Chlamydosaurus Research Articles

Molecular evidence of Monocercomonas and Acanthamoeba in the feces of captive reptiles

Reptiles are frequently kept as pet animals. They are considered as important reservoirs of protozoa with veterinary-medical significance. At a reptile farm in Ireland, fecal samples were collected from 98 captive reptiles, representing 43 species of three orders (Squamata, Testudines, and Crocodylia). After DNA extraction, all samples were screened by conventional PCRs, targeting the ribosomal small subunit (SSU) RNA and alpha-tubulin genes of trichomonads and SSU RNA gene of Acanthamoeba spp. One leopard gecko (Eublepharis macularius) was positive for a not yet reported species/genotype of the genus Monocercomonas, different from M. colubrorum. Various Acanthamoeba genotypes were detected in six reptilian species, i.e., Acanthamoeba genotype T11 in Eunectes notaeus and Heloderma suspectum/horridum; genotype T4 in Varanus exanthematicus, Chlamydosaurus kingii, and Macrochelys temminckii; and the genotype T13 in Iguana iguana. Some of these amoeba species might have clinicopathological significance in both humans and animals. Our findings highlight the importance to monitor pathogenic protozoa in pet as well as wildlife reptiles, as a source of possible infection for animals and humans living nearby.

The acoustical effect of the neck frill of the frill-necked lizard (Chlamydosaurus kingii).

Animals localise sound by making use of acoustical cues resulting from space and frequency dependent filtering of sound by the head and body. Sound arrives at each ear at different times, with different intensities, and with varying spectral content, all of which are affected by the animal's head and the relative sound source position. Location cues in mammals benefit from structures (pinnae) that modify these cues and provide information that helps resolve the cone of confusion and provide cues to sound source elevation. Animals without pinnae must rely on other mechanisms to solve localisation problems. Most non-mammals lack pinna-like structures, but some possess other anatomical features that could influence hearing. One such animal is the frill-necked lizard (Chlamydosaurus kingii). The species' elaborate neck frill has been speculated to act as an aid to hearing, but no acoustical measurements have been reported. In this study, we characterise the frill's influence on the acoustical information available to the animal. Results suggest that the change in binaural cues is not sufficiently large to impact localisation behavior within the species' likely audiometric range; however, the frill does increase gain for sounds directly in front of the animal similar to a directional microphone.

Uncovering the function of an enigmatic display: antipredator behaviour in the iconic Australian frillneck lizard

Abstract When faced with a predator, some animals engage in a deimatic display to startle the predator momentarily, resulting in a pause or retreat, thereby increasing their chance of escape. Frillneck lizards (Chlamydosaurus kingii) are characterised by a large, pronounced frill that extends from the base of the head to beyond the neck and, when displayed, can be up to six times the width of the head. We used behavioural assays with a model avian predator to demonstrate that their display conforms to deimatic display theory. First, juveniles and adults deployed the frill in encounters with a model predator. Second, the display revealed three colour patches (white and red–orange patches on the frill; yellow mouth palate) that facilitate a transition from a cryptic to a conspicuous state as perceived by a raptor visual system. Third, the display was performed with movements that amplified its effect. The frill area was larger in males than in females, which suggests that the frill might also be co-opted for male–male contests. If future research confirms a role of the frill in male agonistic interactions, frillneck lizards will be a rare case in which a structure has a dual function in a deimatic display and a sexually selected signal.

Red carotenoids and associated gene expression explain colour variation in frillneck lizards.

A long-standing hypothesis in evolutionary ecology is that red-orange ornamental colours reliably signal individual quality owing to limited dietary availability of carotenoids and metabolic costs associated with their production, such as the bioconversion of dietary yellow carotenoids to red ketocarotenoids. However, in ectothermic vertebrates, these colours can also be produced by self-synthesized pteridine pigments. As a consequence, the relative ratio of pigment types and their biochemical and genetic basis have implications for the costs and information content of colour signals; yet they remain poorly known in most taxonomic groups. We tested whether red- and yellow-frilled populations of the frillneck lizard, Chlamydosaurus kingii, differ in the ratio of different biochemical classes of carotenoid and pteridine pigments, and examined associated differences in gene expression. We found that, unlike other squamate reptiles, red hues derive from a higher proportion of ketocarotenoids relative to both dietary yellow carotenoids and to pteridines. Whereas red frill skin showed higher expression of several genes associated with carotenoid metabolism, yellow frill skin showed higher expression of genes associated with steroid hormones. Based on the different mechanisms underlying red and yellow signals, we hypothesize that frill colour conveys different information in the two populations. More generally, the data expand our knowledge of the genetic and biochemical basis of colour signals in vertebrates.

Elastic instability during branchial ectoderm development causes folding of the Chlamydosaurus erectile frill

We study the morphogenesis and evolutionary origin of the spectacular erectile ruff of the frilled dragon (Chlamydosaurus kingii). Our comparative developmental analyses of multiple species suggest that the ancestor of Episquamata reptiles developed a neck fold from the hyoid branchial arch by preventing it to fully fuse with posterior arches. We also show that the Chlamydosaurus embryonic neck fold dramatically enlarges and its anterior surface wrinkles, establishing three convex ridges on each lobe of the frill. We suggest that this robust folding pattern is not due to localised increased growth at the positions of the ridges, but emerges from an elastic instability during homogeneous growth of the frill skin frustrated by its attachment to adjacent tissues. Our physical analog experiments and 3D computational simulations, using realistic embryonic tissue growth, thickness and stiffness values, recapitulate the transition from two to three ridges observed during embryonic development of the dragon's frill.

Changes in ontogenetic patterns facilitate diversification in skull shape of Australian agamid lizards

BackgroundMorphological diversity among closely related animals can be the result of differing growth patterns. The Australian radiation of agamid lizards (Amphibolurinae) exhibits great ecological and morphological diversity, which they have achieved on a continent-wide scale, in a relatively short period of time (30 million years). Amphibolurines therefore make an ideal study group for examining ontogenetic allometry. We used two-dimensional landmark-based geometric morphometric methods to characterise the postnatal growth patterns in cranial shape of 18 species of amphibolurine lizards and investigate the associations between cranial morphology, and life habit and phylogeny.ResultsFor most amphibolurine species, juveniles share a similar cranial phenotype, but by adulthood crania are more disparate in shape and occupy different sub-spaces of the total shape space. To achieve this disparity, crania do not follow a common post-natal growth pattern; there are differences among species in both the direction and magnitude of change in morphospace. We found that these growth patterns among the amphibolurines are significantly associated with ecological life habits. The clade Ctenophorus includes species that undergo small magnitudes of shape change during growth. They have dorsoventrally deep, blunt-snouted skulls (associated with terrestrial lifestyles), and also dorsoventrally shallow skulls (associated with saxicolous lifestyles). The sister clade to Ctenophorus, which includes the bearded dragon (Pogona), frill-neck lizard (Chlamydosaurus), and long-nosed dragon (Gowidon), exhibit broad and robust post-orbital regions and differing snout lengths (mainly associated with scansorial lifestyles).ConclusionsAustralian agamids show great variability in the timing of development and divergence of growth trajectories which results in a diversity of adult cranial shapes. Phylogenetic signal in cranial morphology appears to be largely overwritten by signals that reflect life habit. This knowledge about growth patterns and skull shape diversity in agamid lizards will be valuable for placing phylogenetic, functional and ecological studies in a morphological context.

Development of a mobile robot mimicking the frilled lizard

Here a prototype biomimetic robot is presented that imitates the shape and motion of a frilled lizard. The robot’s upper body posture can be controlled using the air resistance generated by the frill around the neck during running. Several experiments were conducted to determine the range of motion of the robot. A fan experiment showed that the robot could adjust the angle of the upper body at intervals of at least 5° to 10° up to 35°. The robot was able to control the angle of its upper body to an accuracy of about 1° while running. Thus, the robot controlled its upper body angle using the membrane around its neck. This is the first robot to use air to control the upper body posture.

Curvilinear telomere length dynamics in a squamate reptile

Summary The lack of consensus concerning the impact of telomere length (TL) dynamics on survival emphasizes the need for additional studies to evaluate the effect of TL on key life‐history processes. Using both cross‐sectional and longitudinal data, we therefore explored age‐specific TL dynamics in a squamate reptile: the frillneck lizard (Chlamydosaurus kingii). Our cross‐sectional analyses revealed that young lizards had short TL, TL increased in medium‐aged lizards, but TL decreased in older age cohorts, revealing a curvilinear relationship between TL and frillneck lizard age. Neither our cross‐sectional nor our longitudinal analyses revealed any association between TL dynamics and lizard survival. We observed a significant positive relationship between TL and telomerase expression (TE), suggesting that TE is a significant determinant of frillneck lizard TL dynamics. Importantly, our longitudinal analyses revealed a positive relationship between initial TL and telomere attrition rate within individual lizards, that is lizards with short initial telomeres were subjected to reduced telomere attrition rates compared to lizards with long initial TL. Our results strongly suggest that TL and TE dynamics in frillneck lizards is not associated with lizard survival but rather reflect an adaptation to maintain TL above a critical minimum length in order to sustain cellular homeostasis. A lay summary is available for this article.

Phylogeographic structure across one of the largest intact tropical savannahs: Molecular and morphological analysis of Australia’s iconic frilled lizard Chlamydosaurus kingii

The spectacular threat display of the savannah specialist Australo-Papuan frilled lizards has made them one of the world’s most iconic reptiles. They are increasingly used as a model system for research in evolutionary biology and ecology but little is known of their population structure. Their distribution across northern Australia and southern New Guinea also provides an opportunity to examine biogeographic patterns as they relate to the large-scale movement of savannah habitat during the Plio/Pleistocene and the associated increase in aridity. We generated sequence data for one mitochondrial and four nuclear DNA loci (5052 base pairs) for 83 frilled lizards sampled throughout their range. We also quantified body proportion variation for 279 individuals. Phylogenetic analyses based on maximum likelihood and Bayesian species-tree methods revealed three shallow clades that replace each other across the monsoon tropics. We found the expected pattern of male biased sexual size dimorphism in both maximum body size and head size but there was no sexual dimorphism in overall body shape or in frill size, relative to head size, supporting the hypothesis that the frill is used primarily as a threat display rather than a sexual display. The genetic clades are broadly consistent with known clinal variation in frill color that gradually shifts from west to east (red, orange, yellow/white) but otherwise show little morphological differentiation in body proportion measures. The biogeographic breaks between clades occur at the Carpentaria Gap and the lowlands surrounding the Ord River, and our ecological niche modeling predicts lower habitat suitability for C. kingii in these regions. While this biogeographic pattern is consistent with numerous other taxonomic groups in northern Australia, the overall low genetic diversity in frilled lizards across the entire monsoon tropics and southern New Guinea contrasts starkly to patterns seen in other terrestrial vertebrates. Extremely low intra-clade genetic diversity over vast geographic areas is indicative of recent gene flow that would likely have been facilitated by widespread savannah during interglacials, or alternatively may reflect population bottlenecks induced by extreme aridity during Pleistocene glacials. The shallow divergence between Australian and New Guinean samples is consistent with recent connectivity between Australia and New Guinea that would have been possible via a savannah corridor across the Torres Strait. Based on our molecular and morphological data, we do not support taxonomic recognition of any of the frilled lizard clades and instead consider C. kingii a single species with shallow phylogeographic structure and clinal variation in frill color.

Proximate mechanisms of colour variation in the frillneck lizard: geographical differences in pigment contents of an ornament

Animal coloration has evolved in contexts such as communication, camouflage, and thermoregulation. Most studies of animal coloration focus on its adaptive benefits, whereas its underlying mechanisms have received less attention despite their potential influence on adaptive benefits. In fish and reptiles, for example, colour variation from yellow to red can be produced by carotenoid and/or pteridine pigments, which differ dramatically in the way they are obtained (carotenoids through diet and pteridines synthesized de novo). Hence, potential adaptive benefits could differ greatly depending on the relative contribution to coloration of different pigments. In the present study, we investigate the mechanisms underlying colour variation in the frill of the Australian frillneck lizard (Sauropsida: Chlamydosaurus kingii). Frill colour varies between populations across the species’ range (red, orange, yellow or white). We argue that this geographical variation results from different concentrations of carotenoids and pteridines in the frill. Frill carotenoid concentrations were lower in eastern populations (yellow and white forms), and pteridines were present only in the red and orange forms, thereby explaining their redder hues. The observed geographical variation in frill carotenoids suggests variation in carotenoid availability across the species’ range, which is backed up by the finding that plasma carotenoid concentrations were higher in the red (western) compared to the yellow (eastern) form. Although no correlations were found between individual colour measurements, frill pigments and plasma carotenoids, our results suggest that selective pressures vary across the species’ range and we speculate that predation pressures and/or intrasexual signalling context differ between forms. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 00, 000–000. ADDITIONAL KEYWORDS: carotenoids ‐ gradient ‐ honest signalling ‐ productionproximate mechanism ‐ pteridines.

Population demography of frillneck lizards (Chlamydosaurus kingii, Gray 1825) in the wet‐dry tropics of Australia

AbstractWe explore the effects of biotic and abiotic factors on the population demography of frillneck lizards (Chlamydosaurus kingii) in the Australian wet‐dry tropics. Annual growth rates of males were significantly higher across all body sizes compared to females, resulting in a significant larger maximum body size in males. Both male and female lizards were highly philopatric and 81% of the among‐year recapture distances were less than 200 m. Juvenile and adult frillnecks were subjected to low but highly variable annual survival rates. Both proportion of juveniles and relative proportion of reproductive females showed extensive among‐year variations. No relationship was, however, observed between proportion of gravid females and that of juveniles captured during the subsequent year. High rainfall in January was negatively correlated with recruitment most likely caused by increased egg/embryo mortality due to flooding of nest sites. We therefore suggest that the lack of association between female reproduction and juvenile recruitment was due to the effects of stochastic variation in January rainfall. Lizard numbers increased during the first five years of the study followed by a decline during the subsequent four years. Our analyses show that annual variation in survival constituted the main determinant in driving the annual change in frillneck numbers. Surprisingly, no relationship was observed between fillneck population dynamics and annual variation in juvenile recruitment. We suggest that the 7‐years over which these analyses were conducted were insufficient to detect any significant effects of recruitment on lizard numbers, demonstrating the need for long‐term studies to accurately document vertebrate population demographic processes in areas experiencing stochastic variations rainfall such as the Australian wet‐dry tropics.

Prevalence of Devriesea agamarum in the lizard collection of The Royal Zoological Society of Antwerp.

In recent times, Devriesea agamarum is more frequently diagnosed as the causative organism of dermatitis in lizards, particularly in spiny-tailed lizards ( Uromastyx sp.). Other lizard species such as bearded dragons ( Pogona vitticeps ) are known as asymptomatic carriers posing a potential threat to the healthy animals in a collection. This study reports on the isolation and phenotypic identification of D. agamarum from six healthy jeweled curly-tailed lizards ( Leiocephalus personatus ) in the reptile collection of the Royal Zoological Society of Antwerp. Two clinical cases were presented in the same study period: a frilled lizard ( Chlamydosaurus kingii ) and a Philippine sailfin lizard ( Hydrosaurus pustulatus ). These animals had abscesses in their beaks from which rich growth of D.agamarum was obtained. It was concluded from this study that a quarantine programme for newly acquired animals is important to detect healthy carriers and prevent the spread of infection.

Fiery frills: carotenoid-based coloration predicts contest success in frillneck lizards

Conspicuous color signals are commonly used by a wide diversity of animals to advertise some specific aspect of their competitive ability. In particular, orange and red colors are often used as an aggressive signal to potential rivals. The iconic Australian frillneck lizard (Chlamydosaurus kingii) has a large and extensible frill that varies geographically in the extent of yellow, orange, and red present. Focusing on the red-orange lizards found in Western Australia, we first established that, in contrast to most lizards studied to date, the red-orange–colored frill is carotenoid rather than pterin based. Second, we measured chromatic and achromatic aspects of male frills before staging dyadic contests between males to determine whether color is used to signal fighting ability. Both chromatic and achromatic measures of the red-orange patches on the lizard’s frills, as well as similarly colored patches on their throats, were reliable predictors of competitive ability; males possessing more colorful displays dominated sizematched competitors in dyadic contests. Apart from large differences in body size and mass (>10%), no other colorimetrics (e.g., white patches), frill traits (e.g., size, relative and absolute patch sizes), or morphological measures (e.g., head size, bite force) were found to predict the outcome of contests. To the best of our knowledge, this is the first example of carotenoid-based patches signaling male fighting ability in a lizard.

Detecting the impact of invasive species on native fauna: Cane toads (Bufo marinus), frillneck lizards (Chlamydosaurus kingii) and the importance of spatial replication

AbstractAn understanding of which native species are severely impacted by an anthropogenic change (such as the arrival of an invasive species) and which are not is critical to prioritizing conservation efforts. However, it is difficult to detect such impacts if the native taxa exhibit strong stochastic variations in abundance; a ‘natural’ population decline might be wrongly interpreted as an impact of the invader. Frillneck lizards (Chlamydosaurus kingii) are large iconic Australian agamids, and have been reported to decline following the invasion of toxic cane toads. We monitored three populations of the species in the savanna woodland of tropical Australia over a 7‐year period bracketing toad arrival. One population crashed, one remained stable and one increased. Hence, studies on any single population might have inferred that cane toads have negative, negligible or positive effects on frillneck lizards. With the benefit of spatial replication, and in combination with observations of prey choice by captive lizards, our data suggest that invasive cane toads have had little or no effect on frillneck abundance.

Population genetic structure, gene flow and sex‐biased dispersal in frillneck lizards (Chlamydosaurus kingii)

By using both mitochondrial and nuclear multiloci markers, we explored population genetic structure, gene flow and sex-specific dispersal of frillneck lizards (Chlamydosaurus kingii) sampled at three locations, separated by 10 to 50 km, in a homogenous savannah woodland in tropical Australia. Apart from a recombinant lizard, the mitochondrial analyses revealed two nonoverlapping haplotypes/populations, while the nuclear markers showed that the frillneck lizards represented three separate clusters/populations. Due to the small population size of the mtDNA, fixation may occur via founder effects and/or drift. We therefore suggest that either of these two processes, or a combination of the two, are the most likely causes of the discordant results obtained from the mitochondrial and the nuclear markers. In contrast to the nonoverlapping mitochondrial haplotypes, in 12 out of 74 lizards, mixed nuclear genotypes were observed, hence revealing a limited nuclear gene flow. Although gene flow should ultimately result in a blending of the populations, we propose that the distinct nuclear population structure is maintained by frequent fires resulting in local bottlenecks, and concomitant spatial separation of the frillneck lizard populations. Limited mark-recapture data and the difference in distribution of the mitochondrial and nuclear markers suggest that the mixed nuclear genotypes were caused by juvenile male-biased dispersal.

Complete mitochondrial genome of the frillneck lizard (Chlamydosaurus kingii, Reptilia; Agamidae), another squamate with two control regions

Using PCR, the complete mitochondrial genome was sequenced in three frillneck lizards (Chlamydosaurus kingii). The mitochondria spanned over 16,761bp. As in other vertebrates, two rRNA genes, 22 tRNA genes and 13 protein coding genes were identified. However, similar to some other squamate reptiles, two control regions (CRI and CRII) were identified, spanning 801 and 812 bp, respectively. Our results were compared with another Australian member of the family Agamidae, the bearded dragon (Pogana vitticeps). The overall base composition of the light-strand sequence largely mirrored that observed in P vitticeps. Furthermore, similar to P. vitticeps, we observed an insertion 801 bp long between the ND5 and ND6 genes. However, in contrast to P vitticeps we did not observe a conserved sequence block III region. Based on a comparison among the three frillneck lizards, we also present data on the proportion of variable sites within the major mitochondrial regions.

Mitochondrial DNA recombination in a free-ranging Australian lizard

Mitochondrial DNA (mtDNA) is the traditional workhorse for reconstructing evolutionary events. The frequent use of mtDNA in such analyses derives from the apparent simplicity of its inheritance: maternal and lacking bi-parental recombination. However, in hybrid zones, the reproductive barriers are often not completely developed, resulting in the breakdown of male mitochondrial elimination mechanisms, leading to leakage of paternal mitochondria and transient heteroplasmy, resulting in an increased possibility of recombination. Despite the widespread occurrence of heteroplasmy and the presence of the molecular machinery necessary for recombination, we know of no documented example of recombination of mtDNA in any terrestrial wild vertebrate population. By sequencing the entire mitochondrial genome (16761bp), we present evidence for mitochondrial recombination in the hybrid zone of two mitochondrial haplotypes in the Australian frillneck lizard (Chlamydosaurus kingii).

Microsatellite loci for Australian agamid lizards

AbstractWe characterize 15 microsatellite loci from two microsatellite libraries developed from the Australian agamid lizards Amphibolurus muricatus and Ctenophorus pictus. All loci were tested for amplification in four other agamids: Ctenophorus fordi, Ctenophorus decresii, Chlamydosaurus kingii, and Physignathus lesueurii. These loci were highly polymorphic within and across species, with nine to 12 loci amplifying for each species tested.

Demography and Home Range of the Frillneck Lizard, Chlamydosaurus kingii (Agamidae), in Northern Australia

The demography and home range of a population of frillneck lizards, Chlamydosaurus kingii, were examined from 1992 to 1994, in Kakadu National Park, Northern Territory, Australia. Lizards were studied using radiotelemetry and mark-recapture techniques. Reproduction occurred between November and April each year, coinciding with monsoonal conditions. Reproductive activity was highest in the first three months of the wet season. Females reached sexual maturity at 18 months of age. Males grew faster than females. Minimum longevity in the field was four years for females and six years for males. The population structure was constant at three sites, and the sex ratio exhibited a strong male bias. Density of frillneck lizards in Eucalyptus open forest varied from 0.13 to 0.78 hasup-1/sup. Males have larger dry-season home ranges (mean=1.96± 0.57 ha) than females (mean=0.63± 0.12 ha). No seasonal difference was evident in size of home range for either male or female lizards. No correlation was evident between snout-vent length and home range for either sex. This suggests that the home ranges of frillneck lizards were not determined by either food resources or body size but possibly related to social behavior. Arid-adapted agamids exhibit broad similarity in timing of the reproductive season, whereas factors such as growth and age at sexual maturity differ with body size and environmental conditions.

Androgen Concentrations and Behavior of Frillneck Lizards (Chlamydosaurus kingii)

We observed adult-like display behavior in newly hatched frillneck lizards, Chlamydosaurus kingii, including hand waving and erection of the frill. Hatchlings were placed together in groups of four for a week at a time and a measure of dominance was scored with respect to gaining access to a basking site. In most cases, the hatchlings were ordered non-randomly with respect to the optimum basking site, suggesting a hierarchy among the lizards. Plasma androgen concentrations were measured in hatchlings and lizards of both sexes of age classes ranging from hatchlings to three or more years old. Hatchling dominance was not related to plasma androgen concentrations, sex, or body size, but there was a positive correlation between dominance and mass gained over the six weeks of observations. Plasma androgen concentrations were low in all age and sex groups except adult males three or more years old, although two-year-old males had slightly elevated concentrations. A few (8%) two year old males had scars, presumably from intraspecific fights, but many (46%) males three or more years old had scars. No females or males younger than two years old were scarred.