Herpetology Notes, volume 7: 75-82 (2014) (published online on 4 February 2014) Snake fauna of Shirahmad wildlife refuge and Parvand protected area, Khorasan Razavi province, Iran Seyyed Saeed Hosseinian Yousefkhani 1*, Masoud Yousefi 1, Ali Khani 2 and Eskandar Rastegar Pouyani 3 Abstract. The snake fauna of Sabzevar was investigated during 3 years (2009-2011). Seventeen species belonging to six families: Boidae, Typhlopidae, Colubridae, Lamprophiidae, Viperidae and Elapidae were recorded. These species are: Typhlops vermicularis (Typhlopidae), Eryx jaculus, Eryx miliaris (Boidae), Psammophis schokari, Psammophis lineolatus (Lamprophiidae), Boiga trigonata melanocephala, Hemorrhois ravergieri, Lytorhynchus ridgewayi, Natrix tessellata, Platyceps karelini, Platyceps ventromaculatus, Platyceps rhodorachis, Spalerosophis diadema (Colubridae), Naja oxiana (Elapidae), Echis carinatus sochureki, Macrovipera lebetina and Pseudocerastes persicus (Viperidae). Keywords. Sabzevar, Snakes, Parvand Protected Area, Shirahmad Wildlife Refuge Introduction Seventy-nine species of snakes belonging to 37 genera have been recorded in Iran (Firouz, 2000, 2005; Majnoonian et al., 2005; Rastegar Pouyani et al., 2008). The studied area is located in the western area of Khorasan Province, approx 200 km west of Mashhad. The geographic and climatic conditions of the area support a rich herpetofauna for an arid region because Sabzevar is located between two different climates: mountainous climate in the north to desert in the south. Sabzevar s latitude is between 35 39 to 36 29 N and its longitude is between 56 43 to 58 15 E. Although the desert is a harsh environment, it contains a considerable high number of animal species, of which the reptiles constitute a major part (Anderson, 1966; Al-Sadoon, 1989; Ananjeva et al., 2004; Fathinia et al., 2010). 1 Young Researchers and Elite Club, Shirvan Branch, Islamic Azad University, Shirvan, Iran 2 Department of Environment, Khorasan Razavi, Sabzevar, Iran 3 Department of Biology, Faculty of Science, Hakim Sabzevari University, Sabzevar, Iran *Corresponding author; Email: mesalina.watsonana@gmail.com The present study is one of the first surveys of the snake fauna of the Sabzevar region. In order to protect the fauna of the regions, the identity and natural history of these species need to be known. Here we present the results of our study on the snakes of the region. Materials and methods Fieldwork was carried out in the Sabzevar region for 3 years, 2009-2011 (Fig. 1). The best time for sampling the reptiles in the area is from March to October, when environmental conditions allow these animals to be active. All specimens were captured by hand and were deposited in the Sabzevar University Herpetological Collection (SUHC) and in the Environment Office of Sabzevar. Specimens were fixed using 96% ethanol and preserved in 75% ethanol. Specimens were identified according to Latifi (1991) using morphometric characters and coloration. Table 1 shows localities in the Sabzevar region where we collected the 17 species of snakes, including museum numbers and coordinates of the specimens. Abbreviations used: SUHC: Sabzevar University Herpetological Collection; EOS: Environment Office of Sabzevar. Results and Discussion Seventeen species of snakes were recorded from the Sabzevar region. The localities of observed species are detailed in Table 1. Of these 17 species, ten snakes are
76 Seyyed Saeed Hosseinian Yousefkhani et al. Figure 1. Surveyed areas in Sabzevar region where 17 species of snakes belonging to 5 families were recorded. nonvenomous; three semivenomous and four venomous. The results of this study indicated that 21.5% of the Iranian snake species occur in the surveyed area (Latifi, 1991; Leviton et al., 1992). Among the identified snakes, Lytorhynchus ridgewayi is reported for the first time in the surveyed area. According to Latifi (1991), there is no prior record of this taxon in Khorasan. Currently, no conservation programs are active in Iran for snakes, and the IUCN redlist only have limited information about them and their condition (Table. 1). Brief Remarks on the snakes in the Sabzevar Area Family Boidae This family is represented by 2 species in Sabzevar region: Eryx jaculus (Linnaeus, 1758) Common English name: Javelin sand boa Remarks: Boulenger reported that the species was found near gardens and rivers. The species lives among and under rocks, sands and soft soils, in scrublands, grasslands and semi desert areas (Leviton et al., 1992). We found Eryx jaculus in the Sabzevar region, Rigdarzi village in the Shirahmad Wildlife Refuge. Eryx miliaris (Pallas, 1773) Common English name: Dwarf sand boa Remarks: We found E. miliaris in most parts of Iran. It is known to eats lizards and some rodents. The body is brown with brown spots; in some specimens uniform spots form a zigzag pattern. The species is viviparous and lives in sandy deserts, sandy soils, among rocks, fields and grasslands. In the Sabzevar region the species was seen in the Rigdarzi village in the Shirahmad Wildlife Refuge. Family Colubridae This family is represented by 8 species in the Sabzevar region and is the most diverse family in the area. Boiga trigonatum (Annandale, 1904) Common English name: Indian gamma Snake Remarks: The shape of the head is triangular and has a dark bluish black color. Boiga trigonata is oviparous and inhabits deserts, fields, rocky areas with soft
Snake fauna of Shirahmad wildlife refuge and Parvand protected area, Iran 77 Table 1. Checklist of the Sabzevar snakes, habitats and their venomous condition, IUCN redlist status and localities in Sabzevar region (most in Shirahmad wildlife refuge and Parvand protected area) are mentioned.
78 Seyyed Saeed Hosseinian Yousefkhani et al. Figure 2. A) Boiga trigonata; B) Hemorrhois ravergieri (photographed by Saeed Hosseinian); C) Lytorhynchus ridgewayi and D) Natrix tessellata (Photographed by Ali Khani). All photos were captured in natural habitat. sand and occasionally grasslands and gardens. In the Sabzevar region the species was found in Parvand, in the south of the region that has dry climate as eastern Khorasan (see Figure 2A). Hemorrhois ravergieri (Menetries, 1832) Common English name: Spotted Whip Snake Remarks: The species is distributed in the gardens and agricultural areas. Body has some crossbars and 3 lines on the tail. In the Sabzevar region we found it in Khooshab and Jovein areas around gardens. The species is known to control rodents, but some farmers kill them and have caused rodent populations to increase. Efforts should be made to educate people on the economic value of this snake (see Figure 2B). Lytorhynchus ridgewayi (Boulenger, 1887) Common English name: Derafshi Snake Remarks: Lytorhynchus ridgewayi lives in desert and semidesert areas. The habitat of this species in Khorasan Razavi province and in Hares Abad is the sand dune and probably it can burrow in the sand. The shape of rostral scale confirms this suggestion. If Latifi (1991) is correct, ours is the first report of this species in Khorasan Province. The body is gray and has a black line from the edge of the eye to its posterior region. Dorsal body with relatively large zigzag-shaped spots. Top of the head, between the eyes, has a brown line that continues to the head and creates a brown circle. The species status in IUCN redlist is LC (least concern) because it has a wide distribution range and the species is present in protected
Snake fauna of Shirahmad wildlife refuge and Parvand protected area, Iran 79 area in NE Iran. The species is distributed in Khuzestan, Mazandaran and Kerman provinces and also in the Central Zagros (see Figure 2C). Natrix tessellata (Laurenti, 1783) Common English name: Dice Snake Remarks: Natrix tessellata lives in valleys and submontane areas. Dorsal scales are keeled and the ventral surface is black. The species is distributed in northwest, west, north and northeastern Iran, except Southeast Iran (see Figure 2D). Platyceps karelini (Brandt, 1838) Common English name: Spotted Desert Racer Remarks: Platyceps karelini lives in the open plain and the foothills. The species feeds on lizards, some rodents and insects. Approached by the collector, these snakes take refuge under shrubs and don t show any aggressive behavior. Range distribution occurs in the eastern half of Iran and it is a common snake in the Khorasan region (see Figure 3A). Platyceps rhodorachis (Jan, 1845) Common English name: Braid Snake Remarks: Platyceps rhodorachis lives in mountainous areas, foothills and deserts, and has a reddish- or brownish-orange stripe extending from nape to tip of tail dorsally. It is distributed in most provinces in Iran with the exception of Azarbaijan and Northern provinces (Guilan, Mazandaran and Golestan) (see Figure 3B). Platyceps ventromaculatus (Gray, 1834) Common English name: Glossy-bellied Racer Remarks: Platyceps ventromaculatus has a different pattern from Platyceps rhodorachis. Anterior part of the body has an irregular zigzag dark stripe with smaller spots on the sides but its posterior portion of body and entire tail is a uniform olive gray. Scalation between the two species has some overlap. Distribution range of the species is similar to P. rhodorachis in Iran (see Figure 3C). Spalerosophis diadema (Jan, 1865) Common English name: diadem snake Remarks: The species lives in deserts and open plains. General pattern of brown color with several zigzag stripes dorsally. Spalerosophis diadema has a cross line between eyes on top of the head. Unlike the other nonvenomous colubrids, Spalerosophis diadema has an aggressive behavior when approached by humans. The distribution of this species in Iran is limited to the southwest, southeast, and eastern half of Iran. Spalerosophis microlepis is another species of the genus Spalerosophis endemic to Iran, but it was not found in the surveyed area (see Figure 3F). Family Lamprophiidae Psammophis lineolatus (Brandt, 1838) Common English name: Steppe Ribbon Snake Remarks: Psammophis lineolatus is one of the backfanged but not dangerous to humans snake. The species doesn t have any aggressive behavior and usually has elusive behavior when in contact with humanity. The species lives in open plains and foothills. Eyes have circular pupils and venom teeth are situated in the posterior part of the mouth (opisthoglyphous) (see Figure 3D). Psammophis schokari (Forsskal, 1775) Common English name: Schokari Sand Racer Remarks: Psammophis schokarilives lives in scrublands, sandy deserts, fields and seasonal rivers. In contrast to Psammophis lineolatus, it has distinct spots on the body and two longitudinal stripes from head to tip of tail. Its distribution includes most parts of Iran except Northwest of Iran. The species is semivenomous ( back-fanged ) as is P. lineolatus (see Figure 3E). Family Viperidae Echis carinatus sochureki (Schneider, 1801) Common English name: Sochurek s saw-scaled viper Remarks: Sochurek s saw-scaled viper is considered the most dangerous snake in Iran, possessing highly potent venom, with LD 50 = 5.0 in mice (i.e., LD 50 is the lowest concentration of a given venom necessary to kill 50% of test animals); that is the lowest among all venomous snakes in Iran (Latifi, 1991). The shape of the head is triangular and has a cross on top of the head. Echis carinatus has an aggressive behavior and feeds on insects, small rodents, lizards and some birds. The species needs more study in Iran (see Figure 4A). Macrovipera lebetina (Linnaeus, 1758) Common English name: Blunt-nosed Viper Remarks: This viper lives in mountains, foothills and rocks. Macrovipera lebetina has LD 50 = 6.4 in mice and is the third-most dangerous snake in Iran, after Montivipera latifi (Latifi, 1991). Macrovipera lebetina has a robust body and a short tail. Examination of morphological characters in M. lebetina shows much variability in the species. The species is distributed across all Iran, with the exception of Sistan-Baluchestan Province (see Figure 4B).
80 Seyyed Saeed Hosseinian Yousefkhani et al. Figure 3. A) Platyceps karelini; B) Platyceps rhodorachis; C) Platyceps ventrimaculatus; D) Psammophis lineolatus; E) Psammophis schokari (photographed by Saeed Hosseinian (A & C) and Masoud Yousefi (B, D & E)); F) Spalerosophis diadema (Photographed by Eskandar Rastegar Pouyani). Pseudocerastes persicus (Bibron & Dumeril, 1854) Common English name: Persian horned viper Remarks: Pseudocerastes persicus doesn t have true horns, as can be observed in the genus Cerastes in Iran. The species has LD 50 = 16.2 in mice and is not especially dangerous. It lives in deserts and sandy areas. When the weather gets warmer, they retreat to the foothills. Pseudocerastes persicus is distributed in most parts of Iran (see Figure 4C). Family Elapidae Naja oxiana (Eichwald, 1831) Common English name: Central Asian cobra Remarks: Naja oxianais distributed in the northeast and east of Iran; usually it can be found in agricultural areas. Its venom effect is on the nervous system and has LD 50 = 8.3 toxicity. Its fangs are not moveable. Iranian specimens have a black color pattern (see Figure 4D).
Snake fauna of Shirahmad wildlife refuge and Parvand protected area, Iran 81 Figure 4. A) Echis carinatus (Photographed by Saeed Hosseinian); B) Macrovipera lebetina cernovi; C) Pseudocerastes persicus; D) Naja oxiana; E) Typhlups vermicularis (Photographed by Ali Khani). Family Typhlopidae Typhlops vermicularis (Merren, 1820) Common English name: Worm Snake Remarks: The species lives under the rocks in the foothills. The species is nocturnal and can usually be found under stones and it may be located by overturning stones. Ants and some arthropods larva consist on its diet. Distribution range includes the Zagros and Elburz Mountains in Iran (see Figure 4E) (Ramezani et al., 2011).
82 Seyyed Saeed Hosseinian Yousefkhani et al. Acknowledgments. We would like to thank all employees of the Environment Office of Sabzevar that cooperated with us in this project. This project was funded by the Environment Office of Sabzevar during the 3 years (2009-2011). Also we thank Sayyad Sheykhi and Ali Sheykhi, for assisting us during field surveys. Our special thanks go to Steven C. Anderson and Boaz Shacham the reviewers who assisted us in reviewing the manuscript. References Al-Sadoon, M.K. (1989): Survey of the Reptilian Fauna of the Kingdom of Saudi Arabia. Journal of King Saudi Arabia University 1: 53-69. Ananjeva, N.B., Orlov, N.L., Khalokov, R.G., Darevsky, I.S., Ryabov, S.A., Barbanov, A.V. (2004): Colored atlas of the reptiles of the North Eurasia (taxonomic diversity, distribution, conservation status). Russian Academy of Sciences.Saint- Petersburg. 232pp [in Russian with English preface]. Anderson, S.C. (1966): The turtles, lizards, and amphisbaenians of Iran. Ph.D thesis. Stanford University, 660 pp. Fathinia, B., Rastegar-Pouyani, N., Darvishnia, H., Rajabizadeh, M. (2010): The snake fauna of Ilam province, southwestern Iran. Iranian Journal of Animal Biosystematics 9: 9-23. Firouz, E. (2000): A Guide to the Fauna of Iran. Tehran University Press, Tehran. 491 pp. [In Persian]. Firouz, E. (2005): The Complete Fauna of Iran. I.B. Tauris, London & New York.322 pp. Latifi, M. (1991): The snakes of Iran. Society for the study of Amphibians and Reptiles, 159 pp. Leviton, A.E., Anderson, S.C., Adler, K., Minton, S.A. (1992): Hand book to Middle East Amphibians and Reptiles. Society for the study of Amphibians and Reptiles, 252 pp + 33 plates. Majnoonian, H., Kiabi, B., Danesh, M. (2005): Readings in zoogeography of Iran. Department of the Environment. 371pp. Ramezani, M., Kami, H.G., Ahmadpanah, N. (2011): Faunistic studies on snakes of West Golestan state. The 2nd International Geography Symposium GEOMED2010.Procedia Social and Behavioral Sciences 19: 811-817. Rastegar-Pouyani, N., Kami, H.G., Rajabizadeh, M., Shafiei, S., Anderson, S.C. (2008): Annotated checklist of amphibians and reptiles of Iran. Iranian Journal of Animal Biosystematics, 4: 43-66. Accepted by Diogo Provete