Susana Clusella-Trullas

Critical thermal limits depend on methodological context

A full-factorial study of the effects of rates of temperature change and start temperatures was undertaken for both upper and lower critical thermal limits (CTLs) using the tsetse fly, Glossina pallidipes. Results show that rates of temperature change and start temperatures have highly significant effects on CTLs, although the duration of the experiment also has a major effect. Contrary to a widely held expectation, slower rates of temperature change (i.e. longer experimental duration) resulted in poorer thermal tolerance at both high and low temperatures. Thus, across treatments, a negative relationship existed between duration and upper CTL while a positive relationship existed between duration and lower CTL. Most importantly, for predicting tsetse distribution, G. pallidipes suffer loss of function at less severe temperatures under the most ecologically relevant experimental conditions for upper (0.06°C min−1; 35°C start temperature) and lower CTL (0.06°C min−1; 24°C start temperature). This suggests that the functional thermal range of G. pallidipes in the wild may be much narrower than previously suspected, approximately 20–40°C, and highlights their sensitivity to even moderate temperature variation. These effects are explained by limited plasticity of CTLs in this species over short time scales. The results of the present study have broad implications for understanding temperature tolerance in these and other terrestrial arthropods.

Climatic predictors of temperature performance curve parameters in ectotherms imply complex responses to climate change.

Determining organismal responses to climate change is one of biology’s greatest challenges. Recent forecasts for future climates emphasize altered temperature variation and precipitation, but most studies of animals have largely focused on forecasting the outcome of changes in mean temperature. Theory suggests that extreme thermal variation and precipitation will influence species performance and hence affect their response to changes in climate. Using an information-theoretic approach, we show that in squamate ectotherms (mostly lizards and snakes), two fitness-influencing components of performance, the critical thermal maximum and the thermal optimum, are more closely related to temperature variation and to precipitation, respectively, than they are to mean thermal conditions. By contrast, critical thermal minimum is related to mean annual temperature. Our results suggest that temperature variation and precipitation regimes have had a strong influence on the evolution of ectotherm performance, so that forecasts for animal responses to climate change will have to incorporate these factors and not only changes in average temperature.

Macrophysiology: A Conceptual Reunification

Widespread recognition of the importance of biological studies at large spatial and temporal scales, particularly in the face of many of the most pressing issues facing humanity, has fueled the argument that there is a need to reinvigorate such studies in physiological ecology through the establishment of a macrophysiology. Following a period when the fields of ecology and physiological ecology had been regarded as largely synonymous, studies of this kind were relatively commonplace in the first half of the twentieth century. However, such large‐scale work subsequently became rather scarce as physiological studies concentrated on the biochemical and molecular mechanisms underlying the capacities and tolerances of species. In some sense, macrophysiology is thus an attempt at a conceptual reunification. In this article, we provide a conceptual framework for the continued development of macrophysiology. We subdivide this framework into three major components: the establishment of macrophysiological patterns, determining the form of those patterns (the very general ways in which they are shaped), and understanding the mechanisms that give rise to them. We suggest ways in which each of these components could be developed usefully.

The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology

The harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), is native to Asia but has been intentionally introduced to many countries as a biological control agent of pest insects. In numerous countries, however, it has been introduced unintentionally. The dramatic spread of H. axyridis within many countries has been met with considerable trepidation. It is a generalist top predator, able to thrive in many habitats and across wide climatic conditions. It poses a threat to biodiversity, particularly aphidophagous insects, through competition and predation, and in many countries adverse effects have been reported on other species, particularly coccinellids. However, the patterns are not consistent around the world and seem to be affected by many factors including landscape and climate. Research on H. axyridis has provided detailed insights into invasion biology from broad patterns and processes to approaches in surveillance and monitoring. An impressive number of studies on this alien species have provided mechanistic evidence alongside models explaining large-scale patterns and processes. The involvement of citizens in monitoring this species in a number of countries around the world is inspiring and has provided data on scales that would be otherwise unachievable. Harmonia axyridis has successfully been used as a model invasive alien species and has been the inspiration for global collaborations at various scales. There is considerable scope to expand the research and associated collaborations, particularly to increase the breadth of parallel studies conducted in the native and invaded regions. Indeed a qualitative comparison of biological traits across the native and invaded range suggests that there are differences which ultimately could influence the population dynamics of this invader. Here we provide an overview of the invasion history and ecology of H. axyridis globally with consideration of future research perspectives. We reflect broadly on the contributions of such research to our understanding of invasion biology while also informing policy and people.

Effects of acclimation temperature on thermal tolerance, locomotion performance and respiratory metabolism in Acheta domesticus L. (Orthoptera: Gryllidae)

The effects of acclimation temperature on insect thermal performance curves are generally poorly understood but significant for understanding responses to future climate variation and the evolution of these reaction norms. Here, in Acheta domesticus, we examine the physiological effects of 7-9 days acclimation to temperatures 4 degrees C above and below optimum growth temperature of 29 degrees C (i.e. 25, 29, 33 degrees C) for traits of resistance to thermal extremes, temperature-dependence of locomotion performance (jumping distance and running speed) and temperature-dependence of respiratory metabolism. We also examine the effects of acclimation on mitochondrial cytochrome c oxidase (CCO) enzyme activity. Chill coma recovery time (CRRT) was significantly reduced from 38 to 13min with acclimation at 33-25 degrees C, respectively. Heat knockdown resistance was less responsive than CCRT to acclimation, with no significant effects of acclimation detected for heat knockdown times (25 degrees C: 18.25, 29 degrees C: 18.07, 33 degrees C: 25.5min). Thermal optima for running speed were higher (39.4-40.6 degrees C) than those for jumping performance (25.6-30.9 degrees C). Acclimation temperature affected jumping distance but not running speed (general linear model, p=0.0075) although maximum performance (U(MAX)) and optimum temperature (T(OPT)) of the performance curves showed small or insignificant effects of acclimation temperature. However, these effects were sensitive to the method of analysis since analyses of T(OPT), U(MAX) and the temperature breadth (T(BR)) derived from non-linear curve-fitting approaches produced high inter-individual variation within acclimation groups and reduced variation between acclimation groups. Standard metabolic rate (SMR) was positively related to body mass and test temperature. Acclimation temperature significantly influenced the slope of the SMR-temperature reaction norms, whereas no variation in the intercept was found. The CCO enzyme activity remained unaffected by thermal acclimation. Finally, high temperature acclimation resulted in significant increases in mortality (60-70% at 33 degrees C vs. 20-30% at 25 and 29 degrees C). These results suggest that although A. domesticus may be able to cope with low temperature extremes to some degree through phenotypic plasticity, population declines with warmer mean temperatures of only a few degrees are likely owing to the limited plasticity of their performance curves.

Lizard thermal trait variation at multiple scales: a review

Thermal trait variation is of fundamental importance to forecasting the impacts of environmental change on lizard diversity. Here, we review the literature for patterns of variation in traits of upper and lower sub-lethal temperature limits, temperature preference and active body temperature in the field, in relation to space, time and phylogeny. Through time, we focus on the direction and magnitude of trait change within days, among seasons and as a consequence of acclimation. Across space, we examine altitudinal and latitudinal patterns, incorporating inter-specific analyses at regional and global scales. This synthesis highlights the consistency or lack thereof, of thermal trait responses, the relative magnitude of change among traits and several knowledge gaps identified in the relationships examined. We suggest that physiological information is becoming essential for forecasting environmental change sensitivity of lizards by providing estimates of plasticity and evolutionary scope.

Directional Evolution of the Slope of the Metabolic Rate–Temperature Relationship Is Correlated with Climate

The evolution of metabolic rate–temperature (MR‐T) reaction norms is of fundamental importance to physiological ecology. Metabolic cold adaptation (MCA) predicts that populations or species from cooler environments will have either a higher metabolic rate at a common temperature or steeper MR‐T relationships, indicating greater sensitivity of respiratory metabolism to temperature. Support for MCA has been found in some insect species by comparing species or populations differing in latitude. However, the generality of these findings are contentious, with most studies either unable to account for phenotypic plasticity or the evolutionary relatedness of species or populations. Hence, the importance of MCA is vigorously debated from both evolutionary and ecological perspectives. Furthermore, few species, particularly from tropical environments, have been shown to differ in MR‐T sensitivity along altitudinal temperature gradients. Here, using four populations of tsetse flies (Glossina pallidipes, Diptera: Glossinidae) from thermally distinct geographic regions, we test the hypothesis that there is evolved variation in MR‐T relationships to cold climates. We found that a high‐altitude equatorial population from a cool habitat has a steeper MR‐T reaction norm. By contrast, other populations from warmer environments in East Africa do not differ with respect to their MR‐T reaction norms. Squared‐change parsimony analyses, based on the combined mitochondrial 16S rDNA ribosomal subunit and cytochrome c oxidase subunit I (COI), support the hypothesis of adaptive differentiation of MR‐T reaction norms in the cool‐climate population. Seasonal adjustments or laboratory‐temperature‐induced phenotypic plasticity changed the intercept of the reaction norm rather than the slope, and thus the observed intraspecific variation in slopes of MR‐T reaction norms could not be accounted for by phenotypic plasticity. These results therefore suggest evolutionary adaptation of MR‐T reaction norms to cool climates (<22°C) in tsetse and provide novel support for MCA within an insect species.

Phenotypic plasticity of gas exchange pattern and water loss in Scarabaeus spretus (Coleoptera: Scarabaeidae): deconstructing the basis for metabolic rate variation

SUMMARY Investigation of gas exchange patterns and modulation of metabolism provide insight into metabolic control systems and evolution in diverse terrestrial environments. Variation in metabolic rate in response to environmental conditions has been explained largely in the context of two contrasting hypotheses, namely metabolic depression in response to stressful or resource-(e.g. water) limited conditions, or elevation of metabolism at low temperatures to sustain life in extreme conditions. To deconstruct the basis for metabolic rate changes in response to temperature variation, here we undertake a full factorial study investigating the longer- and short-term effects of temperature exposure on gas exchange patterns. We examined responses of traits of gas exchange [standard metabolic rate (SMR); discontinuous gas exchange (DGE) cycle frequency; cuticular, respiratory and total water loss rate (WLR)] to elucidate the magnitude and form of plastic responses in the dung beetle, Scarabaeus spretus. Results showed that short- and longer-term temperature variation generally have significant effects on SMR and WLR. Overall, acclimation to increased temperature led to a decline in SMR (from 0.071±0.004 ml CO2 h–1 in 15°C-acclimated beetles to 0.039±0.004 ml CO2 h–1 in 25°C-acclimated beetles measured at 20°C) modulated by reduced DGE frequency (15°C acclimation: 0.554±0.027 mHz, 20°C acclimation: 0.257±0.030 mHz, 25°C acclimation: 0.208±0.027 mHz recorded at 20°C), reduced cuticular WLRs (from 1.058±0.537 mg h–1 in 15°C-acclimated beetles to 0.900±0.400 mg h–1 in 25°C-acclimated beetles measured at 20°C) and reduced total WLR (from 4.2±0.5 mg h–1 in 15°C-acclimated beetles to 3.1±0.5 mg h–1 in 25°C-acclimated beetles measured at 25°C). Respiratory WLR was reduced from 2.25±0.40 mg h–1 in 15°C-acclimated beetles to 1.60±0.40 mg h–1 in 25°C-acclimated beetles measured at 25°C, suggesting conservation of water during DGE bursts. Overall, this suggests water conservation is a priority for S. spretus exposed to longer-term temperature variation, rather than elevation of SMR in response to low temperature acclimation, as might be expected from a beetle living in a relatively warm, low rainfall summer region. These results are significant for understanding the evolution of gas exchange patterns and trade-offs between metabolic rate and water balance in insects and other terrestrial arthropods.

Comment on “Erosion of Lizard Diversity by Climate Change and Altered Thermal Niches”

Using a regionally calibrated model, Sinervo et al. (Reports, 14 May 2010, p. 894) predicted potential climate change impacts on lizard populations and estimated that many extinctions are under way. We argue that this model is not sufficient for predicting global losses in lizard species in response to anthropogenic climate change.

The effects of acclimation and rates of temperature change on critical thermal limits in Tenebrio molitor (Tenebrionidae) and Cyrtobagous salviniae (Curculionidae)

Critical thermal limits provide an indication of the range of temperatures across which organisms may survive, and the extent of the lability of these limits offers insights into the likely impacts of changing thermal environments on such survival. However, investigations of these limits may be affected by the circumstances under which trials are undertaken. Only a few studies have examined these effects, and typically not for beetles. This group has also not been considered in the context of the time courses of acclimation and its reversal, both of which are important for estimating the responses of species to transient temperature changes. Here we therefore examine the effects of rate of temperature change on critical thermal maxima (CT(max)) and minima (CT(min)), as well as the time course of the acclimation response and its reversal in two beetle species, Tenebrio molitor and Cyrtobagous salviniae. Increasing rates of temperature change had opposite effects on T. molitor and C. salviniae. In T. molitor, faster rates of change reduced both CT(max) (c. 2°C) and CT(min) (c. 3°C), while in C. salviniae faster rates of change increased both CT(max) (c. 6°C) and CT(min) (c. 4°C). CT(max) in T. molitor showed little response to acclimation, while the response to acclimation of CT(min) was most pronounced following exposure to 35°C (from 25°C) and was complete within 24 h. The time course of acclimation of CT(max) in C. salviniae was 2 days when exposed to 36°C (from c. 26°C), while that of CT(min) was less than 3 days when exposed to 18°C. In T. molitor, the time course of reacclimation to 25°C after treatments at 15°C and 35°C at 75% RH was longer than the time course of acclimation, and varied from 3-6 days for CT(max) and 6 days for CT(min). In C. salviniae, little change in CT(max) and CT(min) (<0.5°C) took place in all treatments suggesting that reacclimation may only occur after the 7 day period used in this study. These results indicate that both T. molitor and C. salviniae may be restricted in their ability to respond to transient temperature changes at short-time scales, and instead may have to rely on behavioral adjustments to avoid deleterious effects at high temperatures.