Lower CTmin Research Articles

Fatty acid profiles and tolerance to temperature extremes in Daphnia pulex.

Identification of physiological processes setting thermal tolerance limits is essential to describing adaptive response to temperature changes. We used the North American Daphnia pulex complex, which makes a remarkable model for comparative physiology as it is composed of clones differing in heat tolerance and ploidies, and with a wide geographic distribution. The fatty acid composition of 18 diploid and triploid D. pulex clones acclimated to 16°C and 24°C was measured and compared with their tolerance to extreme high and low temperatures (CTmax and CTmin, respectively). Eicosapentaenoic acid (EPA) relative content showed a strong negative relationship with CTmax and a clear association with CTmin. Higher unsaturation and peroxidation indices were associated with better cold tolerance, whereas saturated fatty acids and monounsaturated fatty acids were associated with lower cold tolerance. Triploid D. pulex clones accumulated more EPA and had lower CTmin than diploid clones (better cold tolerance). Triploid clones retained more omega-6 polyunsaturated fatty acids at high temperature. CTmax was positively correlated with CTmin, suggesting the existence of important constraints in temperature tolerance caused by fatty acid composition.

Polyploidy confers better cold tolerance in Daphnia

Despite decades of studies on the differential distribution of polyploid organisms, the causes of this pattern have yet to be elucidated. This study aimed to explore some of the possible physiological mechanisms explaining the differential northern distribution of polyploid clones of Daphnia pulex compared to the one of the diploid parental species. The critical thermal minimum (CTmin) was measured in 17 D. pulex clones of contrasted ploidy (diploid and triploid) and geographic origins (temperate and subarctic climates) reared under low and high temperatures (16 and 24°C). Triploid clones had better cold tolerance (lower CTmin) than both sympatric and temperate diploid clones. No significant association was found between CTmin and body size nor with cell size. We suggest that triploids might express a cold shock resistant phenotype related to higher gene expression and/or fatty acid profiles. Cold tolerance can be viewed as one of the possible reasons for polyploid preponderance in subarctic climates.

It is hot and cold here: the role of thermotolerance in the ability of spiders to colonize tree plantations in the southern Atlantic Forest.

Worldwide, with the decline of natural habitats, species with reduced niche breadth (specialists) are at greater risk of extinction as they cannot colonise or persist in disturbed habitat types. However, the role of thermal tolerance as a critical trait in understanding changes in species diversity in disturbed habitats, e.g., due to forest replacement by tree plantations, is still understudied. To examine the role of thermal tolerance on the responses of specialist and generalist species to habitat disturbances, we measured and compared local temperature throughout the year and thermotolerance traits [upper (CTmax) and lower (CTmin) thermal limits] of the most abundant species of spiders from different guilds inhabiting pine tree plantations and native Atlantic Forests in South America. Following the thermal adaptation hypothesis, we predicted that generalist species would show a wider thermal tolerance range (i.e., lower CTmin and higher CTmax) than forest specialist species. As expected, generalist species showed significantly higher CTmax and lower CTmin values than specialist species with wider thermal tolerance ranges than forest specialist species. These differences are more marked in orb weavers than in aerial hunter spiders. Our study supports the specialisation disturbance and thermal hypotheses. It highlights that habitat-specialist species are more vulnerable to environmental changes associated with vegetation structure and microclimatic conditions. Moreover, thermal tolerance is a key response trait to explain the Atlantic Forest spider's ability (or inability) to colonise and persist in human-productive land uses.

Low heat tolerance and high desiccation resistance in nocturnal bees and the implications for nocturnal pollination under climate change

Predicting insect responses to climate change is essential for preserving ecosystem services and biodiversity. Due to high daytime temperatures and low humidity levels, nocturnal insects are expected to have lower heat and desiccation tolerance compared to diurnal species. We estimated the lower (CTMin) and upper (CTMax) thermal limits of Megalopta, a group of neotropical, forest-dwelling bees. We calculated warming tolerance (WT) as a metric to assess vulnerability to global warming and measured survival rates during simulated heatwaves and desiccation stress events. We also assessed the impact of body size and reproductive status (ovary area) on bees’ thermal limits. Megalopta displayed lower CTMin, CTMax, and WTs than diurnal bees (stingless bees, orchid bees, and carpenter bees), but exhibited similar mortality during simulated heatwave and higher desiccation tolerance. CTMin increased with increasing body size across all bees but decreased with increasing body size and ovary area in Megalopta, suggesting a reproductive cost or differences in thermal environments. CTMax did not increase with increasing body size or ovary area. These results indicate a greater sensitivity of Megalopta to temperature than humidity and reinforce the idea that nocturnal insects are thermally constrained, which might threaten pollination services in nocturnal contexts during global warming.

Colonizing polar environments: thermal niche evolution in Collembola

Temperature is a primary driver to define the ecophysiological activity and performance of ectotherms. Thus, thermal tolerance limits have a profound effect in determining geographic ranges. In regions with extreme cold temperatures, lower thermal limits of species are a key physiological trait for survival. Moreover, thermal niche breadth also plays an important role in allowing organisms to withstand climatic variability and confers species with broader potential to establish in new regions. Here we study the evolution of thermal tolerance limits among Collembola (Arthropoda) and explore how they are affected by the colonization of polar environments. In addition, we test the hypothesis that globally invasive species are more eurythermal than non‐invasive ones. Critical thermal limits (CTmin and CTmax), classic measurements of thermal tolerance, were compiled from the literature and complemented with experimental assays for springtail species. Genetic data of the mitochondrial gene cytochrome oxidase subunit 1 (COI) was used to assemble a phylogeny. Our results show that polar springtails have lower CTmin and lower CTmax compared to species from temperate and tropical regions, consistent with the Polar pressure hypothesis. We found no phylogenetic signal for CTmax, but low values of phylogenetic signal for CTmin. Globally invasive species do not have significantly broader thermal tolerance breadth (CTrange) than non‐invasive ones, thus not supporting the predictions of the Eurythermality hypothesis. We conclude that polar springtails have evolved their thermal niches in order to adapt to extremely cold environments, which has led to decreasing both upper and lower thermal tolerance limits.

Rapid responses are essential: adaptive temporal variation in cold tolerance of the invasive fall armyworm

Overwintering presents an ecological challenge to insects given highly contrasting environments between native versus invaded environments. The capacity for in situ adaptation through tracking temporal changes in ambient conditions through phenotypic plasticity is thus ecologically important. The fall armyworm is a tropical invasive economic pest of cereals that has become a major biosecurity threat globally. While reports suggest fall armyworm overwinter in tropical environments, little is known on how it survives the environmentally-divergent invaded environments. Here, we tested whether fall armyworm critical low temperature activity limits adaptively tracked prevailing temporal ambient environments. Using field collected populations over 2 years, we show that fall armyworm low temperature responses tracked environmental ambient temperatures. Summer 2020 collected larva had significantly lower cold tolerance (high critical thermal minima [CTmin] and chill coma recovery time [CCRT]) than those from winter seasons. However, winter collected larva had the highest cold tolerance (lower CTmin and CCRT). These results show adaptive fall armyworm responses to ambient temperature environments suggesting that both long-term and short-term responses may shape pest thermal traits and overall ecology.

Effect of brief exposures of anesthesia on thermotolerance and metabolic rate of the spotted-wing fly, Drosophila suzukii: Differences between sexes?

The spotted-wing fly, Drosophila suzukii, is a world-wide pest insect for which there is increasing interest in its physiological traits including metabolism and thermotolerance. Most studies focus only on survival to different time exposures to extreme temperatures, mainly in female flies. In addition, it has not been tested yet how anesthesia affects these measurements. We analyzed the effects of anesthesia by brief exposures to cold, anoxia by CO2 or N2 on three standard thermotolerance assays, as well as the aerobic metabolic rate in both sexes. For heat tolerance we measured CTmax by thermolimit respirometry, and CTmin and chill-coma recovery time for cold tolerance. Aerobic metabolism was calculated by CO2 production of individual flies in real time by open flow respirometry. Results showed that females have a significantly higher V̇CO2 for inactive (at 25 °C) and maximum metabolic rate than males. This difference is mainly explained by body mass and disappears after mass correction. Males had a more sensitive MR to temperature than females showed by a significantly higher Q10 (2.19 vs. 1.98, for males and females, respectively). We observed a significantly lower CTmin (X2 = 4.27, P = 0.03) in females (3.68 ± 0.38 °C) than males (4.56 ± 0.39 °C), although we did not find significant effects of anesthesia. In contrast, anesthesia significantly modifies CTmax for both sexes (F3,62 = 7.86, P < 0.001) with a decrease of the CTmax in cold-anesthetized flies. Finally, we found a significantly higher CTmax in females (37.87 ± 0.07 °C) than males (37.36 ± 0.09 °C). We conclude that cold anesthesia seems to have detrimental effects on heat tolerance, and females have broader thermotolerance range than males, which could help them to establish in invaded temperate regions with more variable environmental temperatures.

Responses in thermal tolerance and daily activity rhythm to urban stress in Drosophila suzukii.

Cities experience changes in abiotic factors, such as warming, increases in noise and light. These changes can lead to phenotypic changes. Several studies have revealed that altered environments change phenotypes in plants and animals in cities. However, limited studies have isolated evolutionary from nongenetic changes. Here, we analyzed the evolution of thermal tolerance and diurnal activity patterns in the urban population of the fruit pest, Drosophila suzukii. Urban and rural isofemale lines were reared under constant conditions. We compared the lower and upper thermal limits (CTmin and CTmax, respectively), and effects of temperature exposure on the thermal limits of urban and rural populations. Common garden experiments showed that urban populations exhibit a lower CTmin than rural populations, suggesting genetic difference in CTmin among populations. On the other hand, the difference in CTmax between urban and rural populations was not significant. Exposure to cold temperature did not affect CTmin in both urban and rural populations. In contrast, exposure to hot temperature increased CTmax especially in urban population, suggesting that urban populations evolved in response to urban heat. We also investigated the daily activity patterns of urban and rural populations and the effect of lifelong artificial light at night on daily activity. We found that night-time light (dim light) reduced the total amount of activity compared to dark night condition. In addition, dim light at night altered the daily rhythm of activity and increased the activity rate at night. The effect of night light on total activity was less in urban than that in rural populations, suggesting that populations in cities evolved to mitigate decreased activity under night light. Our results showed that environmental temperature and artificial light at night evolutionarily and plastically influence ecologically important traits, such as temperature tolerance and diurnal activity.

β-glucan modulates non-specific immune gene expression, thermal tolerance and elicits disease resistance in endangered Tor putitora fry challenged with Aeromonas salmonicida

An eight-week feeding trial was performed to assess the effect of different dietary levels (0, 0.5, 1.0, and 1.5%) of β-glucan (sourced from Saccharomyces cerevisiae) on growth, survival, immunological parameters (immune gene expression, lysozyme, and antiprotease), total antioxidant status, thermal tolerance, and disease resistance of Tor putitora fry. Feeding of moderate doses (0.5 and 1.0%) of β-glucan significantly improved survival but not weight gain percentage as compared to that received unsupplemented control and highest dose (1.5%) of glucan. Supplementation of β-glucan in diets differentially influenced the mRNA expression of cytokine and other immune genes. For instance, transcripts of cytokines such as tnf-α and il-1β were significantly upregulated, while ifn-γ and il-10 were unaffected by β-glucan intake. Also, the relative mRNA expression of tlr-5 and hepcidin1 along with lysozyme and antiprotease activities were remained largely unchanged by dietary glucan administration. In contrast, β-glucan induced mRNA expression of defensin1 and c3 while decreased the transcript level of mhc-1. On the other hand, dietary inclusion of β-glucan markedly improved total antioxidant levels and extended the thermal tolerance limits at both the ends, as shown by increased CTmax and lower CTmin than the control group. After feeding β-glucan for eight weeks, the fish were bath challenged with a bacterial pathogen, Aeromonas salmonicida. The challenge study results revealed that β-glucan intake improved most of the studied immune parameters, resulting in lower mortality. Overall, dietary inclusion of β-glucan (0.5–1.0%) was efficient in improving the immune responses, thermal tolerance, and disease resistance of T. putitora fry.

Divergent metabolomic profiles of cold-exposed mature and immature females of tropical versus temperate Drosophila species

Temperate species, contrary to their tropical counterparts, are exposed not only to thermally variable environments with low temperatures but also to long winters. Different selective pressures may have driven divergent physiological adaptations in closely related species with different biogeographic origins. To survive unfavourable winter conditions, Drosophila species in temperate areas generally undergo a period of reproductive dormancy, associated with a cold-induced cessation of oogenesis and metabolic reorganization. This work aims to compare cold tolerance and metabolic signatures of cold-exposed females exhibiting different reproductive maturity status (mature and immature females) of four Drosophila species from tropical vs. temperate origins. We expected that the capacity for delayed reproduction of immature females could result in the redirection of the energy-related metabolites to be utilized for surviving the cold season. To do so, we studied an array of 45 metabolites using quantitative target GC–MS profiling. Reproductively immature females of temperate species showed the lower CTmin and the faster chill coma recovery time (i.e. the most cold-tolerant group). Principal component analysis captured differences across species, but also between reproductive maturity states. Notably, temperate species exhibited significantly higher levels of glucose, alanine, and gluconolactone than tropical ones. As proline and glycerol showed higher abundances in immature females of temperate species compared to the levels exhibited by the rest of the groups, we reasoned that glucose and alanine could serve as intermediates in the synthesis of these compatible solutes. All in all, our findings suggest that cold-exposed females of temperate species accumulate energy-related and protective metabolites (e.g. glycerol and proline) while delaying reproduction, and that these metabolites are relevant to cold tolerance even at modest concentrations.

Low temperatures impact species distributions of jumping spiders across a desert elevational cline

Temperature is known to influence many aspects of organisms and is frequently linked to geographical species distributions. Despite the importance of a broad understanding of an animal’s thermal biology, few studies incorporate more than one metric of thermal biology. Here we examined an elevational assemblage of Habronattus jumping spiders to measure different aspects of their thermal biology including thermal limits (CTmin, CTmax), thermal preference, V̇CO2 as proxy for metabolic rate, locomotor behavior and warming tolerance. We used these data to test whether thermal biology helped explain how species were distributed across elevation. Habronattus had high CTmax values, which did not differ among species across the elevational gradient. The highest-elevation species had a lower CTmin than any other species. All species had a strong thermal preference around 37 °C. With respect to performance, one of the middle elevation species was significantly less temperature-sensitive in metabolic rate. Differences between species with respect to locomotion (jump distance) were likely driven by differences in mass, with no differences in thermal performance across elevation. We suggest that Habronattus distributions follow Brett’s rule, a rule that predicts more geographical variation in cold tolerance than heat. Additionally, we suggest that physiological tolerances interact with biotic factors, particularly those related to courtship and mate choice to influence species distributions. Habronattus also had very high warming tolerance values (> 20 °C, on average). Taken together, these data suggest that Habronattus are resilient in the face of climate-change related shifts in temperature.

Elevational and microclimatic drivers of thermal tolerance in Andean Pristimantis frogs

AbstractAimWe analysed elevational and microclimatic drivers of thermal tolerance diversity in a tropical mountain frog clade to test three macrophysiological predictions: less spatial variation in upper than lower thermal limits (Bretts’ heat‐invariant hypothesis); narrower thermal tolerance ranges in habitats with less variation in temperature (Janzen's climatic variability hypothesis); and higher level of heat impacts at lower elevations.LocationForest and open habitats through a 4,230‐m elevational gradient across the tropical Andes of Ecuador.MethodWe examined variability in critical thermal limits (CTmax and CTmin) and thermal breadth (TB; CTmax–CTmin) in 21 species of Pristimantis frogs. Additionally, we monitored maximum and minimum temperatures at the local scale (tmax, tmin) and estimated vulnerability to acute thermal stress from heat (CTmax–tmax) and cold (tmin–CTmin), by partitioning thermal diversity into elevational and microclimatic variation.ResultsOur results were consistent with Brett's hypothesis: elevation promotes more variation in CTmin and tmin than in CTmax and tmax. Frogs inhabiting thermally variable open habitats have higher CTmax and tmax and greater TBs than species restricted to forest habitats, which show less climatic overlap across the elevational gradient (Janzen's hypothesis). Vulnerability to heat stress was higher in open than forest habitats and did not vary with elevation.Main conclusionsWe suggest a mechanistic explanation of thermal tolerance diversity in elevational gradients by including microclimatic thermal variation. We propose that the unfeasibility to buffer minimum temperatures locally may explain the rapid increase in cold tolerance (lower CTmin) with elevation. In contrast, the relative invariability in heat tolerance (CTmax) with elevation may revolve around the organisms’ habitat selection of open‐ and canopy‐buffered habitats. Secondly, on the basis of microclimatic estimates, lowland and upland species may be equally vulnerable to temperature increase, which is contrary to the pattern inferred from regional interpolated climate estimators.

Complex body size differences in thermal tolerance among army ant workers (Eciton burchellii parvispinum)

In social insects, group members can differ in thermal physiology, and these differences may affect colony function. Upper thermal tolerance limits (CTmax) generally increase with body size among and within ant species, but size effects on lower thermal tolerances (CTmin) are poorly known. To test whether CTmin co-variation with body size matched patterns for CTmax, we measured CTmax and CTmin in workers of four size-based worker subcastes in the army ant Eciton burchellii parvispinum. CTmax increased with worker body size as expected. CTmin showed a more complex relationship with size: the two intermediate-size subcastes (media and porters) tolerated lower temperatures than the smallest (minims) and the largest (soldiers) worker subcastes. Body-size effects on CTmax were not predictive of body-size effects on CTmin. These patterns held for colonies collected across elevations that spanned approximately 8 °C in mean annual temperature, even though high-elevation colonies had significantly lower CTmin overall. We predict Eciton army ant subcastes will be differentially affected by directional changes in high and low temperature extremes. Worker subcastes perform distinct but complementary roles in colony function, and differential temperature effects among subcastes could impair colony performance and negatively impact colony fitness.

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.

Cold tolerance performance of westslope cutthroat trout (Oncorhynchus clarkii lewisi) and rainbow trout (Oncorhynchus mykiss) and its potential role in influencing interspecific hybridization

Hybridization between rainbow trout (Oncorhynchus mykiss (Walbaum, 1792)) and westslope cutthroat trout (Oncorhynchus clarkii lewisi (Girard, 1856)) occurs commonly when rainbow trout are introduced into the range of westslope cutthroat trout. Typically, hybridization is most common in warmer, lower elevation habitats, but much less common in colder, higher elevation habitats. We assessed the tolerance to cold water temperature (i.e., critical thermal minimum, CTMin) in juvenile rainbow trout and westslope cutthroat trout to test the hypothesis that westslope cutthroat trout better tolerate low water temperature, which may explain the lower prevalence of rainbow trout and interspecific hybrids in higher elevation, cold-water habitats (i.e., the “elevation refuge hypothesis”). All fish had significantly lower CTMin values (i.e., were better able to tolerate low temperatures) when they were acclimated to 15 °C (mean CTMin = 1.37 °C) versus 18 °C (mean CTMin = 1.91 °C; p &lt; 0.001). Westslope cutthroat trout tended to have lower CTMin than rainbow trout from two populations, second–generation (F2) hybrids between two rainbow trout populations, and backcrossed rainbow trout at 15 °C (cross type × acclimation temperature interaction; p = 0.018). Differential adaptation to cold water temperatures may play a role in influencing the spatial distribution of hybridization between sympatric species of trout.

The effects of constant and diel-fluctuating temperature acclimation on the thermal tolerance, swimming capacity, specific dynamic action and growth performance of juvenile Chinese bream

We investigated the effects of constant and diel-fluctuating temperature acclimation on the thermal tolerance, swimming capacity, specific dynamic action (SDA) and growth performance of juvenile Chinese bream (Parabramis pekinensis). The critical thermal maxima (CTmax), critical thermal minima (CTmin), lethal thermal maxima (LTmax), lethal thermal minima (LTmin), critical swimming speed (Ucrit) and fast-start escape response after 30d acclimation to three constant temperatures (15, 20 and 25°C) and one diel-fluctuating temperature (20±5°C) were measured. In addition, feeding rate (FR), feeding efficiency (FE) and specific growth rate (SGR) were measured. The diel-fluctuating temperature group showed lower CTmin than the 20°C group but a similar CTmax, indicating a wider thermal scope. SDA linearly increased with the temperature. Temperature variation between 20 and 25°C had little effect on either swimming or growth performance. However, fish in the 15°C group exhibited much poorer swimming and growth performance than those in the 20°C group. Ucrit decreased slightly under low acclimation temperature due to the pronounced improvement in swimming efficiency under cold temperature. Fish in the diel-fluctuating temperature group fed more but exhibited similar SGR compared to 20°C group, possibly due in part to an increase in energy expenditure to cope with the temperature fluctuation. The narrower thermal scope and lower CTmax of Chinese bream together with the conservation of CTmax with temperature acclimation, suggests that local water temperature elevations may have more profound effects on Chinese bream than on other fish species in the Three Gorges Reservoir.

Within-generation variation of critical thermal limits in adult Mediterranean and Natal fruit flies Ceratitis capitata and Ceratitis rosa: thermal history affects short-term responses to temperature

Insect thermal tolerance shows a range of responses to thermal history depending on the duration and severity of exposure. However, few studies have investigated these effects under relatively modest temperature variation or the interactions between short- and longer-term exposures. In the present study, using a full-factorial design, 1 week-long acclimation responses of critical thermal minimum (CTmin) and critical thermal maximum (CTmax) to temperatures of 20, 25 and 30 °C are investigated, as well as their interactions with short-term (2 h) sub-lethal temperature exposures to these same conditions (20, 25 and 30 °C), in two fruit fly species Ceratitis capitata (Wiedemann) and Ceratitis rosa Karsch from South Africa. Flies generally improve heat tolerance with high temperature acclimation and resist low temperatures better after acclimation to cooler conditions. However, in several cases, significant interaction effects are evident for CTmax and CTmin between short- and long-term temperature treatments. Furthermore, to better comprehend the flies' responses to natural microclimate conditions, the effects of variation in heating and cooling rates on CTmax and CTmin are explored. Slower heating rates result in higher CTmax, whereas slower cooling rates elicit lower CTmin, although more variation is detected in CTmin than in CTmax (approximately 1.2 versus 0.5 °C). Critical thermal limits estimated under conditions that most closely approximate natural diurnal temperature fluctuations (rate: 0.06 °C min−1) indicate a CTmax of approximately 42 °C and a CTmin of approximately 6 °C for these species in the wild, although some variation between these species has been found previously in CTmax. In conclusion, the results suggest critical thermal limits of adult fruit flies are moderated by temperature variation at both short and long time scales and may comprise both reversible and irreversible components.

Critical thermal limits and temperature tolerance in the harvester termite Hodotermes mossambicus (Hagen)

The CTMax of pigmented major and minor workers and unpigmented larvae of Hodotermes mossambicus (Hagen) from laboratory colonies range between 43.5–48.53°C while the CTMin range between 5.3–10.31°C over a range of acclimation temperatures between 15 and 35°C. Major and minor workers have both higher CTMax and lower CTMin than unpigmented large larvae. Temperature tolerance limits are influenced by a number of factors such as the age or maturity of the individual, its size and colour, previous thermal history, the extent of its water reserves as well as environmental conditions.