Ontogenetic changes in characteristics required for endothermy in juvenile black skipjack tuna (Euthynnus lineatus)

2000 ◽  
Vol 203 (20) ◽  
pp. 3077-3087 ◽  
Author(s):  
K.A. Dickson ◽  
N.M. Johnson ◽  
J.M. Donley ◽  
J.A. Hoskinson ◽  
M.W. Hansen ◽  
...  

To characterize better the development of endothermy in tunas, we assessed how the abilities to generate heat and to conserve heat within the aerobic, slow-twitch (red) myotomal muscle using counter-current heat exchangers (retia) change with size in juvenile black skipjack tuna (Euthynnus lineatus) above and below the hypothesized minimum size for endothermy of 207 mm fork length (FL). Early juvenile scombrids (10–77 mm FL) collected off the Pacific coast of Panama were raised to larger sizes at the Inter-American Tropical Tuna Commission Laboratory at Achotines Bay, Panama. Evidence of central and lateral rete blood vessels was found in E. lineatus as small as 95.9 mm FL and 125 mm FL, respectively. In larger E. lineatus juveniles (up to 244 mm FL), the capacity for heat exchange increased with fork length as a result of increases in rete length, rete width and the number of vessel rows. The amount (g) of red muscle increased exponentially with fork length in both E. lineatus (105–255 mm FL) and a closely related ectothermic species, the sierra Spanish mackerel Scomberomorus sierra (151–212 mm FL), but was greater in E. lineatus at a given fork length. The specific activity (international units g(−)(1)) of the enzyme citrate synthase in red muscle, an index of tissue heat production potential, increased slightly with fork length in juvenile E. lineatus (84. 1–180 mm FL) and S. sierra (122–215 mm FL). Thus, total red muscle heat production capacity (red muscle citrate synthase activity per gram times red muscle mass in grams) increased with fork length, primarily because of the increase in red muscle mass. Below 95.9 mm FL, E. lineatus cannot maintain red muscle temperature (T(m)) above the ambient water temperature (T(a)) because juveniles of this size lack retia. Above 95.9 mm FL, the relationship between T(x) (T(m)-T(a)) and FL for E. lineatus diverges from that for the ectothermic S. sierra because of increases in the capacities for both heat production and heat retention that result in the development of endothermy.

1999 ◽  
Vol 202 (16) ◽  
pp. 2139-2150 ◽  
Author(s):  
R.E. Shadwick ◽  
S.L. Katz ◽  
K.E. Korsmeyer ◽  
T. Knower ◽  
J.W. Covell

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.


1994 ◽  
Vol 190 (1) ◽  
pp. 79-93 ◽  
Author(s):  
K Dickson

Tunas (family Scombridae) maintain muscle temperatures (Tm) elevated significantly above ambient water temperature (Ta) by using vascular counter-current heat exchangers (retia mirabilia) to conserve metabolic heat generated by continuous contraction of red muscle fibers. Previous work has documented endothermy and both behavioral and physiological thermoregulation in tunas, but only individuals greater than approximately 1 kg body mass had been studied. The purpose of this study was to measure Tm and to examine heat exchanger morphology in smaller fish in order to determine the minimum size at which tunas can elevate Tm significantly above Ta. Measurements of Tm made immediately after capture in field-caught and laboratory-raised tunas (Euthynnus lineatus, Auxis thazard, A. rochei and Thunnus albacares) spanning a size range of 15.5­667 mm fork length (FL) show that tunas 207 mm FL (162.3 g) and larger can elevate red muscle temperature by at least 3.0°C above Ta. E. lineatus, A. thazard and A. rochei of this size possess blood vessels serving the red muscle that are arranged as both lateral and central heat exchangers; the smallest tuna with evidence of a rete was a 108.5 mm FL E. lineatus. In the ectothermic scombrid Scomberomorus sierra (108.7­132.0 mm FL), Tm was elevated 0.2­0.5°C above Ta, and the greatest Tm elevation reported in any ectothermic species is only 2.7°C. Taken together, these data provide evidence that tunas greater than 207 mm FL are endothermic.


1982 ◽  
Vol 60 (12) ◽  
pp. 1143-1147 ◽  
Author(s):  
Harry W. Duckworth ◽  
Alexander W. Bell

Starting with a colicin E1 resistance recombinant plasmid which contains gltA, the gene for citrate synthase in Escherichia coli, we have constructed an ampicillin-resistance plasmid containing the gltA region as a 2.9-kilobase-pair insert in the tetracycline-resistance region of pBR322. Escherichia coli HB101 harbouring this plasmid, when grown on rich medium containing ampicillin, contains citrate synthase as about 8% of its soluble protein. The enzyme has been purified from this rich source and is identical to the chromosomal enzyme prepared previously in every property tested, except for specific activity, which is 64 U∙mg−1 as compared with 45–50 U∙mg−1 previously obtained. The N-terminal sequences of both enzymes are reported, and they are identical up to residue 16 at least. The overall yield of pure enzyme, starting with the cells grown in 15 L of medium, is 600–800 mg.


1999 ◽  
Vol 202 (16) ◽  
pp. 2127-2138 ◽  
Author(s):  
T. Knower ◽  
R.E. Shadwick ◽  
S.L. Katz ◽  
J.B. Graham ◽  
C.S. Wardle

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.


1993 ◽  
Vol 75 (5) ◽  
pp. 2125-2133 ◽  
Author(s):  
A. R. Coggan ◽  
A. M. Abduljalil ◽  
S. C. Swanson ◽  
M. S. Earle ◽  
J. W. Farris ◽  
...  

To examine effects of aging and endurance training on human muscle metabolism during exercise, 31P magnetic resonance spectroscopy was used to study the metabolic response to exercise in young (21–33 yr) and older (58–68 yr) untrained and endurance-trained men (n = 6/group). Subjects performed graded plantar flexion exercise with the right leg, with metabolic responses measured using a 31P surface coil placed over the lateral head of the gastrocnemius muscle. Muscle biopsy samples were also obtained for determination of citrate synthase activity. Rate of increase in P(i)-to-phosphocreatine ratio with increasing power output was greater (P < 0.01) in older untrained [0.058 +/- 0.022 (SD) W-1] and trained men (0.042 +/- 0.010 W-1) than in young untrained (0.038 +/- 0.017 W-1) and trained men (0.024 +/- 0.010 W-1). Plantar flexor muscle cross-sectional area and volume (determined using 1H magnetic resonance imaging) were 11–12% (P < 0.05) and 16–18% (P < 0.01) smaller, respectively, in older men. When corrected for this difference in muscle mass, age-related differences in metabolic response to exercise were reduced by approximately 50% but remained significant (P < 0.05). Citrate synthase activity was approximately 20% lower (P < 0.001) in older untrained and trained men than in corresponding young groups and was inversely related to P(i)-phosphocreatine slope (r = -0.63, P < 0.001). Age-related reductions in exercise capacity were associated with an altered muscle metabolic response to exercise, which appeared to be due to smaller muscle mass and lower muscle respiratory capacity of older subjects.(ABSTRACT TRUNCATED AT 250 WORDS)


1995 ◽  
Vol 269 (1) ◽  
pp. R64-R72 ◽  
Author(s):  
C. M. Bishop ◽  
P. J. Butler ◽  
S. Egginton ◽  
A. J. el Haj ◽  
G. W. Gabrielsen

Preflight development of the goslings was typified by rapid increases in the mitochondrial enzymes of the semimembranosus and heart ventricular muscles resulting in near-adult values by 3 wk of age. In contrast, aerobic capacity of the pectoralis muscle initially developed slowly but showed a rapid increase between 5 and 7 wk of age, in preparation for becoming airborne. Activities of glycolytic enzymes in the pectoralis muscle showed similar patterns of development as those found for the aerobic enzymes, except for hexokinase, which was low at all ages, indicating an adaptation for catabolism of both intracellular glycogen and plasma fatty acids in preference to plasma glucose. Muscle mass specific activity of citrate synthase in the pectoralis increased by only 33% from goslings during the first few days of flight, compared with premigratory geese. Activities of anaerobic glycolytic enzymes in the ventricles were low, but values for hexokinase, which is involved in the phosphorylation of plasma glucose, developed rapidly. Values for lactate dehydrogenase were also high, reflecting the capacity of the heart to catabolize plasma lactate. Substrate flux supplied by carnitine palmitoyltransferase and oxoglutarate dehydrogenase (OGD), in the pectoralis muscles of the premigratory geese, appears to have the smallest excess capacities to meet the requirements of sustained aerobic flight. The average maximum oxygen uptake for premigratory geese during flight, as indicated by values for OGD, is calculated to be 484 ml O2/min (or 208 ml O2.min-1.kg-1).


1993 ◽  
Vol 75 (6) ◽  
pp. 2718-2726 ◽  
Author(s):  
C. R. Woodman ◽  
C. M. Tipton ◽  
J. Evans ◽  
J. K. Linderman ◽  
K. Gosselink ◽  
...  

Rats exposed to head-down suspension (HDS) exhibit reductions in maximal O2 consumption (VO2max) and atrophy of select hindlimb muscles. This study tested the hypothesis that an endocrine-deficient rat exposed to HDS would not exhibit reductions in VO2max or hindlimb muscle mass. Hypophysectomized (HYPX) and sham-operated (SHAM) rats were tested for VO2max before and after 28 days of HDS or cage control (CC) conditions. No significant reductions in VO2max were observed in HYPX rats. In contrast, SHAM-HDS rats exhibited a significant reduction in absolute (-16%) and relative (-29%) measures of aerobic capacity. Time course experiments revealed a reduction in VO2max in SHAM-HDS rats within 7 days, suggesting that cardiovascular adjustments to HDS occurred in the 1st wk. HDS was associated with atrophy of the soleus (-42%) in SHAM rats, whereas HYPX rats exhibited atrophy of the soleus (-36%) and plantaris (-13%). SHAM-HDS rats had significantly lower (-38%) soleus citrate synthase activities per gram muscle mass than SHAM-CC, but no significant differences existed between HYPX-HDS and -CC rats. HDS rats had an impaired ability to thermoregulate, as indicated by significantly greater temperature increases per unit run time, compared with their CC counterparts. Pretreatment plasma epinephrine levels were significantly lower in HYPX than in SHAM rats. Norepinephrine concentration was similar for all groups except HYPX-HDS, in which it was significantly higher. HDS had no significant effect on thyroxine or triiodothyronine. SHAM-HDS rats had significantly lower concentrations of testosterone and growth hormone.(ABSTRACT TRUNCATED AT 250 WORDS)


2002 ◽  
Vol 205 (2) ◽  
pp. 189-200
Author(s):  
Douglas A. Syme ◽  
Robert E. Shadwick

SUMMARY The mechanical power output of deep, red muscle from skipjack tuna (Katsuwonus pelamis) was studied to investigate (i) whether this muscle generates maximum power during cruise swimming, (ii) how the differences in strain experienced by red muscle at different axial body locations affect its performance and (iii) how swimming speed affects muscle work and power output. Red muscle was isolated from approximately mid-way through the deep wedge that lies next to the backbone; anterior (0.44 fork lengths, ANT) and posterior (0.70 fork lengths, POST) samples were studied. Work and power were measured at 25°C using the work loop technique. Stimulus phases and durations and muscle strains (±5.5 % in ANT and ±8 % in POST locations) experienced during cruise swimming at different speeds were obtained from previous studies and used during work loop recordings. In addition, stimulus conditions that maximized work were determined. The stimulus durations and phases yielding maximum work decreased with increasing cycle frequency (analogous to tail-beat frequency), were the same at both axial locations and were almost identical to those used by the fish during swimming, indicating that the muscle produces near-maximal work under most conditions in swimming fish. While muscle in the posterior region undergoes larger strain and thus produces more mass-specific power than muscle in the anterior region, when the longitudinal distribution of red muscle mass is considered, the anterior muscles appear to contribute approximately 40 % more total power. Mechanical work per length cycle was maximal at a cycle frequency of 2–3 Hz, dropping to near zero at 15 Hz and by 20–50 % at 1 Hz. Mechanical power was maximal at a cycle frequency of 5 Hz, dropping to near zero at 15 Hz. These fish typically cruise with tail-beat frequencies of 2.8–5.2 Hz, frequencies at which power from cyclic contractions of deep red muscles was 75–100 % maximal. At any given frequency over this range, power using stimulation conditions recorded from swimming fish averaged 93.4±1.65 % at ANT locations and 88.6±2.08 % at POST locations (means ± s.e.m., N=3–6) of the maximum using optimized conditions. When cycle frequency was held constant (4 Hz) and strain amplitude was increased, work and power increased similarly in muscles from both sample sites; work and power increased 2.5-fold when strain was elevated from ±2 to ±5.5 %, but increased by only approximately 12 % when strain was raised further from ±5.5 to ±8 %. Taken together, these data suggest that red muscle fibres along the entire body are used in a similar fashion to produce near-maximal mechanical power for propulsion during normal cruise swimming. Modelling suggests that the tail-beat frequency at which power is maximal (5 Hz) is very close to that used at the predicted maximum aerobic swimming speed (5.8 Hz) in these fish.


<em>Abstract.</em>—Red snapper <em>Lutjanus campechanus </em>were sampled from commercial landings from the Gulf of Mexico (GOM) off Louisiana from October 2001 to May 2004. Fork length (FL), eviscerated weight, otoliths (both sagittae), and sex determinations were taken from 2,900 specimens; FL was subsequently converted to total length (TL) with the equation TL = 1.073 (FL) + 3.56. Red snapper ages (<EM>N </EM>= 2,867) estimated from counts of opaque annuli in otoliths ranged from 1 to 14 years; however, the vast majority (97.7%) of these were ages 2 to 6 years and the modal age was 3 years. Total lengths among 2,897 specimens ranged from 278 to 940 mm, modal TL was 400 mm, and 98% of all specimens were less than 600 mm TL. We also investigated the fate of red snapper regulatory discards (individuals <381 mm [15 in] TL) during 16 trips on working commercial vessels; over two-thirds of 4,839 red snapper assigned among four discard fate categories (ranging from alive and vigorous to dead) were returned to the water either in moribund or dead condition. Among 399 potential discards retained for age and length analyses, 86% were between 12 and 15 in (305–381 mm) TL and 85% were 2 years of age. The minimum size regulation appears to do little to protect juvenile red snapper from commercial fishing mortality. Heavy red snapper mortality, which begins as bycatch mortality in shrimp trawls, continues as discard mortality at sub-legal lengths when they first recruit to the offshore fishing grounds, and persists as harvest mortality among the youngest legal year- and size-classes. If the minimum size limit is intended to provide a respite from such mortality, a reconsideration of the utility of the minimum length regulation in the commercial harvest of red snapper may be warranted.


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