Three questions about the eco-physiology of overwintering underground.

In cold environments ectotherms can be dormant underground for long periods. In 1941 Cowles proposed an ecological trade-off involving the depth at which ectotherms overwintered: on warm days, only shallow reptiles could detect warming soils and become active; but on cold days, they risked freezing. Cowles discovered that most reptiles at a desert site overwintered at shallow depths. To extend his study, we compiled hourly soil temperatures (5 depths, 90 sites, continental USA) and physiological data, and simulated consequences of overwintering at fixed depths. In warm localities shallow ectotherms have lowest energy costs and largest reserves in spring, but in cold localities, they risk freezing. Ectotherms shifting hourly to the coldest depth potentially reduce energy expenses, but paradoxically sometimes have higher expenses than those at fixed depths. Biophysical simulations for a desert site predict that shallow ectotherms have increased opportunities for mid-winter activity but need to move deep to digest captured food. Our simulations generate testable predictions to eco-physiological questions but rely on physiological responses to acute cold rather than to natural cooling profiles. Furthermore, natural-history data to test most predictions do not exist. Thus, our simulation approach uncovers knowledge gaps and suggests research agendas for studying ectotherms overwintering underground.

Seasonality in Kgalagadi Lizards: Inferences from Legacy Data.

AbstractAn ecological issue can best be studied by gathering original data that are specifically targeted for that issue. But ascertaining-a priori-whether a novel issue will be worth exploring can be problematic without background data. However, an issue's potential merit can sometimes be evaluated by repurposing legacy or other data that had been gathered for unrelated purposes but that are nonetheless relevant. Our present project was initially motivated by an ecological trade-off-proposed eight decades ago-involving the depth at which desert reptiles overwintered. To address those and related issues, we repurposed our five-decades-old natural history data for 18 species of Kgalagadi lizards and then explored the seasonal ecology of these lizards, emphasizing winter. Our data were not gathered for a study of seasonal ecology but nonetheless inform diverse seasonal patterns for a major community of lizards. However, repurposed data (whether recent or legacy) present challenges and ambiguities, and we suggest targeted, next-step studies of seasonal ecology that can circumvent limitations and ambiguities.

Distribution modelling of an introduced species: do adaptive genetic markers affect potential range?

Biological invasions have increased in the last few decades mostly due to anthropogenic causes such as globalization of trade. Because invaders sometimes cause large economic losses and ecological disturbances, estimating their origin and potential geographical ranges is useful. Drosophila subobscura is native to the Old World but was introduced in the New World in the late 1970s and spread widely. We incorporate information on adaptive genetic markers into ecological niche modelling and then estimate the most probable geographical source of colonizers; evaluate whether the genetic bottleneck experienced by founders affects their potential distribution; and finally test whether this species has spread to all its potential suitable habitats worldwide. We find the environmental space occupied by this species in its native and introduced distributions are notably the same, although the introduced niche has shifted slightly towards higher temperature and lower precipitation. The genetic bottleneck of founding individuals was a key factor limiting the spread of this introduced species. We also find that regions in the Mediterranean and north-central Portugal show the highest probability of being the origin of the colonizers. Using genetically informed environmental niche modelling can enhance our understanding of the initial colonization and spread of invasive species, and also elucidate potential areas of future expansions worldwide.

Revisiting a Key Innovation in Evolutionary Biology: Felsenstein's "Phylogenies and the Comparative Method".

The comparative method has long been a fundamental exploratory tool in evolutionary biology, but this venerable approach was revolutionized in 1985, when Felsenstein published "Phylogenies and the Comparative Method" in The American Naturalist. This article forced comparative biologists to start thinking phylogenetically when conducting statistical analyses of correlated trait evolution rather than simply applying conventional statistical methods that ignore evolutionary relationships. It did so by introducing a novel analytical method (phylogenetically "independent contrasts") that required a phylogenetic topology with branch lengths and that assumed a Brownian motion model of trait evolution. Independent contrasts enabled comparative biologists to avoid the statistical dilemma of nonindependence of species values, arising from shared ancestry, but came at the cost of needing a detailed phylogeny and of accepting a specific model of character change. Nevertheless, this article not only revitalized comparative biology but even encouraged studies aimed at estimating phylogenies. Felsenstein's characteristically lucid and concise statement of the problem (illustrated with powerful graphics), coupled with an oncoming flood of new molecular data and techniques for estimating phylogenies, led Felsenstein's 1985 article to become the second most cited article in the history of this journal. Here we present a personal review of comparative biology before, during, and after Joe's article. For historical context, we append a perspective written by Joe himself that describes how his article evolved, unedited transcripts of reviews of his submitted manuscript, and a guide to some nontrivial calculations. These additional materials help emphasize that the process of science does not always occur gradually or predictably.

Climate Warming, Resource Availability, and the Metabolic Meltdown of Ectotherms.

Climate warming may lower environmental resource levels, growth, and fitness of many ectotherms. In a classic experiment, Brett and colleagues documented that growth rates of salmon depended strikingly on both temperature and food levels. Here we develop a simple bioenergetic model that explores how fixed temperatures and food jointly alter the thermal sensitivity of net energy gain. The model incorporates differing thermal sensitivities of energy intake and metabolism. In qualitative agreement with Brett's results, it predicts that decreased food intake reduces growth rates, lowers optimal temperatures for growth, and lowers the highest temperatures sustaining growth (upper thermal limit). Consequently, ectotherms facing reduced food intake in warm environments should restrict activity to times when low body temperatures are biophysically feasible, but-in a warming world-that will force ectotherms to shorten activity times and thus further reduce food intake. This "metabolic meltdown" is a consequence of declining energy intake coupled with accelerating metabolic costs at high temperatures and with warming-imposed restrictions on activity. Next, we extend the model to explore how increasing mean environmental temperatures alter the thermal sensitivity of growth: when food intake is reduced, optimal temperatures and upper thermal limits for growth are lowered. We discuss our model's key assumptions and caveats as well as its relationship to a recent model for phytoplankton. Both models illustrate that the deleterious impacts of climate warming on ectotherms will be amplified if food intake is also reduced, either because warming reduces standing food resources or because it restricts foraging time.

Fifty Years of Mountain Passes: A Perspective on Dan Janzen's Classic Article.

In 1967, Dan Janzen published "Why Mountain Passes Are Higher in the Tropics" in The American Naturalist. Janzen's seminal article has captured the attention of generations of biologists and continues to inspire theoretical and empirical work. The underlying assumptions and derived predictions are broadly synthetic and widely applicable. Consequently, Janzen's "seasonality hypothesis" has proven relevant to physiology, climate change, ecology, and evolution. To celebrate the fiftieth anniversary of this highly influential article, we highlight the past, present, and future of this work and include a unique historical perspective from Janzen himself.

Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation.

Physiological thermal-tolerance limits of terrestrial ectotherms often exceed local air temperatures, implying a high degree of thermal safety (an excess of warm or cold thermal tolerance). However, air temperatures can be very different from the equilibrium body temperature of an individual ectotherm. Here, we compile thermal-tolerance limits of ectotherms across a wide range of latitudes and elevations and compare these thermal limits both to air and to operative body temperatures (theoretically equilibrated body temperatures) of small ectothermic animals during the warmest and coldest times of the year. We show that extreme operative body temperatures in exposed habitats match or exceed the physiological thermal limits of most ectotherms. Therefore, contrary to previous findings using air temperatures, most ectotherms do not have a physiological thermal-safety margin. They must therefore rely on behavior to avoid overheating during the warmest times, especially in the lowland tropics. Likewise, species living at temperate latitudes and in alpine habitats must retreat to avoid lethal cold exposure. Behavioral plasticity of habitat use and the energetic consequences of thermal retreats are therefore critical aspects of species' vulnerability to climate warming and extreme events.

Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures?

Thermal performance curves (TPCs), which quantify how an ectotherm's body temperature (Tb ) affects its performance or fitness, are often used in an attempt to predict organismal responses to climate change. Here, we examine the key - but often biologically unreasonable - assumptions underlying this approach; for example, that physiology and thermal regimes are invariant over ontogeny, space and time, and also that TPCs are independent of previously experienced Tb. We show how a critical consideration of these assumptions can lead to biologically useful hypotheses and experimental designs. For example, rather than assuming that TPCs are fixed during ontogeny, one can measure TPCs for each major life stage and incorporate these into stage-specific ecological models to reveal the life stage most likely to be vulnerable to climate change. Our overall goal is to explicitly examine the assumptions underlying the integration of TPCs with Tb , to develop a framework within which empiricists can place their work within these limitations, and to facilitate the application of thermal physiology to understanding the biological implications of climate change.

Temperature extremes: geographic patterns, recent changes, and implications for organismal vulnerabilities.

Extreme temperatures can injure or kill organisms and can drive evolutionary patterns. Many indices of extremes have been proposed, but few attempts have been made to establish geographic patterns of extremes and to evaluate whether they align with geographic patterns in biological vulnerability and diversity. To examine these issues, we adopt the CLIMDEX indices of thermal extremes. We compute scores for each index on a geographic grid during a baseline period (1961-1990) and separately for the recent period (1991-2010). Heat extremes (temperatures above the 90th percentile during the baseline period) have become substantially more common during the recent period, particularly in the tropics. Importantly, the various indices show weak geographic concordance, implying that organisms in different regions will face different forms of thermal stress. The magnitude of recent shifts in indices is largely uncorrelated with baseline scores in those indices, suggesting that organisms are likely to face novel thermal stresses. Organismal tolerances correlate roughly with absolute metrics (mainly for cold), but poorly with metrics defined relative to local conditions. Regions with high extreme scores do not correlate closely with regions with high species diversity, human population density, or agricultural production. Even though frequency and intensity of extreme temperature events have - and are likely to have - major impacts on organisms, the impacts are likely to be geographically and taxonomically idiosyncratic and difficult to predict.

Global metabolic impacts of recent climate warming.

Documented shifts in geographical ranges, seasonal phenology, community interactions, genetics and extinctions have been attributed to recent global warming. Many such biotic shifts have been detected at mid- to high latitudes in the Northern Hemisphere-a latitudinal pattern that is expected because warming is fastest in these regions. In contrast, shifts in tropical regions are expected to be less marked because warming is less pronounced there. However, biotic impacts of warming are mediated through physiology, and metabolic rate, which is a fundamental measure of physiological activity and ecological impact, increases exponentially rather than linearly with temperature in ectotherms. Therefore, tropical ectotherms (with warm baseline temperatures) should experience larger absolute shifts in metabolic rate than the magnitude of tropical temperature change itself would suggest, but the impact of climate warming on metabolic rate has never been quantified on a global scale. Here we show that estimated changes in terrestrial metabolic rates in the tropics are large, are equivalent in magnitude to those in the north temperate-zone regions, and are in fact far greater than those in the Arctic, even though tropical temperature change has been relatively small. Because of temperature's nonlinear effects on metabolism, tropical organisms, which constitute much of Earth's biodiversity, should be profoundly affected by recent and projected climate warming.

A Few Meters Matter: Local Habitats Drive Reproductive Cycles in a Tropical Lizard.

Reproductive phenology often varies geographically within species, driven by environmental gradients that alter growth and reproduction. However, environments can differ between adjacent habitats at single localities. In lowland Puerto Rico, both open (sunny, warm) and forested (shady, cool) habitats may be only meters apart. The lizard Anolis cristatellus lives in both habitats: it thermoregulates carefully in the open but is a thermoconformer in the forest. To determine whether reproduction differs between habitats, we compared reproductive cycles of females in open versus forest habitats at two localities for over 2 years. Open females were more likely than forest females to be reproductive throughout the year, probably because open females were able to bask and thereby achieve warmer body temperatures. These between-habitat differences in reproduction were especially marked in cool months and are equivalent in magnitude to those between populations separated by elevation. Thus, environmental differences (even on a microlandscape scale) matter to reproduction and probably to demography.

Signatures of geography, climate and foliage on given names of baby girls.

Parents often weigh social, familial and cultural considerations when choosing their baby's name, but the name they choose could potentially be influenced by their physical or biotic environments. Here we examine whether the popularity of month and season names of girls covary geographically with environmental variables. In the continental USA, April, May and June (Autumn, Summer) are the most common month (season) names: April predominates in southern states (early springs), whereas June predominates in northern states (later springs). Whether April's popularity has increased with recent climate warming is ambiguous. Autumn is most popular in northern states, where autumn foliage is notably colourful, and in eastern states having high coverage of deciduous foliage. On a continental scale, Autumn was most popular in English-speaking countries with intense colouration of autumn foliage. These analyses are descriptive but indicate that climate and vegetation sometimes influence parental choice of their baby's name.

Designing a Seasonal Acclimation Study Presents Challenges and Opportunities.

Organisms living in seasonal environments often adjust physiological capacities and sensitivities in response to (or in anticipation of) environment shifts. Such physiological and morphological adjustments ("acclimation" and related terms) inspire opportunities to explore the mechanistic bases underlying these adjustments, to detect cues inducing adjustments, and to elucidate their ecological and evolutionary consequences. Seasonal adjustments ("seasonal acclimation") can be detected either by measuring physiological capacities and sensitivities of organisms retrieved directly from nature (or outdoor enclosures) in different seasons or less directly by rearing and measuring organisms maintained in the laboratory under conditions that attempt to mimic or track natural ones. But mimicking natural conditions in the laboratory is challenging-doing so requires prior natural-history knowledge of ecologically relevant body temperature cycles, photoperiods, food rations, social environments, among other variables. We argue that traditional laboratory-based conditions usually fail to approximate natural seasonal conditions (temperature, photoperiod, food, "lockdown"). Consequently, whether the resulting acclimation shifts correctly approximate those in nature is uncertain, and sometimes is dubious. We argue that background natural history information provides opportunities to design acclimation protocols that are not only more ecologically relevant, but also serve as templates for testing the validity of traditional protocols. Finally, we suggest several best practices to help enhance ecological realism.

Les organismes vivant dans des environnements saisonniers ajustent souvent leurs capacités et leurs sensibilités physiologiques en réponse (ou en prévision de) aux changements environnementaux. De tels ajustements physiologiques et morphologiques (« acclimatation ¼ et termes apparentés) offrent l"opportunité d'explorer les mécanismes sous-jacents à ces ajustements, de détecter les indices qui les induisent et d'élucider leurs conséquences écologiques et évolutives. Les ajustements saisonniers ("acclimatation saisonnière") peuvent être détectés soit en mesurant les capacités physiologiques et les sensibilités d'organismes prélevés directement dans la nature (ou dans des enclos extérieurs) à différentes saisons, soit de manière moins directe en élevant et en mesurant des organismes maintenus en laboratoire dans des conditions qui tentent d"imiter ou de suivre les conditions naturelles. Mais il est difficile de reproduire les conditions naturelles en laboratoire car il faut pour cela connaître les cycles de température corporelle, la photopériode, le régime alimentaire, les environnements sociaux, entre autres variables pertinentes d'un point de vue écologique. Nous argumentons que les conditions traditionnellement utilisées en laboratoire ne parviennent généralement pas à se rapprocher des conditions saisonnières naturelles (température, photopériode, nourriture, « confinement ¼). Par conséquent, il n"est pas certain, et parfois douteux, que les écarts d"acclimatation qui en résultent se rapprochent correctement de ceux de la nature. Nous soutenons que les informations de base sur l"histoire naturelle offrent la possibilité de concevoir des protocoles d"acclimatation qui sont non seulement plus pertinents sur le plan écologique, mais servent également de modèles pour tester la validité des protocoles traditionnels. Enfin, nous suggérons plusieurs bonnes pratiques pour aider à améliorer le réalisme écologique.

Los organismos que viven en ambientes estacionales pueden ajustar sus capacidades y sensibilidades fisiológicas en respuesta (o en anticipación) a cambios ambientales. Estos ajustes fisiológicos y morfológicos ("aclimatación" y términos afines) dan la oportunidad para explorar el mecanismo que subyace a estos ajustes, también para detectar las señales que inducen tales ajustes y finalmente para dilucidar sus consecuencias ecológicas y evolutivas. Los ajustes estacionales ("aclimatación estacional") se pueden detectar midiendo las capacidades y sensibilidades fisiológicas de los organismos, ya sea en especímenes extraídos directamente de la naturaleza (o recintos al aire libre) en diferentes estaciones, como también, de una manera menos directa, en especímenes criados y mantenidos en el laboratorio bajo condiciones que simulan las condiciones naturales y sus cambios estacionales. Sin embargo, esta simulación en el laboratorio es un desafío; hacerlo requiere un conocimiento previo de la historia natural de los ciclos de temperatura corporal, los fotoperíodos, las raciones de alimentos, los entornos sociales, entre otras variables ecológicamente relevantes. Argumentamos que las condiciones tradicionales de laboratorio generalmente no se aproximan a las condiciones estacionales naturales (temperatura, fotoperíodo, comida, "bloqueo"). En consecuencia, es incierto y, a veces, dudoso si los cambios de aclimatación resultantes se aproximan correctamente a los de la naturaleza. Así también, la información de antecedentes de la historia natural brinda oportunidades para diseñar protocolos de aclimatación que no solo son más relevantes desde el punto de vista ecológico, sino que también sirven como plantillas para probar la validez de los protocolos tradicionales. Finalmente, sugerimos varias mejoras prácticas que pueden ayudar a lograr un realismo ecológico optimizado en las simulaciones de laboratorio.

Does thermoregulatory behavior maximize reproductive fitness of natural isolates of Caenorhabditis elegans?

BACKGROUND: A central premise of physiological ecology is that an animal's preferred body temperature should correspond closely with the temperature maximizing performance and Darwinian fitness. Testing this co-adaptational hypothesis has been problematic for several reasons. First, reproductive fitness is the appropriate measure, but is difficult to measure in most animals. Second, no single fitness measure applies to all demographic situations, complicating interpretations. Here we test the co-adaptation hypothesis by studying an organism (Caenorhabditis elegans) in which both fitness and thermal preference can be reliably measured. RESULTS: We find that natural isolates of C. elegans display a range of mean thermal preferences and also vary in their thermal sensitivities for fitness. Hot-seeking isolates CB4854 and CB4857 prefer temperatures that favor population growth rate (r), whereas the cold-seeking isolate CB4856 prefers temperatures that favor Lifetime Reproductive Success (LRS). CONCLUSIONS: Correlations between fitness and thermal preference in natural isolates of C. elegans are driven primarily by isolate-specific differences in thermal preference. If these differences are the result of natural selection, then this suggests that the appropriate measure of fitness for use in evolutionary ecology studies might differ even within species, depending on the unique ecological and evolutionary history of each population.

Impacts of climate warming on terrestrial ectotherms across latitude.

The impact of anthropogenic climate change on terrestrial organisms is often predicted to increase with latitude, in parallel with the rate of warming. Yet the biological impact of rising temperatures also depends on the physiological sensitivity of organisms to temperature change. We integrate empirical fitness curves describing the thermal tolerance of terrestrial insects from around the world with the projected geographic distribution of climate change for the next century to estimate the direct impact of warming on insect fitness across latitude. The results show that warming in the tropics, although relatively small in magnitude, is likely to have the most deleterious consequences because tropical insects are relatively sensitive to temperature change and are currently living very close to their optimal temperature. In contrast, species at higher latitudes have broader thermal tolerance and are living in climates that are currently cooler than their physiological optima, so that warming may even enhance their fitness. Available thermal tolerance data for several vertebrate taxa exhibit similar patterns, suggesting that these results are general for terrestrial ectotherms. Our analyses imply that, in the absence of ameliorating factors such as migration and adaptation, the greatest extinction risks from global warming may be in the tropics, where biological diversity is also greatest.

Mountaineers on Mount Everest: Effects of age, sex, experience, and crowding on rates of success and death.

Mount Everest is an extreme environment for humans. Nevertheless, hundreds of mountaineers attempt to summit Everest each year. In a previous study we analyzed interview data for all climbers (2,211) making their first attempt on Everest during 1990-2005. Probabilities of summiting were similar for men and women, declined progressively for climbers about 40 and older, but were elevated for climbers with experience climbing in Nepal. Probabilities of dying were also similar for men and women, increased for climbers about 60 and older (especially for the few that had summited), and were independent of experience. Since 2005, many more climbers (3,620) have attempted Everest. Here our primary goal is to quantify recent patterns of success and death and to evaluate changes over time. Also, we investigate whether patterns relate to key socio-demographic covariates (age, sex, host country, prior experience). Recent climbers were more diverse both in gender (women = 14.6% vs. 9.1% for 1990-2005) and in age (climbers ≥ 40 = 54.1% vs. 38.7%). Strikingly, recent climbers of both sexes were almost twice as likely to summit-and slightly less likely to die-than were comparable climbers in the previous survey. Temporal shifts may reflect improved weather forecasting, installation of fixed ropes on much of the route, and accumulative logistic equipment and experience. We add two new analyses. The probability of dying from illness or non-traumas (e.g., high-altitude illness, hypothermia), relative to dying from falling or from 'objective hazards' (avalanche, rock or ice fall), increased marginally with age. Recent crowding during summit bids was four-fold greater than in the prior sample, but surprisingly crowding has no evident effect on success or death during summit bids. Our results inform prospective climbers as to their current odds of success and of death, as well as inform governments of Nepal and China of the safety consequences and economic impacts of periodically debated restrictions based on climber age and experience.

Why tropical forest lizards are vulnerable to climate warming.

Biological impacts of climate warming are predicted to increase with latitude, paralleling increases in warming. However, the magnitude of impacts depends not only on the degree of warming but also on the number of species at risk, their physiological sensitivity to warming and their options for behavioural and physiological compensation. Lizards are useful for evaluating risks of warming because their thermal biology is well studied. We conducted macrophysiological analyses of diurnal lizards from diverse latitudes plus focal species analyses of Puerto Rican Anolis and Sphaerodactyus. Although tropical lowland lizards live in environments that are warm all year, macrophysiological analyses indicate that some tropical lineages (thermoconformers that live in forests) are active at low body temperature and are intolerant of warm temperatures. Focal species analyses show that some tropical forest lizards were already experiencing stressful body temperatures in summer when studied several decades ago. Simulations suggest that warming will not only further depress their physiological performance in summer, but will also enable warm-adapted, open-habitat competitors and predators to invade forests. Forest lizards are key components of tropical ecosystems, but appear vulnerable to the cascading physiological and ecological effects of climate warming, even though rates of tropical warming may be relatively low.

Partial thermoregulatory compensation by a rapidly evolving invasive species along a latitudinal cline.

In fewer than two decades after invading the Americas, the European fly Drosophila subobscura evolved latitudinal clines in several traits. Moreover, its chromosomal inversion frequencies at given localities have shifted with climate warming. Temperature may have driven the evolution of both geographic clines and within-site shifts. Nevertheless, whether body temperature (Tb) of active flies actually varies geographically and temporally is unknown: if these flies are effective behavioral thermoregulators, they might maintain relatively constant Tb when active, independent of season and latitude. To evaluate these possibilities, we monitored activity and estimated Tb of active flies in all seasons and at five sites (37-49 degrees N) in western North America. Latitudinal and seasonal shifts in activity are conspicuous. Flies have longer activity seasons (and are much more active) at higher latitudes. Flies are generally active only at midday in cool seasons, and only early and late in the day (if active at all) in warm seasons. Despite these behavioral shifts active flies have much lower Tb in cooler seasons and at higher latitudes. The observed pattern is consistent with the hypothesis that geographic shifts in Tb may be an evolutionary driver of latitudinal clines in this invading species.

Evolution of Chilean colonizing populations of Drosophila subobscura: lethal genes and chromosomal arrangements.

Knowledge of the frequency, distribution, and fate of lethal genes in chromosomal inversions helps to illuminate the evolution of recently founded populations. We analyze the relationship between lethal genes and inversions in two colonizing populations of D. subobscura in Chile. In the ancestral Palearctic populations of this species, lethal genes seem distributed at random on chromosomes. But in colonizing American populations, some lethal genes are associated with specific chromosomal arrangements. Some of these associated lethals were detected only during the first stages of the colonization (O( 3+4+2 )), and never thereafter, whereas others have persisted (O( 3+4+7 ) and O(5)). However, most lethal genes in American populations have been observed only once: they have arisen by novel mutation and soon disappear. Finally, recombination between different inversions has been observed in America. However, the persistence of lethal genes associated with the heterotic inversions O( 3+4+7 ) and O(5) could indicate that recombination inside these inversions is rare.