Publications
Welcome! Below you will find my publications, starting with my most recent work. Note that I have provided a link to the publication at the end of the author list below each publication. I have also bolded any co-authors that were trained as mentees. If you have trouble accessing any of the publications, please feel free to reach out to my e-mail (riddell@unc.edu) to request a copy.
2024
Range shifts as drivers of niche breadth and dispersal ability in wild populationsLustenhouwer, N. and E.A. Riddell. Journal of Animal Ecology, In press. LINK
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Research Highlight: Edwards et al. (2024) make an important contribution to this growing field by demonstrating a compelling case of phenotypic differentiation during native range expansion in the green treefrog (Hyla cinerea). These frogs have expanded their range poleward in North America over the past few decades, representing a rare example of rapid contemporary range shifts in amphibians. Edwards and colleagues collected frogs from wild populations in the historic range and at the expanding range edge and found increased dispersal ability and thermal niche breadth in populations at the range edge. They then address the forecasting implications of their findings by investigating how species distribution models fit separately to the historic and expanded range could better account for this intraspecific variation.Poore, C.L. , E.J. Ibarra-Garibay, A.L. Toth, and E.A. Riddell. Proceedings of the Royal Society B. In press. LINK
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Indices of climate vulnerability are used to predict species’ vulnerability to climate change based on intrinsic physiological traits such as thermal tolerance, thermal sensitivity, and thermal acclimation, but rarely is the consistency among indices evaluated simultaneously. We compared the thermal physiology of queen bumble bees between a species experiencing local declines (Bombus auricomus) and a species exhibiting continent-wide increases (B. impatiens). We conducted a multi-week acclimation experiment under simulated climate warming to measure critical thermal maximum (CTmax), critical thermal minimum (CTmin), the thermal sensitivity of metabolic rate and water loss rate, and acclimation in each of these traits. We also measured survival throughout the experiment and after the thermal tolerance trials. Neither species acclimated to the temperature treatments by adjusting any physiological trait. We found conflicting patterns among indices of vulnerability within and between species. We also found that individuals with the highest CTmax exhibited the lowest survival following the thermal tolerance trial. Our study highlights inconsistent patterns across multiple indices of climate vulnerability within and between species, indicating that physiological studies measuring only one index of climate vulnerability may be limited in their ability to inform species’ responses to environmental change.Porter, C.K. , K.M. Cortes, O. Levy, and E.A. Riddell. Journal of Experimental Biology, jeb. 247357. LINK
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Scholander-Irving curves describe the relationship between ambient temperature and metabolic rate and are fundamental to understanding the energetic demands of homeothermy. However, Scholander-Irving curves are typically measured in dry air, which is not representative of the humidity many organisms experience in nature. Consequently, it is unclear (1) whether Scholander-Irving curves (especially below thermoneutrality) are altered by humidity, given the effects of humidity on thermal properties of air, and (2) whether physiological responses associated with Scholander-Irving curves in the lab reflect organismal performance in humid field conditions. We used laboratory experiments and biophysical models to test the effects of humidity on the thermoregulatory physiology of tree swallows (Tachycineta bicolor). We also tested whether physiological responses measured under lab conditions were correlated with field body temperatures and nestling provisioning rates. We found that humidity reduced rates of evaporative water loss but did not have large effects on body temperature or metabolic rate, suggesting that swallows can decouple evaporative cooling, body temperature and metabolic rate. Although the effect of humidity on metabolic rate in the lab was small, our biophysical models indicated that energetic costs of thermoregulation were ∼8% greater in simulations that used metabolic rates from birds in humid compared with dry conditions. Finally, we found mixed evidence that physiological responses measured in the lab under humid or dry conditions were associated with body temperature and nest provisioning rates in the field. Our results help clarify the effect of humidity on endotherm thermoregulation, which may help forecast organismal responses to environmental change.Riddell, E.A. , I.J. Burger, M.M. Muñoz, S.J. Weaver, M.W. Womack. Integrative and Comparative Biology, 64: 366–376. LINK
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Terrestrial environments pose many challenges to organisms, but perhaps one of the greatest is the need to breathe while maintaining water balance. Breathing air requires thin, moist respiratory surfaces, and thus the conditions necessary for gas exchange are also responsible for high rates of water loss that lead to desiccation. Across the diversity of terrestrial life, water loss acts as a universal cost of gas exchange and thus imposes limits on respiration. Amphibians are known for being vulnerable to rapid desiccation, in part because they rely on thin, permeable skin for cutaneous respiration. Yet, we have a limited understanding of the relationship between water loss and gas exchange within and among amphibian species. In this study, we evaluated the hydric costs of respiration in amphibians using the transpiration ratio, which is defined as the ratio of water loss (mol H2O d−1) to gas uptake (mol O2 d−1). A high ratio suggests greater hydric costs relative to the amount of gas uptake. We compared the transpiration ratio of amphibians with that of other terrestrial organisms to determine whether amphibians had greater hydric costs of gas uptake relative to plants, insects, birds, and mammals. We also evaluated the effects of temperature, humidity, and body mass on the transpiration ratio both within and among amphibian species. We found that hydric costs of respiration in amphibians were two to four orders of magnitude higher than the hydric costs of plants, insects, birds, and mammals. We also discovered that larger amphibians had lower hydric costs than smaller amphibians, at both the species- and individual-level. Amphibians also reduced the hydric costs of respiration at warm temperatures, potentially reflecting adaptive strategies to avoid dehydration while also meeting the demands of higher metabolic rates. Our results suggest that cutaneous respiration is an inefficient mode of respiration that produces the highest hydric costs of respiration yet to be measured in terrestrial plants and animals. Yet, amphibians largely avoid these costs by selecting aquatic or moist environments, which may facilitate more independent evolution of water loss and gas exchange.Burger, I.J. , E. Carter, L. Magner, M.M. Muñoz, M.W. Sears, B. Fitzpatrick, and E.A. Riddell. Functional Ecology, 38:143-152. LINK
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Hybridization between species affects biodiversity and population sustainability in numerous ways, many of which depend on the fitness of the hybrid relative to the parental species. Hybrids can exhibit fitter phenotypes compared to the parental lineages, and this ‘hybrid vigour’ can then lead to the extinction of one or both parental lines. In this study, we analysed the relationship between water loss and gas exchange to compare physiological performance among three tiger salamander genotypes—the native California tiger salamander (CTS), the invasive barred tiger salamanders (BTS) and CTS × BTS hybrids across multiple temperatures (13.5°C, 20.5°C and 23.5°C). We developed a new index of performance, the water-gas exchange ratio (WGER), which we define as the ratio of gas exchange to evaporative water loss (μL VO2/μL H2O). The ratio describes the ability of an organism to support energetically costly activities with high levels of gas exchange while simultaneously limiting water loss to lower desiccation risk. We used flow through respirometry to measure the thermal sensitivity of metabolic rate and resistance to water loss of each salamander genotype to compare indices of physiological performance. We found that temperature had a significant effect on metabolic rate and resistance to water loss, with both traits increasing as temperatures warmed. Across genotypes, we found that hybrids have a higher WGER than the native CTS, owing to a higher metabolic rate despite having a lower resistance to water loss. These results provide a greater insight into the physiological mechanisms driving hybrid vigour and offer a potential explanation for the rapid spread of salamander hybrids. More broadly, our introduction of the WGER may allow for species- or lineage-wide comparisons of physiological performance across changing environmental conditions, highlighting the insight that can be gleaned from multitrait analysis of organism performance.2023
Adaptive and non-adaptive convergent evolution in feather reflectance of California Chanel Islands songbirdsPorter, C.K., F.G. Romero, D.C. Adams, R.C.K. Bowie, and E.A. Riddell. Proceedings of the Royal Society B, 290: 20231914. LINK
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Convergent evolution is widely regarded as a signature of adaptation. However, testing the adaptive consequences of convergent phenotypes is challenging, making it difficult to exclude non-adaptive explanations for convergence. Here, we combined feather reflectance spectra and phenotypic trajectory analyses with visual and thermoregulatory modelling to test the adaptive significance of dark plumage in songbirds of the California Channel Islands. By evolving dark dorsal plumage, island birds are generally less conspicuous to visual-hunting raptors in the island environment than mainland birds. Dark dorsal plumage also reduces the energetic demands associated with maintaining homeothermy in the cool island climate. We also found an unexpected pattern of convergence, wherein the most divergent island populations evolved greater reflectance of near-infrared radiation. However, our heat flux models indicate that elevated near-infrared reflectance is not adaptive. Analysis of feather microstructure suggests that mainland-island differences are related to coloration of feather barbs and barbules rather than their structure. Our results indicate that adaptive and non-adaptive mechanisms interact to drive plumage evolution in this system. This study sheds light on the mechanisms driving the association between dark colour and wet, cold environments across the tree of life, especially in island birds.Riddell, E.A. , I.J. Burger, T.L. Tyner-Swanson, J. Biggerstaff, M.M. Muñoz, O. Levy, and C.K. Porter. Journal of Experimental Biology, 226: jeb245543. LINK
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Mechanistic niche models are computational tools developed using biophysical principles to address grand challenges in ecology and evolution, such as the mechanisms that shape the fundamental niche and the adaptive significance of traits. Here, we review the empirical basis of mechanistic niche models in biophysical ecology, which are used to answer a broad array of questions in ecology, evolution and global change biology. We describe the experiments and observations that are frequently used to parameterize these models and how these empirical data are then incorporated into mechanistic niche models to predict performance, growth, survival and reproduction. We focus on the physiological, behavioral and morphological traits that are frequently measured and then integrated into these models. We also review the empirical approaches used to incorporate evolutionary processes, phenotypic plasticity and biotic interactions. We discuss the importance of validation experiments and observations in verifying underlying assumptions and complex processes. Despite the reliance of mechanistic niche models on biophysical theory, empirical data have and will continue to play an essential role in their development and implementation.Ballinger M.A., K.L. Mack, S.M. Durkin, E.A. Riddell, and M.W. Nachman. Proceedings of the National Academy of Sciences U.S.A. 120: e2214614120. LINK
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Changes in gene expression are thought to play a major role in adaptive evolution. While it is known that gene expression is highly sensitive to the environment, very few studies have determined the influence of genetic and environmental effects on adaptive gene expression differences in natural populations. Here, we utilize allele-specific expression to characterize cis and trans gene regulatory divergence in temperate and tropical house mice in two metabolic tissues under two thermal conditions. First, we show that gene expression divergence is pervasive between populations and across thermal conditions, with roughly 5 to 10% of genes exhibiting genotype-by-environment interactions. Second, we found that most expression divergence was due to cis-regulatory changes that were stable across temperatures. In contrast, patterns of expression plasticity were largely attributable to trans-effects, which showed greater sensitivity to temperature. Nonetheless, we found a small subset of temperature-dependent cis-regulatory changes, thereby identifying loci underlying expression plasticity. Finally, we performed scans for selection in wild house mice to identify genomic signatures of rapid adaptation. Genomic outliers were enriched in genes with evidence for cis-regulatory divergence. Notably, these genes were associated with phenotypes that affected body weight and metabolism, suggesting that cis-regulatory changes are a possible mechanism for adaptive body size evolution between populations. Our results show that gene expression plasticity, largely controlled in trans, may facilitate the colonization of new environments, but that evolved changes in gene expression are largely controlled in cis, illustrating the genetic and nongenetic mechanisms underlying the establishment of populations in new environments.Buckley, L.B., B. Ortiz, I. Caruso, A. John, O. Levy, A. Meyer, E.A. Riddell, Y. Sakairi, J. Simonis. PLoS Climate, 2.8: e0000139. LINK
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Much understanding of organismal responses to climate change and variability relies on the assumption that body temperatures are equal to temporally averaged air temperatures high above the ground. However, most organisms experience microclimates near the ground and acute exposure to solar and thermal radiation and thermal extremes can substantially elevate or depress their body temperatures. We introduce the TrenchR package, which aids in Translating Environmental Change into organismal responses. The package includes microclimate models to vertically scale weather station data to organismal heights. Additional functions model and temporally partition air and soil temperatures and solar radiation. TrenchR biophysical modeling tools include both general models for heat flows and specific models to predict body temperatures for a variety of ectothermic taxa. We also offer utility functions to aid in estimating the organismal and environmental parameters needed for biophysical ecology. TrenchR focuses on simple and modular functions so users can create transparent and flexible models for biophysical applications. The package aims to introduce and enable microclimate and biophysical modeling to improve ecological and evolutionary forecasting. We further this aim through a series of educational modules that introduce the field of biophysical ecology.Riddell, E.A. , M. Mutanen, C.K. Ghalambor. Global Change Biology, gcb.16830.. LINK
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Species' thermal tolerances are used to estimate climate vulnerability, but few studies consider the role of the hydric environment in shaping thermal tolerances. As environments become hotter and drier, organisms often respond by limiting water loss to lower the risk of desiccation; however, reducing water loss may produce trade-offs that lower thermal tolerances if respiration becomes inhibited. Here, we measured the sensitivity of water loss rate and critical thermal maximum (CTmax) to precipitation in nature and laboratory experiments that exposed click beetles (Coleoptera: Elateridae) to acute- and long-term humidity treatments. We also took advantage of their unique clicking behavior to characterize subcritical thermal tolerances. We found higher water loss rates in the dry acclimation treatment compared to the humid, and water loss rates were 3.2-fold higher for individuals that had experienced a recent precipitation event compared to individuals that had not. Acute humidity treatments did not affect CTmax, but precipitation indirectly affected CTmax through its effect on water loss rates. Contrary to our prediction, we found that CTmax was negatively associated with water loss rate, such that individuals with high water loss rate exhibited a lower CTmax. We then incorporated the observed variation of CTmax into a mechanistic niche model that coupled leaf and click beetle temperatures to predict climate vulnerability. The simulations indicated that indices of climate vulnerability can be sensitive to the effects of water loss physiology on thermal tolerances; moreover, exposure to temperatures above subcritical thermal thresholds is expected to increase by as much as 3.3-fold under future warming scenarios. The correlation between water loss rate and CTmax identifies the need to study thermal tolerances from a “whole-organism” perspective that considers relationships between physiological traits, and the population-level variation in CTmax driven by water loss rate complicates using this metric as a straightforward proxy of climate vulnerability.Mason, N.A., E.A. Riddell, F. Romero, C. Cicero, R.C.K. Bowie. The American Naturalist, 201(2). LINK
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Animal coloration serves many biological functions and must therefore balance potentially competing selective pressures. For example, many animals have camouflage in which coloration matches the visual background that predators scan for prey. However, different colors reflect different amounts of solar radiation and may therefore have thermoregulatory implications as well. In this study, we examined geographic variation in dorsal patterning, coloration, and solar reflectance among horned larks (Eremophila alpestris) of the western United States. We found that plumage brightness was positively associated with soil granularity, aridity, and temperature. Plumage redness—both in terms of saturation (i.e., chroma) and hue—was positively associated with soil redness and temperature, while plumage patterning was positively associated with soil granularity. Together, these plumage-environment associations support both background matching and Gloger’s rule, a widespread ecogeographic pattern in animal coloration. We also constructed thermoregulatory models that estimated cooling benefits provided by solar reflectance profiles of the dorsal plumage of each specimen based on the collection site. We found increased cooling benefits in hotter, more arid environments. Finally, cooling benefits were positively associated with residual brightness, such that individuals that were brighter than expected based on environmental conditions also had higher cooling benefits, suggesting a trade-off between camouflage and thermoregulation. Together, these data suggest that natural selection has balanced camouflage and thermoregulation in horned larks, and they illustrate how multiple competing evolutionary pressures may interact to shape geographic variation in adaptive phenotypes.2022
Mechanistic forecasts of species responses to climate change: the promise of biophysical ecologyBriscoe, N., S. Morris, P. Mathewson, L. Buckley, M. Jusup, O. Levy, I. Maclean, S. Pincebourde, E.A. Riddell, J. Roberts, R. Schouten, M.W. Sears, M. Kearney. Global Change Biology. gcb.16557. LINK
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A core challenge in global change biology is to predict how species will respond to future environmental change and to manage these responses. To make such predictions and management actions robust to novel futures, we need to accurately characterize how organisms experience their environments and the biological mechanisms by which they respond. All organisms are thermodynamically connected to their environments through the exchange of heat and water at fine spatial and temporal scales and this exchange can be captured with biophysical models. Although mechanistic models based on biophysical ecology have a long history of development and application, their use in global change biology remains limited despite their enormous promise and increasingly accessible software. We contend that greater understanding and training in the theory and methods of biophysical ecology is vital to expand their application. Our review shows how biophysical models can be implemented to understand and predict climate change impacts on species' behavior, phenology, survival, distribution, and abundance. It also illustrates the types of outputs that can be generated, and the data inputs required for different implementations. Examples range from simple calculations of body temperature at a particular site and time, to more complex analyses of species' distribution limits based on projected energy and water balances, accounting for behavior and phenology. We outline challenges that currently limit the widespread application of biophysical models relating to data availability, training, and the lack of common software ecosystems. We also discuss progress and future developments that could allow these models to be applied to many species across large spatial extents and timeframes. Finally, we highlight how biophysical models are uniquely suited to solve global change biology problems that involve predicting and interpreting responses to environmental variability and extremes, multiple or shifting constraints, and novel abiotic or biotic environments.Riddell, E.A., J.L. Patton, & S.R. Beissinger. Evolution, evo.14463. LINK
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Phenotypic convergence across distantly related taxa can be driven by similar selective pressures from the environment or intrinsic constraints. The roles of these processes on physiological strategies, such as homeothermy, are poorly understood. We studied the evolution of thermal properties of mammalian pelage in a diverse community of rodents inhabiting the Mojave Desert, USA. We used a heat flux device to measure the thermal insulation of museum specimens and determined whether thermal properties were associated with habitat preferences while assessing phylogenetic dependence. Species that prefer arid habitats exhibited lower conductivity and thinner pelage relative to species with other habitat preferences. Despite being thinner, the pelage of arid species exhibited comparable insulation to the pelage of the other species due to its lower conductivity. Thus, arid species have insulative pelage while simultaneously benefitting from thin pelage that promotes convective cooling. We found no evidence of intrinsic constraints or phylogenetic dependence, indicating pelage readily evolves to environmental pressures. Thermoregulatory simulations demonstrated that arid specialists reduced energetic costs required for homeothermy by 14.5% by evolving lower conductivity, providing support for adaptive evolution of pelage. Our study indicates that selection for lower energetic requirements of homeothermy has shaped evolution of pelage thermal properties.Newman, J., E.A. Riddell, M.W. Sears, K. Barrett. Ecography, e06082. LINK
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Rapid global change has increased interest in developing ways to identify suitable refugia for species of conservation concern. Correlative and mechanistic species distribution models (SDMs) represent two approaches to generate spatially-explicit estimates of climate vulnerability. Correlative SDMs generate distributions using statistical associations between environmental variables and species presence data. In contrast, mechanistic SDMs use physiological traits and tolerances to identify areas that meet the conditions required for growth, survival and reproduction. Correlative approaches assume modeled environmental variables influence species distributions directly or indirectly; however, the mechanisms underlying these associations are rarely verified empirically. We compared habitat suitability predictions between a correlative-only SDM, a mechanistic SDM and a correlative framework that incorporated mechanistic layers (‘hybrid models'). Our comparison focused on green salamanders Aneides aeneus, a priority amphibian threatened by climate change throughout their disjunct range. We developed mechanistic SDMs using experiments to measure the thermal sensitivity of resistance to water loss (ri) and metabolism. Under current climate conditions, correlative-only, hybrid and mechanistic SDMs predicted similar overlap in habitat suitability; however, mechanistic SDMs predicted habitat suitability to extend into regions without green salamanders but known to harbor many lungless salamanders. Under future warming scenarios, habitat suitability depended on climate scenario and SDM type. Correlative and hybrid models predicted a 42% reduction or 260% increase in area considered to be suitable depending on the climate scenario. In mechanistic SDMs, energetically suitable habitat declined with both climate scenarios and was driven by the thermal sensitivity of ri. Our study indicates that correlative-only and hybrid approaches produce similar predictions of habitat suitability; however, discrepancies can arise for species that do not occupy their entire fundamental niche, which may hold consequences of conservation planning of threatened species.Ramirez, R.W. , E.A. Riddell, S.R. Beissinger, B.O. Wolf. Journal of Experimental Biology 225 (5), jeb243131. LINK
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Small mammals in hot deserts often avoid heat via nocturnality and fossoriality, and are thought to have a limited capacity to dissipate heat using evaporative cooling. Research to date has focused on thermoregulatory responses to air temperatures (Ta) below body temperature (Tb). Consequently, the thermoregulatory performance of small mammals exposed to high Ta is poorly understood, particularly responses across geographic and seasonal scales. We quantified the seasonal thermoregulatory performance of four cricetid rodents (Neotoma albigula, Neotoma lepida, Peromyscus eremicus, Peromyscus crinitus) exposed to high Ta, at four sites in the Mojave Desert. We measured metabolism, evaporative water loss and Tb using flow-through respirometry. When exposed to Ta≥Tb, rodents showed steep increases in Tb, copious salivation and limited evaporative heat dissipation. Most individuals were only capable of maintaining Ta–Tb gradients of ∼1°, resulting in heat tolerance limits (HTLs) in the range Ta=43–45°C. All species exhibited a thermoneutral Tb of ∼35–36°C, and Tb increased to maximal levels of ∼43°C. Metabolic rates and rates of evaporative water loss increased steeply in all species as Ta approached Tb. We also observed significant increases in resting metabolism and evaporative water loss from summer to winter at Ta within and above the thermoneutral zone. In contrast, we found few differences in the thermoregulatory performance within species across sites. Our results suggest that cricetid rodents have a limited physiological capacity to cope with environmental temperatures that exceed Tb and that a rapidly warming environment may increasingly constrain their nocturnal activity.Perryman, D.C., M.M. Pandit, E.A. Riddell, T.L. Sanders, I.A. Kanda, J.L. Grindstaff. Journal of Avian Biology, e02920. LINK
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Supplemental feeding is a common anthropogenic influence on wildlife which, dependent on natural food availability, can have positive or negative effects on physiological condition. For example, animals may respond negatively to supplemental feeding if the artificial food source increases disease exposure or there may be negative consequences from removal of a supplemental food source. We manipulated supplemental food availability in a wild population of eastern bluebirds Sialia sialis to examine the influence on body mass, physiological metrics and nesting success. Adult and nestling bluebirds were randomly assigned to one of three feeding groups. The first treatment group received mealworm Tenebrio molitor larvae inside nest boxes throughout the breeding attempt, the second treatment group received mealworms from nest completion until nestlings hatched, and the third treatment group received no supplementation. We collected blood samples from adults and nestlings to quantify bacterial killing ability, corticosterone levels and heterophil to lymphocyte ratios. As measures of nesting success, we quantified hatching success and fledging success. Supplement group tended to impact nestling mass near fledging; however, neither the physiological metrics nor the nesting success metrics differed significantly among experimental groups. Our results suggest eastern bluebird supplementation is largely neutral with the exception of its removal at the time of hatching, at least when natural food sources are abundant. Bird feeding by hobbyists may attract birds to locations with available nesting sites without demonstrably negative or positive effects, unless practiced inconsistently during breeding.Gunderson, A.R., E.A. Riddell, M.W. Sears, and E.B. Rosenblum. The American Naturalist 199 (5): 666-678. LINK
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Traits often contribute to multiple functions, complicating our understanding of the selective pressures that influence trait evolution. In the Chihuahuan Desert, predation is thought to be the primary driver of cryptic light coloration in three White Sands lizard species relative to the darker coloration of populations on adjacent dark soils. However, coloration also influences radiation absorption and thus animal body temperatures. We combined comparative physiological experiments and biophysical models to test for thermal consequences of evolving different color morphs in White Sands across the three species. While light and dark morphs have not evolved different physiological heat limits within species, differences in radiation absorption between morphs lead to body temperature differences that impact relative overheating risk and activity patterns. Moreover, for all three species, an idealized morph that matches the White Sands substrate would have considerably less activity time, by approximately 1 month, than existing light morphs. Overall, there are both benefits and costs to greater substrate matching, the balance of which may prevent the evolution of optimal crypsis. Our work highlights the importance of color in dictating thermal performance and the complexity inherent in understanding the evolution of coloration.2021
Why are species traits weak predictors of range shifts?Beissinger S.R. and E.A. Riddell. Annual Reviews of Ecology, Evolution, and Systematics, 52:47-66. LINK
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We examine the evidence linking species’ traits to contemporary range shifts and find they are poor predictors of range shifts that have occurred over decades to a century. We then discuss reasons for the poor performance of traits for describing interspecific variation in range shifts from two perspectives: (a) factors associated with species’ traits that degrade range-shift signals stemming from the measures used for species’ traits, traits that are typically not analyzed, and the influence of phylogeny on range-shift potential and (b) issues in quantifying range shifts and relating them to species’ traits due to imperfect detection of species, differences in the responses of altitudinal and latitudinal ranges, and emphasis on testing linear relationships between traits and range shifts instead of nonlinear responses. Improving trait-based approaches requires a recognition that traits within individuals interact in unexpected ways and that different combinations of traits may be functionally equivalent.Riddell, E.A., K. Iknayan, L. Hargrove, S. Tremor, J.L. Patton, R. Ramirez, B.O. Wolf, & S.R. Beissinger. Science 371: 633-636. LINK
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High exposure to warming from climate change is expected to threaten biodiversity by pushing many species toward extinction. Such exposure is often assessed for all taxa at a location from climate projections, yet species have diverse strategies for buffering against temperature extremes. We compared changes in species occupancy and site-level richness of small mammal and bird communities in protected areas of the Mojave Desert using surveys spanning a century. Small mammal communities remained remarkably stable, whereas birds declined markedly in response to warming and drying. Simulations of heat flux identified different exposure to warming for birds and mammals, which we attribute to microhabitat use. Estimates from climate projections are unlikely to accurately reflect species’ exposure without accounting for the effects of microhabitat buffering on heat flux.2020
Terrestrial salamanders maintain habitat suitability under climate change despite trade-offs between water loss and gas exchangeRiddell, E.A. and M.W. Sears. Physiological and Biochemical Zoology 93: 310-319 LINK
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Physiological acclimation has the potential to improve survival during climate change by reducing sensitivity to warming. However, acclimation can produce trade-offs due to links between related physiological traits. Water loss and gas exchange are intrinsically linked by the need for respiratory surfaces to remain moist. As climates warm and dry, organisms may attempt to lower desiccation risk by limiting water loss but at a cost of inhibiting their ability to breathe. Here we used laboratory experiments to evaluate the trade-off between water loss and gas exchange in a fully terrestrial, lungless salamander (Plethodon metcalfi). We measured acclimation of resistance to water loss and metabolic rates in response to long-term exposure to temperature and humidity treatments. We then integrated the trade-off into a simulation-based species distribution model to determine the consequences of ignoring physiological trade-offs on energy balance and aerobic scope under climate change. In the laboratory, we found a close association between acclimation of resistance to water loss and metabolic rates indicative of a trade-off. After incorporating the trade-off into our simulations, we found that energy balance and aerobic scope were reduced by 49.7% and 34.3%, respectively, under contemporary climates across their geographic range. Under future warming scenarios, incorporating the trade-off lowered the number of sites predicted to experience local extirpation by 52.2% relative to simulations without the trade-off; however, the number of sites capable of supporting the energetic requirements for reproduction declined from 44.6% to 32.6% across the species’ geographic range. These experiments and simulations suggest that salamanders can maintain positive energy balance across their geographic range under climate change despite the costs associated with trade-offs between water loss and gas exchange.2019
Cooling requirements fueled the collapse of a desert bird community from climate changeRiddell, E.A., K. Iknayan, B.O. Wolf, B. Sinervo, and S.R. Beissinger. Proceedings of the National Academy of Sciences U.S.A. LINK
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Climate change threatens global biodiversity by increasing extinction risk, yet few studies have uncovered a physiological basis of climate-driven species declines. Maintaining a stable body temperature is a fundamental requirement for homeothermic animals, and water is a vital resource that facilitates thermoregulation through evaporative cooling, especially in hot environments. Here, we explore the potential for thermoregulatory costs to underlie the community collapse of birds in the Mojave Desert over the past century in response to climate change. The probability of persistence was lowest for species occupying the warmest and driest sites, which imposed the greatest cooling costs. We developed a general model of heat flux to evaluate whether water requirements for evaporative cooling contributed to species’ declines by simulating thermoregulatory costs in the Mojave Desert for 50 bird species representing the range of observed declines. Bird species’ declines were positively associated with climate-driven increases in water requirements for evaporative cooling and exacerbated by large body size, especially for species with animal-based diets. Species exhibiting reductions in body size across their range saved up to 14% in cooling costs and experienced less decline than species without size reductions, suggesting total cooling costs as a mechanism underlying Bergmann’s rule. Reductions in body size, however, are unlikely to offset the 50 to 78% increase in cooling costs threatening desert birds from future climate change. As climate change spreads warm, dry conditions across the planet, water requirements are increasingly likely to drive population declines, providing a physiological basis for climate-driven extinctions.Riddell, E.A., E. Roback, C.E. Wells, K. R. Zamudio, and M.W. Sears. Nature Communications, 10: 4091. LINK
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Organisms rely upon external cues to avoid detrimental conditions during environmental change. Rapid water loss, or desiccation, is a universal threat for terrestrial plants and animals, especially under climate change, but the cues that facilitate plastic responses to avoid desiccation are unclear. We integrate acclimation experiments with gene expression analyses to identify the cues that regulate resistance to water loss at the physiological and regulatory level in a montane salamander (Plethodon metcalfi). Here we show that temperature is an important cue for developing a desiccation-resistant phenotype and might act as a reliable cue for organisms across the globe. Gene expression analyses consistently identify regulation of stem cell differentiation and embryonic development of vasculature. The temperature-sensitive blood vessel development suggests that salamanders regulate water loss through the regression and regeneration of capillary beds in the skin, indicating that tissue regeneration may be used for physiological purposes beyond replacing lost limbs.Sears, M.W., E.A. Riddell, T. Rusch, and M. J. Angilletta, Jr. Integrative and Comparative Biology, icz130. LINK
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Over the past decade, ecologists and physiologists alike have acknowledged the importance of environmental heterogeneity. Meaningful predictions of the responses of organisms to climate will require an explicit understanding of how organismal behavior and physiology are affected by such heterogeneity. Furthermore, the responses of organisms themselves are quite heterogeneous: physiology and behavior vary over different time scales and across different life stages, and because physiological systems do not operate in isolation of one another, they need to be considered in a more integrated fashion. Here, we review case studies from our laboratories to highlight progress that has been made along these fronts and generalizations that might be made to other systems, particularly in the context of predicting responses to climate change.2018
Plasticity reveals hidden resistance to extinction under climate change in the global hotspot of salamander diversityRiddell E.A., J. Odom, J. Damm, and M.W. Sears. Science Advances 4, eaar5471. LINK
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Extinction rates are predicted to rise exponentially under climate warming, but many of these predictions ignore physiological and behavioral plasticity that might buffer species from extinction. We evaluated the potential for physiological acclimatization and behavioral avoidance of poor climatic conditions to lower extinction risk under climate change in the global hotspot of salamander diversity, a region currently predicted to lose most of the salamander habitat due to warming. Our approach integrated experimental physiology and behavior into a mechanistic species distribution model to predict extinction risk based on an individual’s capacity to maintain energy balance with and without plasticity. We assessed the sensitivity of extinction risk to body size, behavioral strategies, limitations on energy intake, and physiological acclimatization of water loss and metabolic rate. The field and laboratory experiments indicated that salamanders readily acclimatize water loss rates and metabolic rates in ways that could maintain positive energy balance. Projections with plasticity reduced extinction risk by 72% under climate warming, especially in the core of their range. Further analyses revealed that juveniles might experience the greatest physiological stress under climate warming, but we identified specific physiological adaptations or plastic responses that could minimize the lethal physiological stress imposed on juveniles. We conclude that incorporating plasticity fundamentally alters ecological predictions under climate change by reducing extinction risk in the hotspot of salamander diversity.Riddell E.A., J. McPhail, J.D. Damm, and M.W. Sears. Functional Ecology 32: 916-925. LINK
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Reversible acclimation increases resilience to environmental stress, but acclimation may have hidden costs due to underlying linkages between related physiological traits. These linkages might result in trade-offs that undermine whole-organism performance if the change in a related trait reduces the net benefits of acclimation or increases susceptibility to alternative environmental stressors. Metabolic rate and water loss rate are two fundamental physiological traits that could interact due to their dependence on gas exchange across shared physical surfaces. Reductions in water loss rate in response to dehydration stress might reduce metabolic rate by constraining the flux of both water and oxygen. We examined acclimation of metabolic rate and water loss rate using a species of woodland salamander (Plethodon metcalfi) in response to temperature and humidity using a full factorial experimental design. We controlled the evaporative demand of the air across temperatures to assess temperature and humidity as independent cues for acclimation. We predicted that reductions in water loss rate would coincide with reductions in metabolic rate in response to temperature due to shared physical and chemical pathways. We also assessed acclimation of heart rates as a potential compensatory mechanism used to promote oxygen delivery. We integrated these responses into a biophysical model developed from first principles to demonstrate the potential for these interactions to influence habitat suitability. We found that reductions in water loss rates during thermal acclimation were associated with simultaneous reductions in metabolic rates, and we did not find a compensatory response in heart rates. We suggest that these linkages underlie whole-organism strategies (e.g. physiological dormancy or arousal) for reducing the energetic costs imposed by warm temperatures. The biophysical model suggested that the interaction between these two traits potentially structures phenotypic variation in our population because certain combinations of trait values were incapable of reaching positive energy balance. Trade-offs between linked physiological traits potentially structure whole-organism strategies for responding to environmental stressors and constrain phenotypic variation. Therefore, predictions of the benefits of acclimation must be interpreted cautiously without knowledge of the underlying trade-offs among linked physiological traits.Carlo, M.C., E.A. Riddell, O. Levy, and M.W. Sears. Ecology Letters, 21:104-116. LINK
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The capacity to tolerate climate change often varies across ontogeny in organisms with complex life cycles. Recently developed species distribution models incorporate traits across life stages; however, these life-cycle models primarily evaluate effects of lethal change. Here, we examine impacts of recurrent sublethal warming on development and survival in ecological projections of climate change. We reared lizard embryos in the laboratory under temperature cycles that simulated contemporary conditions and warming scenarios. We also artificially warmed natural nests to mimic laboratory treatments. In both cases, recurrent sublethal warming decreased embryonic survival and hatchling sizes. Incorporating survivorship results into a mechanistic species distribution model reduced annual survival by up to 24% compared to models that did not incorporate sublethal warming. Contrary to models without sublethal effects, our model suggests that modest increases in developmental temperatures influence species ranges due to effects on survivorship.2017
Physical calculations of resistance to water loss improve species range models: replyRiddell E.A. and M.W. Sears. Ecology 98: 2965-2968. LINK
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Christian et al. (2017) proposed several possible flaws in the methods and logic presented by Riddell et al. (2017) that included potential activity of salamanders during measurements, trimming of the agar model’s legs, misinterpretations of the empirical data, limitations on agar models, and the relationship between body size and skin resistance to water loss (ri). We argue that these criticisms are easily addressable, and here, we reinforce our original claim that the agar method for determination of resistance to water loss is flawed. Before responding to these individual critiques, we begin with a deeper criticism of the agar model method and general methodology for determining resistance to water loss that has resulted in the reification of the boundary layer’s ecological and physiological importance. Christian et al. also promoted misleading information on the established physical processes for estimating the value of the boundary layer resistance (rb) that relate directly to the flaws of the agar model method. We hope that our response enlightens physiological ecologists on the obstacles that impede the progress of water loss studies.Riddell E.A., E.K. Apanovitch, J.P. Odom, and M.W. Sears. Ecological Monographs, 87: 21-33. LINK
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Species ranges are constrained by the physiological tolerances of organisms to climatic conditions. By incorporating physiological constraints, species distribution models can identify how biotic and abiotic factors constrain a species' geographic range. Rates of water loss influence species distributions, but characterizing water loss for an individual requires complex calculations. Skin resistance to water loss (ri) is considered to be the most informative metric of water loss rates because it controls for experimental biases. However, calculating ri requires biophysical equations to solve for the resistance of the air that surrounds an organism, termed the boundary layer resistance (rb). Here, we compared theoretical and empirical methods for measuring skin resistance to water loss of a Plethodon salamander collected from nature. For the empirical methods, we measured rb of agar replicas at five body sizes, two temperatures, three vapor pressure deficits, and six flow rates using a flow-through system. We also calculated rb using biophysical equations under the same experimental conditions. We then determined the ecological implications of incorporating skin and boundary layer resistance into a species range model that estimated potential activity time and energy balance throughout the geographic range of the study species. We found that empirical methods for calculating rb resulted in negative values of ri, whereas biophysical calculations produced meaningful values of ri. The species range model determined that ignoring realistic boundary layer and skin resistances reduced average estimates of energy balance by as much as 64% and potential activity time by 88% throughout the spatial extent of the model. We conclude that the use of agar replicas is an inadequate technique to characterize skin resistance to water loss, and incorporating boundary layer and skin resistances to water loss improves estimates of activity and energetics for mechanistic species distribution models. More importantly, our study suggests that incorporating the physical processes underlying rates of water loss could improve estimates of habitat suitability for many animals.2015
Geographic variation of resistances to water loss within two species of salamanders: implications for activityRiddell E.A. and M.W. Sears. Riddell E.A., and M.W. Sears. Ecosphere 6: Article 86. LINK
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For many organisms, constraints on activity increase energetic costs, which ultimately reduce the suitability of a particular habitat. Mechanistic species distribution models often use estimates of activity to predict how organisms will respond to climate change. These models couple physiology and morphology with climatic data to estimate potential activity. In turn, the duration of activity is used to estimate the energetic balance of individuals at a given location. Whether individuals remain in positive net energetic balance determines if a given location is suitable for the species. However, because these models often assume that physiology does not vary across the species range, estimates of activity (and consequently energetics) are potentially misleading. To test the consequence of this assumption, we measured total resistance to water loss (R) within two species of lungless salamanders (Plethodon metcalfi and P. teyahalee) collected from locations along their elevational extent in southwestern North Carolina. Because hydration state constrains the activity of salamanders, increasing R would increase potential activity. Here, we leveraged the natural changes in environmental conditions along an elevational gradient to determine if salamanders modify R in different environments. We predicted that salamanders collected from low elevations would have higher R to compensate for the warmer, drier conditions at low elevations that may limit activity. We determined R in the laboratory using a flow-through system at two temperatures (12°C, 18°C) and at three vapor pressure deficits (0.2 kPa, 0.35 kPa, 0.5 kPa). For P. metcalfi, individuals collected from low elevations exhibited the highest R, suggesting either acclimatization or adaptation to local conditions. For P. teyahalee, individuals collected from high elevations exhibited the highest R, but these results may reflect alternative pressures due to differences in behavior. The results also suggest that salamanders might use temperature as a cue to increase R, but the capacity to do so depends upon the temperatures experienced in nature. Moreover, we show that variation in R has the potential to alter the duration of activity over the elevational ranges of these species, illustrating the importance of incorporating geographic variation of physiological traits for predicting a species' response to climate.2013
Incidental capture of an alternative prey by a dietary specialist, the endangered Snail KiteRiddell E.A., and D.P. Cavanaugh. Florida Field Naturalist 41:49-50. LINK