The Tamarix feeding Leafhopper genus Opsius Fieber, 1866 (Hemiptera, Cicadellidae, Deltocephalinae, Opsiini) in the Kingdom of Saudi Arabia, with description of a new species

The leafhopper genus Opsius Fieber, 1866 is revised for the Kingdom of Saudi Arabia. Seven species are treated, including three that previously were reported by Dlabola (1979), O. pallasi (Lethierry, 1874), O. tigripes (Lethierry, 1876), and O. versicolor (Distant, 1908). Opsius heydeni (Lethierry, 1876), O. richteri Dlabola 1960, and O. scutellaris (Lethierry, 1874) are reported for the first time from the Kingdom. A new species, O. wilsoni El-Sonbati, sp. nov. is described from the southwestern region of the Kingdom of Saudi Arabia. A key to the species of Opsius of the Kingdom is also provided.


Introduction
The Cicadellidae is the largest family of the suborder Auchenorrhyncha, and the Deltocephalinae is the largest leafhopper subfamily with more than 6,700 valid species (Zahniser and Dietrich 2013). The tribe Opsiini is divided into four subtribes including more than 300 species. Recently, the subtribe Opsiina has had additional genera (El-Sonbati et al. 2016, 2017 and species (El-Sonbati et al. 2015, 2018, 2019 added, doubling the known genera from the Arabian Peninsula. The genus Opsius Fieber, 1866 (Opsiini; type species Opsius stactogalus Fieber, 1866) includes at least 20 valid species distributed worldwide. This study records seven species of Opsius from the Kingdom of Saudi Arabia (KSA), including three previously reported by Dlabola (1979Dlabola ( , 1980. Three additional species are reported herein for the first time from KSA and a new species is also proposed from the southwestern region of the country. This region has strong Afrotropical affinities (von Kéler 1955).
Among the 20 species of Opsius, 17 have been recorded from the Palaearctic Region, with only three shared with other regions, O. stactogalus Fieber, 1866, O. versicolor (Distant, 1908) and O. cypriacus Lindberg, 1958. Only O. stactogalus is considered cosmopolitan (Zahniser 2019). Opsius species are apparently restricted to moist habitats with Tamarix spp. (Tamaricaceae), and especially river valleys. Tamarix spp. are known to be salt tolerant (Newete et al. 2019) and are difficult to identify with many species known. KSA is the center of diversity of the T. nilotica (Ehrenb.) Bunge group and T. aphylla (L. Karst) (Guba and Glennie 1998). Due to their feeding activity, Opsius leafhoppers are well-known honeydew producers on Tamarix spp. (Wiesenborn 2004;Virla et al. 2010;Siemion and Stevens 2015).
The purpose of this study is to clarify the taxonomy of Opsius species of KSA. The morphological characters and global distributions of each species occurring in KSA are presented.

Material and methods
The holotype and paratypes of the new species are deposited in King Saud University Museum of Arthropods (KSMA), College of Food and Agriculture Sciences, King Saud University, Riyadh, KSA and in the National Museum of Wales, Cardiff (NMWC). Other specimens examined are deposited in KSMA.
The morphological terminology follows Dietrich (2005). Measurements are given in millimeters (mm) and are the mean value of 20 specimens of each species; if fewer than 20 specimens were available, all were measured. Genitalia preparations were made by soaking the terminalia in hot 10% KOH solution for 8-10 minutes, and then washed in distilled water. The cleared terminalia were transferred to glycerol for further dissection and examination. After examination, genitalia were moved to fresh glycerol and stored in a micro vial pinned below each specimen.
All specimens were examined with a Leica LABO-PHOT-2 stereomicroscope. Illustrations of the male genitalia were prepared using a NIKON microscope with a drawing tube attachment. Images were taken with a Canon 70D DSLR attached to a Leica Z6 microscope. Individual source images were then stacked using Helicon Focus v. 6.22 software, with calibrated scale bars added using Syncroscopy Automontage v. 5.4. The maps (Figs 75,76) were created using ArcGIS 10.3 software. Aedeagal shafts and basal process parallel throughout its extent, aedeagal shafts equal to basal process (Fig. 35)  -Aedeagal shafts and basal process slightly divergent throughout its extent, aedeagal shafts shorter than basal process ...7 7 Basal process straight but without any curvature (Fig. 23)  Description. The genus Opsius can be recognized by the following combination of features: Head. Head as wide as or slightly wider than pronotum; crown parallel in length or slightly produced, more than or equal to two times the width of eye; ocelli on crown posterad of anterior margin and close to eyes; gena slightly incised; antenna short, near upper corner of eye; Frontoclypeus shorter than wide, with fine erect seta on gena close to lateral frontal suture; lateral frontal suture reaching ocellus, shorter than clypeogenal suture, toward middle of ocelli; ratio of frontoclypeal loral suture to clypellar loral suture more than ⅓; lorum extended nearly to genal margin, wider than clypellus at base; clypellar suture complete and arcuate; clypellus, not inflated, expanded apically ovoid, not protruding beyond the curve of gena, straight or convex apically.

Key to males of Opsius species in the Arabian Peninsula
Thorax. Thorax yellowish green in colour, pronotum more than two times the length of vertex, wider than long, short lateral margin, anterior margin convex, posterior margin concave or slightly straight, about two times as long as scutellum; scutellum wider than long.
* O. stactogalus Fieber and O. cypriacus Lindberg are not known from the Arabian Peninsula but known from neighboring countries and are potential species of the region Wings. Forewings more than three times as long as wide, appendix restricted to anal margin with A veins gently curved distally, A1 crossvein present or absent, A1-A2 crossvein present or absent, two closed anteapical cells, inner anteapical cell open. Hind wing submarginal vein complete.
Legs. Legs generally yellowish green with brown spots, with brown setal areolae; profemur row AM with AM1, profemur with two dorsoapical setae; intercalary row with 8 fine scattered setae gradually reduced apically; AV row with numerous long setae. Protibia dorsal margin rounded, AD row with 1 macrosetae, PD row with 4 macrosetae, AV row with numerous macrosetae, PV row with 1 to 4 macrosetae. Mesofemur AV row with numerous setae, two dorsoapical seta, short and reduced. Metafemur setal formula 2+2+1, setae of penultimate pair set close to each other. Metatibia arched throughout its length, PD row with long and short macrosetae alternating or subequal in length, AD row with macrosetae and one smaller intercalary seta between each pair, AV row with numerous macrosetae and extending nearly to base, gradually increasing in size apically. Metatarsomere I length equal or shorter to tarsomeres II and III combined.
Male genitalia. Pygofer broadly rounded posteriorly, without process, and with well differentiated macrosetae into several rows; valve triangular, laterally, short and pointed articulation with pygofer and free to subgenital plates; subgenital plates triangular, with one row of macrosetae laterally, apex often fingerlike, membranous, with rounded, stout or tapered end; style broadly bilobed basally, with preapical lobe, apophysis not elongate; connective anterior arms linear, contiguous, Y-or U-shaped, not fused, articulated with aedeagus; abdominal apodemes broad, narrow, or tiny, extended to 1 st , 2 nd visible segments, with distance between two branches, posterior margin angled, acute rounded, gradually tapering externally and gradually tapering or tapered internally; aedeagus not hinged at base, with atrium not extending ventrad of shafts, with basal process, basal processes diverging or slightly diverging or parallel or converging, close to each other or distant, arising from socle, divided near base or from middle, aedeagal shafts parallel or diverging or converging or a hump or lamellate, with or without pair of ventral processes at base, aedeagal socle swollen and bulbous.
Female genitalia. Pygofer with scattered macrosetae, ovipositor not protruding far beyond pygofer apex; first valvula convex; second valvula broad, gradually tapered or slender throughout, teeth on apical 1/3 or more, regularly or irregularly shaped, large and prominent.
Diagnosis. The genus Opsius can be distinguished by general colour pattern often greenish brown patches, anterior margin of head without carinae, not angularly curved to the face, face convex, and neither horizontal nor concave, face not elongate; pronotum without longitudinal dark bands or transverse dark markings; aedeagus not hinged at base, with atrium not extending ventrad of shafts, with basal process, basal processes diverging or slightly diverging or parallel or converging, close to each other or distant, arising from socle, divided near base or from middle, aedeagal shafts parallel or diverging or converging or a hump or lamellate, with or without pair of ventral processes at base, aedeagal socle swollen and bulbous.
Comment. Opsius was described by Fieber (1866) with O. stactogalus designated as a type species. Species have been subsequently described, but unfortunately several species have been described only from females, with descriptions often incomplete, lacking illustrations, and without the examination of types of other species. In our examination of available material of the genus, the following morphological characters in males can be used to characterize the genus: the relative lengths of the pairs of basal processes; and the relative lengths of the pair of aedeagal shafts; the relative lengths and distance between aedeagal shafts and pairs of processes at mid-length and tip length. A comprehensive revision of the genus is required to develop a key for all Opsius species. Description. In addition to generic characters, with the following characteristics.

Opsius heydeni (Lethierry)
Male genitalia. Subgenital plates with rounded apex (Fig. 38); connective linear, contiguous (Fig. 40); apodemes broad, extending to mid-length or the end of second abdomen segments, apodeme width 1.5 times the distance between each apodeme, posterior margin angled externally and tapered internally (Fig. 54); aedeagus with only dorsal process, both slightly curved inward preapically but not bent, aedeagal shafts with diverging branches, ratio of distance between two shafts at mid-length to tip length 5/9, straight, shorter than basal process, as wide as basal process, basal process extending close to shafts branches, pointed; phallobase not inflated (Figs 23, 24).
Female genitalia. Female 7 th sternite 2.5 times as broad at base as long medially, posterior margin concave, acutely sinuous with V-shaped notch in middle, posterolateral angles rounded (Fig. 55); first valvula slightly convex; second valvula gradually tapered apically with rather small and serrate teeth on dorsal surface (Figs 56, 57).
Ecology and biology. This species is widespread and common in southwestern KSA and is often associated with the wadies of Asir Province, a habitat that has one of the most diverse floras of the region. In five of these Asir wadies and also in Baha Province, KSA, O. heydeni became common in March, particularly in Wadi Qounonah. Although Opsius is host-specific on Tamarix spp., this species was collected from other plants at these sites including Acacia spp. (Fabaceae) (Figs 77-79).
Diagnosis. Opsius heydeni is similar to O. wilsoni sp. nov. but males of the species can be distinguished easily by the aedeagus and dorsal process slightly curved inward preapically, aedeagal shafts with diverging branches and straight, shorter than basal process, as wide as the basal process, ratio of distance between two shafts at mid-length to tip length 5/9; and the basal process extending close to shafts branches. Specimens examined. No specimens were examined from KSA. Several specimens of this species from Iran were studied but not illustrated.

Opsius richteri Dlabola
Male genitalia. Pygofer slightly angled posteriorly (Fig. 58); subgenital plates with rounded apex (Fig. 41); connective linear, contiguous (Fig. 43); apodemes nar-row, extend to mid-length or the end of first abdomen segments, apodeme width three times as distance between each apodeme, posterior margin angled externally and tapered internally (Fig. 59); aedeagus with only dorsal process, both distinctively curved or bent inward at base, aedeagal shafts with diverging branches, ratio of distance between two shafts at mid-length to tip length 5/11, bent inward at base, shorter than basal process, two times as wide as basal process, basal process extending close to shaft branches, distinctively curved to form distinctive inward pointed tips; phallobase not inflated (Figs 26, 27).
Female genitalia. Female 7 th sternite three times as broad at base as long medially, posterior margin concave, slightly produced with V-shaped notch in middle, posterolateral angles acutely rounded (Fig. 60); first valvula slightly convex; second valvula slender throughout their length with rather small and serrate teeth on dorsal surface (Figs 61, 62).
Ecology and biology. The abundance of this species varied phenologically between areas of the southwestern region of KSA. Peak abundance in Asir Province occurred in March, whereas in Jazan Province, the peak abundance occurred in January. Most specimens were collected by using light traps, but numerous specimens were also collected in Jazan Province from Tamarix spp. with a sweep net and by a portable vacuuming device. Opsius richteri comprised approximately 36% of the total number of specimens of this genus examined from KSA. This species was especially abundant at Wadi Qounonah, Asir Province, KSA (Figs 77-79
Ecology and biology. Two males of O. scutellaris were collected at Sad Abha (dam of Abha) from weedy plants surrounding a large pool in Abha Al Jadidah Park located in the central part of the city. This species is considered uncommon, with only two specimens collected during extensive sampling not only in southwestern region of KSA but also in Abha Al Jadidah Park (Figs 77-79).
Diagnosis. Males of O. scutellaris can be distinguished from all members of the genus by subgenital apex with a lobe-like process; aedeagal shafts three times as wide as basal process, forming a hump or lamellate.
Diagnosis. This species is similar to O. heydeni but the males can be distinguished by the aedeagal shafts and basal process slightly divergent throughout its length, with the aedeagal shafts being shorter than the basal process, and the basal process not straight and curved preapically. Cestius sakroensis Ahmed and Sultana 1994: 126 Description. In addition to generic characters, with the following characteristics.

Opsius versicolor (Distant)
Male genitalia. Pygofer slightly angled posteriorly (Fig.  65); subgenital plates with stout apex (Fig. 47); connective Y-shaped (Fig. 49); apodemes tiny, not exceeding the first segment; apodeme width three times as distance between each apodeme, posterior margin gradually tapering, concave at preapical margin (Fig. 66); aedeagus with only a dorsal process, both straight or slightly curved inward preapically but not bent, aedeagal shafts with diverging branches, ratio of distance between two shafts at mid-length to tip length 5/11, straight, shorter than basal process, two times as wide as basal process, basal process extending narrower to each other, pointed; phallobase not inflated (Figs 32, 33).
Female genitalia. Female 7 th sternite 2.5 times as broad at base as long medially, posterior margin with median lobelike projection with V-shaped notch in middle, posterolateral angles conically rounded (Fig. 67); first valvula convex; second valvula gradually tapered apically with rather small and serrate tooth on dorsal surface (Figs 68, 69).
Ecology and biology. Opsius versicolor was the most common species collected during this study comprising approximately 50% of the total number of specimens examined. Relative abundances varied, with numbers peaking in March in Asir Province, peak abundance in January in Jazan Province, and in November in Baha Province, .
Diagnosis. Males of O. versicolor can be distinguished by tiny apodemes not exceeding the first segment, aedeagal shafts with diverging branches, and the basal process contiguous or coherent to each other. This species dimorphic, with the crown of males being slightly produced , and that of females parallel (Figs 17, 18).
Coloration. General coloration light yellow whitish, greenish brown, with black punctation on forewings (Figs 19-22). Face and vertex yellowish. Pronotum with light yellow anterior margin, and with light green posterior margin. Scutellum light yellow whitish. Forewings greenish brown, with scattered black punctation, transparent at the outer edge, with brownish apical and subapical cells, with some dense brown stripes inside. Legs yellow with brown setal areolae, apices of tarsomeres and claws from brown to dark brown.
Head. Head slightly wider than pronotum. Crown parallel in length, slightly more than two times the width of compound eye, with tiny median groove, with round apex. Ocelli on crown posterad of anterior margin and close to eyes. Gena slightly incised with small projection. Antenna short, near upper corner of eye. Antennal ledge weakly carinate. Frontoclypeus anterodorsal part inflated, posteroventral part not inflated, shorter than wide, with fine erect seta on gena close to lateral frontal suture. Lateral frontal suture reaching ocellus, shorter than clypeogenal suture, toward middle of ocelli, ratio of frontoclypeal loral suture to clypellar loral suture more than ⅓. Lorum extended nearly to genal margin, wider than clypellus at base. Clypellar suture complete and arcuate. Clypellus, not inflated, expanded apically ovoid, not protruding the curve of gena, straight or convex apically.
Thorax. Pronotum wider than long, with convex anterior margin and concave posterior margin, short lateral margin, more than two times the length of vertex, about two times as long as scutellum. Scutellum wider than long.

Wings.
Macropterous, forewings more than three times as long as wide, appendix restricted to anal margin, without reflexed costal veins, with A veins gently curved distally, A1 crossvein absent, A1-A2 crossvein absent, two closed anteapical cells, inner anteapical cell open. Hind wings not visible, submarginal vein complete.
Legs. Profemur and mesofemur inflated. Profemur row AM with AM1, profemur with two dorsoapical setae; intercalary row with eight fine scattered setae gradually reduced apically; AV row with numerous long setae. Protibia dorsal margin rounded, AD row with one macrosetae, PD row with four macrosetae, AV row with numerous macrosetae, PV row with 1-4 macrosetae. Mesofemur AV row with numerous setae, two dorsoapical seta, short and reduced. Metafemur setal formula 2+2+1, setae of penultimate pair set close to each other. Metatibia arched throughout its length, PD row with long and short macrosetae alternating or subequal in length, AD row with macrosetae and one smaller intercalary seta between each pair, AV row with numerous macrosetae and extending nearly to base, gradually increasing in size apically. Protarsomere and mesotarsomere I length shorter than tarsomeres II and III combined. Metatarsomere I length equal or slightly shorter to tarsomeres II and III combined.
Male genitalia. Pygofer slightly angled mid-posteriorly (Fig. 70); subgenital plates with gradually tapered apex (Fig. 50); connective linear (Fig. 52); apodemes narrow, extending to the apex of second abdomen segments, apo- deme width three times as distance between each apodeme, posterior margin a cute rounded externally and gradually tapered internally (Fig. 71); aedeagus with only dorsal process, both curved or bent inward at mid-length, aedeagal shafts with diverging branches, ratio of distance between two shafts at mid-length to tip length 1/3, bent inward at mid-length, as long as basal process, two times as wide as basal process, basal process extending narrow to shafts branches, pointed; phallobase not inflated (Figs 35, 36).
Female genitalia. Female 7 th sternite 1.5 times as broad at base as long medially, posterior margin with median lobe-like projection with V-shaped notch in middle, posterolateral angles conically rounded, narrowed (Fig.  72); first valvula convex; second valvula gradually tapered apically with rather small and serrate tooth on dorsal surface (Figs 73, 74).
Ecology and biology. Opsius wilsoni appeared to reach peak abundance in March. Most specimens were collected from Tamarix spp. (Figs 77-79) by using a vacuum device.
Diagnosis. Females and males of O. wilsoni can be recognized by a slightly incised gena with small projection. Additionally, males can be distinguished by aedeagal shafts with diverging branches at apex, ratio of distance between two shafts at mid-length to tip length 1/3, bent inward at mid-length.
Etymology. This species is named in honour of Dr Michael R. Wilson, Department of Natural Sciences, National Museum of Wales, Cardiff, Wales, United Kingdom.

Conclusions
Seven species of Opsius present in KSA were revised including including the description of a new species, and three new species records for KSA. A key of species based on males is presented that includes new characters for separation of KSA species. Our study also provides maps of the known geographical distribution of the genus and provides examples of typical habitats of the genus. Further study is needed to evaluate the variation in the species of the genus across their entire geographical range.