scholarly journals Oxygen supply limits the heat tolerance of locusts during the first instar only

2020 ◽  
Author(s):  
Jacob P. Youngblood ◽  
John M. VandenBrooks ◽  
Oluwatosin Babarinde ◽  
Megan E. Donnay ◽  
Deanna B. Elliott ◽  
...  

AbstractExtreme heat directly limits an organism’s survival and reproduction, but scientists cannot agree on what causes organisms to lose function or die during heating. According to the theory of oxygen- and capacity-limitation of thermal tolerance, heat stress occurs when a warming organism’s demand for oxygen exceeds its supply, triggering a widespread drop in ATP concentration. This model predicts that an organism’s heat tolerance should decrease under hypoxia, yet most terrestrial organisms tolerate the same amount of warming across a wide range of oxygen concentrations. This point is especially true for adult insects, who deliver oxygen through highly efficient respiratory systems. However, oxygen limitation at high temperatures may be more common during immature life stages, which have less developed respiratory systems. To test this hypothesis, we measured the effects of heat and hypoxia on the survival of locusts (Schistocerca cancellata) throughout development. We demonstrate that the heat tolerance of locusts depends on oxygen supply during the first instar but not during later instars. This finding provides further support for the idea that oxygen limitation of thermal tolerance depends on respiratory performance, especially during immature life stages.

2019 ◽  
Vol 15 (11) ◽  
pp. 20190566 ◽  
Author(s):  
Jon C. Vimmerstedt ◽  
Dylan J. Padilla Pérez ◽  
Michael J. Angilletta ◽  
John M. VandenBrooks

Physiologists have primarily focused on two potential explanations for heat stress in animals—the classic model of molecular stability and an alternative model of oxygen limitation. Although the classic model has widespread support, the oxygen-supply model applies to many aquatic animals and some terrestrial ones. In particular, the embryonic stage of terrestrial animals seems most susceptible to oxygen limitation because embryos acquire oxygen from the atmosphere by diffusion rather than ventilation. We report experiments confirming the two conditions of the oxygen-supply model in Japanese quail embryos, Coturnix coturnix . Hypoxia (12% O 2 ) greatly reduced the chance of survival at 47.5°C, and hyperoxia greatly improved the chance of survival at 48.5°C. This finding expands the scope of the oxygen-supply model to a terrestrial, endothermic species, suggesting that oxygen supply generally limits the heat tolerance of embryos.


2020 ◽  
Vol 127 ◽  
pp. 104157
Author(s):  
Jacob P. Youngblood ◽  
John M. VandenBrooks ◽  
Oluwatosin Babarinde ◽  
Megan E. Donnay ◽  
Deanna B. Elliott ◽  
...  

2015 ◽  
Vol 11 (4) ◽  
pp. 20150113 ◽  
Author(s):  
Colton Smith ◽  
Rory S. Telemeco ◽  
Michael J. Angilletta ◽  
John M. VandenBrooks

The mechanisms that set the thermal limits to life remain uncertain. Classically, researchers thought that heating kills by disrupting the structures of proteins or membranes, but an alternative hypothesis focuses on the demand for oxygen relative to its supply. We evaluated this alternative hypothesis by comparing the lethal temperature for lizard embryos developing at oxygen concentrations of 10–30%. Embryos exposed to normoxia and hyperoxia survived to higher temperatures than those exposed to hypoxia, suggesting that oxygen limitation sets the thermal maximum. As all animals pass through an embryonic stage where respiratory and cardiovascular systems must develop, oxygen limitation may limit the thermal niches of terrestrial animals as well as aquatic ones.


2021 ◽  
Vol 12 ◽  
Author(s):  
Angélica Jaramillo ◽  
Luis E. Castañeda

The gut microbiota can contribute to host physiology leading to an increase of resistance to abiotic stress conditions. For instance, temperature has profound effects on ectotherms, and the role of the gut microbiota on the thermal tolerance of ectotherms is a matter of recent research. However, most of these studies have been focused on single static temperatures instead of evaluating thermal tolerance in a wide range of stressful temperatures. Additionally, there is evidence supporting that the gut microbiota is sensitive to environmental temperature, which induces changes in its composition and diversity. These studies have evaluated the effects of thermal acclimation (>2 weeks) on the gut microbiota, but we know little about the impact of transient thermal stress on the composition and diversity of the gut microbiota. Thus, we investigated the role of the gut microbiota on the heat tolerance of Drosophila subobscura by measuring the heat tolerance of conventional and axenic flies exposed to different heat stressful temperatures (35, 36, 37, and 38°C) and estimating the heat tolerance landscape for both microbiota treatments. Conventional flies exposed to mild heat conditions exhibited higher thermal tolerance than axenic flies, whereas at higher stressful temperatures there were no differences between axenic and conventional flies. We also assessed the impact of transient heat stress on the taxonomical abundance, diversity, and community structure of the gut microbiota, comparing non-stressed flies (exposed to 21°C) and heat-stressed flies (exposed to 34°C) from both sexes. Bacterial diversity indices, bacterial abundances, and community structure changed between non-stressed and heat-stressed flies, and this response was sex-dependent. In general, our findings provide evidence that the gut microbiota influences heat tolerance and that heat stress modifies the gut microbiota at the taxonomical and structural levels. These results demonstrate that the gut microbiota contributes to heat tolerance and is also highly sensitive to transient heat stress, which could have important consequences on host fitness, population risk extinction, and the vulnerability of ectotherms to current and future climatic conditions.


2017 ◽  
Author(s):  
Brent L. Lockwood ◽  
Tarun Gupta ◽  
Rosemary Scavotto

AbstractMany terrestrial ectothermic species exhibit limited variation in upper thermal tolerance across latitude. However, these trends may not signify limited adaptive capacity to increase thermal tolerance in the face of climate change. Instead, thermal tolerance may be similar among populations because behavioral thermoregulation by mobile organisms or life stages may buffer natural selection for thermal tolerance. We compared thermal tolerance of adults and embryos among natural populations of Drosophila melanogaster from a broad range of thermal habitats around the globe to assess natural variation of thermal tolerance in mobile vs. immobile life stages. We found no variation among populations in adult thermal tolerance, but embryonic thermal tolerance was higher in tropical strains than in temperate strains. Average maximum temperature of the warmest month of the year predicted embryonic thermal tolerance in tropical but not temperate sites. We further report that embryos live closer to their upper thermal limits than adultso—i.e., thermal safety margins are smaller for embryos than adults. F1 hybrid embryos from crosses between temperate and tropical populations had thermal tolerance that matched that of tropical embryos, suggesting dominance of heat-tolerant alleles. Together our findings suggest that thermal selection has led to divergence in embryonic thermal tolerance but that selection for divergent thermal tolerance may be limited in adults. Further, our results suggest that thermal traits should be measured across life stages in order to better predict adaptive limits.Impact SummaryClimate change may threaten the extinction of many ectothermic species, unless populations can evolutionarily adapt to rising temperatures. Natural selection should favor individuals with higher heat tolerances in hotter environments. But recent studies have found that individuals from hot and cold places often have similar heat tolerances. This pattern may indicate that the evolution of heat tolerance is constrained. If this were true, then it would have dire consequences for species persistence under novel thermal conditions.An alternative explanation for lack of variation in heat tolerance is that mobile organisms don’t need higher heat tolerances to survive in hotter places. The majority of studies have focused on heat tolerance of the adult life stage. Yet, adults in many species are mobile organisms that can avoid extreme heat by seeking shelter in cooler microhabitats (e.g., shaded locations). In contrast, immobile life stages (e.g., insect eggs) cannot behaviorally avoid extreme heat. Thus, mobile and immobile life stages may face different thermal selection pressures that lead to disparate patterns of thermal adaptation across life stages.Here, we compared heat tolerances of fruit fly adults and eggs (Drosophila melanogaster) from populations in temperate North America and tropical locations around the globe. Consistent with previous studies, we found no differences among populations in adult heat tolerance. However, eggs from tropical flies were consistently more heat tolerant than eggs from North American flies. Further, eggs had lower heat tolerance than adults. Consequently, fly eggs in the hotter tropics may experience heat death more frequently than adult flies later in life. This may explain why patterns of divergence in heat tolerance were decoupled across life stages. These patterns indicate that thermal adaptation may be life-stage-specific and suggest that future work should characterize thermal traits across life stages to better understand the evolution of thermal limits.


2021 ◽  
Vol 8 (3) ◽  
Author(s):  
Kris Sales ◽  
Ramakrishnan Vasudeva ◽  
Matthew J. G. Gage

With climate change creating a more volatile atmosphere, heatwaves that create thermal stress for living systems will become stronger and more frequent. Using the flour beetle Tribolium castaneum , we measure the impacts of thermal stress from experimental heatwaves in the laboratory on reproduction and survival across different insect life stages, and the extent and pace of any recovery. We exposed larvae, pupae, juvenile and mature adult male beetles to 5-day periods of heat stress where temperatures were maintained at either 40°C or 42°C, a few degrees above the 35°C optimum for this species' population productivity, and then measured survival and reproduction compared with controls at 30°C. Mortality due to thermal stress was greatest among juvenile life stages. Male reproductive function was specifically damaged by high temperatures, especially if experienced through pupal or immature life stages when complete sterility was shown at reproductive maturity; larval exposure did not damage adult male fertility. High temperatures impaired testis development and the production of viable sperm, with damage being strongest when experienced during pupal or juvenile adult stages. Despite this disruption, males recovered from heat stress and, depending on the stage of exposure, testis size, sperm production and fertility returned to normal 15–28 days after exposure. Our experiments reveal how thermal stress from heatwave conditions could impact on insect survival and reproduction across different life stages, and the potential and timescales of recovery.


Author(s):  
Quentin Willot ◽  
Ben Loos ◽  
John S. Terblanche

Developmental and adult thermal acclimation can have distinct, even opposite, effects on adult heat resistance in ectotherms. Yet, their relative contribution to heat-hardiness of ectotherms remains unclear despite the broad ecological implications thereof. Furthermore, the deterministic relationship between heat-knockdown and recovery from heat stress is poorly understood but significant for establishing causal links between climate variability and population dynamics. Here, using D. melanogaster in a full-factorial experimental design, we assess flies heat-tolerance in static stress assays, and document how developmental and adult acclimation interact with a distinct pattern to promote survival to heat-stress in adults. We show that warmer adult acclimation is the initial factor enhancing survival to constant stressful high temperatures in flies, but also that the interaction between adult and developmental acclimation becomes gradually more important to ensure survival as the stress persists. This provides an important framework revealing the dynamic interplay between these two forms of acclimation, that ultimately enhance thermal tolerance as a function of stress duration. Furthermore, by investigating recovery rates post-stress, we also show that the process of heat-hardening and recovery post heat knockdown are likely to be based on set of (at least partially) divergent mechanisms. This could bear ecological significance as a tradeoff may exist between increasing thermal tolerance and maximizing recovery rates post-stress, constraining population responses when exposed to variable and stressful climatic conditions.


2017 ◽  
Vol 13 (11) ◽  
pp. 20170309 ◽  
Author(s):  
Collin Teague ◽  
Jacob P. Youngblood ◽  
Kinley Ragan ◽  
Michael J. Angilletta ◽  
John M. VandenBrooks

We used quantitative genetics to test a controversial theory of heat stress, in which animals overheat when the demand for oxygen exceeds the supply. This theory, referred to as oxygen- and capacity-limited thermal tolerance, predicts a positive genetic correlation between hypoxia tolerance and heat tolerance. We demonstrate the first genetic correlation of this kind in a model organism, Drosophila melanogaster . Genotypes more likely to fly under hypoxic stress (12% O 2 ) were also more likely to fly under heat stress (39°C). This finding prompts new questions about mechanisms and limits of adaptation to heat stress.


2016 ◽  
Vol 311 (2) ◽  
pp. R440-R449 ◽  
Author(s):  
Andreas Ekström ◽  
Jeroen Brijs ◽  
Timothy D. Clark ◽  
Albin Gräns ◽  
Fredrik Jutfelt ◽  
...  

Oxygen supply to the heart has been hypothesized to limit cardiac performance and whole animal acute thermal tolerance (CTmax) in fish. We tested these hypotheses by continuously measuring venous oxygen tension (Pvo2) and cardiovascular variables in vivo during acute warming in European perch ( Perca fluviatilis) from a reference area during summer (18°C) and a chronically heated area (Biotest enclosure) that receives warm effluent water from a nuclear power plant and is normally 5–10°C above ambient (24°C at the time of experiments). While CTmax was 2.2°C higher in Biotest compared with reference perch, the peaks in cardiac output and heart rate prior to CTmax occurred at statistically similar Pvo2 values (2.3–4.0 kPa), suggesting that cardiac failure occurred at a common critical Pvo2 threshold. Environmental hyperoxia (200% air saturation) increased Pvo2 across temperatures in reference fish, but heart rate still declined at a similar temperature. CTmax of reference fish increased slightly (by 0.9°C) in hyperoxia, but remained significantly lower than in Biotest fish despite an improved cardiac output due to an elevated stroke volume. Thus, while cardiac oxygen supply appears critical to elevate stroke volume at high temperatures, oxygen limitation may not explain the bradycardia and arrhythmia that occur prior to CTmax. Acute thermal tolerance and its thermal plasticity can, therefore, only be partially attributed to cardiac failure from myocardial oxygen limitations, and likely involves limiting factors on multiple organizational levels.


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