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Comparative studies of high performance swimming in sharks II. Metabolic biochemistry of locomotor and myocardial muscle in endothermic and ectothermic sharks

D. Bernal^1,*, D. Smith², G. Lopez², D. Weitz², T. Grimminger², K. Dickson² and J. B. Graham¹

¹ Center for Marine Biotechnology and Biomedicine and Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093-0204, USA
² Department of Biological Science, California State University, Fullerton, CA 92834-6850, USA

View larger version (18K): [in a new window]   Fig. 1. Relationship between shark white muscle enzyme activity [µmol substrate converted to product per min (IU) per g wet mass of tissue] at 20°C and body mass. (A) Citrate synthase (CS) activity in blue (open circles), scalloped hammerhead (open triangles), leopard (open squares), common thresher (shaded triangles), mako (shaded circles) and salmon (shaded squares) sharks. In cases where the correlation between enzyme activity and mass was significant for a species, a linear regression was fit to the data. For the mako, IU g-1=2.78–0.53x[log10(mass)], r=-0.44, P=0.01, N=31; for the scalloped hammerhead IU g-1=1.17+1.53x[log10(mass)], r=0.72, P=0.01, N=10. (B) Lactate dehydrogenase (LDH) activity for the same species as for CS and two additional shark species: the Atlantic blacknose (open diamonds) and Atlantic sharpnose (open inverted triangles).

View larger version (28K): [in a new window]   Fig. 2. (A) Lactate dehydrogenase (LDH) and (B) citrate synthase (CS) activities at 20°C in shark heart ventricle (HV; an unknown mixture of compact and spongy myocardium). Values are means ±S.E.M. for ectothermic sharks (open bars) and sharks known to be endothermic (shaded bars). Values in parentheses at the base of each bar are the sample size and the data source: a, present study; b, Dickson et al. (1993). Horizontal lines group species that do not differ significantly from the comparison species (indicated by a black circle), as determined by a Tukey—Kramer multiple comparisons test at P<0.05. For example, leopard shark HV CS (bottom horizontal line in B) is not significantly different from that of the blue shark but differs significantly from all other species studied.

View larger version (24K): [in a new window]   Fig. 3. Temperature effects on the activities of RM CS (left column) and LDH (right column) in four mako, two salmon and six common thresher sharks. Symbols identify specimens by body mass, and the lines show mean enzyme activity at each temperature. The thermal rate coefficient (Q10) (±95% C.I.) values were computed for the activities at 5°C and 30°C (see Materials and methods).

View larger version (37K): [in a new window]   Fig. 4. Transverse (A) and longitudinal (B) sections showing myotomal muscle thermal contours (yellow and red lines) for a 148-kg salmon shark (Lamna ditropis) swimming in 10°C water. Contour projections are modified from Carey and Teal (1969a) and Carey et al. (1985) and use a maximum red muscle (RM) temperature of 24°C. Sectors (S1—S6) show the extent of regional endothermy occurring in white muscle (WM) located at different distances from the RM (see Table 4). The transverse section shows the sites where the three WM samples were taken in relation to the body temperature gradient, with highest temperature occurring closest to the RM and lowest temperature near the skin. (C) Graphs show temperature effects on the activities of lactate dehydrogenase (LDH) and citrate synthase (CS) in WM at the three locations (same symbols as in A) of a 49-kg mako and 127-kg salmon shark. (Table 3 contains the full data set for all the sharks.)

View larger version (19K): [in a new window]   Fig. 5. Relationship between white muscle lactate dehydrogenase (LDH) and citrate synthase (CS) activity at 20°C in six shark species. Species identification symbols are as in Fig. 1: shortfin mako (shaded circles), salmon shark (shaded squares), common thresher shark (shaded triangles), blue shark (open circles), scalloped hammerhead shark (open triangles) and leopard shark (open squares). Regression line equation is: CS activity=0.52+0.012(LDH activity), r=0.69, P<0.01, N=60.