Laudakia Research Articles

Tourism influences escape behavior of lizards in relationship with human clothing color

Increased tourism pressure modifies animal behavior, including alterations in anti-predator responses and foraging activity. In areas with high tourist presence, animals may become accustomed to increased human activity and adjust the intensity of some defensive responses. An animal’s anti-predation ability is usually estimated by measuring its Alert Initiation Distance (AID) and Flight Initiation Distance (FID). Both indexes are affected by multiple factors including the color of the observer’s clothing. Animal behavior is also influenced by human presence, and individuals may become accustomed to increased human presence, e.g. in tourist areas. In this study, we analysed the escape behavior of the endemic Cyprus rock agama (Laudakia cypriaca) in relation to the observers clothing color. Our results showed that AIDs and FIDs of agamas in tourist areas were significantly shorter than those in non-tourist areas. Moreover, in non-tourist areas, AIDs and FIDs of agamas were significantly longer when the observer wore red clothes, compared to green and grey clothes. Our results may be helpful in planning research taking into account various colored clothing based on expected reptilian reactions. Furthermore, our results may determine the proximity at which humans interact with animals, considering clothing color, to prevent negative impacts especially on rare and protected lizard species.

Leveraging camera traps and artificial intelligence to explore thermoregulation behaviour.

Behavioural thermoregulation has critical ecological and physiological consequences that profoundly influence individual fitness and species distributions, particularly in the context of climate change. However, field monitoring of this behaviour remains labour-intensive and time-consuming. With the rise of camera-based surveys and artificial intelligence (AI) approaches in computer vision, we should try to build better tools for characterizing animals' behavioural thermoregulation. In this study, we developed a deep learning framework to automate the detection and classification of thermoregulation behaviour. We used lizards, the Rough-tail rock agama (Laudakia vulgaris), as a model animal for thermoregulation. We colour-marked the lizards and curated a diverse dataset of images captured by trail cameras under semi-natural conditions. Subsequently, we trained an object-detection model to identify lizards and image classification models to determine their microclimate usage (activity in sun or shade), which may indicate thermoregulation preferences. We then evaluated the performance of each model and analysed how the classification of thermoregulating lizards performed under different solar conditions (sun or shade), times of day and marking colours. Our framework's models achieved high scores in several performance metrics. The behavioural thermoregulation classification model performed significantly better on sun-basking lizards, achieving the highest classification accuracy with white-marked lizards. Moreover, the hours of activity and the microclimate choices (sun vs shade-seeking behaviour) of lizards, generated by our framework, are closely aligned with manually annotated data. Our study underscores the potential of AI in effectively tracking behavioural thermoregulation, offering a promising new direction for camera trap studies. This approach can potentially reduce the labour and time associated with ecological data collection and analysis and help gain a deeper understanding of species' thermal preferences and risks of climate change on species behaviour.

Seasonal Variation in the Thermoregulation Pattern of an Insular Agamid Lizard.

Ectotherms, including lizards, rely on behavioral thermoregulation to maintain their body temperature within an optimal range. The benign climate of islands is expected to favor the thermoregulation efficiency of reptiles throughout their activity period. In this study, we investigated the seasonal variation in thermoregulation in an insular population of the roughtail rock agama (Laudakia stellio) on Naxos Island, Greece. We measured body, operative, and preferred temperatures across three seasons (spring, summer, and autumn), and we evaluated the effectiveness of thermoregulation, using the Hertz index (E). Our results revealed that the effectiveness of thermoregulation was significantly influenced by seasonality. E was quite high in summer (0.97) and spring (0.92), and lowest in autumn (0.81). Accordingly, the quality of the thermal environment was significantly low during autumn, and maximum during summer. However, despite the environmental temperature fluctuations, lizards exhibited remarkable stability in body temperatures. They also adjusted their preferred temperatures seasonally and doubled the thermal niche breadth they occupied during summer, thus enhancing thermoregulation efficiency. Whether or not these adjustments are plastic or fixed local adaptations remains to be explored in further research across multiple years and seasons, including additional insular populations.

Impact of tourism on the vigilance behavior of the Cyprus rock agama (Laudakia cypriaca).

Escape behavior is a common antipredator strategy among wild animals. Here, we investigated the effect of four factors on the vigilance behavior of the endemic Cyprus rock agama (Laudakia cypriaca). Flight initiation distance (FID, the minimum distance to which an observer can approach a lizard before it flees) was measured in relation to the type of location (tourist vs. nontourist area), the observer's starting distance, air temperature, and substrate temperature. We collected data for 39 agamas in tourist areas and 34 of these lizards in nontourist areas. As a whole, the mean starting distance was 10.5 m and the FID was 3.6 m. The average substrate temperature was 34.0°C and the average air temperature 29.6°C. Only the type of area affected the agamas' escape decisions with FID being 1.8 m shorter in tourist areas than in nontourist areas (2.7 m vs. 4.5 m). This is probably due to the habituation of lizards to the presence of humans in the former areas. This study shows that tourism strongly affects the behavior of lizards, which may have consequences for the functioning of the population. Tourists can increase the safety of lizards by creating a human shield to deter predators. Once the tourist season is over, lizards may become more vulnerable to predators.

Mismatches between phenotype and environment shape fitness at hyperlocal scales.

In the era of human-driven climate change, understanding whether behavioural buffering of temperature change is linked with organismal fitness is essential. According to the 'cost-benefit' model of thermoregulation, animals that live in environments with high frequencies of favourable thermal microclimates should incur lower thermoregulatory costs, thermoregulate more efficiently and shunt the associated savings in time and energy towards other vital tasks such as feeding, territory defence and mate acquisition, increasing fitness. Here, we explore how thermal landscapes at the scale of individual territories, physiological performance and behaviour interact and shape fitness in the southern rock agama lizard (Agama atra). We integrated laboratory assays of whole organism performance with behavioural observations in the field, fine-scale estimates of environmental temperature, and paternity assignment of offspring to test whether fitness is predicted by territory thermal quality (i.e. the number of hours that operative temperatures in a territory fall within an individual's performance breadth). Male lizards that occupied territories of low thermal quality spent more time behaviourally compensating for sub-optimal temperatures and displayed less. Further, display rate was positively associated with lizard fitness, suggesting that there is an opportunity cost to engaging in thermoregulatory behaviour that will change as climate change progresses.

Are all islands the same? A comparative thermoregulatory approach in four insular populations

Abstract As ectotherms, lizards, among the best models in thermal studies, are influenced by many abiotic factors. Interestingly, there is a scarcity of data regarding the impact that insularity may have on thermoregulation. Islands, depending their size and altitude, may differ considerably in the thermal conditions they provide to lizards. Here, we focused on a study system comprising islands that differ in morphological characteristics. We worked with four Rock Agama (Laudakia sp.) insular populations, namely Cyprus, Naxos, Delos, and Corfu. We measured body, operative and preferred temperatures and evaluated thermoregulation effectiveness (E). According to our findings, E differed among populations: Corfu received the lowest E (0.45), Cyprus and Naxos achieved median values (0.66 and 0.67, respectively) and lizards from Delos had the most effective thermoregulation (0.85). Our results underline the complex nature of insularity and its effect on saurian thermoregulation and highlight the importance of studying each insular population separately, taking into account the variable features of islands.

Genome of Laudakia sacra Provides New Insights into High-Altitude Adaptation of Ectotherms.

Anan’s rock agama (Laudakia sacra) is a lizard species endemic to the harsh high-altitude environment of the Qinghai–Tibet Plateau, a region characterized by low oxygen tension and high ultraviolet (UV) radiation. To better understand the genetic mechanisms underlying highland adaptation of ectotherms, we assembled a 1.80-Gb L. sacra genome, which contained 284 contigs with an N50 of 20.19 Mb and a BUSCO score of 93.54%. Comparative genomic analysis indicated that mutations in certain genes, including HIF1A, TIE2, and NFAT family members and genes in the respiratory chain, may be common adaptations to hypoxia among high-altitude animals. Compared with lowland reptiles, MLIP showed a convergent mutation in L. sacra and the Tibetan hot-spring snake (Thermophis baileyi), which may affect their hypoxia adaptation. In L. sacra, several genes related to cardiovascular remodeling, erythropoiesis, oxidative phosphorylation, and DNA repair may also be tailored for adaptation to UV radiation and hypoxia. Of note, ERCC6 and MSH2, two genes associated with adaptation to UV radiation in T. baileyi, exhibited L. sacra-specific mutations that may affect peptide function. Thus, this study provides new insights into the potential mechanisms underpinning high-altitude adaptation in ectotherms and reveals certain genetic generalities for animals’ survival on the plateau.

An expanding cityscape and its multi-scale effects on lizard distribution.

Urbanization results in complex and variable changes to environmental conditions, which translate to shifts in selection pressures for organisms. Size of a city as well as the intensity and extent of urbanization can synergistically influence how organisms are impacted. However, less is known about how landscape heterogeneity, rate of land-use change, and scale of urbanization affect species persistence. We evaluate the ways in which urbanization changes the environment and examine how some of these environmental factors influence the presence of the lizard Psammophilus dorsalis (Peninsular rock agama), in Bengaluru, India. Variability in environmental factors across the study area was characterised by measures of habitat composition and diversity, habitat connectivity, rate of habitat change, predation pressure, land surface temperature (LST) and artificial light at night (ALAN), that were derived from remotely sensed and citizen science data. Most of these factors showed high variance across two measures of urbanization: distance from city center and proportion of built-up area. Habitat diversity and ALAN were the only two factors that changed predictably and in a non-linear way, with distance from the city center and proportion of built-up area. We then used a multi-scale approach to examine the relative importance of some these environmental factors at the landscape scale, as well as additional factors at the microhabitat-scale, in predicting the presence and relative abundance of P. dorsalis respectively. At the landscape scale, LST, which is positively correlated with proportion of cropland, predicted lizard presence; whereas at the microhabitat scale, P. dorsalis was more likely to be found in sites with higher proportions of rocks. Overall, we demonstrate that urbanization can result in environmental predictors that do not vary linearly across the urbanization gradient. For the iconic rock agama, many of these environmental factors do not seem to be strong selection pressures that influence their distribution in the expanding cityscape. Whether this urban utilizer can continue to persist with increasing anthropogenic development is uncertain. To better understand drivers of species persistence, we emphasize the importance of quantifying urbanization across multiple axes, considering environmental factors that are relevant to species at different spatial and temporal scales.

Colours of stress in male Indian rock agamas predict testosterone levels but not performance

Rapid physiological colour change offers dynamic signalling opportunities that can reveal distinct information to receivers in different contexts. Information content in dynamic colours, however, is largely unexplored. In males of the Indian rock agama (Psammophilus dorsalis), stressful events, including male-male agonistic interactions, induce a colour change, wherein the dorsal band turns yellow and the lateral bands turn orange. We aimed to determine whether these pigment-based dynamic colours convey information about individual quality. Using an agamid-specific visual model, we first quantified the chromatic and achromatic contrasts of each colour component displayed by males during handling stress, which induces the maximal response of aggression-typical colours. We then measured baseline testosterone levels, morphology (body mass and size), and performance measures (bite force and sprint speed) of these lizards. Chromatic contrasts of the dorsal yellow and lateral orange bands, individually and relative to each other (internal pair), were negatively correlated with testosterone levels, while the chromatic contrast of the internal pair was positively correlated with body condition. The lack of an association between colour contrasts and both bite force and sprint speed indicate that the conspicuousness of colours expressed during stressful events, such as agonistic interactions, do not reveal male performance ability. Despite our expectations of a positive relationship with testosterone, morphology (body condition), and performance (bite force, sprint speed), we find that for P. dorsalis, the conspicuousness of stress-induced colours provide only some information about individual quality. We speculate that the dynamicity of physiological colours may influence their function as content-containing signals in social interactions.

Lichens and animal camouflage: some observations from central Asian ecoregions

Camouflage is a fitness-relevant trait that supports survival and fosters evolutionary adaptation by which animals match their body pattern to a background setting. Lichens are among the most common of these backgrounds that several animal species use for camouflage. Lichens are omnipresent and grow in wide arrays of colorations and compositions. Their composition and phenotypic diversity might facilitate cryptic coloration and habitat matching by various animal species. Here, we describe the role of lichens in providing camouflage to various animal species in central Asian and Caucasus mountain ecoregions, which are categorized as global biodiversity hotspots. Despite multiple ecological studies, no information is available on the role of this regions‘ lichen diversity in providing animal camouflage. Casual field observations of lichen camouflage are reported for four (one mammal and three reptile) species: the Persian Leopard’s Panthera pardus saxicolor body coat seems to closely match the colors and patterns of saxicolous lichens (Acarospora sp. and Circinaria sp.) in their habitat. A similar background matching pattern was observed in both morphs of the Caucasian Rock Agama Paralaudakia caucasia upon crustose lichens: Caloplaca spp., Circinaria spp., and the Radde’s Rock Lizard Darevskia raddei to the crustose lichens Acarospora sp. and Caloplaca sp. Likewise, the Horny-scaled Agama’s Trapelus ruderatus grey matches with the color of multiple lichens (Lecanora spp., Circinaria spp., Protoparmeliopsis spp., Rinodina spp., and Anaptychia spp.). Our observations preliminarily suggest that lichens play an important role for species of different trophic levels, ensuring adaptation and survival through camouflage. We call for more field-based empirical and experimental studies in various terrestrial ecosystems in other parts of the world to test the role of lichens in local adaption and evolutionary plasticity of regional species.

The correct name for the North African rock lizard is Agama bibronii A. Duméril in Duméril & Duméril, 1851, not Agama impalearis Boettger, 1874 (Reptilia, Squamata)

Over half a century ago, Mertens (1955) noted that the name Agama bibronii A. Duméril in Duméril & Duméril, 1851 for a North African agamid lizard species was preoccupied by Trapelus (Psammorrhoa) bibronii Fitzinger, 1843, a species inhabiting South Africa. He consequently stated that the next available name for Agama bibronii ‘Duméril, 1851’, namely Agama colonorum var. impalearis Boettger, 1874 should be applied to this taxon. Until today, the herpetological literature contains examples where either Agama bibronii ‘Duméril, 1851’ or Agama impalearis Boettger, 1874 is used to denominate the North African rock agama. However, an apparently overlooked ruling by the Commission suppressed the name Trapelus (Psammorrhoa) bibronii Fitzinger, 1843, so that Agama bibronii A. Duméril in Duméril & Duméril, 1851 is the valid name for the North African rock agama.

Urban lizards use sleep sites that mirror the structural, thermal, and light properties of natural sites

Global change processes such as urbanization are likely to affect sleep behavior, by altering abiotic (e.g., thermal and illumination) and biotic conditions (e.g., predation pressure) that influence sleep. However, little is known of how sleep behavior responds to urbanization and whether this response is flexible or conserved across populations. We quantified sleep site characteristics of the peninsular rock agama Psammophilus dorsalis in Bangalore city and surrounding rural areas. We find that P. dorsalis in urban areas display remarkable behavioral flexibility in response to the novel stressor of artificial light at night, being nine times more likely to use covered sleep sites that limit illumination, compared to lizards in rural areas. However, sleep sites in both populations were highly conserved in terms of substrate type (i.e., rocky with high surface rugosity) and their thermal properties. Our findings support behavioral amelioration of potentially adverse effects of night light in urban areas, even within the restricted availability of preferred substrates as sleep sites. Our study is one of the first to comprehensively compare sleep behavior in rural and urban areas and demonstrate substantial behavioral flexibility. The role of sleep behavior in the coping strategies of animals to urbanization needs further research attention. Sleep is essential to animal life, yet it imposes certain costs such as making sleeping individuals vulnerable to predators. “Where” an animal sleeps (or its sleep site) is therefore important to ensure safety from predators but also to provide conducive environmental conditions. Cities can transform the availability of ideal sleep sites and can alter their thermal properties, in addition to being intensely illuminated by night light that hampers sleep. In this study, we compared sleep site characteristics of rural and urban populations of the peninsular rock agama Psammophilus dorsalis. We find that urban lizards sleep in sheltered sleep sites that shield them from night light but are highly dependent on rough, rocky substrates in both the city and rural areas. The remarkable flexibility in sleep behavior displayed by urban lizards is likely to help them cope in a city.

Distribution Modeling of the Caucasian Rock Agama Paralaudakia caucasia (Eichwald, 1831), (Sauria: Agamidae) Based on an Updated Data Set

We present results of analysis and predictions of the potential distribution of the Caucasian rock agama Paralaudakia caucasia (Eichwald, 1831), based on an updated data set and using a distribution model generated with software Maxent (www.cs.princeton.edu/~schapire/maxent). The model was based on an updated data set of 238 localities, including 74 new records from Daghestan and Tajikistan. According to the generated model, the most suitable habitats of the Caucasian rock agama Paralaudakia caucasia are located in the Caucasus (southeastern Ciscaucasia and eastern Transcaucasia), south Turkmenistan and north-eastern Iran.

Dumpsters and other anthropogenic structures as habitat for invasive African rock agama lizards in Florida

Invasive species often use habitat differently than native species and can benefit by occupying underutilized habitats during the invasion process. The Peter’s Rock Agama (Agama picticauda)—native to savannahs of sub-Saharan Africa—is successfully invading urban habitats in Florida, USA. During a field trip in urban southern Florida, we observed apparently high A. picticauda abundance around dumpsters used for human refuse, potentially because dumpsters provide refuge, thermoregulatory opportunities, abundant arthropod prey, and harbor few competitors. In this study, we surveyed abundance and built resource selection functions to better understand habitat use of A. picticauda in urban southern Florida. We tested whether hypothesized habitat features predictably influenced the abundance and occupancy of A. picticauda among sites and whether individuals used specific habitat features within sites. Across sites, we found A. picticauda abundance was positively correlated with the number of dumpsters, and, within sites, dumpsters were preferentially selected as habitat. Similarly, we also found two other anthropogenic structures, building crevices and electrical units, were positively selected habitats at population and individual scales. We hypothesize that dumpsters, crevices, and electrical units are selected resources because they are underutilized habitats by other species and they provide refuge, beneficial thermoregulatory opportunities, and in the case of dumpsters, foraging opportunities. Our study provides the first quantitative assessment of urban habitat use by non-native A. picticauda, and supports the importance of human structures as habitat. Our results suggest the intriguing possibility that the A. picticauda invasion in Florida may be exploiting a vacant niche in urban habitats during the invasion process.

Distance from the Tourist Trail and Daylight Condition Affect the Abundance of Mwanza Flat-Headed Rock Agama (Agama mwanzae) in Saanane National Park, Tanzania

For newly established protected areas, it is important to document the abundance, structure and distribution of the species within the landscape. Here we assessed the variation in total abundance as well as female, male and juvenile abundance of Mwanza flat-headed rock agama (Agama mwanzae) in Saanane National Park, Tanzania, in relation to daylight condition (sunny and non-sunny) and proximity to humans. Twenty-three points of 50-meter radius were randomly placed and thoroughly searched for A. mwanzae. Of 364 individual Mwanza flat-headed rock agamas recorded, 85% were adults and 15% were juveniles. Among adults, 45% were males and 55% were females. Daylight condition was observed to affect total abundance and the abundance of females, males and juveniles of A. mwanzae, with higher abundance being in sunny periods as compared to non-sunny periods. Distance from the tourist trail was the best predictor for total abundance and the abundance of females and juveniles but not males, with abundance decreasing moving away from the tourist trail. Therefore, we suggest these factors be considered when surveying agamas elsewhere.

Peters’s Rock Agama in Florida

There is growing public awareness of Peters’s rock agama in Florida. Adult male agama are highly visible because of their bright red coloration. Juveniles and females are much less colorful. Adult agama are large, fast moving reptiles. This document provides background information about the introduction of agama to Florida as well as biology, conservation issues and management recommendations.

First Record of <i>Stellagama stellio</i> (Squamata: Agamidae) from Karpathos Island, Greece

In this note we report for the first time the occurrence of the Roughtail Rock Agama (Stellagama stellio) from Kaprathos Island, Greece. Greece represents the westernmost range limit of the animal and hosts its only European populations. Although Karpathos is a relatively well-studied island in terms of its herpetofauna, this is the second remarkable herpetological finding within the past year, following the rediscovery of the Grass Snake more than 50 years after it was first described from the island. This report for S. stellio expands the range of the species and it is added to a long series of new records in the Greek herpetofauna that occurred during the last few years.

The Bogert Effect and environmental heterogeneity.

A classic question in evolutionary biology is whether behavioral flexibility hastens or hinders evolutionary change. The latter idea, that behavior reduces the number of environmental states experienced by an organism and buffers that organism against selection, has been dubbed the "Bogert Effect" after Charles Bogert, the biologist who first popularized the phenomenon using data from lizards. The Bogert Effect is pervasive when traits like body temperature, which tend to be invariant across space in species that behaviorally thermoregulate, are considered. Nevertheless, behavioral thermoregulation decreases or stops when spatial variation in operative temperature is low. We compared environmental temperatures, thermoregulatory behavior, and a suite of physiological and morphological traits between two populations of the southern rock agama (Agama atra) in South Africa that experience different climatic regimes. Individuals from both populations thermoregulated efficiently, maintaining body temperatures within their preferred temperature range throughout most of their activity cycle. Nevertheless, they differed in the thermal sensitivity of resting metabolic rate at cooler body temperatures and in morphology. Our results support the common assertion that thermoregulatory behavior may prevent divergence in traits like field-active body temperature, which are measured during periods of high environmental heterogeneity. Nevertheless, we show that other traits may be free to diverge if they are under selection during times when environments are homogenous. We argue that the importance of the Bogert Effect is critically dependent on the nature of environmental heterogeneity and will therefore be relevant to some traits and irrelevant to others in many populations.

The complete mitochondrial genomes of Laudakia Papenfussi (Iguania; Agamidae)

The Papenfuss' Rock Agama Laudakia papenfussi is an endemic species in the Tibet Autonomous Region of China. The complete mitochondrial genome sequence of this species was determined by shotgun sequencing. The total length of mitogenome is 17,005 bp and its base composition was 37.3% for A, 23.9% for T, 12.5% for G, and 26.3% for C, which contains 13 protein-coding genes, 22 tRNA genes, 2 ribosome RNA genes, and 2 control regions. The phylogenetic tree of L. papenfussi and 15 other related species was reconstructed using maximum likelihood (ML) methods. The mitogenome sequence presented here will be useful to understand the phylogenetic relationships of Laudakia.

Genetic variation and cryptic lineage diversity of the Nigerian red-headed rock agama Agama agama associate with eco-geographic zones.

Nigeria is an Afrotropical region with considerable ecological heterogeneity and levels of biotic endemism. Among its vertebrate fauna, reptiles have broad distributions, thus, they constitute a compelling system for assessing the impact of ecological variation and geographic isolation on species diversification. The red-headed rock agama, Agama agama, lives in a wide range of habitats and, thus, it may show genetic structuring and diversification. Herein, we tested the hypothesis that ecology affects its genetic structure and population divergence. Bayesian inference phylogenetic analysis of a mitochondrial DNA (mtDNA) gene recovered four well-supported matrilines with strong evidence of genetic structuring consistent with eco-geographic regions. Genetic differences among populations based on the mtDNA also correlated with geographic distance. The ecological niche model for the matrilines had a good fit and robust performance. Population divergence along the environmental axes was associated with climatic conditions, and temperature ranked highest among all environmental variables for forest specialists, while precipitation ranked highest for the forest/derived savanna, and savanna specialists. Our results cannot reject the hypothesis that niche conservatism promotes geographic isolation of the western populations of Nigerian A. agama. Thus, ecological gradients and geographic isolation impact the genetic structure and population divergence of the lizards. This species might be facing threats due to recent habitat fragmentation, especially in western Nigeria. Conservation actions appear necessary.