Synopsis of the Evippinae (Araneae, Lycosidae) of Israel, with description of a new species

Evippinae (Araneae, Lycosidae) is a subfamily of old-world lycosids, comprising six genera and 67 species, most of them typically found in xeric habitats. Although Israel is located between the two distribution-centers of the subfamily, Africa and central Asia, only two species of the genus Evippa Simon, 1882, namely E. arenaria (Audouin, 1826) and E. praelongipes (O. Pickard-Cambridge, 1871), and a doubtful record of Xerolycosa nemoralis (Westring, 1861) were reported previously. Here we describe a new species: Evippa amitaii sp. nov., and re-describe and report a new record for Israel of E. onager (Simon, 1895 sensu Šternbergs 1979). Additionally, the genus Evippomma Roewer, 1959 is recorded for the first time from the Middle East, with a description of the previously unknown female of Evippomma simoni Alderweireldt, 1992. We discuss the possible vicariance of Evippa arenaria and E. praelongipes. We suggest that the dispersal of E. arenaria along the coastal plain is blocked by the Yarqon river valley. We suggest competition with a similar species (Pardosa subsordidatula (Strand, 1915)) as a factor affecting the seasonal activity of E. arenaria. Additionally, we present a partial molecular phylogeny of Evippinae, to clarify the placement of E. onager, a species with an unusual morphology. European Journal of Taxonomy 733: 87–124 (2021) 88

tibia I (plus an apical pair) (Alderweireldt 1992). It is found mostly in arid climates in Africa (World Spider Catalog 2020).
Here we studied historical material deposited in collections and collected fresh material, to revise the species of Evippinae in Israel and examine their distributions and seasonal activity.

Material and methods
This synopsis is based on material deposited at the Israel National Arachnid Collection, the National Natural History Collections (NNHC), at the Hebrew University of Jerusalem (HUJ). The samples were preserved in 70% ethanol or absolute ethanol (for DNA extraction) and identified using relevant literature (Šternbergs 1979;Alderweireldt 1991Alderweireldt , 1992.

Morphological analysis and distribution maps
Measurements are in mm. Epigynes were detached and temporarily cleared with clove oil. Specimens were examined and measured using a Nikon SMZ25 stereo microscope. Digital microscope images were taken using NIS-elements imaging system with a Nikon DS Fi2 digital camera mounted on a Nikon SMZ25 stereo microscope. Habitus images were taken with a Nikon D7100. Images were edited and drawings generated using GIMP ver. 2.6.10. The distribution map was generated with Inkscape ver. 0.48. Transliterated names of the localities in Israel and Palestine follow the 'Israel Touring Map'(1:250 000) and 'List of Settlements', published by the Israel Survey, Ministry of Labor. Coordinates are given in decimal degrees (DD). Coordinates estimated from Google maps by the locality name are in square brackets, coordinates taken in situ with a GPS are without brackets.

Molecular analysis
DNA was extracted from the legs of eight specimens (Table 1) of five species of lycosids, using the BioVision Insect Genomic DNA Kit (Catalog #: K1412), following the protocol provided with the product (except that the samples were incubated in proteinase K overnight, rather than 30 minutes). Two mitochondrial markers were amplified by PCR using general primers (Table 2) and sequenced bidirectionally with Sanger sequencing. We retrieved a ~650 bp long fragment of cytochrome c oxidase I (COI) and a ~600 bp long fragment of NADH dehydrogenase subunit 1 (NADH). All sequences are deposited in GenBank (see Table 1). To these we added the corresponding COI and NADH fragments from six lycosid species retrieved from GenBank (see Table 1). These two markers were selected for their proven utility in lycosid phylogeny (Piacentini & Ramírez 2019). The sequences were edited and aligned using MEGA 10 (Kumar et al. 2018). We constructed a maximum likelihood phylogenetic tree, with MEGA 10 (Kumar et al. 2018), using the Tamura-Nei substitution model. Nodal support was estimated by running 10 000 non-parametric bootstrap replicates.

Natural history
Most species inhabit deserts, steppes and savannas, but species of open patches in and along forests (Xerolycosa spp.) are known. Zyuzin (1985) described Xerolycosa as found in dry conifer forests, steppes and arable land, while Evippa inhabits flood plains, semideserts and deserts, often as a sole representative of Lycosidae. They are largely presumed vagrant (Alderweireldt & Jocqué 2017), although burrow construction behavior is known from species of Xerolycosa (Marusik et al. 2011) and Evippomma (Bayer et al. 2017). Both diurnal and nocturnal activity has been observed (Zyuzin 1985;

Distribution
The subfamily is restricted to the Old World where it is widely distributed, except in the polar region, wet tropics and wet subtropics. Xerolycosa is found across the Palearctic, from Europe to Japan (with a doubtful species from Zanzibar). Proevippa, Pseudevippa and Zenonina are restricted to sub-Saharan Africa. Evippomma is found in Africa and India (Indian species might belong to a different genus).
Evippa is found across arid and semiarid climates throughout Africa and Eurasia, from Tanzania to Siberia (World Spider Catalog 2020).

Diagnosis
Evippa is distinguished easily from all other lycosids by a combination of characters: elongated tarsal claws, 5-6 pairs of ventral spines on tibia I (apart from apical pair), transverse depression in carapace posterior to ocular area ( Fig. 3) (Alderweireldt 1991).

Description
Small-to medium-sized lycosids. Cephalic region elevated, separated from thoracic region by transverse depression. Ocular area almost as wide as cephalic region, adorned with long, forward-pointing setae. Clypeus vertical. Anterior row of eyes procurved, narrower than PME. AME larger than ALE. Labium wider than long. Most species with long, slender legs (see E. onager; Fig. 3). Claws usually long, toothed near base. Tarsi of many species with pseudoarticulation. Tibia I with 5-6 pairs of spines (apart from apical pair). Coloration cryptic, usually mottled yellow or brown (Fig. 3). Carapace usually with pale median band. Body covered with short setae throughout ( Fig. 14A) (Alderweireldt 1992

Distribution
The species of Evippa are distributed in arid and semiarid environments across Eurasia and Africa. Eight species are reported from Africa, four species are reported from Europe, and 34 are reported from Asia (13 from Central Asia, nine from India, nine from the Middle East, seven from China and one from Siberia) (World Spider Catalog 2020). In Israel four species are found.

Relationships
The genus appears to be closely related to Pseudevippa Simon, 1910, from which it is distinguished by the number of ventral spines on tibia I (Alderweireldt 1991).

Diagnosis
Recognized by a combination of genital characters (compare with Evippa aequalis Alderweireldt, 1991). Male palp: tegular apophysis tip flat, curved ventrad. Basal process of tegular apophysis long, with sharp tip. Bulb differs from the bulbs of other Evippinae species found in Israel, and from that of E. aequalis, by the terminal apophysis (process between tegular apophysis and cymbium) being at least at 40° angle to tegular apophysis and oriented ventrad (in the others the tip of the tegular apophysis is oriented distad) (Figs 6A, 7A, 8A, 12). Epigyne: Atrium borders indistinct. Septum wide, longer than atrium, narrowing slightly anteriorly and mesally, creating a small protrusion (Figs 10A, 13A). Spermathecae club-shaped, long, reaching over frontal edge of atria (Figs 11A, 13C). In contrast, the similar E. praelongipes lacks the protrusion in the septum (Fig. 10D). The similar E. aequalis has a protrusion in the septum, but has short spermathecae, not reaching the frontal edge of the atria (Alderweireldt 1991).

Natural history
No live specimens observed. Adults collected in April, August and September (Table 3), from salt pans and oases (Fig. 16).

Remarks
The species closely resembles the African species Evippa aequalis Alderweireldt, 1991. The Dead Sea area is known to be a refugium for tropical species (Yom-Tov & Tchernov 1988), mainly of African origin. We suggest that populations of E. amitaii sp. nov., or a closely related species, exist in suitable habitats south of Israel. This species does not conform to Roewer's diagnostic character for Evippinae (metatarsus IV shorter than patella IV + tibia IV), as the females' metatarsus IV (5.27 mm) is slightly longer than its patella and tibia IV (1.2 + 3.98 = 5.18 mm).

Natural history
Adults of Evippa arenaria were collected from February through October, and egg-sacs are recorded from February to September (Table 3). Both nocturnal and diurnal activity were observed. Evippa arenaria is the most mesophilic species of the four Evippa species found in Israel. It is found in sand and loess substrate throughout the semi-arid and arid parts of the Negev (Figs 15B, 16). It is also found in the Mediterranean climate zone, along the coastal dune strip (Figs 15D, 16). In the northern edge of its distribution in Israel and Palestine, E. arenaria is a strict psammophile, found only on exposed sand, but in the Negev desert it appears to be more generalist in its edaphic preferences, and is even found on somewhat rocky hillsides.

Remarks
Despite extensive sampling in the Negev in all seasons, no adult E. arenaria were collected from November to January. This may be due to seasonal changes in activity (see Discussion).

Diagnosis
Recognized by short, robust legs (carapace longer than ⅓ of leg I), coloration and its genital morphology. Prosoma of preserved specimens dark brown (other Evippinae in Israel are yellow after preservation). Male palp: tegular apophysis parallel to cymbium, with single, small, subapical process oriented ventrad (Figs 6C, 7C, 8C). It is the only Evippa in Israel with a subapical process directed ventrad at 90° to the tegular apophysis. In the similar Evippa caucasica Marusik, Guseinov & Koponen, 2003, the base of the subapical process reaches the tip of the tegular apophysis, whereas in E. onager, the tip and the process are distinct. Epigyne: atria distinct, widest in middle. Septum narrow, slightly constricted in middle, broadened distally (Figs 10C, 11C).

Natural history
Outside Israel inhabits steppes. In Israel inhabits hyperarid deserts. Specimens were found at night, on and in the cracks of fine-grained floodplain deposits (Fig. 15C). Adult female collected in March, adult male collected in February, juveniles collected in July (Table 3). The short legs, not typical of Evippinae, may be an adaptation for a somewhat fossorial lifestyle.

Remarks
The female of Evippa onager was originally described from China by Simon (1895), and redescribed from both sexes by Šternbergs (1979) from Turkmenistan. It is very unlikely that these later specimens are conspecific with the holotype (fide ). As we have not examined Simon's type specimen, we avoided describing a new species and instead have chosen to treat the species as Evippa onager sensu Šternbergs, following .
The species' population in Israel is by far the southernmost and westernmost of the three known localities, and the only one not in a steppe habitat. Nevertheless, cool steppe habitats are found in Israel and it would be helpfull to search them for E. onager.

Diagnosis
Recognized by a combination of genital characters. Male palp: tegular apophysis parallel to cymbium, with small, prolaterally oriented subapical process. Short terminal apophysis positioned ventrad to tegular apophysis (Figs 6D, 7D, 8D). Epigyne: straight atria with indistinct retrolateral margins. Septum with smooth margins, without protrusions (compare with similar E. amitaii sp. nov. palp, with a small protrusion) (Fig. 10D, 11D) It is the only Evippa in Israel to have a septum without protrusions.

Natural history
Inhabits hyper-arid deserts. Adults were collected January through April, June through September and in November (Table 3). Egg-sacs were observed in April and September. We suggest that E. praelongipes is active and reproducing throughout the year. Specimens were collected at night, mostly in dry stream beds, under and near shrubs (Fig. 15A).

Diagnosis
This is the only known genus of Lycosidae in which the body (mainly, the cephalothorax) is densely covered in scale-like, leaf-shaped setae (Figs 1D, 14B).

Natural history
The species inhabit deserts, grasslands and savannas. Evippomma rechenbergi is known to construct silk-lined burrows in sand (Bayer, Foelix & Alderweireldt 2017), as we recorded for E. simoni as well (Fig. 2D).

Distribution
Found across Africa, with a new record from Israel (but see the section on Composition).

Relationships
Evippomma is traditionally considered to be related to Evippa (Alderweireldt 1992). Our molecular phylogeny supports this placement (see Phylogenetic relationships of Evippinae based on COI and NADH).

Diagnosis
Recognized by a combination of genital characters. Male palp: tegular apophysis small, translucent, oriented distad, parallel to plane of bulb, laterally barb-shaped (Figs 6E,7E,8E). Tegulum presents single sinus shape curve of sperm duct (in Evippa: two) (Fig. 6E). Epigyne: rounded or hat-shaped, wider than long, septum wide. Atria narrow, shallow, greatly constricted distally (in Evippa: width approximately equal throughout), similar to epigyne of E. squamulatum, but proximal portion of atrium wide (in E. squamulatum proximal portion of atrium slit-shaped) (Figs 10E,13B,D). It is the only Evippinae in Israel covered in flat, leaf-shaped setae and without annulations on the legs.

Male
Measurements (n = 12). AME diameter: 0.13-0.2; PME diameter: 0.27-0.4; carapace length: 2.8-3.99; carapace width: 2. leg I (Fe,Pa,Ti,Mt,.0, 2.14-2.58. Color. Carapace yellow to orange and brown, lighter around fovea and in patches behind PME; lateral bands brown to grey, radiated, fused posteriorly; ocular area black; cephalic and thoracic regions separated by sharp, black V-shaped line; perimeter with spots of white setae. Clypeus black near AME, light laterally, with white setae on margin. Chelicerae proximally yellow to orange with grey or brown reticulation connecting to oblique brown band in middle, retrolateral margin white. Legs yellow, proximal part of femur and coxa usually grey. Palps yellow to brownish (femur and tarsus darker). Sternum grey to brown, margin black, sometimes with light radiation. Abdomen dorsum yellow to whitish, sometimes with white spots. Cardiac mark yellow to brown, outlined with black spots, surrounded by posteriorly extending broken light band, outlined with dark spots, not reaching spinnerets. Abdominal venter margins yellow to whitish, center irregularly bordered, grey to black with yellow spots. Book lungs white. Spinnerets yellow (Fig. 4E).
Carapace. Ocular area elevated. Due to the females' strongly raised cephalic region and short legs they resemble a juvenile Lycosa rather than an Evippa. Cheliceral teeth. 3 promarginal, 2 retromarginal.

Natural history
Adult Evippomma simoni were collected April through June, August and September (Table 3) and may have a yearly cycle similar to what was suggested for E. arenaria, with a period of lowered activity in the colder months of the year (see Discussion). A female with eggs (HUJ INV-Ar 20422) was collected in June. The species mostly inhabits sandy desert habitats (Fig. 15B). An anecdotal report raises the possibility that the species also exists along the coastal dune strip, similar to Evippa arenaria (Y. Salaviz, pers. com.). Specimen HUJ INV-Ar 20421 was found by S. Aharon in a silk-lined burrow (Fig. 2), similar to what has been reported for E. rechenbergi (Bayer et al. 2017).

Remarks
This is the first record of Evippomma in Israel, and may also be the first record outside of Africa (depending on the dubious report of the species from India (Roewer 1955)). If there is a continuous distribution with the type locality at the northern Sudanese border, this species is to be present in the sandy desert of northern Sinai and in eastern Egypt. It may be distributed in other hot desert environments in the region, such as the sandy deserts of Jordan.
Most of the specimens were collected in dune areas, but a specimen from the Sedom area, with a clayrich substrate, suggests that this species is not an obligate psammophile.

Phylogenetic relationships of Evippinae based on COI and NADH
The ML tree topology recovered the genus Evippa as monophyletic (bootstrap support [BS] = 89%). Evippinae was only moderately supported in our tree ( Fig. 17; BS = 63%), yet the topology in our tree accords with the tree topology for Lycosidae in Piacentini & Ramírez 2019 and with the composition of Evippinae sensu Alderweireldt 1991.

Habitat use and distribution
The Evippinae are among the most desert-adapted lycosids, often being the only representatives of Lycosidae in desert habitats. Even though mesophilic Evippinae are known (Xerolycosa, Proevippa), the Evippinae of Israel are largely excluded from mesic habitats. The only exception to this rule is E. arenaria. It is found along the southern and central coastal dunes of Israel. The southernmost record is from the coastal dunes of Gaza, where the dunes come in contact with the Negev desert. The northernmost record is from Miqwe Yisra'el, south of Tel-Aviv (Fig. 16). Miqwe Yisra'el was historically located near the northern edge of a large area of dunes, where the coastal sands are interrupted by the alluvial plain of the Yarqon river system. Two major dune areas exist on the Israeli coast north of this point (Qesarya sands and Zevulun valley sands). Visual searches by the authors were performed in both areas. A 2015 study in Qesarya sands, using pitfall traps, did not find E. arenaria (A. Avisar, pers. com.). North of Israel, on the Lebanese coasts, there are no significant dune areas (Kasparek 2004). The Yarqon river is known to be a northern limit for several desert-dwelling species. Examples of this biogeographic limit can be found among mammals (Meriones sacramenti Thomas, 1922 (Alon 1991). The accepted hypothesis is that these species have colonized the dunes from the area of the present-day Negev desert, during the Holocene, with subsequent range expansion and their spread was impeded by physical barriers, such as rivers. Evippa arenaria may have followed the same route of expansion, and if so, the Yarqon may be the northernmost distribution edge of E. arenaria in the Levantine coastal region.  (Brullé, 1832) and Pirata piraticus (Clerck, 1757) as outgroups. Bootstrap supports provided on the nodes. Species appearing twice represent different specimens, as detailed in Table 1.
The xeric habitats populated by the Evippinae are not uniform, differing greatly in annual rainfall, temperatures and substrate. The species assemblage also differs, including occurrence of other lycosids. Many vicariant species of different taxa are known from the Negev, and they replace each other along the climatic gradient and across different edaphic conditions (Yom-Tov & Tchernov 1988). From this it is to be expected that the distributions and activity patterns of the local Evippinae species are not uniform.
Evippa arenaria is the best sampled species in our study, with 62 specimens, collected at 23 localities (Fig. 16). It is found on loess and sandy substrates, in semi-arid steppes and arid deserts in the range of 80-300 mm average annual rainfall (Fig. 15B). It is also found in coastal dunes, in higher rainfall areas (Fig. 15D). Throughout most of its range, E. arenaria co-occurs with other lycosids (Alopecosa spp., Hogna spp., Pardosa spp., Lycosa spp.), including a partial overlap with the range of Evippomma simoni. It is usually less abundant than Pardosa subsordidatula. Of the 23 localities at which E. arenaria was collected, it co-occurs with another Evippa species (E. praelongipes) only in one, at the southern edge of its distribution (Fig. 16). The second most sampled species, E. praelongipes, is largely restricted to the hyper-arid region (<80mm average annual rainfall), mostly in stream beds (Fig. 15A). It is the most common, and often only, lycosid species in its habitat (I. Armiach Steinpress., pers. obs.), rarely co-occurring with E. onager, Lycosa sp., Hogna ferox and Evippomma simoni, as well as E. amitaii and the aforementioned E. arenaria. It is not yet known whether the apparent vicariance between E. arenaria and E. praelongipes is mainly due to habitat requirements, species interactions or other variables.
In our study area, the Dead Sea area (Fig.15A) is the richest in Evippinae species (E. amitaii, E. onager, E. praelongipes and Evippomma simoni) (Fig. 16). The biogeographic mechanism underlying this trend is not known. One possibility is that the different species are specializing in different habitats of the region: mountains, plains, stream beds, salt pans and oases. In recent fieldwork, we found E. praelongipes to be common along stream beds, but could not find the other species. Evippa onager was found in other localities on and under cracked mud crusts. Evippa amitaii is possibly endemic to the Dead Sea region, and may be restricted to a habitat discontinuous with the surrounding desert, such as salt pans or hot oases. The habitat preferences of Evippomma simoni are unknown. Further collecting and in-situ observations need to be done to clarify these questions.

Activity patterns
No Evippa arenaria or Evippomma simoni were collected during the winter months. The lack of adult Evippinae specimens from the winter months in collections (Table 3) might reflect an annual period of lowered activity. A study of arachnids in the northern Negev, that was conducted between 1990 and 1993, using pitfall traps (Lubin, unpublished data) found Evippa arenaria from April through October, and Evippomma simoni in April through September. This area is rich in other lycosid species, including the very common Pardosa subsordidatula (Strand, 1915), which is similar in size to Evippa arenaria and co-occurs throughout its range. In the same study P. subsordidatula was collected in November through April, complementing the activity period of Evippa arenaria and Evippomma simoni. These data are congruent with collection dates of other specimens deposited in The Arachnid National Natural History Collection (HUJ).
These activity patterns contrast with those of E. praelongipes, which is evidently active all year round (Table 3). One notable difference between Evippa arenaria, Evippomma simoni and E. praelongipes is that E. praelongipes is the dominant lycosid species in its habitat. Therefore, we postulate that a contributing factor to the activity patterns of E. arenaria and Evippomma simoni may be temporal habitat partitioning with a winter-active species, possibly P. subsordidatula. Further research is to be done to address this suggestion.