scholarly journals Scaling of organ masses in mammals and birds: phylogenetic signal and implications for metabolic rate scaling

ZooKeys ◽  
2020 ◽  
Vol 982 ◽  
pp. 149-159
Author(s):  
Andrzej Antoł ◽  
Jan Kozłowski

The persistent enigma of why the whole-body metabolic rate increases hypoallometrically with body mass should be solved on both the ultimate and proximate levels. The proximate mechanism may involve hyperallometric scaling of metabolically inert tissue/organ masses, hypoallometric scaling of metabolically expensive organ masses, a decrease in mass-specific metabolic rates of organs or a combination of these three factors. Although there are literature data on the tissue/organ masses scaling, they do not consider phylogenetic information. Here, we analyse the scaling of tissue/organ masses in a sample of 100 mammalian and 22 bird species with a phylogenetically informed method (PGLS) to address two questions: the role of phylogenetic differences in organ/tissue size scaling and the potential role of organ/tissue mass scaling in interspecific metabolic rate scaling. Strong phylogenetic signal was found for the brain, kidney, spleen and stomach mass in mammals but only for the brain and leg muscle in birds. Metabolically relatively inert adipose tissue scales isometrically in both groups. The masses of energetically expensive visceral organs scale hypoallometrically in mammals, with the exception of lungs, with the lowest exponent for the brain. In contrast, only brain mass scales hypoallometrically in birds, whereas other tissues and organs scale isometrically or almost isometrically. Considering that the whole-body metabolic rate scales more steeply in mammals than in birds, the mass-specific metabolic rate of visceral organs must decrease with body mass much faster in birds than in mammals. In general, studying whole-body metabolic rate is not adequate for explaining its scaling, and measuring metabolic rates of organs, together with their contribution to body mass, is urgently required.

2019 ◽  
Author(s):  
Andrzej Antoł ◽  
Jan Kozłowski

The persistent enigma of why the whole-body metabolic rate increases hypoallometrically with body mass should be solved on both the ultimate and proximate levels. The proximate mechanism may involve hyperallometric scaling of metabolically relatively inert tissue/organ masses, hypoallometric scaling of metabolically expensive organ masses, a decrease in mass-specific metabolic rates of organs or, more likely, a combination of these three factors. Although there are in data in the literature on the scaling of tissue/organ masses, they do not take phylogenetic information into account. Here, we analyse the scaling of tissue/organ masses in a sample of 100 mammalian species and 22 bird species with a phylogenetically informed method (PGLS) to address two questions: the role of phylogenetic signal in organ/tissue size scaling and the potential role of organ/tissue mass scaling in interspecific metabolic rate scaling. Strong phylogenetic signal was found for the brain, kidney, spleen and stomach mass in mammals but only for the brain and leg muscle in birds. Metabolically relatively inert adipose tissue scales isometrically in both groups. The masses of energetically expensive visceral organs scale hypoallometrically in mammals, with the exception of lungs, with the lowest exponent occurring for the brain. In contrast, only brain mass scales hypoallometrically in birds, whereas other tissues and organs scale isometrically or almost isometrically. Taking into account that the whole-body metabolic rate scales more steeply in mammals than in birds, the mass-specific metabolic rate of visceral organs must decrease with body mass at a much faster rate in birds than in mammals. To explain this striking difference, there is an urgent need to study the metabolic rates of tissues and organs to supplement measurements of the whole-body metabolic rate.


2018 ◽  
Vol 314 (4) ◽  
pp. R563-R573 ◽  
Author(s):  
Mun Aw ◽  
Tamara M. Armstrong ◽  
C. Michele Nawata ◽  
Sarah N. Bodine ◽  
Jeeeun J. Oh ◽  
...  

In general, the mammalian whole body mass-specific metabolic rate correlates positively with maximal urine concentration (Umax) irrespective of whether or not the species have adapted to arid or mesic habitat. Accordingly, we hypothesized that the thick ascending limb (TAL) of a rodent with markedly higher whole body mass-specific metabolism than rat exhibits a substantially higher TAL metabolic rate as estimated by Na+-K+-ATPase activity and Na+-K+-ATPase α1-gene and protein expression. The kangaroo rat inner stripe of the outer medulla exhibits significantly higher mean Na+-K+-ATPase activity (~70%) compared with two rat strains (Sprague-Dawley and Munich-Wistar), extending prior studies showing rat activity exceeds rabbit. Furthermore, higher expression of Na+-K+-ATPase α1-protein (~4- to 6-fold) and mRNA (~13-fold) and higher TAL mitochondrial volume density (~20%) occur in the kangaroo rat compared with both rat strains. Rat TAL Na+-K+-ATPase α1-protein expression is relatively unaffected by body hydration status or, shown previously, by dietary Na+, arguing against confounding effects from two unavoidably dissimilar diets: grain-based diet without water (kangaroo rat) or grain-based diet with water (rat). We conclude that higher TAL Na+-K+-ATPase activity contributes to relationships between whole body mass-specific metabolic rate and high Umax. More vigorous TAL Na+-K+-ATPase activity in kangaroo rat than rat may contribute to its steeper Na+ and urea axial concentration gradients, adding support to a revised model of the urine concentrating mechanism, which hypothesizes a leading role for vigorous active transport of NaCl, rather than countercurrent multiplication, in generating the outer medullary axial osmotic gradient.


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.


2020 ◽  
Vol 223 (21) ◽  
pp. jeb231993
Author(s):  
Kimberley J. Mathot ◽  
Eva M. A. Kok ◽  
Piet van den Hout ◽  
Anne Dekinga ◽  
Theunis Piersma

ABSTRACTMass regulation in birds is well documented. For example, birds can increase body mass in response to lower availability and/or predictability of food and decrease body mass in response to increased predation danger. Birds also demonstrate an ability to maintain body mass across a range of food qualities. Although the adaptive significance of mass regulation has received a great deal of theoretical and empirical attention, the mechanisms by which birds achieve this have not. Several non-exclusive mechanisms could facilitate mass regulation in birds. Birds could regulate body mass by adjusting food intake (dieting), activity, baseline energetic requirements (basal metabolic rate), mitochondrial efficiency or assimilation efficiency. Here, we present the results of two experiments in captive red knots (Calidris canutus islandica) that assess three of these proposed mechanisms: dieting, activity and up- and down-regulation of metabolic rate. In the first experiment, knots were exposed to cues of predation risk that led them to exhibit presumably adaptive mass loss. In the second experiment, knots maintained constant body mass despite being fed alternating high- and low-quality diets. In both experiments, regulation of body mass was achieved through a combination of changes in food intake and activity. Both experiments also provide some evidence for a role of metabolic adjustments. Taken together, these two experiments demonstrate that fine-scale management of body mass in knots is achieved through multiple mechanisms acting simultaneously.


2019 ◽  
Vol 3 (Supplement_1) ◽  
pp. S835-S835
Author(s):  
Charnae A Henry-Smith ◽  
Xianlin Han

Abstract Alzheimer’s disease is a progressive brain disease that slowly destroys memory and thinking skills. Alzheimer’s is characterized by an increase in Aβ plaques , and tau tangles. Neurons in the brain have axons covered in myelin sheath that connect microglia and astrocytes. The myelin sheath is composed of about 70% lipid composition; Sulfatide contributing to 30% overall. Sulfatide changes the morphology of primary microglia to their activated form. To study the role of microglia activation and sulfatide levels, three different mouse models were created: APP KI mice, CST Whole Body Ko mice, and cCST (conditional) KO. In order to create the genotype of the APP KI mice, a breeding mouse line was created. The APP KI gene had to be introduced in Plp1-Cre and cCST KO crossed mice to receive a working mouse model. During the duration of breeding for the APP KI mice, a preliminary experiment was performed on the CST KO mice. These mice were given the PLX3397 diet with the aim to remove the microglia and to see the effect of Aβ plaques. The PLX3397 will reduce the microglia targeting the CSF1R. After consuming the diet, the mice were harvested to collect tissues from the brain and spinal cord. Lipidomics and immunohistology were performed. In conclusion, we will continue the breeding of the CST flox/flox / Plp1-Cre / APP KI mice, and the drug dosage and treatment to be used in our APP KI mice will be based on preliminary data from our CST mice.


2016 ◽  
Vol 60 ◽  
pp. 132-139 ◽  
Author(s):  
Nigel R. Andrew ◽  
Behnaz Ghaedi ◽  
Berlizé Groenewald

2007 ◽  
Vol 292 (6) ◽  
pp. R2115-R2121 ◽  
Author(s):  
Melanie F. Brown ◽  
Tyson P. Gratton ◽  
Jeffrey. A. Stuart

The allometric scaling of metabolic rate with organism body mass can be partially accounted for by differences in cellular metabolic rates. For example, hepatocytes isolated from horses consume almost 10-fold less oxygen per unit time as mouse hepatocytes [Porter and Brand, Am J Physiol Regul Integr Comp Physiol 269: R226–R228, 1995]. This could reflect a genetically programmed, species-specific, intrinsic metabolic rate set point, or simply the adaptation of individual cells to their particular in situ environment (i.e., within the organism). We studied cultured cell lines derived from 10 mammalian species with donor body masses ranging from 5 to 600,000 g to determine whether cells propagated in an identical environment (media) exhibited metabolic rate scaling. Neither metabolic rate nor the maximal activities of key enzymes of oxidative or anaerobic metabolism scaled significantly with donor body mass in cultured cells, indicating the absence of intrinsic, species-specific, cellular metabolic rate set points. Furthermore, we suggest that changes in the metabolic rates of isolated cells probably occur within 24 h and involve a reduction of cellular metabolism toward values observed in lower metabolic rate organisms. The rate of oxygen delivery has been proposed to limit cellular metabolic rates in larger organisms. To examine the effect of oxygen on steady-state cellular respiration rates, we grew cells under a variety of physiologically relevant oxygen regimens. Long-term exposure to higher medium oxygen levels increased respiration rates of all cells, consistent with the hypothesis that higher rates of oxygen delivery in smaller mammals might increase cellular metabolic rates.


1997 ◽  
Vol 273 (2) ◽  
pp. R777-R783 ◽  
Author(s):  
A. A. Romanovsky ◽  
V. A. Kulchitsky ◽  
C. T. Simons ◽  
N. Sugimoto ◽  
M. Szekely

The repeatedly observed attenuation of fever in vagotomized rats has been accepted as evidence of an essential role of vagal afferents in the transduction of pyrogenic signals from the periphery to the brain. If, however, the general condition of a vagotomized animal is poor (the usual case) and accompanied by malnutrition and body mass loss (common complications of vagotomy), the febrile responsiveness can be suppressed not because of the lack of vagal afferentation, but rather secondarily to a malnutrition-associated thermogenic incompetence. In the present study, we addressed this dilemma. Male Wistar rats were subjected to subdiaphragmatic vagotomy (or sham surgery) and, 24 days later, catheterized in the jugular vein. Postsurgically, the rats were closely watched and fed highly palatable food. Their febrile responsiveness [colonic (Tc) and tail skin (Tsk) temperature responses] to Escherichia coli lipopolysaccharide (LPS: 1 microgram/kg i.v.) was tested on day 27 postvagotomy. To verify the completeness of vagotomy, each rat was food deprived for 24 h and then euthanized; its stomach's evacuatory function was assessed by weighing the organ. One month postsurgery, both food consumption and body mass of the vagotomized rats (33 +/- 2 g/day and 313 +/- 4 g, respectively) were similar to the control values (30 +/- 1 g/day and 315 +/- 8 g). In the sham rats, LPS induced a monophasic Tc rise of 0.5 +/- 0.3 degree C at 70 min postinjection (peak), preceded by a fall in Tsk. Neither this Tsk fall (tail skin vasoconstriction) nor the resultant fever occurred in the vagotomized rats; at 70 min, Tc change was -0.1 +/-0.1 degree C. The gastric mass (4.1 +/- 0.5 g in the vagotomized vs. 1.8 +/- 0.1 g in sham rats) indicated the effectiveness of vagotomy. In sum, although the vagotomy-associated malnutrition was successfully prevented with special perioperative care, the vagotomized animals still did not respond to LPS with fever. Malnutrition is, therefore, unlikely to constitute the main reason of the febrile irresponsiveness of vagotomized rats.


1997 ◽  
Vol 75 (11) ◽  
pp. 1781-1789 ◽  
Author(s):  
Patrice Boily ◽  
David M. Lavigne

Resting metabolic rate (RMR) data obtained from five juvenile and three adult female grey seals (Halichoerus grypus) in captivity over a period of 3.5 years were examined for developmental and seasonal changes. Three juveniles exhibited a significant relationship between log10 RMR and log10 mass, with individual slopes ranging from 0.42 to 1.62. Two of these exhibited a significant relationship between log10 RMR and log10 age. The remaining two juveniles and the three adults exhibited no significant relationship between RMR and body mass. With increasing size and age, RMRs of juveniles approached predicted values for adult mammals, but the large variation made it difficult to establish the precise age at which they achieved an adult-like RMR. RMRs of adults and juveniles exhibited marked seasonal changes. In juveniles, seasonal changes in RMR were limited to the annual moult, when the average RMR was 35% higher than during the rest of the year. In adults, changes in RMR were not limited to the time of the annual moult; rather, RMR was lower (by up to 50%) in the summer than during other seasons.


2000 ◽  
Vol 203 (6) ◽  
pp. 1003-1016 ◽  
Author(s):  
M.J. Donohue ◽  
D.P. Costa ◽  
M.E. Goebel ◽  
J.D. Baker

Young pinnipeds, born on land, must eventually enter the water to feed independently. The aim of this study was to examine developmental factors that might influence this transition. The ontogeny of metabolic rate and thermoregulation in northern fur seal, Callorhinus ursinus, pups was investigated at two developmental stages in air and water using open-circuit respirometry. Mean in-air resting metabolic rate (RMR) increased significantly from 113+/−5 ml O(2)min(−)(1) (N=18) pre-molt to 160+/−4 ml O(2)min(−)(1) (N=16; means +/− s.e.m.) post-molt. In-water, whole-body metabolic rates did not differ pre- and post-molt and were 2.6 and 1.6 times in-air RMRs respectively. Mass-specific metabolic rates of pre-molt pups in water were 2.8 times in-air rates. Mean mass-specific metabolic rates of post-molt pups at 20 degrees C in water and air did not differ (16.1+/−1.7 ml O(2)min(−)(1)kg(−)(1); N=10). In-air mass-specific metabolic rates of post-molt pups were significantly lower than in-water rates at 5 degrees C (18.2+/−1.1 ml O(2)min(−)(1)kg(−)(1); N=10) and 10 degrees C (19.4+/−1.7 ml O(2)min(−)(1)kg(−)(1); N=10; means +/− s.e.m.). Northern fur seal pups have metabolic rates comparable with those of terrestrial mammalian young of similar body size. Thermal conductance was independent of air temperature, but increased with water temperature. In-water thermal conductance of pre-molt pups was approximately twice that of post-molt pups. In-water pre-molt pups matched the energy expenditure of larger post-molt pups while still failing to maintain body temperature. Pre-molt pups experience greater relative costs when entering the water regardless of temperature than do larger post-molt pups. This study demonstrates that the development of thermoregulatory capabilities plays a significant role in determining when northern fur seal pups enter the water.


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