Eric J. Gangloff

Reptile Embryos Lack the Opportunity to Thermoregulate by Moving within the Egg

Historically, egg-bound reptile embryos were thought to passively thermoconform to the nest environment. However, recent observations of thermal taxis by embryos of multiple reptile species have led to the widely discussed hypothesis that embryos behaviorally thermoregulate. Because temperature affects development, such thermoregulation could allow embryos to control their fate far more than historically assumed. We assessed the opportunity for embryos to behaviorally thermoregulate in nature by examining thermal gradients within natural nests and eggs of the common snapping turtle (Chelydra serpentina; which displays embryonic thermal taxis) and by simulating thermal gradients within nests across a range of nest depths, egg sizes, and soil types. We observed little spatial thermal variation within nests, and thermal gradients were poorly transferred to eggs. Furthermore, thermal gradients sufficiently large and constant for behavioral thermoregulation were not predicted to occur in our simulations. Gradients of biologically relevant magnitude have limited global occurrence and reverse direction twice daily when they do exist, which is substantially faster than embryos can shift position within the egg. Our results imply that reptile embryos will rarely, if ever, have the opportunity to behaviorally thermoregulate by moving within the egg. We suggest that embryonic thermal taxis instead represents a play behavior, which may be adaptive or selectively neutral, and results from the mechanisms for behavioral thermoregulation in free-living stages coming online prior to hatching.

Improved Student Learning through a Faculty Learning Community: How Faculty Collaboration Transformed a Large-Enrollment Course from Lecture to Student Centered

The authors describe how a faculty learning community was leveraged to implement active-learning strategies and improve student learning in a large-enrollment introductory course.

Hormonal and metabolic responses to upper temperature extremes in divergent life-history ecotypes of a garter snake

ABSTRACT Extreme temperatures constrain organismal physiology and impose both acute and chronic effects. Additionally, temperature-induced hormone-mediated stress response pathways and energetic trade-offs are important drivers of life-history variation. This study employs an integrative approach to quantify acute physiological responses to high temperatures in divergent life-history ecotypes of the western terrestrial garter snake (Thamnophis elegans). Using wild-caught animals, we measured oxygen consumption rate and physiological markers of hormonal stress response, energy availability and anaerobic respiration in blood plasma across five ecologically relevant temperatures (24, 28, 32, 35 and 38°C; 3 h exposure). Corticosterone, insulin and glucose concentrations all increased with temperature, but with different thermal response curves, suggesting that high temperatures differently affect energy-regulation pathways. Additionally, oxygen consumption rate increased without plateau and lactate concentration did not increase with temperature, challenging the recent hypothesis that oxygen limitation sets upper thermal tolerance limits. Finally, animals had similar physiological thermal responses to high-temperature exposure regardless of genetic background, suggesting that local adaptation has not resulted in fixed differences between ecotypes. Together, these results identify some of the mechanisms by which higher temperatures alter hormonal-mediated energy balance in reptiles and potential limits to the flexibility of this response. Summary: Snakes from divergent life-history ecotypes are affected similarly in their response to high temperatures, which induce a physiological stress response and affect energy-regulation pathways.

Developmental and Immediate Thermal Environments Shape Energetic Trade-Offs, Growth Efficiency, and Metabolic Rate in Divergent Life-History Ecotypes of the Garter Snake Thamnophis elegans

Interactions at all levels of ecology are influenced by the rate at which energy is obtained, converted, and allocated. Trade-offs in energy allocation within individuals in turn form the basis for life-history theory. Here we describe tests of the influences of temperature, developmental environment, and genetic background on measures of growth efficiency and resting metabolic rate in an ectothermic vertebrate, the western terrestrial garter snake (Thamnophis elegans). After raising captive-born snakes from divergent life-history ecotypes on thermal regimes mimicking natural habitat differences (2 × 2 experimental design of ecotype and thermal environment), we measured oxygen consumption rate at temperatures spanning the activity range of this species. We found ecotypic differences in the reaction norms of snakes across the measured range of temperatures and a temperature-dependent allometric relationship between mass and metabolic rate predicted by the metabolic-level boundaries hypothesis. Additionally, we present evidence of within-individual trade-offs between growth efficiency and resting metabolic rate, as predicted by classic life-history theory. These observations help illuminate the ultimate and proximate factors that underlie variation in these interrelated physiological and life-history traits.

Effects of low-oxygen conditions on embryo growth in the painted turtle, Chrysemys picta.

Low-oxygen conditions (hypoxia; <21% O2 ) are considered unfavorable for growth; yet, embryos of many vertebrate taxa develop successfully in hypoxic subterranean environments. Although enhanced tolerance to hypoxia has been demonstrated in adult reptiles, such as in the painted turtle (Chrysemys picta), its effects on sensitive embryo life stages warrant attention. We tested the hypothesis that short-term hypoxia negatively affects growth during day 40 of development in C. picta, when O2 demands are highest in embryos. A brief, but severe, hypoxic event (5% O2 for 0.5 h) moderately affected embryo growth, causing a 13% reduction in mass (relative to a normoxic control). The same condition had no effect during day 27; instead, a nearly anoxic event (1% O2 for 72 h) caused a 5% mass reduction. All embryos survived the egg incubation period. Our study supports the assumption that reptilian embryos are resilient to intermittently low O2 in subterranean nests. Further work is needed to ascertain responses to suboptimal O2 levels while undergoing dynamic changes in developmental physiology.

Reptile embryos are not capable of behavioral thermoregulation in the egg

Reptile embryos have recently been observed moving within the egg in response to temperature, raising the exciting possibility that embryos might behaviorally thermoregulate analogous to adults. However, the conjecture that reptile embryos have ample opportunity and capacity to adaptively control their body temperature warrants further discussion. Using turtles as a model, we discuss the spatiotemporal constraints to movement in reptile embryos. We demonstrate that, as embryos grow, the internal egg space rapidly diminishes such that the temporal window for appreciable displacement is confined to stages that feature incomplete neuromuscular differentiation. During this time, muscles are insufficiently developed to actively and consistently control movement. These constraints are well illustrated by the Chinese softshelled turtle (Pelodiscus sinensis), the first reptile reported to behaviorally thermoregulate. Furthermore, sporadic embryo activity peaks after the temperature‐sensitive period in species with temperature‐dependent sex determination, thus nullifying the opportunity for embryos to exhibit control over this important phenotype. These embryonic constraints add to previously‐identified environmental constraints on behavioral thermoregulation by reptile embryos. We discuss alternative hypotheses to explain previously reported patterns of behavioral thermoregulation. Based on a holistic consideration of embryonic limitations, we conclude that reptile embryos are generally unable to adaptively behaviorally thermoregulate within the egg.

Physiology at near-critical temperatures, but not critical limits, varies between two lizard species that partition the thermal environment

The mechanisms that mediate the interaction between the thermal environment and species ranges are generally uncertain. Thermal environments may directly restrict species when environments exceed tolerance limits (i.e. the fundamental niche). However, thermal environments might also differentially affect relative performance among species prior to fundamental tolerances being met (i.e. the realized niche). We examined stress physiology (plasma glucose and corticosterone), mitochondrial performance and the muscle metabolome of congeneric lizards that naturally partition the thermal niche, Elgaria multicarinata (southern alligator lizards; SALs) and Elgaria coerulea (northern alligator lizards; NALs), in response to a thermal challenge to quantify variation in physiological performance and tolerance. Both NAL and SAL displayed physiological stress in response to high temperature, but neither showed signs of irreversible damage. NAL displayed a higher baseline mitochondrial respiration rate than SAL. Moreover, NAL substantially adjusted their physiology in response to thermal challenge, whereas SAL did not. For example, the metabolite profile of NAL shifted with changes in key energetic molecules, whereas these were unaffected in SAL. Our results indicate that near-critical high temperatures should incur greater energetic cost in NAL than SAL via an elevated metabolic rate and changes to the metabolome. Thus, SAL displace NAL in warm environments that are within NALs fundamental thermal niche, but relatively costly. Our results suggest that subcritical thermal events can contribute to biogeographic patterns via physiological differences that alter the relative costs of living in warm or cool environments.

Merging the "Morphology-Performance-Fitness" Paradigm and Life-History Theory in the Eagle Lake Garter Snake Research Project.

SYNOPSIS The morphology-performance-fitness paradigm for testing selection on morphological traits has seen decades of successful application. At the same time, life-history approaches using matrix methods and perturbation studies have also allowed the direct estimate of selection acting on vital rates and the traits that comprise them. Both methodologies have been successfully applied to the garter snakes of the long-term Eagle Lake research project to reveal selection on morphology, such as color pattern, number of vertebrae, and gape size; and life-history traits such as birth size, growth rates, and juvenile survival. Here we conduct a reciprocal transplant study in a common laboratory environment to study selection on morphology and life-history. To place our results in the ecomorphology paradigm, we measure performance outcomes (feeding rates, growth, insulin-like growth factor 1 titers) of morphological variation (body size, condition) and their fitness consequences for juvenile survival-a trait that has large fitness sensitivities in these garter snake populations, and therefore is thought to be subject to strong selection. To better merge these two complementary theories, we end by discussing our findings in a nexus of morphology-performance-fitness-life history to highlight what these approaches, when combined, can reveal about selection in the wild.

Integrating behaviour into the pace-of-life continuum: Divergent levels of activity and information gathering in fast- and slow-living snakes

An animals life history, physiology, and behaviour can be shaped by selection in a manner that favours strong associations among these aspects of an integrated phenotype. Recent work combining animal personality and life-history theory proposes that animals with faster life-history strategies (i.e., fast growth, high annual reproductive rate, short lifespan) should exhibit higher general activity levels relative to those with slower life-history strategies, but empirical tests of within-species variation in these traits are lacking. In garter snakes from ecotypes which are known to differ in ecology, life-history strategy, and physiology, we tested for differences in tongue-flick rate as a measure of information gathering and movement patterns as a measure of general activity. Tongue flicks and movement were strongly positively correlated and both behaviours were repeatable across trials. Snakes from the fast-living ecotype were more active and showed evidence of habituation. The slow-living ecotype maintained low levels of activity throughout the trials. We propose that environmental factors, such as high predation, experienced by the fast-living ecotype select for both increased information-gathering and activity levels to facilitate efficient responses to repeated challenges. Thus, we offer evidence that behaviour is an important component of co-evolved suites of traits forming a general pace-of-life continuum in this system.

High Temperature, Oxygen, and Performance: Insights from Reptiles and Amphibians

Much recent theoretical and empirical work has sought to describe the physiological mechanisms underlying thermal tolerance in animals. Leading hypotheses can be broadly divided into two categories that primarily differ in organizational scale: 1) high temperature directly reduces the function of subcellular machinery, such as enzymes and cell membranes, or 2) high temperature disrupts system-level interactions, such as mismatches in the supply and demand of oxygen, prior to having any direct negative effect on the subcellular machinery. Nonetheless, a general framework describing the contexts under which either subcellular component or organ system failure limits organisms at high temperatures remains elusive. With this commentary, we leverage decades of research on the physiology of ectothermic tetrapods (amphibians and non-avian reptiles) to address these hypotheses. Available data suggest both mechanisms are important. Thus, we expand previous work and propose the Hierarchical Mechanisms of Thermal Limitation (HMTL) hypothesis, which explains how subcellular and organ system failures interact to limit performance and set tolerance limits at high temperatures. We further integrate this framework with the thermal performance curve paradigm commonly used to predict the effects of thermal environments on performance and fitness. The HMTL framework appears to successfully explain diverse observations in reptiles and amphibians and makes numerous predictions that remain untested. We hope that this framework spurs further research in diverse taxa and facilitates mechanistic forecasts of biological responses to climate change.