Herpetology Notes, volume 11: 481-487 (2018) (published online on 24 June 2018)

A preliminary study on the biology of the Diadem snake (Spalerosophis diadema) from Iran (Reptilia: Colubridae)

Reza Yadollahvandmiandoab1,*, Daniel Oliveira Mesquita1 and Haji Gholi Kami2

Abstract. Iran possesses varied climatic and geographical conditions leading to a rich biodiversity. The Diadem snake, Spalerosophis diadema, is one of the non-venomous oviparous snakes of the family Colubridae, with a wide distribution in Iran. We performed an investigation on the biology of S. diadema in Iran from 2014 to 2015. We examined a total of 62 specimens from zoological museums and collections. We studied the morphologic, morphometric and meristic characters, and also diet, habitat, reproduction and behaviour of S. diadema. To our knowledge, this is the first report on biology of S. diadema from Iran and it provides basic useful information that may be used for population studies.

Key Words: Morphology, Reproduction, Diet, Distribution, Behaviour

Introduction 2014). The genus Spalerosophis Jan 1865, which is belongs to the Colubrinae, is widely distributed in The name “Colubridae” is derived from the rather non- arid and semiarid regions from northwestern Africa to descript Latin, “coluber”, the general term for “snake” northern India; its Saharo-Sindian range area covers or “serpent”. In excess of 3600 species of extant snakes, three distinct regions, i. e. Afro-Arabia, Irano-Turan and the previous definition of the Colubridae comprise one of Indo-Pakistan (Marx, 1959). the largest and most diverse family of snakes (Weinstein Boulenger (1892) synonymized Spalerosophis with et al., 2013; Vitt and Caldwell, 2014). Highly variable in Zamenis, but in the original description of the genus the size, body form, and colour pattern; ranges from short, name is given as Spalerosophis. To date, the number stout, drab species to large, slender, boldly marked of Spalerosophis spp. has doubled from three to six, forms. Fossils attributed to the Colubridae first appear including Spalerosophis arenarius (Boulenger, 1890) in the Lower Oligocene, about 35 million years ago. and S. atriceps (Fischer, 1885) from northern India and Members of the Colubridae occur worldwide, except Pakistan, S. diadema from the western Sahel and Sudan Antarctica, the highest latitudes of North America to Central Asia and northwestern India, S. dolichospilus and Eurasia, and the central and western regions of (Werner, 1923) from the Maghreb, S. josephscorteccii Australia (McDade and Schlager, 2003). This family (Lanza, 1964) from Galgalo Oasis in northwestern has seven subfamilies includes: Colubrinae, Grayiinae, Somalia and S. microlepis Jan, 1865 from western Iran Calamariinae, Dipsadinae, Pseudoxenodontinae, (Zagros range) (Minton, 1966; Baig and Masroor, 2008; Natricinae, Scaphiodontophiinae (Vitt and Caldwell, Uetz and Hošek, 2017). Spalerosophis diadema is a wide-ranging colubrid snake of the semi-arid belt from West Africa to Central Asia and the northwestern Indian Peninsula (Schatti et al., 1 Programa de Pós-graduação em Ciências Biológicas (Zoologia), 2010). Marx (1959) first assigned Asian Spalerosophis Departamento de Sistemática e Ecologia – DSE, Centro de populations from India and Pakistan to the nominate Ciências Exatas e da Natureza – CCEN, Universidade Federal subspecies, Saharo-Arabian populations to S. d. cliffordii da Paraíba – UFPB, Cidade Universitária, Campus I, CEP (Schlegel, 1837), and used S. d. schirasianus (Jan, 1863) 58059-900, João Pessoa, PB, Brazil. for populations from Turkmenistan and most of Iran, to 2 Department of Biology, Faculty of Sciences, Golestan University, Gorgan, Golestan, Iran. Uzbekistan including the Fergana valley (Kyrgyzstan, * Corresponding author. E-mail: Tadzhikistan) and Baluchistan, Pakistan (Marx, 1959). [email protected] Spalerosophis diadema has a wide distribution in Iran 482 Reza Yadollahvandmiandoab et al.

1 Table 1. Traditional morphometricTable characters 1. Traditional recorded. morphometric characters recorded. 2 No. Character Definition Explanation 1 SVL Snout to cloaca From tip of the snout to the cloacal vent 2 TL Tail length From the cloacal vent to the tip of the tail 3 HL Head length From the tip of the snout to the angle of the jaw 4 HW Head width Maximum width of the head 5 SL Snout length From tip of the snout to the anterior edge of the eye 6 SW Snout width Distance between the eyes on the dorsum of the head 3 4 Table 2. Traditional meristic characters recorded. 5 No. Character Definition Explanation occurring1 in differentCS habitatsChin and shield ecological scales conditions, fieldwork,The number during of chin2014–2015. shield scales The collection locations from arid 2and desertV (D) areas Ventral in the scales east (Dowling)and centre of Iran The numberof studied of ventral specimens scales according are showed to Dowling in Fig. method 1. We measured to the mountainous3 SC areas in theSubcaudal west of the country. sixThe standard number of morphometricsubcaudal scales in and one row17 meristic characters Given that4 S. diademaC has notC loacabeen scales poorly studied in Whether(Tables the 1, cloacal 2) on plate each is specimen.divided or undivided All measurements were Iran, the overall5 distributionDF Dorsal of thisscales species (Front) is known,The number performed of dorsal scales using one digitalhead’s length callipers posterior accurate of the head to 0.05 mm. and our knowledge6 DM is based Dorsal on only scales a (Mid) limited number SPSSThe number (version of dorsal 21) wasscales usedat midbody to analyse the data. We of specimens7 housedDH in museumDorsal collections.scales (Hind) Therefore,The number were of dorsal allowed scales oneto dissecthead’s length a small anterior number of the cloaca of specimens our goal 8 was to SL perform a Supralabial preliminary scales study of the Ttohe study number the of supralabialfeeding and scales reproductive (Left-Right) system. We also biological9 characteristics IL of theInfralabial species scales that may lead to usedThe number museum of infralabial records scales and (Left-Right)some personal records from a better understanding10 LO and conservation Loreal scales of S. diadema ourThe sampling number of fieldworks loreal scales (Left-Right)in central and east of Iran, for in Iran. 11 Pr.O Preocular scales behaviourThe number andof preocular habitat scales studies. (Left-Right) 12 SO Subocular scales The number of subocular scales (Left-Right) Material13 and methodsPo.O Postocular scales ResultsThe number of postocular scales (Left-Right) 14 T Temporal scales The number of postocular scales (Left-Right) We collected 62 specimens from zoological museums Brief description and measurements.—Spalerosophis 15 Pr.N Prenasal scales The number of prenasal scales (Left-Right) in Golestan University (ZMGU), Ferdowsi University 16 Po.N Postnasal scales diademaThe number is of an postnasal aglyphous scales (Left-Right) snake with simple, uniform (ZMFUM), Hakim Sabzevari University (HSUZM), 17 CO CirOcular scales Theand number bent backof scales teeth. around The eyes body (Left-Right) is elongated, light gray some personal zoological collections and also from 6 to brown, with 69–95 dark polygonal spots on dorsal 7 Table 3. Standard morphometric measurementssurface for S.and diadema, small black given spots in millimeters. on the sides of the body. 8 The head is distinct from neck. There is a dark brown Character N Minimum Maximumstripe between Mean and behind Std. the Deviation eyes and the ventral SVL 61 271.00 1190.00surface are usually634.90 white to light252.18 cream and unmarked. TL 61 48.00 290.00The eyes are relatively150.96 large with61.84 round pupils (Figs. HL 61 16.01 40.373, 4). 26.45 7.08 HW 61 8.53 26.12The prefrontal15.07 scales are segmented4.35 into 3–4 small SL 61 4.78 14.81scales and three 8.57rows of scales between2.55 the frontal and SW 61 6.33 1rostral4.25 scales. There9.20 are 4–11 loreal1.99 and 3–4 subocular 9 scales. The supralabials are separated from the eye by 10 11 the subocular scales. The temporal scales comprise two vertical scales and small rows of scales; the first row 1 includes 3–7 and second row 4–7 scales. There are 7–12

circumocular scales. The supralabials and infralabials number 10–14 and 11–14 scales respectively, with 3- 4 infralabials scales in contact with the anterior chin shield scale. The posterior and anterior chin shield scales are subequal, and there are 4–5 oblique rows of gulars between the posterior chin shields and the first Figure 1. The locations of examined specimens of S. diadema ventral. This species has 223–251 ventral scales, 21– in Iran. 29 dorsal scales at midbody, 66–89 subcaudal scales, 1 Table 1. Traditional morphometric characters recorded. 2 No. Character Definition Explanation 1 SVL Snout to cloaca From tip of the snout to the cloacal vent 2 TL Tail length From the cloacal vent to the tip of the tail 3 HL Head length From the tip of the snout to the angle of the jaw 4 HW Head width Maximum width of the head A preliminary5 study onSL the biologySnout of the length Diadem snakeFrom from tip Iranof the snout to the anterior edge of the eye 483 6 SW Snout width Distance between the eyes on the dorsum of the head 3 4Table 2. Traditional meristic charactersTable recorded. 2. Traditional meristic characters recorded. 5 No. Character Definition Explanation 1 CS Chin shield scales The number of chin shield scales 2 V (D) Ventral scales (Dowling) The number of ventral scales according to Dowling method 3 SC Subcaudal The number of subcaudal scales in one row 4 C Cloaca scales Whether the cloacal plate is divided or undivided 5 DF Dorsal scales (Front) The number of dorsal scales one head’s length posterior of the head 6 DM Dorsal scales (Mid) The number of dorsal scales at midbody 7 DH Dorsal scales (Hind) The number of dorsal scales one head’s length anterior of the cloaca 8 SL Supralabial scales The number of supralabial scales (Left-Right) 9 IL Infralabial scales The number of infralabial scales (Left-Right) 10 LO Loreal scales The number of loreal scales (Left-Right) 1 11 Pr.O PreocularTable 1. scales Traditional morphometricThe number characters of preocular recorded. scales (Left-Right) 2 12 SO Subocular scales The number of subocular scales (Left-Right) 13No. Po.O Character Postocular Definition scales The number of postocularExplanation scales (Left-Right) 14 1 T SVL TemporalSnout scales to cloaca TheFrom number tip of thepostocular snout to scales the cloacal (Left-Right) vent 15 2 Pr.N TL PrenasalT ailscales length TheFrom number the cloacal of prenasal vent toscales the tip(Left-Right) of the tail 16 3 Po.NHL PostnasalHead scales length FromThe numberthe tip of of the postnasal snout to scales the angle (Left-Right) of the jaw 17 4 CO HW CirOcularHead scales width The numberMaximum of scales width around of eyes the head(Left-Right) 6 5 SL Snout length From tip of the snout to the anterior edge of the eye 7 6 TableSW 3. Standard morphometricSnout width measurementsDistance for between S. diadema, the eyes givenon the dorsumin millimeters. of the head 8 3 Character N Minimum Maximum Mean Std. Deviation 4 Table 2. Traditional meristic characters recorded. 5 and the cloacal plateSVL is undivided.61 The271.00 dorsal scales 1190.00 average annual634.90 rainfall of less than252.18 200 mm in central and are keeled.No. The Character maximumTL length61 Definition of body 48.00 is 1190 mm 290.00east of Iran toExplanation150.96 west of Zagros 61.84Mountains with altitude and maximum1 lengthCSHL of tailChin is61 290shield mm. scales 16.01Tables 1 and 40.37more The than number 2000 26.45of chinm shieldand 200–400 scales 7.08 mm average annual 2 summarize2 theV descriptive (D)HW Ventral statistics61 scales (Dowling) of morphometric 8.53 The number26.12rainfall of ventral (Fig. scales 6).15.07 Also, according the average to Dowling4.35 annual method temperature in SL 61 4.78 14.81 8.57 2.55 and meristic3 measurementsSC for SubcaudalS. diadema . differentThe number regions of subcaudal of the scales distribution in one row zones of this species SW 61 6.33 14.25 9.20 1.99 4 C Cloaca scales Whetheris different the cloacal between plate is divided10 ° C or in undivided the coldest region to 25 9 Reproduction.—Spalerosophis diadema is an 5 DF Dorsal scales (Front) The number of dorsal scales one head’s length posterior of the head 10oviparous snake and reproduces during the summer, the ° C in the warmest region. Vegetation of these areas is 6 DM Dorsal scales (Mid) The number of dorsal scales at midbody 11 composed of dispersed shrubs and annual grasses in female laying7 3–10DH eggs dependingDorsal scales on (Hind) her bodyThe size. number of dorsal scales one head’s length anterior of the cloaca 1 clayey to sandy lands. They are also frequently seen We found8 ten eggsSL in a female Supralabial specimen scales (ZMGU 1484) The number of supralabial scales (Left-Right) in the vicinity of human settlements, gardens and rural with SVL9 1190 mmIL from AhvazInfralabial province scales (Fig. 5). The The number of infralabial scales (Left-Right) houses. largest egg10 measuredLO 52.28 mm Loreal x scales21.35 mm. All ten The number of loreal scales (Left-Right) egg measurements11 Pr.O from this Preocularfemale scalesspecimen (ZMGU TheDiet. number—There of preocular is little scales information (Left-Right) available about the 1484) are included in Table 5. 12 SO Subocular scales Tfeedinghe number habits of subocular of this scales species. (Left-Right) In the digestive system of Habitat.13— SpalerosophisPo.O Postocular diadema scales lives in the arid Thethe number14 studied of postocular specimens, scales (Left-Right)we found fragments of body and semiarid14 plainsT with altitude Temporal ranges scales from 800 m and Tandhe number feathers of postocular of small scales birds, (Left-Right) hair and skin of rodents, 15 Pr.N Prenasal scales The number of prenasal scales (Left-Right) 16 Po.N Postnasal scales The number of postnasal scales (Left-Right) 17 CO CirOcular scales The number of scales around eyes (Left-Right) 6 7 Table 3. StandardTable morphometric 3. Standard measurements morphometric for S. measurementsdiadema, given infor millimeters. S. diadema, given in millimeters. 8 Character N Minimum Maximum Mean Std. Deviation SVL 61 271.00 1190.00 634.90 252.18 TL 61 48.00 290.00 150.96 61.84 HL 61 16.01 40.37 26.45 7.08 HW 61 8.53 26.12 15.07 4.35 SL 61 4.78 14.81 8.57 2.55 SW 61 6.33 14.25 9.20 1.99 9 10 11 1

484 Reza Yadollahvandmiandoab et al.

Table 4. Standard meristic measurements for S. diadema. 12 Table 4. Standard meristic measurements for S. diadema. 13 Character N Minimum Maximum Mean Std. Deviation CS 62 2 2 2.00 0.00 V (D) 62 220 248 232.93 7.47 SC 57 66 89 82.45 3.85 C 62 1 2 1.01 0.12 D.F 62 23 28 25.41 1.23 D.M 62 21 29 27.30 1.48 D.H 62 17 19 17.67 0.91 D+10 62 24 30 26.40 1.45 D-10 62 17 27 17.82 1.48 SL.L 61 10 14 12.34 0.75 SL.R 61 10 13 12.18 0.69 IL.L 60 11 14 13.11 0.69 IL.R 60 11 14 13.26 0.73 LO.L 61 4 10 5.67 1.04 LO.R 61 4 11 5.65 1.13 Pr.O.L 61 1 3 1.96 0.44 Pr.O.R 61 1 3 1.96 0.40 SO.L 61 3 5 4.04 0.28 SO.R 61 3 4 3.93 0.24 Po.O.L 61 2 4 2.93 0.40 Po.O.R 61 2 4 2.86 0.38 T.L1 61 3 7 4.73 0.96 T.L2 61 4 7 5.34 0.83 T.R1 61 3 7 4.85 0.87 T.R2 61 4 7 5.24 0.78 Pr.N.L 61 1 1 1.00 0.00 Pr.N.R 61 1 1 1.00 0.00 Po.N.L 61 1 1 1.00 0.00 Po.N.R 61 1 1 1.00 0.00 CO.L 61 8 12 9.93 0.72 CO.R 61 7 12 9.77 0.76 14 15 16 17 18 19 20 21 22 2  

Figure 2. Histogram of the body length and tail length of S. diadema. A preliminary study on the biology of the Diadem snake from Iran 485

Figure 3. Spalerosophis diadema, Yazd Province, Iran, 2014, (photo by H.G. Kami).

genus Meriones and specimens of lacertid lizard, genus Eremias. Activity and Behaviour.—This species is diurnal, but it avoids the head of the day but sheltering under shrubs or in rocky crevices. When encountered by humans it usually escapes but it may mimic the movements and sounds of the highly venomous saw-scale or carpet vipers of genus Echis. If all else fails it may bite.

Discussion Due to its large size, and geographical diversity, resulting in the existence of diverse habitats with different ecological conditions, Iran also exhibits considerable zoological diversity. The study and identification of biological characteristics of Iranian species is one of the first and most important steps to be taken leading towards a policy of conservation of the biological diversity. Previous researchers have surveyed the snakes of Iran; among them, Mahmoud Latifi (2000) who compiled a handbook “The Snakes of Iran” and Mehdi Rai (1965) who wrote his dissertation on Iranian colubrid snakes. In recent years, Iranian researchers such as Karimi et al. (2001), Rajabizadeh and Rastegar- Pouyani (2006), Bostanchi et al. (2006), Kami and Najafi (2007), Rastegar-Pouyani et al. (2008), and Figure 4. Lateral (A) and Dorsal (B) views of the head of Fathinia et al. (2010) have conducted valuable surveys S. diadema, Golestan University, Iran, ZMGU 1952, 2014, on the snake fauna on the Iranian Plateau. Currently 87 (photo by R. Yadollahvandmiandoab). snake taxa are recorded from Iran, with S. diadema being 486 Reza Yadollahvandmiandoab et al.

Table 5. Biometry of studied eggs of S. diadema. 23 Table 5. Biometry of studied eggs of S. diadema. 24 No. Length Width 1 52.28 21.35 2 32.03 23.16 3 40.29 24.43 4 46.33 20.73 5 44.52 22.85 6 40.81 23.16 7 38.39 22.91 8 42.93 22.92 9 41.13 23.33 10 42.64 21.56 25  Figure 6. S. diadema habitat, Yazd province, Iran, 2017, (photo by J. Shokohi).

one of the most widely distributed snakes. Because of its adaptation to a variety of habitat types and different ecological conditions, S. diadema can occupy a wide studies in Iran (Latifi 2000; Fathinia et al. 2010), however range of habitats (Rastegar-Pouyani et al. 2008). As this variation in morphological measurements may be due species feeds on some rodents with high reproduction to different ecological conditions in different habitat rates, its role may be considerable importance in control zones in Iran and other countries. However, although of some rodent populations. we are not able to perform statistical comparisons According to our study, the population of S. diadema of specimens across habitats, the values are nearly in Iran look similar to specimens from Pakistan, Turkey the same. In addition, due to the lack of information and Iraq in terms of morphological characteristics about the biology of this species in Iran, the current (Baig and Masroor, 2008; Franzen, 2009; Afrasiab and study is the first one conducted concerning population, Mohamad, 2014). The specimens in this study show reproduction, behaviour, feeding and distribution of similar morphological characters as those from previous this species. Although previous studies (Marx 1959; Schatti et al. 2010) divided the Iranian populations of S. diadema into two subspecies based on size (S. diadema cliffordii: less than 80 subcaudal scales, S. diadema schirasianus: more than 80 subcaudal scales), this could potentially be influenced different ecological conditions, and samples from a wider distribution are necessary to confirm this issue. Therefore, it is recommended that a population study using molecular phylogenetic methods should be conducted for Iranian samples in the future. Finally, due to the importance and role of this species in the maintenance and control of the balance of nature in its distribution zones, further studies are 3 necessary. Our study should be considered a prelude to  more comprehensive on this and other Iranian snakes  species.

Acknowledgments. We wish to thank Dr. Eskandar Rastegar- Pouyani from Hakim Sabzevari University and Dr. Farahnaz Molavi from Ferdowsi University for their cooperation on access to specimens from zoological museums. We are grateful to Mr. Figure 5. A female S. diadema and its eggs, Iran, 2014, Reza Babaei and Mr. Mohammad Zarrintab for their help in (ZMGU 1484) (photo by R. Yadollahvandmiandoab) sample collection. A preliminary study on the biology of the Diadem snake from Iran 487

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Accepted by Daniel Portik