New records of bee flies (Diptera, Bombyliidae) from Cuatro Ciénegas, Coahuila, Mexico

Abstract Forty one new records of species of Bombyliidae are reported for Coahuila in northeastern Mexico. Nine of these species are reported for the first time for the country. The specimens were collected in the Cuatro Ciénegas Basin and Sierra La Madera mountains during 2007–2013. The modified distributions of species are discussed. The gaps in the distribution of many species suggest an undersampling of this group of insects in the north of Mexico.


Introduction
The bee flies (Bombyliidae) belong to the superfamily Asiloidea and are the eighth most diverse family within Diptera with 5382 described species (Pape et al. 2011). All species of Bombyliidae are parasitoids, hyperparasitoids or predators of immature stages of Coleoptera, Hymenoptera, Lepidoptera, Orthoptera, Neuroptera, and Diptera (Yeates andGreathead 1997, Boesi et al. 2009). Unlike most other taxa, bee flies are most abundant and diverse in arid and semiarid portions of the world (Hull 1973, Evenhuis 1989). In the immature stages these insects function as a natural control for populations of other insects and as adults are efficient pollinators (Motten et al. 1981, Kearns 2001. Some faunistic studies have been completed including Bombyliidae in Mexico (Rodríguez-Ortuño 1989, Ávalos-Hernández 2007, but the northern region of the country is poorly known for this family. Although Evenhuis and Greathead (1999) list 15 species of Bombyliidae for Coahuila, species richness in this state is probably higher as suggested by the richness of surrounding Mexican states with similar or even smaller size and similar ecosystems (e.g., Nuevo León, 37 species; Durango, 41 species) and of Texas (171 species), the nearest USA state.
Cuatro Ciénegas Basin in the northeast of Coahuila is especially interesting because of its geological history and the presence of water ponds and gypsum dunes, which create a different environment from the surrounding areas. The basin was a shallow sea from the Pangea breakup until the Eocene, 40 Ma, when the Sierra Madre Oriental in the east of Mexico rose isolating the Basin from the Atlantic Ocean . The physiology of Cuatro Ciénegas bacteria is similar to that of marine species, with which they are closely related (Souza et al. 2006). According to Moreno-Letelier et al. (2012) this evidence indicates that some water was kept trapped in the Basin when the ocean retreated giving the basin unique characteristics. These characteristics produced a high number endemism for vertebrates and prokaryotes in Cuatro Ciénegas (Souza et al. 2006.
The present study is the first known long-term systematic sampling of Diptera in Cuatro Ciénegas. The objective of this project is to complete the list of species of Bombyliidae in the basin and surrounding mountains. In this paper, 41 new specieslevel records for Coahuila from Cuatro Ciénegas are presented, including nine new records for Mexico. The modified distributions of the species are discussed.

Methods
Beeflies were collected at nine sites from Cuatro Ciénegas Basin and Sierra La Madera within the Municipality of Cuatrociénegas (Figure 1). Abbreviations for study sites (Table 1) are used throughout. Samplings were performed during 2007-2013, using aerial net and a Malaise trap. The Malaise trap had white polyester netting, was square in configuration, 210 cm tall and 120 cm wide and the collecting head located at the top. Trap was set from 9:00 to 17:00 when weather conditions allowed it. To avoid damage to the specimens no killing agent was used, insects were extracted at the end of the day. Specimens were pinned and labeled. Generic identification was carried out under a stereomicroscope according to the keys by Hall (1981b) and Kits et al. (2008). Species were identified by the first and second authors with specialized keys for each genus and comparison with museum specimens, keys used for identification of each genera are specified below. Taxonomic classification and distribution data are based on Evenhuis and Greathead (1999) and host data are based on Hull (1973), if not indicated otherwise. Distribution gaps are suggested as disjunct distribution patterns or the result of under sampling by comparing the location of records in Mexico with those in the southern states of the USA. All specimens are deposited in the Colección Nacional de Insectos (Instituto de Biología, Universidad Nacional Autónoma de México; CNIN-IBUNAM).

Results
A total of 41 new species-level records are presented for the state of Coahuila. Nine of these 41 species are recorded for the first time in Mexico, being their most southern records. Of the 15 species previously listed for Coahuila, two were collected during this study:  New records of the species included in this paper are from 17 genera for which modern revisions are available. Six taxa of Hemipenthes (3), Lordotus (1), Paravilla (1) and Rhynchanthrax (1) could not be identified accurately, being probably undescribed species. Identification of species in another 10 genera found in the study (e.g. Villa, Chrysanthrax, and Exoprosopa) is difficult and unreliable. The number of morphospecies and specimens collected of these genera are presented in Table 2. Six species of Tmemophlebia (1), Geron (1), Exoprosopa (3) and Villa (1) previously listed for Coahuila were probably collected but specimens of these genera are still being identified. Taxonomic work will continue, updates of the species list and descriptions of the new taxa will be published in subsequent papers.
A total of 28 genera were found during this study, of which 21 are new records for the state. Two genera previously listed for Coahuila (Neacreotrichus and Relictiphthiria) were not found in Cuatro Ciénegas area. With the new records presented here, the list of bee fly species in Coahuila increases to 56 (Table 2).

Subfamily Toxophorinae Genus Toxophora Meigen
Remarks. Toxophora is distributed worldwide, being more diverse in the Afrotropical and Palearctic regions. Mexico's fauna includes three Neotropical species and five Nearctic species. All Nearctic species of Mexico were distributed in the western half of Table 1. Field work sites in Cuatro Ciénegas. Vegetation according to Pinkava (1979).  the country. These two new records represent the first of this genus in Coahuila and the most eastern distribution of the Nearctic species in the country. The New World species of this genus were keyed using Cunha et al. (2011). Comments. In Mexico T. maxima was only known from Baja California Peninsula and now Coahuila. This apparent gap in its distribution is probably due to undersampling. Sampling of the intermediate zones is necessary to know if these populations form a continuous unit as they do in the southern states of USA. Comments. This species is present in the all southwestern states of the USA and northwest of Mexico. This is the first record in the northeast of Mexico. The species is probably also present in Chihuahua, between Sonora and Coahuila.

Subfamily Bombyliinae
Genus Bombylius Linnaeus Remarks. With 278 described species, Bombylius is the second most diverse genus of Bombyliidae. It has a worldwide distribution being especially diverse in the Palearctic and Nearctic regions. One endemic species is present in Coahuila: B. (Parabombylius) coahuilensis (Hall & Evenhuis, 1981). Four other species are reported for the state: B. sylphae Evenhuis, 1984, B. aleophilus (Hall & Evenhuis, 1981), B. paradoxus (Hall & Evenhuis, 1981), B. syndesmus (Coquillett, 1894). A review with identification keys for Nearctic species is presented in Hall and Evenhuis (1980), later Evenhuis (1984) revised and present keys for the comanche group of America.  Comments. This species is restricted to the southwest of the USA and north of Mexico.

Genus Heterostylum Macquart
Remarks. The genus is only present in Nearctic and Neotropical regions. Although not as diverse as other genera (only 12 species), specimens from some species are abun- dant in the field. Heterostylum robustum was previously known from Coahuila and was collected during this study. This species is distributed from Canada to central Mexico. There are two revisions for this genus that contains identification keys, one by Hall and Evenhuis (1980) and the more recent by Cunha et al. (2007). Figure 4 Material examined. REE: Apr (1 F).
Comments. Heterostylum croceum is recorded for the first time in Mexico; previously known from the southern-central United States. Hall and Evenhuis (1980) suggest that H. croceum may be related to H. engelhardti Painter, 1930 or even be a subspecies of that taxon, Heterostylum croceum is the eastern form and H. engelhardti the western form (Arizona, California, Texas, Utah) although both species are present in Texas. Cunha et al. (2007) comment that H. engelhardti can be distinguished by the presence of white to very pale yellow hair and brown-tipped hairs on the abdomen compared with the darker yellow hairs in H. croceum.  pulchrissimus Williston, 1893;L. striatus Painter, 1940;L. zona Coquillett, 1887). The three species present in Coahuila are also found in California; their distribution probably includes all northern states of Mexico. Hall (1954) and Hall and Evenhuis (1982) present reviews of the genus and keys to the species.   Known Nearctic records. Mexico (Baja California, Coahuila, Sinaloa, Sonora); USA (Arizona, California, Nevada, Texas).

Lordotus diplasus Hall, 1954
Comments. Lordotus perplexus has the most southern distribution in the genus, reaching Sinaloa on the Pacific coast.

Genus Triploechus Edwards
Remarks. Four species of Triploechus are present in Nearctic region: T. luridus Hall, 1975;T. novus (Williston, 1893); T. sackeni (Bigot, 1892); T. stagei Hall, 1975. Of these T. stagei is endemic to Mexico and T. novus has the widest distribution of this genus, being present in the south of the USA and center of Mexico. Hall and Evenhuis (1981) present a revision and key for species for this genus. Figure 6 Material examined. CHU: Apr (7 F, 6 M); REE: Apr (1 M); RPA: Apr (1 M).
Comments. This is a widespread and apparently common species. All specimens were collected in April so it may have a short flight season.

Subfamily Lomatiinae
Genus Ogcodocera Macquart Remarks. The only two species in this genus have been collected from the neotropical part of Mexico to north of the USA and Canada. Ogcodocera leucoprocta (Wiedemann, 1828), not sampled during this study, is present in the whole Nearctic region from Canada to south of Mexico.  Comments. This record is the first of this species in the north of Mexico, but it has been previously collected in the south of Mexico and in the south of USA, and thus is probably distributed across the whole country. Unlike O. leucoprocta, O. analis has its most northern distribution in Arizona and Texas.   Known Nearctic records. Mexico (Coahuila, Sonora); USA (Arizona, California, Nevada, Texas).

Ogcodocera analis Williston, 1901
Comments. Paracosmus (P.) morrisoni has the widest distribution within this genus, but in Mexico had previously only been recorded in Sonora. This record represent the most eastern distribution for the genus in the country.

Subfamily Anthracinae Genus Anthrax Scopoli
Remarks. This is a diverse genus with 248 species worldwide. Two old but complete revisions of the genus, including distribution maps and keys, were made by Marston (1963Marston ( , 1970. Thanks to these Anthrax species can be easily identified. Some Anthrax species are widely distributed occupying two biogeographic regions. From the seven Anthrax species collected in this study in Coahuila, just A. cybele (Coquillett, 1894) has a restricted distribution. The other six species are widespread across the Nearctic region. Two species of Anthrax are reported for the first time for Mexico.     Comments. This is a rare species flying in April. Its distribution is disjunct so far, present in the southwest of the USA and northeast of Mexico. It is probably also found in New Mexico and Texas in the USA and Sonora and Chihuahua in Mexico.     Known Nearctic records. Mexico (Baja California, Coahuila, Nayarit, Morelos, Sinaloa, Sonora); USA (Nevada, Texas).

Anthrax georgicus Macquart, 1834
Comments. Apparently closely related to A. irroratus, A. oedipus has a narrow distribution in the Nearctic region but is widely distributed in all South America. In the USA it has been collected only in two southern states, while it occurs in most of the northern states of Mexico and one central state (Morelos); it may be present in most areas from Texas to Argentina. Figure 10b Material examined. CHU: Apr (1 F, 1 M).

Comments.
With just two specimens collected, A. pauper appears to be a rare species in this region. This population is the most southern recorded of this species, mostly present in the center and east of the USA. Presumably adapted to colder climates, it is no coincidence that it was collected in the most elevated site sampled.  Comments. This species is recorded mostly from the south of the USA and north of Mexico, but its presence in Puebla in central Mexico suggests a wider distribution within the country, at least in all northern states.

Genus Dipalta Osten Sacken
Remarks. Dipalta is a small genus with just two species. Dipalta banksi Johnson, 1921 is only present in eastern Canada and USA, while D. serpentina is distributed from Central America to the northern USA.  Comments. This species is probably present in all of Mexico, but this is the only record in the north of Mexico.

Genus Hemipenthes Loew
Remarks. Hemipenthes is equally diverse in the Nearctic (29 species), Neotropical (26 species) and Palearctic (37 species) regions, with just six species in the Oriental region and one in the Afrotropical region. Four species of this genus were collected in Coahuila. All of these have broad distributions but apparently from poor sampling because records are not continuous, especially in Mexico. Ávalos-Hernández (2009) recently published a revision of Hemipenthes, with a key for Nearctic species.     Known Nearctic records. Canada (Alberta); Mexico (Baja California, Baja California Sur, Coahuila, Chihuahua, Guerrero, Morelos, Puebla, San Luis Potosí, Sonora, Tamaulipas); USA (Arizona, California, Colorado, Idaho, Louisiana, Nevada).

Hemipenthes jaennickeana (Osten Sacken, 1886a)
Comments. This species is abundant in the rainy season in most of the Nearctic region but has not been collected in many states of Mexico or the USA where it probably is present.  Comments. Males of this species are abundant all year long but females are unknown. There is no explanation for this lack of females in the collections. Extreme sexual dimorphism and misidentification of females can be dismiss, since there is no Hemipenthes species from which only females are known. One possible explanation is that females life span is too short and therefor encounter probabilities are low. Distribution is discontinuous with populations present in central and northern Mexico and the southern USA; it is unknown whether this species is present in between these areas.  Comments. Hemipenthes sinuosa is only known from Morelos in the center of Mexico and Coahuila in the northeast, but can be found almost in all of the USA. It is clearly undersampled in Mexico.

Genus Lepidanthrax Osten Sacken
Comments. Lepidanthrax hyposcelus is endemic to Mexico, previously only known from the southwest of the country; this record extends its distribution to the northeast of the country.  Known Nearctic records. Mexico (Baja California, Baja California Sur, Coahuila, Durango, Guerrero, Morelos, Sonora); USA (Arizona, California, Nevada, New Mexico, Utah).
Comments. Lepidanthrax proboscideus, L. fuscipennis Hall, 1976 and L. disiunctus are the only species of this genus distributed in both the Nearctic and Neotropical regions. Of these L. proboscideus extends as far as El Salvador, the most southern distribution for a Nearctic species of this genus. This is the first record of this species in the northeast of Mexico.
Comments. Neodiplocampta (N.) miranda and N. (Agitonia) sepia Hull, 1966 are the only two species distributed in both biogeographic regions (Nearctic and Neotropical). This species is distributed from the south of the USA to Nicaragua, but has not been collected in most Mexican states. This lack of records is possibly due its low abundance.

Genus Paravilla Painter
Remarks. Fifty five of the 58 species of the genus are Nearctic. All species of Paravilla collected in Coahuila were exclusively collected in the summer months from April to July. Hall (1981a)        Known Nearctic records. Canada (Ontario, Manitoba); Mexico (Coahuila); USA (Alabama, Florida, Georgia, Iowa, Kansas, Michigan, Minnesota, Mississippi, Nebraska, Ohio, South Dakota, Wisconsin).
Comments. Paravilla separata is present mainly in the eastern half of the USA, and southeastern Canada. This record in Coahuila represents the southern extreme of the distribution of this species, and is the first in Mexico. It may also be present in Tamaulipas and Nuevo León but doubtfully in the northwest of Mexico.

Genus Poecilanthrax Osten Sacken
Remarks. Four species from this mainly Nearctic genus are recorded in Coahuila for the first time. Painter and Hall (1960)   Comments. This record fills a gap in P. effrenus distribution between northwest and northeast populations of Mexico. This species is probably present in Baja California and Nuevo León, but has not yet been recorded.   Comments. This record extends the distribution of P. hyalinipennis into the northwest of Mexico. Considering its distribution in the USA, this species may also be present in the northeast of Mexico. Figure 16d Material examined. REE: Apr (2 M).
Comments. Most of the records in the USA and Mexico of this rarely collected but widespread species are from Pacific Coast states, although, there are records from Nuevo Leon and Coahuila in northeast Mexico.

Genus Rhynchanthrax Painter
Remarks. Of the seven species of this exclusively Nearctic genus, six are present in Mexico, with R. maria (Williston, 1901) and R. nigrofimbriatus (Williston, 1901) being endemic to this country. Only Rhynchanthrax parvicornis (Loew, 1869) has not been collected in Mexico, but it is distributed across the southern USA and may also occur in the north of Mexico.  Known Nearctic records. Mexico (Coahuila); USA (Arizona, California, Colorado, Nebraska, Nevada, New Mexico, Utah).

Rhynchanthrax capreus (Coquillett, 1887)
Comments. This is the first record of this species in Mexico. Rhynchanthrax capreus is the only species occurring in the northwest of the USA, while the other species in the genus are present mainly in the south and east of the country. This species may also be present in the northwest of Mexico (Baja California, Sonora, Chihuahua). (  Known Nearctic records. Mexico (Coahuila, Sonora); USA (Kansas, New Mexico, Texas).

Rhynachantrax texanus
Comments. This is the most eastern record in Mexico for this species. In the USA it is distributed in the southern-center of the country, but in Mexico it has been collected in Sonora so it probably also occurs in Arizona.

Genus Thyridanthrax Osten Sacken
Remarks. Thyridanthrax has twice as many species in the Palearctic region as in the Nearctic and Neotropical regions combined. All 12 species in North America are present in the USA with five also in Mexico. These are the first records of this genus in Coahuila. The distribution of T. selene (Osten Sacken, 1886b) and T. pallidus (Coquillett, 1887) are very similar, being present in all of the southern USA and probably also in all of northern Mexico, although they have been only collected in Sonora and Coahuila to date. Both species are rare and were collected only in April.   Comments. This is the most eastern record in Mexico.

Genus Xenox Evenhuis
Remarks. Of the five species that constitute this genus, four are present in Mexico.
Known host. Xylocopa micheneri micheneri (Hurd) (Apidae) as reported by Minckley (1989).  Comments. Xenox xylocopae appears to be restricted to the northeast of Mexico and south of the USA. Three of the other species also have restricted and separate distributions: X. delila Loew, 1869 is present in the northwest of Mexico and California; X. nigritus (Schaeffer, 1768) occurs from the northeast of Mexico (Veracruz and Tamaulipas without overlap with X. xylocopae) to South America; and X. tigrinus (De Geer, 1776) is present in the eastern USA and southern Ontario. Only X. habrosus (Marston, 1970) has a distribution overlapping with the other four species, being present in all of Mexico and the southwest of the USA.

Discussion
The data presented here increase the knowledge of Bombyliidae in Mexico but also reveals the deficiencies in sampling of the family in the country. The species list for the state increased three-fold, which demonstrates the lack of knowledge of the Bombyliidae fauna in this region. Almost all states of Mexico are in a similar situation but northern states appear to have higher diversity and should be priorities for sampling. Hull (1973) identified the northwest of Mexico as a species concentration area of Bombyliidae, but the northeast portion of the country may have the same species richness. Diversity of this family in the north of Mexico is probably much higher than recorded, as indicated by the richness in the south of USA which has similar environmental characteristics but much better sampling. Therefore northeast Mexico is possibly one of the most under sampled areas in the Nearctic region for Bombyliidae, given the great diversity of this family in the area, combined with the size of this part of the country. The study of Bombyliidae in the northern states of Mexico should be more of a priority than field work in the center or the southern states.
Most of the species collected in this study have a broad distribution in the USA but Mexican records are isolated. There are probably more species yet to be recorded from Coahuila and other Mexican states, especially species present in southern border states of the USA. Some species are recorded only from Coahuila in the northeast of Mexico but are also present in the northwest of the country. More studies are required to determine if these species have a disjunct distribution or if any are represented by distinct, cryptic eastern and western species.
Cuatro Ciénegas' biological and conservational importance has long been recognized for reptiles (McCoy 1984), birds (Contreras-Balderas 1984), plants (Pinkava 1984, Villarreal andEncina 2005), snails (Hershler 1984), Crustacea (Cole 1984) and particularly fishes (Minckley 1984), but little is known of other groups like insects. The insects contain 53% of the described species in the planet (Chapman 2009), so their distribution and diversity should be considered for conservation and natural reserve design. The diversity of insects, especially of Bombyliidae and similar arid-regions-diverse groups, increases the conservational value of Cuatro Ciénegas.

Conclusions
The data presented here indicates the significance of Cuatro Ciénegas for Bombyliidae diversity. Comparison with other nearby areas should be undertaken to confirm whether this area really is richer for this family. Data also reveal that true species richness of Bombyliidae is much higher than previously recorded. This could also be true for other insect groups. More funding should be destined for faunistic studies of megadiverse groups with ecological importance such as Diptera, Coleoptera, Hymenoptera and Lepidoptera. The information obtained from these studies might be used first to quantify the species richness and species exchange between areas (beta diversity) (Whittaker 1972) and later to propose conservation management schemes.