Review of the Bat Flies of Honduras, Central America (Diptera: Streblidae)

Streblid bat flies are obligate and host-specific blood-feeding ectoparasites of bats. While the bat flies of some American countries are well studied (e.g., Panama, Venezuela), little is known about Honduran Streblidae. Accumulation of substantial numbers of specimens, from several different collections, has enabled a relatively thorough treatment of the fauna. This study is based on 2,236 specimens representing 17 genera and 43 species of Streblidae. Of those presently reported, 11 genera and 32 species are new records for Honduras, increasing the number of known genera and species by 65% and 74%, respectively. Collection and host data are listed for all known Honduran streblid bat fly species. Comments regarding host associations and specificity, geographic distribution, and taxonomic problems are given in the species accounts.


Introduction
Streblid bat flies are a worldwide group of obligate, bloodfeeding ectoparasites of bats. The species tend to be host specific, with one fly species typically parasitizing one host species or a few closely related host species [1][2][3]. Some members of the streblid subfamily Nycterophiliinae are rather less host specific, often parasitizing two or more genera of hosts [4]. Distributional evidence suggests that they cospeciate with host species of bat, producing parallel phylogenies of host and parasite [5]. Streblids are often absent from bat species that roost solitarily or in temporary roosts [6]. Conversely, bat fly richness per host species seems generally to increase with roost size, duration, and the number of bats roosting there [7,8]. The dynamics associated with bat roosts as they pertain to the biology, ecology, and host specificity among streblid bat flies is a critically understudied area. Perhaps attributing to the fact that bat host species often harbor more than one species of Streblidae is the observation that some bat flies prefer particular areas (microhabitats, e.g., fur or wing membranes) on the host's body [1,[9][10][11].
The taxonomy of Neotropical streblid genera relies primarily on overall body form, the presence or absence of a ctenidium along the posteroventral margin of the head, gross characteristics of the wings, leg chaetotaxy, and details of the thorax, especially the mesonotal and transverse sutures, and male reproductive structures. Generic identification can always be made using a stereozoom microscope. Specieslevel identifications may often be made using low magnification, but some species (especially Trichobius spp.) are best identified using slide-mounted specimens examined using a high-power compound microscope. A simplified key to New World genera is available in [12]. Other generic keys are available in [4,13,14]. The single best key to most New World streblid species is [4]. For species-level keys, see [13,[15][16][17][18][19]. Guerrero listed characteristics for 36 species of Trichobius [16].
Few Streblidae have been recorded previously from Honduras, largely due to the lack of ectoparasite sampling in the country. Honduran specimens have been previously reported in three publications. Wenzel et al. [1] reported Strebla guajiro (García & Casal) (as S. carolliae Wenzel) and S. wiedemanni Kolenati (as S. vespertilionis (Fabricius)). Wenzel [20] reported 12 species from Honduras but provided no data on specific records. Seven of the species are represented by specimens housed at the Field Museum of Natural History, Chicago (FMNH), and are considered valid records: Trichobius costalimai Guimaraes,

Materials and Methods
The bulk of the specimens treated in this paper were collected by the author during 2001, as part of a survey project led by R. D. Bradley of Texas Tech University and R. A. Van Den Bussche and M. Hamilton of Oklahoma State University. During this expedition, 964 bats were collected at 15 localities. Bats were collected with nylon mist nets and by hand and usually kept individually in cloth bags. Because ectoparasite collection was not the main focus of the expedition, not all captured bats were sampled for parasites, and there were instances when cross-host contamination of parasites was likely. These instances are noted in the species accounts and addressed in the discussion. Bats were anesthetized with ethyl ether and brushed for ectoparasites, which were stored in vials of 95% ethanol. Streblid flies were collected from 242 individual bats. Most of the flies were studied under a dissection microscope. Others were slide-mounted in Canada balsam for examination under a compound microscope. Confirmations of identifications were made by comparison of the Honduran specimens to type specimens and other reference collections housed at the FMNH.
Specimens and specimen records for this project came from three primary sources. The TTU Honduras expedition yielded 381 records and 2051 specimens. Additionally, 47 records and 141 specimens were provided by T. J. McCarthy and R. P. Eckerlin, collected during the project "Mastozoolgía en el Núcleo de Centroamerica" (MANCA). Eighteen records and 44 specimens from the FMNH, representing new and previously reported specimens, were studied. Previously reported specimens (e.g., [1,4,20,21]) were reexamined. Fly identifications were made by the author, but historical FMNH specimens were originally identified by R. L. Wenzel. Thus, a total of 446 records and 2,236 specimens of Streblidae were examined as the basis of this paper. Most fly specimens have been deposited in the FMNH, but representative MANCA specimens were deposited at Carnegie Museum (CM), Pittsburgh, PA, USA, and a synoptic collection was deposited at TTU. Bat host vouchers exist for most of the parasite records; all flies collected during the TTU project can be traced to host bat specimens in the mammal collections of TTU. Flies collected during the MANCA project can be traced to bat specimens housed at CM or the American Museum of Natural History (AMNH), New York. Nomenclature used for bats generally follows Simmons [24]. The accounts below provide an overview of each streblid genus known from Honduras, presented by subfamily. Species accounts list streblid species and primary reference, records from Honduras, and comments when relevant. A concise list of all streblid species known from Honduras appears in Appendix A. A list of Honduran bat fly host associations is presented in Appendix B. A gazetteer of collection localities is presented in Table 1, which corresponds to the map of collection localities ( Figure 1). Unless indicated otherwise, fly specimens were collected by the author.  Figure 1: Map of Honduran bat fly collection localities. Locality numbers (numbered closed circles) correspond to specific localities in Gazetteer (Table 1).

Species Accounts
In Honduras, the vast majority (99.7%) of N. coxata specimens were associated with the mormoopid bat P. parnellii. The single specimen from S. lilium is regarded as a contaminant, as a specimen of P. gymnonotus Natterer was collected on the same day.

Subfamily Streblinae Speiser, 1900
Genus Anastrebla Wenzel, 1966 Anastrebla Wenzel, 1966 Two described species belong to this genus, Paraeuctenodes longipes Pessôa & Guimarães and P. similis Wenzel, and only the former is known from Honduras. In Honduras and Venezuela [4], the primary host species of P. longipes are Glossophaga spp., while the primary host of P. similis is Carollia perspicillata (Linnaeus). Both species of Paraeuctenodes are dorsoventrally flattened and possess a ctenidium of rearward facing spines on the posteroventral margin of the head. These characteristics appear to adapt the species to live within the fur of their hosts [25].

Paraeuctenodes longipes Pessôa and Guimarães
Paraeuctenodes longipes Pessôa and Guimarães, 1937:258. The genus Strebla comprises 25 described species and is second only to the genus Trichobius in number of species. Seven species of this genus are known to occur in Honduras. Species of Strebla are dorsoventrally flattened and possess a ctenidium of rearward facing spines on posteroventral margin of the head. This form appears to adapt species of Strebla to live inside the fur of the host [25].

Strebla chrotopteri Wenzel
Strebla chrotopteri Wenzel, 1976 The characteristic hosts of S. guajiro in Honduras were species of Carollia. In Venezuela, 98.5% of the 586 specimens collected there were taken from Carollia spp., and most of Table 1: Gazetteer of Honduran bat fly collection localities. Locality numbers correspond to map ( Figure 1). Latitude and longitude are in decimal degrees. Specific localities with identical locality numbers are close in proximity, not warranting separate placement on the map ( Figure 1). This genus comprises three species, Aspidoptera delatorrei Wenzel, A. falcata, and A. phyllostomatis [4,23]; the latter two occur in Honduras. Species of this genus are restricted to phyllostomid bats of the subfamily Stenodermatinae.

Aspidoptera falcata Wenzel
Aspidoptera falcata Wenzel, 1976:104, Figure 42A. Aspidoptera falcata is a characteristic parasite of several species of Sturnira Gray, including S. lilium, S. ludovici, and S. tildae de la Torre. In Venezuela, 99.0% of the 755 A. falcata specimens collected there were taken from these three species of Sturnira [4]. The record from the fishing bat Noctilio leporinus almost certainly resulted from sampling contamination. Aspidoptera falcata is morphologically very similar to A. delatorrei and can be positively identified only by examining the postgonites (falciform in A. falcata).

Aspidoptera phyllostomatis (Perty)
Lipoptena phyllostomatis Perty, 1833:190, Figure 17 This genus comprises two described species, Mastoptera guimaraesi Wenzel and M. minuta (Costa Lima), and appears to be restricted to phyllostomid bats of the subfamily Phyllostominae. This genus contains the smallest of New World streblid species, with some specimens of M. minuta measuring only 0.73 mm in total length [12]. The genus is in need of revision [4].
In Venezuela, the characteristic host of M. minuta is Lophostoma silvicolum (d'Orbigny) [4]. The taxonomy of Mastoptera species is complex and poorly understood, and Wenzel [4] noted that there were undescribed species within M. minuta. The 23 Honduran specimens were collected from one host individual of L. brasiliense. The taxonomy of Mastoptera species is complex and poorly understood, and Wenzel [4] noted that there were undescribed species within M. minuta. Here I refer specimens to M. minuta species complex. The group is in need of revision.

Genus Megistopoda Macquart, 1852
Megistopoda Macquart, 1852:332. This genus comprises three described species: Megistopoda aranea, M. proxima, and M. theodori [4]. Wenzel [4] noted that the taxonomy of this genus is confused and in need of revision, as there are undescribed species within this genus. Wenzel [4] questioned the distinctness of M. theodori and stated that it might be synonymous with M. proxima. I consider the two species to be distinct (see M. theodori account below), but note that the proxima group of species contains several undescribed species. Megistopoda of the aranea type possess extremely elongated hind legs and very narrow wings and parasitize species of Artibeus (but not Dermanura spp.). Megistopoda of the proxima type (including M. theodori) possess less elongated hind legs and broader wings and parasitize species of Sturnira. However, recent specimens from western Ecuador document the existence of two other undescribed aranea type species, one from the west The characteristic host of M. proxima in Paraguay was S. lilium (hosting 98.1% of 372 specimens) [29]. In Venezuela, all of the 965 specimens were from S. lilium [4], but specimens from hosts other than S. lilium were simply referred to the M. proxima complex. Megistopoda proxima as currently described represents a complex of species [4], and in general, the true M. proxima are specific to S. lilium. This group of bat flies has not been studied in detail.

Megistopoda theodori Wenzel
Megistopoda theodori Wenzel, 1966:545. Figure 100B.  [4,23]. Species of this genus are restricted to fishing or bulldog bats of the genus Noctilio Linnaeus (family Noctilionidae). Two species are known from N. leporinus and two from N. albiventris Desmarest, but based on data from Venezuela, the two species infesting each host species never cooccur on the same host individual [25]. Noctiliostrebla spp. possess vestigial wings and are rather similar in overall morphology.

Noctiliostrebla traubi Wenzel
Noctiliostrebla traubi Wenzel, 1966 [4,23]. Species of this genus are wholly restricted to fishing or bulldog bats of the genus Noctilio (family Noctilionidae). Two species parasitize only N. leporinus, while three species parasitize only N. albiventris. As with Noctiliostrebla spp., species of Venezuelan Paradyschiria never appear to cooccur on the same host individual [25]. Paradyschiria spp. are the only wingless streblid bat flies.

Paradyschiria fusca Speiser
Paradyschiria fusca Speiser, 1900:56, Figure 1 This genus comprises six described species, Paratrichobius americanus Peterson & Ross, P. dunni (Curran), P. longicrus (Ribeiro), P. lowei Wenzel, P. salvini Wenzel, and P. sanchezi Wenzel. All are known to be associated with bats of the phyllostomid subfamily Stenodermatinae. Paratrichobius spp. are fully winged but possess a shield-like ventral thorax very long hind legs; these characteristics appear to adapt these species to life in the fur and facilitate their evasive behavior of movement over the top of the fur. The taxonomy of this genus is confused and a revision is needed; in particular, the nominal species P. longicrus and P. salvini are most likely species complexes [4].

Paratrichobius dunni (Curran)
Speiseria dunni Curran, 1935:7, Figure 6. More than 98% of the 102 P. dunni collected in Venezuela were taken from Uroderma bilobatum and U. magnirostrum Davis [4]. Species of Dermanura host a unique species, P. lowei, and the present records from D. phaeotis are probably contaminants. As in Venezuela [4], the characteristic host of Paratrichobius longicrus in Paraguay is Artibeus lituratus (hosting 156 of 159 specimens; 98.1%) [29]. Honduran records from hosts other than A. lituratus and A. intermedius are suspect. Simmons [24] considered A. intermedius a junior synonym of A. literatus. Artibeus lituratus is not known to harbor parasites of the genus Megistopoda, which are characteristic parasites of other species of Artibeus and Sturnira spp. Paratrichobius and Megistopoda may be ecological equivalents, being fairly similar in gross morphology with long hind legs. They differ, however, in that Paratrichobius spp. have fully functional wings while Megistopoda spp. have reduced and nonfunctional "strap-like" wings.

Speiseria ambigua Kessel
Speiseria ambigua Kessel, 1925:20, Figures 1-2 Figure 52B (emended by Wenzel, 1984). This species is a characteristic parasite of the phyllostomine bat Phyllostomus discolor. It is not known to occur on either of the other two species of Phyllostomus: P. elongatus (E. Geoffroy) and P. hastatus. All 37 Honduran specimens were collected from P. discolor, as were 97% of the 689 specimens collected in Venezuela [4].
The genus Trichobius currently comprises 68 described species and is the most diverse genus of the family Streblidae. The most recently described species were T. machadoallisoni Guerrero and T. anducei Guerrero [31]. Members of this genus parasitize a wide variety of bats, including representatives of the families Emballonuridae, Furipteridae, Molossidae, Mormoopidae, Natalidae, and Phyllostomidae. The genus has been divided into nine species groups or complexes [1,4]: pallidus group (1 species), caecus group (7 species), uniformis group (4 species), major group (18 species), longipes group (8 species), dugesii group dugesii complex (12 species), dugesii group parasiticus complex (9 species), phyllostomae group (5 species), and the dunni group (4 species). Some of the described species of Trichobius are very distinct morphologically. Based on host associations and morphological affinities to other streblid genera, some workers feel that some if not all of the Trichobius species groups should be described as distinct genera (R. L. Wenzel, pers. comm.). The T. phyllostomae group has, based on morphological analysis, been shown to form a monophyletic group [32]. Yet other species are very similar morphologically and can be positively identified only by microslide mounting and examining under the high magnification of a compound microscope. The entire genus is in need of revision; it is predicted that the genus as currently constituted is widely paraphyletic. Thirteen species of Trichobius are known to occur in Honduras. Trichobius caecus is a member of the caecus group of species [4]. In Venezuela, 97% of the 1,592 collected specimens were taken from the mormoopid bat P. parnellii.

Trichobius diphyllae Wenzel
Trichobius diphyllae Wenzel, 1966 Trichobius galei is a member of the caecus group of species [4]. Species of this group parasitize bats of the families Emballonuridae and Natalidae. In Panama [1] and Paraguay [29], T. galei was restricted to N. stramineus. In Venezuela, however, 98.5% of the 277 specimens collected were taken from the congener N. tumidirostris [4]. The Honduran record from G. soricina probably represents a contaminant. Trichobius hirsutulus is a member of the major group of species. The major group of species is the only true "northern" radiation of Streblidae; species are known from North America, Mexico, Central America, and Antilles, but none from farther south than Peru. Previous to this report, the species was known only from México (Tamaulipas and Yucatán), from the vespertilionid Myotis nigricans Schinz. Trichobius intermedius is a member of the dugesii complex of the dugesii group of species. Throughout its range from Mexico, Antilles, to northern Central America, it is a characteristic parasite of large Artibeus species, particularly A. jamaicensis. Honduras appears to contain the terminus of its southern distribution. Extensive surveys have been undertaken in Costa Rica (C. W. Dick, R. M. Timm, R. L. Wenzel, unpublished data), Nicaragua (C. W. Dick, unpublished data), and Panama [1], but no T. intermedius were present in these collections.