scholarly journals Oxygen supply limits the heat tolerance of lizard embryos

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.

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 ◽  
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.


Crustaceana ◽  
2021 ◽  
Vol 94 (2) ◽  
pp. 159-175
Author(s):  
Zechariah C. Harris ◽  
Jonathan C. Wright

Abstract Venezillo arizonicus (Mulaik & Mulaik, 1942) is the only oniscidean isopod native to the Southwest Desert Province of North America. In accordance with its desert habitat, we hypothesized that V. arizonicus would have a higher upper lethal temperature than mesic oniscideans. If oniscidean thermal tolerance is limited by an oxygen consumption-uptake mismatch (physiological hypoxia), as indicated by recent work with other land isopods, we further hypothesized that V. arizonicus would possess highly efficient pleopodal lungs, as defined by its capacity for metabolic regulation in reduced . Other adaptations to counter oxygen limitation at high temperatures could include reduced temperature sensitivity of metabolism (low ) and an overall reduction in metabolic rate. Thermal tolerance was measured using the progressive method of Cowles & Bogert and the catabolic rate of animals () was measured as a function of temperature and . The critical thermal maximum (CTmax) of winter-acclimatized animals was 43.0 ± 0.85°C, 1.6-2.6°C higher than published values for summer-acclimatized mesic oniscideans. The catabolic rate at 25°C was 1.50 ± 0.203 μl min−1 g−1, markedly lower than values determined for mesic Oniscidea (4-6 μl min−1 g−1) and was unaffected by hypoxia as low as 2% O2 (ca. 2 kPa). Catabolism was, however, quite sensitive to temperature, showing a mean of 2.58 over 25-42°C. The efficient pleopodal lungs and low metabolic rate of V. arizonicus will both tend to mitigate physiological hypoxia, consistent with the species’ high CTmax. A low catabolic rate may also be an adaptation to low habitat productivity and seasonally constrained activity patterns.


2020 ◽  
Vol 17 (23) ◽  
pp. 6051-6080
Author(s):  
Tim Rixen ◽  
Greg Cowie ◽  
Birgit Gaye ◽  
Joaquim Goes ◽  
Helga do Rosário Gomes ◽  
...  

Abstract. Decreasing concentrations of dissolved oxygen in the ocean are considered one of the main threats to marine ecosystems as they jeopardize the growth of higher organisms. They also alter the marine nitrogen cycle, which is strongly bound to the carbon cycle and climate. While higher organisms in general start to suffer from oxygen concentrations < ∼ 63 µM (hypoxia), the marine nitrogen cycle responds to oxygen concentration below a threshold of about 20 µM (microbial hypoxia), whereas anoxic processes dominate the nitrogen cycle at oxygen concentrations of < ∼ 0.05 µM (functional anoxia). The Arabian Sea and the Bay of Bengal are home to approximately 21 % of the total volume of ocean waters revealing microbial hypoxia. While in the Arabian Sea this oxygen minimum zone (OMZ) is also functionally anoxic, the Bay of Bengal OMZ seems to be on the verge of becoming so. Even though there are a few isolated reports on the occurrence of anoxia prior to 1960, anoxic events have so far not been reported from the open northern Indian Ocean (i.e., other than on shelves) during the last 60 years. Maintenance of functional anoxia in the Arabian Sea OMZ with oxygen concentrations ranging between > 0 and ∼ 0.05 µM is highly extraordinary considering that the monsoon reverses the surface ocean circulation twice a year and turns vast areas of the Arabian Sea from an oligotrophic oceanic desert into one of the most productive regions of the oceans within a few weeks. Thus, the comparably low variability of oxygen concentration in the OMZ implies stable balances between the physical oxygen supply and the biological oxygen consumption, which includes negative feedback mechanisms such as reducing oxygen consumption at decreasing oxygen concentrations (e.g., reduced respiration). Lower biological oxygen consumption is also assumed to be responsible for a less intense OMZ in the Bay of Bengal. According to numerical model results, a decreasing physical oxygen supply via the inflow of water masses from the south intensified the Arabian Sea OMZ during the last 6000 years, whereas a reduced oxygen supply via the inflow of Persian Gulf Water from the north intensifies the OMZ today in response to global warming. The first is supported by data derived from the sedimentary records, and the latter concurs with observations of decreasing oxygen concentrations and a spreading of functional anoxia during the last decades in the Arabian Sea. In the Arabian Sea decreasing oxygen concentrations seem to have initiated a regime shift within the pelagic ecosystem structure, and this trend is also seen in benthic ecosystems. Consequences for biogeochemical cycles are as yet unknown, which, in addition to the poor representation of mesoscale features in global Earth system models, reduces the reliability of estimates of the future OMZ development in the northern Indian Ocean.


2019 ◽  
Vol 374 (1778) ◽  
pp. 20190036 ◽  
Author(s):  
Jennifer Sunday ◽  
Joanne M. Bennett ◽  
Piero Calosi ◽  
Susana Clusella-Trullas ◽  
Sarah Gravel ◽  
...  

Linking variation in species' traits to large-scale environmental gradients can lend insight into the evolutionary processes that have shaped functional diversity and future responses to environmental change. Here, we ask how heat and cold tolerance vary as a function of latitude, elevation and climate extremes, using an extensive global dataset of ectotherm and endotherm thermal tolerance limits, while accounting for methodological variation in acclimation temperature, ramping rate and duration of exposure among studies. We show that previously reported relationships between thermal limits and latitude in ectotherms are robust to variation in methods. Heat tolerance of terrestrial ectotherms declined marginally towards higher latitudes and did not vary with elevation, whereas heat tolerance of freshwater and marine ectotherms declined more steeply with latitude. By contrast, cold tolerance limits declined steeply with latitude in marine, intertidal, freshwater and terrestrial ectotherms, and towards higher elevations on land. In all realms, both upper and lower thermal tolerance limits increased with extreme daily temperature, suggesting that different experienced climate extremes across realms explain the patterns, as predicted under the Climate Extremes Hypothesis . Statistically accounting for methodological variation in acclimation temperature, ramping rate and exposure duration improved model fits, and increased slopes with extreme ambient temperature. Our results suggest that fundamentally different patterns of thermal limits found among the earth's realms may be largely explained by differences in episodic thermal extremes among realms, updating global macrophysiological ‘rules’. This article is part of the theme issue ‘Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen’.


2020 ◽  
Vol 16 (1) ◽  
pp. 20190716 ◽  
Author(s):  
Alex R. Gunderson ◽  
Amélie Fargevieille ◽  
Daniel A. Warner

Extreme heat events are becoming more common as a result of anthropogenic global change. Developmental plasticity in physiological thermal limits could help mitigate the consequences of thermal extremes, but data on the effects of early temperature exposure on thermal limits later in life are rare, especially for vertebrate ectotherms. We conducted an experiment that to our knowledge is the first to isolate the effect of egg (i.e. embryonic) thermal conditions on adult heat tolerance in a reptile. Eggs of the lizard Anolis sagrei were incubated under one of three fluctuating thermal regimes that mimicked natural nest environments and differed in mean and maximum temperatures. After emergence, all hatchlings were raised under common garden conditions until reproductive maturity, at which point heat tolerance was measured. Egg mortality was highest in the warmest treatment, and hatchlings from the warmest treatment tended to have greater mortality than those from the cooler treatments. Despite evidence that incubation temperatures were stressful, we found no evidence that incubation treatment influenced adult heat tolerance. Our results are consistent with a low capacity for organisms to increase their physiological heat tolerance via plasticity, and emphasize the importance of behavioural and evolutionary processes as mechanisms of resilience to extreme heat.


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

2009 ◽  
Vol 64 (11-12) ◽  
pp. 853-858 ◽  
Author(s):  
Wenjun Wang ◽  
Longjiang Yu

The effects of oxygen supply on growth and carotenoids accumulation by Xanthophyllomyces dendrorhous were studied. Initial volumetric oxygen transfer coefficients (KLa) within the range 21.5 - 148.5 h-1 had significant effects on growth and carotenoids accumulation, and an increase of the initial KLa value led to higher carotenoids, astaxanthin and biomass yields by X. dendrorhous. At an initial KLa value of 148.5 h-1, a maximal cell concentration of 19.37 g l-1 and optimal carotenoids and astaxanthin productions of 18.1 and 14.5 mg l-1 were obtained, as well as a maximal astaxanthin content of 0.8 mg g DCW-1, respectively. A higher oxygen supply was advantageous to astaxanthin biosynthesis and the ratio of astaxanthin in the total carotenoids. An increasing initial KLa value gave stronger fluorescence intensities by X. dendrorhous, resulting in the maximal intensity of fluorescence at the KLa value 148.5 h-1. The cell growth of X. dendrorhous was significantly inhibited when dissolved oxygen tension (DOT) was controlled at ~20% air saturation, which was due to the oxygen limitation in broth. The astaxanthin yield and content at ~50% DOT were higher than those at ~20% DOT.


2019 ◽  
Vol 374 (1778) ◽  
pp. 20190035 ◽  
Author(s):  
Félix P. Leiva ◽  
Piero Calosi ◽  
Wilco C. E. P. Verberk

Global warming appears to favour smaller-bodied organisms, but whether larger species are also more vulnerable to thermal extremes, as suggested for past mass-extinction events, is still an open question. Here, we tested whether interspecific differences in thermal tolerance (heat and cold) of ectotherm organisms are linked to differences in their body mass and genome size (as a proxy for cell size). Since the vulnerability of larger, aquatic taxa to warming has been attributed to the oxygen limitation hypothesis, we also assessed how body mass and genome size modulate thermal tolerance in species with contrasting breathing modes, habitats and life stages. A database with the upper (CTmax) and lower (CTmin) critical thermal limits and their methodological aspects was assembled comprising more than 500 species of ectotherms. Our results demonstrate that thermal tolerance in ectotherms is dependent on body mass and genome size and these relationships became especially evident in prolonged experimental trials where energy efficiency gains importance. During long-term trials, CTmax was impaired in larger-bodied water-breathers, consistent with a role for oxygen limitation. Variation in CTmin was mostly explained by the combined effects of body mass and genome size and it was enhanced in larger-celled, air-breathing species during long-term trials, consistent with a role for depolarization of cell membranes. Our results also highlight the importance of accounting for phylogeny and exposure duration. Especially when considering long-term trials, the observed effects on thermal limits are more in line with the warming-induced reduction in body mass observed during long-term rearing experiments. This article is part of the theme issue ‘Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen’.


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