Research Article
Print
Research Article
Updated taxonomic keys for European Hippoboscidae (Diptera), and expansion in Central Europe of the bird louse fly Ornithomya comosa (Austen, 1930) with the first record from Slovakia
expand article infoJozef Oboňa‡, Katarína Fogašová‡, Miroslav Fulín§, Stanislav Greš§, Peter Manko‡, Jakub Repaský|, Jindřich Roháček, Oldřich Sychra#, Martin Hromada‡¤
‡ University of Prešov, Prešov, Slovakia
§ Unaffiliated, Sabinov, Slovakia
| Unaffiliated, Ražňany, Slovakia
¶ Silesian Museum, Opava, Czech Republic
# University of Veterinary Sciences Brno, Brno, Czech Republic
¤ University of Zielona Góra, ZielonaGóra, Poland

Corresponding author: Katarína Fogašová ( katarinakanasova2@gmail.com )

Academic editor: Pierfilippo Cerretti
© 2022 Jozef Oboňa, Katarína Fogašová, Miroslav Fulín, Stanislav Greš, Peter Manko, Jakub Repaský, Jindřich Roháček, Oldřich Sychra, Martin Hromada.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Oboňa J, Fogašová K, Fulín M, Greš S, Manko P, Repaský J, Roháček J, Sychra O, Hromada M (2022) Updated taxonomic keys for European Hippoboscidae (Diptera), and expansion in Central Europe of the bird louse fly Ornithomya comosa (Austen, 1930) with the first record from Slovakia. ZooKeys 1115: 81-101. https://doi.org/10.3897/zookeys.1115.80146
ZooBank: urn:lsid:zoobank.org:pub:D7AE9A4C-64D7-41D6-A3EF-07F09F2DCCFD
Open Access

Abstract

The available keys for European Hippoboscidae are outdated and do not cover all species currently known from Europe. Therefore, identification keys to the eleven genera and 31 species of the European hippoboscids are provided here. Ornithomya comosa (Austen, 1930) (Diptera: Hippoboscidae) is recorded for the first time from the territory of Slovakia based on one female found on a sand martin, Riparia riparia (Linnaeus, 1758). The list of keds and louse flies recorded from the territory of Slovakia is increased to 20 species. New host records for Slovakia are presented.

Keywords

Birds, hippoboscid, new host records, new record, parasite, Slovakia, taxonomic keys

Introduction

Keds and louse flies (Diptera: Hippoboscidae) are among the most fascinating as well as disregarded group of blood-feeding ectoparasites, and they thrive on many animal species (Bezerra-Santos and Otranto 2020). This family is included in the superfamily Hippoboscoidea, along with the families Glossinidae (tse-tse flies), Streblidae, and Nycteribiidae (bat flies) (Petersen et al. 2007; Reeves and Lloyd 2019). Hippoboscidae are divided into the subfamilies Lipopteninae (tribe Lipoptenini parasitising exclusively mammals), Ornithomyinae (tribes Olfersiini and Ornithomyini composed of species that mostly parasitise birds) and Hippoboscinae (tribe Hippoboscini with all species in Europe affecting mammals) (Reeves and Lloyd 2019). Phylogenetic studies have indicated a monophyly among Hippoboscoidea members and that the ancestor of this superfamily was a free-living insect feeding on mammal blood (Nirmala et al. 2001; Dittmar et al. 2006; Petersen et al. 2007).

Worldwide, more than 213 hippoboscid species are known (e.g., Maa 1963; Dick 2006; Rahola et al. 2011), and 31 species of Hippoboscidae have been described from Europe (Pape et al. 2015; Nartshuk et al. 2019a; Oboňa et al. 2019b).

Ornithomya comosa (Austen, 1930) (Figs 1, 2), the most recent species found in Europe (see Nartshuk et al. 2019a) and originally described from India (Pusa, Bihar), was first collected from a grey-throated martin, Riparia chinensis (J. E. Gray, 1830) (Austen 1930). The host overview is presented in Table 1. According to Maa (1969a, b, 1977), O. comosa is distributed in India, Nepal (on R. chinensis; Maa (1969a) used the name Riparia paludicola chinensis), and Thailand and Malaysia (on a barn swallow, Hirundo rustica Linnaeus, 1758).

Table 1.
Download as
CSV
XLSX

The overview of hosts of Ornithomya comosa (Austen, 1930).

Host species Countries References
Cecropis daurica Russia Nartshuk et al. (2019b)
Delichon urbicum Kazakhstan, Kyrgyzstan, Russia Doszhanov (1970); Nartshuk et al. (2019a)
Hirundo rustica Japan, Kazakhstan, Kyrgyzstan, Malaysia, Russia, Thailand, Maa (1969a); Doszhanov (1970); Mogi (2014); Nartshuk et al. (2019a)
Otus scops Russia Doszhanov (2003)
Riparia diluta Russia Matyukhin and Gashkov (2020)
Riparia chinensis India, Nepal Austen (1930); Maa (1969a)
Riparia riparia Japan, Kazakhstan, Kyrgyzstan, Russia Doszhanov (1970); Mogi (2014)
Figure 1. 

Ornithomya comosa, imago, dorsal view (left wing removed).

Figure 2. 

Ornithomya comosa, wing.

Subsequently, Doszhanov (1970, 2003) recorded this species from Kazakhstan, Kyrgyzstan and West Siberia of Russia (Novosibirsk), mostly from the host Riparia riparia (Linnaeus, 1758), rarely from H. rustica and Delichon urbicum (Linnaeus, 1758), and also from the Eurasian scops owl, Otus scops (Linnaeus, 1758) of the Strigiformes. Mogi (2014) reported this species from Japan (Honshu, Kyushu and Ryukyu islands on R. riparia and H. rustica hosts). Most recently, Nartshuk et al. (2019a) recorded O. comosa for the first time in Europe from western Russia (Kaliningrad Province, hosts H. rustica and D. urbicum). Further Russian records are from Cecropis daurica (Laxmann, 1769) from Primorskii krai in the Far East (Nartshuk et al. 2019b) and from Riparia diluta (Sharpe & Wyatt, 1893) from Tomsk in west Siberia (Matyukhin and Gashkov 2020). In this study O. comosa is recorded for the first time from Slovakia, demonstrating its further expansion in Central Europe.

A series of new records of louse flies and keds from Slovakia with several new host records is appended to supplement the recent review by Oboňa et al. (2019b). Because the available taxonomic keys for European Hippoboscidae are outdated, we present updated keys covering all species currently known from Europe.

Materials and methods

The key for European genera of Hippoboscidae follows the previous descriptions by Bequaert (1954), Theodor and Oldroyd (1964), and Hutson (1984). Keys for species of European Hippoboscidae follow Falcoz (1926), Povolný and Rosický (1955), Theodor and Oldroyd (1964), Maa (1966, 1969c), Hutson (1981, 1984), Ducháč and Bádr (1998), Farafonova (2001), Petersen et al. (2007), Iwasa and Choi (2013), Nartshuk et al. (2019b), and Salvetti et al. (2020).

In addition, new louse fly specimens from Slovakia were collected by hand on birds caught in mist nets, or keds by hand from humans. The majority of the samples come from the ornithological station “Vtáčí raj – Šalgovské rybníky” (Bird’s Paradise – Šalgov ponds) near the village Uzovský Šalgov (49°05'34.8"N, 21°04'00.4"E, 366 m a.s.l.). The birds were mist-netted in the standardised method (for more information, see Olekšák et al. 2007). Other samples, especially from humans, represent random and non-targeted sampling.

The collected hippoboscids were placed in microvials with 96% ethanol and subsequently identified in the laboratory using determination keys by Povolný and Rosický (1955) and Theodor and Oldroyd (1964). The focus on the local primary hosts follows Oboňa et al. (2019a, b, 2021). The newly recorded species O. comosa (Austen, 1930) was identified by Nartshuk et al. (2019b) using a key modified according Farafonova (2001). The material is deposited in the collection of the Laboratory and Museum of Evolutionary Ecology, Department of Ecology, University of Prešov (LMEE PO). The terminology follows Cumming and Wood (2017).

Results

Key for European genera of Hippoboscidae (updated)

1 Wings fully developed and functional (Figs 3–11) 2
– Wings reduced, with strong veins (Figs 12–16) or absent (either by reduction or loss) 9
2 Tarsal claws simple (Fig. 17), but with a pale basal lobe; humeral callus weak (Figs 21–24), postpronotum rounded, not produced anteriorly as conical lobes 3
– Tarsal claw bifid and with a pale basal lobe (Fig. 18); humeral callus strong, postpronotum rounded, pair of conical lobes on either side of head (Figs 26–28), on birds 5
3 Wing with one or two cross-veins; R4+5 well separated from C until apex; on mammals (Figs 4, 5) 4
– Wings with three cross-veins enclosing cells posterior to radial veins; apical 1/2 of vein R4+5 running very close to C (Fig. 3); on birds Ornithoica
4 Wing clear and hyaline, with only one cross-vein (Fig. 4); head broader than long; thorax markedly flattened (Figs 21–25); on mammals Lipoptena
– Wing distinctly crenulated and tinted, with two cross-veins (Fig. 5); head not broader than long; thorax not so markedly flattened; on mammals Hippobosca
5 Wing with three cross-veins posterior to radial veins (Figs 6, 7); scutellum with four or more strong marginal setae (Figs 32–37) 6
– Wing with one or two cross-veins posterior to radius (Figs 8–11); scutellum at most with two strong marginal setae (Figs 31, 38) 7
6 Vein R2+3 with apical 3/5 fused with C; wing membrane entirely bare (Fig. 6) Ornithophila
– Vein R2+3 well separated from C except at apex; wing membrane usually with microtrichia (Fig. 7) Ornithomya
7 Wing with only one cross-vein (Fig. 8) Pseudolynchia
– Wing with two cross-veins (Figs 9–11) 8
8 Scutellum with two strong setae (Fig. 19) Icosta
– Scutellum with setulae (Fig. 31) Olfersia
9 Wing long and narrow, at least 6 × as long as wide and twice as long as head and thorax (Fig. 12); female abdomen with strong spiniform setae in posterolateral area; male abdomen without spiniform setae Stenepteryx
– Wing short and broad, at most 3 × as long as wide and ~ 1.5 × as long as head and thorax (Figs 13–16); tip of wing usually attenuated, C reaching to about 0.75 length of anterior wing margin; female abdomen only with short fine setae in posterolateral area Crataerina
10 Wings either reduced to a veinless knob or broken off; haltere absent Melophagus
– Wings absent, leaving a broad flat veined stump; haltere present Lipoptena

Keys to species of European genera of Hippoboscidae (updated)

The genus Crataerina von Olfers, 1816

1 Wing shorter than hind femur; wing tip broadly rounded (Fig. 13) Crataerina obtusipennis Austen, 1926
– Wing longer than hind femur 2
2 Wing more than twice as long as hind femur (Fig. 14); male abdomen with tergites 3 and 4 one-third as wide as abdomen and tergite 5 nearly as wide as abdomen; female abdomen with long and thick setae on posterior margin and with group of fine and long setae ventral to genital opening Crataerina melbae (Rondani, 1879)
– Wing < 2 × as long as hind femur; male abdominal tergites small or absent; all setae on posterior margin of female abdomen short and uniform in length 3
3 Wing length 2 × as long as hind femur, extended beyond posterior end of abdomen; distal 1/2 of trailing edge of wing strongly concave (Fig. 15) Crataerina acutipennis Austen, 1926
– Wing length 1.3–1.5 × as long as hind femur, not extended beyond posterior end of abdomen; distal 1/2 of trailing edge of wing not strongly concave (Fig. 16) Crataerina pallida (Olivier in Latreille, 1811)

Host-parasite associations: Aves (Apodiformes, Passeriformes).

The genus Hippobosca Linnaeus, 1758

1 Vein R2+3 meets vein C at same place as R1, shorter than distal section of R4+5 (measured from transverse vein r-m); front edge of thorax, with a transverse row of short thick setae; scutellum almost rectangular, with 2 dark and 3 light spots; wing length 7.0–8.0 mm Hippobosca variegata Megerle, 1803
– Vein R2+3 end into vein C clearly separated from R1, length is approximately equal to distal section of vein R4+5; thorax without mentioned setae and characters; wing length shorter than 7.0–8.0 mm 2
2 Dark brown specimens; veins of wings dark pigmented; scutellum white in middle, dark on sides; wing length 6.0–8.5 mm (Fig. 5) Hippobosca equina Linnaeus, 1758
– Pale specimens; veins of wings light, only transverse veins and sections of longitudinal veins adjoining them are completely or partially dark; scutellum almost entirely white, sometimes with dark edge; wing length 5.0–6.0 mm Hippobosca longipennis Fabricius, 1805

Host-parasite associations: Aves (Accipitriformes), Mammalia (Carnivora, Cetartiodactyla, Perissodactyla).

The genus Icosta Speiser, 1905

1 Large dark specimens; wing length 5.0–6.0 mm 2
– Small pale specimens; wing length 3.5–4.0 mm 3
2 Venter of hind femur bare; palp length more than twice width; microtrichia covering most of wing, but apical 1/2 of cell Cu+1A and entire 2A bare (Fig. 10); prescutum with setae reaching mesonotal suture; pale yellowish specimens; abdomen without tergite 3 (Fig. 39) Icosta minor (Bigot in Thomson, 1858)
3 Venter of hind femur densely setose except near base; length of palp ~ 1.5 × width; wing with microtrichia covering most of its surface, including anterior 1/3 of cell 2A (Fig. 9); prescutum with short setae in several rows not reaching mesonotal suture, smaller and disordered short postalar setae in several rows (Fig. 19); dark specimens; abdomen with distinct tergite 3 (Fig. 40) Icosta ardeae (Macquart, 1835)
– Enigmatic species, so far known from a single specimen; prescutum with one row of fine longer setae that reach mesonotal suture, setae in one row (Fig. 20) Icosta massonati (Falcoz, 1926)

Host-parasite associations: Aves (Passeriformes, Pelecaniformes).

The genus Lipoptena Nitsch, 1818

1 Wing length 6.0 mm 2
– Wing length 4.0 mm or less 3
2 Body length 5.0–6.0 mm; scutellum with 6–8 setae; thorax mostly with 30–35 setae on each side, 9 postalar setae on each side (Fig. 21) Lipoptena cervi (Linnaeus, 1758)
– Body length 4.5–5.5 mm; scutellum with 8–10 setae; thorax mostly with 50–60 setae on each side, 6 postalar setae on each side (Fig. 22) Lipoptena couturieri Séguy, 1935
3 Wing length 4.0 mm; body length 2.8–3.2 mm; scutellum with 4–6 setae; thorax mostly with 8–12 strong setae on each side, 4 postalar setae on each side (Fig. 23) Lipoptena fortisetosa Maa, 1965
– Wing length < 4.0 mm; scutellum with 6 setae; thorax mostly with 25 or more setae on each side, 3 or 4 postalar setae on each side 4
4 Wing length 3.0–3.2 mm; body length 3.0–3.75 mm; body pale; thorax mostly with 30–35 setae on each side (Fig. 24) Lipoptena capreoli Rondani, 1878
– Wing length < 3.0 mm body length 2.3–2.6 mm; body extremely dark; thorax mostly with 25–30 soft setae on each side (Fig. 25) Lipoptena arianae Maa, 1969

Host-parasite associations: Mammalia (Cetartiodactyla, Carnivora).

The genus Melophagus Latreille, 1802

1 Palps almost as long as head, in rest position completely covering proboscis (Fig. 29); parafrontalia almost touching in middle, mediovertex reduced; parafrontalia covered with numerous setae; tergal plates completely absent in male, in females only remnants of tergal plate 7 Melophagus ovinus (Linnaeus, 1758)
– Palps shorter than head, ~ 1/3 of head length, proboscis always protruding (Fig. 30); parafrontalia with few setae on inner margin; in males tergal plate 6 present, in females plates 6 and 7 present Melophagus rupicaprinus Rondani, 1879

Host-parasite associations: Mammalia (Carnivora, Cetartiodactyla, Perissodactyla).

Figures 3–16. 

3 Ornithoica turdi, wing 4 Lipoptena cervi, wing 5 Hippobosca equina, wing 6 Ornithophila metallica, wing 7 Ornithomya avicularia, wing 8 Pseudolynchia canariensis, wing 9 Icosta ardeae, wing (with the border of microtrichia) 10 Icosta minor, wing (with the border of microtrichia) 11 Olfersia spinifera, wing 12 Stenepteryx hirundinis, wing 13 Crataerina obtusipennis, wing 14 Crataerina melbae, wing 15 Crataerina acutipennis, wing 16 Crataerina pallida, wing.

Figures 17–24. 

17 Lipoptena cervi, tarsal claws 18 Ornithomya avicularia, tarsal claws 19 Icosta ardeae, thorax 20 Icosta massonati, thorax 21 Lipoptena cervi, thorax 22 Lipoptena couturieri, thorax 23 Lipoptena fortisetosa, thorax 24 Lipoptena capreoli, thorax. Abbreviations: ms – mesonotal suture, pos – postalar setae, ps – prescutum, sc – scutellum.

Figure 25–30. 

25 Lipoptena arianae, thorax 26 Olfersia spinifera, thorax 27 Olfersia fumipennis, thorax 28 Pseudolynchia canariensis, frontal part of thorax 29 Melophagus ovinus, head with palps 30 Melophagus rupicaprinus, head with palps. Abbreviations: ah – alar horns, pos – postalar setae, ps – prescutum, sc – scutellum.

The genus Olfersia Wiedemann, 1830

1 Head on posterior margin with 3 distinct protrusions and deep indentations between postvertex and posterior orbit; postvertex protrudes noticeably backwards over posterior orbites; tip of alar horns directed obliquely forward (Fig. 26); section of C between Sc and R1 is shorter than section between R1 and R2-3. First basal cell is ca. as long as section of R4+5 distal to transverse vein r-m (Fig. 11); female pygidium separate and finger-shaped Olfersia spinifera (Leach, 1817)
– Head protruding only a little over posterior orbit; tip of alar horns blunt and serrated (Fig. 27); sections of C between Sc and R1 longer than section between R1 and R2+3. First basal cell is significantly shorter than section of R4+5 distal to transverse vein r-m; female pygidium short and fused Olfersia fumipennis (Sahlberg, 1886)

Host-parasite associations: Aves (Accipitriformes, Gaviiformes, Charadriiformes, Pelecaniformes, Suliformes).

The genus Ornithoica Rondani, 1878 – one species only

Ornithoica turdi (Olivier in Latreille, 1812)

Figs 3, 32

Host-parasite associations: Aves (Passeriformes).

The genus Ornithomya Latreille, 1802

1 C sector between R1 and R2+3 not longer than sector between R2+3 and R4+5 2
– C sector between R1 and R2+3 longer than between R2+3 and R4+5 3
2 Brown spots on ventral side of head do not reach jugular setae; scutellum with 4 setae (Fig. 33); wing in hind part with 4 longitudinal stripes of microtrichia; adult 1.9–2.5 mm Ornithomya fringillina Curtis, 1836
– Triangular brown spots on ventral side of head are sharp (Fig. 41), narrowed and reach jugular setae, which are situated on sides of occipital foramen; scutellum usually with 6 or more setae (Fig. 34); wing in hind part with 3 longitudinal stripes of microtrichia; adult 2.1–2.6 mm Ornithomya chloropus Bergroth, 1901
3 Wing dark and all surface evenly covered by microtrichia; scutellum with 10–12 setae (Fig. 35); all body covered by setae; adult 2.0–2.5 mm Ornithomya comosa (Austen, 1930)
– Surface of wing covered by microtrichia no more than 2/3, base of wing without of microtrichia 4
4 Wing with microtrichia only on apex and in cell m1; scutellum with 8 setae (Fig. 36); abdomen on apex with numerous long setae; adult 3.0–3.5 mm Ornithomya avicularia (Linnaeus, 1758)
– Microtrichia covered nearly all wing except base or only cells r3 and m2, long setae absent on apex of abdomen 5
5 Wing dark with intensive microtrichia; thorax with 16–18 mesopleural setae on each side; scutellum with 6 setae (Fig. 37); abdomen similar as in following species; vibrissal spines almost missing Ornithomya biloba Dufour, 1827
– Wing light with extensive microtrichia, thorax with 6–10 mesopleural setae on each side; scutellum with 4 (6) setae; abdomen (Figs 43, 44); vibrissal spines present (Fig. 42) Ornithomya rupes Hutson, 1981

Host-parasite associations: Aves (Accipitriformes, Anseriformes, Falconiformes, Passeriformes, Pelecaniformes, Strigiformes), Mammalia (Primates).

The genus Ornithophila Rondani, 1879

1 4.0–5.0 mm; scutellum dark, except for a narrow, light stripe at base; male tergal plates 3 and 4 as wide as scutellum Ornithophila metallica (Schiner, 1864)
– 5.0–7.0 mm; scutellum with a broad yellow band at base and a yellow triangle at apex; male tergal plates 3 and 4 as wide as a little more than 1/2 width of scutellum Ornithophila gestroi (Rondani, 1878)

Host-parasite associations: Aves (Passeriformes).

The genus Pseudolynchia Bequaert, 1926

1 Hind scutellar margin in dorsal view straight or nearly straight (Fig. 38); interantennal area of frons as wide as or rarely slightly narrower than its distance to eye; prescutum with 20–30 long pale fine setae and before which with 2 or 3 series of shorter ones (Fig. 28); mid tarsus with group of peg-like modified spines under segment 1 at base Pseudolynchia canariensis (Macquart in Webb & Berthelot, 1839)
– Hind scutellar margin in dorsal view distinctly curved; interantennal area of frons always much narrower than its distance to eye; prescutum with 12–18 long, fairly robust and generally black setae and before which, with 1 or 2 series of shorter ones; mid tarsus with only pointed setae under segment 1 at base Pseudolynchia garzettae (Rondani, 1879)

Host-parasite associations: Aves (Accipitriformes).

The genus Stenepteryx Leach, 1817 – one species only

Stenepteryx hirundinis (Linnaeus, 1758)

Fig. 12

Host-parasite associations: Aves (Passeriformes: Hirundinidae).

Figures 31–38. 

31 Olfersia fumipennis, scutellum 32 Ornithoica turdi, scutellum 33 Ornithomya fringillina, scutellum 34 Ornithomya chloropus, scutellum 35 Ornithomya comosa, scutellum 36 Ornithomya avicularia, scutellum 37 Ornithomya biloba, scutellum 38 Pseudolynchia canariensis, scutellum.

Figures 39–44. 

39 Icosta minor, ♀ abdomen, dorsal and ventral view 40 Icosta ardeae, ♀ abdomen, dorsal and ventral view 41 Ornithomya chloropus, head, ventral view 42 Ornithomya rupes, head, ventral view 43 Ornithomya rupes, ♀ abdomen, dorsal and ventral view 44 Ornithomya rupes, ♂ abdomen, dorsal and ventral view. Abbreviations: tbs – triangle brown spot, tp – tergal plate, vs – vibrissal spines.

Discussion

Updated keys to eleven European hippoboscid genera comprising 31 species are provided. We hope that they will contribute as a tool for determining European specimens of the most fascinating and neglected group of blood-feeding ectoparasites from the family Hippoboscidae (see Bezerra-Santos and Otranto 2020).

The recent checklist of louse flies of the family Hippoboscidae from Slovakia (see Oboňa et al. 2019b) includes 19 species; the present paper increases this list to 20 species. Four new host-parasite associations from Slovakia are also recorded (O. avicularia on the reed bunting and European starling, and O. fringillina on the barn swallow and the lesser whitethroat; see also Table 2).

Table 2.
Download as
CSV
XLSX

An overview of recorded host-parasites associations.

Parasites Hosts
Hippobosca equina Mammalia: Primates: Homo sapiens*
Lipoptena cervi Mammalia: Primates: Homo sapiens*
Lipoptena fortisetosa Mammalia: Primates: Homo sapiens*; Aves: Parus major*
Ornithomya avicularia Aves: Passeriformes: Emberiza schoeniclus, Hirundo rustica, Panurus biarmicus, Sturnus vulgaris
Ornithomya biloba Aves: Passeriformes: Hirundo rustica, Riparia riparia
Ornithomya comosa Aves: Passeriformes: Riparia riparia
Ornithomya fringillina Aves: Passeriformes: Curruca curruca, Hirundo rustica
Stenepteryx hirundinis Aves: Passeriformes: Delichon urbicum

* Accidental association, parasite species do not complete development on this host.

Of a total of 20 Slovakian hippoboscid species, 12 are native. The remaining eight species (Hippobosca longipennis Fabricius, 1805, H. variegata Megerle, 1803, Icosta minor (Bigot, 1858), Olfersia fumipennis (Sahlberg, 1886), Ornithoica turdi (Latreille, 1812), Ornithophila metallica (Schiner, 1864), Pseudolynchia canariensis (Macquart, 1839), and the newly recorded Ornithomyia comosa (Austen, 1930) have been recorded from Slovakia based on very few records due to their hosts being usually occasional visitors (Oboňa et al. 2019b).

According to Nartshuk et al. (2019a), there are two possible explanations for the current distribution of O. comosa: O. comosa migrates with adult swallows from West Siberia or Kazakhstan to western Russia or O. comosa has always or for a long time been present in western Russia, but it has not been previously collected. For the European records of O. comosa, migrating swallows cannot bring O. comosa from Africa, as O. comosa does not occur there, but some H. rustica do, spending the winter in Asia, where O. comosa occurs. We also assume that records by Doszhanov (1970, 2003) from Kazakhstan and Kyrgyzstan could represent a bridge between the East Asian-Australasian Flyway and the African-Eurasian Flyway (see Boere and Stroud 2006). In this area, parasites can be transferred between hosts from East Asian countries (e.g., India, Nepal, Thailand, Malaya, Japan) to western Siberia, western Russia, and Europe. However, the question is whether O. comosa has already adapted to local conditions and become a native species in Europe or will it continue to be only an occasionally introduced species.

The collection dates by Austen (1930) from India (February–April), King (1969) from Thailand (Bangkok) (ectoparasites collected during “winter”), and Mogi et al. (2002) from Japan (September–December) suggest that O. comosa is active mainly in autumn and winter (native populations). However, the findings from Kazakhstan by Doszhanov (1970) are from the period May–October, and the most recent records from the Kaliningrad region (Nartshuk et al. 2019a) correspond to the findings presented in this article, i.e., July and August. Therefore, we believe that the parasite does not have to come from the spring migration but, on the contrary, from the summer/autumn migration (possibly also from the Kaliningrad area). A similar phenomenon is recorded for the non-native species Ornithoica turdi (Olivier in Latreille, 1811) (e.g., records from Vienna from August, see Zittra et al. (2020)) transported by hosts from wintering grounds in Africa. The relatively late record after migration from the wintering grounds has two possible explanations. The first is that these parasites are able to live for more than two months (see Chalupský 1980). The second is that it could be a hatched fly, and therefore it may not be a casual traveller from Africa (O. turdi) or Asia (O. comosa), but that it is already breeding here (as a native species?). This is also indirectly confirmed by the negative findings from the spring migration.

Acknowledgements

We thank the subject editor and the anonymous reviewers for their valuable and constructive comments on the first version of the manuscript. The study was supported by the Slovak Research and Development Agency under the contract No. APVV-16-0411, by the grant VEGA 1/0876/21 (J. Oboňa, M. Hromada), by the Grant Agency of University of Prešov in Prešov under the contract No. GaPU 1/2022 (K. Fogašová), and by the Ministry of Culture of the Czech Republic through the institutional financing of long-term conceptual development of a research institution (the Silesian Museum, MK000100595) (J. Roháček).

References

  • Bequaert JC (1954) The Hippoboscidae or louse-flies (Diptera) of mammals and birds. Part II. Taxonomy, evolution and revision of American genera and species. Entomologica Americana 34: 1–232. [New Series]
  • Boere GC, Stroud DA (2006) The flyway concept: what it is and what it isn’t. Waterbirds around the world. In: Boere GC, Galbraith CA, Stroud DA (Eds) The Stationary Office, Edinburgh, Scotland, 40–47. [940 pp]
  • Chalupský J (1980) Hippoboscidae – Klošovití. In: Chvála M (Ed.) Krevsající mouchy a střečci. Fauna ČSSR, 22, Academia, Praha, 447–478. [In Czech]
  • Cumming JM, Wood DM (2017) Adult morphology and terminology. In: Kirk-Spriggs A, Sinclair BJ (Eds) Afrotropical Diptera. Vol. 1. South African National Biodiversity Institute, Pretoria, 89–133.
  • Dick CW (2006) Checklist of World Hippoboscidae (Diptera: Hippoboscoidea). Field Museum of Natural History, Chicago, 7 pp.
  • Dittmar K, Porter ML, Murray S, Whiting MF (2006) Molecular phylogenetic analysis of nycteribiid and streblid bat flies (Diptera: Brachycera, Calyptratae): implications for host associations and phylogeographic origins. Molecular Phylogenetics and Evolution 38(1): 155–170. https://doi.org/10.1016/j.ympev.2005.06.008
  • Doszhanov TN (1970) Ornithomyia comosa Austen (Diptera, Hippoboscidae), a new species for the USSR and the Palaearctic Region. Parazitologiia 4(1): 82–83. [In Russian]
  • Doszhanov TN (2003) Mukhi-krovososki (Diptera, Hippoboscidae) Palearktiki [Louse flies (Diptera, Hippoboscidae) of the Palaearctic Region]. Almaty, 277 pp. [In Russian]
  • Ducháč V, Bádr V (1998) Několik poznámek k druhu Lipoptena fortisetosa (Diptera: Hippoboscidae) [Several remarks of the species Lipoptena fortisetosa (Diptera: Hippoboscidae)]. Východočeský sborník přírodovědný práce a studie 6: 117–122. [In Slovak]
  • Falcoz L (1926) Diptères pupipares. Faune de France 14 - Diptères Pupipares. Fédération française des Sociétés de sciences naturelles (FFSSN), Paris, 53 pp.
  • Farafonova GV (2001) Fam. Hippoboscidae ‒ louse flies. In: Lehr PA (Ed.) Key to the insects of Russian Far East. 6. Diptera and Syphonaptera. Pt 2. Dalnauka, Vladivostok, 252‒258. [In Russian]
  • Hutson AM (1981) A new species of the Ornithomya biloba-group (Dipt., Hippoboscidae) from Crag Martin (Ptyonoprogne rupestris)(Aves, Hirundinidae). Mitteilungen der Schweizerischen Entomologischen Gesellschaft = Bulletin de la Société entomologique suisse 54: 157‒162.
  • Hutson AM (1984) Keds, flat-flies and bat-flies. Diptera, Hippoboscidae and Nycteribiidae. Handbooks for the Identification of British Insects 10(7): 1–40.
  • Iwasa M, Choi CY (2013) Contribution to the knowledge of the Hippoboscidae (Diptera) from the Republic of Korea. Journal of Medical Entomology 50(2): 231–236. https://doi.org/10.1603/ME12179
  • Maa TC (1966) On the genus Pseudolynchia Bequaert. Pacific Insects Monograph 10: 125–138.
  • Maa TC (1969c) Revision of Icosta (= Lynchia Auctt.) with erection of a related genus Phthona (Diptera: Hippoboscidae). Pacific Insects Monograph 20: 25–203.
  • Maa TC (1977) Family Hippoboscidae. A Catalog of the Diptera of the Oriental Region 3: 407–418.
  • Matyukhin AV, Gashkov SI (2020) First data on louse-fleas (Diptera, Hippoboscidae) of Tomsk. In: Ovtshinnikova OG, Shamshev IV (Eds) XI All-Russian Dipterological Symposium (with international participation), Voronezh, 24–29 August 2020: Materials. – St. Petersburg: Russian entomological society: LEMA Publishers, Voronezh, 132–135. [318 pp] https://doi.org/10.47640/978-5-00105-586-0_2020_132
  • Mogi M (2014) Family Hippoboscidae. In: Nakamura T, Saigusa T, Suwa M (Eds) Catalogue of the insects of Japan 8(2): 742–747.
  • Mogi M, Mano T, Sawada I (2002) Records of Hippoboscidae, Nycteribiidae and Streblidae (Diptera) from Japan. Medical Entomology and Zoology 53(Supplement 2): 141–165. https://doi.org/10.7601/mez.53.141
  • Nartshuk EP, Matyukhin AV, Shapoval AP (2019a) First record of the parasitic louse fly Ornithomya comosa (Diptera: Hippoboscidae) in Europe and western Russia. Zoosystematica Rossica 28(2): 356–359. https://doi.org/10.31610/zsr/2019.28.2.356
  • Nartshuk EP, Matyukhin AV, Shokhrin VP, Markovets MY (2019b) New records of ornithophilous louse-flies (Diptera: Hippoboscidae: Ornithomyinae) from the Russian Far East. Far Eastern Entomologist 384: 15–20. https://doi.org/10.25221/fee.384.4
  • Nartshuk EP, Matyukhin AV, Shapoval AP, Markovets MY, Tolstenkov OO (2020) Louse Flies (Diptera, Hippoboscidae) on the Courish Spit (Kaliningrad Province, Russia). Entomological Review 100(2): 231–238. https://doi.org/10.1134/S0013873820020128
  • Nirmala X, Hypša V, Žurovec M (2001) Molecular phylogeny of Calyptratae (Diptera: Brachycera): the evolution of 18S and 16S ribosomal rDNAs in higher dipterans and their use in phylogenetic inference. Insect Molecular Biology 10(5): 475–485. https://doi.org/10.1046/j.0962-1075.2001.00286.x
  • Oboňa J, Krišovský P, Hromada M (2019a) Short-term faunistic sampling of Louse flies (Diptera: Hippoboscidae) from Drienovec Bird Ringing Station, Slovakia. Biodiversity & Environment 11(2): 4–9.
  • Oboňa J, Sychra O, Greš S, Heřman P, Manko P, Roháček J, Šestáková A, Šlapák J, Hromada M (2019b) A revised annotated checklist of louse flies (Diptera, Hippoboscidae) from Slovakia. ZooKeys 862: 129–152. https://doi.org/10.3897/zookeys.862.25992
  • Oboňa J, Greš S, Krišovský P, Hromada M (2021) Faunistic records and new parasite-host associations of Louse flies (Diptera: Hippoboscidae) from Sabinov, Slovakia. Biodiversity & Environment 12(1): 74–79.
  • Olekšák M, Pjenčák P, Fulín M, Matis Š (2007) Bird nesting community of the Drienovec bird Ringing Station – CES programme. Tichodroma 19: 41–47.
  • Pape T, Beuk P, Pont A, Shatalkin A, Ozerov A, Woźnica A, Merz B, Bystrowski C, Raper C, Bergström C, Kehlmaier C, Clements D, Greathead D, Kameneva E, Nartshuk E, Petersen F, Weber G, Bächli G, Geller-Grimm F, Van de Weyer G, Tschorsnig H, de Jong H, van Zuijlen J, Vaňhara J, Roháček J, Ziegler J, Majer J, Hůrka K, Holston K, Rognes K, Greve-Jensen L, Munari L, de Meyer M, Pollet M, Speight M, Ebejer M, Martinez M, Carles-Tolrá M, Földvári M, Chvála M, Barták M, Evenhuis N, Chandler P, Cerretti P, Meier R, Rozkosny R, Prescher S, Gaimari S, Zatwarnicki T, Zeegers T, Dikow T, Korneyev V, Richter V, Michelsen V, Tanasijtshuk V, Mathis W, Hubenov Z, de Jong Y (2015) Fauna Europaea: Diptera – Brachycera. Biodiversity Data Journal 3: e4187. https://doi.org/10.3897/BDJ.3.e4187
  • Petersen FT, Damgaard J, Meier R (2007) DNA taxonomy: How many DNA sequences are needed for solving a taxonomic problem? The case of two parapatric species of louse flies (Diptera: Hippoboscidae: Ornithomya Latreille, 1802). Arthropod Systematics & Phylogeny 65(2): 119–125.
  • Povolný D, Rosický B (1955) Faunisticko-bionomický nástin klošovitých (Hippoboscidae, Diptera) z území ČSR. Zoologické a entomologické listy 4: 5–20. [In Czech]
  • Rahola N, Goodman SM, Robert V (2011) The Hippoboscidae (Insecta: Diptera) from Madagascar, with new records from the “Parc National de Midongy Befotaka”. Parasite 18(2): 127–140. https://doi.org/10.1051/parasite/2011182127
  • Salvetti M, Bianchi A, Marangi M, Barlaam A, Giacomelli S, Bertoletti I, Roy L, Giangaspero A (2020) Deer keds on wild ungulates in northern Italy, with a taxonomic key for the identification of Lipoptena spp. of Europe. Medical and Veterinary Entomology 34(1): 74–85. https://doi.org/10.1111/mve.12411
  • Theodor O, Oldroyd H (1964) Hippoboscidae. In: Lindner E (Ed.) Die Fliegen der Palaearktischen Region 12. Museum Wiesbaden Nafurwillenschaltliche Sammlung, Stuttgards, 1–70. [98 pp]
  • Zittra C, Schoener ER, Wagner R, Heddergott M, Duscher GG, Fuehrer HP (2020) Unnoticed arrival of two dipteran species in Austria: The synanthropic moth fly Clogmia albipunctata (Williston, 1893) and the parasitic bird louse fly Ornithoica turdi (Olivier in Latreille, 1811). Parasitology Research 119(2): 737–740. https://doi.org/10.1007/s00436-019-06563-9
login to comment