A revised annotated checklist of louse flies (Diptera, Hippoboscidae) from Slovakia

Abstract The list of all known locality and host records from the literature on louse flies from Slovakia are summarized, with the addition of new collection data. New locality data are provided for five species. Three species are added to the Slovakian list: Icostaminor (Bigot in Thomson, 1858), which was erroneously cited for Moravia instead of Slovakia in the previous checklist, and Ornithophilametallica (Schiner, 1864) and Ornithomyachloropus (Bergroth, 1901), which were overlooked from the last checklist. As a result, the louse fly fauna of Slovakia increases to 19 species: 12 autochtonous species and seven rare, non-native species only occasionally imported to Slovakia or migrating to the country with their hosts. This is by far the largest regional fauna of Hippoboscidae in Central Europe, and matches the richest southern European faunas. In total, 78 host-parasite associations concerning 46 bird-host species from eight orders and nine species of mammals, including humans, have been found from a literature review in Slovakia. Two host-parasite associations are reported from Slovakia for the first time: Ornithomyaavicularia (Linnaeus, 1758) on Prunellamodularis (Linnaeus, 1758) (Aves: Prunellidae) and Lipoptenafortisetosa Maa, 1965 on Homosapiens Linnaeus, 1758 (Mammalia: Hominidae).


Introduction
Flies in the family Hippoboscidae, known as 'louse flies' or 'keds', belong among the Diptera and are a group of obligate parasites of mammals and birds (Rahola et al. 2011). All species are macrolarviparous, with females retaining the larva in the uterus until the end of the third instar; the three larval instars feed on secretions from the maternal accessory glands. The stage at which larviposition occurs represents a prepupal larva (e.g., Mehlhorn 2016). The larva (or pupa) is deposited in birds' nests or on the hair of a mammalian host, but sometimes it is deposited on the ground by the female (e.g., Halos et al. 2004). Adults of both sexes are blood sucking and are known to act as vectors of many infectious agents, such as protozoa, bacteria, helminths, and possibly also viruses (e.g., Baker 1967, Kečera 1983, Halos et al. 2004, Liu et al. 2016, Skvarla and Machtinger 2019. Some species are host-specific, whereas others feed on a wide array of hosts (e.g., Ibáñez-Bernal et al. 2015, Mehlhorn 2016, Veiga et al. 2018.

Materials and methods
Samples of Hippoboscini, Lipoptenini, and Ornithomyini came from unidentified material in the collections of the Laboratory and Museum of Evolutionary Ecology, Department of Ecology, University of Presov (LMEE PO); of the Department of Entomology, Silesian Museum, Opava (SMOC); and of the Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences Brno (VFU).
Published host records: Canis familiaris (see Chalupský 1980, Chalupský andPovolný 1983). Comments: A rare and non-native species in Central Europe, distributed in the Mediterranean and Afrotropical regions. Up until now, only two individuals have been recorded in Slovakia, in 1953(Chalupský 1980, Straka and Majzlán 2010. It is an ectoparasite of dogs; occasionally it can occur also on other predatory mammals or ungulates (Chalupský 1980). Occassionally, it can be imported via human activities (e.g., through breeding of particular species of mammal).
Comments: A rare and non-native species in Central Europe, distributed in the Afrotropical region. The only record from Slovakia is from 1951. It is an ectoparasite of cattle and domestic equines (Povolný and Rosický 1955). It can be occasionally imported through human activities (e.g., through breeding of particular species of mammals).

Lipoptena fortisetosa
Published host records: Capreolus capreolus (Kočišová et al. 2007).  Comments: A relatively frequent species in Slovakia, distributed in the eastern Palaearctic region. Previously often confused with Lipoptena cervi. L. fortisetosa has a western boundary of distribution in Central Europe. It is an ectoparasite of Cervidae, and also attacks human beings (Ducháč and Bádr 1998). Homo sapiens is here newly recorded as a (common) host of L. fortisetosa in Slovakia.
Comments: It is an ectoparasite of Bovidae, especially sheep (including lambs) (Chalupský and Povolný 1983). Melophagus ovinus is strongly affected by a decline of traditional horse and sheep farming in the monitored area (e.g., Bezák and Petrovič 2006).
Comments: A relatively rare species in Central Europe. In Slovakia it is listed as endangered (EN) (Jedlička and Stloukalová 2001). Until now, only two records from 1951 and 1980 have been published from Slovakia (Chalupský 1980, Chalupský andPovolný 1983). It is an ectoparasite of mammals, collected mainly from R. rupicapra and, secondarily, sheep (Chalupský and Povolný 1983). Rupicapra rupicapra has an isolated population (R. rupicapra ssp. tatrica) in the Tatra Mountains in the north of the country, where M. rupicaprinus are found. Because it is isolated at the edge of its distribution range, this population of M. rupicaprinus is very vulnerable and like many other marginal populations, it could disappear rapidly and suddenly.
Even if the hosts are still widespread, their population density has declined over the past decades, and therefore the parasites will also suffer (BirdLife International 2018).
Comments: A Palaearctic species distributed in the northern and middle belts of the region. It is an ectoparasite mainly of Passeriformes, but also of species of other bird orders (Povolný and Rosický 1955). The only known record from Slovakia is from 1953, and it was "hidden" in the figure legend in Povolný and Rosický (1955). It was incorrectly doubted by Chalupský (1980) and was not listed in the last (Sychra 2009) or all previous checklists (Chalupský and Povolný 1987, 1997, Sychra 2006.
Comments: A Palaearctic species distributed in the northern and middle belts of the region. It is an ectoparasite mainly of Passeriformes, but also parasitizes species of other bird orders (Krištofík 1998).

Discussion
We have critically evaluated all available data on the occurrence of the family Hippoboscidae in Slovakia, and published data are completed with new collection data and unpublished localities. We confirmed 19 species as recorded from the country, which has one of the richest hippoboscid faunas in Europe. Out of 19 total species, 12 are native. While seven species (Crataerina pallida, Lipoptena cervi, L. fortisetosa, Ornithomya avicularia, O. biloba, O. fringillina, and Stenepteryx hirundinis) are widespread, three species (Icosta ardeae, Melophagus rupicaprinus, and Ornithomya chloropus) are known only from a few records, and the occurrence of the last two species (Hippobosca equina and Melophagus ovinus) is strongly affected by a decline of traditional horse and sheep farming in the monitored area (e.g., Bezák and Petrovič 2006). Species S. hirundinis and C. pallida might suffer from the decline of its hosts (BirdLife International 2018). Another seven species (Hippobosca longipennis, H. variegata, Icosta minor, Olfersia fumipennis, Ornithoica turdi, Ornithophila metallica, and Pseudolynchia canariensis) have been recorded from Slovakia based on very few records, due to occasional introduction with their hosts. These species can be introduced naturally due to migrating hosts (e.g., Icosta minor, Olfersia fumipennis, Ornithophila metallica, and Pseudolynchia canariensis) or imported together with domestic animals (e.g., Hippobosca longipennis, H. variegata).
Altogether, 78 host-parasite associations have so far been recorded for Slovakian Hippoboscidae ( Table 2). The hosts of the 19 species of louse flies recorded in Slovakia belong to 46 species of birds from eight orders (Accipitriformes, Anseriformes, Apodiformes, Ciconiiformes, Falconiformes, Passeriformes, Piciformes, Strigiformes) and nine species of mammals, including humans. The host records of Prunella modularis for O. avicularia and Homo sapiens for L. fortisetosa are here recorded from Slovakia for the first time.
The species composition of the hippoboscid fauna of Slovakia is relatively well known, and is, in comparison with other European countries, unexpectedly diverse. In Table 1, a list of European hippoboscid faunas is given, based on Petersen (2004) and Pape et al. (2015) and supplemented with data from relatively recent regional checklists (Büttiker 1998, Chandler 1998, Müller 1999, Beuk 2001, Draber-Monko 1991, Pape et al. 1995, Papp 2001, Carles-Tolrá and Báez 2002, Sychra 2009, Pohjoismäki and Kahanpää 2014. The comparison of species richness of Hippoboscidae across Europe's best studied countries for Diptera surprisingly showed that in Slovakia, the fauna of this group is not only distinctly more diverse than in all surrounding Central European countries, but even comparable with the faunas of much larger and more southern countries, such as Spain or Italy (including their insular areas), which also comprise 19 species (Table  1). However, raising any hypotheses about a possible latitudinal pattern in hippoboscid species richness would require much more thorough data on the continental scale.
We have noted that a number of country occurrences are missing in Fauna Europaea (Petersen 2004, Pape et al. 2015 when compared with the above checklists, most markedly for Spain and its adjacent islands (seven species missing) and Great Britain (six species missing). In contrast, some species listed in Fauna Europaea are missing in national checklists: e.g., I. minor is present in Fauna Europaea for Italy (Petersen 2004, Pape et al. 2015 but is absent in the national checklist (Pape et al. 1995); similarly, O. chloropus is present in Fauna Europaea for Hungary but is missing in the checklist of this country (Papp 2001). The national checklist of Spain (Carles-Tolrá and Báez 2002) also includes the species Crataerina nigriventris Gil Collado, 1932, which was wrongly referred to as C. nigriventris (Strobl, 1906) although it was originally described by Gil Collado (1932). However, according to Schneider-Orelli (1937), it is only an aberrant form of C. melbae (Rondani, 1879) and, therefore, it is omitted from the list in Table 1.
Judging from the occurrences of Hippoboscidae in other European countries, the list of Slovak species of the family is obviously not yet complete, despite its richness. At least the following two species can be expected in Slovakia: Crataerina melbae and Pseudolynchia garzettae (Rondani, 1879), both of which parasitize bird species living in Slovakia and are known from Italy and Switzerland, and Great Britain and Italy, respectively (see Table 1). In addition, the introduction of additional, more exotic hippoboscid species, like Olfersia spinifera (Leach, 1817) (known from G. Britain) or Ornithomya rupes Hutson, 1981 (recorded from Switzerland) to Slovakia cannot be excluded. In conclusion, more than 20 species of louse flies can be expected to occur in Slovakia, including both native residents and sporadic introductions.
Several species of the family Hippoboscidae can interfere with human life and interests, as ectoparasites of some domestic animals, occasionally parasitizing also humans. These are mainly Lipoptena cervi, L. fortisetosa, and relatively rare species Hippobosca equina and Melophagus ovinus. Damage is caused by direct bloodsucking and the venomous saliva of the louse flies, which can lead to permanent loss of blood and to animal wasting (especially ovine wasting), reduced milk and wool production, damage to wool caused by the parasite's faeces, etc. (Hutyra and Marek 1952). A secondary consequence of ectoparasitism by keds is the constant discomfort and scratching by the parasitised host (Hase 1927). Louse flies are also known as possible vectors of various diseases (Baker 1967, Kečera 1983, Oyieke and Reid 2003, Halos et al. 2004, Reeves et al. 2006, Martinković et al. 2012. A few of the above-mentioned species, especially L. cervi and L. fortisetosa, may bite humans in forest environments. In Slovakia, species of the family Hippoboscidae have not received sufficient attention, even though they are among the most abundant ectoparasites in some localities. Therefore, it is important to pay attention to this group and maintain an accurate  (Pape et al. 1995), Switzerland (Büttiker 1998), Great Britain (Chandler 1998), Czech Republic and Slovakia (Sychra 2009, present paper), Finland (Pohjoismäki and Kahanpää 2014), Germany (Müller 1999), Hungary (Papp 2001), Poland (Draber-Monko 1991) and The Netherlands (Beuk 2001).
overview of the species living in our territory, including monitoring of the occurrence of non-native species migrating with their hosts or imported with domestic animals. From a wider perspective, verified and accurate information on the diversity and distribution of louse flies in Slovakia can contribute to knowledge of this parasitic group from a global point of view.