The Carabidae (Coleoptera) of Shada Al-A’Ala Nature Reserve, Southwestern Saudi Arabia, with description of a new species of Paussinae

Abstract We report the Carabidae collected at the Shada Al-A’Ala Nature Reserve (SANR) in Baha Province in southwestern Saudi Arabia during 2013–2015. In total, 62 carabid species and subspecies representing 39 genera, 17 tribes, and 10 subfamilies were identified, including one new species, Paussusminutulus Nagel & Rasool, sp. n, four new country records, and 24 species that are new provincial records for Baha. The carabid fauna was dominated by the Lebiini with 19 species. A high number of species were rarely collected (34 species) in comparison to the more abundant and common species (9 species). The highest number of species (52 species) was collected during autumn. The carabids of SANR are represented by a large component of Afrotropical faunal elements (28.1%) and smaller numbers of Oriental species (3.5%) and endemic taxa (5.3%). In comparison to Garf Raydah Nature Reserve in Asir Province, also in southwestern Saudi Arabia, SANR had an equal number of carabids sharing 64.5% of the species but with lower number of endemic elements. Our study can serve as a component for implementing a conservation plan for SANR using carabid beetles as sentinel taxa. These research results may support future ecological studies on SNAR carabids.


Introduction
Over the past three decades, numerous new wildlife protected areas have been established in Saudi Arabia (SA). Not only the number of national parks has increased but also newly established nature reserves, wildlife sanctuaries, and other protected landscapes and biosphere reserves (Abuzinada 2003). It is noted that SA has currently 16 protected areas and 12 national parks (Abuzinada 2003;SWA 2018). For this network of protected areas, biodiversity monitoring is fundamental for effective management. The invertebrate fauna of these protected areas has attracted relatively little attention as compared to those of vertebrates (Abuzinada et al. 2005), although international conventions signed by SA as a member of the Convention on Biological Diversity since 2001 (CBD 2011). Recent insect biodiversity survey and monitoring research projects in several protected areas in SA have been conducted by King Saud University Museum of Arthropods, Riyadh; resulting in several faunistic and ecological works being published (Aldhafer et al. 2012Sharaf et al. 2013;Abdel-Dayem et al. 2016El-Hawagry et al. 2016. One of these recent projects was focused on the insect biodiversity of Shada Al-A'Ala Nature Reserve (SANR) in Baha Province in southwestern SA. The location and elevation range (470-2,222 m) of the SANR provides relative high rainfall, diverse microclimates, and a distinct biodiversity (SWA 2018). The SANR is undoubtedly one of the most interesting protected areas in SA because of the existence of unique treasure trove of biological diversity. About 22% (495 plant species) of the total SA flora has been reported from the Shada Mountains including 19 endemic plant species and 43% endangered species (Thomas et al. 2017). The SANR harbours important faunas, including griffon vultures and other endemic birds of the southwestern mountains and carnivores (e.g. the rock fox, caracal, striped hyena, wolf, genet, and the Arabian leopard) (SWA 2018). Regarding insects, 119 species of flies (Diptera) have been reported from the SANR (El-Hawagry et al. 2016).
However, despite the urgent conservation concerns associated with the SANR reserve, there have been no studies focused on beetles including the Carabidae. Thus, the objectives of this study are to provide a thorough baseline inventory of the carabid fauna of the SANR and to analyze its zoogeographical affinities. This information will assist in providing an essential cognitive basis for future management of this reserve. Additionally, our results will allow for future ecological studies of carabids of SNAR and will contribute to the overall knowledge of Carabidae of SA, the largest country of the Arabian Peninsula.

Study area
In Shada Al-A'Ala (Upper Shada) Mountain, an outlier of the Sarawat Mountains to the west, the SANR was established in 2002. The reserve is located (latitudes 19°48.894'-19°52.578'N and longitudes 41°17.130'-41°21.000'E) in Al-Mekhwa District (Baha Province); about 20 km southwest of Al-Mekhwa City, the capital of the district (Fig. 1). The SANR occupies an area of 67 km 2 and rises about 2,222 m. There is a perennial small freshwater stream in Wadi Neera at the west and southwest part of the reserve. Geologically the area belongs to the greater Afro-Arabian shield, which is a part of the Precambrian crust plate and is generally exposed and locally covered by tertiary volcanic rocks (Schmidt et al. 1972). There are terraced fields used by small local communities; these fields are very small scale and are used to grow distinctive varieties of coffee, banana, lemon, and natural figs (SWA 2018). The climate is similar to the uplands of southwestern SA. It is highly variable and characterized by cool winters, warmer partly cloudy summer, and high rainfall. The average annual temperature of 26.2 °C, and average annual rainfall of about 200 mm, and with wettest period concentrated between March and May (43% annual precipitation) (El-Hawagry et al. 2016).
The vegetation is rich, with the Leguminosae (Fabaceae) and composites (Asteraceae) having the highest contribution, followed by graminoides (Poaceae) (Al Zubaide et al. 2017, Thomas et al. 2017. The vegetation comprises 72.4% perennials and 27.6% annuals; represented by 17.2% trees, 51.8% shrubs, and 31.1% weeds (Al Zubaide et al. 2017). The vegetation at the foothills of Shada Al-A'Ala Mountain consists predominantly of subtropical Acacia thorn woodlands extending from the base up to

B
A 1500 m a.s.l. The vegetation above 1000 m elevation is dominated by Acacia asak (Thomas et al. 2017

Beetle collection
As part of a research project for studying the insect biodiversity in the SANR the adult ground beetles were sampled from 2013-2015. The sampling was conducted at various sites in varied habitats at 13 different elevation levels (Table 1) within the SANR. The geographical coordinate data of each collecting location were recorded using GPS Garmin, Montana 650 unit (Garmin Instruments Inc., Olathe, Kansas, USA).
Collected beetles were initially sorted to morphospecies level, mounted and then identified to species levels. Some species were sent to experts for identification or confirmation, as indicated in the remarks. The specimens are deposited in the collection of King Saud University Museum of Arthropods (KSMA), King Saud University, Riyadh, SA.
The description of the new species of Paussus was assisted using a Leica M205C dissecting microscope with 10× eyepieces and Planapo 1.0× and 1.6× front lenses, allowing magnification up to 240×. An eyepiece micrometer was used for measurements.

Classification and nomenclature
The subfamily and tribal classification of the family and nomenclature of the species in this study follows the Catalogue of Palaearctic Coleoptera (Löbl and Löbl 2017). However, the taxonomic order of species in the genus Sphaerotachys J. Miller, 1926 (Trechinae, Bembidiini) follows Sciaky and Vigna Taglianti (2003). The subfamilies, tribes, genera and species are listed alphabetically.

Faunal list
For each species, the following information is provided: current nomenclatural combinations, material examined, zoogeography, distribution, published records in SA, and remarks. The label data for examined specimens are listed as follows: elevation level within the SANR, followed by the date of collection (months as Roman numerals), the collecting method (handpicking (HP), light traps (LT), malaise traps (MT), pitfall traps (PT), sweeping net (SW) and vacuuming (VC)) and the number of examined specimens followed by sex (♂ for male, ♀ for female, ex(s) for example with unidentified sex). The material examined is arranged in ascending order with respect to the elevation, then chronologically with respect to the month of collection. A semicolon separates different records; if these are from the same elevation, the elevation is listed only at the beginning with the older record.

General distribution and zoogeography
The zoogeography, which were used in the analysis of carabid faunal affinity, were assigned for each species using the zoogeographic realms of the world suggested by Holt et al. (2013). The zoogeography is based on their modern general geographical distributions (each country is represented by two capital letters according to ISO 3166 "ISO Alpha VC-2 Country code": The Nations Online Project: https://www.nationsonline. org/oneworld/country_code_list.htm :) provided by Löbl and Löbl (2017) and Lorenz (2017) unless otherwise stated.

Results
During this study, 3,287 adult carabid beetles were collected from SANR, comprising 62 species from 39 genera within 17 tribes and 10 subfamilies. These species include the description of a new species (Paussus minutulus sp. n.), three SA endemic species and six confined to Arabian Peninsula. Four species have not been previously recorded from SA, and 24 species recorded for the first time from Baha Province. The details of these species are provided in the faunal list below. Of the carabids collected from SNAR, the most diverse tribe was the Lebiini, represented by 19 species (30.6% of the total species) in 13 genera (33.3% of the total genera) (Fig. 2). About 50% of the tribes are represented by one or two species. Nine species (14.5%) are classified as abundant and common species; Lebia nilotica, Metadromius arabicus, Sphaerotachys conspicuus (Schaum, 1863) were the most abundant species, comprising 50.4% of the total catch. Twenty species (32.3%) are considered rare, represented by four or fewer individuals collected over the two years. The maximum number of species were collected during autumn (52 species). The genus Anthracus Motschulsky, 1850 was recorded for the first time for SA. Three species have been identified to the genus level, belonging to Amblystomus, Metadromius and Singilis.   Remarks. A frequent species that was collected during autumn. The adults were found under stones along the margins of a freshwater stream and collected by hand. Additional adults collected at night by using lights. Erich Kirschenhofer identified this subspecies. Published records. Jizan and Makkah (Britton 1948). New provincial records for Baha.

Chlaenius pachys
Remarks. A rare species that was collected during late autumn. The two adults were found under stones along the edge of freshwater stream collected by hand picking. Erich Kirschenhofer identified this species. Published records. Jizan (Mateu 1990). New record for Baha Province. Remarks. A rare species that was collected during late summer and autumn. The above specimens were collected by light traps set at lower altitude in Acacia thorn woodlands. David Wrase and Boris Kataev identified this taxon.

Remarks.
A rare species that was collected during summer and autumn from Acacia thorn woodlands. David Wrase identified this species. General distribution and zoogeography. OM, SA. This range exemplifies SAR realm. Published records. Asir (Mateu 1986), Baha (Rasool et al. 2018a). Remarks. A rare species that was collected during autumn and summer, represented by a single specimen during each season. Ron Felix identified this species.  (Mateu 1979).

Merizomena buettikeri
Remarks. An abundant species that was collected during all four seasons with most specimens caught during late summer (September). The adults of this species were only collected using light traps. Iftekhar Rasool, Mahmoud Abdel-Dayem and Ron Felix identified this species. Remarks. A rare species that was collected during late winter. It is similar to M. ephippiatus (Fairmaire, 1884), which is known from North Africa (DZ, MA, TN) (Löbl and Löbl 2017). However, these specimens along with SA specimens identified by Mateu (1986) (Mateu 1986). New record for Baha Province.
Remarks. A rare species that was caught by light trapping during the different seasons from Acacia thorn woodlands. Alexander Anichtchenko identified this species. Remarks. A rare species that was collected by light trapping in Acacia thorn woodlands during autumn. This unidentified species is closely related to S. cordiger (Peringuey, 1896), which is known from NA, ZA and ZW. Unfortunately, only a single female was collected, and males are needed for identification. Alexander Anichtchenko identified this species.

Paussinae
follows: antennal club with excavation ending far in front of apex; head with vertex produced, with two distinct pores at the top; collar of anterior pronotum low, with transverse edge rounded and with lateral projections absent; pronotal trichome well developed at both ends of transverse furrow; pygidium with lower (posterior) margin with dense fringe of hair; fore and middle legs robust, not compressed, hind femur dilated and flattened, hind tibiae little wider than thick; small, apically fringed setae present at several body parts, most obvious at antennomere 1 and all legs.
Description of female holotype specimen. (Fig. 5) Standardized body length from tip of head to tip of elytra 3.4 mm (3.5 mm total body length from tip of head to tip of pygidium), width across mid-elytra 1.5 mm. Body castaneous, appendices little darker, ventral abdomen and anterior part of pronotum little lighter; compacted or reinforced marginal areas of head, antennal clubs and pronotum narrowly blackish. Surface smooth and shining, except forehead matt and antennomere 1 (scape) with dense and coarse, yet shallow punctuation. Pubescence of elytra inconspicuous, restricted mostly to apical and lateral parts (abraded in the middle?), of short and upright as well as recumbent, narrowly lanceolate setae; elytra additionally with very few, long, thin, upright setae on lateral part of disc and as series umbilicata; head, pronotum, pygidium and appendices with scattered, short, mostly appressed setae; these short setae have a multiple split (fringed) apex and are most obvious at antennomeres 1, femora and tibiae, yet absent at   elytra; antennal clubs with the normal apical sensory field and with scattered upright or slightly curved medium setae. Head 1.3 times wider than long, frontal margin broadly truncated, slightly biconvex; in dorsal view head in front of eyes little narrowed apically, gena and eye of equal length; temples not projecting; head with vertex produced, with two distinct pores at the top; pores broadly marginate with orifice slightly sunk. Antennomere 1 devoid of distinctly marked longitudinal edges; antennal club excavate on its exterior (posterior) side, 1.5 times longer than wide (basal tooth disregarded), tumid; frontal margin distinctly emarginate near base, with one small and one tiny fenestriform pit; anterior basal angle of club acute, marked; posterior basal projection large, thick, apically truncate; hind (exterior) side of the club with excavation limited by broad dorsal and ventral borders, and ending far before apex; at posterior view dorsal and ventral margins of excavation swollen, undulate with 3 or 4 low tubercles, each with one to three subapical setae; club without distinct trichome near ventral base, just an indistinct assemblage of three slightly thicker setae. Mouthparts as shown in Figure  6, not dissected; ligula at ventral view with longitudinal carinula in the middle of the disc (not shown in Fig. 6); (antepenultimate) maxillary palpomere II at broadest view 1.5 times as long as wide with mesal margin almost straight; (terminal) labial palpomere III long, narrow, five times as long as wide, apically rounded; gula with width/length ratio at narrowest point 0.9 (for measurement see Robertson and Moore (2016). Pronotum approximately as long as wide (1.1 times wider), transversely bipartite, with large trichomes at both ends of furrow; anterior part little wider than head (1.2 times), low, with transverse dorsal edge of collar broadly rounded, slightly indented in the middle, not angulate, lateral angles obscure; posterior part narrowed towards base. Elytral pubescence of two types: a few, very scattered, thin, long, erect setae on lateral parts of the disc (in addition to the similarly looking hairs of the series umbilicornis), plus scattered, recumbent, narrowly lanceolate setae on lateral and apical parts of disc; lateral subapical folds ("flange of Coanda") normal, without peculiarities. Hind wings present. Pygidium with central disc almost even, with indistinct microsculpture, weakly shining; lower (anatomically posterior) margin explanate; pygidial trichome of dense fringe of long hair set semicircular along lower margin; ventral part of explanate margin set with one row of short, appressed setae. Legs robust, femora and tibiae of fore and middle legs not compressed, hind femur and tibia slightly compressed and dilated, the whole inner side of hind tibia with longitudinal shallow groove; pubescence of femora and tibiae of scattered, small, apically fringed setae; all tibiae without terminal spurs; terminal tarsomere of posterior tarsus as long as three preceding ones together; tarsomeres ventrally with few lateral setae, and glabrous in the middle. Inner side of hind femur subbasally with file of stridulatory organ; the file consists of multiple parallel fine grooves and is located at both the anterior and posterior parts of a longitudinal, short carinula.
Male. Unknown. Distribution. The new species is only known from the holotype female specimen from the type locality at Shada Al-A' Ala Nature Reserve.
Ecology. This single specimen of Paussus was found in an area with low impact small-scale agriculture. The vegetation is characterized by dominant cactus pear. The altitude is ca 1610 m, the winters are cool and most of the 200 mm annual rainfall is concentrated between March and May (see details in chapter "Study area" above). The specimen of P. minutulus sp.n. was taken by a pitfall trap which also caught ants of the following taxa: Camponotus aegyptiacus Emery, 1915;Messor ebeninus Santschi, 1927;Monomorium jizane Collingwood & Agosti, 1996;Pheidole Westwood, 1839, sp.;Tetramorium simillimum Smith, 1851) and Tetramorium sericeiventre Emery, 1877. Members of all these genera are known as host of one or more species of Paussini (Geiselhardt et al. 2007). Paussus minutulus sp.n. forms part of the Afrotropical P. cucullatus species group, of which several members are known to be associated with Pheidole sp., including the Arabian P. rougemontianus (see, for example, Luna de Carvalho 1989).
Remarks. The new species is assigned to Paussus subgenus Hylotorus Dalman, 1823, according to the phylogenetically based classification of Robertson and Moore (2016) (see Nagel et al. 2017a). The description of P. minutulus sp.n. given above agrees generally well the diagnosis and characters used in the key provided by Robertson and Moore (2016) and their subgenus description. The labial palpomere III is longer and narrower than described as usual for the Subgenus Hylotorus, yet still within the range of variation of this character, and similar to P. abditus Nagel, 2018. The lacinia was not dissected. The fringed setae are conspicuous, despite their tiny size. Sometimes, individuals of a few Paussus species were found to show the same type of setae with both split and unsplit apices. In these cases, the splitting is most probably an artifact caused by a treatment during or after collecting (use of certain chemicals in the killing bottle or relaxing chamber, for example). In P. minutulus sp.n. this particular shape is obviously an intrinsic character, because they are alike at all body parts where they occur.
Paussus minutulus sp.n. forms part of the P. cucullatus group sensu lato and is most similar to and possibly part of the same clade as P. abditus Nagel, 2018 (SA) and P. rougemontianus Lorenz, 1998 (Yemen) (replacement name for Cochliopaussus rougemonti Luna de Carvalho, 1989). It differs from P. abditus by the slightly shorter pronotum, the less compressed and dilated hind leg, the absence of a distinct subbasal antennal trichome, the smaller extension of the excavation at the posterior antennal club, the large, thick, apically truncated posterior basal projection of the antennal club, the presence of fringed setae, and the clearly marked, distinct cephalic orifices.
It differs from P. rougemontianus by the slightly shorter pronotum, the less compressed and dilated hind leg, the absence of a distinct subbasal antennal trichome, the dorsal hind margin of the antennal club retracted, the presence of fringed setae, and, above all, the large, thick, apically truncated posterior basal projection of the antennal club in the new species. The new species differs from the little-known Ethiopian P. cyathiger Raffray, 1886, among others, by the long, thin peg-like posterior basal angle of the antennal club, and the longitudinal crescent margin at the external part of the cephalic pores of the latter (see Abdel-Dayem et al. 2018).

Abacetus crenulatus
Remarks. A rare species that was collected during late summer, autumn, and winter by light trapping in Acacia thorn woodlands and Barbary fig shrub communities. Paolo Neri and Mahmoud Abdel-Dayem identified this subspecies. Remarks. A frequent species that was sporadically collected during autumn, winter, and spring in Acacia thorn woodlands. Paolo Neri and Mahmoud Abdel-Dayem identified this subspecies. Remarks. An abundant species, which was collected during all four seasons, with highest number of individuals collected during winter (March) and lowest numbers during the late summer (September). The adults were caught by light traps set at various altitudinal zones ( (Mateu 1986;Balkenohl 1994;El-Hawagry et al. 2013;Moore and Robertson;2014;Häckel and Azadbakhsh 2016;Rasool et al. 2017Rasool et al. , 2018a. The study of El-Hawagry et al. (2013) included the first recorded carabid species in the SANR, reporting only Paussus cephalotes. Häckel and Azadbakhsh (2016) and Rasool et al. (2018) documented 13 species in which Lebia raeesae and Microcosmodes arabicus were newly described. It should be noted that none of these three studies specifically targeted this family for the SANR.

Bembidion niloticum niloticum
This study represents the first baseline inventory of the carabid beetles in SNAR, within the mountains in the southwestern Saudi Arabia. The study revealed 62 species belonging to 39 genera, 17 tribes and 10 subfamilies. This number of species represent about 33% of the total known carabid fauna of SA. Also, our study includes a new species, three species endemic to SA, six confined to Arabian Peninsula, four new country records, and 24 species recorded for the first time from Baha Province. The result expands the number of carabid species recorded from Baha to 67. The number of species in this current list is similar to that of Garf Raydah Nature Reserve (GRNR) in Asir Province (61 species), a much smaller area as compared to SANR ). This may be due to the wide altitudinal range (1,150-2,820 m), high annual rainfall range (600-800 mm/annum), cool temperatures, relatively high humidity, and the presence of the last remnants of dense African pencil cedar forest, Juniperus procera Hochst. ex Endl. (Cupressaceae) in GRNR (El-Juhany 2015, SWA 2018). Both nature reserves sharing about 64.5% (40 species) of the recorded carabid species. The Lebiini species are prevailed the carabid fauna of SNAR (30.6% of the total species), a similar finding was recently being reported from GRNR .
Biogeographically, SA is heterogeneous region that hosts an interesting mixture of biodiversity from Afrotropical, Palaearctic, and traces of Oriental realms due to its position between Africa and Eurasia (Büttiker 1979;Larsen 1984;Hölzel 1998). This mixture of taxa is also apparent in Baha Province, including SANR (El-Hawagry et al. 2016. The carabid fauna of the SANR is characterized by the prevalence of Afrotropical (28.1%) and Saharo-Arabian (19.3%) elements. The influence of the Palaearctic species is moderate (10.5%) and Oriental species is noticeably smaller (3.5%) (Fig. 3). Based on the zoogeographical analysis of the insect fauna, El Hawagry et al. (2013) suggested that the fauna of Baha Province is biologically related to the Afrotropical region rather than to the Palaearctic or Eremic zone and has little Oriental affinity. The specificity of the SANR carabid fauna is enhanced by a small fraction of endemics (5.3%). This percentage of endemic species is low compared to the percentage endemic species of the carabid fauna in Garf Raydah Nature Reserve .
In conclusion, our study provides a first account of the carabid beetle fauna of the SANR, Baha Province, in the southwestern SA. The SNAR has a relatively diverse carabid fauna (62 species), reflecting its rich flora. In its composition, the carabid fauna of SANR has almost the same number of species as GRNR, in Asir Province , and shares with the GRNR 64.5% of its species. The SNAR carabid fauna is mostly of Afrotropical origin with high influence of Saharo-Arabian and relatively little influence of the Oriental elements. The carabid fauna of the SNAR has a low level of endemism and high number of Lebiini species. Extensive surveying of the highlands in southwestern SA, may reveal further species. Beyond enhancing our knowledge of the SA carabid fauna, these results will provide useful information for guiding the conservation activities (Koivula 2011;Kotze et al. 2011) in the SANR and starting point to the future more detailed investigation on the fauna in the southwestern SA.