The Hippoboscidae (Insecta: Diptera) from Madagascar, with new records from the “Parc National de Midongy Befotaka”

The Hippoboscidae or “louse-flies” is a family of pupiparous Diptera, which in their adult stage are ectoparasites of mammals and birds. This paper presents a comprehensive review of Malagasy Hippoboscidae. In total, amongst the 213 species of this family known worldwide, 14 have been reported in Madagascar, among which six are considered as endemic to the Malagasy region. In addition, data are presented from a collection of 17 Hippoboscidae obtained from seven species of forest-dwelling birds in the “Parc National de Midongy Befotaka”, southeastern Madagascar, in 2003. The flies in this collection belong to three different species: Icosta malagasii (one), Ornithoica podicipis (ten) and Ornithoctona laticornis (six). The two former species were previously only known from single specimens in museum collections; the later species is distributed across much of the Afrotropical region and the records presented herein are the first for Madagascar. All the seven bird species are new hosts for hippoboscids. We present the first description of the male of Icosta malagasii. An illustrated dichotomous determination key of the 14 Malagasy species, based on morphological criteria only, is presented.


INTRODUCTION
T he members of the family Hippoboscidae, known as "louse flies" or "keds", are obligate ectoparasites of mammals and birds. Members of this Diptera family consist of winged species, some of which have considerable flight capacity, while other species are flightless and highly apomorphic, having vestigial or no wings. Hippoboscidae belong to Pupipara "pupa-bearers", in reference to the fact that, unlike virtually all other insects, most of the larval development takes place within the mother's abdomen and pupation occurs almost immediately after pre-pupae laying (Hutson, 1984). The Hippoboscidae belongs to the super-family of Hippoboscoidea, which groups four families of flies that are bloodsucking at the adult stage for both sexes. The four families consist of Hippoboscidae, the bat flies Nycteribiidae and Streblidae, and the tsetse flies Glossinidae. Hippoboscoidea are considered monophyletic, but based on current data, the basal relationships between the four families are not resolved (Dittmar et al., 2006). A recent checklist of Hippoboscidae across the world retains three subfamilies (Ornithomyinae, Hippoboscinae, and Lipopteninae), 21 genera, and 213 species (Dick, 2006). It has been shown that the two subfamilies Hippoboscinae and Lipopteninae are monophyletic groups (Petersen et al., 2007). Caution must be taken with the name Hippoboscidae. In old taxonomic treatments, it was used to encompass the Hippoboscidae as defined today, as well as the bat-flies (Nycteribiidae and Streblidae). Irwin et al. (2003), following the BDWD (BioSystematic Database of World Diptera), used this old definition and indicated 760 valid species in the world and 15 in Madagascar, among which seven are Hippoboscidae sensu stricto. Members of the Hippoboscidae are known to act as vectors of many infectious agents: protozoan, bacteria, helminthes, and perhaps viruses. They certainly transmit mammal Trypanosomatidae of the genus Megatrypanum (Baker, 1967;Oyieke & Reid, 2003) and probably transmit avian trypanosomes (Kucera, 1983). Hippoboscidae are the only known vectors of Haemoproteus (an apicomplexan parasite of birds). Melophagus ovinus louse flies play a role in the transmission of Bartonella among ruminants (Halos et al., 2004;Reeves et al., 2006). In Kenya, the fly Hippobosca longipennis is thought to transmit to hyenas and domestic dogs the larva of the filarial nematoda Acanthocheilonema dracunculoides (Nelson, 1963). This filaria has been reported from domestic animals in Madagascar (Daynes, 1964). The louse fly Icosta americana is currently suspected in the transmission of West Nile Virus in North America (Farajollahi et al., 2005). Although the importance of Hippoboscidae in the transmission of mammal and bird parasites in Madagascar has been suspected and to some extent documented (Daynes, 1964;Savage et al., 2009), members of this family remain poorly documented on the island. We here present the first comprehensive review of Malagasy Hippoboscidae (sensu stricto i.e. excluding Nycteribiidae and Streblidae). In addition, we propose the first illustrated dichotomous determination key for the genera and species currently known from Madagascar. Recent specimens of hippoboscids have been collected from Malagasy vertebrates and remain unstudied by fly specialists (e.g., Wright et al., 2009). Herein we present details on a hippoboscid collection obtained from forest-dwelling birds in the "Parc National de Midongy Befotaka", previously known as Midongy-Sud, southeastern Madagascar.

REVIEW OF MALAGASY HIPPOBOSCIDAE BASED ON PUBLISHED LITERATURE
I nformation on Malagasy Hippoboscidae is rather limited and notably dispersed in the scientific literature. We found published records of 13 species recorded at least once on Madagascar. The host species (when known) and/or the context for Madagascar are presented in Table I. The numbers of species from the three subfamilies of Hippoboscidae -Ornithomyinae, Hippoboscinae, and Lipopteninae -are 11, two, and zero, respectively. Six species of Ornithomyinae are presently considered as endemic to Madagascar. Individuals of eight species have been collected from a single individual host, including three different specific names proposed for the female flies (Icosta malagasii, Ornithomya sorbens, and Ornithoctona idonea), while the identity of the male remains unknown.
The genus Allobosca is composed by only one known species, A. crassipes. This species, considered endemic to Madagascar, has rudimentary wings and is known from several species of lemurs (Ferris & Cole, 1922;Maa, 1969c). Proparabosca is a genus of Hippoboscidae, with only one known species, P. alata, which is an ectoparasite of the Indriidae Propithecus verreauxi in Namoroka National Park (Theodor & Oldroyd, 1965). Most of the 171 species of Ornithomyinae are bird ectoparasites, with the exceptions of A. crassipes and P. alata (plus five species that parasite wallabies in Australia).
Icosta malagasii is only known by one female. It was collected as a "parasite sur l'aile d'un Coezach/ Sahafanjana/N: 115/R. M./ Inst. Sci. Madagascar" (Maa, 1969b). Sahafanjana is located in close proximity to the "Parc National de Mananara-Nord" and in the zone between Manambato and Anove (Quentin & Villiers, 1973;Flint et al., 1987). One possibility in the identification of the "Coezach" is that it is a poor transliteration of the Malagasy vernacular name "Koa", which are members of the endemic genus Coua (subfamily Couinae). In certain Malagasy dialects, the last syllable of the vernacular name is accented and harshly pronounced. In the Parc Botanique et Zoologique de Tsimbazaza, Antananarivo (previously known as "Institut de Recherche Scientifique de Madagascar") there is a male specimen of C. caerulea, collected on 12 April 1955 by "R.M." at Sahafanjana. This information gives credence to the identity of the "Coezach" as a Coua.
Ornithoctona idonea is only known by one male and two females with two of these specimens, including the male holotype, being from Madagascar (Falcoz, 1929). Theses two Malagasy specimens formerly in the Falcoz collection are now untraceable. Curiously, although the male was designated as the holotype, it remains undescribed. Presently, the only available specimen is a pined female O. idonea (in the Muséum national d'Histoire naturelle, Paris), collected in "Africa" (no precise locality, no host record) and designed as a paratype by Falcoz (1929). Maa (1963)  Pseudolynchia canariensis, the pigeon louse fly, is found in most parts of the tropical and sub-tropical areas of the world and associated with domestic pigeons and doves. Pseudolynchia canariensis is the vector for the Apicomplexa protozoan Haemoproteus columbae, a parasite that can be fatal to young pigeons.
Hippobosca variegata, a species distributed in sub-Saharan Africa and Asia, has also been observed in the Comoros Archipelago, specifically on Grande Comore and Mayotte (Brunhes, 1978). The natural host of this fly is unknown (Maa, 1969c). This species is common on Malagasy cattle (Maa, 1962). Hippobosca longipennis is known from introduced carnivorans on Madagascar (Bequaert, 1939).
On the Aldabra Atoll, Seychelles, which is 420 km NW of Madagascar, Cogan et al. (1971) reported that local land birds were rarely and only lightly parasitized with one unspecified species of Hippoboscidae. In contrast, bird species occurring in marine environments had notably higher concentrations of parasites, particularly far-ranging groups like the boobies and tropicbirds heavily parasitized by Olfersia aenescens and frigates by Olfersia spinifera.

ORIGINAL OBSERVATIONS ON HIPPOBOSCIDAE FROM THE "PARC NATIONAL DE MIDONGY BEFOTAKA"
STUDY AREA T he "Parc National de Midongy Befotka" is located in the southeastern portion of Madagascar and along the western flank of a chain of northsouth oriented mountains running the length of much of eastern Madagascar. All of the sites visited were in undisturbed or largely undisturbed natural forest classified as "Humid Forest" (Moat & Smith, 2007). Meteorological patterns in the village of Midongy-Sud, in close proximity to the park, include an average of 1,825 mm of rain per year, falling on 170 days, with the wettest month being January, and the annual mean temperature of 18 °C (Donque, 1975). Hence, the zone does not have a pronounced dry season.

BIOLOGICAL MATERIAL
During field expeditions, ornithologists mist-netted birds in the "Parc National de Midongy Befotaka". Four-panelled mist-nets measuring 12 × 2.4 m with 36 mm mesh were installed at ground level in the forest understory. After being dispatched, certain birds retained as voucher specimens and for other research purposes, were individually placed in clean plastic bags with a small cotton ball moisten with ethyl acetate. All ectoparasites recovered were preserved in ETOH and are held in the collections of the Field Museum of Natural History, Chicago. All the Hippoboscidae reported on herein were collected from birds captured between 27 October and 14 November 2003; other details on the hosts are presented in Table II. The determination of these Hippoboscidae flies used Maa's (1963) key at the levels of subfamily and genus. The species determination was subsequently inferred using other references (Maa, 1966 for Ornithoica;Maa, 1969a for Ornithoctona;and Maa, 1969b for Icosta). Following Maa (1969b), O. idonea "would be separable from O. laticornis in having antennal appendage relatively more acute at apex, palpus longer, mesosternal processes closer to each other and posterior marginal bristles on laterite two much shorter."

RESULTS
In total, 17 Hippoboscidae specimens were collected from 11 individual birds belonging to seven different bird species (Table II). They belong to three species of Ornithomyinae, namely Icosta malagasii, Ornithoica podicipis, and Ornithoctona laticornis. The two former species were previously only known from single museum specimens and are here represented in the Midongy Befotaka collection by an additional one and ten individuals, respectively. Further, based on this material, the male of I. malagasii can now be described (see below) and for the first time O. laticornis is documented on Madagascar. New records include collection of I. malagasii had been collected from Accipiter francesii; Ornithoica podicipis from Atelornis pittoides, Accipiter francesii, Otus rutilus, Brachypteracias leptosomus, and Streptopelia picturata; and O. laticornis from Atelornis crossleyi, Atelornis pittoides, and Monticola sharpei.

DISCUSSION
The specimens recorded from the "Parc National de Midongy Befotaka" are the first reported in detail from wild Malagasy forest-dwelling birds. Within this material, we identified specimens (five females and one male) as O. laticornis because they perfectly match Maa's description (1969a). However, it is hard to definitely exclude O. idonea because of Falcoz's imprecise drawings and description. Within these six specimens, there is notable polymorphism in antenna shape, setae of the first sternite, and ocellus area. Individuals of both sexes of O. laticornis in Madagascar support Maa's (1963)  Given the high level of endemicity of Malagasy birds at different taxonomic levels, including 51 % of the 209 nesting bird species (Goodman & Hawkins, 2008), it is rather striking that there has not been a greater radiation of hippoboscid species, as is known in other groups of blood-sucking flies parasites of vertebrates (e.g. Dick, 2007). Perhaps current low-levels of measured species diversity within Malagasy hippoboscids are in part associated with few field collections of these flies. Another explanation is that within the species groups with broad extralimital distributions, such as different genera within the Ornithomyinae, unrecognized cryptic species occur on Madagascar. Molecular genetic studies of recent collections of hippoboscids from Madagascar and neighbouring islands should help resolve these questions.

DESCRIPTION OF THE MALE OF ICOSTA (ICOSTA) MALAGASII MAA, 1969
The male is very similar to the female, as described by Maa (1969b), but differs as follows. Abdomen with three tergal plates, the first one is dark, narrow, lining the abdomen basally, and extending antero-laterally. The second tergal plate is linked to the third one by a broad striate zone bearing small and narrow setae. The third tergal plate (tergite VI) bears five to seven pairs of long dark bristles projecting posteriorly. Ventrally the urogenital area is surrounded by small and narrow setae and anteriorly by a spot of dark bristles. The antenna is notably less hirsute than in the female (Plate 1, Figs a, b).

DICHOTOMIC KEY FOR DETERMINATION OF MALAGASY HIPPOBOSCIDAE
• Key to Genera of Hippoboscidae 1-Wing abnormal in size, frons longer than wide, hind femur almost as long as thick and fore tarsus with spatulate setae ( Fig. f)  1-Wing size 3.2-3.5 mm. Wing-setulae covering more than 1/2 of cell 2m and extending to apical 1/2 or more of 2r and to apical margin of r-m. Mesoscutum except small areas at its anterolateral corners, as densely setose as prescutum and scutellum. Bare area at base of cell 3r much less than 2× as that of 1m. Ornithoica (Ornithoica) podicipis von Röder, 1892 -Wing size 2.5-2.8 mm. Wing-setulae covering much less than 1/2 of cell 2m, generally forming very small patch near its antero-apical corner; cell 2r at most setulose at extreme apex. Cell r-m entirely bare, setulose area in cell 2m small confined to antero-apical corner (Plate 5, Figs e, f).