A re-interpretation of the effect of temperature on the metabolism of certain marine invertebrates

Measurements by nieans of an oxygen electrode of the rate of oxygen consumption of a wide variety of common intertidal invertebrates show that at least two rates of uptake can be distinguished in the intact animal. First, there is a rapid rate of oxygen uptake corresponding with activity and second there is a slower rate which corresponds with periods of quiescence and which alternates with the fast rate. Intermediate rates correspond with intermediate rates of overt activity. The maximal and minimal rates of oxygen uptake are affected differently by temperature change. The fast rate corresponding to activity ("active metabolism") increases with temperature in approximate agreement with Arrhenius's law. The slow rate corresponding to quiescence ("maintenance metabolism") does not vary with temperature over much of the range 7 to 22.5°C. It is concluded that, contrary to common belief, the intertidal invertebrates studied have a "basal metabolic rate" with a Q₁₀ of approximately one over much of the normal environmental temperature range and in this respect are well suited to life in a habitat where rapid fluctuations in temperature occur.     

A re-interpretation of the effect of temperature on the metabolism of certain marine invertebrates

Measurements by nieans of an oxygen electrode of the rate of oxygen consumption of a wide variety of common intertidal invertebrates show that at least two rates of uptake can be distinguished in the intact animal. First, there is a rapid rate of oxygen uptake corresponding with activity and second there is a slower rate which corresponds with periods of quiescence and which alternates with the fast rate. Intermediate rates correspond with intermediate rates of overt activity. The maximal and minimal rates of oxygen uptake are affected differently by temperature change. The fast rate corresponding to activity ("active metabolism") increases with temperature in approximate agreement with Arrhenius's law. The slow rate corresponding to quiescence ("maintenance metabolism") does not vary with temperature over much of the range 7 to 22.5C. It is concluded that, contrary to common belief, the intertidal invertebrates studied have a "basal metabolic rate" with a Q₁₀ of approximately one over much of the normal environmental temperature range and in this respect are well suited to life in a habitat where rapid fluctuations in temperature occur.     

Rates of metabolism of planktonic crustaceans as related to body weight and temperature of habitat

The relation between the rates of oxygen consumption and ammoniumexcretion of planktonic crustaceans and their body weight, asexpressed by the allometric equation (M = a W^b), was establishedfor animals collected from two habitats of different temperature:a boreal region, the southeastern Bering Sea, and a subtropicalregion, the Mid-Atlantic Bight. In contrast to findings of previousinvestigations on the effect of temperature of habitat on thebody-size dependence of metabolic rates of zooplankton, theslope of the equation relating rate of metabolism and body weightwas independent of temperature of habitat, but the interceptof the equation was strongly influenced by temperature of habitatand the lipid content of the animals.     

Critical Thermal Maxima of aquatic macroinvertebrates: towards identifying bioindicators of thermal alteration

Water temperature is an important abiotic driver of aquatic ecosystems. It influences many aspects of an organism’s existence including its growth, feeding and metabolic rates; emergence; fecundity; behaviour and ultimately survival. All organisms have an optimum temperature range within which they survive and are able to thrive. Determining upper thermal limits provides insight into the relative sensitivity of organisms to elevated temperatures. Thermally sensitive taxa may be useful as bioindicators of thermal alteration and used in the generation of target thermal thresholds for aquatic systems. This study determined the upper thermal limit (CTmax) of a range of aquatic macroinvertebrates from rivers in the south-western Cape, South Africa, using the dynamic Critical Thermal Method. The study focused on the taxonomic level of family as an initial screening tool for ranking thermal sensitivity. Of the 27 families examined, four were both thermally sensitive and highly suitable as test organisms, including Paramelitidae, Notonemouridae, Teloganodidae and Philopotamidae. Five families were moderately sensitive and highly suitable, including Palaemonidae, Heptageniidae, Leptophlebiidae, Corydalidae and Aeshnidae. Preliminary experiments to determine potential sources of variation in CTmax revealed that thermal sensitivity was relatively uniform within families, but that acclimation temperature influenced CTmax. Further investigation of the influence of thermal history, acclimation temperature and rate of temperature change on CTmax is necessary. Target water temperatures for river management will be derived using CTmax data, in addition to longer duration experimental data, which will be linked to in situ temperature data.     

Upper temperature limits of tropical marine ectotherms: global warming implications

Animal physiology, ecology and evolution are affected by temperature and it is expected that community structure will be strongly influenced by global warming. This is particularly relevant in the tropics, where organisms are already living close to their upper temperature limits and hence are highly vulnerable to rising temperature. Here we present data on upper temperature limits of 34 tropical marine ectotherm species from seven phyla living in intertidal and subtidal habitats. Short term thermal tolerances and vertical distributions were correlated, i.e., upper shore animals have higher thermal tolerance than lower shore and subtidal animals; however, animals, despite their respective tidal height, were susceptible to the same temperature in the long term. When temperatures were raised by 1°C hour(-1), the upper lethal temperature range of intertidal ectotherms was 41-52°C, but this range was narrower and reduced to 37-41°C in subtidal animals. The rate of temperature change, however, affected intertidal and subtidal animals differently. In chronic heating experiments when temperature was raised weekly or monthly instead of every hour, upper temperature limits of subtidal species decreased from 40°C to 35.4°C, while the decrease was more than 10°C in high shore organisms. Hence in the long term, activity and survival of tropical marine organisms could be compromised just 2-3°C above present seawater temperatures. Differences between animals from environments that experience different levels of temperature variability suggest that the physiological mechanisms underlying thermal sensitivity may vary at different rates of warming.     

Metabolic cold adaptation in fishes occurs at the level of whole animal, mitochondria and enzyme

Metabolic cold adaptation (MCA), the hypothesis that species from cold climates have relatively higher metabolic rates than those from warm climates, was first proposed nearly 100 years ago and remains one of the most controversial hypotheses in physiological ecology. In the present study, we test the MCA hypothesis in fishes at the level of whole animal, mitochondria and enzyme. In support of the MCA hypothesis, we find that when normalized to a common temperature, species with ranges that extend to high latitude (cooler climates) have high aerobic enzyme (citrate synthase) activity, high rates of mitochondrial respiration and high standard metabolic rates. Metabolic compensation for the global temperature gradient is not complete however, so when measured at their habitat temperature species from high latitude have lower absolute rates of metabolism than species from low latitudes. Evolutionary adaptation and thermal plasticity are therefore insufficient to completely overcome the acute thermodynamic effects of temperature, at least in fishes.     

Thermal acclimation is not necessary to maintain a wide thermal breadth of aerobic scope in the common killifish (Fundulus heteroclitus)

Loss of aerobic scope at high and low temperatures is a physiological mechanism proposed to limit the thermal performance and tolerance of organisms, a theory known as oxygen- and capacity-limited thermal tolerance (OCLTT). Eurythermal organisms maintain aerobic scope over wide ranges of temperatures, but it is unknown whether acclimation is necessary to maintain this breadth. The objective of this study was to examine changes in aerobic scope in Fundulus heteroclitus, a eurythermal fish, after acclimation and acute exposure to temperatures from 5° to 33°C. The range of temperatures over which aerobic scope was nonzero was similar in acclimated and acutely exposed fish, suggesting that acclimation has modest effects on the thermal breadth of aerobic scope. However, in acclimated fish, there was a clear optimum temperature range for aerobic scope between 25° and 30°C, whereas aerobic scope was relatively constant across the entire temperature range with acute temperature exposure. Therefore, the primary effect of acclimation was to increase aerobic scope between 25° and 30°C, which paradoxically resulted in a narrower temperature range of optimal performance in acclimated fish compared to acutely exposed fish. There was only weak evidence for correlations between the thermal optimum of aerobic scope and the thermal optimum of measures of performance (specific growth rate and gonadosomatic index), and indicators of anaerobic metabolism (lactate accumulation and lactate dehydrogenase activity) only increased at high temperatures. Together these data fit many, but not all, of the predictions made by OCLTT.     

Thermal biology of flight in a butterfly: genotype,flight metabolism,and environmental conditions

Knowledge of the effects of thermal conditions on animal movement and dispersal is necessary for a mechanistic understanding of the consequences of climate change and habitat fragmentation. In particular, the flight of ectothermic insects such as small butterflies is greatly influenced by ambient temperature. Here, variation in body temperature during flight is investigated in an ecological model species, the Glanville fritillary butterfly (Melitaea cinxia). Attention is paid on the effects of flight metabolism, genotypes at candidate loci, and environmental conditions. Measurements were made under a natural range of conditions using infrared thermal imaging. Heating of flight muscles by flight metabolism has been presumed to be negligible in small butterflies. However, the results demonstrate that Glanville fritillary males with high flight metabolic rate maintain elevated body temperature better during flight than males with a low rate of flight metabolism. This effect is likely to have a significant influence on the dispersal performance and fitness of butterflies and demonstrates the possible importance of intraspecific physiological variation on dispersal in other similar ectothermic insects. The results also suggest that individuals having an advantage in low ambient temperatures can be susceptible to overheating at high temperatures. Further, tolerance of high temperatures may be important for flight performance, as indicated by an association of heat‐shock protein (Hsp70) genotype with flight metabolic rate and body temperature at takeoff. The dynamics of body temperature at flight and factors affecting it also differed significantly between female and male butterflies, indicating that thermal dynamics are governed by different mechanisms in the two sexes. This study contributes to knowledge about factors affecting intraspecific variation in dispersal‐related thermal performance in butterflies and other insects. Such information is needed for predictive models of the evolution of dispersal in the face of habitat fragmentation and climate change.     

Extreme climatic events constrain space use and survival of a ground‐nesting bird

Two fundamental issues in ecology are understanding what influences the distribution and abundance of organisms through space and time. While it is well established that broad‐scale patterns of abiotic and biotic conditions affect organisms’ distributions and population fluctuations, discrete events may be important drivers of space use, survival, and persistence. These discrete extreme climatic events can constrain populations and space use at fine scales beyond that which is typically measured in ecological studies. Recently, a growing body of literature has identified thermal stress as a potential mechanism in determining space use and survival. We sought to determine how ambient temperature at fine temporal scales affected survival and space use for a ground‐nesting quail species (Colinus virginianus; northern bobwhite). We modeled space use across an ambient temperature gradient (ranging from ?20 to 38 °C) through a maxent algorithm. We also used Andersen–Gill proportional hazard models to assess the influence of ambient temperature‐related variables on survival through time. Estimated available useable space ranged from 18.6% to 57.1% of the landscape depending on ambient temperature. The lowest and highest ambient temperature categories (35 °C, respectively) were associated with the least amount of estimated useable space (18.6% and 24.6%, respectively). Range overlap analysis indicated dissimilarity in areas where Colinus virginianus were restricted during times of thermal extremes (range overlap = 0.38). This suggests that habitat under a given condition is not necessarily a habitat under alternative conditions. Further, we found survival was most influenced by weekly minimum ambient temperatures. Our results demonstrate that ecological constraints can occur along a thermal gradient and that understanding the effects of these discrete events and how they change over time may be more important to conservation of organisms than are average and broad‐scale conditions as typically measured in ecological studies.     

The effect of temperature,irradiance and animal size on incorporation rates of Simocephalus vetulus

Carbon incorporation rates of Simocephalus vetulus were measured to study the effects of the physical state of the animals, size of the animal, varying temperature and light conditions. Physical state of the animal showed little effect on incorporation rates after the first hour. Incorporation rates increased in proportion to the third power of animal size. Experimental animals collected at temperatures of 12, 20 or 25°C fed maximally at 10, 15 and 25°C respectively, when subjected to a feeding temperature range of 5 to 30°C. We have interpreted this as an indication that S. vetulus is able to acclimate and incorporate maximally at various temperatures after prolonged exposure to that temperature. When fed over an irradiation range of 0 to 4.68 × 10^–3 cal cm^–2 s^–1 incorporation rates were indirectly proportional to irradiance. This suggests a response to decreased irradiance in the weedy, littoral habitat of these animals.     

Demography of the sessile rotifers, <Emphasis Type="Italic">Limnias ceratophylli</Emphasis> and <Emphasis Type="Italic">Limnias melicerta</Emphasis> (Rotifera: Gnesiotrocha), in relation to food (<Emphasis Type="Italic">Chlorella vulgaris</Emphasis> Beijerinck, 1890) density

Circadian rhythms occur widely amongst living organisms, often in response to diel changes in environmental conditions. In aquatic animals, circadian activity is often synchronised with diel changes in the depths individuals occupy and may be related to predator–prey interactions, where the circadian rhythm is determined by ambient light levels, or have a thermoregulatory purpose, where the circadian rhythm is governed by temperature. Here, these two hypotheses are examined using animal-attached accelerometers in juvenile freshwater sawfish occupying a riverine environment displaying seasonal changes in thermal stratification. Across seasons, diel patterns of depth use (shallow at night and deep in the day) tended to occur only in the late dry seasons when the water was stratified, whereas individuals were primarily shallow in the early dry season which featured no thermal stratification. Activity was elevated during crepuscular and nocturnal periods compared to daytime, regardless of the thermal environment. Our observation of resting at cooler depths is consistent with behavioural thermoregulation to reduce energy expenditure, whereas activity appears linked to ambient light levels and predator–prey interactions. This suggests that circadian rhythms in activity and vertical migrations are decoupled in this species and respond to independent environmental drivers.     

The origin of homoiothermy--unsolved problem

The analysis of allometric dependence of energy expenditure on body mass among reptiles, birds and mammals has shown that standard metabolic rate of reptiles when they are warmed up to the temperature of homoiothermic animals is an order of magnitude lower than that of birds and mammals. Basal metabolism is originated as special feature historically related to the metabolism during active behavior, rather than thermal regulation. Facultative endothermy was not advantageous for large animals because of long time needed to warm up the body. The ancestors of birds and animals escaped negative consequences of van't-Hoff equation by choosing constant body temperature. Heat conductivity of reptile's covers is so great, that it cannot keep endogenous warm of resting animal at any temperature of the body. Reptile "dressed" in covers of bird or mammal would be able to keep warm under conditions of maximal aerobic muscular activity and body temperature similar to that of homoiothermic animals. The base of chemical thermoregulation in birds and mammals is a thermoregulatory muscle tonus which remains unknown. One can suppose that during evolution of birds and mammals the saltation-liked origin of endothermy "fixed" the level of metabolism typical for running reptile and transformed in into the basal metabolism. This event took place at the cell and tissue level. The absence of palaeontological evidences and intermediate forms among recent species does not allow easy understanding of homoiothermy origin.     

Thermal Carrying Capacity for a Thermally-Sensitive Species at the Warmest Edge of Its Range

Anthropogenic environmental change is causing unprecedented rates of population extirpation and altering the setting of range limits for many species. Significant population declines may occur however before any reduction in range is observed. Determining and modelling the factors driving population size and trends is consequently critical to predict trajectories of change and future extinction risk. We tracked during 12 years 51 populations of a cold-water fish species (brown trout Salmo trutta) living along a temperature gradient at the warmest thermal edge of its range. We developed a carrying capacity model in which maximum population size is limited by physical habitat conditions and regulated through territoriality. We first tested whether population numbers were driven by carrying capacity dynamics and then targeted on establishing (1) the temperature thresholds beyond which population numbers switch from being physical habitat- to temperature-limited; and (2) the rate at which carrying capacity declines with temperature within limiting thermal ranges. Carrying capacity along with emergent density-dependent responses explained up to 76% of spatio-temporal density variability of juveniles and adults but only 50% of young-of-the-year''s. By contrast, young-of-the-year trout were highly sensitive to thermal conditions, their performance declining with temperature at a higher rate than older life stages, and disruptions being triggered at lower temperature thresholds. Results suggest that limiting temperature effects were progressively stronger with increasing anthropogenic disturbance. There was however a critical threshold, matching the incipient thermal limit for survival, beyond which realized density was always below potential numbers irrespective of disturbance intensity. We additionally found a lower threshold, matching the thermal limit for feeding, beyond which even unaltered populations declined. We predict that most of our study populations may become extinct by 2100, depicting the gloomy fate of thermally-sensitive species occurring at thermal range margins under limited potential for adaptation and dispersal.     

Hot and steady: Elevated temperatures do not enhance muscle disuse atrophy during prolonged aestivation in the ectotherm Cyclorana alboguttata

Animals that undergo prolonged dormancy experience minimal muscle disuse atrophy (MDA) compared to animals subjected to artificial immobilisation over shorter timeframes. An association between oxidative stress and MDA suggests that metabolic depression presumably affords dormant animals some protection against muscle disuse. Because aerobic metabolism is temperature sensitive, we proposed that MDA in dormant (aestivating) ectotherms would be enhanced at elevated temperatures. In the green‐striped burrowing frog, Cyclorana alboguttata, the thermal sensitivity of skeletal muscle metabolic rate is muscle‐specific. We proposed that the degree of atrophy experienced during aestivation would correlate with the thermal sensitivity of muscle metabolic rate such that muscles with a relatively high metabolic rate at high temperatures would experience more disuse atrophy. To test this hypothesis, we examined the effect of temperature and aestivation on the extent of MDA in two functionally different muscles: the M. gastrocnemius (jumping muscle) and M. iliofibularis (non‐jumping muscle), in C. alboguttata aestivating at 24 or 30°C for 6 months. We compared a range of morphological parameters from muscle cross‐sections stained with succinic dehydrogenase to show that muscle‐specific patterns of disuse atrophy were consistent with the relative rates of oxygen consumption of those muscle types. However, despite muscle‐specific differences in thermal sensitivity of metabolic rate, aestivation temperature did not influence the extent of atrophy in either muscle. Our results suggest that the muscles of frogs aestivating at high temperatures are defended against additional atrophy ensuring protection of muscle function during long periods of immobilisation. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.     

Physiological correlates of habitat association in East African sunbirds (Nectariniidae)

East African sunbirds (Nectariniidae) vary in the degree to which they use open habitats and forest habitats. Species that use open habitats may experience more extreme temperatures and greater exposure to solar radiation than those in forest habitats. Basal rates of metabolism, body temperature and thermal conductance were compared for open habitat- and forest-associated sunbirds from Kibale National Park, Uganda. Variation in basal rate of metabolism was associated with body mass, but there was no difference between forest and open habitat species. Variation in body temperature was not associated with body mass or habitat. Variation in thermal conductance was associated with body mass and habitat; open habitat species were characterized by significantly lower thermal conductances than forest species. Because reduced thermal conductance may decrease energy expenditure at low ambient temperatures and reduce exogenous heat gain at high ambient temperatures, this difference may optimize energy expenditure when temperatures are highly variable. This suggests a mechanism by which physiological characteristics may influence energetic consequences of habitat selection.     

Unravelling the effects of elevated temperature on the physiological energetics of Bellamya bengalensis

Temperature is one of the key environmental factors affecting the eco-physiological responses of living organisms and is considered one of the utmost crucial factors in shaping the fundamental niche of a species. The purpose of the present study is to delineate the physiological response and changes in energy allocation strategy of Bellamya bengalensis, a freshwater gastropod in the anticipated summer elevated temperature in the future by measuring the growth, body conditions (change in total weight, change in organ to flesh weight ratio), physiological energetics (ingestion rate, absorption rate, respiration rate, excretion rate and Scope for Growth) and thermal performance, Arrhenius breakpoint temperature (ABT), thermal critical maxima (CTmax), warming tolerance (WT) as well as thermal safety margin (TSM) through a mesocosm experiment. We exposed the animals to three different temperatures, 25 °C (average habitat temperature for this animal) and elevated temperatures 30 °C, 35 °C for 30 days and changes in energy budget were measured twice (on 15th and 30th day). Significant changes were observed in body conditions as well as physiological energetics. The total body weight as well as the organ/flesh weight ratio, ingestion followed by absorption rate decreased whereas, respiration and excretion rate increased with elevated temperature treatments resulting in a negative Scope for Growth in adverse conditions. Though no profound impact was found on ABT/CTmax, the peak of thermal curve was considerably declined for animals that were reared in higher temperature treatments. Our data reflects that thermal stress greatly impact the physiological functioning and growth patterns of B. bengalensis which might jeopardize the freshwater ecosystem functioning in future climate change scenario.     

The combined effects of reactant kinetics and enzyme stability explain the temperature dependence of metabolic rates

A mechanistic understanding of the response of metabolic rate to temperature is essential for understanding thermal ecology and metabolic adaptation. Although the Arrhenius equation has been used to describe the effects of temperature on reaction rates and metabolic traits, it does not adequately describe two aspects of the thermal performance curve (TPC) for metabolic rate—that metabolic rate is a unimodal function of temperature often with maximal values in the biologically relevant temperature range and that activation energies are temperature dependent. We show that the temperature dependence of metabolic rate in ectotherms is well described by an enzyme‐assisted Arrhenius (EAAR) model that accounts for the temperature‐dependent contribution of enzymes to decreasing the activation energy required for reactions to occur. The model is mechanistically derived using the thermodynamic rules that govern protein stability. We contrast our model with other unimodal functions that also can be used to describe the temperature dependence of metabolic rate to show how the EAAR model provides an important advance over previous work. We fit the EAAR model to metabolic rate data for a variety of taxa to demonstrate the model's utility in describing metabolic rate TPCs while revealing significant differences in thermodynamic properties across species and acclimation temperatures. Our model advances our ability to understand the metabolic and ecological consequences of increases in the mean and variance of temperature associated with global climate change. In addition, the model suggests avenues by which organisms can acclimate and adapt to changing thermal environments. Furthermore, the parameters in the EAAR model generate links between organismal level performance and underlying molecular processes that can be tested for in future work.     

Temperature influences whole-animal rates of metabolism but not protein synthesis in a temperate intertidal isopod

The effects of temperature on two important biological rate processes, whole-body rates of oxygen uptake (M dot o2) and protein synthesis (k(s)), were investigated in the temperate intertidal isopod Ligia oceanica at two different times of the year. Animals were collected in January (winter) and June (summer) and either subjected to an acute temperature change after 24 h (acclimatized) or acclimated to various temperatures for 4 wk. In both cases, M dot o2 increased with temperature, with a Q(10) of 2.2 between 5 degrees and 20 degrees C, but increased in thermal sensitivity at 25 degrees C. Winter isopods were characterized by significantly higher M dot o2 levels, greater thermal sensitivities, and lower thermal tolerances than summer animals. Seasonal differences in M dot o2 persisted after acclimation, indicating that temperature alone was not responsible for the changes. In sharp contrast, whole-body k(s) showed no variation with temperature, although overall rates decreased upon acclimation. In acclimatized animals, k(s) was higher in the summer than in the winter. After acclimation, a compensatory increase in RNA capacity in winter animals reversed this situation. The temperature independence of whole-body k(s) in L. oceanica could ensure survival in a highly liable thermal environment, as thermal tolerances of intertidal invertebrates are thought to be more closely related to protein than to energy metabolism.     

Global analysis of thermal tolerance and latitude in ectotherms

A tenet of macroecology is that physiological processes of organisms are linked to large-scale geographical patterns in environmental conditions. Species at higher latitudes experience greater seasonal temperature variation and are consequently predicted to withstand greater temperature extremes. We tested for relationships between breadths of thermal tolerance in ectothermic animals and the latitude of specimen location using all available data, while accounting for habitat, hemisphere, methodological differences and taxonomic affinity. We found that thermal tolerance breadths generally increase with latitude, and do so at a greater rate in the Northern Hemisphere. In terrestrial ectotherms, upper thermal limits vary little while lower thermal limits decrease with latitude. By contrast, marine species display a coherent poleward decrease in both upper and lower thermal limits. Our findings provide comprehensive global support for hypotheses generated from studies at smaller taxonomic subsets and geographical scales. Our results further indicate differences between terrestrial and marine ectotherms in how thermal physiology varies with latitude that may relate to the degree of temperature variability experienced on land and in the ocean.     

The comparative energetics of rigid endothermy: the Arvicolidae

Rate of metabolism and body temperature were examined in 24 species of arvicolid rodents, for 15 of which data are presented here, to determine the factors that influence their level of energy expenditure. Arvicolids are characterized by a high, precisely-regulated body temperature, a high basal rate of metabolism by general mammalian standards, and a standard thermal conductance, except at large masses, when low conductances can occur. No evidence of entrance into torpor is known for any arvicolid; its absence is associated with especially high basal rates at masses smaller than 52 g. Arvicolids that live in cold climates, i.e. at high altitudes and latitudes, have higher basal rates than species that live in other environments. Basal rates, however, appear to be independent of food habits, presumably because of the small mass of most species and possibly because all species are herbivorous. A small size in combination with herbivory has permitted arvicolids to maintain continuous endothermy, which in turn has permitted them to exploit cool-to-cold environments by means of a high rate of production. The use of daily or seasonal torpor might well have prevented arvicolids from attaining the pivotal position in energy transfer that they presently occupy in many high-latitude communities.