Activity affects intraspecific body-size scaling of metabolic rate in ectothermic animals

Metabolic rate is commonly thought to scale with body mass (M) to the 3/4 power. However, the metabolic scaling exponent (b) may vary with activity state, as has been shown chiefly for interspecific relationships. Here I use a meta-analysis of literature data to test whether b changes with activity level within species of ectothermic animals. Data for 19 species show that b is usually higher during active exercise (mean ± 95% confidence limits = 0.918 ± 0.038) than during rest (0.768 ± 0.069). This significant upward shift in b to near 1 is consistent with the metabolic level boundaries hypothesis, which predicts that maximal metabolic rate during exercise should be chiefly influenced by volume-related muscular power production (scaling as M ¹). This dependence of b on activity level does not appear to be a simple temperature effect because body temperature in ectotherms changes very little during exercise.     

Reduction of metabolic rate and thermoregulation during daily torpor

Physiological mechanisms causing reduction of metabolic rate during torpor in heterothermic endotherms are controversial. The original view that metabolic rate is reduced below the basal metabolic rate because the lowered body temperature reduces tissue metabolism has been challenged by a recent hypothesis which claims that metabolic rate during torpor is actively downregulated and is a function of the differential between body temperature and ambient temperature, rather than body temperature per se. In the present study, both the steady-state metabolic rate and body temperature of torpid stripe-faced dunnarts, Sminthopsis macroura (Dasyuridae: Marsupialia), showed two clearly different phases in response to change of air temperature. At air temperatures between 14 and 30°C, metabolic rate and body temperature decreased with air temperature, and metabolic rate showed an exponential relationship with body temperature (r ²=0.74). The Q ₁₀ for metabolic rate was between 2 and 3 over the body temperature range of 16 to 32°C. The difference between body temperature and air temperature over this temperature range did not change significantly, and the metabolic rate was not related to the difference between body temperature and air temperature (P=0.35). However, the apparent conductance decreased with air temperature. At air temperatures below 14°C, metabolic rate increased linearly with the decrease of air temperature (r ²=0.58) and body temperature was maintained above 16°C, largely independent of air temperature. Over this air temperature range, metabolic rate was positively correlated with the difference between body temperature and air temperature (r ²=0.61). Nevertheless, the Q ₁₀ for metabolic rate between normothermic and torpid thermoregulating animals at the same air temperature was also in the range of 2–3. These results suggest that over the air temperature range in which body temperature of S. macroura was not metabolically defended, metabolic rate during daily torpor was largely a function of body temperature. At air temperatures below 14°C, at which the torpid animals showed an increase of metabolic rate to regulate body temperature, the negative relationship between metabolic rate and air temperature was a function of the differential between body temperature and air temperature as during normothermia. However, even in thermoregulating animals, the reduction of metabolic rate from normothermia to torpor at a given air temperature can also be explained by temperature effects.Abbreviations BM body mass - BMR basal metabolic rate - C apparent conductance - MR metabolic rate - RMR resting metabolic rate - RQ respiratory quotient - T _a air temperature - T _b body temperature - T _lc lower critical temperature - T _tc critical air temperature during torpor - TMR metabolic rate during torpor - TNZ thermoneutral zone - T difference between body temperature and air temperature - VO₂ rate of oxygen consumption     

Metabolic turnover rate: a physiological meaning of the metabolic rate per unit body weight.

In analogy to “specific gravity” or “specific heat” the expression “weight specific metabolic rate” (Ultsch, 1973) would be correct if the metabolic rate were directly proportional to body weight. In that case the quotient metabolic rate divided by body weight would be a constant, independent of body weight like density or specific heat are constants. The metabolic rate, however, is not proportional to body weight but to its $\text{3}\text{4}$ power. I have stated that heat flow per unit body weight has no proper physical or physiological meaning (Kleiber, 1970), but since found such a physiological meaning: in work with tracers turnover rates are measured as quotients of transfer rates/pool content. For similometric animals pool contents are proportional to body weight. For such animals therefore the quotient metabolic rate/body weight may have a proper physiological meaning, namely the turnover rate of chemical energy in the animal body.The usefulness of the turnover rate is limited. For the calculation of the energy requirement of horizontal animal locomotion, for example, the calculation from the metabolic rate per animal is preferable to the calculation based on the metabolic rate per unit body weight.     

Thermal dependence of clearance and metabolic rates in slow- and fast-growing spats of manila clam Ruditapes philippinarum

Thermal dependence of clearance rate (CR: l h^?1), standard (SMR: J h^?1) and routine metabolic rates (RMR: J h^?1), were analyzed in fast (F)- and slow (S)-growing juveniles of the clam Ruditapes philippinarum. Physiological rates were measured at the maintenance temperature (17 °C), and compared with measurements performed at 10 and 24 °C after 16 h and 14 days to analyze acute and acclimated responses, respectively. Metabolic rates (both RMR and SMR) differed significantly between F and S seeds, irrespective of temperature. Mass-specific CRs were not different for F and S seeds but were significantly higher in F clams for rates standardized according to allometric size-scaling rules. Acute thermal dependency of CR was equal for F and S clams: mean Q ₁₀ were ≈3 and 2 in temperature ranges of 10–17 and 17–24 °C, respectively. CR did not change after 2 weeks of acclimation to temperatures. Acute thermal effects on SMR were similar in both groups (Q ₁₀ ≈ 1 and 1.6 in temperature ranges of 10–17 and 17–24 °C, respectively). Large differences between groups were found in the acute thermal dependence of RMR: Q ₁₀ in F clams (≈1.2 and 1.9 at temperature ranges of 10–17 and 17–24 °C, respectively) were similar to those found for SMR (Q ₁₀ = 1.0 and 1.7). In contrast, RMR of S clams exhibited maximum thermal dependence (Q ₁₀ = 3.1) at 10–17 °C and become depressed at higher temperatures (Q ₁₀ = 0.9 at 17–24 °C). A recovery of RMR in S clams was recorded upon acclimation to 24 °C. Contrasting metabolic patterns between fast and slow growers are interpreted as a consequence of differential thermal sensitivity of the fraction of metabolism associated to food processing and assimilation.     

Oscillatory pattern in oxygen consumption of Hummingbirds

Mammals and birds offer the most conspicuous example of homeothermic endothermy, a metabolic feature that implies maintenance of a constant body temperature along broad ranges of ambient temperature. The concept of homeothermic endothermy has been developed in close association with the terms thermoneutral zone and basal metabolic rate. These two metabolic parameters, however, are not easily estimated in micro-endotherms, a difficulty that might emerge from intrinsic aspects of endothermy in minute animals. To address this issue, we used empirical work derived from theoretical considerations. Our theoretical analysis is based on a model of body temperature control by shifts in metabolic rate, and assumes that micro-endotherms lose heat very quickly due to body size, and exhibit a remarkable capacity to rapidly increase metabolic output. We found that these two metabolic traits can lead to non-equilibrium metabolic rate and body temperature. We then measured metabolic rate and body temperature during euthermia in two species of hummingbirds, and analyzed data using the χ² periodogram statistic and a power spectral analysis. We found long-range correlation in both oxygen consumption and body temperature during euthermia, a finding that suggests non-random 1/f oscillations. A similar pattern was not found in the rat, a much larger endotherm. Hummingbirds, then, do not appear to maintain steady-state metabolic conditions during euthermia. If, as we suggest, this pattern applies to micro-endotherms in general, the traditional concepts of thermoneutral zone and basal rate of metabolism might not apply to these animals.     

Possible roles of two quinone molecules in direct and indirect proton pumps of bovine heart NADH-quinone oxidoreductase (complex I)

In many energy transducing systems which couple electron and proton transport, for example, bacterial photosynthetic reaction center, cytochrome bc₁-complex (complex III) and E. coli quinol oxidase (cytochrome bo₃ complex), two protein-associated quinone molecules are known to work together. T. Ohnishi and her collaborators reported that two distinct semiquinone species also play important roles in NADH-ubiquinone oxidoreductase (complex I). They were called SQ_Nf (fast relaxing semiquinone) and SQ_Ns (slow relaxing semiquinone). It was proposed that Q_Nf serves as a “direct” proton carrier in the semiquinone-gated proton pump (Ohnishi and Salerno, FEBS Letters 579 (2005) 4555), while Q_Ns works as a converter between one-electron and two-electron transport processes. This communication presents a revised hypothesis in which Q_Nf plays a role in a “direct” redox-driven proton pump, while Q_Ns triggers an “indirect” conformation-driven proton pump. Q_Nf and Q_Ns together serve as (1e^?/2e^?) converter, for the transfer of reducing equivalent to the Q-pool.     

Respiratory metabolism of temperature acclimated Fundulus heteroclitus (L.): Zones of compensation and dependence

The oxygen consumption of temperature acclimated mummichogs, Fundulus heteroclitus (L.) weighing ≈0.1–10.0 g, was measured at 5, 13, 21, and 29 C. Between 13 and 21°C and 21 and 29°C, the values of Q₁₀ were 1.55 and 1.04, respectively, indicating relative thermal independence of respiratory metabolic rate over this 16°C range (Q₁₀ = 1.27). This range encompasses the normal late spring, summer, and early fall range of habitat temperature in Maine estuaries, so that mummichogs are able to grow and reproduce relatively independent of environmental temperature. Between 5 and 13°C, respiratory metabolism is very temperature sensitive (Q₁₀ = 4.42) indicating a substantial reduction of metabolic processes at low temperatures. This enables mummichogs to conserve any metabolic reserves during the coldest months. The regression of log weight-specific oxygen consumption on log body weight was determined at each experimental temperature. All had significantly negative slopes indicating the importance of body size in mummichog respiration.     

Site of bicarbonate effect in Hill reaction. Evidence from the use of artificial electron acceptors and donors

Using artificial electron donors and acceptors, it is shown here that the major HCO₃^? effect in the Hill reaction is after the “primary” electron acceptor (Q) of Photosystem II and before the site of action of 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone (at the plastoquinone pool). Chloroplasts in the presence of both 3-(3′,4′-dichlorophenyl)-1,1-dimethylurea, which blocks electron flow from the reduced primary acceptor Q^? to the plastoquinone pool, and silicomolybdate, which accepts electrons from Q^?, show no significant bicarbonate stimulation of electron flow. However, a 6–7-fold stimulation is clearly observed when oxidized diaminodurene, as an electron acceptor, and dibromothymoquinone, as an inhibitor of electron flow beyond the plastoquinone pool, are used. In the same chloroplast preparation no measurable effect of bicarbonate is observed in a Photosystem I reaction as monitored by electron flow from reduced diaminodurene to methyl viologen in the presence of 3-(3′,4′-dichlorophenyl)-1,1-dimethylurea. The insensitivity of the bicarbonate effect to uncouplers of photophosphorylation and the dependence of this effect on the presence of a weak acid anion and on external pH are also reported.     

Temperature dependence and ontogenetic changes of metabolic rate of an endemic earthworm <Emphasis Type="Italic">Dendrobaena mrazeki</Emphasis>

Ontogenetic changes and temperature dependency of respiration rate were studied in Dendrobaena mrazeki, an earthworm species inhabiting relatively warm and dry habitats in Central Europe. D. mrazeki showed respiration rate lower than in other earthworm species, < 70 μl O₂ g⁻¹ h⁻¹, within the temperature range of 5–35°C. The difference of respiration rate between juveniles and adults was insignificant at 20°C. The response of oxygen consumption to sudden temperature changes was compared with the temperature dependence of respiratory activity in animals pre-acclimated to temperature of measurement. No significant impact of acclimation on the temperature response of oxygen consumption was found. The body mass-adjusted respiration rate increased slowly with increasing temperature from 5 to 25°C (Q₁₀ from 1.2 to 1.7) independently on acclimation history of earthworms. Oxygen consumption decreased above 25°C up to upper lethal limit (about 35°C). Temperature dependence of metabolic rate is smaller than in other earthworm species. The relationships between low metabolic sensitivity to temperature, slow locomotion and reactivity to touching as observed in this species are discussed.     

Human nonshivering thermogenesis

Metabolic responses, skin temperatures and changes in heart rate and blood pressure were measured in a control group and in “polar swimmers” after infusion of different doses of epinephrine, norepinephrine and isoprenaline. In controls the highest infusion dose of isoprenaline (0.1 μg min⁻¹ kg⁻¹) increased metabolic rate in normal humans by 36%, while the highest infusion doses of epinephrine and norepinephrine (0.45 μg min⁻¹ kg⁻¹) increased metabolic rate by 24%, only. In “polar swimmers” the epinephrine thermogenesis was potentiated significantly, reaching about 45% of the basal metabolic rate. The norepinephrine and isoprenaline thermogenesis were not different from that of the control group. It is concluded that in humans the epinephrine thermogenesis is probably located in muscles and in the white fat (Simonsen et al., 1992), and may be the principal mechanism of metabolic adaptation to cold. It was calculated that the increased capacity of epinephrine thermogenesis in cold exposed “polar swimmers” could theoretically shift the survival limit downwards to lower environmental temperatures by about 5°C.     

The influence of hydrogen bonds on electron transfer rate in photosynthetic RCs

Hydrogen bonds formed between photosynthetic reaction centers (RCs) and their cofactors were shown to affect the efficacy of electron transfer. The mechanism of such influence is determined by sensitivity of hydrogen bonds to electron density rearrangements, which alter hydrogen bonds potential energy surface. Quantum chemistry calculations were carried out on a system consisting of a primary quinone Q_A, non-heme Fe²⁺ ion and neighboring residues_. The primary quinone forms two hydrogen bonds with its environment, one of which was shown to be highly sensitive to the Q_A state. In the case of the reduced primary quinone two stable hydrogen bond proton positions were shown to exist on [Q_A-His^M219] hydrogen bond line, while there is only one stable proton position in the case of the oxidized primary quinone. Taking into account this fact and also the ability of proton to transfer between potential energy wells along a hydrogen bond, theoretical study of temperature dependence of hydrogen bond polarization was carried out. Current theory was successfully applied to interpret dark P⁺/Q_A⁻ recombination rate temperature dependence.     

Neuere mathematische Formulierungen der biologischen Temperaturfunktion und des Wachstums

The effects of temperature on metabolic rates cannot be assessed satisfactorly on the basis of Q₁₀-values or by theArrhenius formula. In many cases a surprisingly exact expression is obtained if a lower temperature value is used in the power of the denominator of theArrhenius-formula instead of the reciprocal value of the absolute temperature. An analysis ofKrogh's data shows that the examples upon which he based his “standard-curve” may be expressed very appropriately by the new expression presented in this paper. By using principally the same formula it becomes possible to express growth rates (in units of weight or length) of different kinds of animals. Its parameters allow to deduce the parameters of the allometric formula. The new formula seems to be suitable for expressing values of metabolic rates as a function of age. Considerations concerning the results ofJob (1955) on the troutSalvelinus fontinalis demonstrate that it is principally also possible to express mathematically changes of temperature-rate functions during growth.     

Mössbauer spectroscopy studies of photosynthetic reaction centers from Rhodopseudomonas sphaeroides R-26

⁵⁷Fe Mössbauer spectroscopy measurements on reaction centers differing in ubiquinone content, detergent, oxidation state, or the presence of o-phenanthroline all show a single quadrupole doublet of similar splitting (ΔE_Q), center shift (δ) and temperature dependence. The results are indicative of high-spin Fe²⁺ with an approximately invariant first coordination sphere. A crystal field model with strong electron delocalization can account for the temperature dependence of ΔE_Q, but further data are needed to achieve a unique parameterization.     

Studies on the regulation of initiation of chromosome replication in Escherichia coli.

The total initiation frequency of chromosome replication in Escherichia coli is dependent on two factors; the timing or time interval between successive initiations on an individual chromosome (initiation pace) and the number of individual chromosomes which are being replicated per cell. We have examined these parameters in a dnaA^ts, conditionally-lethal, “initiation mutant” of an E. coli K12 strain growing at different permissive temperatures. Our results indicate that at temperatures between 30 and 35 °C the gene product of the dnaA167 allele becomes limiting with respect to the number of replicating chromosomes per cell, which decreases from two at 30 °C to one at 35 °C. However, over this same temperature range it is clear that cell growth is balanced and the initiation pace, as determined from the growth rate, increases with temperature and is indistinguishable from that of the dnaA⁺ parent. These results demonstrate that one can alter the total initiation frequency independently of the initiation pace, indicating the involvement of at least two cellular components in the regulation of initiation. They also suggest that while the dnaA product may be involved in determining the total number of initiation events which can occur per cell per doubling time it does not control the timing or pace at which successive initiation events are triggered on each chromosome, i.e. it is not the “pace-maker” for initiation.     

NMR characterization of three forms of ferredoxin from Desulphovibrio gigas, a sulphate reducer

A NMR and magnetic susceptibility study of the oxidized and reduced states of three different oligomers (forms) of a [4Fe-4S] ferredoxin protein from Desulphovibrio gigas, FdI, FdI′, and FdII was carried out. FdI and FdI′ are different trimers and FdII a tetramer of the same basic subunit. A probable assignment of the contact shifted resonances is indicated. Since the temperature dependences of the contact shifted resonances associated with each [4Fe-4S] are not all similar a delocalized model for the spin densities on the 4Fe does not apply. The exchange rate between oxidized and reduced states is slow on the NMR time scale. The three oligomers are not magnetically equivalent. Using the “three state hypothesis” terminology it is shown that FdI_ox is predominantly in the C^2? state and changes upon reduction into the C^3? state, while FdII_ox is in the C^? state and changes into the C^2? state. FdI′ does not easily fit into this classification. This study shows a similarity of magnetic behaviour between FdI and bacterial ferredoxins (e.g. Bacillus polymyxa) and between FdII and HiPIP from Chromatium sp.. The influence of the quaternary structure on the stabilization of the different oxidation states of ferredoxins as well as on their redox potentials is discussed.     

T-lymphocyte mediated cytolysis: Temperature dependence of killer cell dependent and independent phases and lack of recovery from the lethal hit at low temperatures

Using alloantiserum and complement to inactivate cytolytic T-lymphocytes after they had administered the “lethal hit” to target cells, the rate of killer-cell independent lysis (KCIL) as measured by radiochromium release was followed at various temperatures. Under usual conditions, KCIL was half-completed on the average after 1.7 hr at 37 °C. The average Q₁₀ of KCIL is about 1.6 during the first few hours after cooling, but near 0 °, lysis slows down at later times. Thus, the extent of KCIL after 6–8 hr at 0 ° is frequently less than one-tenth of that at 37 °C. The Q₁₀ of the whole killing process is 2.5 near 37 °C but exceeds 6 near 22 °C.Evidence has been presented elsewhere suggesting that recovery from complement mediated damage may occur under appropriate conditions. Since KCIL can largely be arrested at low temperatures, we tested for possible recovery from or repair of the T-cell administered “lethal hit” during incubations at low temperature following (i) inactivation of killer cells by antiserum and complement or (ii) detachment of killer cells with EDTA and prevention of subsequent killer-target cell contact with dextran. No evidence for recovery from the “lethal hit” was found during incubations from 0.3 to 5 hr at 20 °, 15 °, or 0 °C. The temperature dependence of KCIL raises the possibility that metabolic events are of importance during KCIL. However, the previous finding that lysis following damage mediated by antiserum and complement is equally temperature sensitive leaves no basis for postulating such metabolic events. Hence, although unequivocal direct evidence has been difficult to obtain, colloid osmotic lysis is at present the simplest and most plausible explanation of killer-cell independent lysis.     

Environmental modulation of metabolic allometry in ornate rainbowfish Rhadinocentrus ornatus

The nature of the relationship between the metabolic rate (MR) and body mass (M) of animals has been the source of controversy for over seven decades, with much of the focus on the value of the scaling exponent b, where MR is proportional to M^b. While it is well known that MR does not generally scale isometrically (i.e. b is seldom equal to 1), the value of b remains the subject of heated debate. In the present study, we examine the influence of an ecologically relevant abiotic variable, pH, on the metabolic allometry of an Australian freshwater fish, Rhadinocentrus ornatus. We show that the value of b is lower for rainbowfish acclimated to acidic (pH 5.0) conditions compared to rainbowfish acclimated to alkaline conditions (pH 8.5), but that acute exposure to altered pH does not alter the value of b. This significant effect of an abiotic variable on metabolic allometry supports a growing body of evidence that there is no universal value of b and demonstrates that experimental manipulations of metabolic allometry represent powerful, and as yet underused, tools to understand the factors that constrain and influence the allometry of metabolic rate.     

Kinetics of amino acid incorporation into serum proteins

1. The effect of varying body temperature on the rate of amino acid incorporation into serum protein does not give support to the idea that the rate of this process is adjusted in vivo to restore those protein molecules destroyed by thermal denaturation. The experimentally observed Q₁₀ was about 3.9. 2. When amino acids are injected into the blood of animals in a steady state of serum protein turnover, a period of time elapses before these amino acids can be found in the serum proteins. This has been called transit time. At a given temperature (31°) it is the same in rabbits, turtles, and Limulus (1 hour). In rabbits and turtles it has a Q₁₀ of 3.2. It appears to be specifically related to the process of synthesis (or release) of serum proteins. 3. It was not possible to affect the transit time or the incorporation rate by the administration of amino acid analogues.     

Body temperature and metabolic rate during natural hypothermia in endotherms

During daily torpor and hibernation metabolic rate is reduced to a fraction of the euthermic metabolic rate. This reduction is commonly explained by temperature effects on biochemical reactions, as described by Q ₁₀ effects or Arrhenius plots. This study shows that the degree of metabolic suppression during hypothermia can alternatively be explained by active downregulation of metabolic rate and thermoregulatory control of heat production. Heat regulation is fully adequate to predict changes in metabolic rate, and Q ₁₀ effects are not required to explain the reduction of energy requirements during hibernation and torpor.Abbreviations BMR basal metabolic rate - BW body weight - C thermal conductance - C_HL thermal conductance as derived from HL - C_HP thermal conductance as derived from HP - HL heat loss - HP heat production - MR metabolic rate - RQ respiratory quotient - T_a ambient temperature - T_b body temperature