New Record of Lipoptena fortisetosa (Diptera: Hippoboscidae) Collected from Siberian Roe Deer on Jeju Island, Korea Author(s): Chang-Yong Choi, Sang Lee, Kyoung-Ha Moon, Chang-Wan Kang, and Young-Min Yun Source: Journal of Medical Entomology, 50(5):1173-1177. Published By: Entomological Society of America URL: http://www.bioone.org/doi/full/10.1603/ME12150

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New Record of Lipoptena fortisetosa (Diptera: Hippoboscidae) Collected From Siberian Roe Deer on Jeju Island, Korea CHANG-YONG CHOI,1,2 SANG LEE,1 KYOUNG-HA MOON,1 CHANG-WAN KANG,3 1,4 AND YOUNG-MIN YUN

J. Med. Entomol. 50(5): 1173Ð1177 (2013); DOI: http://dx.doi.org/10.1603/ME12150

ABSTRACT Lipoptena deer keds (Diptera: Hippoboscidae) are blood-sucking ectoparasites of mammals, and only one species, Lipoptena cervi (L.), has previously been reported from the Republic of Korea. A study of Siberian roe deer Capreolus pygargus Pallas on Jeju Island, south of the Korean mainland, led to the discovery of a second species of deer ked, Lipoptena fortisetosa Maa, for Korea. In total, 518 deer keds were collected from 19 adult and juvenile deer examined from May to October 2012. The infestation of all of the deer examined and the occurrence on newly born deer suggest a high prevalence and abundance of L. fortisetosa parasitizing Siberian roe deer throughout Jeju Island. This deer represents a new host species for L. fortisetosa. KEY WORDS deer ked, Hippoboscidae, Jeju Island, Lipoptena fortisetosa, Siberian roe deer

Deer keds (genus Lipoptena) are dorsoventrally ßattened blood-sucking ectoparasites belonging to the family Hippoboscidae (Allan 2001). These ßies typically parasitize mammals, particularly cervids. They are hematophagous arthropods with piercing mouthparts, which shed their wings once established on a host on which they will live permanently or nearpermanently (Yamauchi and Nakayama 2006, Nakayama 2007). The impacts of deer keds parasitizing wild and domestic animals were poorly known in terms of pathology and disease transmission until recently (Allan 2001), but recent studies have conÞrmed that deer keds are potential vectors of various diseases including Bartonella spp. (Dehio et al. 2004, Halos et al. 2004, Matsumoto et al. 2008), Rickettsia spp. (Hornok et al. 2011), and Anaplasma ovis (Hornok et al. 2011). Therefore, information on the distribution, prevalence, and abundance of deer keds is important for understanding the hostÐparasite interaction and potential disease transmission in wild and domestic animals. In the Republic of Korea, the largest study on the occurrence of ectoparasites including hippoboscid ßies was conducted mainly for avian species during the Migratory Animals Pathological Survey during the 1960s (McClure et al. 1973). The survey, focusing on louse ßies parasitizing wildlife, was essentially discontinued, until three recent reports emerged (Kim et al. 2010, Suh et al. 2012, and Iwasa and Choi 2013) up1 Jeju Wildlife Rescue Center, Jeju National University, Jeju City, Jeju 690-121, Republic of Korea. 2 Present address: Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul 151-921, Republic of Korea. 3 Jeju Wildlife Research Center, 865-2, Hogeun-dong, Seogwipo City, Jeju 697-090, Republic of Korea. 4 Corresponding author, e-mail: [email protected].

dating the checklist of louse ßies based on new collections in Korea. Of 30 Lipoptena species known worldwide (Dick 2006), and of 13 hippoboscid species known from Korea (Iwasa and Choi 2013), only one deer ked species, Lipoptena cervi (L., 1758), was recorded from mainland Korea, where it parasitized Korean Water Deer Hydropotes inermis (Swinhoe) (Kim et al. 2010, Suh et al. 2012, Iwasa and Choi 2013). Kim et al. (2010) examined a Siberian roe deer Capreolus pygargus Pallas on KoreaÕs largest island of Jeju, but collected no deer keds. However, Yamauchi et al. (2009) reported that a specimen collected on 27 July 1990 from Halla Mountain, Jeju, was reidentiÞed as Lipoptena fortisetosa Maa, a species not currently included in the checklist of louse ßies in Korea. The collection of a single L. fortisetosa, without any host information, could not rule out the possibility of an accidental record leaving the status of deer ked species on Jeju Island uncertain. In this study, we report on a collection of L. fortisetosa from Jeju Island, Korea, and conÞrm the Siberian roe deer as a new host for this deer ked. We also discuss the potential prevalence of the deer ked on Jeju, and update the list of its associated hosts. Materials and Methods Jeju Island (33.3667 N, 126.5333 E) is the largest island in the Republic of Korea. It is an oval-shaped volcanic island located 80 km south of the Korean Peninsula between the East China Sea and the Korea Strait (Fig. 1). In total, 1,601 insect species has been recorded from Jeju, as of January 2006, but that list does not include any deer ked species (genus Lipoptena spp.) (Cultural Heritage Administration [CHA] 2006).

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Fig. 1. Jeju Island and the localities of 19 Siberian roe deer C. pygargus examined. Numbers represent the identiÞcation number of each deer.

From May to October 2012, we examined a total of 19 Siberian roe deer from 14 different localities on Jeju Island to determine the occurrence of deer keds there (Fig. 1). Deer keds were collected from the deer manually or by means of Þne forceps. No attempt was made to collect all deer keds from each deer examined, as we tried to minimize the stress caused to wild caught or injured deer. We recorded information concerning the status and condition of the host, and collected and labeled deer ked specimens including location and the date and time of collection. Specimens were stored in 2- or 4-ml cryovials containing 70% ethyl alcohol and identiÞed under a dissecting microscope using Table 1.

standard keys and previous descriptions (e.g., Maa 1967, 1969; Mogi 1975) at the Jeju Wildlife Rescue CenterÕs laboratory, Jeju National University, Korea. Results and Discussion Nineteen Siberian roe deer were examined; two were captive, four were wild caught, and 13 had been rescued owing to injury or having become lost; seven were new born (0.5Ð1 mo old). Overall, 518 deer keds (336 females and 182 males) were collected, and all of them were identiÞed as L. fortisetosa (Diptera: Hippoboscidae) (Table 1; Fig. 2). Eight deer ked speci-

Deer keds L. fortisetosa collected from Siberian roe deer C. pygargus on Jeju Island, Korea No. of L. fortisetosa collected

Host Collection date 07 May 2012 08 May 2012 09 May 2012 13 June 2012 13 June 2012 13 June 2012 13 June 2012 19 June 2012 20 June 2012 21 June 2012 22 June 2012 23 June 2012 25 June 2012 01 July 2012 02 July 2012 11 July 2012 12 July 2012 19 July 2012 31 July 2012 18 Aug. 2012 29 Aug. 2012 06 Oct. 2012 Total

ID

Sex

Age

Condition

1 2 3 1 4 5 6 7 8 9 10 11 12 13 1 14 15 16 17 18 4 19

Female Male Female Female Male Male Female Female Female Male Female Female Male Male Female Female Female Female Female Female Male Male

Adult Adult Adult Adult Adult Juvenile Adult Adult Juvenile Juvenile Adult Juvenile Juvenile Juvenile Adult Juvenile Adult Adult Adult Juvenile Adult Adult

Captive Rescued Wild Captive Captive Rescued Wild Rescued Rescued Rescued Rescued Wild Rescued Rescued Captive Rescued Wild Rescued Rescued Rescued Captive Rescued

De-alate Female

De-alate Male

Alate Female

Alate Male

Total

3 0 2 1 38 4 6 2 1 4 30 8 5 24 0 3 3 59 103 33 0 5 334

0 2 0 0 17 0 2 1 0 0 17 7 3 22 7 9 1 37 35 15 1 3 179

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 2

0 0 0 1 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 3

3 2 2 2 55 4 8 3 1 4 47 15 8 47 7 12 5 98 138 48 1 8 518

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Fig. 2. De-alate form of two female L. fortisetosa collected on 1 July 2012 from a juvenile Siberian roe deer C. pygargus in the Republic of Korea: dorsal (left) and ventral view (right). Scale bar indicates 1 mm. (Online Þgure in color.)

mens (four females and four males) were sent to the National Institute of Biological Resources in Korea (NIBR-IN-0000566520 and NIBR-IN-0000566521), and eight (four females and four males) were deposited in the Bernice Pauahi Bishop Museum, Honolulu, HI (Bishop Museum Accession No. 2013.063). The remaining ked specimens were kept for future destructive analysis, such as disease surveillance. The mean length of the head and thorax of L. fortisetosa from Jeju was 1.4 mm (range: 1.3Ð1.5 mm), and the total length ranged from 2.5 to 3.9 mm, that length being largely dependent on how recently they had fed. These measurements correspond to previous descriptions of L. fortisetosa, which emphasized its small size (Maa 1965, 1967; Mogi 1975; Schumann and Messner 1993; Fukumoto et al. 2000; Kowal et al. 2009). L. cervi, the only Lipoptena spp. previously recorded in Korea (Kim et al. 2010), is larger than L. fortisetosa, ranging in size from 4 to 7 mm (Kowal et al. 2009, Kim et al. 2010, Ac¸ ici et al. 2012). Whereas the length of the head and thorax of L. cervi is around 2 mm (Ac¸ ici et al. 2012), that of L. fortisetosa ranges from 1.3 mm (Maa 1967, Mogi 1975, Fukumoto et al. 2000) to 1.6 mm (Fujisaki et al. 1993). The 15 setae on each mesonotum were distributed unevenly, as noted by Maa (1967), Fujisaki et al. (1993), and Kowal et al. (2009). With the exception of two winged females and three males, most of the L. fortisetosa collected during this study were de-alate forms (Figs. 2 and 3) In Japan, alate L. fortisetosa have been observed from May to December in Japan (Nakayama 2007); we collected such forms on Jeju only in June and July. The wings were 3 mm in length and had 12 or 13 setulae between the apices of R1 and R4 ⫹ 5 of each wing, showing the characteristics of L. fortisetosa described by Mogi (1975). Although L. fortisetosa has been found in several European countries such as Germany (Schumann and

Messner 1993), the Czech Republic (Zeman 1998), Poland (Kowal et al. 2009), Lithuania (Lithuanian Entomological Society [LES] 2006) as well as Roma-

Fig. 3. Dorsal view of the winged male L. fortisetosa collected from an adult female Siberian roe deer C. pygargus on 13 June 2012 in the Republic of Korea. Scale bar indicates 1 mm. (Online Þgure in color.)

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Table 2.

Vol. 50, no. 5

The known mammalian and avian hosts of L. fortisetosa

Host

ScientiÞc name

Mammal Japanese Deer Siberian roe deer European roe deer Cattle Human Bird Black-Faced Bunting

Locality

Source

Cervus nippon

Japan

Capreolus pygargus Capreolus capreolus Bos taurus Homo sapiens

Jeju Island (Republic of Korea) Kazakhstan Moldavia (former USSR) Kazakhstan, Japan

Maa 1965, 1967, 1969; Fujisaki et al. 1993; Fukumoto et al. 2000; Mogi et al. 2002 This study Edwards et al. 1978 Metelitsa and Veselkin 1989 Edwards et al. 1978, Mogi et al. 2002

Emberiza spodocephala

Yakushima (Japan)

Yamauchi et al. 2009

nia and Moldavia (Metelitsa and Veselkin 1989, Paˆrvu 2005), they may have been introduced there along with introduced Japanese Deer Cervus nippon Temminck (e.g., Schumann and Messner 1993, LES 2006). The distribution of L. fortisetosa was originally reported as being conÞned to Honshu, central Japan (Maa 1965, 1967, 1969); however, further reports now suggest that it occurs throughout Japan from Hokkaido to Kyushu (Fukumoto et al. 2000, Mogi et al. 2002, Nakayama 2007). Yamauchi et al. (2009) reported that a single specimen from Jeju IslandÕs Mt. Halla was reidentiÞed as L. fortisetosa thereby extending the speciesÕ distribution from Japan to Korea, but that specimen lacks data concerning its host. Our results show that L. fortisetosa is not of accidental occurrence on Jeju Island, but rather it is widely distributed there. Because specimen collection during our study was not quantitative, but determined by collection effort, the number of keds we collected was only a small proportion of the hundreds parasitizing each individual deer. The complete infestation of all roe deer examined regardless of locality, as well as the occurrence of keds even on new-born deer in June and July suggests a wide distribution, and a high prevalence and abundance of L. fortisetosa on Siberian roe deer throughout Jeju Island. The major host of L. fortisetosa is the Japanese Deer, and few other host species have been reported (Maa 1965, 1967, 1969; Fujisaki et al. 1993; Mogi et al. 2002; Table 2). From this study, the Siberian roe deer, a species closely related to the European roe deer Capreolus capreolus (L.) but conÞned to northeast Asia, was conÞrmed as a common host of L. fortisetosa for the Þrst time. Our survey also indicates that L. fortisetosa is the dominant, prevalent, and abundant deer ked on Jeju Island, whereas L. cervi may occur on the Korean Peninsula (Kim et al. 2010). Given the co-existence of native L. cervi and introduced L. fortisetosa in Europe, further Þeld surveys are required throughout the Korean Peninsula and its adjacent islands to document the status, distribution, hosts, and interactions of these two Lipoptena species. Acknowledgments We thank Tae-jung Jin, of the Jeju Wildlife Rescue Center, who is dedicated to the rescue of injured roe deer. We also appreciate the help of Nam-Jun Ji, Hee-Man Kang, and other

members of the Jeju Wildlife Research Center in capturing wild roe deer.

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New record of Lipoptena fortisetosa (Diptera: Hippoboscidae) collected from Siberian roe deer on Jeju Island, Korea.

Lipoptena deer keds (Diptera: Hippoboscidae) are blood-sucking ectoparasites of mammals, and only one species, Lipoptena cervi (L.), has previously be...
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