Michael E. Dillon

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.

Into thin air: Physiology and evolution of alpine insects

Numerous physical parameters that influence insect physiology vary substantially with altitude, including temperature, air density, and oxygen partial pressure. Here, we review existing literature and present new empirical data to better characterize the high-altitude environment, and then consider how this environment affects the physiology and evolution of insects. Using weather balloon data from fifty-three sites across the globe, we estimate a mean altitudinal temperature lapse rate of 6.0 °C/km. We also present empirically determined lapse rates for P(o(2)) and air density. The temperature decline with elevation may substantially compromise insect thermoregulation at high altitude. However, heat-transfer models predict that lower air density at elevation reduces convective heat loss of insects by to a surprisingly large degree. This effect combined with behavioral thermoregulation and the availability of buffered microhabitats make the net thermal consequences of high-altitude residence strongly context-specific. The decline in P(o(2)) with elevation may compromise insect development and physiology, but its effects are difficult to predict without simultaneously considering temperature and air density. Flying insects compensate for low air densities with both short-term responses, such as increased stroke amplitude (but not wingbeat frequency), and with long-term developmental and/or evolutionary increases in wing size relative to body size. Finally, in contrast to predictions based on Bergmanns Rule, a literature survey of thirty-six insect species suggests that those living in colder, higher altitudes do not tend to have larger body sizes.

The roles of microclimatic diversity and of behavior in mediating the responses of ectotherms to climate change

We analyze the effects of changing patterns of thermal availability, in space and time, on the performance of small ectotherms. We approach this problem by breaking it into a series of smaller steps, focusing on: (1) how macroclimates interact with living and nonliving objects in the environment to produce a mosaic of thermal microclimates and (2) how mobile ectotherms filter those microclimates into realized body temperatures by moving around in them. Although the first step (generation of mosaics) is conceptually straightforward, there still exists no general framework for predicting spatial and temporal patterns of microclimatic variation. We organize potential variation along three axes-the nature of the objects producing the microclimates (abiotic versus biotic), how microclimates translate macroclimatic variation (amplify versus buffer), and the temporal and spatial scales over which microclimatic conditions vary (long versus short). From this organization, we propose several general rules about patterns of microclimatic diversity. To examine the second step (behavioral sampling of locally available microclimates), we construct a set of models that simulate ectotherms moving on a thermal landscape according to simple sets of diffusion-based rules. The models explore the effects of both changes in body size (which affect the time scale over which organisms integrate operative body temperatures) and increases in the mean and variance of temperature on the thermal landscape. Collectively, the models indicate that both simple behavioral rules and interactions between body size and spatial patterns of thermal variation can profoundly affect the distribution of realized body temperatures experienced by ectotherms. These analyses emphasize the rich set of problems still to solve before arriving at a general, predictive theory of the biological consequences of climate change.

Allometry of Maximum Vertical Force Production During Hovering Flight of Neotropical Orchid Bees (Apidae: Euglossini)

SUMMARY The ability of orchid bees to generate vertical forces was evaluated using a load-lifting method that imposed asymptotically increasing loads during ascending flight, ultimately eliciting maximum forces while hovering. Among 11 orchid bee species varying by approximately an order of magnitude in body mass, the capacity to produce vertical forces expressed relative either to body weight or to flight muscle weight declined linearly with increased body mass. Allometric analysis of log-transformed data, by contrast, found maximum vertical force to scale isometrically with body mass, but also to exhibit a slightly negative allometry with respect to flight muscle mass. Maximum stroke amplitude at limiting loads averaged 140° and was remarkably constant among species, a result consistent with anatomical constraints of the hymenopteran thorax on wing motions. By contrast, wing-beat frequencies during maximum performance declined with increasing body mass. Repeated lifting by individual bees reduced performance only when the number of consecutive lifts exceeded 15. Variation in linear mass density of the lifted load did not systematically alter performance estimates, although measurements on one species in two consecutive years at different thermal environments yielded significant differences in estimates of maximum force production. These findings suggest an adverse scaling of vertical force production at greater body mass even if flight muscle mass scales isometrically.

Life history consequences of temperature transients in Drosophila melanogaster.

SUMMARY The physiological and life history consequences of chronic temperatures are well studied in ectotherms. However, little is known about the consequences of short-term exposure to unusually high or low temperatures, as would occur during a weather front. What are the immediate life-history effects of such thermal transients? Can ectotherms recover quickly or do they suffer carry-over effects that persist after weather returns to normal? We measured the impact of thermal transients on egg and progeny production of Drosophila melanogaster Meigen from Washington State. We reared flies at 25°C and then transferred 3- to 5-day old adults to one of three transient treatments (1 or 3 days at 18°C, 1 day at 29°C) before returning them to 25°C. We monitored daily egg production and egg-to-adult viability before (as a control), during, and after the transient as well as fecundity and viability of flies held at constant 18°, 25° and 29°C. This population appears particularly heat tolerant as neither constant nor transient exposure to 29°C (usually a stressful temperature for this species) affected female fecundity or the viability of her progeny. However, a 1- or 3-day exposure to 18°C reduced female fecundity by 75–90% relative to controls, and eggs laid during the 3-day exposure had greatly reduced viability. When returned to 25°C after transient exposure to 18°C, females immediately matched the fecundity and viability of females maintained constantly at 25°C. Therefore, these flies do not suffer negative carry-over effects from these moderate thermal transients. Surprisingly, fitness (intrinsic rate of population growth) was not depressed by transient temperature exposure. However, the severity and especially the timing of the transient will probably determine the likelihood of carry-over effects as well as its effect on fitness.

Drosophila melanogaster locomotion in cold thin air

SUMMARY The alpine environment is likely to challenge insect locomotion because of low mean temperatures and reduced barometric pressure. In this study, we measured the direct and interactive effects of these factors on walking and flight performance of wild-caught Drosophila melanogaster Meigen. We found that decreased temperature and decreased air pressure both reduced walking speed and flight performance. Flies walked more slowly at 18°C and in the lowest air pressure treatment (34 kPa). This treatment, equivalent in air pressure to the top of Mount Everest, was the only air pressure that significantly reduced fly walking speed. Therefore, walking performance in the wild is likely limited by temperature, but not oxygen availability. In contrast to walking performance, low but ecologically realistic air pressures dramatically reduced overall flight performance. The effects of reduced air pressure on flight performance were more pronounced at colder temperatures. Reduced flight performance in high altitude conditions was primarily driven by an increased reluctance for flies to initiate flight rather than outright failure to fly. Such reluctance to fly in high altitude conditions may in part explain the prevalence of aptery and brachyptery in high altitude insects. The observed interactive effects of temperature and air pressure on flight performance confirm the importance of simultaneously manipulating both of these factors when studying the impact of altitudinal conditions on insect physiology and behavior.

Beyond the Mean: Biological Impacts of Cryptic Temperature Change

Studies have typically used shifts in mean temperatures to make predictions about the biotic impacts of climate change. Though shifts in mean temperatures correlate with changes in phenology and distributions, other hidden, or cryptic, changes in temperature, such as temperature variation and extreme temperatures, could pose greater risks to species and ecological communities. Yet, these cryptic temperature changes have received relatively little attention because mean temperatures are readily available and the organism-appropriate temperature response is often elusive. An alternative to using mean temperatures is to view organisms as physiological filters of hourly temperature data. We explored three classes of physiological filters: (1) nonlinear thermal responses using performance curves of insect fitness, (2) cumulative thermal effects using degree-day models for corn emergence, and (3) threshold temperature effects using critical thermal maxima and minima for diverse ectotherms. For all three physiological filters, we determined the change in biological impacts of hourly temperature data from a standard reference period (1961-90) to a current period (2005-10). We then examined how well mean temperature changes during the same time period predicted the biotic impacts we determined from hourly temperature data. In all cases, mean temperature alone provided poor predictions of the impacts of climate change. These results suggest that incorporating high frequency temperature data can provide better predictions for how species will respond to temperature change.

Population genomics of divergence among extreme and intermediate color forms in a polymorphic insect

Abstract Geographic variation in insect coloration is among the most intriguing examples of rapid phenotypic evolution and provides opportunities to study mechanisms of phenotypic change and diversification in closely related lineages. The bumble bee Bombus bifarius comprises two geographically disparate color groups characterized by red‐banded and black‐banded abdominal pigmentation, but with a range of spatially and phenotypically intermediate populations across western North America. Microsatellite analyses have revealed that B. bifarius in the USA are structured into two major groups concordant with geography and color pattern, but also suggest ongoing gene flow among regional populations. In this study, we better resolve the relationships among major color groups to better understand evolutionary mechanisms promoting and maintaining such polymorphism. We analyze >90,000 and >25,000 single‐nucleotide polymorphisms derived from transcriptome (RNAseq) and double digest restriction site associated DNA sequencing (ddRAD), respectively, in representative samples from spatial and color pattern extremes in B. bifarius as well as phenotypic and geographic intermediates. Both ddRAD and RNAseq data illustrate substantial genome‐wide differentiation of the red‐banded (eastern) color form from both black‐banded (western) and intermediate (central) phenotypes and negligible differentiation among the latter populations, with no obvious admixture among bees from the two major lineages. Results thus indicate much stronger background differentiation among B. bifarius lineages than expected, highlighting potential challenges for revealing loci underlying color polymorphism from population genetic data alone. These findings will have significance for resolving taxonomic confusion in this species and in future efforts to investigate color‐pattern evolution in B. bifarius and other polymorphic bumble bee species.

Thermodynamics Constrains Allometric Scaling of Optimal Development Time in Insects

Development time is a critical life-history trait that has profound effects on organism fitness and on population growth rates. For ectotherms, development time is strongly influenced by temperature and is predicted to scale with body mass to the quarter power based on 1) the ontogenetic growth model of the metabolic theory of ecology which describes a bioenergetic balance between tissue maintenance and growth given the scaling relationship between metabolism and body size, and 2) numerous studies, primarily of vertebrate endotherms, that largely support this prediction. However, few studies have investigated the allometry of development time among invertebrates, including insects. Abundant data on development of diverse insects provides an ideal opportunity to better understand the scaling of development time in this ecologically and economically important group. Insects develop more quickly at warmer temperatures until reaching a minimum development time at some optimal temperature, after which development slows. We evaluated the allometry of insect development time by compiling estimates of minimum development time and optimal developmental temperature for 361 insect species from 16 orders with body mass varying over nearly 6 orders of magnitude. Allometric scaling exponents varied with the statistical approach: standardized major axis regression supported the predicted quarter-power scaling relationship, but ordinary and phylogenetic generalized least squares did not. Regardless of the statistical approach, body size alone explained less than 28% of the variation in development time. Models that also included optimal temperature explained over 50% of the variation in development time. Warm-adapted insects developed more quickly, regardless of body size, supporting the “hotter is better” hypothesis that posits that ectotherms have a limited ability to evolutionarily compensate for the depressing effects of low temperatures on rates of biological processes. The remaining unexplained variation in development time likely reflects additional ecological and evolutionary differences among insect species.

Altitudinal variation in bumble bee (Bombus) critical thermal limits.

Organism critical thermal limits are often tightly linked to current geographic distribution and can therefore help predict future range shifts driven by changing environmental temperatures. Thermal tolerance of diverse organisms often varies predictably with latitude, with upper thermal limits changing little and lower thermal limits decreasing with latitude. Despite similarly steep gradients in environmental temperatures across altitude, few studies have investigated altitudinal variation in critical thermal limits. We estimated critical thermal minimum (CTmin), critical thermal maximum (CTmax) and recovery temperature (Trec) by tracking righting response of three bumble bee species during thermal ramps: Bombus huntii collected from 2180m asl, and Bombus bifarius and Bombus sylvicola collected from 3290m asl in Wyoming, USA. Overall, larger bees could tolerate more extreme temperatures, likely due to a thermal inertia driven lag between core body temperatures and air temperatures. Despite their smaller size, high altitude bumble bees tolerated colder air temperatures: they had ~1°C lower CTmin and recovered from cold exposure at ~3-4°C lower air temperatures. Conversely, low altitude bees tolerated ~5°C hotter air temperatures. These altitudinal differences in thermal tolerance parallel differences in average daily minimum (1.2°C) and maximum (7.5°C) temperatures between these sites. These results provide one of the few measurements of organism thermal tolerance across altitude and the first evidence for geographical differences in tolerance of temperature extremes in heterothermic bumble bees.