scholarly journals Fast ontogenetic growth drives steep evolutionary scaling of metabolic rate

2021 ◽  
Author(s):  
Tommy Norin

Metabolic rate (MR) changes with body mass (BM) as MR = aBMb, where a is a normalisation constant (log–log intercept) and b the scaling exponent (log–log slope). This scaling relationship is fundamental to biology and widely applied, yet a century of research has provided little consensus on why and how steeply metabolic rate scales with body mass. I here show that ontogenetic (within-individual) b can be strongly and positively related to growth rates of juvenile fish when food availability is naturally restricted, with fast growing individuals having steep and near-isometric metabolic scaling (b ≈ 1). I suggest that the steep evolutionary (among-species) scaling also found for fishes (b also approaching 1) is a by-product of natural selection for these fast growing individuals early in ontogeny, and that a weaker relationship between metabolic scaling and growth later in life causes variation in b at lower taxonomic levels (within orders or species). I support these ideas by showing that b within fish orders is linked to natural mortality rates of fish larvae.

2020 ◽  
Vol 223 (21) ◽  
pp. jeb232322 ◽  
Author(s):  
Douglas S. Glazier ◽  
Jeffrey P. Gring ◽  
Jacob R. Holsopple ◽  
Vojsava Gjoni

ABSTRACTAccording to the metabolic theory of ecology, metabolic rate, an important indicator of the pace of life, varies with body mass and temperature as a result of internal physical constraints. However, various ecological factors may also affect metabolic rate and its scaling with body mass. Although reports of such effects on metabolic scaling usually focus on single factors, the possibility of significant interactive effects between multiple factors requires further study. In this study, we show that the effect of temperature on the ontogenetic scaling of resting metabolic rate of the freshwater amphipod Gammarus minus depends critically on habitat differences in predation regime. Increasing temperature tends to cause decreases in the metabolic scaling exponent (slope) in population samples from springs with fish predators, but increases in population samples from springs without fish. Accordingly, the temperature sensitivity of metabolic rate is not only size-specific, but also its relationship to body size shifts dramatically in response to fish predators. We hypothesize that the dampened effect of temperature on the metabolic rate of large adults in springs with fish, and of small juveniles in springs without fish are adaptive evolutionary responses to differences in the relative mortality risk of adults and juveniles in springs with versus without fish predators. Our results demonstrate a complex interaction among metabolic rate, body mass, temperature and predation regime. The intraspecific scaling of metabolic rate with body mass and temperature is not merely the result of physical constraints related to internal body design and biochemical kinetics, but rather is ecologically sensitive and evolutionarily malleable.


2019 ◽  
Vol 286 (1911) ◽  
pp. 20191693 ◽  
Author(s):  
Boël Mélanie ◽  
Romestaing Caroline ◽  
Voituron Yann ◽  
Roussel Damien

Metabolic activity sets the rates of individual resource uptake from the environment and resource allocations. For this reason, the relationship with body size has been heavily documented from ecosystems to cells. Until now, most of the studies used the fluxes of oxygen as a proxy of energy output without knowledge of the efficiency of biological systems to convert oxygen into ATP. The aim of this study was to examine the allometry of coupling efficiency (ATP/O) of skeletal muscle mitochondria isolated from 12 mammal species ranging from 6 g to 550 kg. Mitochondrial efficiencies were measured at different steady states of phosphorylation. The efficiencies increased sharply at higher metabolic rates. We have shown that body mass dependence of mitochondrial efficiency depends on metabolic intensity in skeletal muscles of mammals. Mitochondrial efficiency positively depends on body mass when mitochondria are close to the basal metabolic rate; however, the efficiency is independent of body mass at the maximum metabolic rate. As a result, it follows that large mammals exhibit a faster dynamic increase in ATP/O than small species when mitochondria shift from basal to maximal activities. Finally, the invariant value of maximal coupling efficiency across mammal species could partly explain why scaling exponent values are very close to 1 at maximal metabolic rates.


ISRN Zoology ◽  
2012 ◽  
Vol 2012 ◽  
pp. 1-9 ◽  
Author(s):  
ZiMian Wang ◽  
Junyi Zhang ◽  
Zhiliang Ying ◽  
Steven B. Heymsfield

Background. Kleiber’s law describes the quantitative association between whole-body resting energy expenditure (REE, in kcal/d) and body mass (M, in kg) across mature mammals as REE =70.0×M0.75. The basis of this empirical function is uncertain. Objectives. The study objective was to establish an organ-tissue level REE model across mammals and to explore the body composition and physiologic basis of Kleiber’s law. Design. We evaluated the hypothesis that REE in mature mammals can be predicted by a combination of two variables: the mass of individual organs/tissues and their corresponding specific resting metabolic rates. Data on the mass of organs with high metabolic rate (i.e., liver, brain, heart, and kidneys) for 111 species ranging in body mass from 0.0075 (shrew) to 6650 kg (elephant) were obtained from a literature review. Results. REEp predicted by the organ-tissue level model was correlated with body mass (correlation r=0.9975) and resulted in the function REEp=66.33×M0.754, with a coefficient and scaling exponent, respectively, close to 70.0 and 0.75 (P>0.05) as observed by Kleiber. There were no differences between REEp and REEk calculated by Kleiber’s law; REEp was correlated (r=0.9994) with REEk. The mass-specific REEp, that is, (REE/M)p, was correlated with body mass (r=0.9779) with a scaling exponent −0.246, close to −0.25 as observed with Kleiber’s law. Conclusion. Our findings provide new insights into the organ/tissue energetic components of Kleiber’s law. The observed large rise in REE and lowering of REE/M from shrew to elephant can be explained by corresponding changes in organ/tissue mass and associated specific metabolic rate.


1987 ◽  
Vol 253 (1) ◽  
pp. R195-R199 ◽  
Author(s):  
J. P. Butler ◽  
H. A. Feldman ◽  
J. J. Fredberg

In several recent article, Heusner used dimensional reasoning to derive important biological conclusions regarding the scaling of metabolism with body mass [Respir. Physiol. 48: 13-25, 1982; J. Appl. Physiol. 54: 867-873, 1983; Am. J. Physiol. 246 (Regulatory Integrative Comp. Physiol. 15): R839-R845, 1984]. We demonstrate errors in the derivation and show that dimensional analysis, correctly applied, not only fails to determine the mass scaling exponent but also fails to constrain the relationship to a power law at all.


2008 ◽  
Vol 86 (8) ◽  
pp. 890-899 ◽  
Author(s):  
M. Kjeld ◽  
Ö. Ólafsson

Hematocrit (HCT), blood hemoglobin (HGB), and serum concentrations of 14 commonly measured serum constituents in mammals were extracted from 131 publications published within the last 35 years and then subjected to allometric study (Y = aWb, where Y is the characteristic studied, W is body mass, and b is the scaling exponent). HCT and HGB values decreased (b < 0; p < 0.001) with body mass (W), as did serum K+, glucose, triglycerides, and urea values. In contrast, serum total protein and creatinine values increased (b > 0; p < 0.02 and p < 0.001, respectively) with W. The associations of HCT, HGB, glucose, triglycerides, and urea values with W may be assumed to coincide with the well-known reduction of metabolic rate per unit mass with increasing W of mammals. The decrease in serum K+values (p < 0.001) has yet to be adequately explained. Despite the ratio of muscle mass and W being constant for large and small mammals, serum values of creatinine rose (b = 0.14; p < 0.0001) with W. This suggests increased phosphocreatine turnover in muscles with W, which in turn might be connected to the increased efficiency reported for leg muscles in larger animals and, conceivably, might affect the measurement of metabolic rate and hence its scaling in mammals.


PeerJ ◽  
2020 ◽  
Vol 8 ◽  
pp. e9242
Author(s):  
Qian Li ◽  
Xiaoling Zhu ◽  
Wei Xiong ◽  
Yanqiu Zhu ◽  
Jianghui Zhang ◽  
...  

The surface area (SA) of organs and cells may vary with temperature, which changes the SA exchange limitation on metabolic flows as well as the influence of temperature on metabolic scaling. The effect of SA change can intensify (when the effect is the same as that of temperature) or compensate for (when the effect is the opposite of that of temperature) the negative effects of temperature on metabolic scaling, which can result in multiple patterns of metabolic scaling with temperature among species. The present study aimed to examine whether metabolic scaling in black carp changes with temperature and to identify the link between metabolic scaling and SA at the organ and cellular levels at different temperatures. The resting metabolic rate (RMR), gill surface area (GSA) and red blood cell (RBC) size of black carp with different body masses were measured at 10 °C and 25 °C, and the scaling exponents of these parameters were compared. The results showed that both body mass and temperature independently affected the RMR, GSA and RBC size of black carp. A consistent scaling exponent of RMR (0.764, 95% CI [0.718–0.809]) was obtained for both temperatures. The RMR at 25 °C was 2.7 times higher than that at 10 °C. At both temperatures, the GSA scaled consistently with body mass by an exponent of 0.802 (95% CI [0.759–0.846]), while RBC size scaled consistently with body mass by an exponent of 0.042 (95% CI [0.010–0.075]). The constant GSA scaling can explain the constant metabolic scaling as temperature increases, as metabolism may be constrained by fluxes across surfaces. The GSA at 10 °C was 1.2 times higher than that at 25 °C, which suggests that the constraints of GSA on the metabolism of black carp is induced by the higher temperature. The RBC size at 10 °C was 1.1 times higher than that at 25 °C. The smaller RBC size (a larger surface-to-volume ratio) at higher temperature suggests an enhanced oxygen supply and a reduced surface boundary limit on bR, which offset the negative effect of temperature on bR.


Author(s):  
Mofei Wang ◽  
Shigeta Mori ◽  
Yoko Kurosawa ◽  
Juan Pedro Ferrio ◽  
Keiko Yamaji ◽  
...  

AbstractBoth Moso bamboo (Phyllostachys pubescens) and tree forests have a large biomass; they are considered to play an important role in ecosystem carbon budgets. The scaling relationship between individual whole-shoot (i.e., aboveground parts) respiration and whole-shoot mass provides a clue for comparing the carbon budgets of Moso bamboo and tree forests. However, nobody has empirically demonstrated whether there is a difference between these forest types in the whole-shoot scaling relationship. We developed whole-shoot chambers and measured the shoot respiration of 58 individual mature bamboo shoots from the smallest to the largest in a Moso bamboo forest, and then compared them with that of 254 tree shoots previously measured. For 30 bamboo shoots, we measured the respiration rate of leaves, branches, and culms. We found that the scaling exponent of whole-shoot respiration of bamboo fitted by a simple power function on a log–log scale was 0.843 (95 % CI 0.797–0.885), which was consistent with that of trees, 0.826 (95 % CI 0.799–0.851), but higher than 3/4, the value typifying the Kleiber’s rule. The respiration rates of leaves, branches, and culms at the whole-shoot level were proportional to their mass, revealing a constant mean mass-specific respiration of 1.19, 0.224, and 0.0978 µmol CO2 kg− 1 s− 1, respectively. These constant values suggest common traits of organs among physiologically integrated ramets within a genet. Additionally, the larger the shoots, the smaller the allocation of organ mass to the metabolically active leaves, and the larger the allocation to the metabolically inactive culms. Therefore, these shifts in shoot-mass partitioning to leaves and culms caused a negative metabolic scaling of Moso bamboo shoots. The observed convergent metabolic scaling of Moso bamboo and trees may facilitate comparisons of the ecosystem carbon budgets of Moso bamboo and tree forests.


2020 ◽  
Vol 287 (1927) ◽  
pp. 20200488 ◽  
Author(s):  
Wilco C. E. P. Verberk ◽  
Piero Calosi ◽  
François Brischoux ◽  
John I. Spicer ◽  
Theodore Garland ◽  
...  

Diving as a lifestyle has evolved on multiple occasions when air-breathing terrestrial animals invaded the aquatic realm, and diving performance shapes the ecology and behaviour of all air-breathing aquatic taxa, from small insects to great whales. Using the largest dataset yet assembled, we show that maximum dive duration increases predictably with body mass in both ectotherms and endotherms. Compared to endotherms, ectotherms can remain submerged for longer, but the mass scaling relationship for dive duration is much steeper in endotherms than in ectotherms. These differences in diving allometry can be fully explained by inherent differences between the two groups in their metabolic rate and how metabolism scales with body mass and temperature. Therefore, we suggest that similar constraints on oxygen storage and usage have shaped the evolutionary ecology of diving in all air-breathing animals, irrespective of their evolutionary history and metabolic mode. The steeper scaling relationship between body mass and dive duration in endotherms not only helps explain why the largest extant vertebrate divers are endothermic rather than ectothermic, but also fits well with the emerging consensus that large extinct tetrapod divers (e.g. plesiosaurs, ichthyosaurs and mosasaurs) were endothermic.


2010 ◽  
Vol 6 (5) ◽  
pp. 715-717 ◽  
Author(s):  
Dong-Liang Cheng ◽  
Tao Li ◽  
Quan-Lin Zhong ◽  
Gen-Xuan Wang

The WBE theory proposed by West, Brown and Enquist predicts that larger plant respiration rate, R , scales to the three-quarters power of body size, M . However, studies on the R versus M relationship for larger plants (i.e. trees larger than saplings) have not been reported. Published respiration rates of field-grown trees (saplings and larger trees) were examined to test this relationship. Our results showed that for larger trees, aboveground respiration rates R A scaled as the 0.82-power of aboveground biomass M A , and that total respiration rates R T scaled as the 0.85-power of total biomass M T , both of which significantly deviated from the three-quarters scaling law predicted by the WBE theory, and which agreed with 0.81–0.84-power scaling of biomass to respiration across the full range of measured tree sizes for an independent dataset reported by Reich et al . (Reich et al . 2006 Nature 439 , 457–461). By contrast, R scaled nearly isometrically with M in saplings. We contend that the scaling exponent of plant metabolism is close to unity for saplings and decreases (but is significantly larger than three-quarters) as trees grow, implying that there is no universal metabolic scaling in plants.


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