976). Except for a few species, the behavioral and habitat information for many of the members of the Family Tabanidae are not well known due to their wide range and that most of adult flies only survive a single season in the geographical area under consideration. Adult tabanids generally appear in June, with numbers collected through August in temperate climates. However, some species appear during late spring/ early summer season, while others appear in larger numbers during the
latter part of the summer/early fall season in temperate zones (Mundoch and Takahasi, 1969). Seasonal surveillance of tabanids in Gyeonggi province, Republic of Korea (ROK) during June-August (Suh et al., 2005) and April-October (Suh et al., 2015) showed that few specimens were collected during April and September-October. While the horse flies, Tabanus chrysurus and Tabanus mandarinus, from Jeju Island, ROK, were first recorded by Okamoto (1924), they have not been investigated as biological and mechanical vectors of pathogens of medical or veterinary importance. In this study, we investigated the seasonal abundance of adult tabanids at US military installation/training sites and nearby villages in/near the demilitarized zone (DMZ) and Camp Humphreys in northern and southern Gyeonggi province, respectively, in the ROK.
⁎
Corresponding author at: School of Applied Biosciences, Kyungpook National University, Daegu 41566, Republic of Korea. E-mail address: [email protected] (S.J. Suh). 1 These authors contributed equally to this work. 2 Current address: School of Medicine, Kangwon National University, Chuncheon 24341, Republic of Korea. https://doi.org/10.1016/j.aspen.2020.02.005 Received 1 October 2019; Received in revised form 31 January 2020; Accepted 14 February 2020 Available online 14 February 2020 1226-8615/ © 2020 Published by Elsevier B.V. on behalf of Korean Society of Applied Entomology.
Journal of Asia-Pacific Entomology 23 (2020) 315–319
K.S. Choi, et al.
Fig. 1. Map of the northern and southern part of Gyeonggi province denoting collection sites of horse and deer flies at (A) Neutral Nations Supervisory Commission (NNSC) camp adjacent to the Panmunjom, (B) Daeseongdong village of approximately 200 residents inside the Demilitarized zone (DMZ), (C) South Gate (Southernboundary of the 2km wide DMZ), (D) Camp Bonifas (US Army Installation), (E) Warrior Base (US Army training site approximately 3 km from the DMZ, (F) Tongilchon (village of approximately 200 residents; trap set at a beef farm with approximately 50 cattle and 3 km from the DMZ, (G) Dagmar North training site (DNTA) and (H) Camp Humphreys.
Materials and methods
Table 1 Annual numbers of deer and horse flies collected in Gyeonggi province in the ROK from 2015 to 2018.
Collection sites and sample information
Species
Tabanids (deer and horse flies) were collected concurrently with other biting flies (mosquitoes and biting gnats) at three sites in the DMZ [Neutral Nations Supervisory Commission camp (NNSC) (37°57′16.39′’N, 126°40′50.03′’E), Daeseongdong village (37°56′26.92′’N, 126°40′37.42′’E), and South Gate (gate to the southern boundary of the DMZ) (37°56′03.53″N; 126°43′15.46″E)], and four sites near the DMZ [Camp Bonifas (37°56′0.87′’N, 126°43′17.02′’E), Warrior Base training area (37°55′17.01′’N, 126°44′30.22′’E), Tongilchon village (37°54′32.18′’N, 126°44′01.88′’E), and Dagmar North training area (37°58′29.85″N; 126°50′40.88″E)] in northern Gyeonggi province and at Camp Humphreys (36°57′14.46″N; 127° 1′33.21″E) in southern Gyeonggi province in the ROK using New Jersey light traps and Mosquito Magnet® traps from May-October 2015–2018 (Fig. 1). The tabanids were separated from other biting flies following each collection, and placed dry in 2 ml cryovials and maintained at −80 °C until transported to Kyungpook National University, Daegu in the ROK where they were identified morphologically using a stereoscopic microscope and taxonomic keys of Mundoch and Takahasi (1969) and Suh et al. (2002a,b; 2003).
Year
Total
%
2015
2016
2017
2018
Chrysopsinae (deer flies) Atylotus horvathi Atylotus miser Chrysops dissectus Chrysops japonicus Chrysops mlokosiewiczi Chrysops suavis
8 5 0 0 468 11
0 0 1 0 199 5
12 31 0 1 4075 62
0 2 0 5 4782 70
20 38 1 6 9524 148
0.2 0.38 0.01 0.06 95.39 1.48
Tabaninae (horse flies) Haematopota antennata Haematopota koryoensis Haematopota sinensis Haematopota tamerlani Tabanus aurotestaceus Tabanus griseinus Tabanus loukashkini Tabanus mandarinus Tabanus sapporoensis Tabanus taiwanus Tabanus trigeminus
0 12 1 0 0 0 1 0 0 2 2
0 29 0 0 0 0 0 0 0 0 0
4 66 54 5 1 1 0 0 1 0 0
55 0 11 2 0 0 0 1 0 0 0
59 107 66 7 1 1 1 1 1 2 2
0.59 1.07 0.66 0.07 0.01 0.01 0.01 0.01 0.01 0.02 0.02
Total
510
234
4313
4928
9985
100
Results and discussion population abundance. The highest numbers of tabanids were collected from June-August (Table 2). Similar to results of Suh et al. (2015), C. mlokosiewiczi was collected from late-May-mid-September, with bimodal peaks observed during June (72.26%) and late July (12.26%) (Fig. 2). Bimodal peaks were observed for C. suavis during mid-late June (75.81%) and midSeptember (19.36%) in 2017, while the numbers of specimens collected during 2015–2016 and 2018 were not peaked bimodally (Fig. 3). A unimodal peak was observed for H. koryoensis in mid-July (50.47%) during the study period (Fig. 4). Recent study similarly reported that C. suavis demonstrated bimodal peaks in mid-June and early-September during 2010–2013, while peak populations of H. koryoensis were only observed during late-July (Suh et al., 2015). Although insufficient numbers of Chrysops japonicus and Haematopota antennata were collected for analysis, specimens were collected only during mid-May and late-June-July respectively. Haematopota sinensis demonstrated a
A total of 9985 deer and horse flies belonging to 2 subfamilies, 4 genera and 17 species were collected at US military installations and training areas and associated villages, Gyeonggi province, ROK from 2015 to 2018 (Table 1). Previous surveillance of tabanids from 2003 to 2004 (Suh et al., 2005) reported the presence of only 14 species, while surveillance from 2010 to 2013 reported 20 species (Suh et al., 2015) at sites near/in the DMZ. Similar to the other studies Chrysops mlokosiewiczi was the predominant species, and in collections from 2015 to 2018, it was the most commonly collected species (95.39%), followed by Chrysops suavis (1.48%) and Haematopota koryoensis (1.07%), while the other 14 species accounted for only 2.06% of all species collected. A total of 49.35% of all deer and horse flies were collected during 2018, followed by 2017 (43.2%), 2015 (5.11%), and 2016 (2.34%). No correlations between climate (temperature and precipitation) and the number of collected specimens during each of the years were observed. Further studies are needed to determine factors that affect relative 316
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Table 2 Seasonal prevalence of tabanid flies collected in Gyeonggi province in the ROK from 2015 to 2018 Month
MAY
JUN
JUL
AUG
SEP
Oct
Total
Species
E
M
L
E
M
L
E
M
L
E
M
L
E
M
L
E
M
L
Atylotus horvathi Atylotus miser Chrysops dissectus Chrysops japonicus Chrysops mlokosiewiczi Chrysops suavis Haematopota antennata Haematopota koryoensis Haematopota sinensis Haematopota tamerlani Tabanus aurotestaceus Tabanus griseinus Tabanus loukashkini Tabanus mandarinus Tabanus sapporoensis Tabanus taiwanus Tabanus trigeminus
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 6 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 18 10 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 1641 20 0 0 0 1 0 0 0 0 0 0 0
0 1 0 0 2824 63 0 0 8 2 0 0 0 0 0 0 0
4 4 0 0 2417 25 2 0 19 0 0 1 0 0 1 0 0
4 2 0 0 801 0 18 3 21 4 0 0 0 0 0 0 0
0 4 0 0 312 1 15 54 8 0 0 0 0 0 0 2 0
2 6 0 0 1168 0 24 43 4 0 0 0 0 1 0 0 2
3 4 0 0 197 0 0 6 3 0 0 0 0 0 0 0 0
3 5 0 0 120 2 0 1 3 0 1 0 0 0 0 0 0
0 5 1 0 20 3 0 0 0 0 0 0 0 0 0 0 0
4 2 0 0 5 4 0 0 0 0 0 0 1 0 0 0 0
0 5 0 0 1 17 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
20 38 1 6 9524 148 59 107 66 7 1 1 1 1 1 2 2
Total
0
6
28
1662
2898
2473
853
396
1250
213
135
29
16
23
3
0
0
0
9985
Fig. 2. Annual distributions of the predominant species, Chrysops mlokosiewiczi in Gyeonggi province, ROK from 2015 to 2018. Early and mid-summer bimodal peaks were observed. Data in October were not included due to no collected specimens.
Fig. 4. Annual distributions of the third most commonly collected species, Haematopota koryoensis, in Gyeonggi province, ROK from 2015 to 2018. Only a mid-season unimodal peak was observed. Data in October were not included due to no collected specimens.
Fig. 3. Annual distributions of the second most frequently collected species, Chrysops suavis in Gyeonggi province, ROK from 2015 to 2018. A bimodal peak was observed only for 2017. Data in October were not included due to no collected specimens.
317
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Table 3 Seasonal abundance of adult tabanids collected at eight sites in Gyeonggi province in the ROK from 2015 to 2018 Month
MAY
JUN
JUL
AUG
SEP
Oct
Total
Locality
E
M
L
E
M
L
E
M
L
E
M
L
E
M
L
E
M
L
Camp Bonifas Daeseongdong Dagmar North TA NNSC Camp South Gate Tongilchon Warrior Base Camp Humphreys
0 0 0 0 0 0 0 0
0 0 2 3 1 0 0 0
4 0 6 9 8 0 1 0
38 143 817 481 117 0 63 3
92 42 1659 869 111 0 116 9
103 30 978 1114 154 0 89 5
103 13 167 487 43 0 38 2
31 44 48 126 63 20 58 6
159 32 130 756 25 0 133 15
29 5 19 137 3 0 0 20
6 3 20 101 2 0 1 2
0 0 9 14 2 0 1 3
5 0 3 6 2 0 0 0
0 0 16 5 1 0 1 0
0 0 0 3 0 0 0 0
0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0
570 312 3874 4111 532 20 501 65
Total
0
6
28
1662
2898
2473
853
396
1250
213
135
29
16
23
3
0
0
0
9985
Table 4 A total number of deer and horse flies collected at seven sites in/near the DMZ in northern Gyeonggi province and at Camp Humphreys in southern Gyeonggi province, ROK, from 2015 to 2018 Locality Species
Camp Bonifas
Daeseongdong Village
Dagmar North TA
NNSC Camp
South Gate
Tongilchon Village
Warrior Base TA
Camp Humphreys
Total
Atylotus horvathi Atylotus miser Chrysops dissectus Chrysops japonicus Chrysops mlokosiewiczi Chrysops suavis Haematopota antennata Haematopota koryoensis Haematopota sinensis Haematopota tamerlani Tabanus aurotestaceus Tabanus griseinus Tabanus loukashkini Tabanus mandarinus Tabanus sapporoensis Tabanus taiwanus Tabanus trigeminus
4 2 0 0 559 0 0 2 2 0 0 0 1 0 0 0 0
0 0 0 0 307 1 0 1 2 1 0 0 0 0 0 0 0
10 27 1 2 3664 108 6 1 49 4 1 0 0 1 0 0 0
6 6 0 3 3981 13 36 55 3 2 0 1 0 0 1 2 2
0 3 0 1 452 21 7 44 4 0 0 0 0 0 0 0 0
0 0 0 0 20 0 0 0 0 0 0 0 0 0 0 0 0
0 0 0 0 487 5 5 1 3 0 0 0 0 0 0 0 0
0 0 0 0 54 0 5 3 3 0 0 0 0 0 0 0 0
20 38 1 6 9524 148 59 107 66 7 1 1 1 1 1 2 2
Total
570
312
3874
4111
532
20
501
65
9985
North training area (72.97%). Haematopota koryoensis (1.07%) was the third most commonly collected species, with the NNSC camp accounting and the South Gate entrance area accounting for 51.4% and 41.2%, respectively, of all specimens collected. The NNSC camp is located near a low lying area that often floods and an intermittent stream bordered by a forest that might provide adequate diversity of tabanids collected (Hyun and Shin, 1975; Kim et al., 1973). This study provides basic information for the relative species abundance of tabanids that are biological, mechanical, and potential vectors of viruses, bacteria, and helminths that pose a threat to local and military populations, wildlife, and domestic animals and birds. Further studies are needed to determine the seasonal and annual distribution of this and other species to determine factors related to ecological behavior of tabanids for the development of mitigation strategies for their control.
unimodal peak in late-June-early July (60.61%) similar to results of Suh et al. (2005) (75.31%), while an apparent peak populations were not observed during 2010–2013 (Suh et al., 2015). The remaining species were generally collected throughout June-August. Although the numbers and species of horse and deer flies collected during this study differed from previous surveillance (Suh et al., 2005, 2015), all studies showed that the peak occurrence of tabanids was from June-August. Surveillance of adult tabanids in the southern part of Korea demonstrated that most species populations peaked between the end of June and early July (Hyun and Shin, 1975; Kim et al., 1973). Previous surveillance data indicated that low winter temperatures and precipitation affect adult population more than high temperatures during the adult stage. However, this study reported that the results between the mean numbers of tabanids collected based on annual temperatures and precipitation variations were not significantly different (Suh et al., 2015). A total of 17 species of tabanids were distributed at eight sites in this study area from 2015 to 2018 (Tables 3 and 4). The highest numbers of tabanids were collected at NNSC (41.17%) and Dagmar North (38.8%). Chrysops mlokosiewiczi was the most frequently collected species at all collection sites (95.39%). NNSC (41.8%) accounted for the highest proportion of C. mlokosiewiczi collected, followed by Dagmar North training area (38.47%), while the remaining collection sites accounted for 19.73% of all specimens collected. Chrysops mlokosiewiczi (0.2%) were collected only during mid-July at a beef farm in Tongilchon. Surveillance at the site was only performed during 2015. At Dagmar North TA, the highest numbers of tabanids were collected during June (89.16%). Chrysops suavis (1.48%) was the second most frequently collected tabanid, with the highest proportion collected at Dagmar
Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments We thank COL Derek C. Cooper, Commander, 65th Medical Brigade and COL Jon Allison, Chief, Force Health Protection and Preventive Medicine, 65th Medical Brigade for their support of vector-borne disease surveillance at US military installations/training sites and 318
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associated villages in the Republic of Korea. Funding for this work was provided by the Armed Forces Health Surveillance Branch, Global Emerging Infections Surveillance and Response System, Silver Spring, MD (ProMIS ID # P0025-2016-2018-ME). The opinions or assertions contained herein are the private views of the authors, and are not to be construed as official, or as reflecting the views of the Department of the Army or the Department of Defense. This research was also supported by Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education, Republic of Korea (grant No. 2017R1D1A2B03029971).
Korea. Bull. Korean Entomol. Inst. Korea Univ. 5, 55–62 (in Korean). Krinsky, W.L., 1976. Animal disease agents transmitted by horse flies and deer flies (Diptera: Tabanidae). J. Med. Entomol. 13, 225–275. Mundoch, W.P., Takahasi, H., 1969. The female Tabanidae of Japan, Korea and Manchuria. Mem. Ent. Soc. Washington 6 pp. 4, 110–118. Okamoto, H., 1924. The insect fauna of Quelpart Island. Bull. Agri. Expt. Stn. Govt. Gen. Chosen. 1, 157–158. Polyakov, V.A., Anisimovich, V., Uzakov, U., Veselkin, G., 1990. Tabanidae. In: Veterinary Entomology and Arachnology. Agropromizdat, Moscow, pp. 14–19. Suh, S.J., Choi, K.S., Kwon, Y.J., 2002a. Taxonomic revision of Tabanus mandarinus species group (Diptera: Tabanidae) from Korea. Entomol. Res. 32, 113–118. Suh, S.J., Choi, K.S., Kwon, Y.J., 2002b. Taxonomy of Tabanus immanis species group (Diptera: Tabanidae) in Korea. Insect Koreana 19, 277–282. Suh, S.J., Choi, K.S., Kwon, Y.J., 2003. Taxonomy of Tabanus cordiger species group (Diptera: Tabanidae) in Korea. Entomol. Res. 33, 1–3. Suh, S.J., Kim, H.C., Chong, S.T., Kim, M.S., Klein, T.A., 2015. Seasonal abundance of deer and horse flies (Diptera: Tabanidae) in the northern part of Gyeonggi-do, Republic of Korea. Korean J. Parasitol. 53, 307–314. Suh, S.J., Kim, H.C., Klein, T.A., Chong, S.T., Lee, W.J., Kwon, Y.J., 2005. Tabanid flies (Diptera: Tabanidae) of the northern part of Gyeonggi province, Republic of Korea. Entomol. Res. 35, 195–198.
References Foil, L.D., 1989. Tabanids as vectors of disease agents. Parasitol. Today 5, 88–96. Hyun, J.S., Shin, T.H., 1975. Seasonal abundance of tabanid flies in Jeong-up based on the numbers captured in traps. Korean J. Entomol. 5, 17–21 (in Korean). Kim, C.W., Kim, J.I., Shin, T.H., 1973. On the Tabanidae from Cheunra-Bukdo province in
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