Snakes of the genus Eirenis in Jordan ( Reptilia : Squamata : Colubridae )

Snakes of the genus Eirenis are referred to as dwarf racers or peace snakes. So far, 16 species of this genus were reported and distributed from southern former Soviet Union States, through Iran to Pakistan eastward, to Greece, Cyprus, Turkey, Iran through the Levant and extending into Sinai (MARX, 1968; GASPERETTI, 1988; LEVITON et al., 1992; BAHA EDIN, 2006; SCHMIDTLER et al., 2009). Turkey has the highest number of species (SCHMIDTLER & EISELT, 1991, SCHMIDTLER, 1993, 1997). Other studies revised the genus Eirenis including DOTSENKO (1989) where he subdivided this genus into two subgenera: Eirenis, containing species with 17 dorsals at mid-body; and Collaria, including species with 15 dorsals. SCHMIDTLER & EISELT (1991) argued the validity of this revision, and stated that 17 dorsals reflects the original state of Eirenis, while 15 dorsals may have evolved many times in the past. SIVAN & WERNER (2003) revised the status of Eirenis corronella in the Middle East, employing principal coordinate analysis. They recognized two main groups assigned as: Eirenis coronella, for specimens from Sinai, Palestine, western Saudi Arabia, Jordan, Iraq and Syria, and E. coronelloides, characterized by dark crown, ventral stripe or both; in all specimens examined from Turkey and some specimens from Jordan, Iraq and Syria. In Jordan, this genus is represented by four species distributed in mountainous and arid dry regions. In this study, we investigated the distribution, meristic characteristics, hemipenial morphology, and food contents for four species of the genus Eirenis in Jordan.


Introduction
Snakes of the genus Eirenis are referred to as dwarf racers or peace snakes.So far, 16 species of this genus were reported and distributed from southern former Soviet Union States, through Iran to Pakistan eastward, to Greece, Cyprus, Turkey, Iran through the Levant and extending into Sinai (MARX, 1968;GASPERETTI, 1988;LEVITON et al., 1992;BAHA EDIN, 2006;SCHMIDTLER et al., 2009).Turkey has the highest number of species (SCHMIDTLER & EISELT, 1991, SCHMIDTLER, 1993, 1997).Other studies revised the genus Eirenis including DOT-SENKO (1989) where he subdivided this genus into two subgenera: Eirenis, containing species with 17 dorsals at mid-body; and Collaria, including species with 15 dorsals.SCHMIDTLER & EISELT (1991) argued the validity of this revision, and stated that 17 dorsals reflects the original state of Eirenis, while 15 dorsals may have evolved many times in the past.SIVAN & WERNER (2003) revised the status of Eirenis corronella in the Middle East, employing principal coordinate analysis.They recognized two main groups assigned as: Eirenis coronella, for specimens from Sinai, Palestine, western Saudi Arabia, Jordan, Iraq and Syria, and E. coronelloides, characterized by dark crown, ventral stripe or both; in all specimens examined from Turkey and some specimens from Jordan, Iraq and Syria.In Jordan, this genus is represented by four species distributed in mountainous and arid dry regions.In this study, we investigated the distribution, meristic characteristics, hemipenial morphology, and food contents for four species of the genus Eirenis in Jordan.

Materials and methods
A total of 136 preserved snake specimens from different localities were examined.The examined specimens were kept at the Jordan University Museum, Amman (JUM), Mu'tah University Museum, Mu'tah (MUM), the Jordan Natural History Museum, Irbid (JNHM) and the Jordan University of Science and Technology Museum, Irbid (JUSTM).

Hemipenis preparation
The following method for hemipenis preparation was modifi ed after PESANTES (1994).The hemipenis was removed from the tail region by using fi ne and sharp scalpel through a careful incision from the vent along the midline section between the subcaudal scales and the tail.The hemipenis was freed from the surround tissues and soaked in 2 % potassium hydroxide solution for about two weeks at room temperature.The hemipenis was removed and washed with distilled water and kept in distilled water for one day, and was soaked in 0.1 N hydrochloric acid solution at 20 o C for one day.The following day, the hemipenis was washed and soaked in distilled water for one day.A syringe was fi lled with distilled water and its needle was introduced into the hemipenis through its base.The water was gently forced in while the organ was pressed between the fi ngers to help the distension of the walls.The muscle, rectus caudae should be cut to facilitate its eversion.For hemipenis eversion, a very fi ne forceps was used.During this procedure the hemipenis must be kept wet.Then, the everted hemipenis was kept in 75% ethyl alcohol in a small glass vials.All the prepared hemipenes were examined by using dissecting microscope.At the end of preparation photographs were taken for the hemipenis of each species, using black and white fi lms (Ilford Pan-F 135, 50 ASA, 18 DIN, Ciba-Geigy, England).Then, drawings for the hemipenes were made.
Description.Body is cylindrical; mainly with regular narrow transverse dark brown bands on the dorsum (Fig 1 ); collar is present.Lips are yellowish; a blackish vertical streak below the eye and another between the last two labials.One loreal; nasal single; one preocular; two postoculars; 1+2 temporals; seven upper labials, third and fourth entering the eye; 7-8 lower labials, the fourth in contact with anterior chin shields; anterior chin shields are larger in size than posterior chin shields, The latter may be separated by one small scale; 17 or 19 scale rows around the neck; scales smooth; anal scale and subcaudals are divided.
The ventral and subcaudal scales count was 118-156 and 29-55 respectively.Additional information about the  scale count and measurements for both sexes are summarized in Table 1.Specimens collected from southern parts of Jordan showed higher scale counts and body measurements than those collected from northern and middle parts of Jordan.
Distribution.The Crowned Dwarf Snake has a wide range of distribution extending from southern Turkey to western Iran to Iraq, across Syria, Lebanon, Jordan and Palestine, to Suadi Arabia to the south and Sinai to the West.This species is distributed in the Mediterranean, and the Irano-Turanean biotopes.Also, it is a common species in the southern part of Jordan.It appears that this species is aridophilous (Fig. 2).
Remarks.One specimen collected from Dana Wildlife Reserve had laid 5 eggs in July; the average length of the eggs was 2.2 cm and 0.6 cm in width.The activity pattern for this is diurnal in moderate spring and autumn; while crepuscular or nocturnal during June-September.They are found mainly under small stones without a defi ned burrow.
Description.Body is brown above, uniform or with two thin, dark stripes running the length of the body and tail (Fig. 3).Lower parts uniform white.The neck is distinct from the body.Seven upper labials, third and fourth entering the eye; eight lower labials, the fourth in contact with the anterior chin shield; one loreal; one preocular and two postoculars; six scales around the eye; dorsal scales in 17 rows at mid body; anal and subcaudals divided.Scale counts for all the studied specimens are presented in Table 2.The ventral and subcaudal scale counts in 40 specimens was 136-183 and 40-83 respectively.
Distribution.The Narrow-striped Dwarf Snake has a distribution range extending from Turkey to the north, reaching Iran and Iraq to the east and extends across Syria and Lebanon to Jordan and Palestine to the south.The species are distributed mainly in northern areas of Jordan (Fig. 4).It is restricted to the Mediterranean biotope.
Remarks.In the early spring and late autumn it is active in the early morning and late afternoon, while during the hot months it becomes nocturnal.It inhabits the vegetated areas, and is usually found under stones where humidity is high.Habkha-Irbid (DISI, 1985;DISI et al., 1988).
Scale counts for the studied specimens are presented in Table 3.The ventral and subcaudal scales count  in 12 specimens was 110-145 and 32-47 respectively.
Distribution.The distribution of the Striped Dwarf Snake extends from SE Turkey, Iraq across Syria and Lebanon, reaching its most southern range of distribution in Jordan and Palestine.In Jordan, this species has a limited distribution to the Mediterranean biotope of Jordan (Fig. 6).Vertebrate Zoology ■ 59 (1) 2009

Eirenis rothi JAN, 1863
Description.Three dark bands are on top of the head of 43 studied, preserved specimens (Fig. 7); body is brownish yellow above; the lower part of the body is uniform white; 7 upper labials, third and fourth entering the eye; 7 lower labials, four in contact with the anterior chin shields; one loreal; one preocular; two postoculars; one anterior temporal; two posterior temporals; six scales around the eye; dorsal scales in 15 rows at midbody; anal and subcaudals divided.Scale counts for the studied specimens are presented in Table 4.
Distribution.The distribution range of the Roth's Dwarf Snake extends from Turkey in the north across Syria and Lebanon to reach its most southern range in Jordan and Palestine.This species inhabits both the Mediterranean and the Irano-Turanean biotops of Jordan (Fig. 8).
Remarks: E. rothi has a wider range of distribution than any other species of this genus in Jordan.

Dietary contents of stomach and intestine of the studied Eirenis species
Food remains were recovered from 106 specimens belonging to the four studied species of the genus Eirenis (Table 5).The food remains consists mainly of arthropods.Ingested preys in all examined snakes were taken by the head fi rst.Of the 30 E. coronella specimens, 5 were found to contain food remains.In three snakes, a single spider was found in each, the other two contained a centipede of the genus Scolopondra, and an unidentifi ed scorpion respectively.Six specimens of E. decemlineata were found with ingesta consisting of a spider, Acrididae, caterpillars and unidentifi ed beetles.Two specimens of E. rothi yielded centipedes.

Hemipenial Morphology
The hemipenes of the four examined species were similar to each other; but minor differences were ob-Pervious records.Jarash (=Jerash), HAAS (1951), Ain Lahtha, Jubyha (Al Jubayhah), Ajlune (Ajlun), Ael, Swileh (Suwaylih), Hisban, Amman, Ma'an, Ramtha (Ar Ramtha), Um Al dananeer (Umm Al Dananir), Anjarah, Dair Abu Said (Dayr Abu Sa'id), Ain Ghazal, Madaba, Irbid, Salt (As Salt) (DISI et al., 1988), Wadi Musa, Er Rajif, Karak (Al Karak), Ayl (AMR et al., 1994), Wadi Musa, Er Rajif, Ash Shawbak, Ghwair, Al Mazar, Mutah, El Adananeyeh, Ar Ra'ba (EL ORAN et al., 1994), Az Zarqa, Dana, Wadi Al Hashad (DISI et al., 2001).The obtained results suggest that there is a clear difference in the scale counts and total body length within the same species of Eirenis coronella.Specimens collected from southern part of Jordan have a higher scale counts and higher body length than specimens collected from other parts of Jordan.It seems clear that there is a positive correlation between scalation and ambient temperature.The mean annual temperature in the south is higher than that in the north and middle parts of Jordan.These fi ndings are in agreement with FOX (1948) who indicated that there are reductions in several scale characters from warm to cooler regions.Moreover, KLAUER (1941) reported that there is an almost universal tendency toward a higher number of ventrals in the desert specimens, as compared to those collected from more humid region in San Diego.Also, these fi ndings are in agreement with the reported scale counts in the Eastern Mediterranean region.E. coronella is the only taxon of the genus Eirenis, which penetrates into dry habitats of southern and eastern Jordan (Fig. 2).LEVITON et al. (1992) reported the highest scale counts (> 180 in females; > 200 in males) in comparison with previous reports, as well as the present investigation without specifi cation to any given country.ARNOLD (1982) described Eirenis coronella fennelli from Arabia.served.All have cylindrical simple hemipenis; single sulcus; with macro-ornamentation of large spines; also micro-ornamentation of small spines and calyculate.
Eirenis decemlineata has cylindrical hemipenes with single sulcus which turns left; it has macro-ornamentation of three rows of large spines.Micro-ornamentation of a calyculate and spinulate.Total Length 10-20 mm (Fig. 9A).
Eirenis coronella has cylindrical hemipenes with single sulcus which turns right and rarely left (Fig 9B).The hemipenis with ornamentation of four rows of large spines or medium spines; fi ner ornamentation is calyculate with short spines.Total Length: 10-12 mm.
Eirenis lineomaculata has cylindrical hemipenes with single sulcus which turns left; they have macroornamentation of three rows of large spines; and micro-ornamentation of a calyculate and spinulate.Total length 7-19 mm (Fig. 9C).
Eirenis rothi has cylindrical hemipenis with single sulcus which turns left or right; macro-ornamentation of 3-4 rows of large spines.In one snake, the hemipenis was covered with spines all of the same size.Micro-ornamentation is calyculate and spinulate.Total length 5-10 mm (Fig 9D).

Discussion
The genus Eirenis seems closely related to the whip snakes and, according to different authors, is consid-

The Hemipenis Morphology
The hemipenis is a diagnostic feature often used in supraspecifi c systematic investigations of snakes (UTI- GER et al., 2002).The hemipenes of the four studied species of the genus Eirenis are very similar to each other.All have single, subcylindrical hemipenis with a single sulcus, which may turn left or right.In addition, they have macro-ornamentation of large spines and micro-ornamentation of acalycate, and spinulate structures ZIEGLER & RASMUSSEN (2002) stated that despite variation, size and ornamentation of the hemipenes among species of the genus Crotaphopeltis, they serve to distinguish between sympatric and parapatric species.
The hemipenis morphology in this study for Eirenis coronella is similar to that given by ARNOLD (1982) for the Arabian population of this species.COPE (1895) indicated that Eirenis has a naked organ, but POPE (1935) demonstrated that COPE was in error.This study shows that the four studied species have a calyculate organ covered with a complex ornamentation of retiform ridges as in typical colubrids.

Dietary contents of the genus Eirenis in Jordan
A total of 106 snakes were examined for food contents, only 14 specimens (13.2%) were found to contain ingesta.The four studied species preyed mainly on small arthropods and insects (Table 5).In Turkey ÇIÇEK & MERMER (2007) found that Eirenis modestus fed mainly on arthropods including Coleoptera, Orthoptera, and Scolopendromorpha, as well as other small lizards.They did not recover scorpions or spiders.Previous studies have reported prey from the taxa such as Orthoptera, Coleoptera, Isopoda, Myriapoda, Scorpiones, and Aranea (TERENTJEV & CHERNOV, 1949;BANNIKOV et al., 1977).It seems that snakes of the genus Eirenis feed mainly on various rock-dwelling arthropods.This investigation shows a positive correlation between the size of the snake and its prey.For example the large E. rothi was found to feed on large centipede while the small E. rothi feeds on smaller centipedes.Also, most of the snakes examined feed on spiders and Acrididae.
Examining the food contents show that these snakes are opportunistic feeders and depend on the availability of prey and their size in the surrounding environment.Ingested preys in all examined snakes were taken by the head fi rst.Same results were obtained by AMR and DISI (1998).
Further molecular studies should address the phylogentic relationship for species of the genus Eirenis in Jordan and the Middle East and relate their relationship from an evolutionary perspective.This taxon is larger and more robust than the nominal form.Also, pholidosis (131-154 ventrals) and color (pale grayish brown) patterns are different from those studied specimens.GASPERETTI (1988) described E. c. coronella from Arabia (123-163 ventrals, and 37-52 subcaudals), and also posterior chinshields were separated by a single scale.
Eirenis coronella has a wide range of distribution.It was collected from the Mediterranean and Saharo-Sindian biotopes in Jordan.This is the only taxon that can inhabit the desert region in Arabia while the other three studied species are mainly restricted to the Mediterranean habitats.Similar observations were made by HAAS (1951) in Palestine.
Jordan represents the most southern range of distribution for E. decemlineata.Scale counts of the studied specimens from Jordan are within the range of the reported studies in the Eastern Mediterranean countries (SCHMIDTLER & SCHMIDTLER, 1978).E. decemlineata have two form of coloration, striped and non-striped.The striped color pattern may act as protective mechanism from biotic dangers.It would be expected that striped color patterns are more effective in diurnal snakes since the visual confusion is caused by movement (WOLF & WERNER, 1994).Moreover, KARK et al. (1997) indicated that the distribution of striped/nonstriped Psammophis schokari is correlated to rainfall, solar radiation and vegetation.Eirenis decemlineata is restricted to the Mediterranean habitats, which has almost similar characteristics in neighboring countries.This may explain the reason of the minimum variations in scale counts along its range of distribution.It seems that the striped form is more common in forested areas while the non-striped form is common to open rocky areas of the Mediterranean ecozone.
The scale counts for E. lineomaculata are within the reported ranges for the eastern Mediterranean countries.However, higher scale counts  were reported from Turkey (SCHMIDTLER & SCHMIDTLER, 1978).Jordan represents its most southern range of distribution.It inhabits humid areas and avoids deserts.HAAS (1951) and DISI (1987) stated that E. lineomaculata reacts positively with humidity parameters and negatively with temperature.
The reported scale counts in this study for E. rothi are in agreement with previous studies from the Eastern Mediterranean countries (BARAN, 1978).Examining both pholidosis and measurements of E. rothi from Jordan suggests sexual dimorphism.Females attain larger body size, but their tails are shorter than in males (Table 4).Accordingly, the ventral scales are 171-200 in females, while 133-182 in males.Moreover, the subcaudal scale counts are 50-62 for females and 40-72 in males.Jordan represents its most southern outpost of distribution and it penetrated into the Irano-Turanian biotope.
s.s.(NAGY et al., 2003) or of the clade composed by "Coluber" caspius, "C." jugularis and "C." schmidti (SCHÄTTI & UTIGER, 2001).NAGY et al. (2003) propose a phylogeny based on molecular data, allocating the species to four subgenera: Eirenis JAN, 1863, including modestus and aurolineatus, the new subgenus Eoseirenis for decemlineatus, Pseudocyclophis BOETT-GER, 1888 for persicus and Pediophis FITZINGER, 1843 for all remaining taxa.The nominate subspecies ibrahimi SIVAN & WER-NER, 2003 is endemic to the southern Sinai, fennelli ARNOLD, 1982 is known from W Saudi Arabia and coronelloides (JAN, 1862) occurs in Jordan, Syria, SE Turkey and NE Iraq.Populations from SW Iran, S Iraq and NE Saudi Arabia cannot be assigned with certainty to any subspecies, although so far are considered to belong to E. c. coronella.SIVAN & WERNER (2003) raise Eirenis coronelloides at the species level, but this point of view requires confi rmation (VENCHI & SINDACO, 2006).
Scale counts and measurements for Eirenis lineomaculata.

examined No. with ingesta % with ingesta. Food remains recovered
Tab. 5. Ingest recovered from four species of the genus Eirenis.