Urosaurus Research Articles

Intraspecific variation in tree lizard escape behaviour in relation to habitat and temperature

Abstract Optimal escape theory has proven useful for understanding the dynamics of antipredator behaviour in animals; however, approaches are often limited to single-population studies. We studied how the escape behaviour of tree lizards (Urosaurus ornatus) varied across a disturbance gradient. We also considered how sex, body temperature, and perch temperature affected their escape decisions. Both sexes exhibited similar response patterns; however, lizards in the most-disturbed habitat, as well as cooler (body or perch temperature) lizards, initiated escape earlier (but did not flee further) than other animals. Increased wariness as indicated by earlier escape suggests that frequently-disturbed, more-open localities may be stressful habitats for species like U. ornatus. In addition, because cooler temperatures limit locomotor performance capacity, escape decisions should also depend on a species’ thermal ecology. Overall, we stress the importance of multi-population approaches for capturing the variety of ways species adaptively respond to the threat of predation across habitat gradients.

Reproductive cycle and maturation of Swinhoe's tree lizard (Diploderma swinhonis (Günther, 1864)) in Hyuga City, Miyazaki Prefecture, Japan.

Swinhoe’s tree lizard (Diploderma swinhonis) is an arboreal agamid that is native to Taiwan. The species has been introduced to some areas of Japan and is regarded as an invasive alien species. In 2016, a nonnative population of D. swinhonis was discovered in Hyuga City, Miyazaki Prefecture, Japan, but little information was available on the ecology of the population at the time. The main purpose of this study was therefore to investigate the reproductive cycle and maturation of this population. Field research was conducted from 2017 to 2019, and 764 lizards were collected. Euthanized lizards were dissected and the reproductive organs were examined to determine the reproductive period, clutch size, clutch frequency and size at sexual maturity. Females with oviductal eggs or vitellogenic ovarian follicles were observed from May to October. Clutch size ranged from 2 to 8, and clutch frequency was more than twice a year. In males, spermiogenesis started in early May and testicular regression was observed in September. Males with spermatozoa in the epididymides were found from May to November. Minimum snout-vent length at sexual maturity was 50.2 mm in females and 53.0 mm in males. Comparisons of the findings of this study and reports from Taiwan suggest that the nonnative population of D. swinhonis in Hyuga City has a higher fecundity than populations in Taiwan. It is therefore considered necessary to exterminate the population in Hyuga City before this species colonizes other areas.

Iridescence and thermal properties of Urosaurus ornatus lizard skin described by a model of coupled photonic structures

This research shows that the morphological characteristics of the external microstructure of the beautiful skin of the Urosaurus ornatus lizard contribute to the explanation of the origin of their iridescent and thermal properties. High-resolution scanning electron microscopy studies revealed that the skin surface of the U. ornatus lizard is constituted by a semi-ordered array of hexagonal photonic crystals with sub-micrometric structural parameters. The iridescence properties of the ventral patch and dorsal surface of the U. ornatus lizard were numerically simulated modeling both surfaces by a set of coupled photonic crystals with structural parameters proposed from statistical measurements of the lattice parameter and holes diameter of its skin surface. The dorsal surface showed the ability to reflect visible light and at least in a significant range the ultraviolet and near infrared radiation. A complete photonic band gap for the transverse magnetic polarization mode of the incident light in both dorsal and ventral surfaces was predicted by calculations. The spectral reflectance and the structure of photonic bands obtained explain the reflection of the infrared radiation by the dorsal surface which might help to the thermoregulation of the lizard body. The results obtained suggest that the selective reflection of incident light performed by the photonic structural array defined on the skin surface of the U. ornatus has a significant contribution to its apparent color.

Ornate tree lizards (Urosaurus ornatus) thermoregulate less accurately in habitats of high thermal quality.

Temperature plays a critical role for ectotherm performance and thus for fitness. Ectotherms, since unable to regulate their body temperature internally, use behavioural thermoregulation to maintain their body temperature within a range that maximizes performance. According to the cost-benefit model of thermoregulation, investment into thermoregulation is dictated by the trade-off between the costs and benefits of thermoregulating. The thermal quality of the environment is a major cost of thermoregulation because it directly affects the amount of time and energy that must be invested by an individual to achieve and maintain an optimal body temperature. Thus, in habitats of poor thermal quality, lizards should thermoregulate less. Using Urosaurus ornatus living at 10 sites each straddling two adjacent habitats (wash and upland), we tested the hypothesis that investment in thermoregulation is dependent on the thermal quality of the habitat. We found that the wash habitat had higher thermal quality indicated by a longer duration when optimal body temperatures could be reached. Lizards had more accurate body temperatures in the upland despite its poorer thermal quality. These results suggest that discrepancies in thermal quality between adjacent habitats affect investment in thermoregulation by lizards, but in a direction opposite to the main prediction of the cost-benefit model of thermoregulation.

Antagonistic Responses of Exposure to Sublethal Temperatures: Adaptive Phenotypic Plasticity Coincides with a Reduction in Organismal Performance.

A fitness benefit of phenotypic plasticity is the ability of an organism to survive short-term, deleterious environmental fluctuations. Yet the influence of selection on plasticity in modulating shifts in phenotypic traits remains unclear. Short-term phenotypic plasticity in thermal tolerance traits is attained by exposure to sublethal hot or cold temperatures (i.e., the hardening response). Heat hardening is expected to buffer organisms from the unpredictability of extreme thermal fluctuations in the environment so as to minimize interruptions in activity and enhance survival. However, exposure to sublethal temperatures might entail other phenotypic costs that constrain or inhibit the prolonged use of hardening responses across longer timescales. Here we estimated the onset of the heat hardening response, physiological and behavioral shifts during heat hardening, and geographic variation in heat hardening using tree lizards (Urosaurus ornatus). Peak heat hardening occurred 6 h after exposure to sublethal temperatures. We found that both preferred body temperatures and locomotor performance diminished following exposure to sublethal temperatures, and performance levels did not approach preexposure levels until after the peak hardening response. We also found support for intraspecific variation in the hardening response along an environmental gradient, where populations in more thermally variable environments exhibited stronger plastic responses and populations with higher baseline heat tolerances exhibited weaker plastic responses. Sublethal temperature exposure might induce adaptive plasticity in thermal tolerance; however, we find that these responses entail other phenotypic shifts that might curtail chronic reliance on plasticity in thermal traits as a mechanism of responding to changes in thermal environments induced by climate warming.

Spatiotemporal variation in thermal niches suggests lability rather than conservatism of thermal physiology along an environmental gradient

Abstract Temperature variation throughout a species range can be extensive and exert divergent spatiotemporal patterns of selection. The estimation of phenotypic differences of populations along environmental gradients provides information regarding population-level responses to changing environments and evolutionary lability in climate-relevant traits. However, few studies have found physiological differentiation across environmental gradients attributable to behavioural thermoregulation buffering physiological evolution. Here, we compared thermal sensitivity of physiological performance among three populations of the ornate tree lizard (Urosaurus ornatus) along a 1100 m elevational gradient in southeastern Arizona across years in order to determine whether spatial differences in thermal environments are capable of driving local physiological differentiation. Lizards exhibited significant population-level differences in thermal physiology. The thermal traits of lizards at low elevations included warmer body temperatures and higher preferred and critical thermal temperatures. In contrast, lizards at higher elevations had cooler body temperatures and lower preferred and critical thermal temperatures. Populations also exhibited differences in the optimal temperature for performance and thermal performance breadth. The direction of population variation was consistent across years. Environmental gradients can provide model systems for studying the evolution of thermal physiology, and our study is one of the first to suggest that population differentiation in thermal physiology could be more prominent than previously thought.

Systematics of reptile-associated scale mites of the genus Pterygosoma (Acariformes: Pterygosomatidae) derived from external morphology.

The phylogeny of the mite genus Pterygosoma Peters, 1849 (Acariformes: Pterygosomatidae), permanent parasites of lizards of the families Agamidae, Gerrhosauridae and Liolaemidae (Reptilia: Squamata), was inferred with maximum parsimony, successive weighting and implied weighting approaches based on 182 characters of 48 ingroup and 12 outgroup species. All undertaken analyses questioned the monophyly of the genus. Based on this research, Pterygosoma includes 56 mite species associated with agamas from Africa and Asia (Sauria: Agamidae). Within the genus seven natural species groups were found: mutabilis, inermis, melanum, caucasica, fimbriata, singularis and foliosetis; 13 species of the genus were not assigned to any of the groups due to their unique morphological characters. For the ligare group of the subgenus Pterygosoma s. str. (7 species) associated with the South American tree lizards from the family Liolaemidae, a new genus, Neopterygosoma gen. nov., is established. The subgenus Gerrhosaurobia Lawrence, 1959 (3 species) associated with the African plated lizards of the family Gerrhosauridae is elevated to the genus rank. Diagnoses for the three genera are presented. Historical associations are reconstructed by fitting the obtained mite tree into the host topology on the family level. Results of coevolutionary analysis highlight the coincidence of both trees. The studies suggest that the ancestor of the genus Pterygosoma switched from the hosts of Gerrhosaurobia i.e. from the plated lizards (Gerrhosauridae) to the agamas (Agamidae), and the genus Pterygosoma has its biogeographic origin in North Africa, and colonized Asia via the Arabian Peninsula, which is congruent with the historical biogeography of its hosts.

Notes on the feeding habits of the Okinawan fishing spider, Dolomedes orion (Araneae: Pisauridae), in the southwestern islands of Japan

Fishing spiders, Dolomedes Latreille, 1804 (Pisauridae), are thought to be important predators in semi-aquatic ecosystems, but relatively few studies have investigated feeding ecology of Asian species. Here, we report on the diet of the Okinawan fishing spider, Dolomedes orion Tanikawa, 2003, the largest cursorial spider in Japan, based upon field observations on Amami Oshima Island in Kagoshima Prefecture and a literature review. A total of 13 predation events were observed in field surveys and 10 records were found in the literature. Together, these indicate the consumption of a broad range of food items from arthropods to vertebrates, e.g., insects, harvestman, conspecific spiders, crustaceans (freshwater crab and prawn), two species of endemic frogs (Rana ulma, Odorrana narina), and an Okinawa tree lizard (Japalura polygonata polygonata). Because this species has substantial energy demands for growth, large prey items such as crustaceans and vertebrates seem to be its primary food resources with 10 of 23 prey items [= 43%] belonging to these two large-sized prey groups.

Tree lizard (Urosaurus ornatus) growth decreases with population density, but increases with habitat quality.

Habitat selection models can explain spatial patterns in the relative abundance of animals in different habitats based on the assumption that fitness declines as density in a habitat increases. Ectotherms, such as lizards, may not follow predictions of density-dependent habitat selection models because temperature, which is unaffected by density, strongly influences their habitat selection. If competition for limited resources decreases fitness, then crowding should cause a decrease in body size and growth rates. We used skeletochronology and body size data from tree lizards (Urosaurus ornatus) at six sites that each spanned two habitats varying in quality to test the hypothesis that habitat selection is density dependent because growth is limited by competition for resources and by habitat quality. First, we tested that the maximum body size of lizards decreased with higher densities in a habitat by comparing growth between sites. Second, we tested whether body size and growth were higher in the habitat with more resources by controlling for density in a habitat and comparing growth between habitats in different sites. We found evidence of density-dependent growth in females, but not in males. Females in more crowded sites reached a smaller maximum size. Females in the higher quality habitat also grew larger than females in the lower quality habitat after controlling for differences in density between the habitats. Therefore, we found partial support for our hypothesis that competition for resources limits growth and causes density-dependent habitat selection.

Experimental removal reveals only weak interspecific competition between two coexisting lizards

Competition for resources is an important mechanism that shapes ecological communities. Interspecific competition can affect habitat selection, fitness, and abundance in animals. We used a removal experiment and mark–recapture to test the hypothesis that competition with the larger and more abundant Striped Plateau Lizard (Sceloporus virgatus H.M. Smith, 1938) limits habitat selection, fitness, and abundance in Ornate Tree Lizards (Urosaurus ornatus (Baird in Baird and Girard, 1852)). Ornate Tree Lizards in the plots where Striped Plateau Lizards were removed switched between habitat types more frequently and moved farther than Ornate Tree Lizards in control plots. However, there were no significant changes in the relative densities of Ornate Tree Lizards in each habitat type or in microhabitat use. We also found no changes in growth rates, survival, or abundance of Ornate Tree Lizards in response to the removal of Striped Plateau Lizards. Our results suggest that interspecific competition was not strong enough to limit habitat use or abundance of Ornate Tree Lizards. Perhaps interspecific competition is weak between coexisting species when resource levels are not severely depleted. Therefore, it is important to consider environmental conditions when assessing the importance of interspecific competition.

Local adaptation of tree lizards to canyon dwelling

How and under what situations populations adapt to local conditions remains a key question in evolutionary biology. This study tests if the particular morphology of a population of Tree lizards, Urosaurus ornatus, located in a canyon on the margin of the species range represents an adaptation to canyon habitat. Morphology was compared across 40 populations showing that relative hind limb length, tail length, and mass were all outliers for this population. The function of the relatively longer hind limbs, tail, and lower mass was proposed to be for better sprinting ability on the sheer canyon walls that provide the only available habitat structure for this population. Partial least squares regression found significant effects of tail length on top speed on a broad, steep surface. Partial least squares logistic regression identified significant effects of tail length on survival as well in males but not females of this population. Another canyon population of Tree lizards with access to alternative substrates (trees) showed no evidence of selection on the same morphological features. Ancestral state reconstruction using a phylogeny inferred for 21 populations found that the unique morphology of the focal population was evolutionarily derived compared to closely related populations and so likely arose under the present environmental conditions. Population genetic structure also supported the process of adaptive divergence as there was no evidence for migration and/or a recent genetic bottleneck in the focal population. Lizards in this population appear to have responded to selection allowing them to become specialists for running on canyon walls while other canyon populations with access to a greater variety of habitat structure have not.

Male throat colour polymorphism is related to differences in space use and in habitat selection in tree lizards

AbstractHabitat selection is the disproportionate use of some habitats relative to their availability and is used by animals to maximize fitness. Habitat selection has been the dominant framework for predicting the spatial distribution of animals, but different habitat selection strategies can occur within a population when there are physical or behavioural differences between individuals. Colour polymorphism is often linked to differences in other behavioural and morphological traits, and may therefore affect habitat selection strategy. Male ornate tree lizards (Urosaurus ornatus) exhibit a throat colour polymorphism associated with differences in behaviour and in reproductive strategy. Blue‐throated males are dominant and defend home ranges containing several females; orange‐throated males are either nomadic or sedentary and do not defend territories; and yellow‐ or green‐throated males are reproductive parasites that sneak copulations with females. We tested the hypothesis that throat colour in tree lizards affects habitat selection and space use with mark‐recapture data collected from 10 sites in the Chiricahua Mountains of southeastern Arizona, USA. We found that males with green throats moved more than males with blue throats, and that males with orange throats occupied smaller home ranges. Male ornate tree lizards were closer to the highest quality habitat than if their spatial distribution was random, and green‐throated males had a more marked preference for the highest quality habitat than blue‐throated males. We found no difference in the departures of body temperatures from the preferred body temperature range between males of different throat colours. Survival rates were similar for blue‐, green‐ and orange‐throated males. We demonstrated that throat colour polymorphism in ornate tree lizards is related to habitat selection strategy and this may help maintain the colour polymorphism.

Distinguishing discrete polymorphism from continuous variation in throat colour of tree lizards, Urosaurus ornatus

Distinguishing discrete polymorphism from continuous variation in throat colour of tree lizards, Urosaurus ornatus

Male mate choice and the potential for complex mating dynamics in the tree lizard (Urosaurus ornatus)

AbstractA growing body of literature is recognizing that males may also play a role in the mating process by behaving non‐randomly toward potential female mates during courtship. In numerous species, discrete color polymorphisms in males are inferred to represent alternative mating tactics, which often correspond with concomitant asymmetries in ecology and behavior. In terms of their mating behavior, these ecological outcomes of a color polymorphism should affect a morph's likelihood and frequency of encountering females in a population, possibly favoring the evolution of morph‐specific mating preferences. Knowledge of how male morphs contribute to a species’ overall mating dynamics will improve our understanding of how sexual selection shapes phenotypic diversity in color polymorphic systems. We conducted a mate choice experiment to evaluate the extent and morph specificity of non‐random mating preferences by male ornate tree lizards, Urosaurus ornatus. We observed the behavior of blue and yellow males in an experimental arena in response to a choice between an orange or yellow female. We found that blue males preferred yellow females over orange females, and although yellow males visited females more often than blue males overall, their attention was not morph‐specific. Given male morph differences in choosiness, and their differences in social dominance, we conclude that female throat color may be partly under sexual selection in U. ornatus. However, a lack of concordance between male and female mating preferences (drawn from an earlier study) suggests that overall mating dynamics may serve to maintain, rather than enhance, color morph differences in this species.

Geometric Morphometric Differentiation of Two Western USA Lizards (Phrynosomatidae: Squamata):Uta stansburianaandUrosaurus ornatus, with Implications for Fossil Identification

Squamate fossil identification has been challenging due to the incomplete understanding and sometimes complete lack of osteological research of extant species. Here we compared the maxilla of two similar species of phrynosomatids: Uta stansburiana (Common Side-blotched Lizard) and Urosaurus ornatus (Ornate Tree Lizard). Through landmark-based geometric morphometric analyses, we determined which characters significantly separated the two species. A principle component analysis (PCA) and a stepwise discriminant function analysis (DFA) were conducted, in which we compared 15 landmarks between U. stansburiana and U. ornatus. Both the PCA and stepwise DFA showed separation between the two species. The stepwise DFA selected five of the 15 characters as statistically significant, three of which are considered apomorphies and show promise for fossil identification. The first character is in the ventral region of the posterior maxilla process; U. ornatus has a defined notch, whereas U. stansburiana does not. The second and third characters are in the anterior portion of the maxilla, which is curved dorsally in U. stansburiana, whereas U. ornatus shows no curving. The results of this study are used to identify fossil Uta vs Urosaurus, but more analyses need to be conducted on other phrynosomatid species for comprehensive identification.

Density‐dependent habitat selection predicts fitness and abundance in a small lizard

Density‐dependent habitat selection has been used to predict and explain patterns of abundance of species between habitats. Thermal quality, a density‐independent component of habitat suitability, is often the most important factor for habitat selection in ectotherms which comprise the vast majority of animal species. Ectotherms may reach high densities such that individual fitness is reduced in a habitat due to increased competition for finite resources. Therefore, density and thermal quality may present conflicting information about which habitat will provide the highest fitness reward and ectotherm habitat selection may be density‐independent. Using ornate tree lizards Urosaurus ornatus at 10 sites each straddling two adjacent habitats (wash and upland), we tested the hypothesis that habitat selection is density‐dependent even when thermal quality differs between habitats. We first tested that fitness proxies decline with density in each habitat, indicating density‐dependent effects on habitat suitability. We also confirmed that the two habitats vary in suitability (quantified by food abundance and thermal quality). Next, we tested the predictions that habitat selection depends on density with isodar analyses and that fitness proxies are equal in the two habitats within a site. We found that monthly survival rates decreased with density, and that the wash habitat had more prey and higher thermal quality than the upland habitat. Lizards preferred the habitat with more food and higher thermal quality, lizard densities in the two habitats were positively correlated, and fitness proxies of lizards did not differ between habitats. These patterns are consistent with density‐dependent habitat selection, despite differences in thermal quality between habitats. We expect that density‐dependent habitat selection is widespread in terrestrial ectotherms when densities are high and temperatures are close to their optimal performance range. In areas where thermal quality is low, however, we expect that depletable resources, such as food, become less limiting because assimilating resources is more difficult.

Physiological Consequences of Food Limitation for a Color Polymorphic Lizard: Are Coping Responses Morph-Specific?

Color polymorphism in animals often reflects discrete intraspecific variation in suites of traits linked with survival and reproductive success, as well as an ability to exploit diverse habitat types. Given those considerations, it has been hypothesized that color polymorphic species may be better able to withstand broad-scale environmental disturbances compared to monomorphic taxa. An assumption underlying this hypothesis is that morphs differ in their responses to the consequences of a disturbance. We test whether two color morphs of the Ornate Tree Lizard (Urosaurus ornatus) differ in their physiological responses to a likely outcome of a habitat disturbance, food limitation. We subjected blue and yellow morph U. ornatus to one of two feeding treatments (control [fed every other day] and food-limited [fed every five days]) and monitored their changes in body mass and stamina capacity for the next four weeks. We found that in general, food-limited males lost mass and had reduced stamina over time. Altho...

Riding the Kuroshio Current: Stepping stone dispersal of the Okinawa tree lizard across the East Asian Island Arc

AbstractAimLocated hundreds of kilometres offshore of continental mainland Asia, the extremely high level of land vertebrate endemism in the East Asian Island Arc provides an excellent opportunity to test hypotheses regarding biogeographic processes and speciation. In this study, we aim to test alternative explanations for lineage diversification (vicariance versus dispersal models), and further develop a temporal framework for diversification in our focal taxon, which is consistent with the known age of these islands. We achieve these tests by investigating the historical biogeography of the Okinawa tree lizard (Japalura polygonata), one of the few widely‐distributed reptiles across this archipelago.LocationThe East Asian Island Arc: (1) Central Ryukyu (Amami and Okinawa groups); (2) Southern Ryukyu (Miyako and Yaeyama groups); (3) Taiwan and adjacent islands.MethodsA total of 246 tissues were sampled from 10 localities in the Ryukyu archipelago and 17 localities in Taiwan, covering the entire distributional range of this species, including all subspecies. DNA sequences of the mitochondrial cytochrome b, 16S ribosomal RNA, nuclear BACH‐1 and RAG‐1 genes (total: 4,684 bp) were obtained from these samples. We used maximum likelihood and Bayesian methods to infer phylogeny and divergence time, and used a model‐fitting method of biogeographical inference to estimate ancestral range evolution.ResultsMultiple lines of evidence combine to identify a general pattern of dispersal‐mediated diversification northward through the archipelago, following initial dispersal from Taiwan. These included (1) a phylogenetic estimate, revealing a sequential, south‐to‐north branching pattern; (2) ancestral range estimation, inferring multiple overseas dispersals and subsequent colonization of new landmasses; and (3) a reduction in genetic variation observed in successively‐diverging lineages, decreasing from Taiwan northward, towards more remote islands. These results provide strong statistical support for an interpretation of successive bouts of dispersal via the powerful, well‐documented, south‐to‐north Kuroshio Current. Estimation of divergence times suggests that most clades in southern Ryukyu and Taiwan diverged early, giving rise to lineages that have remained isolated, and that more recently‐diverged lineages then colonized northward to subsequently occupy the landmasses of the Central Ryukyu archipelago.Main conclusionsOur general inference of biogeographic history in Japalura polygonata suggested that this species originated on Taiwan and the Yaeyama group, and arrived at its current distribution in Miyako, Okinawa, Toku and Amami islands by a series of stepping‐stone dispersals, which we report for the first time for a terrestrial vertebrate endemic to this region.

Distinguishing discrete polymorphism from continuous variation in throat colour of tree lizards, Urosaurus ornatus

Distinguishing discrete polymorphism from continuous variation in throat colour of tree lizards, Urosaurus ornatus

Too hard to swallow: a secret secondary defence of an aposematic insect.

Anti-predator strategies are significant components of adaptation in prey species. Aposematic prey are expected to possess effective defences that have evolved simultaneously with their warning colours. This study tested the hypothesis of the defensive function and ecological significance of the hard body in aposematic Pachyrhynchus weevils pioneered by Alfred Russel Wallace nearly 150 years ago. We used predation trials with Japalura tree lizards to assess the survivorship of 'hard' (mature) versus 'soft' (teneral) and 'clawed' (intact) versus 'clawless' (surgically removed) weevils. The ecological significance of the weevil's hard body was evaluated by assessing the hardness of the weevils, the local prey insects, and the bite forces of the lizard populations. The existence of toxins or deterrents in the weevil was examined by gas chromatography-mass spectrometry (GC-MS). All 'hard' weevils were instantly spat out after being bitten once and survived attacks by the lizards. In contrast, the 'soft' weevils were chewed and subsequently swallowed. The results were the same regardless of the presence or absence of the weevil's tarsal claws. The hardness of 'hard' Pachyrhynchus weevils was significantly higher than the average hardness of other prey insects in the same habitat and the mean bite forces of the local lizards. The four candidate compounds of the weevil identified by GC-MS had no known toxic or repellent functions against vertebrates. These results reveal that the hardness of aposematic prey functions as an effective secondary defence, and they provide a framework for understanding the spatio-temporal interactions between vertebrate predators and aposematic insect prey.