Rock Agamas of Eurasia = Горные агамы Евразии

A.N. Severtsov Institute of Ecology and Evolution
Russian Academy of Sciences 
 
Rock Agamas of Eurasia
by
E.N. Panov and L.Yu. Zykova
KMK Scientifi
 c Press
 Moscow 2016 

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 компактного таксона ящериц (около 20 видов), обитающих  в  пересеченных аридных и высокогорных 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 номенклатуре 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 коммуникативного 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 взрослых 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
ISBN 978-5-9907838-6-7
© Е.Н. Панов, Л.Ю.Зыкова, 2016
© 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

AUTHORS’ PREFACE
Objectives, goals and background
Rock agamas are one of the most characteristic components of the fauna of terrestrial vertebrates 
in rugged arid and high-altitude landscapes of the Old World. Partly because of this they have attracted close attention of herpetologists. At the same time, by the standards of modern zoological 
research the up-to-date state of knowledge of rock agamas leaves much to be desired.
Rock agamas might serve as excellent model objects in studies of ecology, behavior, adaptive radiation and microevolution of squamate reptiles. This is due to several features of their 
biology such as conspicuousness associated with a rather large size and a strict diurnality, a 
high population density in many species and some others.
However, instead of comprehensively studying the mode of life of various rock agamas 
or the interactions between co-occurring species, herpetologists seem to confi
 ne themselves 
to the nomenclature issues. This is often expressed in revisions of species and subspecies 
names, which may drag on for decades. These purely formal procedures, which sometimes 
resemble the setting out of cards in a game of patience, propagate synonyms and plunge 
nomenclature into chaos (some examples will be given in the Introduction). Such exercises 
based on museum collections add nothing new to our knowledge of rock agamas and their 
biological specifi
 city as compared to other squamate reptiles. 
Serious studies dealing with the mode of life, autecology, population ecology and behavior 
of rock agamas are virtually absent. Khisroon et al. (2012) remarked: ‘…no extensive studies 
on the reptiles have ever been conducted in the district Chitral but as per baseline studies of 
Chitral Gol National Park, 14 species of reptiles have so far been reported mainly based on 
derived information’. There are ten species of rock agamas in that region and none of them has 
been extensively studied in respect of fi
 eld biology. The same state of things is characteristic 
of other regions and, unfortunately, applies to the cited study too. It is entitled ‘Systematics, 
ecology and distribution of Caucasian Rock Agama, Paralaudakia caucasia in district Chitrak, 
Khyber Pakhtunkhwa province, Pakistan’ (Khisroon et al., 2012), but actually the utterly scarce 
ecological information in it is mostly derived from the faunistic reviews of 1960–1990s.
Lack of progress in behavioral ecology and ethology of rock agamas is ‘compensated for’ 
by attempts to substitute fi
 eld research with laboratory experiments. However, the results 
obtained in the laboratory are often misleading and the hypothesis based on them, which are 
supposed to refl
 ect what happens in the nature, are far-fetched. Examples of such ‘theoretical’ 
speculations can be found below.
Working on the fi
 rst edition of this book, we managed to fi
 nd only one consistently systematic 
and complex study of almost all life strategy aspects of rock agamas in the nature. This is the study 
by Robert Waltner (1991) presenting comparative analysis of the biology of two populations of 
the Kashmir Rock Agama occupying different altitudinal belts in the Western Himalaya. 
Waltner worked in the fi
 eld for two years from April to December, that is, during the entire 
period of the lizards’ activity. By marking numerous individuals from both local populations, 

Authors preface
he obtained detailed information on the demographic population structure, the sex ratio, the 
survival rates of lizards from different age groups and the population renewal rates.
Waltner revealed differences in the growth dynamics of males and females, concluding 
that individual pholidosis characters were constant throughout the lifetime of a lizard. He 
carefully studied seasonal and daily activity of lizards from various sex and age groups as 
well as the role of thermoregulation mechanisms in maintaining the species existence under 
different climatic conditions at high and low altitudes.
Waltner studied all aspects of the reproductive phenology, the physiology of gonad maturation, noting differences in fertility of females of different age. He paid much attention to 
the behavior of rock agamas, in particular, the individual variability and seasonal dynamics 
of feeding behavior. His study contains valuable observations of the social behavior and the 
description of both visual and olfactory communication signals. 
In our opinion, the work by Waltner is a paragon of biological studies of squamate reptiles. 
Anyone willing to make a substantial contribution to herpetology should follow the example 
set out by this researcher.
Another study of rock agamas corresponding to the desirable standards of reptiles research 
in the nature is that by Loman et al. (2013). It deals with the territorial behavior of the Hardun 
Stellagama stellio cypriaca. Similarly to Waltner (1991), Loman et al. (2013) observed marked 
lizards (altogether 74 individuals from various age-sex groups). The results obtained in that 
study will be discussed in sections 1.8 and 12.3. Unfortunately, the work by Loman and colleagues spanned a short time, only two sessions (5 and 8 days) in the spring of one year.
Our study of the Caucasian Rock Agama followed the same principles as those having been realized in Waltner’s research (1991). Our work was started before Waltner’s study, carried out and 
continued for a longer time (1975–1985). Its emphasis was also somewhat different from that in 
Waltner’s study. We concentrated on the analysis of social behavior as a factor integrating the local population into a certain systemic entity. Our primary interest was to examine social structure 
of deme in its continual transformations over successive years. Or, in other words, to understand 
course of events as a process of changes in the behavior and social roles of older individuals, as 
well as of annually arriving offspring being recruited in contingent of the local population.
To solve this task, we had to perform a detailed analysis of communication means. Their 
description followed the principles developed during long-term studies of signal behavior in 
birds (see, e.g., Panov, 1978/2009; Panov et al., 2010; Panov, 2015). The approach elaborated 
for birds appeared to be works equally well in the case of signal behavior in lizards (Panov 
and Zykova, 1997, 1999; Panov et al., 2004). 
Our study also encompassed such ‘traditional’ topics as the analysis of individual, between 
age and sex and geographical variation. It was based on the descriptions of 725 living lizards 
and some data obtained from museum collections.
The pivotal place in our research belongs to ethology. We attempted to trace ontogenetic 
trajectories of individuals, to understand the structure of communicative process and the role 
of competition and behavioral isolation mechanisms in the areas where closely related species of rock agamas co-occur. To demonstrate a specifi
 ty of our approach against the background of the current state of the reptile ethology, it seems useful to examine at fi
 rst what was 
done to date in a fi
 eld of lizards communicative and social behavior.

E.N. Panov   L. Yu Zykova    Rock Agamas of Eurasia
State of our knowledge of communicative behavior in lizards 
Lizards have recently been attracting much attention in the context of sexual selection. The 
very discussions of this topic would have been pointless without the comprehensive and valid 
data on lizard behavior. Advocates of sexual selection constantly refer to the communicative 
and social behavior in lizards in a way that makes the uninitiated believe that this issue is 
thoroughly studied. In fact, this is not so. Therefore, many of the recent evolutionary generalizations are, in our opinion, at best unconvincing and often downright misleading.
Charles Carpenter, an eminent researcher of lizard behavior wrote thirty years ago1: ‘This 
is an inventory of species for which a display-action-pattern graph or a similar graphical 
representation or description has been noted in the literature. Some of these references are 
marginal, but can lead the investigator to what little is known about the display-action-pattern 
of a species... It is quite evident that we have only begun to record these display-action-patterns which I feel certain are present in the great majority (if not all) of the species of lizards 
in the Iguanidae, Agamidae, and Chameleonidae’ (Carpenter, 1986: 1). 
The fi
 rst page of Carpenter’s review has a picture of a lizard performing characteristic 
Push-Up and Head-Bob displays. Of all the elements of lizard behavior, these movements 
are the most conspicuous and easy to observe. So, instead of dealing with the entire range of 
lizard communicative behavior, ethologists often focus solely on this narrow topic. 
Thus, a quarter of a century ago the state of our knowledge of lizard ethology was summarized as follows: ‘In fact, most of the research on the Push-Up display has focused on the 
physical structure of the male lizard display in captivity. [fi
 ve works published between 1971 
and 1986 are cited] Differences among individual males in other aspects of the Push-Up display 
and among females have not been studied. The little work that has been done previously on the 
Push-Up display of S graciosus consists primarily of general descriptions of the Head-Bob pattern of adult male lizards [still more three studies are mentioned]. I was interested in studying 
some of the other components of the Push-Up display as well as the Head-Bob pattern, as well 
as looking at the behavior of both males and females in the fi
 eld’ (Martins, 1991: 404).
Thus, one can see that the so-called Push-Up and Head-Bob displays are considered as the 
major component of signal behavior both in case of confrontations between males and interactions between males and females. In this way, troublesome and time-consuming fi
 eldwork 
is avoided and the behavioral elements are observed in the comfort of the laboratories. Such 
studies have been sprouting like mushrooms after a summer rain (see, e.g., Ord et al., 2002; 
Ord, Evans, 2003; Peters and Evans, 2003; Peters and Ord, 2003; Van Dyk and Evans, 2008).
In a review of lizard behavior being published eleven years later, we fi
 nd: ‘Agamid and 
iguanid lizards have an extraordinary diversity of visual signals. Social communication in these 
animals is conducted primarily through discrete and sequentially predictable motor patterns 
centered on a core display of push-ups and head-nods. These visual signals are important in 
territorial acquisition/defence and mate selection. Signal complexity, or the repertoire of components used in displays, varies across species and can be quantifi
 ed by the number of ‘modifi
 ers’ accompanying a display. Modifi
 ers may include: dewlap extensions/throat engorging, tail 
1 A thorough critical analysis of these views is given in the book ‘Sexual Selection: Theory or Myth’ (Panov, 
2014: section 4.2).