New fly records of potential biological control importance in Saudi Arabia (order Diptera)

The Ministry of Environment, Water and Agriculture in Saudi Arabia has begun funding some projects to set up some agricultural pest control programs. Therefore, it is very important to enumerate all the predacious or parasitic insects that live on or in other agricultural insect pests and have the potential to become biological control agents against these pests. In the present study, nine fly species of potential importance in biological pest control are recorded for the first time from Saudi Arabia, namely, Spogostylum ventrale Bezzi, 1924, Prothaplocnemis anthracina (Becker, 1902) [family Bombyliidae], Alloxytropus anomalus Bezzi, 1925, Scenopinus minusculus (Séguy, 1934) [family Scenopinidae], Actorthia frontata Kröber, 1912, Hoplosathe brevistyla Lyneborg & Zaitzev, 1980 [family Therevidae], Hilara sp. [family Empididae], Tomosvaryella demeyeri Kuznetzov, 1993 [family Pipunculidae] and Orchisia costata (Meigen, 1826) [family Muscidae]. In addition, this is the first time to record the four genera Prothaplocnemis Bezzi, Alloxytropus Bezzi, Hilara Meigen and Orchisia Rondani from Saudi Arabia. World and local distributions, diagnoses, feeding behaviors and some colored photographs of recorded species are provided. In the present study, nine species of predacious and parasitic flies belonging to nine genera and six families are recorded for the first time in Saudi Arabia.


Background
Traditional management of agricultural pests using pesticides has damaging effects on many non-target terrestrial arthropods in agro-ecosystems, including the natural enemies (predators and parasitoids) of these agricultural pests (El-Wakeil et al. 2013).Insecticide treatments are also challenged by the stringent residue levels applied in export markets, in the broader context of the adverse effects that have been recognized on human and ecosystem health.As a result, management practice has evolved toward alternative methods such as biological control techniques (Bourguet and Guillemaud 2016).Biological control has been the most researched control tactic within any management programs, and parasitoids have been the main natural enemies used against pestiferous arthropod species (Dias et al. 2018).However, although predators are not the focus of many biological control programs, they play an important role in conservation biological control, and studies that evaluate or use agricultural techniques that do not affect an assemblage of predators of some pests, such as the use of selective pesticides, must be intensified (Garcia et al. 2020).Also, predators are the key natural enemies important in the biological control of certain pests as aphids (Bugg et al. 2008).
There are many essential integrated elements and steps for any successful classical biological control program.The preliminary taxonomy and survey studies of candidate natural enemies as predators and parasitoids are among the most essential of these steps.Although all other steps are necessary in any program, the major research objectives concentrate on the preliminary taxonomic and survey of natural enemies (Van Driesche and Bellows 1996).
In the present study, nine species of predacious and parasitic flies belonging to nine genera and six families have been recorded for the first time in Saudi Arabia.Four of the genera have been also recorded for the first time, giving taxonomic and faunistic significance to the study, namely Prothaplocnemis Bezzi (family Bombyliidae), Alloxytropus Bezzi (family Scenopinidae), Hilara Meigen (family Empididae) and Orchisia Rondani (Family Muscidae).
Considering the southwestern part of Saudi Arabia as affiliated to the Afrotropical Region, Actorthia frontata Kröber (family Therevidae) has been recorded herein for the first time from the Afrotropical Region, as it was collected from Najran Province.
Only two families, out of the six treated, were extensively studied in Saudi Arabia, Bombyliidae [by El Hawagry and Al Dhafer (2019a) and El-Hawagry et al. (2022)] and Muscidae [by Dawah et al. (2020)]; however, only a few number of species from the remaining four families were separately recorded in some miscellaneous papers.

Methods
Material was collected since 2018 by the authors and/or their coworkers using aerial nets from various locations in Saudi Arabia.Only three specimens of Tomosvaryella demeyeri were also collected using Malaise traps from Tabuk in 2021.Specimens were identified by the first author using relevant keys, and identifications of the Therevidae and Muscidae were confirmed by Dr. Martin Hauser and Dr. Adrian Pont, respectively.
The type locality for each recorded species is given.For recorded species, world distributions as reported in world catalogs and related studies, local distributions, diagnoses, comments on feeding behaviors and some colored photographs are provided.
Photographs were taken using a Leica MZ 125 stereo microscope (Leica Microsystems Ltd, St. Gallen, Switzerland), fitted with a digital camera (Q-imaging Micro Publisher 5.0 RTV; Zerene Systems LLC, Richland, WA, USA) at the Plant Protection Department, College of Food and Agriculture Sciences, King Saud University.Photograph auto-montage was performed using the Zerene stacker program version 1.04 (Innovative Solutions, Bucharest, Romania).
Since Saudi Arabia has no distinct ecological zones, administrative divisions (also called regions or provinces) are used instead, namely: Al-Baha, Al-Jawf, Al-Madinah, Al-Qasim, Jazan, Najran, Riyadh, Tabuk, etc. Countries in world distributions and regions in local distributions are listed alphabetically.Localities within each region are written after a colon, followed by the coordinates in parentheses, followed by the governorates to which they belong within square brackets, e.g., "Al-Jawf: Baseita (29.872219°N, 38.306257° E) [Tabarjal Gov.]."
Diagnosis Large flies, about 10 mm in length (Fig. 1); frons with black hairs, usually mixed with white or yellowish-white hairs and scales; lower part of face with long white hairs mixed with few black ones; thorax with scutum and scutellum clothed with yellowish-white tomentum, with black bristles at margins; wings hyaline, with only two submarginal cells, with inconspicuous ill-defined brownish spots on cross-veins and origin of vein R 2+3 ; abdomen covered with yellowish-brown scales and black hairs, with tufts of long flattened black or dark brown hairs and scaly hairs on sides of 2nd and Feeding behavior Species of the genus Spogostylum are known as ectoparasitoids of solitary bees, wasps, egg pods of Acrididae and cocoons of pyralid moths (Yeates and Greathead 1997).
Remark This is the first time to record the genus Prothaplocnemis Bezzi and its species P. anthracina Becker from Saudi Arabia.
Diagnosis Small fly, about 3 mm in length; cuticle shining black with patches of white hairs and scales and glossy black scales; frons and lower part of face with short black hairs; face slightly gray pollinose; occiput with some white scales; wings iridescent, hyaline; legs black, covered with faint yellowish scales; fore tibiae smooth; laterotergite with a tuft of white hairs; 1 st abdominal tergite covered with white scales, its sides with tufts of white hairs; other tergites covered with only sparse black hairs and traces of white scales on the last two tergites, their sides with white hairs.
Feeding behavior This species is thought to be a predator of the eggs of Acrididae and the pupae of noctuid moths (Greathead and Evenhuis 2001).
Remark This is the first time to record the genus Alloxytropus Bezzi and its species A. anomalus Bezzi from Saudi Arabia.
Feeding behavior In general, the larvae of the family Scenopinidae are all predaceous on other arthropods (Kelsey 1969).
World distribution AF: Madagascar, Seychelles.PA: Saudi Arabia (first record).[Sources: Kelsey (1969)  Diagnosis Small fly, about 2.5 mm in length; head dark brown; frons shining with central depression; ocellar triangle slightly prominent; antennae black with flagellum covered with short hairs; thorax shining; wings smoky white; halter white; legs brownish, with tarsi yellowish; abdomen dark brown, with 8th sternum short.
Feeding behavior In general, the larvae of the family Scenopinidae are all predaceous on other arthropods (Kelsey 1969).

Family Therevidae
Actorthia frontata Kröber 1912  Remark Considering the southwestern part of Saudi Arabia including Najran Province as affiliated to the Afrotropical Region, this species is recorded herein for the first time from the Afrotropical Region.
Diagnosis Medium-sized fly, about 6.5 mm in length (Fig. 3); head dusted light ash gray, with short white hairs; antennae yellowish, with flagellum somewhat darkened; thorax black in ground color, dusted yellowish-gray, with fine pale yellow hairs, with basal half of scutellum velvety black-brown; thoracic pleura light ash gray; halter creamy-white; legs blackish with, with basal half of mid and hind tibia reddish-yellow, with coxae and femora gray dusted; anterior cubital cell (cua) and third medial cell (m 3 ) cell closed and long stalked; abdomen reddish brown at basal half, shiny black at apical half; abdominal tergites with creamy apical margins, with short white hairs.
Feeding behavior Larvae are important predators of soft bodied arthropods in agricultural and forestry ecosystems, attacking a wide variety of pest insect larvae (Hauser 2017a andHauser et al. 2017b).
World distribution AF: United Arab Emirates.PA: Iran, Saudi Arabia (first record).Diagnosis Large fly, about 10 mm in length (Fig. 4); head whitish-gray tomentose, tinged yellowish on upper part of occiput; antennae yellowish, with terminal stylus blackish; flagellum at most 2.5 × as long as wide from lateral view; mesonotum with three brownish-gray vittae, all three vittae with same color; scutellum brownish, slightly darkened on dorsal surface; wings banded; femora predominantly grayish, yellowish-brown apically and at extreme bases; abdomen with orange coloration on the first five tergites; postero-lateral corners of 2nd, 3rd and 5th abdominal tergites with small white pollinose spots; halter yellowish-brown with knob darkened at tip.
Feeding behavior Larvae are important predators of soft bodied arthropods in agricultural and forestry ecosystems, attacking a wide variety of pest insect larvae (Hauser 2017a andHauser et al. 2017b).Diagnosis Small fly, about 2.3 mm in length (Fig. 6); head spherical; face almost equal in width to lower part of frons; frons not swollen when seen from lateral view; occiput swollen, clearly visible from lateral view; flagellum dark brown with yellowish tip, distinctly larger than pedicel; wing without pterostigma; discal medial cell (dm) expanded convexly distally after r-m cross-vein; cross-vein r-m located at middle of cell dm; legs mainly dark brown, yellowish or tawny brown at tips of femora, bases and tips tibiae and basal tarsomeres; hind femur with distinct ventro-basal protuberance, with some distinct spines; epandrium longer than wide; surstyli short, widened in the middle and gradually tapering toward the tip when viewed from the dorsal view.

and present study]
Remark This is the first time to record the genus Orchisia Rondani and its species O. costata (Meigen) from Saudi Arabia.Diagnosis Small-to medium-sized fly, about 4 mm in length (Fig. 7); head yellowish in ground color, with frontal vitta brownish to orange; fronto-orbital plates with grayish dust; parafacialia and cheeks yellowish with grayish dust; antenna yellowish with flagellum slightly darkened and arista short plumose along its entire length; palpi yellowish; thorax black in ground color, gray dusted; scutellum with only the apical pair of setae strong; legs predominantly yellowish-brown; wings pale smokybrown, conspicuously darkened along costal margin, with spinules along costa strong and erect; halter yellowishbrown to orange; abdomen predominantly yellowishbrown, grayish dusted, darkened at last three tergites.

Local distribution
Feeding behavior As members of the muscid subfamily Coenosiinae, adults are predaceous (Gregor et al. 2002).

Discussion
The present paper is a part of serial studies planned in the Kingdom of Saudi Arabia aiming to enumerate all the predacious or parasitic flies living on or in other agricultural insect pests.These flies have the potential to be used as biological control agents against these pests and as a key component in any agricultural pest management (El-Hawagry and Al Dhafer 2019).
Native parasitoid and predator species surely adapt better to natural environmental conditions and can even be used to complement exotic parasitoid and predator species that may be introduced from other places for biological control programs (Miranda et al. 2015).
In different farming systems, various parasitic and predatory insects play important roles in reducing problems with agricultural pests (Bugg et al. 2008), and biological control has been the most researched control tactic within many pest management programs (Garcia et al. 2020).Information regarding the diversity of parasitoids and predators on agricultural pests in Saudi Arabia is still limited; therefore, this study may help in compiling a list of parasitoid and predator species associated with agricultural pests and have the potential to be used as biological control agents against these pests and a key component in any future agricultural pest management.
Although the family Bombyliidae, for instance, was studied intensively in Saudi Arabia and 123 different species were recorded by El-Hawagry and Al Dhafer (2019) and El-Hawagry et al. (2022), two other species have been recorded for the first time in the present study.This certainly indicates that the data on fly distribution in Saudi Arabia are still scanty, and more efforts are highly desired in the future.

Conclusions
In the present study, nine species of predacious and parasitic flies belonging to nine genera and six families have been recorded for the first time from Saudi Arabia and added to the country's fly fauna.