Contribution to the Knowledge of the Hippoboscidae (Diptera) From the Republic of Korea Open Access

Abstract

Eight species of Hippoboscidae from 13 bird hosts are reported from the Republic of Korea (ROK). A new species of the genus Crataerina von Olfers with reduced wings is described, and it was collected from a Pacific Swift (Apus pacificus Latham; Apodiformes, Apodidae). Icosta fenestella Maa is recorded for the first time from the ROK. Ornithoica tridens Maa is synonymized with O. momiyamai Kishida. Turdus chrysolaus Temminck and Zoothera (=Turdus) sibirica (Pallas) are recorded as new birds host for I. fenestella and O. unicolor Speiser, respectively. Morphological identification keys are also presented for the species of the genus Crataerina in the Palaearctic region, and for the species of the Hippoboscidae in the ROK.

The flies of Hippoboscidae are haematophagous, obligate ectoparasites of birds and certain groups of mammals, and they comprise over 213 species worldwide (Maa 1977, Soós and Hůrka 1986, Dick 2006). Extensive studies have been done with ubiquitous (Maa 1962, 1963, 1965, 1966, 1969a, 1969b, 1969c, 1980), and Palaearctic species (Theodor and Oldroyd 1964). In East Palaearctic Asia, 26 species have been recorded from Japan (Maa 1967, Mogi et al. 2002), but only nine species were from China and eight from the Far East of Russia (Soós and Hůrka 1986, Sun 1999).

In the Republic of Korea (ROK, South Korea), 11 hippoboscid species have been recorded by Okamoto (1924), Bequaert (1941), Maa (1967, 1969a,b,c), Kim et al. (2010), and Suh et al. (2012). There is no record of the Crataerina species and no keys are available for the genera and species in the ROK.

Recently, we examined the specimens of hippoboscid flies obtained from 13 avian hosts collected from the ROK. In the present article, we describe a new species of the genus Crataerina von Olfers, and provide a new country record, synonym, host records, and identification keys to the hippoboscid species in the ROK and to the species of the Palaearctic Crataerina.

Materials and Methods

In total, 35 specimens were collected from 13 host birds in the ROK during 2008–2009. All specimens were preserved in 70% ethanol, examined under a stereomicroscope, and measured with an ocular micrometer. The male genitalia were macerated with 10% KOH and examined. Terminology follows those of Bequaert (1942), Maa (1965), and Maa and Peterson (1987).

Crataerina koreana Iwasa, New Species

Male.

Head (Fig. 1) prognathous, broad, and moderately flattened; eyes small and narrower than half of combined width of frons and fronto-orbital plates in dorsal view; vertex with ocellar triangle, ocelli absent; wide frons, bearing rows of interfrontal setae; inner vertical setae nearly parallel; wide lunule; antenna dorsally flattened, leaf-like, bearing setae; palpus well-developed, inner surface concave, compressed laterally, with numerous setae; labium needle-like and bulbous laterally.

Thorax: flattened; presutural scutum large with developed postpronotal lobes; postsutural scutum small; scutellum flattened and rhombic. Dorsal thoracic chaetotaxy: 1 notopleural; 1–5 postalar; 1 prescutellar; 4–6 subapical scutellars; postpronotal lobe and anepisternum with numerous setae; acrostichals and laterocentrals absent. Mesosternum bare, only marginal setae along border of mid coxa; metasternum with horizontal row of setae. Wings (Fig. 2) reduced in length, just extending to middle of abdomen and rounded at tip; costa fringed with long black setae and short setulae from base to tip of R₁; R_{4 + 5} thick and fused with M_{1 + 2} at point of cross vein r-m; bm cell formed by basal part of M_{1 + 2} and CuA₁ and cross vein dm-cu thick and short; CuA₂ absent. Legs: yellow and robust; coxae short; fore and mid femora swollen and covered with setae and setulae anteriorly and posteriorly; hind femur covered with dorsal apical setae; all tibia with row of anterodorsal setae; fore and mid first to fourth tarsomeres flat and nearly equal in length, fifth one longest and thick, tapering basally; hind first tarsomere twice the length of second to fourth ones, fifth one longest (1.7 times first tarsomere in length); claws black and bifid, with prominent flattened heel-like base.

Abdomen (Fig. 3): extensively membranous and covered densely with short setulae; syntergites 1 + 2 sclerotized and developed to lateral plates; tergites three and four depressed and triangular; tergite five large, chevron-shaped, clothed with long setae; tergite six divided into widely separated plates, each tergite covered with 8–11 long setae; sternite one represented by sclerotized plate, covered with setulae posteriorly; other sternites membranous, densely setose. Epandrium (Fig. 4): a narrow ring-like sclerite covered with setulae; surstylus present in form of setose flaps articulating with ventral margins of epandrium; aedeagus rod-like, slender and pointed apically (Fig. 5); gonopod elongate and triangular.

Female.

Abdomen (Fig. 6): tergites three to five small; tergite four smallest, with triangular shape; membranous area between tergites five and six sparsely covered with short setulae; tergite six divided into two widely separated plates with long setae and small setulae. Terminalia with round-shaped genital opening, consisting of sternite 10, cerci flap-like covered with setulae and membranous hypoproct; other characteristics same as those of male.

Length.

body, ♂ ♀, 6.2 mm; wing, 2.7–3.1 mm.

Type Materials.

Holotype: ♂ Chilbaldo Islet, Jeonnam, ROK, ex Apus pacifica, 10 July 2008, C. Y. Choi (deposited in The National Institute of Biological Resources (NIBR), ROK. Paratypes: 1 ♀, same data and host as holotype; 1 ♀, same locality, date, and host as holotype, Jong-Gil Park (deposited in Obihiro University of Agriculture and Veterinary Medicine, Hokkaido, Japan).

Remarks.

This species is closely similar to C. obtusipennis Austen from Mongolia, but differs by lacking vein CuA₂ in wings and its vein A_{1 +} CuA₂ not reaching wing margin. This new species is also similar to C. pacifica Iwasa from Japan, but is distinguishable from it having bm cell and cross vein dm-cu.

Distribution.

ROK.

Etymology.

This is named after the country in which the type specimens were collected.

Key to the Palaearctic Species of Genus Crataerina (♂ ♀)

1. Wing crossvein dm-cu absent. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. pacifica Iwasa

   Wing crossvein dm-cu present . . . . . . . . . . . 2

2. Wing crossvein CuA₂ absent . . . . . . . . . . . . . . . . . . . . . . . C. koreana Iwasa, new species

   Wing crossvein CuA₂ present . . . . . . . . . . . . 3

3. Wing length 2.5–3 mm, shorter than hind femur; wing tip broadly rounded. . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. obtusipennis Austen

   Wing length 4–8 mm, longer than hind femur . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

4. Wing length 7–8 mm, more than twice as long as hind femur; tergites three and 4 ≈one-thirds as wide as abdomen and tergite five nearly as wide as abdomen; female abdomen with long and thick setae on posterior margin and with group of elongate setae ventral to genital opening . . . . . . . . . . . C. melbae (Rondani)

   Wing length 5 mm or shorter; wing less than twice as long as hind femur; male tergites small or absent; all setae on posterior margin of female abdomen short and uniform in length . . . . . . 5

5. Wing length nearly twice as long as hind femur, extended beyond posterior end of abdomen; distal half of trailing edge of wing strongly concave . . . . . . . . . . . C. acutipennis Austen

   Wing length 1.3–1.5 times as long as hind femur, not extended beyond posterior end of abdomen; distal half of trailing edge of wing not strongly concave . . . . . . . C. pallida (Oliver)

Icosta fenestella Maa

Icosta fenestella Maa, 1969:109.

Specimen Examined.

One ♀, Chilbaldo Islet, Jeonnam, 30 April 2008, C. Y. Choi, ex Turdus chrysolaus. New host record.

Distribution.

Burma, Indonesia (Java and Komodo Is.), Malaysia (Borneo), Philippines, Taiwan (Maa 1977), and ROK. New to ROK.

Ornithomya avicularia aobatonis (Matsumura)

• Onithomya aobatonis Matsumura, 1905:119.

• Ornithomya avicularia aobatonis Matsumura: Maa, 1967:735.

Specimens Examined.

Three ♂, Hongdo Is., Jeonnam, ROK, 24–25 August 2008, C. Y. Choi, ex Turdus pallidus; 3 ♂, 6 ♀, same locality, 19–29 September 2008, C. Y. Choi, ex Turdus pallidus; 2 ♀, same locality, 13 September 2008, H.Y. Nam, ex Accipiter gularis.

Distribution.

Japan, Russia (East Siberia), and ROK (Soós and Hůrka 1986).

Ornithomya chloropus extensa Maa,

• Ornithomya chloropus extensa Maa, 1967:737.

Specimens Examined.

One ♀, Hongdo Is., Jeonnam, ROK, 12 October 2008, C. Y. Choi, ex Emberiza spodocephala; 1 ♀, Hekusando Is., Jeonnam, 27 October 2008, C. Y. Choi, ex Emberiza pallasi; 1 ♀, Hongdo Is., Jeonnam, 16 October 2008, C. Y. Choi, ex Anthus hodgsoni.

Distribution.

Japan and ROK (Maa 1967).

Ornithoica unicolor Speiser, 1900

• Ornithoica unicolor Speiser, 1900:556.

Specimen Examined.

One ♀, Hongdo Is., Jeonnam, ROK, 22 September 2008, C. Y. Choi, ex Zoothera (=Turdus) sibirica (Adult). New host record.

Distribution.

Burma, Indonesia (Sumatra), Japan (Hokkaido), Malaysia (Borneo), Pakistan, Russia (East Siberia), ROK, and Thailand (Maa 1977).

Ornithoica momiyamai Kishida

• Ornithoica momiyamai Kishida, 1932:245.

• Ornithoica tridens Maa, 1966:413. Syn. n.

There has been confusion in taxonomic status of this species. Ornithoica momiyamai Kishida was described from Japan, based on the specimens collected from avian hosts of Turdus and Lanius. Maa (1963) synonymized O. momiyamai with O. stipituri (Schiner, 1868), but later Maa (1966) described O. tridens from Taiwan and upon examination of male and gynandromorph suggested that it possibly was identical to O. momiyamai. In a review of Japanese species, Maa (1967) listed O. momiyamai as a valid species. Then, O. tridens Maa was listed as O. stipituri tridens Maa in the Oriental catalog by Maa (1977). Thereafter, O. momiyamai was treated as a synonym of O. stipituri in the Palaearctic catalog by Soós and Hůrka (1986), probably based on the proposal by Maa (1963). However, Mogi et al. (2002) examined specimens of males and gynandromorphs of O. momiyamai and pointed out their similarity. The present specimens of males also agree with O. tridens. Therefore, we synonymize O. tridens with O. momiyamai, based on male and female specimens from hosts of Turdus and Lanius in the ROK.

Specimens Examined.

One ♂, Hongdo Is., Jeonnam, ROK, 28 September 2008, C. Y. Choi, ex Lanius bucephalus; 1 ♀, same locality, 22 September 2008, C. Y. Choi, ex Trudus pallidus; 1 ♀, same locality, 22 April 2009, C. Y. Choi, ex T. pallidus.

Distribution.

Japan (Hokkaido, Honshu), Taiwan (Maa 1977), and ROK.

Ornithophila metallica (Schiner)

• Ornithomyia metallica Schiner, 1864:646.

• Ornithophila metallica: Rondani, 1879:20.

Specimens Examined.

One ♀, Hongdo Is., Jeonnam, ROK, 19 April 2009, Chang-Yong, Choi, ex Zoothera dauma; 1 ♀, same locality, 30 April 2008, C.Y. Choi, ex T. chrysolaus; 1 ♂, same locality, 22 April 2009, C.Y. Choi, ex T. pallidus; 1 ♀, same locality, 23 April 2009, C. Y. Choi, ex Muscicapa dauurica; 1 ♀, Heuksando Is., 16 April 2009, C. Y. Choi, ex Motacilla cinerea.

Distribution.

Europe, North Africa, Russia, Asia, Afganistan, China, Japan, ROK, and Turkey (Soós and Hůrka 1986).

Discussion

In total, 13 species of Hippoboscidae in eight genera were recorded from the ROK (Kim et al. 2010, Suh et al. 2012, and the current study), which is considerably fewer than the 26 species found in Japan (Mogi et al. 2002). Our knowledge of hippoboscid fauna in the ROK is still poor, but even from our limited data, it is now feasible to show an outline of species composition in relation to geographical distribution and hosts. Hippoboscid species in ROK are composed of eight Palaearctic, four Palaearctic-Oriental (distributed from Palaearctic to Oriental regions), and one Oriental species. Mogi et al. (2002) pointed out that the Japanese deer (Cervus nippon Temminck) endemic to Japan is parasitized by three species of the genus Lipotena. In ROK, only one species, Lipotena cervi (L.) was recorded from Korean water deer (Hydropotes intermis argyropus Swinhoe) (Kim et al. 2010). This may be because of less endemism in cervid deer in the Korean peninsula. There is no record of the Palaearctic Stenepteryx hirundinis (L.) in ROK, and this may be because of the absence of the host (house martin, Delichon urbica) in the country. The genus Crataerina now comprises seven species worldwide (six Palaearctic and one Neotropical) including Crataerina koreana. The known Palaearctic species of the Crataerina are known to be monoxenous, parasitizing the Apus swift (Apodiformes, Apodidae) (Maa 1963, Iwasa 2001). The western Palaearctic species of Crataerina (C. acutipennis Austen, C. melbae (Rondani), and C. pallida (Latreille)) are parasite of the western Palaearctic Apus swift (Apus apus, Apus melbae, Apus affinis, etc.) (Maa 1969a). Though the host of a central Palaearctic species C. obtusipennis Austen is unknown, in Japan (easternmost of Palaearctic Region) C. pacifica Iwasa parasitizes Apus pacificus, which is distributed in the east Palaearctic region (Iwasa 2001). C. koreana and C. pacifica are probably vicariant species resulting from geographical isolation of the same host. There are some hippoboscid subspecies described from Japan and Korea, but there are no studies of China and Russian populations (Mogi et al. 2002, Sato and Mogi 2008). Because of limited knowledge, examinations of the hippoboscid specimens from the Palaearctic and Oriental regions are important to further understand the species status and distributions.

Many hippoboscid species parasitizing birds have been introduced after seasonal migration of their hosts (Bear and Freidberg 1995, Mogi et al. 2002). Though ROK is located in the Palaearctic region, there are some Oriental species reported in this country, such as Icosta ardere ardere (Macqart) and Ornithophila metallica (Schiner), which have been recorded from avian hosts collected only in April (Suh et al. 2012, and the current study). This may suggest that these species have arrived and spread from the Oriental region with migratory birds during the spring migration.

A widespread species O. unicolor was collected from a passage migrant (Zoothera sibirica (Pallas)) in the current study, but this species was recorded from a migratory bird (summer visitor) and resident birds in the ROK (Suh et al. 2012). This parasite probably reproduces during the breeding season of hosts. A newly recorded Oriental species, I. fenestella Maa was also collected in the ROK from a passage migrant, Turdus chrysolaus Temminck. However, it can be not ascertained whether this species is a transient or permanent resident in the ROK. Further survey of hippoboscids in the ROK and the Asian continent is necessary determine the fauna, distribution, host relationship, and transmission of pathogens in the east Palaearctic region.

Key to the Species of Hippoboscidae in the ROK (♂ ♀)

1. Wing reduced, without CuA₂ vein. . . . . . . . . . . . . . . . . . Crataerina koreana Iwasa, sp. nov.

   Wing ample . . . . . . . . . . . . . . . . . . . . . . . 2

2. Wing with three longitudinal veins and one crossvein . . . . . . . . . . . . Lipotena cervi (L.)

   Wing with 5–6 longitudinal veins . . . . . . . . . 3

3. Apical one-thirds of vein R_{4 + 5} running very closely to and almost confluent with costa . . . . . . . . . . . . . . . . . . . Ornithoica Rondani 4

   Veins R_{4 + 5} and costa well apart from each other except at extreme apices . . . . . . . . . . . . . 5

4. Prosternum anteriorly acute; ♀ with anchor-like spines near abdominal apex markedly smaller than those near abdominal base; ♂ abdomen dorsally and laterally with moderate setulae; wing length 3.9–4.4 mm. . . . . . . . . . . . . . . . . . . . . . . . . . . Ornithoica unicolor Speiser

   Prosternum anteriorly truncate; ♀ with only minute setulae near abdominal apex; ♂ abdomen dorsally and laterally with very weak setulae; wing length 2.5 mm . . . . . . . . . . . . . . . . . . . . . . Ornithoica momiyamai Kishida

5. Tarsal claws outwardly bifid, actually simple; wing surface strongly wrinkled, never with setulae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Hippobosca L. 6

   Tarsal claws outwardly trifid, actually bifid; wing surface without fine wrinkles . . . . . . . . . . 7

6. Prosternum shorter than wide, anteriorly subacute; ♀, supra anal plate shorter than wide. . . . . . . . . . . . . . . Hippobosca longipennis F.

   Prosternum nearly 2× as wide as long, anterior margin gently convex; ♀ supra-anal plate markedly wider than long. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Hippobosca equina L.

7. Wing with three cross veins, hence three closed basal cells; veins CuA₁ well developed . . . . 8

   Wing with two crossveins; veins CuA₁ atrophied, represented by very short inconspicuous stub at base . . . . . . . . . . . . . . . Icosta Speiser 12

8. Apical three-fifths of vein R_{2 + 3} fused with C; axillary lobe subtriangular, exceptionally large; vein 2A prominent and deeply pigmented; ♀ pregenital plate stose, divided into two (1 + 1) very large pieces . . . . . . . . . . . . . . . . . . . . . . . Ornithophila metallica (Schiner)

   Veins R_{2 + 3} and C well separated from one another except at apex; axillary lobe lanceolate; vein 2A inconspicuous; ♀ pregenital plate single or absent . . . . . . . . . . . . . . . . . . . 9

9. Antenna large, leaf or spoon-like, bare near extreme apex, dorsolateral margin often sharply rimmed; crossveins r-m and dm-cu often apart from one another; axillary cord with strong black setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ornithoctona plicata (von Olfers)

   Antenna relatively small, never leaf or spoon-like, extreme apex bearing setae, dorsolateral margin never sharply rimmed; crossveins r-m and dm-cu always very close to one another; axillary cord with pale soft setae . . . . . . . . . . . . . . . . . . . . . . . Ornithomya Latreille 10

10. Basal comb on venter of basitarsis three composed of two setal rows; segments 2–4 of tarsus three ventrally each with five strong spine-like setae and small fine setae near apex; lateral part of tergite three with moderately long setulae; scutellum with eight setulae with range from 6 to 10 . . . . . . . . . . Ornithomya aviculata aobatonis (Matsumura)

    Basal comb on venter of basitarsis three composed of single setal row; segments 2–4 of tarsus three ventrally each with four strong spine-like setae near apex in addition to small fine ones; lateral part of tergite three with long slender setae or short spines . . . . . . 11

11. Dark markings on venter of head extending to vibrissal area; costal setulae more extensive; lateral part of tergite three with long slender setae; scutellum with six setulae . . . . . . . . . . . . . . . . Ornithomya chloropus extensa Maa

    Dark markings on venter of head extending only to midway of bristle area; costal setulae less extensive; lateral part of tergite three with short spines; scutellum with four setulae. . . . . . . . . . . Ornithomya fringillina (Curtis)

12. ♂ tergite three absent; ♀ abdomen ventrally without long setae near apex . . . . . . . . . . . . . . . . . . Icosta ardere aredere (Macquart)

    ♂ tergite three present; ♀ abdomen ventrally with long setae near apex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Icosta fenestella Maa

Acknowledgments

We wish to express our sincere thanks to Jong-Gill Park and Hyun-Young Nam of the Migratory Birds Center in the National Park Research Institute for their assistance during the field trip. Our thanks are also due to Assistant Professor G. A. Hill of Obihiro University of Agriculture and Veterinary Medicine for checking the English language in this manuscript.

References Cited