Metabolic biochemistry of water- vs. air-breathing fishes: muscle enzymes and ultrastructure

1978 ◽  
Vol 56 (4) ◽  
pp. 736-750 ◽  
Author(s):  
P. W. Hochachka ◽  
M. Guppy ◽  
H. E. Guderley ◽  
K. B. Storey ◽  
W. C. Hulbert
Keyword(s):  
White Muscle ◽  
Large Diameter ◽  
Oxidative Capacity ◽  
The Body ◽  
Muscle Enzymes ◽  
Air Breathing ◽  
Red Muscle ◽  
Phosphofructokinase Activity ◽  
Metabolic Biochemistry ◽  
Myotomal Muscle

To delineate what modifications in muscle metabolic biochemistry correlate with transition to air breathing in fishes, the myotomal muscles of aruana, an obligate water breather, and Arapaima, a related obligate air breather, were compared using electron microscopy and enzyme methods. White muscle in both species maintained a rather similar ultrastructure, characterized by large-diameter fibers, very few mitochondria, and few capillaries. However, aruana white muscle displayed nearly fivefold higher levels of pyruvate kinase, threefold higher levels of muscle-type lactate dehydrogenase, and a fourfold higher ratio of fructose diphosphatase –phosphofructokinase activity; at the same time, enzymes in aerobic metabolism occurred at about one-half the levels in Arapaima. Red muscle was never found in the myotomal mass of aruana, but in Arapaima, red muscle was present and seemed fueled by glycogen, lipid droplets never being observed. From these and other data, it was concluded that in myotomal muscle two processes correlate with the transition to air breathing in Amazon osteoglossids: firstly, an emphasis in oxidative metabolism, and secondly, a retention of red muscle. However, compared with more active water-breathing species, Arapaima sustains an overall dampening of enzyme activities in its myotomal muscle, which because of the large myotome mass explains why its overall metabolic rate is relatively low. By keeping the oxidative capacity of its myotomal muscle low, Arapaima automatically conserves O2 either for a longer time or for other more O2-requiring organs in the body, a perfectly understandable strategy for an air-breathing, diving fish, comparable with that observed in other diving vertebrates. A similar comparison was also made of two erythrinid fishes, one that skimmed the O2-rich surface layers of water and one that obtained three quarters of its O2 from water, one quarter from air. Ultrastructural and enzyme data led to the unexpected conclusion that the surface skimmer sustained a higher oxidative capacity in its myotomal muscles than did the facultative air breather.

Glycogen 'seas,' glycogen bodies, and glycogen granules in heart and skeletal muscle of two air-breathing, burrowing fishes

1978 ◽  
Vol 56 (4) ◽  
pp. 774-786 ◽  
Author(s):  
P. W. Hochachka ◽  
W. C. Hulbert
Keyword(s):  
Energy Source ◽  
Skeletal Muscle ◽  
White Muscle ◽  
Large Diameter ◽  
The Other ◽  
Air Breathing ◽  
Fermentative Metabolism ◽  
Red Muscle ◽  
Carbon Reservoir ◽  
Α Particles

Studies of the ultrastructures of heart, white muscle, and red muscle of two air-breathing, burrowing Amazon fishes, Lepidosiren paradoxa and Synbranchus marmarotus, indicated an overwhelming dependence upon glycogen as a storage carbon and energy source. In lungfish white muscle, unusually high quantities of glycogen were packaged as large-diameter rosettes or α-particles, typical of organs such as the liver in other species. In lungfish red muscle, glycogen was stored as the usual smaller β-particles, either randomly dispersed or organized into membrane–glycogen complexes called glycogen bodies. The hearts of both species also displayed numerous glycogen bodies, the membrane–glycogen complexes apparently being formed from specialized regions of the interfibrillar sarcoplasmic reticulum. These immense glycogen depots could be mobilized to support either oxidative or fermentative metabolism. However, neither mitochondrial abundance nor the levels of enzymes in oxidative metabolism were abnormally high compared with other fishes. Heart lactate dehydrogenase, on the other hand, occurred at higher levels than thus far found in any vertebrate heart, suggesting that heart glycogen bodies in these species serve primarily as a carbon reservoir for emergency use under conditions of O2 lack.

The potential for lactate utilization by red and white muscle of the eel Anguilla rostrata L.

1978 ◽  
Vol 56 (1) ◽  
pp. 128-135 ◽  
Author(s):  
W. C. Hulbert ◽  
T. W. Moon
Keyword(s):  
Lactate Dehydrogenase ◽  
White Muscle ◽  
Anguilla Rostrata ◽  
Lactate Oxidase ◽  
American Eel ◽  
Muscle Enzymes ◽  
Phosphoenol Pyruvate ◽  
Red Muscle ◽  
Lactate Utilization

The activities of lactate dehydrogenase (LDH) (L-lactate: NAD+ oxidoreductase, EC 1.1.1.27) can be divided into a lactate oxidase (lactate to pyruvate) and pyruvate reductase (pyruvate to lactate) component. These activities were examined in red and white muscle excised from the American eel Anguilla rostrata as an estimate of tissue lactate utilization, and compared with the kidney, gill, heart, and liver patterns. Phosphoenol pyruvate carboxykinase (PEP CK) activities in red and white muscle and liver were estimated as a marker for tissue gluconeogenic potential. Consistent with the possibility of lactate utilization for gluconeogenesis, both red muscle and liver possessed an active PEP CK and a bifunctional LDH, where oxidase activities were of the same magnitude as reductase activities. Kidney, which in mammals possesses gluconeogenic capabilities, together with heart and gill, also demonstrated LDH profiles consistent with the liver and red muscle enzymes. White muscle LDH was found to be essentially a pyruvate reductase and no PEP CK activity could be detected. These results suggest that eel red muscle has the potential to utilize lactate and has at least some of the enzymes required for gluconeogenesis. Therefore, the capacity of red muscle to perform a metabolic recycling function in addition to contraction cannot be excluded.

Distribution and relative proportions of red muscle in scombrid fishes: consequences of body size and relationships to locomotion and endothermy

1983 ◽  
Vol 61 (9) ◽  
pp. 2087-2096 ◽  
Author(s):  
J. B. Graham ◽  
F. J. Koehrn ◽  
K. A. Dickson
Keyword(s):  
Body Weight ◽  
Body Size ◽  
White Muscle ◽  
The Body ◽  
Thunnus Albacares ◽  
Katsuwonus Pelamis ◽  
Scaling Relationships ◽  
Red Muscle ◽  
Scombrid Fish ◽  
Scombrid Fishes

The scaling of red muscle with body weight and the distribution of red muscle within the body were compared in seven scombrid fish species to determine relationships between red muscle function and the maintenance of endothermy by tunas. In ectothermic Sarda chiliensis and Scomber japonicus, red muscle occurs along the body edge, is concentrated posteriorly, and the total amount of this tissue is proportional to body weight raised to a power significantly greater than 1.0. In five endothermic tunas, Auxis thazard, Euthynnus lineatus, Katsuwonus pelamis, Thunnus albacares, and T. alalunga, red muscle scaling coefficients are 1.0 or less, and red muscle is positioned deep and anterior in the body. The power needed to overcome drag increases with fish body size (weight and length) and velocity and is reflected in the red muscle scaling relationships of both Sarda and Scomber. By contrast, decreasing relative amounts of red muscle in larger tunas suggest these fishes increase propulsion efficiency as they grow. This may be a result of either or both greater muscle efficiency and reduced division of labor between red and white muscle to which both endothermy and thermoregulation could contribute.

EVIDENCE FOR A DIFFERENT RESPONSE OF RED AND WHITE SKELETAL MUSCLE OF THE RAT IN DIFFERENT THYROID STATES

1978 ◽  
Vol 87 (4) ◽  
pp. 768-775 ◽  
Author(s):  
J. W. Janssen ◽  
C. van Hardeveld ◽  
A. A. H. Kassenaar
Keyword(s):  
Skeletal Muscle ◽  
Body Weight ◽  
Weight Gain ◽  
Protein Content ◽  
White Muscle ◽  
Mitochondrial Protein ◽  
The Body ◽  
Mitochondrial Enzymes ◽  
Muscle Weight ◽  
Red Muscle

ABSTRACT The influence of thyroid hormone depletion and experimental hyperthyroidism on red and white skeletal muscle of the rat during periods of 2, 4 and 8 weeks were studied. Body weight, muscle weight, mitochondrial protein content, and specific activities of the mitochondrial enzymes α-glycerophosphate dehydrogenase (EC 1.1.99.5) (α-GPD) and succinate dehydrogenase (EC 1.3.99.1) (SDH) were used as parameters. The largest differences in body weight gain and muscle weight gain (both red and white muscle) in the hypothyroid rats were seen after 8 weeks of T4 treatment. In the hyperthyroid rats the weight of the red muscle and the ratio of the red muscle weight to the body weight increased, whereas the white muscle weight and the ratio of the white muscle weight to the body weight decreased relative to the control animals. In hypothyroid rats the mitochondrial protein content was lowered in both red and white muscle, the specific α-GPD activity only in the latter. No changes in specific SDH activity were observed in either type of muscle. The hyperthyroid rats showed an increase in the mitochondrial protein content and the specific α-GPD and SDH activity in the red muscle, whereas no significant changes were observed in the white muscle. The changes in the parameters under study show that the effect of the thyroid state differs in red and white muscle. An explanation for a possibly greater sensitivity of red than of white muscle to thyroid hormones is discussed.

Ca2+ handling and oxidative capacity are greatly impaired in swimming muscles of hatchery-reared versus wild Atlantic salmon (Salmo salar)

2008 ◽  
Vol 65 (1) ◽  
pp. 10-16 ◽  
Author(s):  
Katja Anttila ◽  
Matti Järvilehto ◽  
Satu Mänttäri
Keyword(s):  
Atlantic Salmon ◽  
Salmo Salar ◽  
White Muscle ◽  
Oxidative Capacity ◽  
Wild Fish ◽  
Muscle Performance ◽  
Calcium Handling ◽  
Relative Level ◽  
Atlantic Salmon Salmo Salar ◽  
Red Muscle

The swimming capacity of fish is strongly associated with muscle performance, although the prerequisites for effective movements have not been fully described at the molecular level. To compare the condition of swimming musculature of hatchery-reared Atlantic salmon (Salmo salar) with that of wild fish, we analyzed the relative level of two excitation–contraction coupling components (i.e., dihydropyridine receptor (DHPR) and ryanodine receptor (RyR)) and the oxidative capacity of muscles with histochemical and Western blot methods. The density of DHPR and RyR was considerably higher in swimming muscles of wild fingerlings (age 0+) (109.8% and 123.3% in red muscle; 128.6% and 186.0% in white muscle, respectively) and yearlings (age 1+) (153.5% and 459.1% in red muscle; 131.2% and 858.4% in white muscle) as compared with those in reared fish. Similar difference was also observed in the oxidative capacity of muscles. Moreover, the oxidative activity correlated positively with the level of DHPR and RyR. Our data indicate that calcium handling, as well as oxidative capacity of swimming muscles of reared salmon, is clearly separable from the corresponding capacities of wild fish. We suggest that the observed alteration is a major contributing factor to the well-documented differences in swimming ability between wild and hatchery-reared salmon.

Tolerance of unacclimated and cold-acclimated rats to exercise in the cold: serum, red and white muscle enzymes, and histological changes

1970 ◽  
Vol 48 (10) ◽  
pp. 723-731 ◽  
Author(s):  
M. P. Dieter ◽  
P. D. Altland ◽  
B. Highman
Keyword(s):  
Enzyme Activity ◽  
White Muscle ◽  
Lactic Dehydrogenase ◽  
Glycolytic Enzymes ◽  
Muscle Enzymes ◽  
Histological Changes ◽  
Glycerophosphate Dehydrogenase ◽  
Cold Room ◽  
Aerobic Function ◽  
Red Muscle

Unacclimated and cold-acclimated rats were exercised for 3 h, 5 h, or 9 h in a cold room maintained at 1.7 °C. The cold-acclimated rats tolerated these exercise periods, but two-thirds of the unacclimated rats died during 9 h exercise. In red and white muscle the intermediate exercise interval (5 h) induced significantly greater increases in the activities in muscle of creatinephosphokinase and glycolytic enzymes of unacclimated rats, while during 9 h exercise enzyme activity declined in muscles of unacclimated rats and increased in cold-acclimated ones. The rise in serum enzyme activity during exercise was consistently greater in unacclimated than in cold-acclimated rats. Apparently the reduction in exercise tolerance was associated with and may have been in part due to loss of enzyme content and activity in muscles. Collectively, these and other biochemical responses suggested that homeostatic mechanisms had been exhausted in the rats dually stressed by cold exposure and exercise. Except for the activities of aldolase and the ratio of lactic dehydrogenase to alpha-glycerophosphate dehydrogenase, those enzymes associated with "aerobic" function (transaminases) showed the predominant changes in red muscle, and those associated with "anaerobic" function (glycolytic enzymes) the predominant changes in white muscle. The greater responses of the glycolytic enzymes in a predominantly "aerobic" tissue suggest that the biochemical adaptability of red muscle is greater than that of white muscle.

Muscle dynamics in skipjack tuna: timing of red muscle shortening in relation to activation and body curvature during steady swimming

1999 ◽  
Vol 202 (16) ◽  
pp. 2139-2150 ◽  
Author(s):  
R.E. Shadwick ◽  
S.L. Katz ◽  
K.E. Korsmeyer ◽  
T. Knower ◽  
J.W. Covell
Keyword(s):  
Fork Length ◽  
Muscle Length ◽  
The Body ◽  
Emg Activity ◽  
Skipjack Tuna ◽  
Force Transmission ◽  
Muscle Strain ◽  
Muscle Shortening ◽  
Red Muscle ◽  
Length Changes

Cyclic length changes in the internal red muscle of skipjack tuna (Katsuwonus pelamis) were measured using sonomicrometry while the fish swam in a water tunnel at steady speeds of 1.1-2.3 L s(−)(1), where L is fork length. These data were coupled with simultaneous electromyographic (EMG) recordings. The onset of EMG activity occurred at virtually the same phase of the strain cycle for muscle at axial locations between approximately 0.4L and 0.74L, where the majority of the internal red muscle is located. Furthermore, EMG activity always began during muscle lengthening, 40–50 prior to peak length, suggesting that force enhancement by stretching and net positive work probably occur in red muscle all along the body. Our results support the idea that positive contractile power is derived from all the aerobic swimming muscle in tunas, while force transmission is provided primarily by connective tissue structures, such as skin and tendons, rather than by muscles performing negative work. We also compared measured muscle length changes with midline curvature (as a potential index of muscle strain) calculated from synchronised video image analysis. Unlike contraction of the superficial red muscle in other fish, the shortening of internal red muscle in skipjack tuna substantially lags behind changes in the local midline curvature. The temporal separation of red muscle shortening and local curvature is so pronounced that, in the mid-body region, muscle shortening at each location is synchronous with midline curvature at locations that are 7–8 cm (i.e. 8–10 vertebral segments) more posterior. These results suggest that contraction of the internal red muscle causes deformation of the body at more posterior locations, rather than locally. This situation represents a unique departure from the model of a homogeneous bending beam, which describes red muscle strain in other fish during steady swimming, but is consistent with the idea that tunas produce thrust by motion of the caudal fin rather than by undulation of segments along the body.

Red muscle activation patterns in yellowfin (Thunnus albacares) and skipjack (Katsuwonus pelamis) tunas during steady swimming

1999 ◽  
Vol 202 (16) ◽  
pp. 2127-2138 ◽  
Author(s):  
T. Knower ◽  
R.E. Shadwick ◽  
S.L. Katz ◽  
J.B. Graham ◽  
C.S. Wardle
Keyword(s):  
Muscle Activation ◽  
Fork Length ◽  
Force Transducer ◽  
The Body ◽  
Thunnus Albacares ◽  
Katsuwonus Pelamis ◽  
Activation Patterns ◽  
Muscle Activation Patterns ◽  
Red Muscle ◽  
Swimming Mode

To learn about muscle function in two species of tuna (yellowfin Thunnus albacares and skipjack Katsuwonus pelamis), a series of electromyogram (EMG) electrodes was implanted down the length of the body in the internal red (aerobic) muscle. Additionally, a buckle force transducer was fitted around the deep caudal tendons on the same side of the peduncle as the electrodes. Recordings of muscle activity and caudal tendon forces were made while the fish swam over a range of steady, sustainable cruising speeds in a large water tunnel treadmill. In both species, the onset of red muscle activation proceeds sequentially in a rostro-caudal direction, while the offset (or deactivation) is nearly simultaneous at all sites, so that EMG burst duration decreases towards the tail. Muscle duty cycle at each location remains a constant proportion of the tailbeat period (T), independent of swimming speed, and peak force is registered in the tail tendons just as all ipsilateral muscle deactivates. Mean duty cycles in skipjack are longer than those in yellowfin. In yellowfin red muscle, there is complete segregation of contralateral activity, while in skipjack there is slight overlap. In both species, all internal red muscle on one side is active simultaneously for part of each cycle, lasting 0.18T in yellowfin and 0.11T in skipjack. (Across the distance encompassing the majority of the red muscle mass, 0.35-0.65L, where L is fork length, the duration is 0.25T in both species.) When red muscle activation patterns were compared across a variety of fish species, it became apparent that the EMG patterns grade in a progression that parallels the kinematic spectrum of swimming modes from anguilliform to thunniform. The tuna EMG pattern, underlying the thunniform swimming mode, culminates this progression, exhibiting an activation pattern at the extreme opposite end of the spectrum from the anguilliform mode.

Electrical and Mechanical Properties of the Red and White Muscles in the Silver Carp

1972 ◽  
Vol 57 (2) ◽  
pp. 551-567
Author(s):  
T. YAMAMOTO
Keyword(s):  
Mechanical Properties ◽  
White Muscle ◽  
Silver Carp ◽  
Membrane Resistance ◽  
Resting Potential ◽  
Resting Membrane Potential ◽  
Mechanical Responses ◽  
Red Muscle ◽  
Red And White Muscles ◽  
Specific Membrane

1. Electrical and mechanical properties of the red muscle (M. levator pinnae pectoralis) and white muscle (M. levator pinnae lateralis abdominis) in the silver carp (Carassius auratus Linné) were investigated by using caffeine and thymol. 2. A complete tetanus could be produced in the red muscle. But in the white muscle no tetanus was produced and there was a gradual decrease in tension during continuous stimulation, even at a frequency of 1 c/s or less. 3. Caffeine (0.5-1 mM) and thymol (0.25-0.5 mM) potentiated the twitch tension in both muscles without an increase in the resting tension; they produced a contracture in both muscles when the concentration was increased further. 4. The falling phase of the active state of contraction was nearly the same in both muscles and was prolonged by caffeine (0.5 mmM) and by thymol (0.25 mM). 5. The resting membrane potential of the red muscle was scarcely affected by caffeine (0.5-5 mM), whereas in the white muscles a depolarization of 10 mV was observed with caffeine of more than 2 mM. The resting potential of both muscles was little changed by o.25 mm thymol. However, at a concentration of more than 0.5mM thymol depolarized the membrane in both muscles to the same extent. 6. In caffeine (2-3 mM) solution the mean specific membrane resistance was reduced from 8.8 kΩ cm2 to 6.0 kΩ cm2 in the red muscle, and from 5.0 kΩ cm2 to 2.7 kΩ cm2 in the white muscle. In thymol (0.5-1 mM) solution it was reduced from 11.2 kΩcm2 to 6.5 kΩ cm2 in the red muscle, and from 5.4kΩ cm2 to 3.1 kΩ) cm2 in the white muscle. The specific membrane capacitance, calculated from the time constant and the membrane resistance, remained more or less the same in both muscles after a treatment with these agents. 7. Electrical properties of the muscles and the effects of caffeine and thymol on mechanical responses suggest that there are no fundamental differences between red and white muscles except for the excitation-contraction coupling. A lack of summation of twitch, a successive decline of twitch, and inability to produce potassium contracture in the white muscle may be due to the fact that the Ca-releasing mechanism is easily inactivated by depolarization of the membrane.

Water-tunnel studies of heat balance in swimming mako sharks

2001 ◽  
Vol 204 (23) ◽  
pp. 4043-4054 ◽  
Author(s):  
Diego Bernal ◽  
Chugey Sepulveda ◽  
Jeffrey B. Graham
Keyword(s):  
Heat Transfer ◽  
Heat Balance ◽  
Underlying Mechanism ◽  
The Body ◽  
Morphological Properties ◽  
Water Tunnel ◽  
Vascular Networks ◽  
Red Muscle ◽  
Counter Current ◽  
New Evidence

SUMMARY The mako shark (Isurus oxyrinchus) has specialized vascular networks (retia mirabilia) forming counter-current heat exchangers that allow metabolic heat retention in certain regions of the body, including the aerobic, locomotor red muscle and the viscera. Red muscle, white muscle and stomach temperatures were measured in juvenile (5–13.6 kg) makos swimming steadily in a water tunnel and exposed to stepwise square-wave changes in ambient temperature (Ta) to estimate the rates of heat transfer and to determine their capacity for the activity-independent control of heat balance. The rates of heat gain of red muscle during warming were significantly higher than the rates of heat loss during cooling, and neither the magnitude of the change in Ta nor the direction of change in Ta had a significant effect on red muscle latency time. Our findings for mako red muscle are similar to those recorded for tunas and suggest modulation of retial heat-exchange efficiency as the underlying mechanism controlling heat balance. However, the red muscle temperatures measured in swimming makos (0.3–3°C above Ta) are cooler than those measured previously in larger decked makos. Also, the finding of non-stable stomach temperatures contrasts with the predicted independence from Ta recorded in telemetry studies of mako and white sharks. Our studies on live makos provide new evidence that, in addition to the unique convergent morphological properties between makos and tunas, there is a strong functional similarity in the mechanisms used to regulate heat transfer.

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