3D printed models are an accurate, cost-effective, and reproducible tool for quantifying terrestrial thermal environments.

Predicting ecological responses to rapid environmental change has become one of the greatest challenges of modern biology. One of the major hurdles in forecasting these responses is accurately quantifying the thermal environments that organisms experience. The distribution of temperatures available within an organism's habitat is typically measured using data loggers called operative temperature models (OTMs) that are designed to mimic certain properties of heat exchange in the focal organism. The gold standard for OTM construction in studies of terrestrial ectotherms has been the use of copper electroforming which creates anatomically accurate models that equilibrate quickly to ambient thermal conditions. However, electroformed models require the use of caustic chemicals, are often brittle, and their production is expensive and time intensive. This has resulted in many researchers resorting to the use of simplified OTMs that can yield substantial measurement errors. 3D printing offers the prospect of robust, easily replicated, morphologically accurate, and cost-effective OTMs that capture the benefits but alleviate the problems associated with electroforming. Here, we validate the use of OTMs that were 3D printed using several materials across eight lizard species of different body sizes and living in habitats ranging from deserts to tropical forests. We show that 3D printed OTMs have low thermal inertia and predict the live animal's equilibration temperature with high accuracy across a wide range of body sizes and microhabitats. Finally, we developed a free online repository and database of 3D scans (https://www.3dotm.org/) to increase the accessibility of this tool to researchers around the world and facilitate ease of production of 3D printed models. 3D printing of OTMs is generalizable to taxa beyond lizards. If widely adopted, this approach promises greater accuracy and reproducibility in studies of terrestrial thermal ecology and should lead to improved forecasts of the biological impacts of climate change.

Prey consumption does not restore hydration state but mitigates the energetic costs of water deprivation in an insectivorous lizard.

To cope with limited availability of drinking water in their environment, terrestrial animals have developed numerous behavioral and physiological strategies including maintaining an optimal hydration state through dietary water intake. Recent studies performed in snakes, which are generalist carnivorous reptiles, suggest that the benefits of dietary water intake are negated by hydric costs of digestion. Most lizards are generalist insectivores that can shift their prey types, but firm experimental demonstration of dietary water intake is currently missing in these organisms. Here, we performed an experimental study in the common lizard Zootoca vivipara, a keystone mesopredator from temperate climates exhibiting a great diversity of prey in its mesic habitats, in order to investigate the effects of food consumption and prey type on physiological responses to water deprivation. Our results indicate that common lizards cannot improve their hydration state through prey consumption, irrespective of prey type, suggesting that they are primarily dependent upon drinking water. Yet, high-quality prey consumption reduced the energetic costs of water deprivation, potentially helping lizards to conserve a better body condition during periods of limited water availability. These findings have important implications for understanding the physiological responses of ectotherms to water stress, and highlight the complex interactions between hydration status, energy metabolism and feeding behavior in insectivorous lizards.

Stop, then go! Rapid acceleration offsets the costs of intermittent locomotion when turning in Florida scrub lizards.

Intermittent locomotion is a common locomotor mode in small vertebrates. Pausing is thought to aid in locating a predator or prey, enhancing crypsis, lowering energy costs, and/or maneuvering around obstacles or toward a refuge. Many lizards flee predators by turning into potential refugia and subsequently pausing, presumably to conceal themselves. Intermittent locomotion may be associated with turning by allowing an animal time to assess its surroundings and/or decreasing the likelihood of losing its footing. In this study, we quantify locomotor performance and the use of intermittent locomotion in Florida scrub lizards (Sceloporus woodi) when navigating either a 45° or 90° turn. Lizards paused in 92.91% of all trials, and yet despite pausing, instantaneous speed was not different entering or exiting the turn. This result suggests that turning comes at minimal cost to forward speed for lizards under these conditions. Pausing during a turn, however, did slow speed in the turn. Interestingly, the speed in the turn did not differ in trials with a pause before the turn versus trials without a pause. The angle of the turn also had no effect on whether lizards paused. We found that lizards increase peak acceleration following pauses to compensate for lost speed during the pause, providing a mechanism that may minimize negative fitness effects associated with slow running speeds and allow intermittent locomotion to be such a common strategy in lizards.

Fitness Costs of Maternal Ornaments and Prenatal Corticosterone Manifest as Reduced Offspring Survival and Sexual Ornament Expression.

Colorful traits (i.e., ornaments) that signal quality have well-established relationships with individual condition and physiology. Furthermore, ornaments expressed in females may have indirect fitness effects in offspring via the prenatal physiology associated with, and social consequences of, these signaling traits. Here we examine the influence of prenatal maternal physiology and phenotype on condition-dependent signals of their offspring in adulthood. Specifically, we explore how prenatal maternal testosterone, corticosterone, and ornament color and size correlate with female and male offspring survival to adulthood and ornament quality in the lizard Sceloporus undulatus. Offspring of females with more saturated badges and high prenatal corticosterone were less likely to survive to maturity. Badge saturation and area were negatively correlated between mothers and their male offspring, and uncorrelated to those in female offspring. Maternal prenatal corticosterone was correlated negatively with badge saturation of male offspring in adulthood. Our results indicate that maternal ornamentation and prenatal concentrations of a stress-relevant hormone can lead to compounding fitness costs by reducing offspring survival to maturity and impairing expression of a signal of quality in surviving males. This mechanism may occur in concert with social costs of ornamentation in mothers. Intergenerational effects of female ornamentation and prenatal stress may be interdependent drivers of balancing selection and intralocus sexual conflict over signaling traits.

Allocation costs of regeneration: tail regeneration constrains body growth under low food availability in juvenile lizards.

The balance of energy allocated to development and growth of different body compartments may incur allocation conflicts and can thereby entail physiological and evolutionary consequences. Regeneration after autotomy restores the functionality lost after shedding a body part but requires a strong energy investment that may trade-off with other processes, like reproduction or growth. Caudal autotomy is a widespread antipredator strategy in lizards, but regeneration may provoke decreased growth rates in juveniles that could have subsequent consequences. Here, we assessed the growth of intact and regenerating hatchling wall lizards (Podarcis muralis) exposed to different food regimens. Regenerating juveniles presented slightly but significantly lower body growth rates than individuals with intact tails when facing low food availability, but there were no differences when food was supplied ad libitum. Regenerating individuals fed ad libitum increased their ingestion rates compared to intact ones during the period of greatest tail growth, which also reveals a cost of tail regeneration. When resources were scarce, hatchlings invested more in tail regeneration in relation to body growth, rather than delay regeneration to give priority to body growth. We propose that, in juvenile lizards, regeneration could be prioritized even at the expense of body growth to restore the functionality of the lost tail, likely increasing survivorship and the probability to reach reproductive maturity. Our study indicates that food availability is a key factor for the occurrence of trade-offs between regeneration and other growth processes, so that environmental conditions would be determinant for the severity of the costs of regeneration.

Cost-effective surveillance of invasive species using info-gap theory.

Invasive species can lead to community-level damage to the invaded ecosystem and extinction of native species. Most surveillance systems for the detection of invasive species are developed based on expert assessment, inherently coming with a level of uncertainty. In this research, info-gap decision theory (IGDT) is applied to model and manage such uncertainty. Surveillance of the Asian House Gecko, Hemidactylus frenatus Duméril and Bibron, 1836 on Barrow Island, is used as a case study. Our research provides a novel method for applying IGDT to determine the population threshold ([Formula: see text]) so that the decision can be robust to the deep uncertainty present in model parameters. We further robust-optimize surveillance costs rather than minimize surveillance costs. We demonstrate that increasing the population threshold for detection increases both robustness to the errors in the model parameter estimates, and opportuneness to lower surveillance costs than the accepted maximum budget. This paper provides guidance for decision makers to balance robustness and required surveillance expenditure. IGDT offers a novel method to model and manage the uncertainty prevalent in biodiversity conservation practices and modelling. The method outlined here can be used to design robust surveillance systems for invasive species in a wider context, and to better tackle uncertainty in protection of biodiversity and native species in a cost-effective manner.

The movement dynamics of autotomized lizards and their tails reveal functional costs of caudal autotomy.

Autotomy has evolved independently several times in different animal lineages. It frequently involves immediate functional costs, so regeneration evolved in many instances to restore the functionality of that body part. Caudal autotomy is a widespread antipredator strategy in lizards, although it may affect energy storage, locomotion dynamics, or survival in future encounters with predators. Here, we assessed the effect of tail loss on the locomotor performance of wall lizards (Podarcis muralis), as well as the recovery of locomotor functionality of lizards with regenerated tails, and the movement dynamics of shed tails that were either intact or having regenerated portions. Tail loss had no effect on locomotion over unhindered spaces, possibly due to compensation between a negative effect on the stride of front limbs, and a positive effect of losing mass and friction force. We found a clear negative impact of tail loss on locomotion in spaces with interspersed obstacles, in which tailed lizards jumped larger distances when leaving the obstacles. Besides, lizards that used the tail to push off the ground were able to approach the obstacles from further, so that the tail seemed to be useful when used during jumping. Regeneration fully restores lizard's locomotor capacities, but tail antipredator value, as indicated by the intensity of post-autotomic movements, is only partially retrieved. From these results, we propose that, together with the recovery of post-autotomy antipredator capacities, the restoration of the organismal locomotor performance may have been an important, yet frequently neglected factor in the evolution of lizard's regeneration ability.

Camera-traps are a cost-effective method for surveying terrestrial squamates: A comparison with artificial refuges and pitfall traps.

INTRODUCTION: Fundamental data on the distributions, diversity, and threat status of terrestrial snakes and lizards (hereafter squamates) is limited. This is due to the cryptic nature of species in this faunal group, and to limitations in the effectiveness of the survey methods used to detect these species. Camera-traps are a useful tool for detecting numerous vertebrate species, yet their use for detecting squamates has been limited. Here, we apply recent methodological advancements in camera-trapping and assessed the utility of camera-traps for inventorying a squamate assemblage by comparing camera-trapping survey results with two widely used labour-intensive methods: artificial refuges and pitfall traps. METHODS: We conducted a 74-day survey using camera-traps and, concurrently, four by four-day surveys using labour-intensive methods. Given the duration and three detection methods, we compared seven variants of survey protocol, including using each method alone or all methods simultaneously. We compared both the effectiveness and cost-effectiveness of each survey protocol by estimating the number of species detected at the transect level, and by calculating the costs of conducting those surveys. RESULTS: We found the camera-trapping survey was most cost-effective, costing 687 AUD (CI 534-912) per squamate species detected, compared with the 2975 AUD (CI 2103-4486) per squamate species detected with the labour-intensive methods. Using all methods together was less cost-effective than using camera-traps alone. Additionally, there was a 99% probability that camera-traps would detect more species per transect than the labour-intensive methods examined. DISCUSSION & CONCLUSION: By focusing the analysis at the level of the survey, rather than the level of the device, camera-traps are both a more effective and cost-effective technique for surveying terrestrial squamates. Where circumstances are appropriate, those wildlife researchers and managers currently using camera-traps for non-squamate surveys, can adopt the methods presented to incorporate squamate surveys with little upfront cost. Additionally, researchers currently using traditional techniques can be confident that switching to camera-traps will likely yield improved results. Still, camera-traps are not a panacea and careful consideration into the benefits and usefulness of these techniques in individual circumstances is required.

Heart rate variability in the tegu lizard, Salvator merianae, its neuroanatomical basis and role in the assessment of recovery from experimental manipulation.

Using long-term, remote recordings of heart rate (fH) on fully recovered, undisturbed lizards, we identified several components of heart rate variability (HRV) associated with respiratory sinus arrhythmia (RSA): 1.) A peak in the spectral representation of HRV at the frequency range of ventilation. 2.) These cardiorespiratory interactions were shown to be dependent on the parasympathetic arm of the autonomic nervous system. 3.) Vagal preganglionic neurons are located in discrete groups located in the dorsal motor nucleus of the vagus and also, in a ventro-lateral group, homologous to the nucleus ambiguus of mammals. 4.) Myelinated nerve fibers in the cardiac vagus enabling rapid communication between the central nervous system and the heart. Furthermore, the study of the progressive recovery of fH in tegu following anesthesia and instrumentation revealed that 'resting' levels of mean fH and reestablishment of HRV occurred over different time courses. Accordingly, we suggest that, when an experiment is designed to study a physiological variable reliant on autonomic modulation at its normal, resting level, then postsurgical reestablishment of HRV should be considered as the index of full recovery, rather than mean fH.

An integrative assessment of the diversity, phylogeny, distribution, and conservation of the terrestrial reptiles (Sauropsida, Squamata) of the United Arab Emirates.

In the present study we use an unprecedented database of 5,535 distributional records to infer the diversity, ecological preferences and spatial distribution of the 60 species of terrestrial reptiles of the United Arab Emirates (UAE), and use the 57 native species to test the effectiveness of the protected areas' network in conserving this unique vertebrate fauna. We infer a time-calibrated phylogeny with 146 species of squamates and 15 genes including all UAE terrestrial reptile species to determine the phylogenetic diversity (PD) and evolutionary distinctiveness (ED) of the native species and to compare it with the distribution of the hotspots of native species richness. The results of this study indicate that the sampling effort is remarkable, covering 75% of the country's territory representing nearly the entire climatic space of the UAE defined by the mean annual temperature and the total annual precipitation, as well as the multivariate climatic space defined by a principal component analysis (PCA). Species richness is highest in the northeast of the country, in a transitional area from sandy desert to the mountainous terrain of the Hajar Mountains. The highest PD of a single square cell of 10 arc-minutes grid is of 2,430 million years (my) of accumulated evolutionary history and the strong correlation between PD and species richness suggests that the raw number of species is a good surrogate to quantify the evolutionary history (i.e., PD). The species with the highest values of ED are those in families represented by only one species in the UAE. Finally, the assessment of the UAE protected areas shows that, despite their relevance in protecting the terrestrial reptiles, they do not offer adequate protection for some threatened species. Therefore, a reassessment of some of the protected areas or the creation of species specific conservation action plans are recommended in order to ensure the preservation of the unique diversity of UAE terrestrial reptiles.

Independent influence of thermoregulatory cost on the lower and upper set-points of a heliothermic lizard.

Studies on ectothermic vertebrates generally lead to average indicators of thermal preferences measured in the laboratory, which do not say about responses to natural environmental change and may not inform about individual variation and its triggering mechanisms. We studied whether and how changes in costs of thermoregulation influence the preferred temperature (Tp) of individual lizards and their energetic investment in thermoregulation by exposing specimens to three treatments of increasing costs, recording body temperature (Tb) and distance walked (energetic investment). Moderate costs induced an investment trade-off between energy-investment in thermoregulation and Tb, and highlighted individual variation that decreased with higher costs. Lower average Tp's were observed in the high costs trials as a result of the decreased values of the lower and upper voluntary Tb's. As costs increased, lizards walked a shorter overall distance and accepted lower Tb's, but lizards still engaged in costly thermoregulation. Individual variation resulted in two main thermoregulatory patterns that in certain ecological contexts may have an important role in decision-making and adjusting to temperatures that are far from optimal temperatures for performance and physiological processes.

Thermal dependence of feeding performance and resting metabolic expenditure in different altitudinal populations of toad-headed lizards.

Inter-population variations in growth rate can result from independent or interactive effects of genetic and environmental factors, and be induced by some physiological differences as well. Toad-headed lizards (Phrynocephalus vlangalii) from a higher-elevation population were shown to have a higher growth rate than those from a lower-elevation population. The physiological basis of growth rate variation in this species is not well understood. Here, we investigated the feeding performance and resting metabolic rate (RMR) of lower- and higher-elevation individuals at different test ambient temperatures to evaluate the role of differences in energy intake, assimilation efficiency and metabolic expenditure on growth rate variations. Within the range of 25-35 °C, lizard RMR increased with increasing test ambient temperature, but food intake, apparent digestive coefficient (ADC, food energy minus faecal energy divided by food energy), and assimilation efficiency (AE, food energy minus faecal and urinary energy divided by food energy) were less thermally sensitive in both populations. Higher-elevation lizards tended to eat more food and have a lower RMR than lower-elevation ones, despite the lack of differences in ADC and AE. Our result showed that more energy intake and reduced maintenance cost may be associated with the higher growth rate of higher-elevation lizards. Accordingly, inter-population differences in energy acquisition and expenditure could act as potential sources for geographic variation in growth rate.

From conceptual to computational: Cost and benefits of lizard thermoregulation revisited.

A classic paper detailed conceptual analyses of behavioral thermoregulation (Huey and Slatkin, 1976) and has served as the theoretical foundation for hundreds of investigative studies. Most recently, investigators have revisited this theoretical presentation to offer additional interpretation for both heterogeneity and spatial structure of temperature and how it may influence energetic costs (Sears and Angilletta, 2015). Interestingly, this foundational presentation by Huey and Slatkin, over 40 years ago, has never received formal computational analyses to address mathematically the postulates of this conceptual model. Here we use functions that closely mimic those that were described by Huey and Slatkin to provide both a theoretical and computational analysis for the cost and benefits of lizard thermoregulation. We demonstrate both the utility and inherent accuracy of their analyses using a model that was developed conceptually without the use of now readily available computational tools. But contrary to Huey and Slatkin's analyses, we provide a mathematical proof that perfect thermoregulation is never an optimal strategy and show by computational analysis that thermoregulatory strategy (k ) may decrease, not increase, with increasing cost.

Energetic costs of performance in trained and untrained Anolis carolinensis lizards.

The energetic costs of performance constitute a non-trivial component of animals' daily energetic budgets. However, we currently lack an understanding of how those costs are partitioned among the various stages of performance development, maintenance and production. We manipulated individual investment in performance by training Anolis carolinensis lizards for endurance or sprinting ability. We then measured energetic expenditure both at rest and immediately following exercise to test whether such training alters the maintenance and production costs of performance. Trained lizards had lower resting metabolic rates than controls, suggestive of a maintenance saving associated with enhanced performance as opposed to a cost. Production costs also differed, with sprint-trained lizards incurring a larger energetic performance cost and experiencing longer recovery times compared with endurance trained and control animals. Although performance training modifies metabolism, production costs are probably the key drivers of trade-offs between performance and other life-history traits in this species.

Influence of adaptive capacity on the outcome of climate change vulnerability assessment.

Climate change vulnerability assessment (CCVA) has become a mainstay conservation decision support tool. CCVAs are recommended to incorporate three elements of vulnerability - exposure, sensitivity and adaptive capacity - yet, lack of data frequently leads to the latter being excluded. Further, weighted or unweighted scoring schemes, based on expert opinion, may be applied. Comparisons of these approaches are rare. In a CCVA for 17 Australian lizard species, we show that membership within three vulnerability categories (low, medium and high) generally remained similar regardless of the framework or scoring scheme. There was one exception however, where, under the warm/dry scenario for 2070, including adaptive capacity lead to five fewer species being classified as highly vulnerable. Two species, Eulamprus leuraensis and E. kosciuskoi, were consistently ranked the most vulnerable, primarily due to projected losses in climatically suitable habitat, narrow thermal tolerance and specialist habitat requirements. Our findings provide relevant information for prioritizing target species for conservation and choosing appropriate conservation actions. We conclude that for the species included in this study, the framework and scoring scheme used had little impact on the identification of the most vulnerable species. We caution, however, that this outcome may not apply to other taxa or regions.

How Do We Measure the Cost of Whole-Organism Performance Traits?

SYNOPSIS: Whole-organism performance traits, such as maximal speed and endurance capacity are undoubtedly costly, but we know little about how or when all of the costs associated with performance are paid to individuals or how to measure them. To understand how performance traits might be involved in trade-offs with other life-history traits it is critical to determine the development, production, and maintenance costs of performance traits, as well as how each of these changes with increased or decreased use of the performance trait. We discuss the advantages and disadvantages of several potential phenotypic measures of dynamic whole-organism performance that may be used in life-history studies, including direct performance measures; metabolic rates; ecological cost of transport; and changes in metabolic rate after training. We use the first approach, direct performance measures, to show trade-offs between endurance capacity and several traditional life history variables in phrynosomatid lizards. The largest problem currently in determining the costs of performance traits and how those costs might lead to life-history trade-offs is that there are estimates of performance costs in very few taxa, and when there are, those species typically are not studied with respect to "traditional" life-history traits.

Physiological Trade-Offs in Lizards: Costs for Individuals and Populations.

SYNOPSIS: The immune system is a critical component of health and fitness, whereby organisms must maintain sufficient health to survive to reproduce. Because of the key role of immunity in an organism's fitness, the use of immunological indices is widespread. However, there is a paucity of empirical support for the best way to interpret immunological data, and the internal energetic state of the organism, as well as the external environmental pressures it faces, are often not considered concurrently. A stronger immune response is not always beneficial to the organism; a more attenuated response may ultimately lead to improved fitness if the animal incurs fewer performance costs on competing systems, especially reproduction. Additionally, the external pressures animals encounter (such as anthropogenic disturbance) must be considered along with the animal's internal state. A synthesis of results addressing resource allocation between the immune and reproductive systems is presented using a well-studied organism, the side-blotched lizard, from a combination of field and laboratory studies under varying environmental conditions. Specifically, experiments involving specific immune, reproductive, metabolic, and performance costs in a laboratory setting are discussed, as well as associated demographic trade-offs between survival and reproductive success, demonstrating essential links between immunity and the population.

Low-resistive vibratory penetration in granular media.

Non-cohesive materials such as sand, dry snow or cereals are encountered in various common circumstances, from everyday situations to industry. The process of digging into these materials remains a challenge to most animals and machines. Within the animal kingdom, different strategies are employed to overcome this issue, including excavation methods used by ants, the two-anchor strategy employed by soft burrowers such as razor-clams, and undulatory motions exhibited by sandfish lizards. Despite the development of technology to mimic these techniques in diggers and robots, the limitations of animals and machines may differ, and mimicry of natural processes is not necessarily the most efficient technological strategy. This study presents evidence that the resisting force for the penetration of an intruder into a dry granular media can be reduced by one order of magnitude with small amplitude (A ≃ 10 µm) and low frequency (f = 50 - 200 Hz) mechanical vibrations. This observed result is attributed to the local fluidization of the granular bed which induces the rupture of force chains. The drop in resistive force on entering dry granular materials may be relevant in technological development in order to increase the efficiency of diggers and robots.

Diminishing returns limit energetic costs of climate change.

Changes in the time available for organisms to maintain physiologically preferred temperatures (thermal opportunity) is a primary mechanism by which climate change impacts the fitness and population dynamics of organisms. Yet, it is unclear whether losses or gains in thermal opportunity result in proportional changes in rates of energy procurement and use. We experimentally quantified lizard food consumption and energy assimilation at different durations of thermal opportunity. We incorporated these data in an individual-based model of foraging and digestion in lizards to explore the implications of nonlinear responses to shifts in thermal opportunity across a wide geographic range. Our model predicts that shifts in thermal opportunities resulting from climate change alter energy intake primarily through digestion rather than feeding, because simulated lizards were able to fill their gut faster than they can digest their food. Moreover, since rates of energy assimilation decelerate with increasing thermal opportunity, shifts in daily energetic assimilation would depend on the previous opportunity for thermoregulation. In particular, the same changes in thermal opportunity will have little impact on lizards from warm locations, while having a large impact on lizards from cold locations where thermoregulation is possible for only a few hours each day. Energy expenditure followed spatial patterns in thermal opportunity, with greater annual energy expenditure occurring at warmer locations. Our model predicts that lizards will spend more energy under climate change by maintaining higher body temperatures and remaining active longer. However, the predicted changes in energy assimilation following climate change greatly exceeded the predicted increases in energy expenditure. Simple models, which assume constant rates of energy gain during activity, will potentially mislead efforts to understand and predict the biological impacts of climate change.

An energetic perspective on tissue regeneration: The costs of tail autotomy in growing geckos.

Tail autotomy is a crucial antipredatory lizard response, which greatly increases individual survival, but at the same time also compromises locomotor performance, sacrifices energy stores and induces a higher burden due to the ensuing response of regenerating the lost body part. The potential costs of tail autotomy include shifts in energy allocation and metabolic rates, especially in juveniles, which invest their energy primarily in somatic growth. We compared the metabolic rates and followed the growth of juvenile males with and without regenerating tails in the Madagascar ground gecko (Paroedura picta), a nocturnal ground-dwelling lizard. Geckos with intact tails and those that were regrowing them grew in snout-vent-length at similar rates for 22weeks after autotomy. Tail regeneration had a negligible influence on body mass-corrected metabolic rate measured at regular intervals throughout the regenerative process. We conclude that fast-growing juveniles under the conditions of unrestricted food can largely compensate for costs of tail loss and regeneration in their somatic growth without a significant impact on the total individual body mass-corrected metabolic rate.