Asian Agamid Research Articles

Testing the factors on the evolution of movement-based visual signal complexity in an Asian agamid lizard

Testing the factors on the evolution of movement-based visual signal complexity in an Asian agamid lizard

Tail display is regulated by anaerobic metabolism in an Asian agamid lizard.

Understanding the mechanism underlying signal variation is an important goal in the study of animal communication. Several potential causes have been proposed for signal variation, including environmental noise (e.g. wind, sound), energy limitation, and predation risk, among others, but the physiological control of many signals are often unclear. Here, we examined the correlation between tail display signal variation and energy metabolic activity using an Asian agamid lizard Phrynocephalus vlangalii. Individual tail display signals were observed in the field, and blood lactate concentration as well as 2 energy metabolic enzymes was assayed. Our results showed that average tail coil speed was positively associated with blood lactate concentration, while tail coil duration was negatively associated with LDH activity. We also found that average tail lash speed was positively associated with blood lactate concentration, suggesting that the tail display behavior of P. vlangalii was regulated by anaerobic metabolism. Furthermore, the correlation between tail display behavior and energy metabolism was not sex-dependent. Taken together, our research provides insight into the physiological mechanisms underlying tail display variation in lizards, and suggests that tail display variation likely transmits important information on individual body condition and resource holding potential.

A new agamid lizard in mid-Cretaceous amber from northern Myanmar

The first amber-embedded fossil representing the lizard family Agamidae, Protodraco monocoli gen. et sp. nov., is described in burmite of the lowermost Cenomanian (ca. 99 Ma; mid-Cretaceous) from northern Myanmar. It is among both the oldest known amber lizards and the oldest fossils of the family. The fossil is a well preserved left hind foot with shank, morphologically similar to basal taxa of modern Southeast Asian agamids. Because of the sparse Cretaceous fossil record it could provide a calibration point for divergence-time analyses and contradicts views that agamids colonized SE Asia during the Paleogene.

Dragons in neglect: Taxonomic revision of the Sulawesi sailfin lizards of the genus Hydrosaurus Kaup, 1828 (Squamata, Agamidae).

Currently three different species are recognized within the Southeast Asian agamid genus Hydrosaurus: H. amboinensis (Schlosser, 1768) from Ambon, Seram, Sulawesi and New Guinea, H. pustulatus (Eschscholtz, 1829) from the Philippines and H. weberi Barbour, 1911 from Halmahera and adjacent islands. Historically, two additional species were described from the island of Sulawesi, but were synonymized with H. amboinensis more than a century ago and have been treated as such in most subsequent publications. In order to revise the taxonomy and diversity of these enigmatic agamid lizards, we examined the corresponding type specimens and additional material originating from Sulawesi and compared them to photographs of live specimens from field trips. Due to differences in colour pattern and scalation characters, we resurrect the taxa celebensis Peters, 1872 and microlophus Bleeker, 1860 from the synonymy of H. amboinensis, which in turn is restricted to the central Moluccas and New Guinea. Hence, Sulawesi is currently the only known island within the genus' range to be inhabited by two different species of sailfin lizards. Our systematic investigation brings the number of recognized species within the genus Hydrosaurus to five.

On the systematic status of the genus Oriocalotes Günther, 1864(Squamata: Agamidae: Draconinae) with the description of a new species from Mizoram state, Northeast India.

The montane agamid lizard genus Oriocalotes is currently considered monotypic, represented by the species, O. paulus. The systematic status of this taxon has remained questionable since its initial descriptions in the mid-1800s. A detailed molecular and morphological study was carried out to assess the validity of this genus, and its systematic position within the Asian agamid subfamily, Draconinae. Freshly collected and historical museum specimens from the type locality of O. paulus were examined morphologically, along with additional samples collected from localities in Mizoram state, Northeast India. Utilising newly generated molecular sequences (two mitochondrial and three nuclear genes), combined with those previously published for representative genera from the subfamilies Draconinae and Agaminae, Maximum Likelihood and Bayesian phylogenetic trees were constructed. Phylogenetic results suggest that Oriocalotes is part of the widespread South and Southeast Asian radiation of Calotes. Comparative morphological studies (including external morphology, hemipenis and osteology) between Oriocalotes and related genera further support this systematic placement. Oriocalotes is herein regarded as a junior subjective synonym of Calotes. Calotes paulus comb. nov. is also assigned a lectotype and given a detailed redescription based on the lectotype, paralectotypes and additional topotypic material. Furthermore, the specimens collected from Mizoram populations are found to be morphologically and genetically distinct from Calotes paulus comb. nov., and are described herein as a new species, Calotes zolaiking sp. nov.

Covariations between personality behaviors and metabolic/performance traits in an Asian agamid lizard (Phrynocephalus vlangalii).

Ecological factors related to predation risks and foraging play major roles in determining which behavioral traits may mediate life history trade-offs and, therefore, the pace-of-life syndrome (POLS) structure among behavioral, physiological, and life-history traits. It has been proposed that activity/exploration or risk-taking behaviors are more likely to impact resource acquisition for organisms (individuals, populations, and species) foraging on clumped and ephemeral food sources than for organisms foraging on abundant and evenly distributed resources. In contrast, vigilance or freezing behavior would be expected to covary with the pace of life when organisms rely on food items requiring long bouts of handling. Nevertheless, it remains unclear how general this pattern is. We tested this hypothesis by examining the associations between exploration/risk-taking behaviors and metabolic/performance traits for the viviparous agamid lizard, Phrynocephalus vlangalii. This species forages on sparse and patchy food sources. The results showed positive correlations between exploration and endurance capacity, and between bite force and risk-taking willingness. Our current findings, in conjunction with our previous work showed no correlations between freezing behavior and performance in this species, support the idea that behaviors in life-history trade-offs are natural history-dependent in P. vlangalii, and provide evidence that behavioral types play functional roles in life history trade-offs to supporting POLS hypothesis.

The driving forces behind female-female aggression and its fitness consequence in an Asian agamid lizard

Female-female aggression and its effect on fitness are poorly understood compared to male-male aggression. We quantified female-female aggression in the viviparous toad-headed agama, Phrynocephalus vlangalii, and tested the mate limitation and resource competition hypotheses, to explain the driving forces behind heightened female-female aggression. We established populations in outdoor enclosures and separately manipulated mate and food availability while quantifying aggressive interactions between known females. Female mass and offspring quantity and quality were monitored for 2 years and used as an index of female fitness. Interestingly, female-female aggression was highest outside the mating season, when females were pregnant. Also, male availability did not significantly influence female-female aggression. Consequently, we found no evidence in support of the mate limitation hypothesis. Female-female aggression, however, was greatest during periods of low-food availability. Greater food availability did have positive fitness consequence for females: high-food treatment females were more likely to gain mass and give birth than females from the low-food treatment, and offspring from high-food treatment females were more likely to survive the first winter. However, we did have an effect of year: female mass was negatively associated with female-female aggression in year 1 but positively associated in year 2, although the association was not significant. The same pattern appeared in the association between offspring sprint speed and female-female aggression: higher levels of female-female aggression in year 1 were associated with slower offspring, while in year 2, higher female-female aggression was associated with faster offspring. Overall, our results demonstrate a link between female-female aggression and competition for resource (food) and highlight the potential importance of female aggressive behavior as a mechanism that influences female fitness. Male-male contest competition has been a cornerstone of sexual selection theory for decades because dominant males can control more space and access to females. Conversely, female aggression is poorly understood and sometimes considered a paradox, especially in species lacking parental care. We tested whether female-female aggression in the viviparous lizard P. vlangalii is best explained by competition for males (mate limitation hypothesis) or competition over food (food limitation hypothesis). Interestingly, female aggression peaks after mating, while females are still pregnant. Heightened aggression at this time supports the food limitation hypothesis because any advantage females have in terms of access to resources will benefit offspring born into her home range. Likewise, access to additional food resources may improve female survival and future reproductive investment through greater energy storage.

A molecular phylogenetic hypothesis for the Asian agamid lizard genus Phrynocephalus reveals discrete biogeographic clades implicated by plate tectonics.

Phylogenetic relationships of the agamid lizard genus Phrynocephalus are described in the context of plate tectonics. A near comprehensive taxon sampling reports three data sets: (1) mitochondrial DNA from ND1 to COI (3' end of ND1, tRNAGln, tRNAIle, tRNAMet, ND2, tRNATrp, tRNAAla, tRNAAsn, tRNACys, tRNATyr, and the 5' end of COI) with 1761 aligned positional sites (1595 included, 839 informative), (2) nuclear RAG-1 DNA with 2760 aligned positional sites (342 informative), and (3) 25 informative allozyme loci with 213 alleles (107 informative when coded as presence/absence). It is hypothesized that Phrynocephalus phyletic patterns and speciation reflect fault lines of ancient plates now in Asia rejuvenated by the more recent Indian and Arabian plate collisions. Molecular estimates of lineage splits are highly congruent with geologic dates from the literature. A southern origin for the genus in Southwest Asia is resolved in phylogenetic estimates and a northern origin is statistically rejected. On the basis of monophyly and molecular evidence several taxa previously recognized as subspecies are recognized as species: P. hongyuanensis, P. sogdianus, and P. strauchi as "Current Status"; Phrynocephalus bannikovi, Phrynocephalus longicaudatus, Phrynocephalus turcomanus, and Phrynocephalus vindumi are formally "New Status". Phylogenetic evaluation indicates a soft substrate habitat of sand for the shared ancestor of modern Phrynocephalus. Size diversity maximally overlaps in the Caspian Basin and northwestern Iranian Plateau. The greatest species numbers of six in sympatry and regional allopatry are found in the southern Caspian Basin and southern Helmand Basin, both from numerous phylogenetic lineages in close proximity attributed to tectonic induced events.

Female–female aggression functions in mate defence in an Asian agamid lizard

Female–female aggression and its functions are poorly understood compared with male–male aggression. Here, we examined the role of female–female aggression in mate defence in an Asian agamid lizard, Phrynocephalus vlangalii, in which male neighbours are valuable to females in both mating success and resource defence. We provided three social contexts by pairing a resident female with either a neighbour male, unfamiliar male or unfamiliar female, then introduced a tethered unknown female (intruder). We carried out our experiments during and outside the mating season to test the links between female–female aggression and mate defence. The aggressive responses of resident females in these different social contexts were compared by quantifying variation in their territorial displays. Resident females were faster to display to the intruder in the presence of a neighbour male compared with both the unfamiliar male and female. We also found that female lizards signalled faster in the presence of the neighbour male than the other contexts, but only during the mating season. To separate the effects of familiarity from those of sex, we carried out a second experiment in which we paired a resident female with a neighbour male or neighbour female, before introducing a tethered unfamiliar female. In this experiment, resident females responded sooner to intruder females when paired with the neighbour male, although signalling speeds were equivalent. Taken together, our results suggest female–female aggression is used for both resource and mate defence, and so might be under direct selection. Our study highlights that female aggression more broadly requires further work.

A taxonomic mystery for more than 180 years: the identity and systematic position of Brachysaura minor (HARDWICKE & GRAY, 1827)

Brachysaura is a monotypic genus of agamid lizard found in the Indian subcontinent; the identity and systematic position of B. minor has been long debated, and it has at times been subsumed into Agama, Charasia and Laudakia, with some authors suggesting affinities to Calotes. We constructed nuclear and mitochondrial phylogenetic trees including Brachysaura and allied agamid genera to resolve its phylogenetic position. We also compared osteology and external morphology with the genera Agama, Calotes and Laudakia. Hemipenial morphology was compared with Calotes and some other agamids from South Asia. Both nuclear and mitochondrial phylogenies demonstrate that Brachysaura is nested within the widespread South and Southeast Asian genus Calotes, with which it also shares certain external morphological, osteological and hemipenial characters. Adaptations to ground dwelling in Brachysaura minor has resulted in unique modifications to its body plan, which is likely why generic allocation has been long confused. This study also highlights the need for an integrated systematic approach to resolve taxonomic ambiguity in Asian agamids.

An atypical reproductive cycle in a common viviparous Asia Agamid Phrynocephalus vlangalii.

Viviparous lizards living in cold climate of high altitude often exhibit atypical reproductive cycles, in which mating and fertilization occur synchronously and annually with parturition occurring at the end of the year. Nevertheless, detailed case studies on atypical reproductive cycles are few. Using anatomical data combined with behavioral observations, we examined the reproductive cycle of a common Asian agamid, Phrynocephalus vlangalii, from a high-elevation area in Sichuan, China. Male spermiation of P.vlangalii occurred in May, and spermatogenesis began in June and reached a maximum in October. For females, ovulation and fertilization occurred in May, and females developed gestation and pregnancy in 3months from June to August, without vitellogenesis during this period. Females gave birth synchronously in late August, then vitellogenesis began and lasted until May of the next year. All adult males and females were synchronized in the same reproductive condition each month. The synchronous and annual reproductive cycle of P.vlangalii clearly represents an atypical cycle. The male courtship and mating behaviors were concordant with gonadal cycle and mainly happened in May and June. Despite the short growth period for neonates, they had a high over-winter survival rate of 84.4%, suggesting that autumn parturition did not generate high costs to this reproductive cycle. We propose that the high over-winter survival rate of neonates is likely linked with female delayed sexual maturity, female asynchronous vitellogenesis and gestation, large relative clutch mass (RCM), and adult-offspring burrow sharing behavior during hibernation.

Sex- and performance-based escape behaviour in an Asian agamid lizard, Phrynocephalus vlangalii

In lizards, males are predicted to sprint faster and run for longer than females by virtue of higher testosterone levels and differences in morphology. Consequently, escape behaviour is also predicted to be associated with sex and locomotor performance, yet these links have rarely been explored. Here, we tested whether escape behaviour is associated with locomotor performance in the toad-headed agama, Phrynocephalus vlangalii, and whether it is sex-dependent. This species is also characterized by elaborate tail displays, which we examined as a potential pursuit-deterrent signal. Tail waves were performed by a very small proportion (2/58, 3 %) of individuals during predatory trials, suggesting that tail signalling functions exclusively in a social context. To understand the relationships between sex, escape behaviour and performance, we first measured escape behaviour (flight initiation distance, flight distance—measured differently compared to previous studies of lizard escape behaviour, and refuge use) in the field before measuring maximal sprint speed and endurance on the same individuals in the laboratory. Flight initiation distance did not differ between the sexes and was unrelated to performance capacity (maximal endurance and sprint speed) but was positively related to body size with larger individuals fleeing earlier. Males fled farther than females, but flight distance was also unrelated to either endurance or sprint speed. Interestingly, faster females were less likely to enter a refuge than slower females, whereas sprint speed and the probability of taking refuge were unrelated for males. Our results suggest that when males and females are not obviously sexually dimorphic, they are more likely to overlap in escape tactics.

Research on Asian Agamid Lizards: Contribution of Zoological Institute, Russian Academy of Sciences, St. Petersburg

In this paper, I give an overview of the study of agamid lizards in the Zoological Institute of the Russian Academy of Sciences (ZISP), St.Petersburg. Naturally , history of this study is inseparabl y associated with general zoological research in Russia. During the period of exploration and organized scientific expeditions, the Russian Academy of Sciences aimed to study the natural resources of the unbounded territories of Russia, and a number of prominent foreign scientists were invited to Russia for these research expeditions. One of the most prominent scientists was Peter S. Pallas (1741-1811) , whose activities resulted in the first inventory of biological resources of the country. This period was also a time of exploration and descriptions in herpetology. Among the first expeditions, of interest to herpetologists was Peter S. Pallas’s trip to eastern Russia and Siberia (1768-1773), and herpetological studies can be traced to this scientist , whose 270th Anniversary we celebrated in 2011. One of the results of Pallas 's great expedition was the first inventory of amphibians and reptiles of the fauna of Russia and of description of numerous new species of amphibians and reptiles. Most of the collections (including amphibians and reptiles) were taken to the Crimea where he finished writing his classical book, «Zoographia Rosso-Asiatica» (Svetovidov, 1978) that can be regarded as the first complete inventory of amphibians and reptiles. Unfortunately, most of his material is no longer available ; some specimens were transferred later to the Zoological Museum of the Humboldt-University in Berlin and the National Museum of Natural History in Paris.

Skin Receptors of Laudakia (Agamidae, Sauria) with Some Comments about Scalation of Asian Rock Agamids

The structure of scale and receptors in the integument of six species of Laudakia ( L. caucasia , L. chernovi , L. erythrogastra , L. himalayana , L. lehmanni , and L. stoliczkana) has been studied. The comparison of the integument and the skin receptors was made using the methods of histology and scanning electron microscopy (SEM). The variation in scale morphology (papillous scales and scales with jagged margins) in L. caucasia and L. erythrogastra have been noted. The comparison of receptors density for the unit of the square on the ventral and dorsal surface and among different species shows the association of receptors density and number of scales around the midbody of Asian rock agamids.

THE SKULL STRUCTURE OF SOME ARID ASIAN AGAMIDS OF Phrynocephalus GENUS (AGAMIDAE, SAURIA)

The skull structure of some species of arid Asian agamids genus Phrynocephalus from the Middle Asia was studied. It differs from other lizards of this family by some specific characters. The construction of the short and wide skull forms its “bulldog”-like shape created by the strong protruding of the lower jaw together with quadratum bone. Of special comparative interest are the following cranial characters: the angles between maxillae and its appendices, the shift of the occipital junction, the dental formula and the size of the parietal foramen. In general the juvenile specimens have larger parietal foramen that decreases during their ontogeny. The differences in the size of the parietal foramen in several species of Phrynocephalus are noted and compared. The paedomorphic characters in the skull structure and dentition are discussed.

Some Aspects of Historical Biogeography of Asian Rock Agamids

The genesis of areals of Asian rock agamids belonging to the genus Laudakia Gray, 1845 is considered. The hypothesis about two routes of radiation of these lizards endemic for arid mountain regions of Palearctic is offered. The southern route from the hypothetical center of origin in the area of mountain systems of Hindukush and Himalayas passed in the conditions of southern subtropics with well developed belt of sclerophilous forests. This evolutional line with « caucasia » complex remains the relic areas in forest regions. Northern group of species with « himalayana » complex had its speciation in northern subtropic area with more severe climatic situation determined by strong continental and arid conditions. Altitudinal and biotopic differences of Laudakia species under their sympatric distribution are specially discussed.

Systematic and taxomonic revaluation of four little known Asian agamid species, Calotes kingdonwardi Smith, 1935, Japalura kaulbacki Smith, 1937, Salea kakhienensis Anderson, 1879 and the monotypic genus Mictopholis Smith, 1935 (Reptilia: Agamidae)

The systematic status of many Asian Draconine agamids has long been in dispute. Herein, four such species, Mictopholis austeniana, Japalura kaulbacki, Calotes kingdonwardi and Salea kakhienensis are examined on the basis of external morphological characters. The monotypic genus Mictopholis was compared to other Asian Draconine genera and found to be indistinguishable from Pseudocalotes, with which it is here considered a synonym. Japalura kaulbacki is compared to other members of the genus Japalura as well as other similar species. Based on external morphology it is found to be separable from Japalura and conspecific with Calotes kingdonwardi, under which it is considered a junior subjective synonym. Salea kakhienensis is redefined morphologically based on nontype material and shown to represent a close member of this group. C. kingdonwardi is most similar to Salea kakhienensis both of which share a complement of characters with M. austeniana. The generic placement of S. kakhienensis relative to Salea, both with strongly overlapping synapomorphic characters is briefly discussed with respect to biogeographical implications that strongly support the exclusion of this species from the genus. Mictopholis austeniana, Calotes kingdonwardi and Salea kakhienensis are redescribed in detail and transferred to Pseudocalotes. The inclusion of these three species provides a generic range extension of approximately 800 km north-west of the previously considered range. The nomen Oriocalotes discolor is considered a primary objective synonym of Pseudocalotes kakhienensis new comb. and the systematic status of Calotes kingdonwardi bapoensis is briefly discussed.

Historical biogeography, phylogenetic relationships and intraspecific diversity of agamid lizards in the Central Asian deserts of Kazakhstan and Uzbekistan

The Central Asian agamid lizards are ecologically and morphologically diverse, occurring across a broad range of desert environments in this biogeographically important region. It is probable that past climatic shifts have significantly influenced the diversification patterns and distributions of the agamid lizards of this region. To assess this within a phylogenetic framework we sequenced a ∼1200 bp region of mitochondrial DNA and a ∼1200 bp nuclear gene (RAG-1), incorporating both inter- and intraspecific sampling across Central Asian agamids. Our topology and divergence time estimates support an Eocene origin of the Agaminae subfamily on the Indian subcontinent, coinciding with the collision of India into Eurasia. The onset of aridification in Central Asia during the Late Oligocene, resulting from the retreat of the Paratethys Sea and the intensified uplift of the Tibetan–Himalayan complex, probably played an important role in the diversification of Phrynocephalus, one of the three genera studied. Intensification of aridity and geologic events in the Plio-Pleistocene and Quaternary glacial cycling probably had a significant influence on intraspecific diversification patterns within Phrynocephalus.

Costs of reproduction and the evolution of sexual dimorphism in a ‘flying lizard’Draco melanopogon (Agamidae)

AbstractLife‐history models suggest that ‘costs of reproduction’ can influence the evolution of sexual dimorphism, but empirical data on this effect are scarce. We tested the idea using ‘flying lizards’ (Asian agamids of the genus Draco), because the evolution of ‘flight’ (gliding) is likely to have increased the degree to which pregnancy affects maternal locomotor ability (and hence, we infer, has increased the ‘costs of reproduction’). As predicted, Draco display patterns of sexual dimorphism that are different from those seen in most other lizards. The ‘wings’ (gliding membranes) of female D. melanopogon are significantly larger than those of males of the same body size, a dimorphism that we attribute to natural selection on the ability to glide while encumbered with eggs. Comparisons with non‐flying lizards suggest that the same selective pressure has also reversed pre‐existing patterns of sexual dimorphism in body size and body proportions (relative head size, relative tail length). Measurements of wing‐loading, centre of balance and gliding distances of preserved specimens support the hypothesis that a larger body, relatively larger head, and longer tail may improve a female's aerial mobility when she is gravid. Thus, selection for locomotor ability in egg‐burdened females (reduction in ‘costs of reproduction’) may have been responsible for a reversal of sexually‐selected traits in this lineage.