Seasonal and altitudinal variation in dorsal skin reflectance and thermic rates in a high-altitude montane lizard.

Temperature is one of the most important factors in the life histories of ectotherms, as body temperature has an undeniable effect on growth, activity, and reproduction. Lizards have a wide variety of strategies to acquire and maintain body temperature in an optimal range. The "Thermal Melanism Hypothesis" proposes that individuals with lower skin reflectance can heat up faster as a result of absorbing more solar radiation compared to lighter conspecifics. Therefore, having a darker coloration might be advantageous in cold habitats. Dorsal skin reflectance has been found to change rapidly with body temperature in several lizard species, and it can also vary over longer, seasonal time scales. These variations may be important in thermoregulation, especially in lizards that inhabit areas with a large temperature variation during the year. Here, we study how dorsal reflectance fluctuates with body temperature and varies among seasons. We compared dorsal skin reflectance at three body temperature treatments, and measured thermal rates (i.e., heat and cool rate, thermic lapse, and net heat gain) by elevation (2500-4100 m) and seasons (spring, summer, and autumn) in the mesquite lizard, Sceloporus grammicus. Our results show that lizards were darker at high elevations and during the months with the lowest environmental temperatures. The rate of obtaining and retaining heat also varied during the year and was highest during the reproductive season. Our results indicate that the variation of dorsal skin reflectance and thermal rates follows a complex pattern in lizard populations and is affected by both elevation and season.

Thermoregulatory behavior varies with altitude and season in the sceloporine mesquite lizard.

In ectothermic animals, body temperature is the most important factor affecting physiology and behavior. Reptiles depend on environmental temperature to regulate their body temperature, so geographic variation in environmental temperature can affect the biology of these organisms in the short and long term. We may expect physiological and behavioral responses to temperature change to be especially important in ectotherms inhabiting temperate zones, where different seasons present different thermal challenges. High-mountain temperate systems represent a natural laboratory for studies of evolutionary and plastic variation in thermal biology. The aim of the present study is to evaluate operative temperature with biophysical models, active body temperature under field conditions, preferred temperature in a thermal gradient in the laboratory, and thermal indexes in Sceloporus grammicus lizards along an elevational gradient. We measured these traits in three populations at 2500, 3400, and 4100 m elevation at different seasons of the year (spring, summer and autumn). Our results showed that operative temperature varied with season and elevation, with greater variation at middle and high elevations than at low elevations. Body temperature and preferred temperature varied with altitude and season but did not differ between sexes. Thermal quality was lowest in the high-altitude population and in the summer season. Thermoregulatory efficiency was highest in the three populations in the autumn. Our results suggest that thermoregulatory strategies vary with elevation and season, allowing individual lizards to confront annual fluctuations in the thermal environment and conflicting with some previous descriptions of Sceloporus lizards as thermally conservative.

Elevation and blood traits in the mesquite lizard: Are patterns repeatable between mountains?

Ecogeographical patterns describe predictable variation in phenotypic traits between ecological communities. For example, high-altitude animals are expected to show elevated hematological values as an adaptation to the lower oxygen pressure. Mountains act like ecological islands and therefore are considered natural laboratories. However, the majority of ecophysiological studies on blood traits lack replication that would allow us to infer if the pattern reported is a local event or whether it is a widespread pattern resulting from larger-scale ecological processes. In lizards, in fact, the increase of hematological values at high altitudes has received mixed support. Here, for the first time, we compare blood traits in lizards along elevational gradients with replication. We tested the repeatability of blood traits in mesquite lizards between different elevations in three different mountains from the Trans-Mexican Volcanic Belt. We measured hematocrit, hemoglobin concentration, mean corpuscular hemoglobin concentration, and erythrocyte size in blood samples of low, medium, and high-elevation lizards. We obtained similar elevational patterns between mountains, but the blood traits differed among mountains. Middle-altitude populations had greater oxygen-carrying capacity than lizards from low and high altitudes. The differences found between mountain systems could be the result of phenotypic plasticity or genetic differentiation as a consequence of abiotic factors not considered.

Phenological variation in parasite load and inflammatory response in a lizard with an asynchronous reproductive cycle.

We present the first study that compares phenological variation in parasite load and inflammatory response in a lizard with asynchronous male and female gonadal cycles. Other studies have used many species with seasonal and synchronous reproductive cycles, in which it is difficult to decouple the effects of internal and external factors that can affect parasite abundance in each sex. Species with asynchronous reproductive cycles provide the opportunity to study the effects of seasonality and reproductive condition separately, but few studies have documented variation in parasite abundance in these species. We made an extensive comparison of parasite load and inflammatory response of the lizard Sceloporus torquatus, a species with asynchronous reproductive cycles, throughout its active period. We hypothesized that the parasite load would be higher in the period of maximum gonadal activity for each sex, negatively related to body condition and inflammatory response. Our results partially support the hypothesis; males had more parasites in summer than in spring and autumn, while females had more parasites in spring and summer than in autumn; however, we do not find a relationship between parasite load, body condition and inflammatory response. Our results indicated that host-parasite interactions are complex and depend upon both environmental and internal factors. Therefore, longer-term studies may provide a more comprehensive picture of host-parasite dynamics in populations of wild lizards.

Fast and dark: The case of Mezquite lizards at extreme altitude.

Sprint speed is a major performance trait in animal fitness involved in escaping from predators, obtaining food, and defending territory. Biotic and abiotic factors may influence sprint speed in lizards. Temperature decreases at higher altitude. Therefore, lizards at high elevations may require longer basking times to reach optimal body temperatures, increasing their vulnerability to predation and decreasing their time for other activities such as foraging or reproduction. Here, we tested whether the maximum sprint speed of a lizard that shows conservative thermal ecology varied along an altitudinal gradient comprising low (2500 m), middle (3400 m) and high-altitude (4300 m) populations. We also tested whether sprint speed was related to dorsal reflectance at different ecologically relevant temperatures. Given that the lizard Sceloporus grammicus shows conservative thermal ecology with altitude, we expected that overall average sprint speed would not vary with altitude. However, given that darker lizards heat up quicker, we expected that darker lizards would be faster than lighter lizards. Our results suggest that S. grammicus at high altitude are faster and darker at 30 °C, while lizards from low and middle altitude are faster and lighter in color at 20 °C than high altitude lizards. Also, our results suggest a positive relationship between sprint speed and dorsal skin reflectance at 10 and 20 °C. Sprint speed was also affected by snout-vent length, leg length, and leg thickness at 10 °C. These results suggest that, even though predation pressure is lower at extreme altitudes, other factors such as vegetation cover or foraging mode have influenced sprint speed.

Hypoxia by Altitude and Welfare of Captive Beaded Lizards (Heloderma Horridum) in Mexico: Hematological Approaches.

Heloderma horridum is one of the few known venomous lizards in the world. Their populations are in decline due to habitat destruction and capture for the pet trade. In México, many zoos have decided to take care of this species, most of them at altitudes greater than the natural altitudinal distribution. However, we know little about the capacity of the reptiles to face high-altitude environments. The objective of this study was to compare hematological traits of H. horridum in captivity in high and low altitude environments. Our findings show that H. horridum does not respond to hypoxic environments, at least in blood traits, and that the organisms appear to be in homeostasis. Although we cannot know if individual H. horridum housed in high-altitude environments are completely comfortable, it appears hypoxia can be avoid without modifications of blood parameters. We suggest that future work should address changes in metabolic rates and in behavioral aspects to understand how to maintain the health and comfort of the reptiles native to low altitude when they are housed in high-altitude environments.

Patterns, Mechanisms and Genetics of Speciation in Reptiles and Amphibians.

In this contribution, the aspects of reptile and amphibian speciation that emerged from research performed over the past decade are reviewed. First, this study assesses how patterns and processes of speciation depend on knowing the taxonomy of the group in question, and discuss how integrative taxonomy has contributed to speciation research in these groups. This study then reviews the research on different aspects of speciation in reptiles and amphibians, including biogeography and climatic niches, ecological speciation, the relationship between speciation rates and phenotypic traits, and genetics and genomics. Further, several case studies of speciation in reptiles and amphibians that exemplify many of these themes are discussed. These include studies of integrative taxonomy and biogeography in South American lizards, ecological speciation in European salamanders, speciation and phenotypic evolution in frogs and lizards. The final case study combines genomics and biogeography in tortoises. The field of amphibian and reptile speciation research has steadily moved forward from the assessment of geographic and ecological aspects, to incorporating other dimensions of speciation, such as genetic mechanisms and evolutionary forces. A higher degree of integration among all these dimensions emerges as a goal for future research.

Detection and quantification of a ß-neurotoxin (crotoxin homologs) in the venom of the rattlesnakes Crotalus simus, C. culminatus and C. tzabcan from Mexico.

Snake venom may vary in composition and toxicity across the geographic distribution of a species. In the case of the three species of the Neotropical rattlesnakes Crotalus simus, C. culminatus and C. tzabcan recent research has revealed that their venoms can contain a neurotoxic component (crotoxin homologs), but is not always the case. In the present work, we detected and quantified crotoxin homologs in venom samples from three species distributed across Mexico, to describe variation at the individual and subspecific levels, using slot blot and ELISA immunoassays. We found that all C. simus individuals analyzed had substantial percentages of crotoxin homologs in their venoms (7.6-44.3%). In contrast, C. culminatus lacked them completely and six of ten individuals of the species C. tzabcan had low percentages (3.0-7.7%). We also found a direct relationship between the lethality of a venom and the percentage of crotoxin homologs it contained, indicating that the quantity of this component influences venom lethality in the rattlesnake C. simus.

Behavioral and physiological polymorphism in males of the austral lizard Liolaemus sarmientoi.

Integrative behavioral studies show that the interplay between individual physiology and social behavior influences the ecology of the species, ultimately affecting individual fitness. Particularly in lizards, color polymorphism is associated with differential behaviors and reproductive strategies, which are evident in mature males during the mating season. Dominant males generally have greater endurance, higher body temperature, and larger bodies than submissive males, so they can acquire and defend larger territories and have greater access to females for mating. We studied whether the color morphs observed in males of one of the world's southernmost reptiles, Liolaemus sarmientoi, are related to behavioral variation during agonistic interactions, thermal physiology, morphology, and/or locomotor stamina. Liolaemus sarmientoi males exhibit three color morphs: red (RR), red-yellow (RY), and yellow (YY). These lizards exhibit subtle behavioral displays and we did not observe stamina differences among morphs. However, we found that RR males are more aggressive than YY males during agonistic encounters. In addition, greater body temperature change during trials, higher field body temperatures, and greater head sizes of RR males compared to RY or YY indicate that RR is a dominant morph, which may influence their ability to acquire and defend territory and tactics for achieving reproductive success.

Histological characteristics of gills and dorsal skin in ambystoma leorae and ambystoma rivulare: morphological changes for living at high altitude / Características histológicas de la piel del dorso y las branquias en ambystoma leorae y ambystoma rivulare: cambios morfológicos para vivir a gran altitud

SUMMARY: Vertebrates exhibit structural changes in their cardiovascular and gas exchange systems in response to hypoxic conditions in high altitude environments. In highland neotenic mole salamanders, as other amphibians, the majority of gases exchange is carried out for skin and gills. But, in high altitude environments, the available oxygen is lower than it is in the air thus, the scarcity of oxygen limits the survival of organisms. Many studies on this subject have focused on understanding the hematological mechanisms that amphibians exhibit in response to hypoxia. However, little is known about possible morphological changes in respiratory structures that may permit increased gas exchange during respiration in high altitude amphibians like Ambystoma leorae and A. rivulare, two threatened Mexican salamander species. The aim of the present study was to describe and compare the histological characteristics of the gills and dorsal skin of A. leorae and A. rivulare from populations at low and high altitudes. We found that, in comparison to lowland organisms, highland ones exhibited more pronounced skin folds, greater numbers of secondary branches in the gills, thinner dorsal and gill epidermises, and greater quantity of melanin surrounding the gill blood vessels. These differences permit a greater capacity for gas exchange and also increase thermoregulatory capacity in high altitude environments.

RESUMEN: Los anfibios que viven en ambientes de altitud se enfrentan a factores abióticos que limitan la vida, tales como la disminución de la presión barométrica con la consecuente disminución de la presión parcial de oxígeno (O2). Conocer los mecanismos que optimizan la obtención del O2 en estos animales es de gran importancia para entender las diferencias en la sensibilidad a la hipoxia de las diferentes especies. Ambystoma rivulare y A. leorae son anfibios endémicos del Estado de México que viven en ambientes de alta altitud por lo que se cree presentan estrategias fenotípicas para asimilar eficazmente el O2 y poder subsistir en los ambientes de altitud. El objetivo de este trabajo fue analizar las características histológicas de branquias y piel cefálica (que son las principales estructuras que se encargan del intercambio gaseoso) provenientes de tres poblaciones con diferente altitud. Nuestros resultados muestran que los organismos que habitan a mayor altitud tienden a aumentar la superficie de intercambio gaseoso, como es el caso de pliegues epidérmicos y ramas branquiales secundarias. Las diferencias histológicas de branquias y piel cefálica tanto interespecíficas como intraespecíficas respecto a la altitud parecen apoyar la idea de que los organismos modifican sus estructuras para contrarrestar las limitantes de la vida en ambientes de altitud.

A Mountain or a Plateau? Hematological Traits Vary Nonlinearly with Altitude in a Highland Lizard.

High-altitude organisms exhibit hematological adaptations to augment blood transport of oxygen. One common mechanism is through increased values of blood traits such as erythrocyte count, hematocrit, and hemoglobin concentration. However, a positive relationship between altitude and blood traits is not observed in all high-altitude systems. To understand how organisms adapt to high altitudes, it is important to document physiological patterns related to hypoxia gradients from a greater variety of species. Here, we present an extensive hematological description for three populations of Sceloporus grammicus living at 2,500, 3,400, and 4,300 m. We did not find a linear increase with altitude for any of the blood traits we measured. Instead, we found nonlinear relationships between altitude and the blood traits erythrocyte number, erythrocyte size, hematocrit, and hemoglobin concentration. Erythrocyte number and hematocrit leveled off as altitude increased, whereas hemoglobin concentration and erythrocyte size were highest at intermediate altitude. Additionally, lizards from our three study populations are similar in blood pH, serum electrolytes, glucose, and lactate. Given that the highest-altitude population did not show the highest levels of the variables we measured, we suggest these lizards may be using different adaptations to cope with hypoxia than lizards at low or intermediate altitudes. We discuss future directions that research could take to investigate such potential adaptations.

Variation in the thermal ecology of an endemic iguana from Mexico reduces its vulnerability to global warming.

The persistence of reptile populations in a specific location is influenced by individuals' capacity to regulate their body temperatures, among other factors. Anthropogenic climate change may pose a risk to the survival of ectothermic animals due to their dependence on external heat sources to thermoregulate. In this study, we calculated indices of thermal habitat quality, thermoregulatory precision, and thermoregulatory effectiveness for the endemic spiny-tailed iguana Ctenosaura oaxacana. We evaluated these indices and the thermoregulatory behavior of the iguanas in the four types of vegetation that provide the most favorable conditions for thermoregulation. We also performed our experiments during both the wet and dry seasons to capture the full range of thermal conditions available to C. oaxacana over the course of a year. Finally, we evaluated the potential niche for the iguana in the years 2020, 2050, and 2080. Thermoregulation depends on both seasonal and environmental factors in this species. We found that thermoregulation effectiveness in both wet and dry seasons depends not only on the thermal conditions of the immediate environment, but also on the cover vegetation and habitat structure available across the range of habitats the species uses. Thus, heterogeneous habitats with dispersed vegetation may be most suitable for this species' thermoregulatory strategy. Likewise, niche modeling results suggested that suitable habitat for our study species may continue to be available for the next few decades, despite global warming tendencies, as long as cover vegetation remains unaltered. Our results suggest that thermoregulation is a complex process that cannot be generalized for all ectothermic species inhabiting a given region. We also found that temperature changes are not the only factor one must consider when estimating the risk of species loss. To understand the necessary thermal conditions and extinction risk for any ectothermic species, it is necessary to focus studies on the species' general ecology.

Female preference for sympatric vs. allopatric male throat color morphs in the mesquite lizard (Sceloporus grammicus) species complex.

Color polymorphic sexual signals are often associated with alternative reproductive behaviors within populations, and the number, frequency, or type of morphs present often vary among populations. When these differences lead to assortative mating by population, the study of such polymorphic taxa may shed light on speciation mechanisms. We studied two populations of a lizard with polymorphic throat color, an important sexual signal. Males in one population exhibit orange, yellow, or blue throats; whereas males in the other exhibit orange, yellow, or white throats. We assessed female behavior when choosing between allopatric and sympatric males. We asked whether females discriminated more when the allopatric male was of an unfamiliar morph than when the allopatric male was similar in coloration to the sympatric male. We found that female rejection of allopatric males relative to sympatric males was more pronounced when males in a pair were more different in throat color. Our findings may help illuminate how behavioral responses to color morph differences between populations with polymorphic sexual signals contribute to reproductive isolation.

Evidence of maternal effects on temperature preference in side-blotched lizards: implications for evolutionary response to climate change.

Natural populations respond to selection pressures like increasing local temperatures in many ways, including plasticity and adaptation. To predict the response of ectotherms like lizards to local temperature increase, it is essential to estimate phenotypic variation in and determine the heritability of temperature-related traits like average field body temperature (T b) and preferred temperature (T p). We measured T p of Uta stansburiana in a laboratory thermal gradient and assessed the contribution of sex, reproductive status and throat color genotype to phenotypic variation in T b of adult lizards. Females had higher T p than males. However, they temporarily preferred lower temperature when gravid than when nongravid. Using a nested half-sib design for genetic crosses in the laboratory, we estimated relative contributions of additive genetic variation and maternal effects to T p of hatchlings. Our results show that maternal effects, but not additive genetic variation, influence T p of hatchlings in U. stansburiana. Maternal T p and the presence or absence of blue throat color alleles significantly influenced T p of hatchlings. We discuss ecological and evolutionary consequences of these maternal effects in the context of rapid climate change and natural selection that we measure on progeny survival to maturity as a function of maternal T p.

Erosion of lizard diversity by climate change and altered thermal niches.

It is predicted that climate change will cause species extinctions and distributional shifts in coming decades, but data to validate these predictions are relatively scarce. Here, we compare recent and historical surveys for 48 Mexican lizard species at 200 sites. Since 1975, 12% of local populations have gone extinct. We verified physiological models of extinction risk with observed local extinctions and extended projections worldwide. Since 1975, we estimate that 4% of local populations have gone extinct worldwide, but by 2080 local extinctions are projected to reach 39% worldwide, and species extinctions may reach 20%. Global extinction projections were validated with local extinctions observed from 1975 to 2009 for regional biotas on four other continents, suggesting that lizards have already crossed a threshold for extinctions caused by climate change.