Lower Critical Thermal Limits Research Articles

Age and mating status have complex but modest effects on the critical thermal limits of adult Mediterranean fruit flies from geographically divergent populations.

The highly invasive Mediterranean fruit fly (medfly), Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), is currently expanding its geographic distribution into cooler temperate areas of the Northern Hemisphere. In marginal conditions, the invasion potential of medfly depends in part on innate tolerance to the novel environmental conditions. Physiological tolerances are potentially influenced by interactions among multiple factors, such as organism age or reproductive maturity, sex, and mating status. Furthermore, the relationships between the above factors and tolerances may differ among geographically distinct populations. Here, the effects of age and mating status on thermal tolerance of three geographically distinct medfly populations along a latitudinal gradient ranging from Greece (Crete & Volos) to Croatia (Dubrovnik) were examined. The upper and lower critical thermal limits (scored as loss of neuromuscular function during controlled cooling or heating) of adult males and females (a) at 1-, 6-, 15-, and 35 days old and of (b) both mated and virgin flies were assessed. Results showed that estimates of lower and upper thermal limits (CTmin and CTmax) were both population- and age-dependent. In most age classes tested, CTmin values were lower for the adults obtained from Crete and higher for those from Dubrovnik. CTmax values were lower for the females from Dubrovnik compared to the females from any other population on day one after emergence but not on days 6, 15 and 35. Differences among populations were observed across different age classes both for cold and heat tolerance but mostly in CTmin estimates. Mating status had a little effect on cold and heat tolerance. Complex patterns of thermal limit variation within and among populations suggest a suite of factors determine population-level mortality from thermal extremes under field conditions in medfly. These results contribute towards understanding the invasion dynamics of medfly and its range expansion to northern, more temperate regions of Europe.

Insecticide resistant mosquitoes remain thermal stress resistant, without loss of thermal plasticity

A major component of mosquito's climate change response is their heat tolerance, and any ability to rapidly adjust to extreme environmental conditions through phenotypic plasticity. The excessive use of insecticides for the control of major mosquito species leads to resistant populations, however it is largely unclear if this concurrently impacts thermal stress resistance and their potential to adjust tolerance via phenotypic plasticity. Culex pipiens pipiens, Culex pipiens molestus and Aedes albopictus populations obtained from the same region were subjected for 12 generations to selection trials to larvicides Diflubenzuron (DFB) and Bacillus thuringiensis subsp. israelensis (Bti) to develop insecticide resistance. Adults emerging from the selected populations were acclimated at different temperatures and the upper and lower critical thermal limits (CTmax and CTmin) were estimated using dynamic thermal assays. In addition, the supercooling points (SCPs) of non-acclimated adults of resistant and control populations were determined. Our results revealed marked differences in thermal response among the three species, the different acclimation regimes and sexes. Aedes albopictus was more resistant in high than low temperatures compared to both Culex pipiens biotypes. Culex forms responded similarly to heat but differently to cold stress. In both forms, females responded better than males to all thermal stressors. Acclimation at higher and lower temperatures improves CTmax and CTmin values, respectively in both insecticide resistant and control populations of all three species. Overall, selection to insecticides did not affect the thermal performance of adults. Hence, insecticide-resistant mosquito populations perform similarly to untreated ones and are capable of readily adapting to new environmental changes rising concerns regarding their geographic range expansion and disease transmission globally.

Adequate sample sizes for improved accuracy of thermal trait estimates

Abstract Thermal traits, such as upper and lower critical thermal limits, are vital indicators of the vulnerability of populations and species to environmental change. Thus, accurate estimates of these traits are needed to explain biological patterns and forecast responses to the changing thermal environment. However, many thermal trait studies measure relatively few individuals to estimate traits for whole populations or species. To ascertain if, and how, sample size affects the accuracy of reported trait means and variances, we applied a subsampling and equivalency testing approach to empirical and simulated trait data to investigate the accuracy of trait estimates relative to sample size and the skew and variance of the trait distribution in the source population. Simulation results indicated that only 7.9% of the 428 critical thermal limit traits documented in a recent synthesis of thermal trait data reported sufficiently large sample sizes, relative to variance, to ensure confidence in the reported mean trait value with negligible (±0.25°C) error. Greater inter‐individual trait variance in the source population requires a larger number of individuals to be measured to accurately estimate the mean and variance of that trait. This pattern is mitigated somewhat by the tendency of thermal traits to exhibit skew‐normal distributions. As measurements of few individuals from a population are unlikely to provide accurate estimates of thermal traits, the propensity towards small sample sizes in thermal trait studies is concerning. Macrophysiological syntheses often use these data to describe, explain and predict broad‐scale ecological patterns. Thus, insufficient sample sizes in the original studies could diminish the robustness of these patterns and predictions. For future studies, we recommend that preliminary data be used to estimate trait variance and calculate minimum sample sizes. If small sample sizes are unavoidable, larger error around the measured trait mean must be assumed and accounted for in subsequent analyses. A free Plain Language Summary can be found within the Supporting Information of this article.

Sub-critical limits are viable alternatives to critical thermal limits.

Thermal traits are frequently used to explain variation in species distributions, abundance, and sensitivity to climate change. Due to their utility and ease of measurement, critical thermal limits in particular have proliferated across the ecophysiological literature. Critical limit assays can, however, have deleterious or even lethal effects on individuals and there is growing recognition that intermediate metrics of performance can provide a further, nuanced understanding of how species interact with their environments. Meanwhile, the scarcity of data describing sub-critical or voluntary limits, which have been proposed as alternatives to critical limits and can be collected under less extreme conditions, reduces their value in comparative analyses and broad-scale syntheses. To overcome these limitations and determine if sub-critical limits are viable proxies for upper and lower critical thermal limits we measured and compared the critical and sub-critical thermal limits of 2023 ants representing 51 species. Sub-critical limits in isolation were a satisfactory linear predictor for both individual and species critical limits and when species identity was also considered there were substantial gains in variance explained. These gains indicate that a species-specific conversion factor can further improve estimates of critical traits using sub-critical proxies. Sub-critical limits can, therefore, be integrated into broader syntheses of critical limits and confidently used to calculate common ecological metrics, such as warming tolerance, so long as uncertainty in estimates is explicitly acknowledged. Although lower thermal traits exhibited more variation than their upper counterparts, the stronger phylogenetic signal of lower thermal traits indicates that appropriate conversions for lower thermal traits can be inferred from congenerics or other closely related taxa.

Increased acclimation ability accompanies a thermal niche shift of a recent invasion.

Globalization is removing dispersal barriers for the establishment of invasive species and enabling their spread to novel climates. New thermal environments in the invaded range will be particularly challenging for ectotherms, as their metabolism directly depends on environmental temperature. However, we know little about the role climatic niche shifts play in the invasion process, and the underlining physiological mechanisms. We tested if a thermal niche shift accompanies an invasion, and if native and introduced populations differ in their ability to acclimate thermal limits. We used an alien ant species-Tapinoma magnum-which recently started to spread across Europe. Using occurrence data and accompanying climatic variables, we measured the amount of overlap between thermal niches in the native and invaded range. We then experimentally tested the acclimation ability in native and introduced populations by incubating T. magnum at 18, 25 and 30°C. We measured upper and lower critical thermal limits after 7 and 21days. We found that T. magnum occupies a distinct thermal niche in its introduced range, which is on average 3.5°C colder than its native range. Critical thermal minimum did not differ between populations from the two ranges when colonies were maintained at 25 or 30°C, but did differ after colony acclimation at a lower temperature. We found twofold greater acclimation ability of introduced populations to lower temperatures, after prolonged incubation at 18°C. Increased acclimation ability of lower thermal limits could explain the expansion of the realized thermal niche in the invaded range, and likely contributed to the spread of this species to cooler climates. Such thermal plasticity could be an important, yet so far understudied, factor underlying the expansion of invasive insects into novel climates.

Temperature and oxygen related ecophysiological traits of snow trout (Schizothorax richardsonii) are sensitive to seasonal changes in a Himalayan stream environment.

In this study, we investigated the seasonal changes in key eco-physiological traits of a wild population of snow trout, Schizothorax richardsonii from river Gola in the Indian Himalayan region over one year. Live specimens (5.8-31.4 g) were electro-fished from their natural habitat during representative months of four seasons with notable differences in water temperature, oxygen concentration and saturation. After 24-72 h of captive-acclimation, the fishes were examined for upper and lower critical thermal limits (CTmax and CTmin), incipient lethal oxygen thresholds (ILOC and ILOS), apparent routine and maximum oxygen consumption rates (MO2rout and MO2max), and blood haemoglobin-haematocrit. Across the seasons, mean CTmin and CTmax values ranged from ∼0 to 34.6 °C, suggesting a relatively wide acute thermal tolerance range for this predominantly cold-water fish. Changes in the habitat's thermal condition during winter to summer was reflected in the CTmin (∼0-2.4 °C) and CTmax (31.7-34.4 °C) estimates, while the highest thermal scope (CTmax-CTmin; 33.2 °C) was recorded in autumn. Concurrently, the incipient lethal hypoxia threshold observed in autumn (ILOS-2.6% and ILOC-0.19 mgO2/L) was significantly lower than the other three seasons, possibly linked to warm-acclimation. The reduction in blood haemoglobin-haematocrit levels during winter could limit the oxygen carrying capacity, with possible reciprocations in thermal tolerance and aerobic metabolism. Concerning body mass corrected oxygen consumption, the apparent MO2rout was found to increase in a temperature-dependent manner from 150.3 mgO2/kg/h at 12 °C to 315.2 mgO2/kg/h at 26 °C, with Q10 ranging from 1.6 to 2.2. Whereas, changes in MO2max was not temperature sensitive (Q10 of 0.7-1.3), except during spring-summer (Q10-2), with lowest and highest measurements in spring and autumn (934 and 1514 mgO2/kg/h), respectively. Collectively, these data form the first information report on the seasonal plasticity in thermal and respiratory physiology of a Schizothoracine fish species, bearing significance for their conservation, aquaculture and habitat monitoring.

Extensive Acclimation in Ectotherms Conceals Interspecific Variation in Thermal Tolerance Limits.

Species’ tolerance limits determine their capacity to tolerate climatic extremes and limit their potential distributions. Interspecific variation in thermal tolerances is often proposed to indicate climatic vulnerability and is, therefore, the subject of many recent meta-studies on differential capacities of species from climatically different habitats to deal with climate change. Most studies on thermal tolerances do not acclimate animals or use inconsistent, and insufficient, acclimation times, limiting our knowledge of the shape, duration and extent of acclimation responses. Consequently patterns in thermal tolerances observed in meta-analyses, based on data from the literature are based on inconsistent, partial acclimation and true trends may be obscured. In this study we describe time-course of complete acclimation of critical thermal minima in the tropical ectotherm Carlia longipes and compare it to the average acclimation response of other reptiles, estimated from published data, to assess how much acclimation time may contribute to observed differences in thermal limits. Carlia longipes decreased their lower critical thermal limits by 2.4°C and completed 95% of acclimation in 17 weeks. Wild populations did not mirror this acclimation process over the winter. Other reptiles appear to decrease cold tolerance more quickly (95% in 7 weeks) and to a greater extent, with an estimated average acclimation response of 6.1°C. However, without data on tolerances after longer acclimation times available, our capacity to estimate final acclimation state is very limited. Based on the subset of data available for meta-analysis, much of the variation in cold tolerance observed in the literature can be attributed to acclimation time. Our results indicate that (i) acclimation responses can be slow and substantial, even in tropical species, and (ii) interspecific differences in acclimation speed and extent may obscure trends assessed in some meta-studies. Cold tolerances of wild animals are representative of cumulative responses to recent environments, while lengthy acclimation is necessary for controlled comparisons of physiological tolerances. Measures of inconsistent, intermediate acclimation states, as reported by many studies, represent neither the realised nor the potential tolerance in that population, are very likely underestimates of species’ physiological capacities and may consequently be of limited value.

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 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.