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Global warming is exposing many organisms to severe thermal conditions and is having impacts at multiple levels of biological organisation, from individuals to species and beyond. Biotic and abiotic factors can influence organismal thermal tolerance, shaping responses to climate change. In eusocial ants, thermal tolerance can be measured at the colony level (among workers within colonies), the population level (among colonies within species), and the community level (among species). We analysed critical thermal maxima (CTmax) across these three levels for ants in a semiarid region of northeastern Brazil. We examined the individual and combined effects of phylogeny, body size (BS), and nesting microhabitat on community-level CTmax and the individual effects of BS on population- and colony-level CTmax. We sampled 1864 workers from 99 ant colonies across 47 species, for which we characterised CTmax, nesting microhabitat, BS, and phylogenetic history. Among species, CTmax ranged from 39.3 to 49.7°C, and community-level differences were best explained by phylogeny and BS. For more than half of the species, CTmax differed significantly among colonies in a way that was not explained by BS. Notably, there was almost as much variability in CTmax within colonies as within the entire community. Monomorphic and polymorphic species exhibited similar levels of CTmax variability within colonies, a pattern not always explained by BS. This vital intra- and inter-colony variability in thermal tolerance is likely allows tropical ant species to better cope with climate change. Our results underscore why ecological research must examine multiple levels of biological organisation.
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Hormigas , Hormigas/fisiología , Animales , Brasil , Filogenia , Ecosistema , Tamaño Corporal , Termotolerancia , Cambio ClimáticoRESUMEN
Wildfires cause significant changes in natural habitats and can impact lizard populations. Through changes in the thermal environment, reduced prey availability, and increased exposure to parasite vectors, wildfires affect lizard physiology, immunity, and health. We sampled 56 Tropidurus oreadicus lizards from Cerrado savannas of Brazil living in two adjacent sites: one burned 14 days before the study, and the other unburned for 6 years. We logged the air temperatures of those sites throughout fieldwork. We assessed the short-term possible homeostatic imbalances caused by the fires via measuring body mass, circulating levels of corticosterone (CORT), leukocytes profile changes in heterophile-lymphocyte ratios (HLRs), innate immunity using the bacterial killing assay (BKA), and the diagnosis of hemoparasites using molecular techniques. The air temperature was significantly higher in the burned site. There was no difference in lizard body mass between the two sites, suggesting that prey availability was not affected by the wildfire. While parasite presence was seemingly not affected by fire, the timing of initial parasite infection for animals in the study was unknown, so we also evaluated parasitism as an independent variable relative to the other metrics. Our results showed that parasitic infections lead to reduced bactericidal capacity and body mass in lizards, suggesting clinical disease and depletion of innate immune resources. Moreover, we observed increased HLR with fire and parasitic infections and a strong negative correlation with BKA. These findings suggest that the increased environmental temperature following wildfires may lead to increased CORT and decreased BKA.
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Lagartos , Incendios Forestales , Animales , Lagartos/fisiología , Ecosistema , Corticosterona , HomeostasisRESUMEN
Environmental conditions often affect developmental processes and consequently influence the range of phenotypic variation expressed at population level. Expansion of urban sites poses new challenges for native species, as urbanization usually affects the intensity of solar exposure and shade availability, determining the thermal regimes organisms are exposed to. In this study, we evaluate the effects of different developmental conditions in a Tropidurus lizard commonly found in Brazilian urban sites. After incubating embryos of Tropidurus catalanensis in two different thermal regimes (Developmental Environments [DE]: cold 24°C and warm 30°C), we measured morphological traits in the neonates and quantified locomotor performance in horizontal and vertical surfaces at three temperatures [Test Temperatures (TT) = 24°C, 30°C and 36°C]. Results indicate effects of developmental temperatures on morphological features, expressing functional implications that might be decisive for the viability of T. catalanensis in urbanized areas. Lizards ran similarly on horizontal and vertical surfaces, and isolated analyses did not identify significant effects of DE or TT on the sprint speeds measured. Absolute Vmax (i.e., the maximum sprint speed reached among all TTs) positively correlated with body size (SVL), and neonates from the warm DE (30°C) were larger than those from the cold DE (24°C). Morpho-functional associations of absolute Vmax also involved pelvic girdle width and forelimb, hindlimb, trunk, and tail lengths. Emerging discussions aim to understand how animals cope with abrupt environmental shifts, a likely common challenge in urbanized sites. Our findings add a new dimension to the topic, providing evidence that temperature, an environmental parameter often affected by urbanization, influences the thermal sensitivity of locomotion and the morphological profile of T. catalanensis neonates. Thermal sensitivity of specific developmental processes may influence the ability of these lizards to remain in habitats that change fast, as those suffering rapid urbanization due to city growth.
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Amphibians and reptiles are ectothermic animals and therefore depend on environmental temperatures to maintain their physiological functions. Despite being poorly documented, data on thermal behavioral thresholds to avoid overheating in their habitats are essential to improve the understanding of their thermal ecology and physiology. Here we provide a data set of 312 individual voluntary thermal maximum (VTMax ) values, the maximum temperature tolerated by individuals before actively moving to a colder place, for 53 species of amphibians and reptiles of the Atlantic Forest and Cerrado savannas of southeastern South America. Voluntary thermal maximum values were recorded as the body temperature at which the individuals exited a heating box experimental setup. This data set comprises 25 species of 15 genera and eight families of amphibians and 28 species of 24 genera and 12 families of reptiles. Of the total number of individual records, 67.9% derived from the Cerrado and 32.0% derived from the Atlantic Forest ecoregions. Overall, lizards had higher VTMax than amphibians and snakes, and individuals in the Atlantic Forest had overall higher VTMax values than the ones in Cerrado. This data set is the first to compile VTMax values for South American herpetofauna, along with detailed experimental information such as heating rates and time to reach VTMax . This data set provides a baseline for understanding thermal tolerances and requirements of Neotropical ectothermic vertebrate species, which might be useful for future research on the impact of climate change and to test novel ecological hypotheses. There are no copyright or proprietary restrictions except that this data paper should be cited when data are used for publications. In addition, the authors would appreciated being informed of research projects or teaching purposes when these data are used.
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Lagartos , Reptiles , Anfibios , Animales , Brasil , Ecosistema , Reptiles/fisiología , TemperaturaRESUMEN
Ectotherms depend on temperature to maintain their physiological functions and through behavioral changes, they can avoid overheating in their habitats. The voluntary thermal maximum (VTMax ) represents the maximum temperature tolerated by individuals before actively moving to a colder place. However, if and how VTMax might change after capture and in captivity remains understudied. We investigate if measurements taken in captivity are a good proxy for thermal tolerance of wild individuals. As thermal history has been shown to affect behavioral response and physiological parameters, herein we hypothesized that VTMax of the neotropical viper Bothrops pauloensis varies throughout the captivity period. We measured the VTMax of individuals immediately after capture and in three trials during a short-term period in captivity. Measurements were done by recording their body temperature at which they exited a heating box experimental setup. In contrast to our hypothesis, the VTMax was not significantly affected by time in captivity but there was interindividual variation. There were also no significant differences between field and captivity measurements, in spite of the small effect size. Our results indicate that the VTMax of this snake population is not affected by a short-term captivity period. Furthermore, an invariant VTMax might indicate low phenotypic plasticity, as individuals do not appear to adjust their tolerance to short-term exposure to higher temperatures and potential vulnerability to threats such as global warming. We expect that our results can contribute to understanding the effect of captivity on thermal tolerance in neotropical squamates, allowing for insights into their thermal physiology and ecology.
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Conducta Animal/fisiología , Regulación de la Temperatura Corporal/fisiología , Bothrops/fisiología , Crianza de Animales Domésticos , Animales , Femenino , MasculinoRESUMEN
Most of the literature on temperature-organism interactions rely on mean temperature (mostly air), disregarding the real complexity of this variable. There is a growing consensus about the importance of considering the temperature fluctuations as a mechanism improving organism's performance. Tadpoles are small body size ectotherm organisms that behave isothermally with their environment. As such, are good models for studying their thermal biology relative to their immediate environment. We studied six anuran tadpole species in North Patagonia, Alsodes gargola, Hylorina sylvatica, Batrachyla taeniata, Pleurodema thaul, P. bufoninum and Rhinella spinulosa, distributed in a West-East altitudinal cline with different environments and thermal conditions. We evaluated the relationship between thermal descriptors at a local scale and the thermal biology patterns of these temperate tadpoles. We estimated thermal tolerance limits and thermal sensitivity of locomotion of each species. The different aquatic environments showed important differences in local thermal conditions, associated with observed differences in the thermal traits in these tadpoles. Species exposed to lower temperature fluctuations and lower environmental mean temperatures showed lower swimming optimal temperatures and narrower thermal tolerance ranges. We found greater variability in the upper than in the lower critical limits in these Patagonian anuran tadpoles. Minimum critical temperatures were close to freezing temperature, possibly in detriment of their tolerance to high temperatures. Overall, our results suggest that these species are adapted to low temperatures. Finally, warming tolerances and predicted thermal safety margins, show that none of the studied species appear to be under thermal stress that may compromise their survival at the present time or in the near future, under a moderate climate change scenario.
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Anuros/fisiología , Larva/fisiología , Termotolerancia , Animales , Argentina , Locomoción , TemperaturaRESUMEN
Phenotypic evolution is often exceptionally rapid on islands, resulting in numerous, ecologically diverse species. Although adaptive radiation proceeds along various phenotypic axes, the island effect of faster evolution has been mostly tested with regard to morphology. Here, we leveraged the physiological diversity and species richness of Anolis lizards to examine the evolutionary dynamics of three key traits: heat tolerance, body temperature, and cold tolerance. Contrary to expectation, we discovered slower heat tolerance evolution on islands. Additionally, island species evolve toward higher optimal body temperatures than mainland species. Higher optima and slower evolution in upper physiological limits are consistent with the Bogert effect, or evolutionary inertia due to thermoregulation. Correspondingly, body temperature is higher and more stable on islands than on the American mainland, despite similarity in thermal environments. Greater thermoregulation on islands may occur due to ecological release from competitors and predators compared to mainland environments. By reducing the costs of thermoregulation, ecological opportunity on islands may actually stymie, rather than hasten, physiological evolution. Our results emphasize that physiological diversity is an important axis of ecological differentiation in the adaptive radiation of anoles, and that behavior can impart distinct macroevolutionary footprints on physiological diversity on islands and continents.
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Evolución Biológica , Regulación de la Temperatura Corporal , Temperatura Corporal , Rasgos de la Historia de Vida , Lagartos/fisiología , Animales , Islas , Filogenia , TermotoleranciaRESUMEN
Ectotherms are vulnerable to climate change, given their dependence on temperature, and amphibians are particularly interesting because of their complex life cycle. Tadpoles may regulate their body temperature by using suitable thermal microhabitats. Thus, their physiological responses are the result of adjustment to the local thermal limits experienced in their ponds. We studied three anuran tadpole species present in Argentina and Chile: Pleurodema thaul and Pleurodema bufoninum that are seasonal and have broad geographic ranges, and Batrachyla taeniata, a geographically restricted species with overwintering tadpoles. Species with restricted distribution are more susceptible to climate change than species with broader distribution that may cope with potential climatic changes in the environments in which they occur. We aim to test whether these species can buffer the potential effects of climate warming. We used ecological niche models and the outcomes of their thermal attributes (critical thermal limits, optimal temperature, and locomotor performance breadth) as empirical evidence of their capacity. We found that Pleurodema species show broader performance curves, related to their occurrence, while the geographically restricted B. taeniata shows a narrower thermal breadth, but is faster in warmer conditions. The modeled distributions and empirical physiological results suggest no severe threats for these three anurans. However, the risk level is increasing and a retraction of their distribution range might be possible for Pleurodema species, and some local population extinctions may happen, particularly for the narrowly distributed B. taeniata.
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Anuros/fisiología , Regulación de la Temperatura Corporal/fisiología , Cambio Climático , Animales , Argentina , Chile , Ecosistema , Extinción Biológica , LarvaRESUMEN
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.
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Conducta Animal , Lagartos/fisiología , Pigmentación , Agresión , Animales , Temperatura Corporal , Cabeza/anatomía & histología , Lagartos/anatomía & histología , Masculino , Movimiento , Tamaño de los Órganos , Resistencia FísicaRESUMEN
In anurans, changes in ambient temperature influence body temperature and, therefore, energy consumption. These changes ultimately affect energy supply and, consequently, heart rate (HR). Typically, anurans living in different thermal environments have different thermal sensitivities, and these cannot be distinguished by changes in HR. We hypothesized that Rhinella jimi (a toad from a xeric environment that lives in a wide range of temperatures) would have a lower thermal sensitivity regarding cardiac control than R. icterica (originally from a tropical forest environment with a more restricted range of ambient temperatures). Thermal sensitivity was assessed by comparing animals housed at 15° and 25°C. Cardiac control was estimated by heart rate variability (HRV) and heart rate complexity (HRC). Differences in HRV between the two temperatures were not significant (P=0.214 for R. icterica and P=0.328 for R. jimi), whereas HRC differences were. All specimens but one R. jimi had a lower HRC at 15°C (all P<0.01). These results indicate that R. jimi has a lower thermal sensitivity and that cardiac control is not completely dependent on the thermal environment because HRC was not consistently different between temperatures in all R. jimi specimens. This result indicates a lack of evolutive trade-offs among temperatures given that heart rate control at 25°C is potentially not a constraint to heart rate control at 15°C.
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Understanding how quickly physiological traits evolve is a topic of great interest, particularly in the context of how organisms can adapt in response to climate warming. Adjustment to novel thermal habitats may occur either through behavioural adjustments, physiological adaptation or both. Here, we test whether rates of evolution differ among physiological traits in the cybotoids, a clade of tropical Anolis lizards distributed in markedly different thermal environments on the Caribbean island of Hispaniola. We find that cold tolerance evolves considerably faster than heat tolerance, a difference that results because behavioural thermoregulation more effectively shields these organisms from selection on upper than lower temperature tolerances. Specifically, because lizards in very different environments behaviourally thermoregulate during the day to similar body temperatures, divergent selection on body temperature and heat tolerance is precluded, whereas night-time temperatures can only be partially buffered by behaviour, thereby exposing organisms to selection on cold tolerance. We discuss how exposure to selection on physiology influences divergence among tropical organisms and its implications for adaptive evolutionary response to climate warming.