УДК 598.112.13(4/5) ББК 28.693.34(051) П16

Панов Е.Н., Зыкова Л.Ю. Горные агамы Евразии. М.: Товарищество научных изданий КМК. 2016. 289 c., библ. 302 назв., 69 табл., 39 илл., 36 цветных вкладок (на англ. яз.). Книга представляет собой первый обзор на английском языке систематики и биологии ком- пактного таксона ящериц (около 20 видов), обитающих в пересеченных аридных и высоко- горных ландшафтах Евразии и северо-восточной Африки. Эти рептилии в последнее время привлекают пристальное внимание герпетологов из-за своей заметности, обязанной сугубо дневному образу жизни и высокой численности и плотности популяций, характерной для большинства видов. До сих пор интерес герпетологов был сосредоточен главным образом на систематике и номен- клатуре горных агам, а серьезные исследования по их образу жизни, экологии и поведению крайне немногочисленны. В этой книге наряду с обзором наиболее важной опубликованной информацией по изученным представителям таксона дана развернутая картина всех сторон биологии модельного вида – кавказской агамы Paralaudakia caucasia и его взаимоотношений с другим – хорасанской агамой P. erythrogaser. На протяжении 10 лет полевых исследований прослеживались биографии многих конкретных особей и изучались тонкие детали коммуника- тивного процесса в нескольких локальных популяциях. В основу исследования положен анализ социального поведения как фактора, интегрирующего дем в некую общность системной природы. Главной задачей было рассмотреть структуру в ее трансформациях из года в год как процесс изменений в поведении и социальных ролях взрос- лых особей и детенышей, ежегодно пополняющих контингент дема. Другие важные темы, затронутые в книге — это разнообразие носителей коммуникативной информации (оптическая, химическая, тактильная) у модельного и ряда других видов, а также характер взаимоотношений между близкородственными формами в зонах их контакта. К книге прилагается цифровой диск с многочисленными видеозаписями поведения 12 видов ящериц.

On the front cover: Caucasian Rock Agama Paralaudakia caucasia. SW Turkmenistan. Photo by E.N. Panov

© Е.Н. Панов, Л.Ю.Зыкова, 2016 ISBN 978-5-9907838-6-7 © Товарищество научных изданий КМК, издание, 2016 CONTENTS

Authors preface ...... 8 Objectives, goals and background ...... 8 State of our knowledge of communicative behavior in lizards ...... 10 The state of things as deduced from systematic fi eld research data ...... 11 The interdependence between the structure of the covers, coloration and behavior of lizards ...... 12 The nature of theoretical generalizations on the evolution of signal behavior in lizards ...... 13

Materials and methods ...... 14

Acknowledgements ...... 17

Introduction ...... 18 Taxonomic structure of the genus Laudakia s. lato ...... 20 Usual sources of disagreements in classifi cations of rock agamas ...... 21 Intraspecifi c geographical variability...... 21 Erroneous description of ‘new’ species based on specimens of a hybrid origin ...... 24 Undue haste in describing new forms ...... 24 Description of new taxa as an end in itself ...... 24 Modern state of the rock agamas systematic ...... 27

Chapter 1. General information on Eurasian rock agamas ...... 29 1.1. Morphological features ...... 33 1.1.1. General characteristic ...... 33 1.1.2. Size and proportions ...... 37 1.1.3. Pholidosis ...... 39 1.1.4. Coloration ...... 51 1.1.5. Molt ...... 56 1.1.6. Karyotypes ...... 56 1.2. Habitats and numbers ...... 57 1.2.1. Terrain and substrate structure ...... 57 1.2.2. Temperature and the altitudinal range ...... 58 1.2.3. Vegetation ...... 59 1.2.4. Numbers ...... 61 1.3. Social organisation and demographic structure of rock agama populations ...... 62 1.3.1. Social organisation ...... 63 1.3.2. Use of space by rock agamas ...... 64 1.3.3. Sex and age structure of demes ...... 65 1.3.4. Population renewal rate ...... 66 1.4. Seasonal and diel activity patterns ...... 67 1.5. Thermoregulation ...... 70 1.5.1. Body temperature of active lizards ...... 70 1.5.2. Body temperature of inactive rock agamas ...... 72 1.5.3. Thermoregulatory behavior ...... 74 1.6. Diet and foraging behavior ...... 75 1.6.1. Diet ...... 75 1.6.2. Variability of food spectra ...... 77 1.6.3. Foraging behavior ...... 78 1.7. Reproduction ...... 79 1.7.1. Sexual maturity ...... 79 1.7.2. Reproductive phenology ...... 80 1.7.3. Physiological changes during reproductive season ...... 81 1.7.4. Fecundity ...... 82 1.7.5. Mating behavior...... 85 1.7.6. Female behavior during laying ...... 86 1.8. Social behavior and communication ...... 87 1.8.1. Territorial behavior ...... 87 1.8.2. Socio-sexual relations ...... 89 1.8.3. Communicative channels used in communication ...... 89 1.8.4. Signalling repertoire ...... 90 1.8.5. Signal behavior in socio-sexual interactions ...... 91 1.8.6. Species specifi city of push-ups movement...... 92 1.8.7. Functional aspects of communication in rock agamas ...... 93 1.9. Relationships between species and their place in biotic community ...... 96 1.9.1. Spatial relationships between sympatric species of rock agamas ...... 96 1.9.2. Interspecies hybridization ...... 97 1.9.3. Enemies and parasites ...... 99

Chapter 2. Caucasian rock agama: Distribution and geographic variation ...... 101 2.1. General outline ...... 101 2.2. Geographic range ...... 102 2.2.1. Geographic range of the species and history of its research ...... 102 2.2.2. Hypothesis on the development of the current ...... 107 Caucasian rock agama distribution range 2.3. Variation of characters ...... 108 2.4. Geographic variation ...... 109 2.4.1. Pholidosis ...... 112 2.4.2. Development of abdominal callous scalation and similar structures at precloacal position ...... 116 2.4.3. Coloration ...... 117 2.5. Population structure of the complex Paralaudakia caucasia – P. microlepis ...... 124 2.6. A possible evolutionary history of the compex Laudakia caucasia – L. microlepis ...... 126 2.7. Caucasian Rock Agama as a polytypic species ...... 127 Chapter 3. Caucasian Rock Agama: Growth and lifespan ...... 129 3.1. The study of growth rates in individually marked population of Caucasian rock agamas ...... 129 3.2. Age and size ...... 130 3.3. Interpopulation difference in Caucasian rock agama body size and a possible impact of growth rate ...... 134 3.4. Age-depended variability of body proportions and callous glands ...... 135 3.5. Individual age and population dynamics ...... 137

Chapter 4. Caucasian Rock Agama: Habitats and numbers ...... 139 4.1. Habitats ...... 139 4.1.1. Altitudinal distribution ...... 139 4.1.2. Vegetation ...... 140 4.1.3. Climatic conditions ...... 140 4.1.4. The signifi cance of shelters ...... 141 4.1.5. Plasticity in habitat preferences ...... 142 4.2. Numbers ...... 145

Chapter 5. Caucasian Rock Agama: Social organisation and demography ...... 148 5.1. Spatial structure of rock agama populations ...... 148 5.2. Formation of territorial structure ...... 150 5.2.1. Dynamics of space utilization within home range ...... 151 5.2.2. Long-term dynamics of territory use by the male owner ...... 154 5.3. Individual ontogenetic trajectories ...... 155 5.3.1. Ontogenetic trajectories of males ...... 157 5.3.2. Satellite males ...... 158 5.3.3. Ontogenetic trajectories of females ...... 160 5.4. Family groups ...... 163 5.5. Dynamics of numbers and sex and age structure ...... 165 5.5.1. Sex ratio ...... 165 5.5.2. Dynamics of sex and age structure in natural populations ...... 166 5.5.3. Dynamics of sex and age structure in the introduced population of Krasnovodsk ...... 168 5.6. Movement and dispersal ...... 171

Chapter 6. Caucasian Rock Agama: Reproduction ...... 174 6.1. Maturity ...... 174 6.2. Phenology of reproduction...... 175 6.3. Dynamics of testes function ...... 177 6.4. Dynamics of females gonad development ...... 178 6.5. Fertility...... 181 6.6. Laying behavior and incubation periods ...... 182

Chapter 7. Caucasian Rock Agama: Seasonal and diel activity ...... 184 7.1. Seasonal activity ...... 184 7.2. Hibernation ...... 186 7.3. Diel activity...... 188

Chapter 8. Caucasian Rock Agama: Food ...... 192 8.1. Diet...... 192 8.2. Diet variability ...... 192 8.3. Use of plant matter ...... 193 8.4. Other features of foraging behavior ...... 194 8.5. Foraging and activity rhythms ...... 195

Chapter 9. Caucasian Rock Agama: Social behavior and communication ...... 196 9.1. Repertoire of actions that may be regarded as carriers of visual information ..... 196 9.1.1. The EMA level 1 ...... 196 9.1.2. The second level of motor constructions integration ...... 199 9.1.3. The third level of the signal behavior integration ...... 201 9.1.4. The degeneracy of the signal repertoire ...... 201 9.2. The living space personalization and territorial behavior ...... 202 9.2.1. Spatial relations among mature males ...... 203 9.2.2. Spatial relations among females ...... 204 9.2.3. Spatial relations among juveniles ...... 205 9.3. Socio-sexual relations and corresponding signal behavior ...... 205 9.3.1. Joint roosting ...... 206 9.3.2. Greeting ceremonies (GC) ...... 206 9.3.3. GC’s and dynamics of female socio-sexual behavior ...... 207 9.3.4. Organisation ot dyadic GC-type interactions ...... 208 9.3.6. Use of the signal means in GC ...... 209 9.3.7. Copulation ...... 211 9.4. On the stereotype and species-specifi ty of Push-Up actions ...... 212 9.5. Some general comments ...... 213

Chapter 10. Caucasian Rock Agama: Injuries ...... 215

Chapter 11. Redbelly Rock Agama Paralaudakia erythrogaster Nikolsky, 1896 ...... 219 11.1. Range and habitats ...... 219 11.2. Some features of outer morphology ...... 221 11.3. Variation ...... 222 11.3.1. Geographic variation ...... 222 11.3.2. Aberrant specimens ...... 223 11.4. Population structure ...... 223 11.4.1. Sex and age structure ...... 223 11.4.2. Territorial structure ...... 224 11.4.3. Family groups ...... 225 11.5. Activity ...... 227 11.6. Reproduction ...... 228 11.7. Diet ...... 229 11.8. Molt ...... 229 Chapter 12. Relationships between closely related species and parapatric hybridization in genera Paralaudakia and Stellagama ...... 230 12.1. Relationships of Caucasian rock agama and redbelly agama in the sympatry zone ...... 230 12.1.1. Habitats, distribution and numbers of the co-existing species ...... 231 12.1.2. Relationship to the main environmental conditions and resources ...... 232 12.1.3. Sex and age structure and social organisation in the populations in contact ...... 233 12.1.4. Territorial relationships in the mixed agama populations ...... 234 12.1.5. Violation of the ethological isolation and the possibility of interbreeding between Caucasian rock agamas and redbelly agamas ...... 236 12.1.6. Lack of competitive exclusion ...... 239 12.2. Parapatric hybridisation in the P. caucasia – P. microlepis complex in the western Kopet Dag...... 239 12.2.1. Differentiation of populations by external morphology ...... 241 12.2.2. Phenotypic peculiarity of hybrid populations...... 250 12.2.3. Population genetic structure of the caucasia-triannulata-microlepis complex in southwestern Turkmenistan and the possible ways of its formation ...... 253 12.2.4. Ecological conditions in the intergradation zone and factors that govern gene fl ow ...... 255 12.2.5. Conclusion ...... 257 12.3. Differentiation and interrelations of two representatives of the Hardun Stellagama stellio complex in Israel ...... 258 12.3.1. Situation in the Middle East ...... 260 12.3.2. Morphological features of the populations studied ...... 261 Middle East Stellion ...... 261 Population of Qiryat Shemona ...... 261 Population of Jerusalem ...... 263 Short-toed Rock Agama ...... 264 12.3.3. Habitats and Number ...... 266 Middle East Stellion ...... 266 Short-toed Rock Agama ...... 266 12.3.4. Population structure and social behavior ...... 267 Middle East Stellion ...... 267 Short-toed Rock Agama ...... 267 12.3.5. Signal behavior ...... 268 12.3.6. On the possibility of intergradation between the two representatives of the S. stellio complex in the secondary contact zone ...... 271

References ...... 274

Index of lizards’ scientifi c names ...... 287

Authors’ index ...... 288 Chapter 1. General information on Eurasian rock agamas

The genus Laudakia sensu lato comprises 19 or 20 species (according to Baig et al., 2012 and Hoser, 2012, respectively). However, we will not mention L. dayana, L. papenfussi and L. wui so as not to replicate potentially erroneous information. Our review is based on the materials on the 16 relatively well studied forms of the species status as understood by Hoser (2012) (Table 1.1). Rock agamas are a young group in the evolutionary respect. Agamids appeared in Africa and Eurasia ca. 190 Myr ago (Evans et al., 2002). Laudakia sensu lato began to diverge as late as 24 Myr ago, with the age of the youngest sister species being estimated at ca. 18 Myr (Fig. 1.1).

FIG. 1.1. Revision of the genus Laudakia s.l., based on comparative mtDNA. Node ages are shown in Mya. After Melville et al., 2009 modifi ed by Baig et al., 2012.

The distribution area of the genus Laudakia sensu lato embraces the central part of the Alpine- Himalayan belt. This is a blanketed folded terrain formed during the Caenozoic. In the west the distribution area of these lizards coincides with the mountain systems passing along the Adriatic Sea across the Dinaric Alps and Hellenic mountains and the Crete crossing the Aegean Sea. Fur- ther to the east these mountain ranges continue into the Taurus in the south of Anatolia and the Zagros mountains in the south-west of Iran. Two other branches of the mountain ranges are repre- sented by the Greater Caucasus and the Pontic mountains of the north Anatolia transiting into the Lesser Caucasus and Alborz Mountains in the north of Iran. Still further to the east the latter join the Kopet Dag to form the Turkmenistan-Khorasan Mountain Range. The easternmost part of the distribution area of rock agamas is confi ned to the mountain systems of Altay in the north and the Baluchistan chains of Pakistan and the Himalayas (Fig. 1.2, 12.12). 30 E.N. Panov L. Yu Zykova Rock Agamas of Eurasia

FIG. 1.2. Range of rock agamas Laudakia s. l. After Rastegar-Pouyani and Nilson, 2002.

Table 1.1. List of taxa of the species level within the genus Laudakia sensu lato

Genus Scientifi c names Common names Number of Range subspecies Stellagama S. stellio (Linnaeus, Hardun, Hardim, Star 5–6 Eastern spurs of Balkhans, 1758) Lizard, Starred Agama, islands of Aegean Sea, Sling-tailed Agama, Cyprus, Asia Minor, Near Roughtail Rock Agama East, northeastern Africa Laudakia1 L. agrorensis Agror Agama Southern Hindu Kush, (Stoliczka, 1872) western Himalayas L. fusca (Blanford, Yellow-headed Agama – Hindu Kush 1876)2 L. melanura (Blyth, Black Agama 2 Southeastern and eastern 1854) parts of the Iranian Plateau L. nupta (De Filippi, Large-scaled Rock 2 The Zagros Mountains, 1843) Agama southern parts of the Iranian Plateau L. nuristanica Leviton’s Rock Agama – Hindu Kush (Anderson et Leviton, 1969) L. pakistanica (Baig, Pakistan Rock Agama 2 Western Himalayas 1989) L. sacra (Smith, 1935) Sacred Rock Agama – Southeastern Tibet L. tuberculata Kashmir Rock Agama Hindu Kush and The (Hardwicke et Gray, Himalayas (eastern 1827) Afghanistan, northwestern Pakistan, Kashmir, parts of Uttar Pradesh, India, southwestern Nepal. Chapter 1. General information on Eurasian rock agamas 31 Table 1.1. Paralaudakia P. caucasia (Eichwald, Caucasian 1 (2?) Caucasus and South 1831) Rock Agama Caucasus, Alborz, Kopet Dag, Iranian Plateau (mainly its northern parts)

P. erythrogaster Redbelly Rock Agama 1 (2?) Eastern Kopet Dag, (Nikolsky, 1896) northwestern Hindu Kush

P. badakhshana Badakhshan Rock – Hindu Kush (Anderson et Leviton, Agama 1969) 3

P. bochariensis Bukhara Rock Agama – Kugitangtau, Pamiro-Alay (Nikolsky, 1897) 3

P. himalayana Himalayan Rock – Kugitangtau, Pamiro- (Steindachner, 1869) 3 Agama Alay, southwestern Tien Shan, Hindu Kush, western Himalayas

P. lehmanni (Nikolsky, Turkestan Rock Agama – Kugitangtau, Pamiro- 1896) Alay, western Tien Shan

P. microlepis Small-scaled Rock – Iranian Plateau (mainly its (Blanford, 1894) Agama southern parts)

P. stoliczkana Mongolian Rock 2 Eastern Tien Shan, (Blanford, 1875) Agama Mongolian Altay, Gobi- Altay

Underlined are the names of species with restricted ranges of the relict type. 1 Forms dayana, papenfussi и wui regarded by us as doubtful are not mentioned. 2 Cheatsazan et al. (2008) suggest: ‘Based on the co-occurrence of these subspecies in Kuh-e-Bang and morphological clues for their reproductive isolation at this site, they are recognised as full species. But Baig et al. (2012) consider it as subspecies of L. nupta. They wrote: ‘Morphological differences are clearly not distinct enough to recognize them as full species like Cheatsazan et al. (2008) did, but the small differences recognized by Rastegar-Pouyani and Nilson (2002) could indicate an initiating speciation’. 3 These three forms are treated by Baig et al., 2012 as belonging to the superspecies P. himalayana.

A relatively young evolutionary age of rock agamas is also indicated by the fact that the distribution of most species is allopatric (Fig. 1.3) and the species themselves are usually monotypic. 32 E.N. Panov L. Yu Zykova Rock Agamas of Eurasia

FIG. 1.3. Tentative scheme of the rock agamas genera Stellagama, Paralaudakia and Laudakia s. str. distribution. Original. Chapter 1. General information on Eurasian rock agamas 33 1.1. Morphological features

1.1.1. General characteristic

Eurasian rock agamas are medium-sized lizards. The body mass of the mature males varies in different species between 60–140 g and that of females, between 30–130 g. Smaller species are few. General appearance and body proportions are rather uniform across all species (Fig. 1.4). Rock agamas have fl at bodies and a triangular head, making up ca. 35% of the body length. Legs are not long, forelegs make up some 50% of body length, while hind legs are longer: 66–76% in the males of different species and 64–70% in the females (Ananjeva et al., 1990). The usual locomotion type is running and the main allure is fast trot. Rock agamas may run very fast. The maximum speed of the Hardun, for instance, makes up 2.3–2.7 m/s, positively correlating with the body mass and body temperature (Hertz et al., 1983; Van Damme and Vanhooydonck, 2001). Eurasian rock agamas are medium-sized lizards. Smaller species are few. General appear- ance and body proportions are rather uniform across all species (Fig. 1.4). The body mass of the mature males varies in different species between 60–140 g and that of females, between 30–130 g. Rock agamas have fl at bodies and a triangular head, making up ca. 35% of the body length. Legs are not long, forelegs make up some 50% of body length, while hind legs are longer (66–76% in the males of different species and 64–70% body length in the females; (Ananjeva et al., 1990). Leg thickness and toe length also vary between species. Toes are comparatively long, with strong claws. In hind legs the fourth toe is much longer than the others. Tail is somewhat fl attened at its base, towards the tip it has a round profi le. In most species the tail is much longer than the body and the head taken together (1.3–2.5 times longer in different species). It is relatively short (<110% of the body with the head) only in a few species. These proportions vary with age and sex and show geographic varia- tion across all the species for which suffi cient morphological data are available (Table 1.2). The cranium of rock agamas is fl at and the surface of frontal and parietal bones is nearly smooth. Eurasian rock agamas differ from the closely related Trapelus and Phrynocephalus aga- mas by the details of maxillae and dental bones (Ananjeva, 1992). The nostrils, cut on the side surface of the infl ated naricorn, are invisible from above. Their openings may be round (S. stellio subsp., L. nuristanica, L. melanura, L. agrorensis, L. tuberculata) or oval (L. sacra, P. hima- layana, P. bochariensis), being elongated along the cranial-caudal axis (Ananjeva et al., 1990). Some species have a parietal foramen in the occipital scutum. The eyes are covered with mov- able lids and the iris is round. The eye sockets are depressed and covered from above by a lateral projection of the supraorbital tuber, so that the eyes are almost invisible from the above. The tym- panum is located more or less superfi cially. Behind tympanum on the sides skin's fold is of neck a well-defi ned. Its bulge is covered by large cone-shaped scales, with the spikes on them being developed in varying degrees in different species. The skin of the lower part of the head forms the so-called gular fold (Plate IX). When an animal is agitated, the skin of the ‘chin’ is lowered down by a hyoid apparatus forming a small bulge the size of which varies in different species. At least in one form [S. stellio brachydactyla] this bulge is shaped similarly to the typical gular sac of some Trapelus species (in particular, the Steppe Agama T. sanguinolentus). 34 E.N. Panov L. Yu Zykova Rock Agamas of Eurasia

FIG. 1.4. Variants of external morphology in some representatives of the genus Paralaudakia. a —

Himalayan Rock Agama P. himalayana, а1 — its head; b — Turkestan Rock Agama P. lehmanni; c — Bukhara Agama P. bochariensis, c1 — its head; d — head of the Mongolian Rock Agama L. stoliczkana. After Bedryaga, 1907. Chapter 1. General information on Eurasian rock agamas 35 ad. Weight Weight females max. (g), Table 1.2. Table ad. (mm), females SVL max. SVL Weight Weight max. (g), males ad. (mm), males ad. SVL max. SVL s. l. species. – 140 88 138 84 3–10 150 128 140 118 Laudakia juv after rst winter rst Weight (g) Weight fi rst – 57 – 138 70 135 58 ( 49 ) Molt 46–66 35–65 after fi SVL (mm), SVL – 2–7 ( 2.4 ) 1.9–3.6 (g) shortly Egg weight after hatching ( 43.3 ) 35–37 38–46 hatching SVL (mm), SVL shortly after – 32 – – – 120 – 112 – . 2 (g) Egg ( 1.8 ) weight 0 . 8–1 0.3–3.0 Size of eggs and indivudials of different ages in some Size of eggs and indivudials different – – 35 11 15 Egg 9–12 (mm) width (13.3) 11–15 12–14 ( 13.5 ) 2 19 (mm) ( 19.6 ) 24–27 length 19–26 15–19 18–19 21–23 19–25 9–1416–22 – 10–12 – 45 35–39 3,3 – – 63–70 8,5 – 108 154 60 143 148 96 129 30 19–21 ( 22.7 )* ( 21 . 8 ) 2 1 According to different sources. According to different stellio ssp. caucasia Species Egg tuberculata himalayanа lehmanni erythrogaster 2 * Means. 36 E.N. Panov L. Yu Zykova Rock Agamas of Eurasia The dental system is usually well differen- tiated. Usually two or three teeth are located on premaxilla, while 12–15 (rarely up to 18) triangular acrodont teeth are positioned on maxilla and the dental bone. Each side of both the maxilla and the mandible bears an ‘incisor’, a ‘fang’ and 12–15 broader ‘mo- lars’, named by analogy with the heterodont teeth of mammals (Ananjeva, 1992; Fig. 1.5). Rock agamas chew hard food items by mov- ing their jaws. A large agama can bite quite hard. A lizard imprudently offered a fi nger, holds on to it with an iron grip. The only way to get rid of it is to stand completely still for several minutes. The tongue is thick and fl eshy, not bifurcated. Skin receptors are goblet-shaped and sub- merged. The signal is perceived by a thin pa- pilla (‘hair’) which goes from the body of the skin receptor and protrudes through a micro- FIG. 1.5. Scull (from above) and lower jaw of the Caucasian Rock Agama P. саucasia. After scopic opening in the scale. In all species stud- Orlova, 1981. ied the number of receptors per scale is usu- ally greater on the dorsal side (up to 2–4 vs. solitary receptors on ventral scales). However, due to the larger number of small scales on the ventral side the total number of receptors there is1.2–1.9-fold greater than on the dorsal side (Ananjeva et al., 2000). In P. caucasia and P. lehmanii the highest density of skin receptors is recorded on the jaws, up to 6–9 on each scale. In P. erythrogaster the papillae of these recep- tors form structures similar to mammals’ eye- lashes around the eyes (Ananjeva et al., 2000). Skin receptors are very similar in the Himalay- an Agama and the Bukhara Rock Agama, dif- fering from those in all the other Eurasian rock agamas studied (Ananjeva, 1992; Ananjeva et al., 2000). Old receptors are lost during each Molt, and FIG. 1.6. Bifurcation of the tail distal new ones develop. The function of skin recep- portion during its regeneration in Caucasian tors in rock agamas remains obscure. It is as- Rock Agama. Bottom — radiograph of this sumed that they are mechano- or thermorecep- individual. After Ananjeva and Danov, 1991. tors (Ananjeva, 1992; Ananjeva et al., 1991; Chapter 1. General information on Eurasian rock agamas 37 Matveyeva and Ananjeva, 1995). However, they might also function as chemoreceptors (Panov and Zykova, 1999). A characteristic feature of rock agamas is their ability for tail autotomy (the break oc- cur between the vertebrae) and regeneration of the lost tip, which may bifurcate (Fig. 1.6). In some species (P. caucasia, P. stoliczkana, L. agrorensis, L. nupta L. tuberculata) up to 80% of individuals have autotomised tails. These species can regenerate their tails, but this ability is most pronounced in some species of the ‘himalayana’ group (P. himalayana, P. bochariensis), in which the regenerated portion may reach 90 mm. On the other hand, in the Turkestan Rock Agamas P. lehmanni the regeneration ability is practically lacking (Ananjeva, 1992). The fl attened body, the spiky scales with caudally directed spikes and the ability for au- totomy are considered as adaptations for using narrow cracks in rocky surfaces as shelters. Indeed, a rock agama cannot be pulled from such a crack by the tail. In such situations these reptiles invariably resort to autotomy, even though a quite signifi cant pulling force is often necessary to break the caudal part of the spine.

1.1.2. Size and proportions

Rock agamas are typical K-strategists, which means, in particular, that they live for a long time in the wild: defi nitely up to 7 years and up to 12–13 years according to some data (Zykova and Panov, 1991). In Stellagama stellio SVL ranged between 90.05–133.14 mm (mean: 109.58 ± 10.26) in males and 86.24–130.43 mm (mean: 105.83 ± 10.68) in fe- males. The age ranged between 2–9 (mean: 5.34 ± 1.63) in females and 3–10 years (mean: 5.72 ± 1.82) in males. No signifi cant difference in terms of age and SVL between sexes was found in this species (Ergül et al., 2014). Intersexual differences in body size were male-biased (SDI= – 0.03) but this relation was not statistically signifi cant. A signifi cant difference between the lowland (below 800 m) and mountain (above 800 m) populations was found in respect of SVL, with mountain individuals being larger than the lowland. However, the age difference between lowland and mountain populations appears to be not signifi cant. A signifi cant positive correlation was found between the age and SVL both in males and females. Individuals reached maturity between 2 and 3 years (Ergül1 et al., 2014). Rock agamas grow each year until their death. This explains the fact that the body size varies broadly in each population. The length of the body with the head (SVL) of an adult rock agama may exceed 300% of this value for a newly hatched individual from the same population. Actually, lizards younger than 1.5 years and those that have survived more than three winters, can be considered as two different life forms. They have very different foraging and spatial strategies, avoid predators differently and exhibit different social behavior. In differ- ent populations of the same species with the same starting body size of hatchlings, growth rate may differ. Therefore, the body size of the lizards of maximum age in such populations is also signifi cantly. It is these maximum size values rather than the means for samples of males or females that should be considered as the characteristic features of a local population, a geographic race or a species (Zykova and Panov, 1991). 38 E.N. Panov L. Yu Zykova Rock Agamas of Eurasia The varying growth rate, the fi xed maximum attainable size of adults and a similar size of hatchlings are probably stable population-specifi c characteristics. In species with large and small maximum size of adults egg size is very similar (Table 1.2). The same can be said of lizards at early stages of post-hatching development. Unfortunately, the scarcity of the data on early ontogenetic stages precludes statistical comparisons of the data summarised in Table 1.2. The size of closely related species is sometimes comparable (P. himalayana – P. bo- chariensis – P. badakhshana). However, this is not always so (cf. data on P. himalayana and P. stoliczkana). Therefore, the maximum size can hardly be used for verifying genealogical relationships between species. There may be distinct differences in the general size even when two forms exchange genes in the zone of parapatry, e.g. S. stellio braсhydactyla vs. ‘Near East rock agama’ S. stellio ssp. (Panov and Zykova, 1997). The degree of size variation between species from the genera Laudakia, Paralaudakia and Stellagama can be assessed using the data in Table 1.3. This table also gives the values of ratio ‘tail length / SVL’, which may be used as a morphological character for taxonomic purposes. Table 1.3. Maximum size and proportion tail length/SVL in some rock agama species

Taxon SVL max (mm) Tail length: SVL Sources Males Females Males Females S. stellio brachydactyla 148 141 1.2 1.2 Panov and Zykova,1997 S. stellio subsp. 120 112 1.5 1.4 Panov and Zykova,1997 L. agrorensis 92 90 2.31 Boulenger, 1885 Anderson and Leviton, 1969 L. melanura 142 130 2.3–2.71 Minton, 1966 2.1 1.9 Anderson, 1999 L. nupta nupta 151 148 1.8–2.21 Minton, 1966 L. nupta fusca 162 140 1.81 Minton, 1966 L. nuristanica 131 932 2.0 1,9 Anderson and Leviton, 1969 L. pakistanica 150, 156 124 2.1–2.4 2.1–2.3 Baig, Bohme, 1996 L. tuberculata 140 138 2.0 1,9 Waltner, 1991 L. sacra 147 130 1.6 1.5 Ananjeva et al., 1990 P. badakhshana 823 803 1.7 1.7 Anderson and Leviton, 1969 P. bochariensis 120 95 1.8–2.2 Ananjeva et al., 1981 P. caucasia 139–1744 135–1584 1.4 1.3 Panov and Zykova,1995 ‘triannulata’ 159 158 1.5 1.5 Ananjeva and Ataev , 1984 P. erythrogaster 150 145 1.1 1.0 Panov and Zykova,1996 P. himalayana 853 783 1.9–2.0 1.6–1.7 Yakovleva, 1964 108 96 1.5 1.4 Ataev, 1985 – – 1.7–2.0 1.4–1.6 Ananjeva et al., 1981 P. lehmanni 143 140 1.5 1.4 Ataev, 1985 P. microlepis 133 149 1.135 – Anderson, 1999 P. stoliczkana stoliczkana 1441 1.61 Ananjeva, 1997 P. stoliczkana altaica 1501 1.4 –1.61 Ananjeva, 1997

1 Both sexes pooled. 2 On examination of single specimens (eggs in oviducts). Chapter 1. General information on Eurasian rock agamas 39 Sex-related variation is apparent not only in the general size but also in the relative tail length1. Males usually have longer tails than females; however, this may be true for some popu- lations of a given species but not for the others (Panov and Zykova, 1995). The yearlings of the Caucasian Rock Agama have longer tails than the adults (Panov and Zykova, 1995). The same is true of the Kashmir Rock Agama L. tuberculata, in which the tail growth rate declines with sexual maturity (in males to a lesser degree than in females). This difference is not statistically signifi cant, however, so that the adult males and females have similar ‘tail : SVL’ ratio. Interestingly, in this species tail grows faster at low altitudes as compared with high-al- titude populations within the same region, so that the former have relatively longer tails. Besides, toes are longer in low-altitude Kashmir Rock Agama populations, and in both low and high-altitude populations the fourth hindleg toe is signifi cantly longer in males than in females of the same age (Waltner, 1991). The relative size and and shape of the head is also sex-biased: it is longer and higher in males. Head : body ratio (expressed as percentage) in males and females varies in different populations of S. stellio between 31–33 and 29–30, respectively; in P. caucasia, between 24–27 and 24–25; and in four species of the so-called ‘himalayana’ group, between 26–28 and 25–26 (Daan, 1967; Ananjeva et al., 1990; Panov and Zykova, 1995). In the Caucasian Rock Agama the relative growth rate of the head decreases with age: in yearlings it makes up 27–30% body length (Panov and Zykova, 1995). A faster growth of the head with increasing age in males as compared to females has been reported in L. tuberculata (Waltner, 1991). Daan (1967) suggested that a similar pat- tern exists in S. stellio. Species of rock agamas sometimes differ by the skull height, which is estimates as head breadth : head height ratio. The difference is usually small (1.7–2.0 within the genus) and not statistically signifi cant. P. erythrogaster, P. lehmanni and L. sacra are ‘high-headed’ species (Ananjeva et al., 1990). However, this viewpoint needs to be clarifi ed. In one Caucasian rock agama population the yearlings had signifi cantly higher heads than the adults. Adult males tend to have higher values of this parameter than adult females.

1.1.3. Pholidosis

Scales signifi cantly differ in different parts of of the body. Their arrangement is in general species-specifi c, even though most characters vary broadly within species. The most impor- tant species-specifi c character is the overall number of scales on the surface of an individual. A proxy for this character is the number of elements on the line drawn around the middle part of the body. The mean values vary between 87–92 in the Redbelly Rock Agama L. erythro-

1A series of recent publications on sexual dimorphism in different species of rock agamas (Cheatsazan et al., 2006, Cheatsazan et al., 2008, Heidari et al., 2010, Aghili et al., 2011) is beneath criticism. Sample sizes of males and females are either too small (the minimum of 9–12 individuals) or, on the contrary, infl ated by including the individuals from younger age groups. The failure to reveal statistically signifi cant difference between the size characters of males and females is apparently due to these drawbacks in two cases out of four. 3 Possibly on immature individuals. 4 For different populations (see Chapters 2 and 3). 5 On examination of a single specimen, tail may be broken (see Boulenger, 1885: 366). 40 E.N. Panov L. Yu Zykova Rock Agamas of Eurasia 2 – – – + + + crest Nuchal Table 1.4. Table 11 1 ) 1.0 ) ( 13 ± ( 13 ± 13–14 12–17 12–13 Lower labials 01 ?? ± 1 ) Upper 12–15 labials ( 14 ± 1 ), ( 12 ± 2.1 ) tail 18–28 12–18 ( 15 13–22 ? ? 18–28 Scales number ( 21 ± 5 ) ( 30 ± 2 ) around the 3 28–33 in of 2(1) 12–14 10 –14 2(3) 12–13 ? ? As in the Segment s starts with 2–3 whorls may be 4 in tail segment occasionally terminal end inconsistent, terminal part 3 whorls, but and gradually nominate form changes into 5, sometimes 6 in Whorls number Only little away segment consists from pelvic, each on ++ anks Spiny scales fl band +++ ++ Lateral extensions Sometimes of vertebral 1 ––– – – +++ ++ +–– +–– + band jagged edge of vertebral Posterior vertically scales are Some features of pholidosis in rock agamas band spines spines spines spined keeled Keeled Slightly vertebral Scales of Distinctly mucronate with strong keeled with keeled with 3 the 5–7 Strongly 5)+1 band most 1+(3– dorsal across (cover Scales parts of number surface) vertebral 2 ) ( 119 Scales around 97–127 116–147 106–130 8–12120–130 Distinctly 6–11 midbody max. 180 13–16 Strongly ( 132 , 137 ) 75–106 ( 92 ) 15–18 1234567891 L. nupta fusca S . stellio brachydactyla L. nupta S. stellio subsp. Taxon L. agrorensis L. melanura Chapter 1. General information on Eurasian rock agamas 41 2 – – – – – – – – mentary Table 1.4. Table 11 1.0 ) 8–12 9–10 ( 11 ± 10–12 01 9–11 9–11 8–12 9–10 11–13 10–16 10–16 12–15 2–15 13–15 13–15 ( 10 ± 1 ) ( 10 ±0.4 ) ( 12 ± 0.8 ) in ± 4 ) ( 23 ) ( 20 ), 31–36 11–13 11–13 Rudi- 43–48 30–32 18–21 25–30 ( 46 ± 2 ) (25 ± 2) Pakistan ( 27 ± 2 ) ( 31± 1.0 ) 28–46 ( 36 4 4 3 26–32 10–13 10–13 3 20–26 3 22–27 2 24–29 2 into 4 4, but 3 on 4, but 3 on ventral side ventral side starts with 3, the tail changes but from mid of only at few sectors Sometimes + –+?++ ––– ––– ––++ ––++ – + +++ – +–+ + +++ +++ equal keeled keeled spined keeled spined almost is very in size, Smooth Slightly Slightly strongly different different spines in variable) enlarged, enlarged, distinctly to weakly Distinctly (character Smooth to keeled and keeled with populations 3 3 3 8 Keeled – 7–8 Keeled ( 12 ) 6–7 5–10 7–16 ( 7 , 9 ) ( 6 – 7 ) 10–12 11–16 171 ) ( 171 ) ( 240 ) ( 190 ) ( 105 ) 98–112 80–118 ( 87–94) 112–132 6–8 134–221 230–247 230–248 10–12 Strongly 167–208 125–150 146– 178 ( 154, 157, ( 149 – 133 ) ’ 1234567891 L. tuberculata L. pakistanica L. sacra P. badakshana P. L. nuristanica ‘ triannulata P. bochariensis P. P. erythrogaster P. P. caucasia P.