Mechanistic forecasts of species responses to climate change: The promise of biophysical ecology.

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.

Thermal Costs and Benefits of Replicated Color Evolution in the White Sands Desert Lizard Community.

AbstractTraits 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.

Repeatability of Voluntary Thermal Maximum and Covariance with Water Loss Reveal Potential for Adaptation to Changing Climates.

AbstractAlthough climate warming poses a grave threat to amphibians, little is known about the capacity of this group to evolve in response to warming. The capacity of key traits to evolve depends on the presence of genetic variation on which selection can act. Here, we use repeatability estimates to estimate the potential upper bounds of heritable genetic variation in voluntary and critical thermal maxima of gray-cheeked salamanders (Plethodon metcalfi). Increases in thermal tolerance may also require concordant increases in resistance to water loss because hotter temperatures incur greater evaporative risk. Therefore, we also tested for a correlation between voluntary thermal maxima and resistance to water loss and conducted an acclimation study to test for covariation between these traits in response to warming. Voluntary thermal maxima exhibited low to moderate levels of repeatability (R=0.32, P=0.045), while critical thermal maxima exhibited no statistically significant repeatability (R=0.10, P=0.57). Voluntary thermal maxima also correlated positively with resistance to water loss (R=0.31, P=0.025) but only when controlling for body mass. Voluntary thermal maxima and resistance to water loss also exhibited different acclimatory responses across control (12°C-18°C) and warm (18°C-24°C) temperature regimes, indicating a potential decoupling of traits in different thermal environments. By addressing the repeatability of thermal tolerance and the potential for covariation with resistance to water loss, we begin to address some of the key requirements of amphibians to evolve in warming climates.

A chromosome-level genome assembly for the eastern fence lizard (Sceloporus undulatus), a reptile model for physiological and evolutionary ecology.

BACKGROUND: High-quality genomic resources facilitate investigations into behavioral ecology, morphological and physiological adaptations, and the evolution of genomic architecture. Lizards in the genus Sceloporus have a long history as important ecological, evolutionary, and physiological models, making them a valuable target for the development of genomic resources. FINDINGS: We present a high-quality chromosome-level reference genome assembly, SceUnd1.0 (using 10X Genomics Chromium, HiC, and Pacific Biosciences data), and tissue/developmental stage transcriptomes for the eastern fence lizard, Sceloporus undulatus. We performed synteny analysis with other snake and lizard assemblies to identify broad patterns of chromosome evolution including the fusion of micro- and macrochromosomes. We also used this new assembly to provide improved reference-based genome assemblies for 34 additional Sceloporus species. Finally, we used RNAseq and whole-genome resequencing data to compare 3 assemblies, each representing an increased level of cost and effort: Supernova Assembly with data from 10X Genomics Chromium, HiRise Assembly that added data from HiC, and PBJelly Assembly that added data from Pacific Biosciences sequencing. We found that the Supernova Assembly contained the full genome and was a suitable reference for RNAseq and single-nucleotide polymorphism calling, but the chromosome-level scaffolds provided by the addition of HiC data allowed synteny and whole-genome association mapping analyses. The subsequent addition of PacBio data doubled the contig N50 but provided negligible gains in scaffold length. CONCLUSIONS: These new genomic resources provide valuable tools for advanced molecular analysis of an organism that has become a model in physiology and evolutionary ecology.

Terrestrial Salamanders Maintain Habitat Suitability under Climate Change despite Trade-Offs between Water Loss and Gas Exchange.

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.

Thermal cues drive plasticity of desiccation resistance in montane salamanders with implications for climate change.

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.

The World Still Is Not Flat: Lessons Learned from Organismal Interactions with Environmental Heterogeneity in Terrestrial Environments.

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.

Fundamental Flaws with the Fundamental Niche.

For more than 70 years, Hutchinson's concept of the fundamental niche has guided ecological research. Hutchinson envisioned the niche as a multidimensional hypervolume relating the fitness of an organism to relevant environmental factors. Here, we challenge the utility of the concept to modern ecologists, based on its inability to account for environmental variation and phenotypic plasticity. We have ample evidence that the frequency, duration, and sequence of abiotic stress influence the survivorship and performance of organisms. Recent work shows that organisms also respond to the spatial configuration of abiotic conditions. Spatiotemporal variation of the environment interacts with the genotype to generate a unique phenotype at each life stage. These dynamics cannot be captured adequately by a multidimensional hypervolume. Therefore, we recommend that ecologists abandon the niche as a tool for predicting the persistence of species and embrace mechanistic models of population growth that incorporate spatiotemporal dynamics.

Sibling sex, but not androgens, shapes phenotypes in perinatal common marmosets (Callithrix jacchus).

When offspring share a womb, interactions among fetuses can impart lasting impressions on phenotypic outcomes. Such intrauterine interactions often are mediated by sex steroids (estrogens and androgens) produced by the developing fetuses. In many mammals, intrauterine interactions between brothers and sisters lead to masculinization of females, which can induce fitness consequences. Many litter-bearing primates, though, seem to escape androgen-mediated litter effects, begging why? Here, we investigated how the sex composition (i.e., same- or mixed-sex) of litters influences perinatal outcomes in the common marmoset monkey (Callithrix jacchus), using a combination of physiological, morphological, and behavioural assays. We hypothesized that androgens from male fetuses would mediate developmental differences across litter types. We found that newborns (24-36 hours old) from same- and mixed-sex litters were indistinguishable by urinary androgen profiles, birth weights, morphometrics, and behaviour. However, monkeys born into same- and mixed-sex litters exhibited subtle morphological and neurobehavioral differences later in the perinatal period, independent of their androgen profiles. Our findings suggest that while androgens from male fetuses likely do not organize their siblings' phenotypes, perinatal stimuli may initiate divergent developmental trajectories among siblings, which, in turn, promotes inter-individual variability within families.

Lizards perceived abiotic and biotic stressors independently when competing for shade in terrestrial mesocosms.

Hormones such as glucocorticoids and androgens enable animals to respond adaptively to environmental stressors. For this reason, circulating glucocorticoids became a popular biomarker for estimating the quality of an environment, and circulating androgens are frequently used to indicate social dominance. Here, we show that access to thermal resources influence the hormones and behavior of male lizards (Sceloporus jarrovi). We exposed isolated and paired males to different thermal landscapes, ranging from one large patch of shade to sixteen smaller patches. Both the presence of a competitor and the patchiness of the thermal environment influenced hormone concentrations and movement patterns. When shade was concentrated in space, paired lizards competed more aggressively and circulated more corticosterone. Even without competitors, lizards circulated more corticosterone in landscapes with fewer patches of shade. Conversely, shifts in circulating testosterone depended only on the relative body size of a lizard; when paired, large males and small males circulated more and less testosterone, respectively. Furthermore, isolated males moved the farthest and covered the most area when shade was concentrated in a single patch, but paired males did the opposite. Because the total area of shade in each landscape was the same, these hormonal and behavioral responses of lizards reflect the ability to access shade. Thus, circulating glucocorticoids should reflect the thermal quality of an environment when researchers have controlled for other factors. Moreover, a theory of stress during thermoregulation would help ecologists anticipate physiological and behavioral responses to changing climates.

Plasticity reveals hidden resistance to extinction under climate change in the global hotspot of salamander diversity.

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.

Recurrent sublethal warming reduces embryonic survival, inhibits juvenile growth, and alters species distribution projections under climate change.

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.

Configuration of the thermal landscape determines thermoregulatory performance of ectotherms.

Although most organisms thermoregulate behaviorally, biologists still cannot easily predict whether mobile animals will thermoregulate in natural environments. Current models fail because they ignore how the spatial distribution of thermal resources constrains thermoregulatory performance over space and time. To overcome this limitation, we modeled the spatially explicit movements of animals constrained by access to thermal resources. Our models predict that ectotherms thermoregulate more accurately when thermal resources are dispersed throughout space than when these resources are clumped. This prediction was supported by thermoregulatory behaviors of lizards in outdoor arenas with known distributions of environmental temperatures. Further, simulations showed how the spatial structure of the landscape qualitatively affects responses of animals to climate. Biologists will need spatially explicit models to predict impacts of climate change on local scales.

Fine-Scale Microclimatic Variation Can Shape the Responses of Organisms to Global Change in Both Natural and Urban Environments.

When predicting the response of organisms to global change, models use measures of climate at a coarse resolution from general circulation models or from downscaled regional models. Organisms, however, do not experience climate at such large scales. The climate heterogeneity over a landscape and how much of that landscape an organism can sample will determine ultimately the microclimates experienced by organisms. This past few decades has seen an important increase in the number of studies reporting microclimatic patterns at small scales. This synthesis intends to unify studies reporting microclimatic heterogeneity (mostly temperature) at various spatial scales, to infer any emerging trends, and to discuss the causes and consequences of such heterogeneity for organismal performance and with respect to changing land use patterns and climate. First, we identify the environmental drivers of heterogeneity across the various spatial scales that are pertinent to ectotherms. The thermal heterogeneity at the local and micro-scales is mostly generated by the architecture or the geometrical features of the microhabitat. Then, the thermal heterogeneity experienced by individuals is modulated by behavior. Second, we survey the literature to quantify thermal heterogeneity from the micro-scale up to the scale of a landscape in natural habitats. Despite difficulties in compiling studies that differ much in their design and aims, we found that there is as much thermal heterogeneity across micro-, local and landscape scales, and that the temperature range is large in general (>9 °C on average, and up to 26 °C). Third, we examine the extent to which urban habitats can be used to infer the microclimatic patterns of the future. Urban areas generate globally drier and warmer microclimatic patterns and recent evidence suggest that thermal traits of ectotherms are adapted to them. Fourth, we explore the interplay between microclimate heterogeneity and the behavioral thermoregulatory abilities of ectotherms in setting their overall performance. We used a random walk framework to show that the thermal heterogeneity allows a more precise behavioral thermoregulation and a narrower temperature distribution of the ectotherm compared to less heterogeneous microhabitats. Finally, we discuss the potential impacts of global change on the fine scale mosaics of microclimates. The amplitude of change may differ between spatial scales. In heterogeneous microhabitats, the amplitude of change at micro-scale, caused by atmospheric warming, can be substantial while it can be limited at the local and landscape scales. We suggest that the warming signal will influence species performance and biotic interactions by modulating the mosaic of microclimates.

Costs and benefits of thermoregulation revisited: both the heterogeneity and spatial structure of temperature drive energetic costs.

In recent years, ecologists have stepped up to address the challenges imposed by rapidly changing climates. Some researchers have developed niche-based methods to predict how species will shift their ranges. Such methods have evolved rapidly, resulting in models that incorporate physiological and behavioral mechanisms. Despite their sophistication, these models fail to account for environmental heterogeneity at the scale of an organism. We used an individual-based model to quantify the effects of operative environmental temperatures, as well as their heterogeneity and spatial structure, on the thermoregulation, movement, and energetics of ectotherms. Our simulations showed that the heterogeneity and spatial structure of a thermal landscape are as important as its mean temperature. In fact, temperature and heterogeneity interact to determine organismal performance. Consequently, the popular index of environmental quality (d(e)), which ignores variance and spatial structure, is inherently flawed as a descriptor of the thermal quality of an environment. Future efforts to model species' distributions should link thermoregulation and activity to environmental heterogeneity at fine scales.

Widespread rapid reductions in body size of adult salamanders in response to climate change.

Reduction in body size is a major response to climate change, yet evidence in globally imperiled amphibians is lacking. Shifts in average population body size could indicate either plasticity in the growth response to changing climates through changes in allocation and energetics, or through selection for decreased size where energy is limiting. We compared historic and contemporary size measurements in 15 Plethodon species from 102 populations (9450 individuals) and found that six species exhibited significant reductions in body size over 55 years. Biophysical models, accounting for actual changes in moisture and air temperature over that period, showed a 7.1-7.9% increase in metabolic expenditure at three latitudes but showed no change in annual duration of activity. Reduced size was greatest at southern latitudes in regions experiencing the greatest drying and warming. Our results are consistent with a plastic response of body size to climate change through reductions in body size as mediated through increased metabolism. These rapid reductions in body size over the past few decades have significance for the susceptibility of amphibians to environmental change, and relevance for whether adaptation can keep pace with climate change in the future.

Predicting the physiological performance of ectotherms in fluctuating thermal environments.

Physiological ecologists have long sought to understand the plasticity of organisms in environments that vary widely among years, seasons and even hours. This is now even more important because human-induced climate change is predicted to affect both the mean and variability of the thermal environment. Although environmental change occurs ubiquitously, relatively few researchers have studied the effects of fluctuating environments on the performance of developing organisms. Even fewer have tried to validate a framework for predicting performance in fluctuating environments. Here, we determined whether reaction norms based on performance at constant temperatures (18, 22, 26, 30 and 34°C) could be used to predict embryonic and larval performance of anurans at fluctuating temperatures (18-28°C and 18-34°C). Based on existing theory, we generated hypotheses about the effects of stress and acclimation on the predictability of performance in variable environments. Our empirical models poorly predicted the performance of striped marsh frogs (Limnodynastes peronii) at fluctuating temperatures, suggesting that extrapolation from studies conducted under artificial thermal conditions would lead to erroneous conclusions. During the majority of ontogenetic stages, growth and development in variable environments proceeded more rapidly than expected, suggesting that acute exposures to extreme temperatures enable greater performance than do chronic exposures. Consistent with theory, we predicted performance more accurately for the less variable thermal environment. Our results underscore the need to measure physiological performance under naturalistic thermal conditions when testing hypotheses about thermal plasticity or when parameterizing models of life-history evolution.

The world is not flat: defining relevant thermal landscapes in the context of climate change.

Although climates are rapidly changing on a global scale, these changes cannot easily be extrapolated to the local scales experienced by organisms. In fact, such generalizations might be quite problematic. For instance, models used to predict shifts in the ranges of species during climate change rarely incorporate data resolved to <1 km(2), although most organisms integrate climatic drivers at much smaller scales. Empirical studies alone suggest that the operative temperatures of many organisms vary by as much as 10-20 °C on a local scale, depending on vegetation, geology, and topography. Furthermore, this variation in abiotic factors ignores thermoregulatory behaviors that many animals use to balance heat loads. Through a set of simulations, we demonstrate how variability in elevational topography can attenuate the effects of warming climates. These simulations suggest that changing climates do not always impact organisms negatively. Importantly, these simulations involve well-known relationships in biophysical ecology that show how no two organisms experience the same climate in the same way. We suggest that, when coupled with thermoregulatory behavior, variation in topographic features can mask the acute effect of climate change in many cases.

Introduction to the symposium: responses of organisms to climate change: a synthetic approach to the role of thermal adaptation.

On a global scale, changing climates are affecting ecological systems across multiple levels of biological organization. Moreover, climates are changing at rates unprecedented in recent geological history. Thus, one of the most pressing concerns of the modern era is to understand the biological responses to climate such that society can both adapt and implement measures that attempt to offset the negative impacts of a rapidly changing climate. One crucial question, to understand organismal responses to climate, is whether the ability of organisms to adapt can keep pace with quickly changing environments. To address this question, a syntheses of knowledge from a broad set of biological disciplines will be needed that integrates information from the fields of ecology, behavior, physiology, genetics, and evolution. This symposium assembled a diverse group of scientists from these subdisciplines to present their perspectives regarding the ability of organisms to adapt to changing climates. Specifically, the goals of this symposia were to (1) highlight what each discipline brings to a discussion of organismal responses to climate, (2) to initiate and foster a discussion to break barriers in the transfer of knowledge across disciplines, and (3) to synthesize an approach to address ongoing issues concerning biological responses to climate.