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 degrees C min(-1); 35 degrees C start temperature) and lower CTL (0.06 degrees C min(-1); 24 degrees 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 degrees 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.
For tsetse (Glossina spp.), the vectors of human and animal trypanosomiases, the physiological mechanisms linking variation in population dynamics with changing weather conditions have not been well established. Here, we investigate high- and low-temperature tolerance in terms of activity limits and survival in a natural population of adult Glossina pallidipes from eastern Zambia. Due to increased interest in chilling flies for handling and aerial dispersal in sterile insect technique control and eradication programmes, we also provide further detailed investigation of low-temperature responses. In wild-caught G. pallidipes, the probability of survival for 50% of the population at low-temperatures was at 3.7, 8.9 and 9.6 degrees C (95% CIs: +/-1.5 degrees C) for 1, 2 and 3 h treatments, respectively. At high temperatures, it was estimated that treatments at 37.9, 36.2 and 35.6 degrees C (95% CIs: +/-0.5 degrees C) would yield 50% population survival for 1, 2 and 3 h, respectively. Significant effects of time and temperature were detected at both temperature extremes (GLZ, p<0.05 in all cases) although a time-temperature interaction was only detected at high temperatures (p<0.0001). We synthesized data from four other Kenyan populations and found that upper critical thermal limits showed little variation among populations and laboratory treatments (range: 43.9-45.0 degrees C; 0.25 degrees C/min heating rate), although reduction to more ecologically relevant heating rates (0.06 degrees C/min) reduce these values significantly from approximately 44.4 to 40.6 degrees C, thereby providing a causal explanation for why tsetse distribution may be high-temperature limited. By contrast, low-temperature limits showed substantial variation among populations and acclimation treatments (range: 4.5-13.8 degrees C; 0.25 degrees C/min), indicating high levels of inter-population variability. Ecologically relevant cooling rates (0.06 degrees C/min) suggest tsetses are likely to experience chill coma temperatures under natural conditions (approximately 20-21 degrees C). The results from acute hardening experiments in the Zambian population demonstrate limited ability to improve low-temperature tolerance over short (hourly) timescales after non-lethal pre-treatments. In flies which survived chilling, recovery times were non-linear with plateaus between 2-6 and 8-12 degrees C. Survival times ranged between 4 and 36 h and did not vary between flies which had undergone chill coma by comparison with flies which had not, even after factoring body condition into the analyses (p>0.5 in all cases). However, flies with low chill coma values had the highest body water and fat content, indicating that when energy reserves are depleted, low-temperature tolerance may be compromised. Overall, these results suggest that physiological mechanisms may provide insight into tsetse population dynamics, hence distribution and abundance, and support a general prediction for reduced geographic distribution under future climate warming scenarios.
The beneficial acclimation hypothesis (BAH) is controversial. While physiological work all but assumes that the BAH is true, recent studies have shown that support for the BAH is typically wanting. The latter have been criticized for assessing the benefits of developmental plasticity rather than acclimation. Here we examine the BAH within a strong inference framework for five congeneric species of ameronothroid oribatid mites that occupy marine to terrestrial habitats. We do so by assessing responses of maximum speed, optimum temperature, and performance breadth, measured from -10 degrees C to 35 degrees C, to four treatment temperatures (0 degrees , 5 degrees , 10 degrees , and 15 degrees C). We show that the BAH and its alternatives often make similar empirical predictions. Weak beneficial acclimation is characteristic of one of the more marine species. In the other two upper-shore and marine species, evidence exists for deleterious acclimation and the colder-is-better hypothesis. In the two fully terrestrial species, there is no plasticity. Lack of plasticity is beneficial when cue reliability is low or costs of plasticity are high, and the former seems plausible in terrestrial habitats. However, weak plasticity in the upper-shore/marine species and the absence of plasticity in the terrestrial species might also be a consequence of phylogenetic constraint.
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 degrees C) in tsetse and provide novel support for MCA within an insect species.
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