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Original Article

Seasonal Abundance of Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae), Collected at Cowsheds in the Southern Part of the Republic of Korea

Heung Chul Kim1, Glenn A. Bellis2, Myung-Soon Kim1, Sung-Tae Chong1, Dong-Kyu Lee3, Jee-Yong Park4, Jung-Yong Yeh4, Terry A. Klein5
The Korean Journal of Parasitology 2012;50(2):127-131.
Published online: May 24, 2012

15th Medical Detachment, 168th Multifunctional Medical Battalion, 65th Medical Brigade, Unit 15247, APO AP 96205-5247, Seoul, Korea.

2Department of Agriculture, Fisheries and Forestry, PO Box 37846, Winnellie, Northern Territory 0821, Australia.

3Department of Health and Environment, Kosin University, Busan 606-701, Korea.

4Foreign Animal Disease Division, Animal Plant and Fisheries Quarantine and Inspection Agency, Anyang 430-016, Korea.

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Corresponding author (terry.klein@us.army.mil)
• Received: December 8, 2011   • Revised: April 11, 2012   • Accepted: April 12, 2012

© 2012, Korean Society for Parasitology

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  • Black light traps were used to measure the seasonal and geographical distribution of Culicoides spp. (biting midges or no-see-ums) at 9 cowsheds in the southern half of the Republic of Korea (ROK) from June through October 2010. A total of 25,242 Culicoides females (24,852; 98.5%) and males (390; 1.5%) comprising of 9 species were collected. The most commonly collected species was Culicoides punctatus (73.0%) followed by C. arakawae (25.7%), while the remaining 7 species accounted for <1.0% of all Culicoides spp. collected. The mean number of Culicoides spp. collected per trap night (Trap Index [TI]) was highest for C. punctatus (409.3), followed by C. arakawae (144.2), C. tainanus (4.1), C. oxystoma (1.2), C. circumscriptus (0.7), C. homotomus (0.6), C. erairai (0.4), C. kibunensis (0.3), and C. nipponensis (0.04). Peak TIs were observed for C. punctatus (1,188.7) and C. arakawae (539.0) during July and August, respectively. C. punctatus and C. arakawae have been implicated in the transmission of arboviruses and other pathogens of veterinary importance that adversely impact on animal and bird husbandry.
  • Key words: Culicoides punctatus, Culicoides arakawae, biting midge, seasonal abundance
Members of the genus Culicoides Latreille (Diptera: Ceratopogonidae), often referred to as biting midges or no-see-ums, are small (0.5-2.0 mm in length) bloodsucking insects of medical and veterinary importance [1]. Culicoides spp. have a broad distribution and impact on human and veterinary health as vectors of viruses (e.g., bluetongue virus, African horse sickness, epizootic hemorrhagic disease of deer, Akabane, Aino, Chuzan, and bovine ephemeral fever), protozoan parasites (e.g. Haemoproteus spp. and Leucocytozoon spp.), and filarial worms (e.g., Onchocerca spp. and Dipetalonema spp.) throughout their range [2-10]. In addition, the bites of Culicoides often result in extreme annoyance, itching, lesions, and secondary infections that impact on both animal and human health [11,12].
The majority of Culicoides spp. records from the Republic of Korea (ROK) were made by foreign researchers from 1918 to 1960 [13-19], with the first nationwide surveys of Culicoides spp. reported in the 1970s [20,21]. Currently, 28 described species of Culicoides are reported from the ROK [21]. Of these, C. arakawae (Arakawa), C. oxystoma Kieffer, C. pulicaris (L.), C. actoni Smith, and C. obsoletus (Meigen) have been implicated in the transmission of domestic livestock pathogens [9,22-24].
More recently, Kang and Yu [25] reported on the seasonal abundance and host blood meal analysis of Culicoides spp. collected from cattle and poultry farms in Gyeonggi Province. Lee [26] conducted ecological surveys that provided information on the host-seeking activity, host preferences, and seasonal and geographical distributions of Culicoides spp. at Incheon Metropolitan City and 12 other localities from 1992-1993. Since 1993, there have been no ecological or epidemiological surveys for Culicoides spp. reported in the ROK, even though they transmit pathogens of veterinary importance in the ROK [10].
As part of the vector-borne disease surveillance, the Entomology Section, 5th Medical Detachment (MED DET), 168th Multifunctional Medical Battalion, 65th Medical Brigade, in coordination with Kosin University conducted monthly surveys to determine the species composition and seasonal and geographical distributions for Culicoides spp. collected at black light traps at cowsheds in the southern part of the ROK.
Black light traps (model 'Black Hole' by BioTrap, http://www.bio-trap.com), equipped with fine mesh screen nets and two 4-watt black light bulbs as the attractant and dependent upon local electrical sources, were used for surveillance of Culicoides spp. at 9 cowsheds distributed throughout Jeongeup (126° 50' 50.60" E, 35° 06' 26.88" N) in Jeollabuk-do (Province), Damyang (126° 59' 13.94" E, 35° 20' 25.45" N) and Gurye (127° 27' 20.74" E, 35° 12' 10.80" N) in Jeollanam-do, Yeongcheon (128° 52' 18.95" E, 36° 10' 30.94" N) and Gunwi (128° 44' 08.37" E, 36° 09' 58.56" N) in Gyeongsangbuk-do, Jinju (128° 06' 02.28" E, 35° 06' 26.88" N), Changnyeong (128° 26' 33.57" E, 35° 31' 17.67" N) and Yangsan (129° 02' 53.12" E, 35° 25' 11.95" N) in Gyeongsangnam-do, and Ulju (129° 10' 22.72" E, 35° 39' 21.11" N) in Ulsan Metropolitan City in the southern part of the ROK (Fig. 1). Black light traps were placed 1.5 m above the ground and operated for one night each month (June-October) from 06:00 p.m. to 08:00 a.m. the following day at each of the 9 cowsheds. Specimens were collected the following morning after each trap night, trap contents transported on dry ice to the 5th MED DET, and Culicoides spp. separated and identified using the keys of Arnaud [18] and the checklist of Cho and Chong [21]. Voucher specimens are lodged in the Australian Quarantine and Inspection Service Northern Territory (AQISNT) collection, Darwin, Northern Territory, Australia.
A total of 25,242 Culicoides females (24,852; 98.5%) and males (390; 1.5%) comprising 9 species were collected. The most commonly collected species was Culicoides punctatus (Meigen) (73.0%), followed by C. arakawae (25.7%), C. tainanus Kieffer (0.73%), C. oxystoma (0.21%), C. circumscriptus Kieffer (0.13%), C. homotomus Kieffer (0.11%), C. erairai Kono and Takahashi (0.06%), C. kibunensis Tokunaga (0.06%), and C. nipponensis Tokunaga (<0.01%) (Table 1). C. punctatus was the most frequently collected species at Yangsan and Yeongcheon, and these sites accounted for 53.2% and 35.9% of all C. punctatus collected, respectively. C. arakawae was the most frequently collected species at Yeongcheon (Gyeongsangbuk-do), Jinju (Gyeongsangnam-do), Gurye (Jeollanam-do), and Changnyeong (Gyeongsangnam-do) and accounted for 67.8%, 11.4%, 9.4%, and 7.4% of all C. arakawae collected at these sites, respectively.
Monthly and total trap indices (TIs) (mean number of Culicoides spp. collected/trap night) are shown in Table 2. Overall TIs were highest for C. punctatus (409.3), followed by C. arakawae (144.2), C. tainanus (4.1), C. oxystoma (1.2), C. circumscriptus (0.7), C. homotomus (0.6), C. erairai (0.4), C. kibunensis (0.3), and C. nipponensis (0.04) (Table 2). Peak populations of C. punctatus and C. arakawae were observed during July (TI=1,188.7) and August (539.0), respectively (Table 2).
The relative proportion of C. punctatus, C. arakawae, and other Culicoides spp. for each site surveyed is shown in Fig. 1. Geographically, collections with the highest proportions of C. punctatus were observed at Yangsan (98.6%), Ulju (94.2%), and Jeongeup (73.8%), Yeongcheon (59.3), while at the other surveillance sites the proportions ranged from 17.3% to 48.1%, with the lowest proportions observed at Damyang (19.3%) and Gurye (17.3%), Jeollanam Province. Conversely, the highest proportions of C. arakawae were observed at Damyang (76.1%) and Gurye (76.3%).
Culicoides species (biting midges) are vectors of both medical and veterinary importance, and as such, may impact on the economy of the animal industry in the ROK. Culicoides punctatus and C. arakawae were the primary species collected during this study and have been associated with important livestock diseases in other countries, e.g., Leucocytozoon cauleryi [21] and fowl pox [27], Fukuoka [28], Aino, and Ibaraki viruses [29,30]. Consequently, surveillance of these and other species of Culicoides and the pathogens they transmit are an important part of the veterinary health service to identify relative vector populations, their distributions, and associated pathogen infection rates (reported separately).
The dominance of C. punctatus and C. arakawae is similar to findings by Lee [26], who reported that C. punctatus, C. arakawae, and C. tainanus were the most commonly collected species at inland sites similar to those in our study. Whereas C. nipponensis and C. sinanoensis, which were not collected during our survey, were the predominant species collected from the southern coastal and eastern areas in the ROK. However, Kang and Yu [25] found that C. nipponensis was the dominant species (975.3/trap/night), followed by C. punctatus (misidentified as C. pulicaris) (73.5), and C. arakawae (38.8) among a total of 13 species collected from a cattle farm in Gyeonggi Province. The disparity from these studies suggests that Culicoides populations in the ROK are highly localized and extrapolations between areas must be viewed cautiously.
The dominance of C. punctatus around cowsheds agrees with the host preference of this species for cattle [26,29,30]. Although C. arakawae appears to have a preference for feeding on birds [31] it also readily feeds on cattle [25,26], which would explain its abundance around cowsheds. Further studies on Culicoides spp. geographical and seasonal distributions, host attraction (i.e., placement of traps near human habitation and poultry, cattle, and swine farms) and biting activity, pathogen infection rates, and their role as potential vectors of zoonotic pathogens that impact on human and animal health are warranted. Although limited, these data provide a better understanding of the biology, ecology, and environmental parameters that affect relative population abundance of Culicoides spp. that can be used to predict potential human and animal health risks and develop and implement mitigation strategies.
We thank Hyun-Doo Kim, and Joo-Oh Kang, Kosin University, for their assistance in conducting Culicoides collections. We also thank Dr. Joel Gaydos, Armed Forces Health Surveillance Center, Global Emerging Infections Surveillance and Response System (AFHSC-GEIS), Silver Spring, Maryland, USA, for his administrative and technical support. This work was supported, as part of the Japanese encephalitis and malaria surveillance programs, through the joint partnership between the Uniformed Services University, Bethesda, Maryland, USA, the AFHSC-GEIS, Silver Spring, Maryland, USA, the National Center for Medical Intelligence, and the 65th Medical Brigade, ROK. The views expressed are those of the authors and should not be construed to represent the positions of the US Department of the Army or Department of Defense.
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Fig. 1
Surveyed areas and relative proportion of Culicoides spp. collected by black light traps in each collection site, Republic of Korea, 2010.
kjp-50-127-g001.jpg
Table 1.
Number (%) of Culicoides spp. collected from 9 surveyed areas from June to October 2010
Table 1.
Species Jeongeup Damyang Gurye Gunwi Yeongcheon Ulju Chang- nyeong Yangsan Jinju Total
Culicoides arakawae 41 (20.3) 83 (76.1) 612 (76.3) 122 (52.4) 4,399 (39.8) 26 (4.7) 480 (52.5) 11 (0.1) 717 (49.6) 6,491 (25.7)
Culicoides circumscriptus 0 0 0 3 (1.3) 24 (0.2) 1 (0.2) 2 (0.2) 0 2 (0.1) 32 (0.1)
Culicoides erairai 0 1 (0.9) 0 0 7 (0.1) 1 (0.2) 0 7 (0.1) 0 16 ( < 0.1)
Culicoides homotomus 0 0 1 (0.1) 0 0 0 0 0 27 (1.9) 28 (0.1)
Culicoides tainanus 12 (5.9) 1 (0.9) 3 (0.4) 0 51 (0.5) 3 (0.5) 0 114 (1.1) 1 (0.1) 185 (0.7)
Culicoides nipponensis 0 0 0 0 0 0 0 0 2 (0.1) 2 ( < 0.1)
Culicoides oxystoma 0 3 (2.8) 41 (5.1) 0 7 0 0 2 ( < 0.1) 0 53 (0.2)
Culicoides kibunensis 0 0 6 (0.7) 0 6 (0.1) 1 (0.2) 0 1 ( < 0.1) 1 (0.1) 15 ( < 0.1)
Culicoides punctatus 149 (73.7) 21 (19.3) 139 (17.3) 108 (46.4) 6,547 (59.3) 520 (94.2) 433 (47.3) 9,807 (98.6) 696 (48.1) 18,420 (73.0)
Total 202 109 802 233 11,041 552 915 9,942 1,446 25,242
Table 2.
Monthly trap indices of Culicoides spp. collected from black light traps at 9 collection sites (cowsheds) in the southern part of the ROK, 2010
Table 2.
Culicoides species June July August September October Trap Indexb
C. arakawae 21.0a 155.9 539.0 4.2 1.1 144.2
C. circumscriptus 0.4 2.4 0.7 0 0 0.7
C. erairai 0.2 0.9 0.7 0 0 0.4
C. homotomus 1.8 1.3 0 0 0 0.6
C. tainanus 0.1 3 14.9 0 2.6 4.1
C. nipponensis 0.1 0 0.1 0 0 < 0.1
C. oxystoma 0 0.4 5.3 0 0.1 1.2
C. kibunensis 0.4 0.1 1.1 0 0 0.3
C. punctatus 114.4 1,188.7 622.8 75.7 45.1 409.3
Total 138.4 1,352.7 1,184.6 79.9 48.9 560.8

aMonthly trap index=number of each species of biting midges collected per month per trap night.

bTotal trap index=total number of each species of biting midges collected per trap night.

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Seasonal Abundance of Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae), Collected at Cowsheds in the Southern Part of the Republic of Korea
Korean J Parasitol. 2012;50(2):127-131.   Published online May 24, 2012
DOI: https://doi.org/10.3347/kjp.2012.50.2.127
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Seasonal Abundance of Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae), Collected at Cowsheds in the Southern Part of the Republic of Korea
Korean J Parasitol. 2012;50(2):127-131.   Published online May 24, 2012
DOI: https://doi.org/10.3347/kjp.2012.50.2.127
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Seasonal Abundance of Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae), Collected at Cowsheds in the Southern Part of the Republic of Korea
Image
Fig. 1 Surveyed areas and relative proportion of Culicoides spp. collected by black light traps in each collection site, Republic of Korea, 2010.

Fig. 1

Seasonal Abundance of Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae), Collected at Cowsheds in the Southern Part of the Republic of Korea
Species Jeongeup Damyang Gurye Gunwi Yeongcheon Ulju Chang- nyeong Yangsan Jinju Total Culicoides arakawae 41 (20.3) 83 (76.1) 612 (76.3) 122 (52.4) 4,399 (39.8) 26 (4.7) 480 (52.5) 11 (0.1) 717 (49.6) 6,491 (25.7) Culicoides circumscriptus 0 0 0 3 (1.3) 24 (0.2) 1 (0.2) 2 (0.2) 0 2 (0.1) 32 (0.1) Culicoides erairai 0 1 (0.9) 0 0 7 (0.1) 1 (0.2) 0 7 (0.1) 0 16 ( < 0.1) Culicoides homotomus 0 0 1 (0.1) 0 0 0 0 0 27 (1.9) 28 (0.1) Culicoides tainanus 12 (5.9) 1 (0.9) 3 (0.4) 0 51 (0.5) 3 (0.5) 0 114 (1.1) 1 (0.1) 185 (0.7) Culicoides nipponensis 0 0 0 0 0 0 0 0 2 (0.1) 2 ( < 0.1) Culicoides oxystoma 0 3 (2.8) 41 (5.1) 0 7 0 0 2 ( < 0.1) 0 53 (0.2) Culicoides kibunensis 0 0 6 (0.7) 0 6 (0.1) 1 (0.2) 0 1 ( < 0.1) 1 (0.1) 15 ( < 0.1) Culicoides punctatus 149 (73.7) 21 (19.3) 139 (17.3) 108 (46.4) 6,547 (59.3) 520 (94.2) 433 (47.3) 9,807 (98.6) 696 (48.1) 18,420 (73.0) Total 202 109 802 233 11,041 552 915 9,942 1,446 25,242 Culicoides species June July August September October Trap Indexb C. arakawae 21.0a 155.9 539.0 4.2 1.1 144.2 C. circumscriptus 0.4 2.4 0.7 0 0 0.7 C. erairai 0.2 0.9 0.7 0 0 0.4 C. homotomus 1.8 1.3 0 0 0 0.6 C. tainanus 0.1 3 14.9 0 2.6 4.1 C. nipponensis 0.1 0 0.1 0 0 < 0.1 C. oxystoma 0 0.4 5.3 0 0.1 1.2 C. kibunensis 0.4 0.1 1.1 0 0 0.3 C. punctatus 114.4 1,188.7 622.8 75.7 45.1 409.3 Total 138.4 1,352.7 1,184.6 79.9 48.9 560.8
Table 1. Number (%) of Culicoides spp. collected from 9 surveyed areas from June to October 2010
Table 2. Monthly trap indices of Culicoides spp. collected from black light traps at 9 collection sites (cowsheds) in the southern part of the ROK, 2010

Monthly trap index=number of each species of biting midges collected per month per trap night.

Total trap index=total number of each species of biting midges collected per trap night.

Table 1.

Table 2.

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