New faunistic records and host-parasite interactions of louse flies (Diptera: Hippoboscidae) from a community of birds collected by mist-netting in the Spanish Central System

Around 31 hippoboscid species have been described in Europe and up to 20 species (distributed in 11 genera and three subfamilies) have been recorded from the Iberian Peninsula and the Balearic and Canary islands (‍Sánchez & Carles-Tolrá, 2007; ‍Oboňa et al., 2019a, ‍2022). The Spanish fauna of Hippoboscidae includes 15 species parasitizing mostly birds and 5 that feed primarily on mammals. The best-known species in Spain are the forest fly Hippobosca equina Linnaeus, 1758, a ked that feeds on horses and other large mammals, and among avian-feeding species, Stenepteryx hirundinis (Linnaeus, 1758) and Pseudolynchia canariensis (Macquart in Webb & Berthelot, 1839), that are most likely the two most prevalent species parasitizing swifts and pigeons, respectively (‍González, 2022). However, very scarce information is available from other avian hosts.

Bird ringing stations provide an excellent opportunity to study the fauna of Hippoboscidae parasitizing bird species. In fact, most data on the fauna of louse flies comes from bird-ringing surveys. In this pilot study, we recorded data on louse flies from avian hosts in one of the main mountain ranges in the Iberian Peninsula.

The study was carried out between the summer and autumn seasons of 2021 and 2022 at two ringing stations located in the Central System mountains in Madrid, Spain (Collado Cerrado, Canencia: 40º52’ N, 03º45’ W, and Arroyo de la Laguna, Somosierra: 41º09’ N, 03º36’ W, 1.480 and 1.530 m a.s.l., respectively). Birds were captured using mist nets and were placed individually in cotton bags to avoid mixing ectoparasites among birds. Louse flies were collected by hand from birds and stored in capped tubes containing 70% ethanol for further identification in the laboratory. Not all louse flies could be collected, as is common in similar studies (‍Oboňa et al., 2019b). Louse fly specimens were identified to species level under a stereomicroscope following updated identification keys recently published for European Hippoboscidae (‍Oboňa et al., 2022).

MATERIAL EXAMINED. New host-parasite interactions for Spain are denoted with an asterisk (*).

Ornithoica turdi (Olivier in Latreille, 1811).

1 ♂ ex European robin Erithacus rubecula (Linnaeus, 1758), 05.09.2021; 1 ♂ ex Melodious warbler Hippolais polyglotta (Vieillot, 1817)*, 27.08.2022; 1 ♀ ex Red-backed shrike Lanius collurio Linnaeus, 1758*, 30.07.2022.

Ornithomya avicularia (Linnaeus, 1758)

1 ♀ ex Whitethroat Curruca communis (Latham, 1787)*, 16.07.2022; 1 ♂ ex Barn swallow Hirundo rustica Linnaeus, 1758, 12.08.2021; 2 ♀♀ ex Blackbird Turdus merula Linnaeus, 1758, 28.06.2022.

Ornithomya fringillina (Curtis, 1836)

1 ♂, 1 ♀ ex Rock bunting Emberiza cia Linnaeus, 1766*, 28.08.2021, 24.07.2022; 1 ♀ ex Melodious warbler Hippolais polyglota*, 24.07.2021; 5 ♀♀ ex Woodchat shrike Lanius senator Linnaeus, 1758*, 16.07.2022, 20.08.2022; 2 ♀♀ ex Dunnock Prunella modularis (Linnaeus, 1758)*, 28.08.2021, 24.07.2022; 1 ♀ ex Stonechat Saxicola rubicula (Linnaeus, 1766)*, 12.09.2021.

Ornithomyia sp. (specimen damaged)

1 ♀ Blackbird Turdus merula 26.06.2021.

Ornithophila metallica (‍Schiner, 1864)

1 ♀ ex Crested tit Lophophanes cristatus (Linnaeus, 1758)*, 24.07.2021; 2 ♂♂ ex Dunnock Prunella modularis Linnaeus, 1758*, 19.07.2021; 1 ♂ ex Western orphean warbler Curruca hortensis (J.F. Gmelin, 1789)*, 24.07.2021; 1 ♀ ex Blackbird Turdus merula, 12.08.2022; 1 ♀ ex Song thrush Turdus viscivorus Linnaeus, 1758*, 12.06.2022.

In total, four louse fly species, all of the subfamily Ornithomyinae, were identified (Ornithomya fringillina, n = 11; Ornithophila metallica, n = 6; Ornithomya avicularia, n = 4; and Ornithoica turdi, n = 3) (Fig. 1). They were parasitizing 13 avian host species between June and September, with higher collection numbers in July. The most parasitized avian species was the Woodchat shrike - Lanius senator (n = 5), followed by Dunnock- Prunella modularis (n = 4), Blackbird (n = 4), Melodious warbler- Hippolais polyglotta (n = 2) and the remaining nine hosts (n = 1).

Ornithomya fringillina and O. metallica were parasitized by five species each and O. turdi and O. avicularia by three each. Ornithophila metallica parasitized mostly sedentary or short distance facultative migrant bird species, except Curruca hortensis that winters in equatorial Africa, while the other parasitized species are long or short distance migrants, except T. merula, E. cia and S. rubicula, with a more sedentary character in the study area.

The four louse flies collected are considered polyxenous species attacking multiple bird species (‍Droz & Haenni, 2011; ‍Nartshuk & Matyukhin, 2019; ‍Lehikoinen et al., 2021). Ornithomyia avicularia, O. fringillina and O. metallica are common louse fly species reported across many European countries (‍Oboňa et al., 2019a). These species have been classified as broad host range species preferring several avian hosts, although a notable pattern in their host preference, which was influenced not only by the host size but also by the habitat and host breeding strategy, has been recently attributed to O. avicularia and O. fringillina (‍Lehikoinen et al., 2021). It is also interesting to note that the occurrence of the previous two species varies depending on the migratory status (‍Santolíková et al., 2022). Despite the low numbers collected in the present study, our data agree with previous studies showing that O. fringillina is more common in long-distance migrants, whereas O. metallica seems to be harbored mostly by sedentary bird species. On the contrary, our study corroborates that the presence of O. turdi is restricted to Southern Europe regions (‍Oboňa et al., 2019a), as they are widely distributed in Africa, but the number of records of this species is also increasing in Central Europe during the last years (‍Droz & Haenni, 2011).

The Spanish fauna of Hippoboscidae and their hosts was last reviewed by Cordero del Campillo et al. (‍1994), and since then very few studies have been published (e.g., ‍Carles-Tolrá, 1998, ‍2001); therefore, most records in our study represent new host-parasite interactions of the four louse fly species recorded in the country. The study of louse flies should be promoted in southern Europe, where there is a limited understanding of their distribution, bio-ecology and role as potential vectors of infectious diseases.