Mass-independent Metabolic Rate Research Articles

Metabolic rate and saliva cortisol concentrations in socially housed adolescent guinea pigs.

An individual's energetic demands and hence metabolic rate can strongly change during adolescence, a phase characterized by profound morphological, physiological, and endocrine changes. Glucocorticoid hormones (e.g. cortisol) are released in response to hypothalamic-pituitary-adrenal-axis activity, modulate several metabolic processes, and can also be linked to increased metabolic rate. In domestic guinea pigs (Cavia aperea f. porcellus) housed in same-sex groups, cortisol concentrations increase during adolescence in males but remain stable in females, which was suggested to be related to different energetic demands by age. We therefore measured metabolic rate through oxygen (O2) consumption over 2.5h in male and female guinea pigs housed in same-sex groups during adolescence at ages of 60, 120, and 180days, which was paralleled by analyses of saliva cortisol concentrations before and after the measurement. The statistical analyses involved whole body metabolic rate (ml O2/h), body mass-corrected metabolic rate (ml O2/h/kg), and body mass-independent metabolic rate (ml O2/h statistically corrected for body mass). We found increasing cortisol concentrations with age in males only, but none of the three metabolic rate analyses revealed a sex difference by age. On the individual level, repeatability across ages was found in metabolic rate as well as in body mass and cortisol concentrations after the measurement, but not in "basal" cortisol concentrations. Our results suggest no sex-specific changes in metabolic rate and hence equal energetic demands in male and female guinea pigs during adolescence. Moreover, metabolic rate clearly represents a highly stable physiological trait already early in a guinea pig's life irrespective of rather fluctuating cortisol concentrations.

Estimating the relationship between fitness and metabolic rate: which rate should we use?

As physiologists seek to better understand how and why metabolism varies, they have focused on how metabolic rate covaries with fitness-that is, selection. Evolutionary biologists have developed a sophisticated framework forexploring selection, but there are particular challenges associated with estimating selection on metabolic rate owing to its allometric relationship with body mass. Most researchers estimate selection on mass and absolute metabolic rate; or selection on mass and mass-independent metabolic rate(MIMR)-the residuals generated from a nonlinear regression. These approaches are sometimes treated as synonymous: their coefficients are often interpreted in the same way. Here, we show that these approaches are not equivalent because absolute metabolic rate and MIMR are different traits. We also show that it is difficult to make sound biological inferences about selection on absolute metabolic rate because its causal relationship with mass is enigmatic. By contrast, MIMR requires less-desirable statistical practices (i.e. residuals as a predictor), but provides clearer causal pathways. Moreover, we argue that estimates of selection on MIMR have more meaningful interpretations for physiologists interested in the drivers of variation in metabolic allometry. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

Great tits (Parus major) in a west European temperate forest show little seasonal variation in metabolic energy requirements

Understanding how birds annually allocate energy to cope with changing environmental conditions and physiological states is a crucial question in avian ecology. There are several hypotheses to explain species' energy allocation. One prominent hypothesis suggests higher energy expenditure in winter due to increased thermoregulatory costs. The "reallocation" hypothesis suggests no net difference in seasonal energy requirements, while the "increased demand" hypothesis predicts higher energy requirements during the breeding season. Birds are expected to adjust their mass and/or metabolic intensity in ways that are consistent with their energy requirements. Here, we look for metabolic signatures of seasonal variation in energy requirements of a resident passerine of a temperate-zone (great tit, Parus major). To do so, we measured whole-body and mass-independent basal (BMR), summit (Msum), and field (FMR) metabolic rates during late winter and during breeding in Belgian great tits. During the breeding season, birds had on average 10% higher whole-body BMR and FMR compared to winter, while their Msum decreased by 7% from winter to breeding. Mass-independent metabolic rates showed a 10% increase in BMR and a 7% decrease in Msum from winter to breeding. Whole-body BMR was correlated with Msum, but this relationship did not hold for mass-independent metabolic rates. The modest seasonal change we observed suggests that great tits in our temperature study area maintain a largely stable energy budget throughout the year, which appears mostly consistent with the reallocation hypothesis.

Host Sex Modulates the Energetics of Pathogen Proliferation and Its Dependence on Environmental Resources

AbstractSex differences in immunity are predicted to underlie much of the frequently observed sex differences in the prevalence or severity of infection. We propose the additional hypothesis that differences in the ability of males and females to acquire and use resources will also affect how readily a pathogen can convert host energy into transmission stages, thereby contributing to sex differences in infection dynamics. To test this we manipulated the resource environment of male and female Daphnia magna by altering the availability of food and then exposed hosts to a bacterial pathogen. We measured the production of transmission spores and virulence via the reduction in life span, together with feeding rates and changes in mass-independent metabolic rate, as a measure of the intake and expenditure of energy during infection. When raised in the presence of high resource levels, females more readily allowed for resources in the environment to be translated to pathogen exploitation, as represented by increased spore production, greater virulence, and higher energy use. In contrast, the traits of infected males were robust to changes in resource availability. High food availability thus exaggerated the degree of sexual dimorphism observed between the sexes. It also modified the relationship between host energy use, virulence, and pathogen spore production for each sex. These results suggest that a host's resource environment can affect how a male or female is exploited by a pathogen and may thus be an additional factor driving sex-specific patterns of disease susceptibility or severity.

Speeding up Growth: Selection for Mass-Independent Maximal Metabolic Rate Alters Growth Rates.

Investigations into relationships between life-history traits, such as growth rate and energy metabolism, typically focus on basal metabolic rate (BMR). In contrast, investigators rarely examine maximal metabolic rate (MMR) as a relevant metric of energy metabolism, even though it indicates the maximal capacity to metabolize energy aerobically, and hence it might also be important in trade-offs. We studied the relationship between energy metabolism and growth in mice (Mus musculus domesticus Linnaeus) selected for high mass-independent metabolic rates. Selection for high mass-independent MMR increased maximal growth rate, increased body mass at 20 weeks of age, and generally altered growth patterns in both male and female mice. In contrast, there was little evidence that the correlated response in mass-adjusted BMR altered growth patterns. The relationship between mass-adjusted MMR and growth rate indicates that MMR is an important mediator of life histories. Studies investigating associations between energy metabolism and life histories should consider MMR because it is potentially as important in understanding life history as BMR.

A strong response to selection on mass-independent maximal metabolic rate without a correlated response in basal metabolic rate.

Metabolic rates are correlated with many aspects of ecology, but how selection on different aspects of metabolic rates affects their mutual evolution is poorly understood. Using laboratory mice, we artificially selected for high maximal mass-independent metabolic rate (MMR) without direct selection on mass-independent basal metabolic rate (BMR). Then we tested for responses to selection in MMR and correlated responses to selection in BMR. In other lines, we antagonistically selected for mice with a combination of high mass-independent MMR and low mass-independent BMR. All selection protocols and data analyses included body mass as a covariate, so effects of selection on the metabolic rates are mass adjusted (that is, independent of effects of body mass). The selection lasted eight generations. Compared with controls, MMR was significantly higher (11.2%) in lines selected for increased MMR, and BMR was slightly, but not significantly, higher (2.5%). Compared with controls, MMR was significantly higher (5.3%) in antagonistically selected lines, and BMR was slightly, but not significantly, lower (4.2%). Analysis of breeding values revealed no positive genetic trend for elevated BMR in high-MMR lines. A weak positive genetic correlation was detected between MMR and BMR. That weak positive genetic correlation supports the aerobic capacity model for the evolution of endothermy in the sense that it fails to falsify a key model assumption. Overall, the results suggest that at least in these mice there is significant capacity for independent evolution of metabolic traits. Whether that is true in the ancestral animals that evolved endothermy remains an important but unanswered question.

Intraspecific variation in flight metabolic rate in the bumblebeeBombus impatiens: repeatability and functional determinants in workers and drones

The evolution of flight energetics requires that phenotypes be variable, repeatable and heritable. We studied intraspecific variation in flight energetics in order to assess the repeatability of flight metabolic rate and wingbeat frequency, as well as the functional basis of phenotypic variation in workers and drones of the bumblebee species Bombus impatiens. We showed that flight metabolic rate and wingbeat frequency were highly repeatable in workers, even when controlling for body mass variation using residual analysis. We did not detect significant repeatability in drones, but a smaller range of variation might have prevented us from finding significant values in our sample. Based on our results and previous findings, we associated the high repeatability of flight phenotypes in workers to the functional links between body mass, thorax mass, wing size, wingbeat frequency and metabolic rate. Moreover, differences between workers and drones were as predicted from these functional associations, where drones had larger wings for their size, lower wingbeat frequency and lower flight metabolic rate. We also investigated thoracic muscle metabolic phenotypes by measuring the activity of carbohydrate metabolism enzymes, and we found positive correlations between mass-independent metabolic rate and the activity of all enzymes measured, but in workers only. When comparing workers and drones that differ in flight metabolic rate, only the activity of the enzymes hexokinase and trehalase showed the predicted differences. Overall, our study indicates that there should be correlated evolution among physiological phenotypes at multiple levels of organization and morphological traits associated with flight.

HOW DOES EVOLUTIONARY VARIATION IN BASAL METABOLIC RATES ARISE? A STATISTICAL ASSESSMENT AND A MECHANISTIC MODEL

Metabolic rates are related to the pace of life. Hence, research into their variability at global scales is of vital importance for several contemporary theories in physiology, ecology, and evolution. Here we evaluated the effect of latitude, climate, primary productivity, habitat aridity, and species trophic habits, on mass-independent basal metabolic rates (BMRs) for 195 rodent species. The aims of this article were twofold. First, we evaluated the predictive power of different statistical models (via a model selection approach), using a dimensional reduction technique on the exogenous factor matrix to achieve a clear interpretation of the selected models. Second, we evaluated three specific predictions derived from a recently proposed hypothesis, herein called the "obligatory heat" model (OHM), for the evolution of BMR. Obtained results indicate that mean/minimum environmental temperature, rainfall/primary productivity and, finally, species trophic habits are, in this order, the major determinants of mass-independent BMR. Concerning the mechanistic causes behind this variation, obtained data agree with the predictions of the OHM: (1) mean annual environmental temperature was the best single predictor of residual variation in BMR, (2) herbivorous species have greater mass-independent metabolic rates, and tend to be present at high-latitude cold environments, than species in other trophic categories.

Metabolic rate in the whip-spider, Damon annulatipes (Arachnida: Amblypygi)

Metabolic rate estimates as well as a measure of their repeatability and response to laboratory acclimation are provided for the amblypygid Damon annulatipes (Wood). This species (mean±S.E. mass: 640±66 mg) shows continuous gas exchange, as might be expected from its possession of book lungs, and at 21 °C has a metabolic rate of 30.22±2.87 μl CO 2 h −1 (≈229.6±21.8 μW, R.Q.=0.72). The intraclass correlation coefficient ( r=0.74–0.89) indicated substantial repeatability in metabolic rate which did not change with laboratory acclimation over a period of 2 weeks. By contrast, absolute metabolic rate declined by c. 16–33%, although this was not a consequence of changes in mass (which were non-significant over the same period). Rather, it appears that a reduction in overall stress or activity in the laboratory might have been responsible for the decline in mass-independent metabolic rate. At the intraspecific level, metabolic rate scaled as μW=342 M 0.857, where mass is in grams. Metabolic rates of this species are in keeping with its sedentary behaviour such that for a given body size they are lower than those of most arthropods (spiders and insects), higher than the very sedentary ticks, and equivalent to scorpions. These findings have implications for the understanding of the evolution of metabolic rates in arthropods.

Respiration and energetics of embryonic development in a large altricial bird, the Australian pelican (Pelecanus conspicillatus).

We examined whether the previously reported low cost of embryonic development in pelicans could be attributed to a more efficient conversion of egg energy to hatchling tissues as a result of high initial egg water content, low embryonic metabolic rate and growth later in incubation than in more precocious species. We therefore determined egg and hatchling composition and the development of embryonic respiration in the Australian pelican Pelecanus conspicillatus, which lays one of the largest eggs (140-210 g) with an altricial developmental mode. The small yolk fraction (21%) is typical of all pelecaniforms; however, we found that intraspecific variability in fresh egg mass was related to water content (principally in the albumen), but independent of yolk mass (mean 13 g dry mass). P. conspicillatus eggs have, on average, 635 kJ of energy, irrespective of egg mass across the whole range of egg mass. The embryonic developmental pattern of O(2) consumption and CO(2) production showed clear plateaus lasting 2-3 days immediately prior to internal pipping, resembling the typical precocial pattern. However, the rate of pre-internal pipping O(2) consumption was low in comparison with that of precocial species of similar egg mass. There is no evidence to support the hypothesis that the observed plateau in rates of O(2) uptake is due to a diffusion limitation of the eggshell gas conductance in this species. Embryonic metabolic rate nearly doubled during the pipping period, but the mass-independent metabolic rate of the hatchling was low in comparison with that of the resting adult. The total O(2) consumed (11 063 ml) is equivalent to 217.3 kJ (or 34% of egg energy) based on indirect calorimetry and the observed respiratory exchange ratio of 0.71. Thus, the cost of development (direct calorimetry) was 0.29 kJ J(-1) in the egg (mean egg mass 168 g), which is one of lowest reported values. As a result, the production efficiency of pelican embryonic development was 61.6%, higher than the average for birds in general (56.9%) and, in particular, of seabirds that have prolonged incubation periods on the basis of egg mass. High efficiency in embryonic development in this species was attained as a result of rapid embryonic growth later in incubation, low hatchling energy density (23.6 kJ g(-1) dry matter) and dry matter content, low embryonic metabolic rate throughout incubation and a shorter than expected incubation period of 33 days (predicted 36 days).

Development of thermoregulation and posthatching growth in the altricial cockatiel Nymphicus hollandicus.

The development of thermoregulation and growth during the nestling period of cockatiel Nymphicus hollandicus were examined in this study. It was hypothesised that, in comparison to other altricial species of similar body mass, cockatiel chicks develop endothermy earlier and consequently have less energy available for growth, resulting in reduced growth rates. While poorly insulated and blind at hatching, cockatiel developed endothermic responses in their first week, and were individually effectively homeothermic (with 75% of adult ability to maintain body temperature during exposure to 20 degrees-25 degrees C), by maintaining high metabolic rates (at all ambient temperatures tested) above the predicted resting rates of an adult of similar body mass before parental brooding ceased (12-13 d). Mass-independent metabolic rates were equivalent to those of fledglings at only 20% of the nestling period (37 d), well before adequate insulation was obtained. The Gompertz growth constants of cockatiel were significantly lower than those of other altricial land birds, which supports the hypothesis of this study.

Seasonal variation in brown adipose tissue mass and lipid droplet size of Sorex minutus, the pygmy shrew; The relationship between morphology and metabolic rate

1. 1. Metabolic rate, brown adipose tissue (BAT) mass and BAT lipid droplet size, were measured in winter-, summer- and spring-acclimatized Pygmy shrews, Sorex minutus. 2. 2. BAT mass changed significantly with season both in relative and absolute terms. Winter-acclimatized shrews had the smallest (135 ± 10 mg) and spring-acclimatized shrews had the heaviest BAT depots (310 ± 28 mg). Relative BAT mass varied between 2–7% depending on season. Median BAT lipid droplet size (μm 2) was smallest in winter-acclimatized (106 μm 2) and largest in spring-acclimatized shrews (326 μm 2). 3. 3. Resting metabolic rate and thermoregulatory thermogenesis were significantly positively related to BAT mass. There was a significant inverse relationship between mass independent metabolic rate and lipid droplet size in all seasonally acclimatized shrews. 4. 4. Winter-acclimatization of BAT in S. minutus is characterised by a decrease in BAT mass signifying a marked utilisation of lipid stores and by a reduction in BAT lipid droplet size, signifying an increase in thermogenic activity.

Dietary and Digestive Constraints on Basal Energy Metabolism in a Small Herbivorous Rodent

McNab (1986, 1988) has hypothesized that mammals using food with low energy content should exhibit basal metabolic rates (BMR) lower than those expected on the basis of their body mass (mb). That is, those species that exploit food with low energy content and/or high cost of digestion tend to have low, mass—independent metabolic rates. To date there is not an experimental test of this pattern. The aim of this work was to examine experimentally the effect of diet quality on BMR, digestive efficiency, and the relationship between digestion and energy expenditure in a small herbivorous mammal. We used as a model the herbivorous caviomorph burrowing rodent Octodon degus (mb nearly 200 g), an inhabitant of semi—arid and mediterranean communities of northern and central Chile. Individuals maintained during 27 wk with a diet high in dietary fiber showed significantly lower BMRs (28%) than those feeding on low fiber. Daily food intake and ingestion rates (energy and dry matter) of individuals under a high—fiber diet were significantly higher than animals maintained with a low—fiber diet. The same pattern was obtained for total feces production and rate of feces production. The total intake and rate of ingestion of proteins were not significantly different between treatments. However, a significantly higher amount of protein was excreted by the individuals exposed to a high—fiber diet. Apparent digestibility of dry matter, energy, and protein were consistently lower in individuals maintained with high fiber. However, nonsignificant differences were observed between gut contents in the two treatments (P > .58), but significantly higher digesta turnover rate was observed in animals exposed to a high—fiber diet (P >.05). A significant correlation was found between digestibility and the basal metabolic rate of individuals (rs = 0.781, P >.01), suggesting that elevated digestibilities on high—quality diets allow increased basal rates of metabolism. We suggest that, although small mammals like degus may select sparsely distributed plants of high quality in their habitat, their capability to drop their metabolic demands may help them meet their nutritional and energy requirements when nutritional conditions in the environment deteriorate.

Basal rate of metabolism and temperature regulation of two desert herbivorous octodontid rodents: Octomys mimax and Tympanoctomys barrerae.

We studied the energetics of two herbivorous desert rodents from South America. The two species had slightly lower basal metabolic rates, lower thermal conductances, and higher temperature differentials than those expected from their body mass. Mass-independent basal rates of metabolism were higher than those reported for seed-eating desert rodents from North America. Our observations support the hypothesis that desert rodents that eat foods with high water content have higher mass-independent metabolic rates than seed-eating desert rodents.

Effect of Gender on the Response to a High Fat Diet in Aging Fischer 344 Rats

The purpose of this study was to describe the effects of high fat (HF) and low fat (LF) diets in male and female Fischer 344 (F344) rats ages 5, 23 and 27 mo. Rats were fed the diet for 3 mo, and then resting metabolic rate, body composition and adipose tissue cellularity were evaluated. Although body mass was greater in rats fed the HF diet, this difference was due to a rapid increase in mass within the first 2 wk. There was no difference in the rate of body mass gain after this period. Resting mass-independent metabolic rate did not significantly differ due to age, diet or gender. In general, percentage fat mass was greater in rats fed the HF diet and in female than in male rats in both diet groups. However, lean body mass (%) was not altered due to diet or age. Cell number of the retroperitoneal depot increased with age and diet between 5 and 23 mo of age in both male and female rats. There was no effect of age, diet or gender on retroperitoneal cell size or gonadal cell number and size. These data suggest that age, gender and diet do not significantly alter the ability of F344 rats to regulate body composition or fat cell proliferation.