Phrynocephalus Maculates

Cibtech Journal of Zoology ISSN: 2319–3883 (Online) An Open Access, Online International Journal Available at http://www.cibtech.org/cjz.htm 2014 Vol. 3 (3) September-December, pp.60-67/Hojati et al. Research Article A PRELIMINARY STUDY ON THE BIOLOGY OF THE BLACK-TAILED TOAD AGAMA, PHRYNOCEPHALUS MACULATUS MACULATUS IN IRAN *Vida Hojati, Mahsa Malekmohammadi and Soheila Rahmani Department of Biology, Damghan Branch, Islamic Azad University, Damghan, Iran *Author for Correspondence

ABSTRACT The understudied Black-tailed toad agama, Phrynocephalus maculatus maculatus, (Anderson, 1872) belongs to the Agamidae family. Iranian specimens are rare in collections and are distributed in the central and south-eastern deserts of Iran. In this research, biological studies including food habits, morphology, behaviors and habitats of these species were performed from April to September, 2013. A total of 30 adult specimens including 15 adult males and 15 adult females were collected by hand at midday from southern parts of Damghan County, located in Semnan Province of Iran. Results show that the animal is active from early April to September, and that it hibernates from October to March. They are sit-and-wait predators. They are insectivores and their main food items belong to seven insect families including: Formicidae, Tenebrionidae, Acrididae, Noctuidae, Termitidae, Muscidae and Ixodidae. No plant consumption was observed in this species. This agama inhabits the desert, especially harder sandy surfaces. Ph. maculatus maculatus is a fairly understudied subspecies in the Middle East region and this study presents some useful information regarding this poorly known animal.

Keywords: Lizards, Agamidae, Phrynocephalus Maculatus Maculatus, Food Habit, Morphology

INTRODUCTION The Spotted Toad-headed Agama, Phrynocephalus maculatus, is a member of Agamidae family, which is also known as the chameleons of the Old World due to their striking ability to change their body color (Firouz, 2005). This species originates from Iran, Iraq, Afghanistan, Pakistan Turkmenistan, Syria, Oman, northern Saudi Arabia, Kuwait and the United Arab Emirates. The only identified subspecies of this species in Iran is Black-tailed toad agama, Ph. maculatus maculatus (Anderson, 1872) scattered on the Central Plateau of Iran, at elevations between 500 and 3000 m, east through southern Afghanistan and Baluchistan, and extending into Nushki, Pakistan (Anderson, 1999). Ph. maculatus longicaudatus (Haas, 1957) is found along the Persian Gulf coast of Saudi Arabia, and may extend into both Iraq and south- western Iran. No species of Phrynocephalus crosses the Zagros Mountains and there are no ecologically continuous areas between the present ranges of Ph. m. maculatus and Ph. m. longicaudatus (Anderson, 1999). Iranian specimens are rare in collections and are distributed in the central and south-eastern deserts of Iran. This agama inhabits desert regions, desiring harder sandy surfaces (Hellyer and Aspinall, 2005). This animal is capable of sinking rapidly into the sand through vibrating the body in a process called ‘shimmy burial’, and this behavior is used to escape from predators or create a nocturnal shelter (Firouz, 2005; Hellyer and Aspinall, 2005). This species has yet to be assessed by the IUCN. Consequently, it is currently unclear whether there are many major threats to the species or not (Alsharhan et al., 2008). Like many other species of reptile in the Middle East, the spotted toad-headed agama is a fairly understudied species. As such, it is currently unclear if there are many major threats to the species. Since no enough information is available regarding the biology of this subspecies, this research was performed to conduct preliminary studies on the biology including food habits, morphology, behaviors and habitats of this subspecies in Iran.

MATERIALS AND METHODS Study Area: all specimens were collected from the four following stations: Hassan Abad, Saleh Abad, Alian and Yazdan Abad villages located in south of Damghan County, Semnan Province (54°19′E, © Copyright 2014 | Centre for Info Bio Technology (CIBTech) 60

Cibtech Journal of Zoology ISSN: 2319–3883 (Online) An Open Access, Online International Journal Available at http://www.cibtech.org/cjz.htm 2014 Vol. 3 (3) September-December, pp.60-67/Hojati et al. Research Article 35°55′N). Damghan is situated 1170 m above sea level and north of the Central Kavir Desert (Figures 1 and 2). Sampling: sampling was conducted periodically during the activity period of this species from April to September, 2013. All specimen collections were by hand, from 9 AM to 4 PM. In total, 30 specimens (15 adult males and 15 adult females) were captured. To study their morphology, food habits and behavior, some specimens were kept in terrarium. Methods: the specimens were transferred alive to the Zoology Laboratory of Islamic Azad University, Damghan Branch. Their food habits and behaviors were studied both in terrarium and in the environment.

Figure 1: Map showing the sampling site (Damghan County) in northern Iran

Figure 2: Hassan Abad station located in south of Damghan County, Semnan Province, Iran

Cibtech Journal of Zoology ISSN: 2319–3883 (Online) An Open Access, Online International Journal Available at http://www.cibtech.org/cjz.htm 2014 Vol. 3 (3) September-December, pp.60-67/Hojati et al. Research Article Then, they were anaesthetized by chloroform and morphological characters including W (Weight), SVL (South-Vent Length), TL (Tail Length) and HL (Head Length), HW (Head Width), and SMB (Scales around the Middle of the Body) were measured. Length, width and diameter measurements were done by a dial caliper with an accuracy of 0.02 mm. Weight was measured by a scale with an accuracy of 0.001 g. Then animals were dissected and the stomach containing was fixed in 10% formalin. Data was analyzed by SPSS 18 software, one-way ANOVA and Tukey test to compare biometric data among monthly samples (P> 0.05).

RESULTS AND DISCUSSION Results Morphology: There was no cutaneous fold at angle of mouth (Figure 3) and nasal scales were separated by one to three scales (Figure 4). No fringe of scales occurred on posterior border of tight and sides of base of tail. Sides of head and neck were without projecting fringe-like scales. Dorsal scales were homogeneous. There were no enlarged scales along flanks. Scales on vertebral region were considerably larger than those on flanks. Tail length was 140-158 percent of snout-vent length. Dorsum was light gray, flecked with lighter and darker pigments. There were four indistinct dark broad transverse marks on their back which were absent on large adults. Limbs and toes were barred with dark gray in young specimens; tail barred with dark gray dorsally in young, fading to indistinct spots in adults; barred with light gray on posterior half, coalescing with age to form more or less uniform gray ventral surface of distal half of tail of young lizards of both sexes sometimes with considerable orange-red in life. SVL and LCD of males reach to 66.67 and 102.18 mm, respectively. SVL and LCD of females reached to 60 and 85 mm, respectively. Table 1 indicates the descriptive statistics of morphometrical characters in males and females.

Table 1: Descriptive statistics of the males (M) and females (F) of Phrynocephalus maculatus maculatus Mean Characters Sex N Minimum Maximum Statistic Std. Error Std. Deviation Variance W (g) M 15 5.36 11.04 7.72 0.409 1.58 2.51 F 15 3.93 9.36 5.20 0.395 1.53 2.34 SVL (mm) M 15 51.91 66.76 60.05 1.042 4.03 16.30 F 15 39.00 60.00 50.34 1.293 5.01 25.10 LCD (mm) M 15 85.00 102.18 92.32 1.153 4.46 19.95 F 15 69.98 85.93 78.53 1.066 4.12 17.05 HL (mm) M 15 11.17 15.54 13.23 0.300 1.16 1.35 F 15 11.34 14.32 12.19 0.194 0.75 0.56 HW (mm) M 15 11.23 13.54 12.57 0.167 0.64 0.42 F 15 10.10 14.37 11.51 0.278 1.07 1.16 SMB M 15 92 118 99.80 4.613 17.86 319.17 F 15 97.00 115.00 106.73 1.538 5.95 35.49

Figure 3: Phrynocephalus maculatus maculates

Figure 4: Phrynocephalus maculatus maculatus

Food Habits: Ph. maculatus maculatus is insectivore and its prey items identified in their stomach and in the environment are shown in Table 2. There is no significant difference in prey items of males and females. Larger and adult specimens can take larger insects. They are sit-and-wait predators. The most abundant prey items observed in their locality and found in their stomach were ants belonging to Formicidae family (Figure 5). Figures 6 to 11 demonstrate the identified prey items in Ph. maculatus maculatus.

Cibtech Journal of Zoology ISSN: 2319–3883 (Online) An Open Access, Online International Journal Available at http://www.cibtech.org/cjz.htm 2014 Vol. 3 (3) September-December, pp.60-67/Hojati et al. Research Article Table 2: Prey items in Phrynocephalus maculatus maculatus Class Order Family Name Frequency of Prey Items (%) Male Females Insecta Hymenoptera Formicidae Ants 82 84 Coleoptera Tenebrionidae Darkling Beetle 7 4 Orthoptera Acrididae Desert Locusts 3 2 Lepidoptera Noctuidae Moths 2 3 Isoptera Termitidae Termites 2 2 Diptera Muscidae Domestic Flies 2 3 Arachnida Acarina Ixodidae Ticks 2 2

Figure 5: Ant-hunting in Phrynocephalus maculatus maculatus in Hassan Abad, Iran

Figure 6: Darkling Beetle (Tenebrionidae(Figure 7: Ant (Formicidae)

Figure 8: Desert Locust (Acrididae) Figure 9: Moth (Noctuidae)

Figure 10: Fly (Muscidae) Figure 11: Tick (Ixodidae)

Behavior: The animal activities begin from early April to September, and it hibernates from October to March. The activity of this species occurs during all but the hottest hours of the day, scurrying across the sand and in the hunt for its insect prey. During the hottest periods to limit contact with the sand, it will stand high on extended legs trying to balance on fingertips and heels while using the tail as a prop. Their reproductive activity occurs in May and June and reduces in July and ends in August. Ph. maculatus curls the tail upward when alarmed. The activity of matures is decreased from mid-August to late September, but the activity of juveniles will be increased. This animal is diurnal. In spring, the activity of specimens is decreased from 1:00 to 4:00 p.m. and in autumn is decreased from 1:00 to 5:00 p.m. Because of their similar color with the environment, they have very strong camouflage with their surroundings and do not appear as long as they move. They escape from the heat by going under the shade of bushes and even into their hiding places and burrows. They remain in the same location until the temperature is decreased again. The heat does not reach its peak in the first half of day and surface of the sand is not still warm and they prefer to activate on the sand. But in the afternoon, near sunset, the surface sand is hotter than deep sand and to regulate their body temperature sink into the sand. The strategy of burrowing or sinking under the sand was only observed in the afternoon from 1:00 to 5:00 p.m. © Copyright 2014 | Centre for Info Bio Technology (CIBTech) 65

Cibtech Journal of Zoology ISSN: 2319–3883 (Online) An Open Access, Online International Journal Available at http://www.cibtech.org/cjz.htm 2014 Vol. 3 (3) September-December, pp.60-67/Hojati et al. Research Article Habitat: The study area was composed of alkaline saline soils containing clay and sand. The lizards are diurnal and stay on clay and loamy soils. Most of the lizards were observed on highly saline, loose soil covered with a thin salt crust, and were common near Tamarix bushes. The vegetation in this locality is scanty, mostly herbaceous. The dominant plant species are Tamarix sp., Salsola sp., Alhaji sp., Peganum sp., Atriplex sp. and Astragalus sp. The annual average temperature is 17.2°C. Figure 3 shows the Ph. maculatus in its natural habitat at Hassan Abad. Other lizards collected with it in this region were: Teratoscincus bedriagai, Bunopus tuberculatus, Tenuidactylus caspius, Eremias fasciata, Eremias intermedia, Eremias persica, Eremias velox velox, Mesalina watsonana, Phrynocephalus scutellatus, Trapelus agilis; and collected snakes were: Eryx jaculus turcicus, Psammophis schokari, Spalerosophis diadema schiraziana, Platyceps karelini karelini, and Hemorrhois ravergieri. Discussion The head of Ph. maculatus is short and broad, with a deep forehead and snub nose, and the flattened body is wide and strong and covered in rough skin with overlapping scales (Halliday and Adler, 2002; Ananjeva et al., 2006). The long, flattened tail is rounded at the base and has a black tip on the underside which, when raised, is used in visual signals (Halliday and Adler, 2002). The body color of this lizard is significantly variable, but typically has distinct brown bars across the body and tail. It also tends to match the color of its background and lizards found on pale coastal sands are known to be paler and less patterned than those on red, inland sands (Hellyer and Aspinall, 2005). In present study, nocturnal activity was not observed in this species. In a previous study, SVL and LCD of males were recorded to reach to 91 and 128 mm, respectively (Anderson, 1999). In this research, maximum SVL and LCD of males were recorded 66.76 and 102.18 mm, respectively and results show that males' size probably are larger than females. Like other species of Phrynocephalus, Ph. maculatus curls the tail upward when alarmed reminiscent of inguids such as Callisaurus, Holbrookia, and Liocephalus, which also have dark bars on the ventral surface of tail (Anderson, 1999). In Sistan, they perched on almost every pile of dirt and gravel heaped at the edge of the road for road maintenance. From these perches, they would run for up to 75 m across the hammada, freezing suddenly, their color rendering them invisible. They were never seen seeking refuge in burrows (Anderson, 1999). It has been reported that they are lizards of flat deserts, occurring in sandy flats with low, scattered shrubs in Kerman, on sandy, gravel-strewn hammada in Sistan, and on barren salt flats in Khorasan. Blanford (1876) and Minton (1966) found them in similar areas in both Iran and Pakistan. Anderson has recorded the SMB of Iranian and Arabian specimens of Ph. maculatus 99-115 and 106–119, respectively; but in this study, SMB was recorded between 92 and118. Earlier, it was reported that the ants were the most common prey item for most of insectivorous lizards of Iran (Anderson, 1999), and in this research, we observed that the ants were the favorite item for this species and they prefer ants to other items. It's probably because ant-hunting is very comfortable and the lizards stand near ants and just bring out their tongue. Also, little energy is required for preying them. On the other hand, the mass distribution of ants decreases the pursuing energy (Saenz, (1996). The identified ants in Damghan County belong to 23 species from twelve genera and three subfamily including: Cataglyphis sp., Cataglyphis nodus, Cataglyphis sp., Cataglyphis sp., Cataglyphis emeryi, Camponotus sp., Camponotus sp., Camponotus turkestanus, Proformica sp., Plagiolepis sp., Lepisiota semenovi, Lepisiota sp., Tetramorium sp., Tetramorium sp., Crematogaster sp., Crematogaster sp., Messor sp., Messor intermedius, Messor sp., Cardiocondyla sp., Pheidole sp.,Monomorium kusenzovi and Tapinoma erraticum (Hojati et al., 2009). Cataglyphis nodus was the most common species in steppe region and Monomorium kusenzovi was the most common species in desert region of Damghan (Hojati et al., 2009). There were more species with high abundance in desert regions of Damghan such as the study area (Hojati et al., 2009). Blanford (1876) chiefly found ants in specimens collected from Iran and Minton (1966) reported beetle and other insect remains, as well as seeds and other plant materials. Vegetation diet was not observed in this study. Scurrying across the sand, seeking out its insect prey, the spotted toad-headed agama is active in all but the hottest hours of the day. During the hottest periods, it will stand high on extended legs to limit contact

Cibtech Journal of Zoology ISSN: 2319–3883 (Online) An Open Access, Online International Journal Available at http://www.cibtech.org/cjz.htm 2014 Vol. 3 (3) September-December, pp.60-67/Hojati et al. Research Article with the sand, balancing on fingertips and heels while using the tail as a prop. It may remain dormant during cold winter days (Hellyer and Aspinall, 2005). To sum up, this preliminary study on the biology of Ph. maculatus maculatus in Iran will pave the way for further studies on this species for herpetologists all around the world.

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