scholarly journals The performing animal: causes and consequences of body remodeling and metabolic adjustments in red knots facing contrasting thermal environments

2017 ◽  
Vol 313 (2) ◽  
pp. R120-R131 ◽  
Author(s):  
François Vézina ◽  
Alexander R. Gerson ◽  
Christopher G. Guglielmo ◽  
Theunis Piersma

Using red knots ( Calidris canutus) as a model, we determined how changes in mass and metabolic activity of organs relate to temperature-induced variation in metabolic performance. In cold-acclimated birds, we expected large muscles and heart as well as improved oxidative capacity and lipid transport, and we predicted that this would explain variation in maximal thermogenic capacity (Msum). We also expected larger digestive and excretory organs in these same birds and predicted that this would explain most of the variation in basal metabolic rate (BMR). Knots kept at 5°C were 20% heavier and maintained 1.5 times more body fat than individuals kept in thermoneutral conditions (25°C). The birds in the cold also had a BMR up to 32% higher and a Msum 16% higher than birds at 25°C. Organs were larger in the cold, with muscles and heart being 9–20% heavier and digestive and excretory organs being 21–36% larger than at thermoneutrality. Rather than the predicted digestive and excretory organs, the cold-induced increase in BMR correlated with changes in mass of the heart, pectoralis, and carcass. Msum varied positively with the mass of the pectoralis, supracoracoideus, and heart, highlighting the importance of muscles and cardiac function in cold endurance. Cold-acclimated knots also expressed upregulated capacity for lipid transport across mitochondrial membranes [carnitine palmitoyl transferase (CPT)] in their pectoralis and leg muscles, higher lipid catabolism capacity in their pectoralis muscles [β-hydroxyacyl CoA-dehydrogenase (HOAD)], and elevated oxidative capacity in their liver and kidney (citrate synthase). These adjustments may have contributed to BMR through changes in metabolic intensity. Positive relationships among Msum, CPT, and HOAD in the heart also suggest indirect constraints on thermogenic capacity through limited cardiac capacity.

1987 ◽  
Vol 252 (4) ◽  
pp. R786-R793 ◽  
Author(s):  
R. L. Marsh ◽  
T. L. Taigen

The muscle features that accommodate the extraordinarily high aerobic respiration during calling by the gray tree frog Hyla versicolor were examined. We compared the muscles used for calling by males (external and internal obliques and laryngeal muscles) with the homologous muscles of females and with the leg muscles of males and females. The leg muscles consisted of 75% by volume fast glycolytic fibers, a composition typical of other muscles described in anuran amphibians. In contrast the calling muscles of males consisted of 100% fast oxidative fibers and had citrate synthase (CS) activities among the highest recorded for ectothermic vertebrates, 65-80 mumol X min-1 X g fresh mass-1. We also noted a strong sexual dimorphism in size and oxidative capacity of these muscles. The external and internal obliques of females weighed an order of magnitude less than the corresponding muscles of males and had CS activities of only 6 mumol X min-1 X g-1. Morphometric measurements of transmission electron micrographs revealed that the calling muscles of males contained high mitochondrial densities (approximately 20% of fiber volume) and capillary densities (approximately 700 mm-2) compared with a representative hindlimb muscle, the sartorius (mitochondrial density, 6% of fiber volume; capillary density, 230 mm-2). These frog muscles, which operate at approximately 20 degrees C, have lower capillary densities per mitochondrial volume than are found in mammalian muscles that function at higher temperatures.


1982 ◽  
Vol 242 (5) ◽  
pp. R563-R569 ◽  
Author(s):  
R. L. Marsh ◽  
W. R. Dawson

Concentration of ([Glc]) and turnover (Ro) of plasma glucose, concentration of free fatty acids in plasma ([FFA]), and concentration of glycogen in muscle and liver were measured in freshly captured summer- and winter-acclimatized American goldfinches (Carduelis tristis). These birds were acutely exposed to one of three thermal regimes: 1) “thermoneutral,” 30 degrees C in air, 2) “cold,” -15 degrees C in air, and 3) “severe cold,” 0 degrees C in 79% He and 21% O2. Additionally, the activities of citrate synthase (CS), phosphofructokinase (PFK), and beta-hydroxyacyl-CoA dehydrogenase (HOAD) were measured in pectoralis and leg muscles of winter and summer birds. Ro for goldfinches at 30 degrees C is unchanged between winter and summer, whereas it is 25% lower at -15 degrees C in winter than in summer birds, even though rates of heat production are similar. Additionally, winter animals depleted muscle glycogen at slower rates than summer individuals when exposed to “cold” or “severe cold.” [Glc] and [FFA] for each test regime did not vary between seasons. The activity of the beta-oxidative enzyme HOAD is the pectoralis muscle (the main thermogenic tissue) increases by 50% from summer to winter, but the activities of PFK and CS remain essentially constant. We conclude that the ability to restrict carbohydrate use under cold stress is a component of the winter acclimatization process in the American goldfinch. One mechanism which might foster this ability in the increase in beta-oxidative capacity of the flight muscles, permitting a greater reliance on fatty acids by winter animals during cold-induced thermogenesis.


1991 ◽  
Vol 161 (1) ◽  
pp. 383-403 ◽  
Author(s):  
A. Tullis ◽  
B. A. Block ◽  
B. D. Sidell

Maximal in vitro activities of key metabolic enzymes were measured in brain and eye heaters of five species of scombroid fishes. Istiophorid billfishes (blue marlin, striped marlin and Mediterranean spearfish), xiphiid billfishes (Pacific and Mediterranean stocks) and a scombrid fish (butterfly mackerel) were included in the analysis. Our main objectives were (1) to assess the maximum possible substrate flux in heater tissue, and (2) to determine what metabolic substrates could fuel heat production. Heater tissue of all scombroids examined showed extremely high oxidative capacity. Activities of citrate synthase, a commonly measured index of oxidative metabolism, included the highest value ever reported for vertebrate tissue. In most billfishes, citrate synthase activities were similar to or higher than those found for mammalian cardiac and avian flight muscle. Marker enzymes for aerobic carbohydrate metabolism (hexokinase) and fatty acid metabolism (carnitine palmitoyltransferase and 3-hydroxyacyl-CoA dehydrogenase) also displayed extraordinarily high activities. Activities of carnitine palmitoyltransferase measured in heater organs were among the highest reported for vertebrates. These results indicate that heat production could be fueled aerobically by either lipid or carbohydrate metabolism. Inter- and intraspecifically, heater organs of fishes from the colder Mediterranean waters had a higher aerobic capacity and, hence, a greater heat-generating potential, than fishes from the warmer waters of the Pacific. This difference may be attributed to different thermal environments or it may result from allometry, since fishes caught in the Mediterranean were considerably smaller than those caught in the Pacific.


2002 ◽  
Vol 282 (3) ◽  
pp. E593-E600 ◽  
Author(s):  
Gregory R. Steinberg ◽  
Arend Bonen ◽  
David J. Dyck

Leptin acutely increases fatty acid (FA) oxidation and triacylglycerol (TG) hydrolysis and decreases TG esterification in oxidative rodent muscle. However, the effects of chronic leptin administration on FA metabolism in skeletal muscle have not been examined. We hypothesized that chronic leptin treatment would enhance TG hydrolysis as well as the capacity to oxidize FA in soleus (SOL) muscle. Female Sprague-Dawley rats were infused for 2 wk with leptin (LEPT; 0.5 mg · kg−1 · day−1) by use of subcutaneously implanted miniosmotic pumps. Control (AD-S) and pair-fed (PF-S) animals received saline-filled implants. Subsequently, FA metabolism was monitored for 45 min in isolated, resting, and contracting (20 tetani/min) SOL muscles by means of pulse-chase procedures. Food intake (−33 ± 2%, P < 0.01) and body mass (−12.5 ± 4%, P = 0.01) were reduced in both LEPT and PF-S animals. Leptin levels were elevated (+418 ± 7%, P < 0.001) in treated animals but reduced in PF-S animals (−73 ± 8%, P< 0.05) relative to controls. At rest, TG hydrolysis was increased in leptin-treated rats (1.8 ± 2.2, AD-S vs. 23.5 ± 8.1 nmol/g wet wt, LEPT; P < 0.001). In contracting SOL muscles, TG hydrolysis (1.5 ± 0.6, AD-S vs. 3.6 ± 1.0 μmol/g wet wt, LEPT; P = 0.02) and palmitate oxidation (18.3 ± 6.7, AD-S vs. 45.7 ± 9.9 nmol/g wet wt, LEPT; P < 0.05) were both significantly increased by leptin treatment. Chronic leptin treatment had no effect on TG esterification either at rest or during contraction. Markers of overall (citrate synthase) and FA (hydroxyacyl-CoA dehydrogenase) oxidative capacity were unchanged with leptin treatment. Protein expression of hormone-sensitive lipase (HSL) was also unaltered following leptin treatment. Thus leptin-induced increases in lipolysis are likely due to HSL activation (i.e., phosphorylation). Increased FA oxidation secondary to chronic leptin treatment is not due to an enhanced oxidative capacity and may be a result of enhanced flux into the mitochondrion (i.e., carnitine palmitoyltransferase I regulation) or electron transport uncoupling (i.e., uncoupling protein-3 expression).


2007 ◽  
Vol 39 (Supplement) ◽  
pp. S103
Author(s):  
Ryan G. Larsen ◽  
Ian R. Lanza ◽  
Damien M. Callahan ◽  
Jane A. Kent-Braun

1989 ◽  
Vol 256 (4) ◽  
pp. H1110-H1116 ◽  
Author(s):  
D. C. Poole ◽  
O. Mathieu-Costello ◽  
J. B. West

The total capillary length available for blood-tissue transfer is determined by the number and orientation of the capillaries. Therefore, whether capillary tortuosity changes with exercise training has important implications for peripheral gas exchange. To determine the effects of exercise training on capillary orientation and capillary length per volume of muscle fiber [Jv(c,f)] female rats were trained by treadmill running (30 m/min, up to 60 min/day, 5 days/wk) for 4 wk. Muscles from control and trained rats were perfusion fixed at sarcomere lengths (l) ranging from 1.59 to 2.15 microns, and morphometric techniques were used to estimate capillary orientation and Jv(c,f). Training increased (P less than 0.05) musculus soleus oxidative capacity 35% [as estimated from citrate synthase activity: 24.7 +/- 1.4 to 34.7 +/- 1.0 (SE) mumol.g-1.min-1], capillary-to-fiber ratio 30% (2.17 +/- 0.06 to 2.83 +/- 0.05), and Jv(c,f) 32% (1,886 +/- 73 to 2,496 +/- 180 mm-2). Capillary tortuosity (as determined from comparisons of transverse and longitudinal sections) was a direct function of l in control and trained rats and contributed 17-73% of capillary length above that estimated from capillary counts on transverse sections. We conclude that capillary tortuosity in m. soleus is unchanged by training. Therefore, Jv(c,f) increases as a consequence of increased capillary number. M. soleus citrate synthase activity is best correlated with Jv(c,f) and not with capillary counts on transverse sections. We hypothesize that training-induced muscle changes of capillary geometry improve O2 delivery to skeletal muscle and may therefore alter the metabolic response (e.g., lactate accumulation) to exercise after training.(ABSTRACT TRUNCATED AT 250 WORDS)


1995 ◽  
Vol 305 (2) ◽  
pp. 675-680 ◽  
Author(s):  
B Prieur ◽  
L Cordeau-Lossouarn ◽  
A Rotig ◽  
J Bismuth ◽  
J P Geloso ◽  
...  

In the rat kidney, NaK-ATPase activity increased between days 19 and 20 of gestation (+50%) and between 1 and 24 h after birth (+20%), requiring an increased energy supply. In order to determine whether mitochondrial changes were involved, renal mitochondrial development was investigated from day 19 of gestation to 1 day after birth. Slot-blot analyses of mitochondrial-DNA/nuclear-DNA ratio and determination of citrate synthase activity showed a doubling in the mitochondrial pool between days 19 and 20 of gestation. In isolated mitochondria, oxygen consumption remained unchanged between days 19 and 20 of gestation, and then it was enhanced between days 20 and 21 of gestation (+70%) and between 1 and 24 h after birth (+50%). We also focused on one of the respiratory-chain complexes, ATP synthase, and measured its activity and content during the perinatal period. We demonstrated increases in both activity and content of ATP synthase between days 20 and 21 of gestation and between 1 and 24 h after birth, thus suggesting that changes in ATP synthase activity are ascribed to an increase in the mitochondrial density of ATP synthase complexes. Moreover, the mitochondrial ATP/ADP ratio only increased between 1 and 24 h (+90%), indicating a critical step in the renal respiratory-chain maturation at that time. We therefore conclude that the postnatal enhancement of renal mitochondrial oxidative capacity might depend on protein synthesis de novo and on changes in the adenine nucleotide concentrations.


2017 ◽  
Vol 312 (4) ◽  
pp. R520-R528 ◽  
Author(s):  
Naoki Horii ◽  
Natsuki Hasegawa ◽  
Shumpei Fujie ◽  
Masataka Uchida ◽  
Eri Miyamoto-Mikami ◽  
...  

The purpose of this study was to investigate the effect of chronic chlorella intake alone or in combination with high-intensity intermittent exercise (HIIE) training on exercise performance and muscle glycolytic and oxidative metabolism in rats. Forty male Sprague-Dawley rats were randomly assigned to the four groups: sedentary control, chlorella intake (0.5% chlorella powder in normal feed), HIIE training, and combination of HIIE training and chlorella intake for 6 wk ( n = 10 each group). HIIE training comprised 14 repeats of a 20-s swimming session with a 10-s pause between sessions, while bearing a weight equivalent to 16% of body weight, 4 days/week. Exercise performance was tested after the interventions by measuring the maximal number of HIIE sessions that could be completed. Chlorella intake and HIIE training significantly increased the maximal number of HIIE sessions and enhanced the expression of monocarboxylate transporter (MCT)1, MCT4, and peroxisome proliferator-activated receptor γ coactivator-1α concomitantly with the activities of lactate dehydrogenase (LDH), phosphofructokinase, citrate synthase (CS), and cytochrome- c oxidase (COX) in the red region of the gastrocnemius muscle. Furthermore, the combination further augmented the increased exercise performance and the enhanced expressions and activities. By contrast, in the white region of the muscle, MCT1 expression and LDH, CS, and COX activities did not change. These results showed that compared with only chlorella intake and only HIIE training, chlorella intake combined with HIIE training has a more pronounced effect on exercise performance and muscle glycolytic and oxidative metabolism, in particular, lactate metabolism.


1999 ◽  
Vol 82 (4) ◽  
pp. 299-308 ◽  
Author(s):  
Cécile Piot ◽  
Jean-François Hocquette ◽  
Jacques H. Veerkamp ◽  
Denys Durand ◽  
Dominique Bauchart

The oxidative capacity of the liver, the heart and skeletal muscles for fatty acids were investigated in preruminant calves fed for 19 d on a milk-replacer containing either coconut oil (CO, rich in 12:0) or tallow (rich in 16:0 and 18:1). Weights of the total body and tissues did not differ significantly between the two groups of animals but plasma glucose and insulin concentrations were lower in the CO group. Feeding on the CO diet induced an 18-fold increase in the hepatic concentration of triacylglycerols. Rates of total and peroxisomal oxidation of [1-14C]laurate, [1-14C]palmitate and [1-14C]oleate were measured in fresh tissue homogenates. Higher rates of total oxidation in liver homogenate and of peroxisomal oxidation in liver, heart and rectus abdominis muscle homogenates were observed with laurate used as substrate. Furthermore, the relative contribution of peroxisomes to total oxidation was 1·9-fold higher in the liver and in the heart with laurate than with oleate or palmitate. Finally, the peroxisomal oxidation rate of oleate was 1·5-fold higher in the hearts of calves fed on the CO diet. Whatever the tissue, citrate synthase (CS, EC 4.1.3.7) and cytochrome c oxidase (COX, EC 1.9.3.1) activities were similar between the two groups of calves but the COX : CS activity ratio was lower in the liver of the CO group. In conclusion, laurate is better catabolized by peroxisomes than long-chain fatty acids, especially in the liver. Elongation of lauric acid after partial oxidation might explain the hepatic triacylglycerol accumulation in calves fed on the CO diet.


2020 ◽  
Vol 8 (1) ◽  
Author(s):  
Amanda J Frazier ◽  
Nathan R Jensen ◽  
Shawn P Young ◽  
Anne E Todgham

Abstract The practice of mitigating cannibalism in aquaculture is an important focus for hatcheries seeking to maximize yield and has been maintained in hatcheries focusing on wild stock restoration. We hypothesize, however, that a cannibal feeding strategy may confer performance advantages over a non-cannibal feeding strategy and that perhaps cannibal size grading may not be optimal for hatcheries focusing on conservation goals. This study examined metabolic performance differences between cannibal and non-cannibal burbot, Lota lota maculosa, at the Kootenai Tribe of Idaho Twin Rivers Hatchery in Moyie Springs, ID, USA. After habitat alteration led to functional extinction of burbot in the region, the Twin Rivers Hatchery has played a leading role in the reestablishment of burbot in the Kootenai River, ID, and British Columbia. We examined morphometric data (weight, length and condition factor), whole animal resting metabolic rate and the enzyme activity of lactate dehydrogenase, citrate synthase and 3-hydroxyacyl-CoA dehydrogenase to describe the baseline metabolic performance of cannibal and non-cannibal burbot. Taken together, our results demonstrated significant differences in the metabolic strategies of cannibal vs. non-cannibal burbot, where cannibals relied more heavily on carbohydrate metabolism and non-cannibals relied more heavily on glycolytic and lipid metabolism. This study demonstrates the need to reevaluate the traditional practice of removing cannibal fish in conservation hatcheries, as it may not be the ideal strategy of raising the most robust individuals for release. When natural habitat conditions cannot be restored due to permanent habitat alteration, prioritizing release of higher performing individuals could help achieve conservation goals.


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