Temperature Sensitivity Of Metabolism Research Articles

Multigenerational exposure to increased temperature reduces metabolic rate but increases boldness in Gambusia affinis.

Acute exposure to warming temperatures increases minimum energetic requirements in ectotherms. However, over and within multiple generations, increased temperatures may cause plastic and evolved changes that modify the temperature sensitivity of energy demand and alter individual behaviors. Here, we aimed to test whether populations recently exposed to geothermally elevated temperatures express an altered temperature sensitivity of metabolism and behavior. We expected that long‐term exposure to warming would moderate metabolic rate, reducing the temperature sensitivity of metabolism, with concomitant reductions in boldness and activity. We compared the temperature sensitivity of metabolic rate (acclimation at 20 vs. 30°C) and allometric slopes of routine, standard, and maximum metabolic rates, in addition to boldness and activity behaviors, across eight recently divergent populations of a widespread fish species (Gambusia affinis). Our data reveal that warm‐source populations express a reduced temperature sensitivity of metabolism, with relatively high metabolic rates at cool acclimation temperatures and relatively low metabolic rates at warm acclimation temperatures compared to ambient‐source populations. Allometric scaling of metabolism did not differ with thermal history. Across individuals from all populations combined, higher metabolic rates were associated with higher activity rates at 20°C and bolder behavior at 30°C. However, warm‐source populations displayed relatively bolder behavior at both acclimation temperatures compared to ambient‐source populations, despite their relatively low metabolic rates at warm acclimation temperatures. Overall, our data suggest that in response to warming, multigenerational exposure (e.g., plasticity, adaptation) may not result in trait change directed along a simple “pace‐of‐life syndrome” axis, instead causing relative decreases in metabolism and increases in boldness. Ultimately, our data suggest that multigenerational warming may produce a novel combination of physiological and behavioral traits, with consequences for animal performance in a warming world.

Conceptualizing Biogeochemical Reactions With an Ohm's Law Analogy

AbstractIn studying problems like plant‐soil‐microbe interactions in environmental biogeochemistry and ecology, one usually has to quantify and model how substrates control the growth of, and interaction among, biological organisms (and abiotic factors, e.g., adsorptive mineral soil surfaces). To address these substrate‐consumer relationships, many substrate kinetics and growth rules have been developed, including the famous Monod kinetics for single‐substrate‐based growth and Liebig's law of the minimum for multiple‐nutrient‐colimited growth. However, the mechanistic basis that leads to these various concepts and mathematical formulations and the implications of their parameters are often quite uncertain. Here, we show that an analogy based on Ohm's law in electric circuit theory is able to unify many of these different concepts and mathematical formulations. In this Ohm's law analogy, a resistor is defined by a combination of consumers’ and substrates’ kinetic traits. In particular, the resistance is equal to the mean first passage time that has been used to derive the Michaelis‐Menten kinetics under substrate replete conditions for a single substrate as well as the predation rate of individual organisms. We further show that this analogy leads to important insights on various biogeochemical problems, such as (a) multiple‐nutrient‐colimited biological growth, (b) denitrification, (c) fermentation under aerobic conditions, (d) metabolic temperature sensitivity, and (e) the legitimacy of Monod kinetics for describing bacterial growth. We expect that our approach will help both modelers and nonmodelers to better understand and formulate hypotheses when studying certain aspects of environmental biogeochemistry and ecology.

The physiology of Venezillo arizonicus (Isopoda, Armadillidae): metabolism and thermal tolerance

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.

Metabolic physiology of the freshwater planaria Girardia dorotocephela and Schmidtea mediterranea: reproductive mode, specific dynamic action, and temperature.

Planarians are widely used animal models for studies in regeneration, developmental biology, neurobiology, and behavior. However, surprisingly little is known about other aspects of their basic biology, even though such information might help validate these flatworms as a general animal model. We hypothesized that planaria, although dependent on simple diffusion of O2 across the integument for O2 uptake, would nonetheless show changes in oxygen consumption (V̇o2) associated with reproductive mode (sexual or asexual), feeding (specific dynamic action; SDA), temperature (Q10 values), and photoperiod typical of those responses of more complex invertebrates. In the current experiments, routine V̇o2 was measured over the range of 13-28°C in Schmidtea mediterranea and Girardia dorotocephala. At the long-term maintenance temperature of 18°C, routine V̇o2 was ~13 µL O2·g-1·h-1 in the two asexual strains, but approximately twice as high (27 µL O2·g-1·h-1) in the sexual strain of S. mediterranea, suggesting a metabolic cost for sexual reproduction. Metabolic temperature sensitivity, measured by Q10, was about one to three for all three groups. All three groups showed a large (~2- to 3-fold) increase in V̇o2 within a day following feeding, suggesting a large SDA effect. Starvation, causing "degrowth" in some planaria, resulted in a loss of one-third of body mass in sexual S. mediterranea but no body mass loss in either asexual strains. Collectively, these data indicate that, while being a relatively simple flatworm with no dedicated respiratory or circulatory system, their metabolic physiological responses are quite similar to those shown by more complex invertebrates and vertebrates, contributing to their validation as an animal model.

High Heat Tolerance Is Negatively Correlated with Heat Tolerance Plasticity in Nudibranch Mollusks.

Rapid ocean warming may alter habitat suitability and population fitness for marine ectotherms. Susceptibility to thermal perturbations will depend in part on plasticity of a species' upper thermal limits of performance (CTmax). However, we currently lack data regarding CTmax plasticity for several major marine taxa, including nudibranch mollusks, thus limiting predictive responses to habitat warming for these species. In order to determine relative sensitivity to future warming, we investigated heat tolerance limits (CTmax), heat tolerance plasticity (acclimation response ratio), thermal safety margins, temperature sensitivity of metabolism, and metabolic cost of heat shock in nine species of nudibranchs collected across a thermal gradient along the northeastern Pacific coast of California and held at ambient and elevated temperature for thermal acclimation. Heat tolerance differed significantly among species, ranging from to ( ), but did not vary with collection site within species. Thermal plasticity was generally high ( , ) and was strongly negatively correlated with CTmax in accordance with the trade-off hypothesis of thermal adaptation. Metabolic costs of thermal challenge were low, with no significant alteration in respiration rate of any species 1 h after exposure to acute heat shock. Thermal safety margins, calculated against maximum habitat temperatures, were negative for nearly all species examined ( , [confidence interval]). From these data, we conclude that warm adaptation in intertidal nudibranchs constrains plastic responses to acute thermal challenge and that southern warm-adapted species are likely most vulnerable to future warming.

The Sensitivity of Subsurface Microbes to Ocean Warming Accentuates Future Declines in Particulate Carbon Export

Under future warming Earth System Models (ESMs) project a decrease in the magnitude of downward particulate organic carbon (POC) export, suggesting the potential for carbon storage in the deep ocean will be reduced. Projections of POC export can also be quantified using an alternative physiologically-based approach, the Metabolic Theory of Ecology (MTE). MTE employs an activation energy (Ea) describing organismal metabolic sensitivity to temperature change, but does not consider changes in ocean chemistry or physics. Many ESMs incorporate temperature dependent functions, where rates (e.g. respiration) scale with temperature. Temperature sensitivity describes how temperature dependence varies across metabolic rates or species. ESMs acknowledge temperature sensitivity between rates (e.g. between heterotrophic and autotropic processes), but due to a lack of empirical data cannot parameterise for variation within rates, such as differences within species or biogeochemical provinces. Here we investigate how varying temperature sensitivity affects heterotrophic microbial respiration and hence future POC export. Using satellite-derived data and ESM temperature projections we applied microbial MTE, with varying temperature sensitivity, to estimates of global POC export. In line with observations from polar regions and the deep ocean we imposed an elevated temperature sensitivity (Ea = 1.0 eV) to cooler regions; firstly to the Southern Ocean (south of 40 S) and secondly where temperature at 100 m depth < 13 C. Elsewhere in both these scenarios Ea was set to 0.7 eV (moderate sensitivity/classic MTE). Imposing high temperature sensitivity in cool regions resulted in projected declines in export of 17  1 % (< 40 S) and 23  1 % (< 13 C) by 2100 relative to the present day. Hence varying microbial temperature sensitivity resulted in at least twofold greater declines in POC export than suggested by classic MTE derived in this study (12  1 %, Ea = 0.7 eV globally) or ESMs (1-12 %). The sparse observational data currently available suggests metabolic temperature sensitivity of organisms likely differs depending on the oceanic province they reside in. We advocate temperature sensitivity to be incorporated in biogeochemical models to improve projections of future carbon export, which could be currently underestimating future POC export.

Continental-scale decrease in net primary productivity in streams due to climate warming

An increase in stream temperature leads to a convergence of metabolic balance, overall decline in net ecosystem productivity, and higher CO2 emissions from streams, according to analyses of temperature sensitivity of stream metabolism across six biomes. Streams play a key role in the global carbon cycle. The balance between carbon intake through photosynthesis and carbon release via respiration influences carbon emissions from streams and depends on temperature. However, the lack of a comprehensive analysis of the temperature sensitivity of the metabolic balance in inland waters across latitudes and local climate conditions hinders an accurate projection of carbon emissions in a warmer future. Here, we use a model of diel dissolved oxygen dynamics, combined with high-frequency measurements of dissolved oxygen, light and temperature, to estimate the temperature sensitivities of gross primary production and ecosystem respiration in streams across six biomes, from the tropics to the arctic tundra. We find that the change in metabolic balance, that is, the ratio of gross primary production to ecosystem respiration, is a function of stream temperature and current metabolic balance. Applying this relationship to the global compilation of stream metabolism data, we find that a 1 °C increase in stream temperature leads to a convergence of metabolic balance and to a 23.6% overall decline in net ecosystem productivity across the streams studied. We suggest that if the relationship holds for similarly sized streams around the globe, the warming-induced shifts in metabolic balance will result in an increase of 0.0194 Pg carbon emitted from such streams every year.

Interspecific Differences in Metabolic Rate and Metabolic Temperature Sensitivity Create Distinct Thermal Ecological Niches in Lizards (Plestiodon).

Three congeneric lizards from the southeastern United States (Plestiodon fasciatus, P. inexpectatus, and P. laticeps) exhibit a unique nested distribution. All three skink species inhabit the US Southeast, but two extend northward to central Ohio (P. fasciatus and P. laticeps) and P. fasciatus extends well into Canada. Distinct interspecific differences in microhabitat selection and behavior are associated with the cooler temperatures of the more Northern ranges. We hypothesized that interspecific differences in metabolic temperature sensitivity locally segregates them across their total range. Resting oxygen consumption was measured at 20°, 25° and 30°C. Plestiodon fasciatus, from the coolest habitats, exhibited greatly elevated oxygen consumption compared to the other species at high ecologically-relevant temperatures (0.10, 0.17 and 0.83 ml O2. g-1. h-1 at 20°, 25° and 30°C, respectively). Yet, P. inexpectatus, from the warmest habitats, exhibited sharply decreased oxygen consumption compared to the other species at lower ecologically-relevant temperatures (0.09, 0.27 and 0.42 ml O2. g-1. h-1 at 20°, 25° and 30°C, respectively). Plestiodon laticeps, from both open and closed microhabitats and intermediate latitudinal range, exhibited oxygen consumptions significantly lower than the other two species (0.057, 0.104 and 0.172 ml O2. g-1. h-1 at 20°, 25° and 30°C, respectively). Overall, Plestiodon showed metabolic temperature sensitivities (Q10s) in the range of 2–3 over the middle of each species’ normal temperature range. However, especially P. fasciatus and P. inexpectatus showed highly elevated Q10s (9 to 25) at the extreme ends of their temperature range. While morphologically similar, these skinks are metabolically distinct across the genus’ habitat, likely having contributed to their current distribution.

Responses of the arcto-boreal krill species Thysanoessa inermis to variations in water temperature: coupling Hsp70 isoform expressions with metabolism.

Recent studies have indicated a metabolic temperature sensitivity in both the arcto-boreal krill species Thysanoessa inermis and Thysanoessa raschii that may determine these species' abundance and population persistence at lower latitudes (up to 40° N). T. inermis currently dominates the krill community in the Barents Sea and in the high Arctic Kongsfjord. We aimed to increase the knowledge on the upper thermal limit found in the latter species by estimating the CT50 value (19.7°C) (critical temperature at which 50% of animals are reactive) and by linking metabolic rate measurements with molecular approaches. Optical oxygen sensors were used to measure respiration rates in steps of 2°C (from 0 to 16°C). To follow the temperature-mediated mechanisms of passive response, i.e., as a proxy for molecular stress, molecular chaperone heat shock protein 70 (Hsp70) sequences were extracted from a transcriptome assembly, and the gene expression kinetics were monitored during an acute temperature exposure to 6 or 10°C with subsequent recovery at 4°C. Our results showed upregulation of hsp70 genes, especially the structurally constitutive and mitochondrial isoforms. These findings confirmed the temperature sensitivity of T. inermis and showed that the thermal stress took place before reaching the upper temperature limit estimated by respirometry at 12°C. This study provides a baseline for further investigations into the thermal tolerances of arcto-boreal Thysanoessa spp. and comparisons with other krill species under different climatic regimes, especially Antarctica.

Acclimation to temperature and temperature sensitivity of metabolism by ectomycorrhizal fungi

This was published in GCB (2008/14:1169–1180). The corrections as follow do not change the main results in any way, do not affect calculations of Q10, and have no bearings on the statistical analysis of the data. (1) Fig. 2 & Fig. 3: The y-axes should read Respiration (pmol s−1 mg−1). (2) On page 1177, in the first full paragraph in column 2, respiration rates cited from Taber & Taber 1987, Souto et al. 2000, and Rygiewicz & Andersen 1994 should be 10–16 pmol CO2 s−1 mg−1, 50–70 pmol CO2 s−1 mg−1, and 11–16 pmol CO2 s−1 mg−1, respectively. These changes affect nothing in the following field respiration calculation other than the final number, which is 24 μmol CO2 s−1 mg−1 but should be 24 pmol CO2 s−1 mg−1. We apologize for the above mentioned errors.

Acclimation to temperature and temperature sensitivity of metabolism by ectomycorrhizal fungi

AbstractEctomycorrhizal (ECM) fungi contribute significantly to ecosystem respiration, but little research has addressed the effect of temperature on ECM fungal respiration. Some plants have the ability to acclimate to temperature such that long‐term exposure to warmer conditions slows respiration at a given measurement temperature and long‐term exposure to cooler conditions increases respiration at a given measurement temperature. We examined acclimation to temperature and temperature sensitivity (Q10) of respiration by ECM fungi by incubating them for a week at one of three temperatures and measuring respiration over a range of temperatures. Among the 12 ECM fungal isolates that were tested, Suillus intermedius, Cenococcum geophilum, and Lactarius cf. pubescens exhibited significant acclimation to temperature, exhibiting an average reduction in respiration of 20–45% when incubated at 23 °C compared with when incubated at 11 or 17 °C. The isolates differed significantly in their Q10 values, which ranged from 1.67 to 2.56. We also found that half of the isolates significantly increased Q10 with an increase in incubator temperature by an average of 15%. We conclude that substantial variation exists among ECM fungal isolates in their ability to acclimate to temperature and in their sensitivity to temperature. As soil temperatures increase, ECM fungi that acclimate may require less carbon from their host plants than fungi that do not acclimate. The ability of some ECM fungi to acclimate may partially ameliorate the anticipated positive feedback between soil respiration and temperature.

Effect of Temperature on Oxygen Consumption of the Leopard Shark, Triakis Semifasciata

The leopard shark, Triakis semifasciata, regularly resides in California's Tomales Bay, which is characterized by thermally different regions ranging from 10°C to 26°C during the summer. Past studies have shown that leopard sharks feed on benthic invertebrate prey similar to that of the sympatric bat ray, Myliobatis californica. Fishes' metabolic (oxygen consumption) rates typically increase with temperature increases, and we measured leopard sharks' metabolic responses and sensitivity to ambient temperature, using flow-through respirometry. Leopard shark oxygen consumption rate increased with increasing temperature, over a range of 12–24°C, with a typical temperature sensitivity (Q10 = 2.51). Whereas bat rays use a highly temperature-sensitive metabolism to efficiently feed (in warmer waters) and digest (in cooler waters) during different phases of the diel cycle, leopard sharks possess a more typical metabolic temperature sensitivity that allows for high-tide foraging, throughout the diel cycle.

The Influence of Habitat and Altitude on Oxygen Uptake in Sub-Antarctic Weevils

Whole-organism oxygen uptake rate and its temperature sensitivity (determined using regression analyses and estimates of Q10) were examined in six closely related weevil species (Palirhoeus eatoni, Bothrometopus randi, Bothrometopus elongatus, Bothrometopus parvulus, Ectemnorhinus similis, and Ectemnorhinus marioni) from sub-Antarctic Marion Island over a short time period and using the same methods. Bothrometopus elongatus, B. parvulus, and the two Ectemnorhinus species have populations at both high and low elevations, and pairwise comparisons of these species were made. Regressions of the log of oxygen uptake rate on temperature and Q10 values revealed that the Ectemnorhinus species have a significantly greater thermal sensitivity than do species in the genera Bothrometopus and Palirhoeus. This may be considered an adaptation of the former to their moist lowland habitats and the requirements of angiosperm-feeding in E. similis. It is argued that elevated oxygen uptake rates and reduced slopes of the regression of the log of oxygen uptake rate on temperature in species and populations from high altitudes compared with those from low elevations provide evidence for metabolic cold adaptation. In addition, it seems likely that elevated oxygen uptake rates and their reduced thermal sensitivity within the genera Bothrometopus and Palirhoeus are an adaptation to the cold Neogene environments they evolved in. However, because data on the more basal taxa in the Ectemnorhinus group of weevils are not available, this temperature compensation could not be attributed conclusively to adaptation. Q10's of the lowland populations of all the species were negatively correlated with body water content, and it is suggested that the low temperature sensitivity of metabolism in P. eatoni and the Bothrometopus species may also be due to constraints imposed on them by their dry habitats.

Activity and thermoregulation of the snake Natrix maura. 2. A synoptic model of thermal biolgy and the physiological ecology of performance

Biophysical, physiological and behavioral approaches to reptilian thermal biology have been combined in a synoptic model, using data derived from a study of the snake Natrix maura in a Spanish river and in the laboratory. The model investigates the relations between the costs and benefits of physiological performance, body temperature, the season of activity, and the thermal benefits of physiological performance, body temperature, the season of activity, and the thermal environment. The performance variale chosen was aerobic metabolism. The cost associated with high aerobic metabolism at low body temperatures is the energy requirement for maintenance; the benefit is an increased activity season.The cost of maintenance was more sensitive to differences in the level and temperature sensitivity of metabolism than was the benefit of the time for activity. The pattern of performance and body temperature obesrved in N. maura was close to that predicted for maximum efficiency, in terms of the activity season produced per unit of annual maintenance cost. It is noted, however, that animals will be selected for net benefit, and not for efficiency as such.A definition of fitness for the study of the physiological ecology of performance was developed, to take account of the level of performance available during activity, and of selection for net benefit. This definition is: the energy intake above maintenance costs x the probability of survival. It is related to general ecological fitness by considering lifetime strategies of survival and reproduction, and the energy equivalence of offspring. These strategies are the subject of the physiological ecology of allocation, which is thus complementary to that of performance.The following are also discussed: the role of performance in interactions with predators and prey; other possible evolutionary determinants of body temperature; the limitations of different approachs to thermal biology; suitable systems for further study.

Energetics of development of the alpine charr,salvelinus alpinus, in relation to temperature and oxygen

1. Eggs ofSalvelinus alpinus were maintained from the eyed stage to several weeks after hatching at two temperatures (4 and 8 °C) and three levels of oxygen concentration (20% of air saturation at 4 °C, 30% at 8 °C, 50% and 100%). Mortality was low under all conditions except after hatching at 8 °C and 30% air saturation. 2. Weight-specific oxygen consumption increased in the growing embryos under all conditions. The total amount of oxygen consumed by the embryos up to peak hatching time is directly dependent on the oxygen concentration of the medium but is nearly independent of temperature. 3. The average weight at which an embryo hatches depends directly onPO2, but is only little influenced by temperature. This is at variance with observations on other salmonids. 4. The ‘factorial aerobic scope for activity’ after hatching is highest (\(\bar x\) up to 5.2) at 8 °C and 50–100% air saturation, and lowest (1.6) at 4 °C and 20% air saturation. 5. The large effect of temperature between 4 and 8°C on the rate of metabolism of the hatched larvae may be explained by the stimulating effect of the higher temperature on swimming activity. Oxygen concentration in the medium has no apparent effect on the temperature sensitivity of metabolism. 6. If compared with the respiratory rate of adultS. alpinus as measured by Holeton (1973) the respiratory rates of the embryos remained below the size corrected basal rate of fish living at 2–6 °C. There is no indication of ‘cold acclimation’ of the metabolism ofS. alpinus. 7. The slopes of the functional relationship between rate of oxygen consumption andPO2 are not influenced by temperature. 8. Production efficiency of the embryo is only slightly affected byPO2 and temperature. On the other hand, the production efficiencies of the swimming larvae at the yolk sac stage are higher at 4 than at 8 °C and show an unexpected maximum at 50% oxygen concentration, particularly at the higher temperature. 9. A hypothesis is presented which relates the experimental findings to the ecology and behaviour ofS. alpinus, suggesting various adaptive responses of the species to low oxygen concentration and temperature increase in the medium.